Clostridium perfringens Epsilon Toxin Compromises the Blood-Brain Barrier in a Humanized Zebrafish Model

Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's b...

Full description

Saved in:
Bibliographic Details
Published iniScience Vol. 15; pp. 39 - 54
Main Authors Adler, Drew, Linden, Jennifer R., Shetty, Samantha V., Ma, Yinghua, Bokori-Brown, Monika, Titball, Richard W., Vartanian, Timothy
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 31.05.2019
Elsevier
Subjects
Model Organism
Molecular Mechanism of Behavior
Pathogenic Organism
Vascular Remodeling
Vascular Remodeling
Pathogenic Organism
Molecular Mechanism of Behavior
Model Organism
Online AccessGet full text

Cover

Abstract Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor. [Display omitted] •ProETX binds specifically to hMAL in live humanized zebrafish•hMAL expression in zebrafish confers susceptibility to ETX-mediated BBB breakdown•Live imaging reveals ETX-mediated edema, hMAL downregulation, stenosis, and stasis•Antibody neutralization abrogates ETX-mediated vascular pathology Pathogenic Organism; Vascular Remodeling; Molecular Mechanism of Behavior; Model Organism
AbstractList Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor.
Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor. : Pathogenic Organism; Vascular Remodeling; Molecular Mechanism of Behavior; Model Organism Subject Areas: Pathogenic Organism, Vascular Remodeling, Molecular Mechanism of Behavior, Model Organism
Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor.Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor.
Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor. [Display omitted] •ProETX binds specifically to hMAL in live humanized zebrafish•hMAL expression in zebrafish confers susceptibility to ETX-mediated BBB breakdown•Live imaging reveals ETX-mediated edema, hMAL downregulation, stenosis, and stasis•Antibody neutralization abrogates ETX-mediated vascular pathology Pathogenic Organism; Vascular Remodeling; Molecular Mechanism of Behavior; Model Organism
Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein (MAL) on the luminal surface of endothelial cells (ECs). However, the kinetics of this interaction and a general understanding of ETX's behavior in a live organism have yet to be appreciated. Here we investigate ETX binding and BBB breakdown in living Danio rerio (zebrafish). Wild-type zebrafish ECs do not bind ETX. When zebrafish ECs are engineered to express human MAL (hMAL), proETX binding occurs in a time-dependent manner. Injection of activated toxin in hMAL zebrafish initiates BBB leakage, hMAL downregulation, blood vessel stenosis, perivascular edema, and blood stasis. We propose a kinetic model of MAL-dependent ETX binding and neurovascular pathology. By generating a humanized zebrafish BBB model, this study contributes to our understanding of ETX-induced BBB permeability and strengthens the proposal that MAL is the ETX receptor. • ProETX binds specifically to hMAL in live humanized zebrafish • hMAL expression in zebrafish confers susceptibility to ETX-mediated BBB breakdown • Live imaging reveals ETX-mediated edema, hMAL downregulation, stenosis, and stasis • Antibody neutralization abrogates ETX-mediated vascular pathology Pathogenic Organism; Vascular Remodeling; Molecular Mechanism of Behavior; Model Organism
Author Vartanian, Timothy
Shetty, Samantha V.
Titball, Richard W.
Bokori-Brown, Monika
Adler, Drew
Linden, Jennifer R.
Ma, Yinghua
AuthorAffiliation 1 Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
3 Department of Biosciences, University of Exeter, Exeter, Devon EX4 4SB, UK
2 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14850, USA
AuthorAffiliation_xml – name: 1 Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
– name: 3 Department of Biosciences, University of Exeter, Exeter, Devon EX4 4SB, UK
– name: 2 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14850, USA
Author_xml – sequence: 1
  givenname: Drew
  surname: Adler
  fullname: Adler, Drew
  organization: Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
– sequence: 2
  givenname: Jennifer R.
  surname: Linden
  fullname: Linden, Jennifer R.
  organization: Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
– sequence: 3
  givenname: Samantha V.
  surname: Shetty
  fullname: Shetty, Samantha V.
  organization: Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
– sequence: 4
  givenname: Yinghua
  surname: Ma
  fullname: Ma, Yinghua
  organization: Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
– sequence: 5
  givenname: Monika
  surname: Bokori-Brown
  fullname: Bokori-Brown, Monika
  organization: Department of Biosciences, University of Exeter, Exeter, Devon EX4 4SB, UK
– sequence: 6
  givenname: Richard W.
  surname: Titball
  fullname: Titball, Richard W.
  organization: Department of Biosciences, University of Exeter, Exeter, Devon EX4 4SB, UK
– sequence: 7
  givenname: Timothy
  orcidid: 0000-0002-1794-9963
  surname: Vartanian
  fullname: Vartanian, Timothy
  email: tiv2002@med.cornell.edu
  organization: Brain and Mind Research Institute, Weill Cornell Medical College of Cornell University, New York, NY 10065, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31030181$$D View this record in MEDLINE/PubMed
BookMark eNp9kt9rFDEQx4NUbD37D_gg--jLrkl2s0lABO-otlDxpb74ErLJ5C7HbnIme0X96815rbQ-FAIZZub7GebHS3QSYgCEXhPcEEz6d9vGZ-MbiolscNcU1zN0RpmQNcYdPXlgn6LznLcYY1peJ_sX6LQluMVEkDO0WY0xz8lbv5-qHSSXfFhDyNXFLvsxhuom_vShWsVpl-LkM-Rq3kC1HGO09TLpElvqlDykqpi6utxPOvjfYKvvMCTtfN5UX6KF8RV67vSY4fzuX6Bvny5uVpf19dfPV6uP17VhlMw1t9QZoEJw3krSO6GZM5IAG4hjzlHZS0eIYbgXpNVMGzsI4bjhhjipuWwX6OrItVFv1S75SadfKmqv_jpiWiudZm9GUJYxaXEPHW9Zx1osKZieayGYlQOnXWF9OLJ2-2ECayDMSY-PoI8jwW_UOt6qvhO85awA3t4BUvyxhzyrMkID46gDxH1WlJKe95KXXhbozcNa_4rcr6okiGOCSTHnBE4ZP-vZx0NpPyqC1eEw1FYdDkMdDkPhThVXkdL_pPf0J0XvjyIo27otC1YlA4IB6xOYuYzTPyX_AxK60lw
CitedBy_id crossref_primary_10_1016_j_jpha_2025_101249
crossref_primary_10_1186_s12987_021_00299_4
crossref_primary_10_3390_toxins15070423
crossref_primary_10_1172_JCI163239
crossref_primary_10_1002_smtd_202300028
crossref_primary_10_3390_cells13131140
crossref_primary_10_1016_j_heliyon_2024_e28429
crossref_primary_10_3390_toxins14040288
crossref_primary_10_3390_toxins16040180
crossref_primary_10_3390_ijms222212111
crossref_primary_10_3390_toxins16120525
crossref_primary_10_3390_cells10051065
crossref_primary_10_3390_toxins15030191
crossref_primary_10_3390_toxins14110757
Cites_doi 10.1371/journal.pone.0017787
10.1016/j.anaerobe.2003.08.003
10.1371/journal.pone.0038149
10.1128/IAI.71.9.5371-5375.2003
10.1016/S0140-6736(55)91275-7
10.1523/JNEUROSCI.15-08-05753.1995
10.1053/jcpa.2001.0514
10.1371/journal.ppat.1004896
10.1128/iai.42.3.1183-1186.1983
10.1371/journal.ppat.1001269
10.1007/978-1-60761-938-3_18
10.1023/A:1026598300052
10.1177/0897190012456366
10.1111/j.1742-4658.2011.08145.x
10.1128/MCB.00086-18
10.1177/104063870401600506
10.1016/j.devcel.2017.02.019
10.1016/j.brainres.2015.10.011
10.1242/dev.128.19.3675
10.1371/journal.pone.0046866
10.1038/nrd4627
10.1371/journal.pone.0013741
10.1016/j.addr.2005.01.017
10.1191/096032700678815710
10.1016/0021-9975(84)90031-8
10.1371/journal.pone.0076359
10.1371/journal.pone.0013046
10.1371/journal.pone.0140321
10.1371/journal.ppat.1003588
10.1016/0021-9975(76)90029-3
10.1128/mBio.02513-14
10.1186/1478-811X-8-11
10.1111/j.1348-0421.1997.tb01888.x
10.1177/1040638714530127
10.1111/exd.12728
10.1016/0021-9975(84)90024-0
10.3389/fcimb.2017.00011
10.1523/JNEUROSCI.1860-14.2014
10.1128/IAI.66.6.2501-2508.1998
10.1099/00221287-144-2-333
10.1074/jbc.M206731200
10.1083/jcb.200406092
10.1089/zeb.2016.1392
10.1016/0306-9877(86)90134-9
10.1016/j.msard.2016.11.010
10.1074/jbc.M011527200
10.1016/j.toxicon.2007.04.025
10.1002/glia.22755
10.1371/journal.pone.0077548
10.1089/154065802761001293
10.1016/0041-0101(91)90105-Z
10.1177/0960327110371700
10.1111/j.1751-0813.2003.tb11474.x
10.1042/BJ20110803
10.1002/lt.20227
10.1128/iai.60.3.1237-1240.1992
10.1038/nprot.2013.068
10.1016/0021-9975(75)90034-1
10.1038/nsmb804
10.1016/S0140-6736(55)91276-9
10.1091/mbc.e11-09-0823
10.1128/IAI.01643-06
10.1021/ic200050g
10.4049/jimmunol.1003771
10.1073/pnas.0712195105
10.1046/j.1462-5822.2003.00262.x
10.1016/j.brainresbull.2007.10.043
10.1128/iai.60.1.102-110.1992
10.1371/journal.pone.0022053
10.1016/j.anaerobe.2016.06.006
10.1016/j.anaerobe.2003.08.005
10.1111/j.1742-4658.2011.08140.x
10.1016/j.devcel.2011.11.018
10.1002/pro.2250
10.1038/sj.clpt.6100223
10.1016/j.vetmic.2007.09.013
10.3390/antib7040037
10.1128/jb.90.3.826-826.1965
10.1006/dbio.2002.0711
10.1016/j.bbamem.2014.11.028
10.1177/1352458518767327
10.1186/1471-213X-10-76
10.1016/j.vetmic.2008.02.015
10.1006/exnr.2001.7652
10.1128/jb.179.20.6480-6487.1997
ContentType Journal Article
Copyright 2019 The Authors
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
2019 The Authors 2019
Copyright_xml – notice: 2019 The Authors
– notice: Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
– notice: 2019 The Authors 2019
DBID 6I.
AAFTH
AAYXX
CITATION
NPM
7X8
5PM
DOA
DOI 10.1016/j.isci.2019.04.016
DatabaseName ScienceDirect Open Access Titles
Elsevier:ScienceDirect:Open Access
CrossRef
PubMed
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle CrossRef
PubMed
MEDLINE - Academic
DatabaseTitleList PubMed

MEDLINE - Academic
Database_xml – sequence: 1
  dbid: DOA
  name: Open Access资源_DOAJ
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
EISSN 2589-0042
EndPage 54
ExternalDocumentID oai_doaj_org_article_d559d06e4735453092ec67a885d9b724
PMC6487375
31030181
10_1016_j_isci_2019_04_016
S2589004219301130
Genre Journal Article
GrantInformation_xml – fundername: NINDS NIH HHS
  grantid: R01 NS066007
– fundername: NINDS NIH HHS
  grantid: R01 NS104350
GroupedDBID 0R~
53G
6I.
AACTN
AAEDW
AAFTH
AALRI
AAMRU
AAXUO
ABMAC
ADBBV
ADVLN
AEXQZ
AFTJW
AITUG
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
AOIJS
BCNDV
EBS
EJD
FDB
GROUPED_DOAJ
HYE
M41
OK1
ROL
RPM
SSZ
AAYWO
AAYXX
ACVFH
ADCNI
AEUPX
AFPUW
AIGII
AKBMS
AKYEP
APXCP
CITATION
NCXOZ
NPM
7X8
5PM
ID FETCH-LOGICAL-c521t-7d2fce288773916f8a5fc91e5b1f5ff2969f11c506813a5acdb88f7c7c1f9a793
IEDL.DBID DOA
ISSN 2589-0042
IngestDate Wed Aug 27 01:31:46 EDT 2025
Thu Aug 21 18:24:19 EDT 2025
Fri Jul 11 06:08:52 EDT 2025
Thu Jan 02 22:53:22 EST 2025
Tue Jul 01 01:03:25 EDT 2025
Thu Apr 24 23:10:03 EDT 2025
Sun Apr 06 06:54:18 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords Vascular Remodeling
Pathogenic Organism
Molecular Mechanism of Behavior
Model Organism
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c521t-7d2fce288773916f8a5fc91e5b1f5ff2969f11c506813a5acdb88f7c7c1f9a793
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Lead Contact
ORCID 0000-0002-1794-9963
OpenAccessLink https://doaj.org/article/d559d06e4735453092ec67a885d9b724
PMID 31030181
PQID 2216769781
PQPubID 23479
PageCount 16
ParticipantIDs doaj_primary_oai_doaj_org_article_d559d06e4735453092ec67a885d9b724
pubmedcentral_primary_oai_pubmedcentral_nih_gov_6487375
proquest_miscellaneous_2216769781
pubmed_primary_31030181
crossref_citationtrail_10_1016_j_isci_2019_04_016
crossref_primary_10_1016_j_isci_2019_04_016
elsevier_sciencedirect_doi_10_1016_j_isci_2019_04_016
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2019-05-31
PublicationDateYYYYMMDD 2019-05-31
PublicationDate_xml – month: 05
  year: 2019
  text: 2019-05-31
  day: 31
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle iScience
PublicationTitleAlternate iScience
PublicationYear 2019
Publisher Elsevier Inc
Elsevier
Publisher_xml – name: Elsevier Inc
– name: Elsevier
References Murrell, O'Donoghue, Ellis (bib51) 1986; 19
Bokori-Brown, Savva, Fernandes da Costa, Naylor, Basak, Titball (bib7) 2011; 278
Worthington, Mulders (bib81) 1975; 42
Anton, Andres-Delgado, Reglero-Real, Batista, Alonso (bib4) 2011; 186
Wagley, Bokori-Brown, Morcrette, Malaspina, D'Arcy, Gnanapavan, Lewis, Popoff, Raciborska, Nicholas (bib80) 2018; 25
Shortt, Titball, Lindsay (bib70) 2000; 19
Miyata, Minami, Tamai, Matsushita, Shimamoto, Okabe (bib47) 2002; 277
Parng, Seng, Semino, McGrath (bib56) 2002; 1
Takaki, Davis, Winglee, Ramakrishnan (bib72) 2013; 8
Finnie (bib17) 1984; 94
Dorca-Arevalo, Soler-Jover, Gibert, Popoff, Martin-Satue, Blasi (bib12) 2008; 131
Kim, Im, Yang, Lee, Kim, Chae, Shin, Song, Ahn, Lee (bib30) 2017; 14
Morgan, Kelly, Buxton (bib48) 1975; 85
Fernandez Miyakawa, Zabal, Silberstein (bib15) 2011; 30
Tam, Richmond, Kaminker, Modrusan, Martin-McNulty, Cao, Weimer, Carano, van Bruggen, Watts (bib73) 2012; 22
Miyata, Matsushita, Minami, Katayama, Shimamoto, Okabe (bib46) 2001; 276
Blanch, Dorca-Arevalo, Not, Cases, Gomez de Aranda, Martinez Yelamos, Martinez Yelamos, Solsona, Blasi (bib5) 2018; 38
Zhou, Liang, Romih, Wang, Liao, Ghiso, Luque-Garcia, Neubert, Kreibich, Alonso (bib85) 2012; 23
Freedman, McClane, Uzal (bib23) 2016; 41
Jeong, Kwon, Ahn, Kang, Kwon, Park, Kim (bib28) 2008; 75
Preston, Macklin (bib59) 2015; 63
Fennessey, Sheng, Rubin, McClain (bib14) 2012; 7
Finnie (bib18) 1984; 94
Linden, Ma, Zhao, Harris, Rumah, Schaeren-Wiemers, Vartanian (bib35) 2015; 6
Manni, Sot, Goni (bib40) 2015; 1848
Miller, Florman, Kim-Schluger, Lento, De La Garza, Wu, Xie, Zhang, Bottone, Zhang (bib43) 2004; 10
Xie, Farage, Sugimoto, Anand-Apte (bib82) 2010; 10
Rumah, Vartanian, Fischetti (bib65) 2017; 7
Ando, Fukuhara, Izumi, Nakajima, Fukui, Kelsh, Mochizuki (bib3) 2016; 143
Bokori-Brown, Kokkinidou, Savva, Fernandes da Costa, Naylor, Cole, Moss, Basak, Titball (bib6) 2013; 22
Zhu, Ghabriel, Blumbergs, Reilly, Manavis, Youssef, Hatami, Finnie (bib86) 2001; 169
Ludwig, Palha, Torhy, Briolat, Colucci-Guyon, Bremont, Herbomel, Boudinot, Levraud (bib38) 2011; 7
Nakajima, Yamamoto, Agarwala, Terai, Fukui, Fukuhara, Ando, Miyazaki, Yokota, Schmelzer (bib54) 2017; 40
Taylor, Grant, Temperley, Patton (bib75) 2010; 8
Schaeren-Wiemers, Bonnet, Erb, Erne, Bartsch, Kern, Mantei, Sherman, Suter (bib67) 2004; 166
Kulkarni, Yellanki, Medishetti, Sriram, Saxena, Yogeeswari (bib32) 2017; 11
Nagahama, Sakurai (bib53) 1992; 60
Ivie, Fennessey, Sheng, Rubin, McClain (bib27) 2011; 6
Rumah, Ma, Linden, Oo, Anrather, Schaeren-Wiemers, Alonso, Fischetti, McClain, Vartanian (bib64) 2015; 11
Schaeren-Wiemers, Valenzuela, Frank, Schwab (bib68) 1995; 15
Lonchamp, Dupont, Wioland, Courjaret, Mbebi-Liegeois, Jover, Doussau, Popoff, Bossu, de Barry (bib37) 2010; 5
Sakurai, Nagahama, Fujii (bib66) 1983; 42
Oyston, Payne, Havard, Williamson, Titball (bib55) 1998; 144
Soler-Jover, Dorca, Popoff, Gibert, Saura, Tusell, Serratosa, Blasi, Martin-Satue (bib71) 2007; 50
Eliceiri, Gonzalez, Baird (bib13) 2011; 686
Zhang, Chen, Sloan, Bennett, Scholze, O'Keeffe, Phatnani, Guarnieri, Caneda, Ruderisch (bib84) 2014; 34
Mostowy, Boucontet, Mazon Moya, Sirianni, Boudinot, Hollinshead, Cossart, Herbomel, Levraud, Colucci-Guyon (bib50) 2013; 9
Zhang, Ni, Yang, Piontek, Chen, Wang, Fan, Qin, Piontek (bib83) 2015; 24
Gleeson-White, Bullen (bib25) 1955; 268
Linden, Telesford, Shetty, Winokour, Haigh, Cahir-McFarland, Antognetti, Datta, Wang, Meier (bib36) 2018; 7
Rumah, Linden, Fischetti, Vartanian (bib63) 2013; 8
Lawson, Weinstein (bib34) 2002; 248
Ackerman, Monk (bib1) 2016; 1641
Finnie, Manavis, Casson, Chidlow (bib21) 2014; 26
Bolcome, Sullivan, Zeller, Barker, Collier, Chan (bib8) 2008; 105
Serbedzija, Flynn, Willett (bib69) 1999; 3
Hunter, Clarke, Kelly, Titball (bib26) 1992; 60
Uzal, Kelly, Morris, Bermudez, Baison (bib79) 2004; 16
Lawson, Scheer, Pham, Kim, Chitnis, Campos-Ortega, Weinstein (bib33) 2001; 128
Finnie (bib20) 2004; 10
MacRae, Peterson (bib39) 2015; 14
McClain, Cover (bib42) 2007; 75
Minami, Katayama, Matsushita, Matsushita, Okabe (bib44) 1997; 41
Morinaga, Nakamura, Yoshizawa, Nishida (bib49) 1965; 90
Cole, Gibert, Popoff, Moss, Titball, Basak (bib10) 2004; 11
Nagahama, Sakurai (bib52) 1991; 29
Finnie (bib19) 2003; 81
Kohn, Warrack (bib31) 1955; 268
Urich, Lazic, Molnos, Wells, Freskgard (bib76) 2012; 7
Tamai, Ishida, Miyata, Matsushita, Suda, Kobayashi, Sonobe, Okabe (bib74) 2003; 71
Uzal (bib77) 2004; 10
Ramnarayanan, Tuma (bib61) 2011; 439
Robertson, Li, Uzal, McClane (bib62) 2011; 6
Popoff (bib87) 2011; 278
Fernandez-Miyakawa, Jost, Billington, Uzal (bib16) 2008; 127
Buxton (bib9) 1976; 86
Uzal, Kelly, Morris, Assis (bib78) 2002; 126
Miyamoto, Minami, Toyoshima, Nakamura, Masada, Nagao, Negi, Itano, Okabe (bib45) 1998; 66
Anderson, Bokor (bib2) 2012; 25
Daneman, Zhou, Agalliu, Cahoy, Kaushal, Barres (bib11) 2010; 5
Fleming, Diekmann, Goldsmith (bib22) 2013; 8
Kari, Rodeck, Dicker (bib29) 2007; 82
Gil, Dorca-Arevalo, Blasi (bib24) 2015; 10
Petit, Gibert, Gourch, Bens, Vandewalle, Popoff (bib58) 2003; 5
Mantis (bib41) 2005; 57
Petit, Gibert, Gillet, Laurent-Winter, Boquet, Popoff (bib57) 1997; 179
Radaram, Ivie, Singh, Grudzien, Reibenspies, Webster, Zhao (bib60) 2011; 50
Freedman (10.1016/j.isci.2019.04.016_bib23) 2016; 41
Miyata (10.1016/j.isci.2019.04.016_bib46) 2001; 276
Mostowy (10.1016/j.isci.2019.04.016_bib50) 2013; 9
Finnie (10.1016/j.isci.2019.04.016_bib21) 2014; 26
Ando (10.1016/j.isci.2019.04.016_bib3) 2016; 143
Jeong (10.1016/j.isci.2019.04.016_bib28) 2008; 75
Kim (10.1016/j.isci.2019.04.016_bib30) 2017; 14
Fleming (10.1016/j.isci.2019.04.016_bib22) 2013; 8
Oyston (10.1016/j.isci.2019.04.016_bib55) 1998; 144
Daneman (10.1016/j.isci.2019.04.016_bib11) 2010; 5
MacRae (10.1016/j.isci.2019.04.016_bib39) 2015; 14
Zhu (10.1016/j.isci.2019.04.016_bib86) 2001; 169
Petit (10.1016/j.isci.2019.04.016_bib58) 2003; 5
Tam (10.1016/j.isci.2019.04.016_bib73) 2012; 22
Finnie (10.1016/j.isci.2019.04.016_bib20) 2004; 10
Xie (10.1016/j.isci.2019.04.016_bib82) 2010; 10
Rumah (10.1016/j.isci.2019.04.016_bib64) 2015; 11
Bokori-Brown (10.1016/j.isci.2019.04.016_bib7) 2011; 278
Finnie (10.1016/j.isci.2019.04.016_bib19) 2003; 81
Sakurai (10.1016/j.isci.2019.04.016_bib66) 1983; 42
Zhang (10.1016/j.isci.2019.04.016_bib84) 2014; 34
Kari (10.1016/j.isci.2019.04.016_bib29) 2007; 82
Bokori-Brown (10.1016/j.isci.2019.04.016_bib6) 2013; 22
Gil (10.1016/j.isci.2019.04.016_bib24) 2015; 10
Nagahama (10.1016/j.isci.2019.04.016_bib53) 1992; 60
Rumah (10.1016/j.isci.2019.04.016_bib65) 2017; 7
Uzal (10.1016/j.isci.2019.04.016_bib79) 2004; 16
Linden (10.1016/j.isci.2019.04.016_bib36) 2018; 7
Bolcome (10.1016/j.isci.2019.04.016_bib8) 2008; 105
Schaeren-Wiemers (10.1016/j.isci.2019.04.016_bib67) 2004; 166
Lonchamp (10.1016/j.isci.2019.04.016_bib37) 2010; 5
Soler-Jover (10.1016/j.isci.2019.04.016_bib71) 2007; 50
Radaram (10.1016/j.isci.2019.04.016_bib60) 2011; 50
Miyata (10.1016/j.isci.2019.04.016_bib47) 2002; 277
Anton (10.1016/j.isci.2019.04.016_bib4) 2011; 186
Morgan (10.1016/j.isci.2019.04.016_bib48) 1975; 85
Tamai (10.1016/j.isci.2019.04.016_bib74) 2003; 71
Buxton (10.1016/j.isci.2019.04.016_bib9) 1976; 86
Fernandez Miyakawa (10.1016/j.isci.2019.04.016_bib15) 2011; 30
Worthington (10.1016/j.isci.2019.04.016_bib81) 1975; 42
Schaeren-Wiemers (10.1016/j.isci.2019.04.016_bib68) 1995; 15
Miller (10.1016/j.isci.2019.04.016_bib43) 2004; 10
Minami (10.1016/j.isci.2019.04.016_bib44) 1997; 41
Eliceiri (10.1016/j.isci.2019.04.016_bib13) 2011; 686
Taylor (10.1016/j.isci.2019.04.016_bib75) 2010; 8
Ludwig (10.1016/j.isci.2019.04.016_bib38) 2011; 7
Murrell (10.1016/j.isci.2019.04.016_bib51) 1986; 19
Takaki (10.1016/j.isci.2019.04.016_bib72) 2013; 8
Blanch (10.1016/j.isci.2019.04.016_bib5) 2018; 38
Manni (10.1016/j.isci.2019.04.016_bib40) 2015; 1848
Ivie (10.1016/j.isci.2019.04.016_bib27) 2011; 6
Rumah (10.1016/j.isci.2019.04.016_bib63) 2013; 8
Robertson (10.1016/j.isci.2019.04.016_bib62) 2011; 6
Finnie (10.1016/j.isci.2019.04.016_bib18) 1984; 94
Linden (10.1016/j.isci.2019.04.016_bib35) 2015; 6
Morinaga (10.1016/j.isci.2019.04.016_bib49) 1965; 90
Fernandez-Miyakawa (10.1016/j.isci.2019.04.016_bib16) 2008; 127
Hunter (10.1016/j.isci.2019.04.016_bib26) 1992; 60
Petit (10.1016/j.isci.2019.04.016_bib57) 1997; 179
Serbedzija (10.1016/j.isci.2019.04.016_bib69) 1999; 3
Shortt (10.1016/j.isci.2019.04.016_bib70) 2000; 19
Popoff (10.1016/j.isci.2019.04.016_bib87) 2011; 278
Zhou (10.1016/j.isci.2019.04.016_bib85) 2012; 23
Gleeson-White (10.1016/j.isci.2019.04.016_bib25) 1955; 268
Preston (10.1016/j.isci.2019.04.016_bib59) 2015; 63
Wagley (10.1016/j.isci.2019.04.016_bib80) 2018; 25
Ackerman (10.1016/j.isci.2019.04.016_bib1) 2016; 1641
Urich (10.1016/j.isci.2019.04.016_bib76) 2012; 7
Fennessey (10.1016/j.isci.2019.04.016_bib14) 2012; 7
McClain (10.1016/j.isci.2019.04.016_bib42) 2007; 75
Miyamoto (10.1016/j.isci.2019.04.016_bib45) 1998; 66
Uzal (10.1016/j.isci.2019.04.016_bib77) 2004; 10
Finnie (10.1016/j.isci.2019.04.016_bib17) 1984; 94
Lawson (10.1016/j.isci.2019.04.016_bib33) 2001; 128
Uzal (10.1016/j.isci.2019.04.016_bib78) 2002; 126
Nagahama (10.1016/j.isci.2019.04.016_bib52) 1991; 29
Mantis (10.1016/j.isci.2019.04.016_bib41) 2005; 57
Anderson (10.1016/j.isci.2019.04.016_bib2) 2012; 25
Dorca-Arevalo (10.1016/j.isci.2019.04.016_bib12) 2008; 131
Kulkarni (10.1016/j.isci.2019.04.016_bib32) 2017; 11
Cole (10.1016/j.isci.2019.04.016_bib10) 2004; 11
Zhang (10.1016/j.isci.2019.04.016_bib83) 2015; 24
Lawson (10.1016/j.isci.2019.04.016_bib34) 2002; 248
Ramnarayanan (10.1016/j.isci.2019.04.016_bib61) 2011; 439
Nakajima (10.1016/j.isci.2019.04.016_bib54) 2017; 40
Parng (10.1016/j.isci.2019.04.016_bib56) 2002; 1
Kohn (10.1016/j.isci.2019.04.016_bib31) 1955; 268
References_xml – volume: 30
  start-page: 275
  year: 2011
  end-page: 282
  ident: bib15
  article-title: Clostridium perfringens epsilon toxin is cytotoxic for human renal tubular epithelial cells
  publication-title: Hum. Exp. Toxicol.
– volume: 90
  start-page: 826
  year: 1965
  ident: bib49
  article-title: Isolation of Clostridium perfringens Type D from a case of gas gangrene
  publication-title: J. Bacteriol.
– volume: 268
  start-page: 385
  year: 1955
  ident: bib31
  article-title: Recovery of Clostridium welchii type D from man
  publication-title: Lancet
– volume: 29
  start-page: 211
  year: 1991
  end-page: 217
  ident: bib52
  article-title: Distribution of labeled Clostridium perfringens epsilon toxin in mice
  publication-title: Toxicon
– volume: 24
  start-page: 605
  year: 2015
  end-page: 610
  ident: bib83
  article-title: Specific binding of Clostridium perfringens enterotoxin fragment to Claudin-b and modulation of zebrafish epidermal barrier
  publication-title: Exp. Dermatol.
– volume: 11
  start-page: 797
  year: 2004
  end-page: 798
  ident: bib10
  article-title: Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin
  publication-title: Nat. Struct. Mol. Biol.
– volume: 126
  start-page: 71
  year: 2002
  end-page: 75
  ident: bib78
  article-title: Effects of intravenous injection of Clostridium perfringens type D epsilon toxin in calves
  publication-title: J. Comp. Pathol.
– volume: 268
  start-page: 384
  year: 1955
  end-page: 385
  ident: bib25
  article-title: Clostridium welchii epsilon toxin in the intestinal contents of man
  publication-title: Lancet
– volume: 7
  start-page: e1001269
  year: 2011
  ident: bib38
  article-title: Whole-body analysis of a viral infection: vascular endothelium is a primary target of infectious hematopoietic necrosis virus in zebrafish larvae
  publication-title: PLoS Pathog.
– volume: 7
  start-page: 37
  year: 2018
  ident: bib36
  article-title: A novel panel of rabbit monoclonal antibodies and their diverse applications including inhibition of Clostridium perfringens epsilon toxin oligomerization
  publication-title: Antibodies
– volume: 22
  start-page: 403
  year: 2012
  end-page: 417
  ident: bib73
  article-title: Death receptors DR6 and TROY regulate brain vascular development
  publication-title: Dev. Cell
– volume: 23
  start-page: 1354
  year: 2012
  end-page: 1366
  ident: bib85
  article-title: MAL facilitates the incorporation of exocytic uroplakin-delivering vesicles into the apical membrane of urothelial umbrella cells
  publication-title: Mol. Biol. Cell
– volume: 169
  start-page: 72
  year: 2001
  end-page: 82
  ident: bib86
  article-title: Clostridium perfringens prototoxin-induced alteration of endothelial barrier antigen (EBA) immunoreactivity at the blood-brain barrier (BBB)
  publication-title: Exp. Neurol.
– volume: 10
  start-page: e0140321
  year: 2015
  ident: bib24
  article-title: Clostridium perfringens epsilon toxin binds to membrane lipids and its cytotoxic action depends on sulfatide
  publication-title: PLoS One
– volume: 19
  start-page: 27
  year: 1986
  end-page: 39
  ident: bib51
  article-title: A review of the sheep-multiple sclerosis connection
  publication-title: Med. Hypotheses
– volume: 75
  start-page: 619
  year: 2008
  end-page: 628
  ident: bib28
  article-title: Functional and developmental analysis of the blood-brain barrier in zebrafish
  publication-title: Brain Res. Bull.
– volume: 71
  start-page: 5371
  year: 2003
  end-page: 5375
  ident: bib74
  article-title: Accumulation of Clostridium perfringens epsilon-toxin in the mouse kidney and its possible biological significance
  publication-title: Infect. Immun.
– volume: 5
  start-page: 155
  year: 2003
  end-page: 164
  ident: bib58
  article-title: Clostridium perfringens epsilon toxin rapidly decreases membrane barrier permeability of polarized MDCK cells
  publication-title: Cell Microbiol.
– volume: 50
  start-page: 530
  year: 2007
  end-page: 540
  ident: bib71
  article-title: Distribution of Clostridium perfringens epsilon toxin in the brains of acutely intoxicated mice and its effect upon glial cells
  publication-title: Toxicon
– volume: 143
  start-page: 1328
  year: 2016
  end-page: 1339
  ident: bib3
  article-title: Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish
  publication-title: Development
– volume: 60
  start-page: 1237
  year: 1992
  end-page: 1240
  ident: bib53
  article-title: High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain
  publication-title: Infect. Immun.
– volume: 41
  start-page: 527
  year: 1997
  end-page: 535
  ident: bib44
  article-title: Lambda-toxin of Clostridium perfringens activates the precursor of epsilon-toxin by releasing its N- and C-terminal peptides
  publication-title: Microbiol. Immunol.
– volume: 25
  start-page: 653
  year: 2018
  end-page: 660
  ident: bib80
  article-title: Evidence of Clostridium perfringens epsilon toxin associated with multiple sclerosis
  publication-title: Mult. Scler.
– volume: 5
  start-page: e13741
  year: 2010
  ident: bib11
  article-title: The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells
  publication-title: PLoS One
– volume: 439
  start-page: 497
  year: 2011
  end-page: 504
  ident: bib61
  article-title: MAL, but not MAL2, expression promotes the formation of cholesterol-dependent membrane domains that recruit apical proteins
  publication-title: Biochem. J.
– volume: 94
  start-page: 363
  year: 1984
  end-page: 370
  ident: bib17
  article-title: Histopathological changes in the brain of mice given Clostridium perfringens type D epsilon toxin
  publication-title: J. Comp. Pathol.
– volume: 186
  start-page: 6345
  year: 2011
  end-page: 6356
  ident: bib4
  article-title: MAL protein controls protein sorting at the supramolecular activation cluster of human T lymphocytes
  publication-title: J. Immunol.
– volume: 8
  start-page: 1114
  year: 2013
  end-page: 1124
  ident: bib72
  article-title: Evaluation of the pathogenesis and treatment of Mycobacterium marinum infection in zebrafish
  publication-title: Nat. Protoc.
– volume: 22
  start-page: 650
  year: 2013
  end-page: 659
  ident: bib6
  article-title: Clostridium perfringens epsilon toxin H149A mutant as a platform for receptor binding studies
  publication-title: Protein Sci.
– volume: 7
  start-page: e46866
  year: 2012
  ident: bib14
  article-title: Oligomerization of Clostridium perfringens epsilon toxin is dependent upon caveolins 1 and 2
  publication-title: PLoS One
– volume: 85
  start-page: 461
  year: 1975
  end-page: 466
  ident: bib48
  article-title: Vascular leakage produced in the brains of mice by Clostridium welchii type D toxin
  publication-title: J. Comp. Pathol.
– volume: 6
  start-page: e02513
  year: 2015
  ident: bib35
  article-title: Clostridium perfringens epsilon toxin causes selective death of mature oligodendrocytes and central nervous system demyelination
  publication-title: MBio
– volume: 14
  start-page: 721
  year: 2015
  end-page: 731
  ident: bib39
  article-title: Zebrafish as tools for drug discovery
  publication-title: Nat. Rev. Drug Discov.
– volume: 9
  start-page: e1003588
  year: 2013
  ident: bib50
  article-title: The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy
  publication-title: PLoS Pathog.
– volume: 277
  start-page: 39463
  year: 2002
  end-page: 39468
  ident: bib47
  article-title: Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes
  publication-title: J. Biol. Chem.
– volume: 50
  start-page: 10564
  year: 2011
  end-page: 10571
  ident: bib60
  article-title: Water oxidation by mononuclear ruthenium complexes with TPA-based ligands
  publication-title: Inorg. Chem.
– volume: 105
  start-page: 2439
  year: 2008
  end-page: 2444
  ident: bib8
  article-title: Anthrax lethal toxin induces cell death-independent permeability in zebrafish vasculature
  publication-title: Proc. Natl. Acad. Sci. U S A
– volume: 3
  start-page: 353
  year: 1999
  end-page: 359
  ident: bib69
  article-title: Zebrafish angiogenesis: a new model for drug screening
  publication-title: Angiogenesis
– volume: 7
  start-page: 11
  year: 2017
  ident: bib65
  article-title: Oral multiple sclerosis drugs inhibit the in vitro growth of epsilon toxin producing gut bacterium, Clostridium perfringens
  publication-title: Front. Cell Infect. Microbiol.
– volume: 42
  start-page: 1183
  year: 1983
  end-page: 1186
  ident: bib66
  article-title: Effect of Clostridium perfringens epsilon toxin on the cardiovascular system of rats
  publication-title: Infect. Immun.
– volume: 38
  year: 2018
  ident: bib5
  article-title: The cytotoxicity of Epsilon toxin from Clostridium perfringens on lymphocytes is mediated by MAL protein expression
  publication-title: Mol. Cell Biol.
– volume: 128
  start-page: 3675
  year: 2001
  end-page: 3683
  ident: bib33
  article-title: Notch signaling is required for arterial-venous differentiation during embryonic vascular development
  publication-title: Development
– volume: 10
  start-page: 145
  year: 2004
  end-page: 150
  ident: bib20
  article-title: Neurological disorders produced by Clostridium perfringens type D epsilon toxin
  publication-title: Anaerobe
– volume: 276
  start-page: 13778
  year: 2001
  end-page: 13783
  ident: bib46
  article-title: Cleavage of a C-terminal peptide is essential for heptamerization of Clostridium perfringens epsilon-toxin in the synaptosomal membrane
  publication-title: J. Biol. Chem.
– volume: 5
  start-page: e13046
  year: 2010
  ident: bib37
  article-title: Clostridium perfringens epsilon toxin targets granule cells in the mouse cerebellum and stimulates glutamate release
  publication-title: PLoS One
– volume: 6
  start-page: e17787
  year: 2011
  ident: bib27
  article-title: Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens epsilon-toxin
  publication-title: PLoS One
– volume: 10
  start-page: 76
  year: 2010
  ident: bib82
  article-title: A novel transgenic zebrafish model for blood-brain and blood-retinal barrier development
  publication-title: BMC Dev. Biol.
– volume: 131
  start-page: 14
  year: 2008
  end-page: 25
  ident: bib12
  article-title: Binding of epsilon-toxin from Clostridium perfringens in the nervous system
  publication-title: Vet. Microbiol.
– volume: 60
  start-page: 102
  year: 1992
  end-page: 110
  ident: bib26
  article-title: Cloning and nucleotide sequencing of the Clostridium perfringens epsilon-toxin gene and its expression in Escherichia coli
  publication-title: Infect Immun.
– volume: 82
  start-page: 70
  year: 2007
  end-page: 80
  ident: bib29
  article-title: Zebrafish: an emerging model system for human disease and drug discovery
  publication-title: Clin. Pharmacol. Ther.
– volume: 66
  start-page: 2501
  year: 1998
  end-page: 2508
  ident: bib45
  article-title: Neurotoxicity of Clostridium perfringens epsilon-toxin for the rat hippocampus via the glutamatergic system
  publication-title: Infect. Immun.
– volume: 41
  start-page: 27
  year: 2016
  end-page: 31
  ident: bib23
  article-title: New insights into Clostridium perfringens epsilon toxin activation and action on the brain during enterotoxemia
  publication-title: Anaerobe
– volume: 8
  start-page: e76359
  year: 2013
  ident: bib63
  article-title: Isolation of Clostridium perfringens type B in an individual at first clinical presentation of multiple sclerosis provides clues for environmental triggers of the disease
  publication-title: PLoS One
– volume: 34
  start-page: 11929
  year: 2014
  end-page: 11947
  ident: bib84
  article-title: An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex
  publication-title: J. Neurosci.
– volume: 15
  start-page: 5753
  year: 1995
  end-page: 5764
  ident: bib68
  article-title: Characterization of a rat gene, rMAL, encoding a protein with four hydrophobic domains in central and peripheral myelin
  publication-title: J. Neurosci.
– volume: 278
  start-page: 4589
  year: 2011
  end-page: 4601
  ident: bib7
  article-title: Molecular basis of toxicity of Clostridium perfringens epsilon toxin
  publication-title: FEBS J.
– volume: 19
  start-page: 108
  year: 2000
  end-page: 116
  ident: bib70
  article-title: An assessment of the in vitro toxicology of Clostridium perfringens type D epsilon-toxin in human and animal cells
  publication-title: Hum. Exp. Toxicol.
– volume: 179
  start-page: 6480
  year: 1997
  end-page: 6487
  ident: bib57
  article-title: Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex
  publication-title: J. Bacteriol.
– volume: 10
  start-page: 1315
  year: 2004
  end-page: 1319
  ident: bib43
  article-title: Fulminant and fatal gas gangrene of the stomach in a healthy live liver donor
  publication-title: Liver Transpl.
– volume: 10
  start-page: 135
  year: 2004
  end-page: 143
  ident: bib77
  article-title: Diagnosis of Clostridium perfringens intestinal infections in sheep and goats
  publication-title: Anaerobe
– volume: 1641
  start-page: 79
  year: 2016
  end-page: 91
  ident: bib1
  article-title: The scales and tales of myelination: using zebrafish and mouse to study myelinating glia
  publication-title: Brain Res.
– volume: 25
  start-page: 521
  year: 2012
  end-page: 529
  ident: bib2
  article-title: Bioterrorism: pathogens as weapons
  publication-title: J. Pharm. Pract.
– volume: 7
  start-page: e38149
  year: 2012
  ident: bib76
  article-title: Transcriptional profiling of human brain endothelial cells reveals key properties crucial for predictive in vitro blood-brain barrier models
  publication-title: PLoS One
– volume: 8
  start-page: e77548
  year: 2013
  ident: bib22
  article-title: Functional characterisation of the maturation of the blood-brain barrier in larval zebrafish
  publication-title: PLoS One
– volume: 14
  start-page: 322
  year: 2017
  end-page: 330
  ident: bib30
  article-title: Zebrafish as a screening model for testing the permeability of blood-brain barrier to small molecules
  publication-title: Zebrafish
– volume: 94
  start-page: 445
  year: 1984
  end-page: 452
  ident: bib18
  article-title: Ultrastructural changes in the brain of mice given Clostridium perfringens type D epsilon toxin
  publication-title: J. Comp. Pathol.
– volume: 26
  start-page: 470
  year: 2014
  end-page: 472
  ident: bib21
  article-title: Retinal microvascular damage and vasogenic edema produced by Clostridium perfringens type D epsilon toxin in rats
  publication-title: J. Vet. Diagn. Invest.
– volume: 16
  start-page: 403
  year: 2004
  end-page: 411
  ident: bib79
  article-title: The pathology of peracute experimental Clostridium perfringens type D enterotoxemia in sheep
  publication-title: J. Vet. Diagn. Invest
– volume: 11
  start-page: 32
  year: 2017
  end-page: 39
  ident: bib32
  article-title: Novel Zebrafish EAE model: a quick in vivo screen for multiple sclerosis
  publication-title: Mult. Scler. Relat. Disord.
– volume: 1848
  start-page: 797
  year: 2015
  end-page: 804
  ident: bib40
  article-title: Interaction of Clostridium perfringens epsilon-toxin with biological and model membranes: a putative protein receptor in cells
  publication-title: Biochim. Biophys. Acta
– volume: 278
  start-page: 4602
  year: 2011
  end-page: 4615
  ident: bib87
  article-title: Epsilon toxin: a fascinating pore-forming toxin
  publication-title: FEBS J.
– volume: 75
  start-page: 1785
  year: 2007
  end-page: 1793
  ident: bib42
  article-title: Functional analysis of neutralizing antibodies against Clostridium perfringens epsilon-toxin
  publication-title: Infect. Immun.
– volume: 686
  start-page: 371
  year: 2011
  end-page: 378
  ident: bib13
  article-title: Zebrafish model of the blood-brain barrier: morphological and permeability studies
  publication-title: Methods Mol. Biol.
– volume: 40
  start-page: 523
  year: 2017
  end-page: 536.e6
  ident: bib54
  article-title: Flow-dependent endothelial YAP regulation contributes to vessel maintenance
  publication-title: Dev. Cell
– volume: 6
  start-page: e22053
  year: 2011
  ident: bib62
  article-title: Evidence for a prepore stage in the action of Clostridium perfringens epsilon toxin
  publication-title: PLoS One
– volume: 144
  start-page: 333
  year: 1998
  end-page: 341
  ident: bib55
  article-title: Production of a non-toxic site-directed mutant of Clostridium perfringens epsilon-toxin which induces protective immunity in mice
  publication-title: Microbiology
– volume: 42
  start-page: 25
  year: 1975
  end-page: 27
  ident: bib81
  article-title: Effect of Clostridium perfringens epsilon toxin on the blood brain barrier of mice
  publication-title: Onderstepoort J. Vet. Res.
– volume: 11
  start-page: e1004896
  year: 2015
  ident: bib64
  article-title: The myelin and lymphocyte protein MAL is required for binding and activity of Clostridium perfringens epsilon-toxin
  publication-title: PLoS Pathog.
– volume: 57
  start-page: 1424
  year: 2005
  end-page: 1439
  ident: bib41
  article-title: Vaccines against the category B toxins: Staphylococcal enterotoxin B, epsilon toxin and ricin
  publication-title: Adv. Drug Deliv. Rev.
– volume: 81
  start-page: 219
  year: 2003
  end-page: 221
  ident: bib19
  article-title: Pathogenesis of brain damage produced in sheep by Clostridium perfringens type D epsilon toxin: a review
  publication-title: Aust. Vet. J.
– volume: 63
  start-page: 177
  year: 2015
  end-page: 193
  ident: bib59
  article-title: Zebrafish as a model to investigate CNS myelination
  publication-title: Glia
– volume: 8
  start-page: 11
  year: 2010
  ident: bib75
  article-title: Small molecule screening in zebrafish: an in vivo approach to identifying new chemical tools and drug leads
  publication-title: Cell Commun. Signal.
– volume: 127
  start-page: 379
  year: 2008
  end-page: 385
  ident: bib16
  article-title: Lethal effects of Clostridium perfringens epsilon toxin are potentiated by alpha and perfringolysin-O toxins in a mouse model
  publication-title: Vet. Microbiol.
– volume: 248
  start-page: 307
  year: 2002
  end-page: 318
  ident: bib34
  article-title: In vivo imaging of embryonic vascular development using transgenic zebrafish
  publication-title: Dev. Biol.
– volume: 166
  start-page: 731
  year: 2004
  end-page: 742
  ident: bib67
  article-title: The raft-associated protein MAL is required for maintenance of proper axon–glia interactions in the central nervous system
  publication-title: J. Cell Biol.
– volume: 86
  start-page: 67
  year: 1976
  end-page: 72
  ident: bib9
  article-title: Use of horseradish peroxidase to study the antagonism of Clostridium welchii (Cl. perfringens) type D epsilon toxin in mice by the formalinized epsilon prototoxin
  publication-title: J. Comp. Pathol.
– volume: 1
  start-page: 41
  year: 2002
  end-page: 48
  ident: bib56
  article-title: Zebrafish: a preclinical model for drug screening
  publication-title: Assay Drug Dev. Technol.
– volume: 6
  start-page: e17787
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib27
  article-title: Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens epsilon-toxin
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0017787
– volume: 10
  start-page: 145
  year: 2004
  ident: 10.1016/j.isci.2019.04.016_bib20
  article-title: Neurological disorders produced by Clostridium perfringens type D epsilon toxin
  publication-title: Anaerobe
  doi: 10.1016/j.anaerobe.2003.08.003
– volume: 7
  start-page: e38149
  year: 2012
  ident: 10.1016/j.isci.2019.04.016_bib76
  article-title: Transcriptional profiling of human brain endothelial cells reveals key properties crucial for predictive in vitro blood-brain barrier models
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0038149
– volume: 71
  start-page: 5371
  year: 2003
  ident: 10.1016/j.isci.2019.04.016_bib74
  article-title: Accumulation of Clostridium perfringens epsilon-toxin in the mouse kidney and its possible biological significance
  publication-title: Infect. Immun.
  doi: 10.1128/IAI.71.9.5371-5375.2003
– volume: 268
  start-page: 384
  year: 1955
  ident: 10.1016/j.isci.2019.04.016_bib25
  article-title: Clostridium welchii epsilon toxin in the intestinal contents of man
  publication-title: Lancet
  doi: 10.1016/S0140-6736(55)91275-7
– volume: 15
  start-page: 5753
  year: 1995
  ident: 10.1016/j.isci.2019.04.016_bib68
  article-title: Characterization of a rat gene, rMAL, encoding a protein with four hydrophobic domains in central and peripheral myelin
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.15-08-05753.1995
– volume: 126
  start-page: 71
  year: 2002
  ident: 10.1016/j.isci.2019.04.016_bib78
  article-title: Effects of intravenous injection of Clostridium perfringens type D epsilon toxin in calves
  publication-title: J. Comp. Pathol.
  doi: 10.1053/jcpa.2001.0514
– volume: 11
  start-page: e1004896
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib64
  article-title: The myelin and lymphocyte protein MAL is required for binding and activity of Clostridium perfringens epsilon-toxin
  publication-title: PLoS Pathog.
  doi: 10.1371/journal.ppat.1004896
– volume: 42
  start-page: 1183
  year: 1983
  ident: 10.1016/j.isci.2019.04.016_bib66
  article-title: Effect of Clostridium perfringens epsilon toxin on the cardiovascular system of rats
  publication-title: Infect. Immun.
  doi: 10.1128/iai.42.3.1183-1186.1983
– volume: 7
  start-page: e1001269
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib38
  article-title: Whole-body analysis of a viral infection: vascular endothelium is a primary target of infectious hematopoietic necrosis virus in zebrafish larvae
  publication-title: PLoS Pathog.
  doi: 10.1371/journal.ppat.1001269
– volume: 686
  start-page: 371
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib13
  article-title: Zebrafish model of the blood-brain barrier: morphological and permeability studies
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-60761-938-3_18
– volume: 3
  start-page: 353
  year: 1999
  ident: 10.1016/j.isci.2019.04.016_bib69
  article-title: Zebrafish angiogenesis: a new model for drug screening
  publication-title: Angiogenesis
  doi: 10.1023/A:1026598300052
– volume: 25
  start-page: 521
  year: 2012
  ident: 10.1016/j.isci.2019.04.016_bib2
  article-title: Bioterrorism: pathogens as weapons
  publication-title: J. Pharm. Pract.
  doi: 10.1177/0897190012456366
– volume: 278
  start-page: 4602
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib87
  article-title: Epsilon toxin: a fascinating pore-forming toxin
  publication-title: FEBS J.
  doi: 10.1111/j.1742-4658.2011.08145.x
– volume: 38
  year: 2018
  ident: 10.1016/j.isci.2019.04.016_bib5
  article-title: The cytotoxicity of Epsilon toxin from Clostridium perfringens on lymphocytes is mediated by MAL protein expression
  publication-title: Mol. Cell Biol.
  doi: 10.1128/MCB.00086-18
– volume: 16
  start-page: 403
  year: 2004
  ident: 10.1016/j.isci.2019.04.016_bib79
  article-title: The pathology of peracute experimental Clostridium perfringens type D enterotoxemia in sheep
  publication-title: J. Vet. Diagn. Invest
  doi: 10.1177/104063870401600506
– volume: 40
  start-page: 523
  year: 2017
  ident: 10.1016/j.isci.2019.04.016_bib54
  article-title: Flow-dependent endothelial YAP regulation contributes to vessel maintenance
  publication-title: Dev. Cell
  doi: 10.1016/j.devcel.2017.02.019
– volume: 1641
  start-page: 79
  year: 2016
  ident: 10.1016/j.isci.2019.04.016_bib1
  article-title: The scales and tales of myelination: using zebrafish and mouse to study myelinating glia
  publication-title: Brain Res.
  doi: 10.1016/j.brainres.2015.10.011
– volume: 128
  start-page: 3675
  year: 2001
  ident: 10.1016/j.isci.2019.04.016_bib33
  article-title: Notch signaling is required for arterial-venous differentiation during embryonic vascular development
  publication-title: Development
  doi: 10.1242/dev.128.19.3675
– volume: 7
  start-page: e46866
  year: 2012
  ident: 10.1016/j.isci.2019.04.016_bib14
  article-title: Oligomerization of Clostridium perfringens epsilon toxin is dependent upon caveolins 1 and 2
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0046866
– volume: 14
  start-page: 721
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib39
  article-title: Zebrafish as tools for drug discovery
  publication-title: Nat. Rev. Drug Discov.
  doi: 10.1038/nrd4627
– volume: 5
  start-page: e13741
  year: 2010
  ident: 10.1016/j.isci.2019.04.016_bib11
  article-title: The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0013741
– volume: 57
  start-page: 1424
  year: 2005
  ident: 10.1016/j.isci.2019.04.016_bib41
  article-title: Vaccines against the category B toxins: Staphylococcal enterotoxin B, epsilon toxin and ricin
  publication-title: Adv. Drug Deliv. Rev.
  doi: 10.1016/j.addr.2005.01.017
– volume: 19
  start-page: 108
  year: 2000
  ident: 10.1016/j.isci.2019.04.016_bib70
  article-title: An assessment of the in vitro toxicology of Clostridium perfringens type D epsilon-toxin in human and animal cells
  publication-title: Hum. Exp. Toxicol.
  doi: 10.1191/096032700678815710
– volume: 94
  start-page: 445
  year: 1984
  ident: 10.1016/j.isci.2019.04.016_bib18
  article-title: Ultrastructural changes in the brain of mice given Clostridium perfringens type D epsilon toxin
  publication-title: J. Comp. Pathol.
  doi: 10.1016/0021-9975(84)90031-8
– volume: 8
  start-page: e76359
  year: 2013
  ident: 10.1016/j.isci.2019.04.016_bib63
  article-title: Isolation of Clostridium perfringens type B in an individual at first clinical presentation of multiple sclerosis provides clues for environmental triggers of the disease
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0076359
– volume: 5
  start-page: e13046
  year: 2010
  ident: 10.1016/j.isci.2019.04.016_bib37
  article-title: Clostridium perfringens epsilon toxin targets granule cells in the mouse cerebellum and stimulates glutamate release
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0013046
– volume: 10
  start-page: e0140321
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib24
  article-title: Clostridium perfringens epsilon toxin binds to membrane lipids and its cytotoxic action depends on sulfatide
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0140321
– volume: 9
  start-page: e1003588
  year: 2013
  ident: 10.1016/j.isci.2019.04.016_bib50
  article-title: The zebrafish as a new model for the in vivo study of Shigella flexneri interaction with phagocytes and bacterial autophagy
  publication-title: PLoS Pathog.
  doi: 10.1371/journal.ppat.1003588
– volume: 42
  start-page: 25
  year: 1975
  ident: 10.1016/j.isci.2019.04.016_bib81
  article-title: Effect of Clostridium perfringens epsilon toxin on the blood brain barrier of mice
  publication-title: Onderstepoort J. Vet. Res.
– volume: 86
  start-page: 67
  year: 1976
  ident: 10.1016/j.isci.2019.04.016_bib9
  article-title: Use of horseradish peroxidase to study the antagonism of Clostridium welchii (Cl. perfringens) type D epsilon toxin in mice by the formalinized epsilon prototoxin
  publication-title: J. Comp. Pathol.
  doi: 10.1016/0021-9975(76)90029-3
– volume: 6
  start-page: e02513
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib35
  article-title: Clostridium perfringens epsilon toxin causes selective death of mature oligodendrocytes and central nervous system demyelination
  publication-title: MBio
  doi: 10.1128/mBio.02513-14
– volume: 8
  start-page: 11
  year: 2010
  ident: 10.1016/j.isci.2019.04.016_bib75
  article-title: Small molecule screening in zebrafish: an in vivo approach to identifying new chemical tools and drug leads
  publication-title: Cell Commun. Signal.
  doi: 10.1186/1478-811X-8-11
– volume: 41
  start-page: 527
  year: 1997
  ident: 10.1016/j.isci.2019.04.016_bib44
  article-title: Lambda-toxin of Clostridium perfringens activates the precursor of epsilon-toxin by releasing its N- and C-terminal peptides
  publication-title: Microbiol. Immunol.
  doi: 10.1111/j.1348-0421.1997.tb01888.x
– volume: 26
  start-page: 470
  year: 2014
  ident: 10.1016/j.isci.2019.04.016_bib21
  article-title: Retinal microvascular damage and vasogenic edema produced by Clostridium perfringens type D epsilon toxin in rats
  publication-title: J. Vet. Diagn. Invest.
  doi: 10.1177/1040638714530127
– volume: 24
  start-page: 605
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib83
  article-title: Specific binding of Clostridium perfringens enterotoxin fragment to Claudin-b and modulation of zebrafish epidermal barrier
  publication-title: Exp. Dermatol.
  doi: 10.1111/exd.12728
– volume: 94
  start-page: 363
  year: 1984
  ident: 10.1016/j.isci.2019.04.016_bib17
  article-title: Histopathological changes in the brain of mice given Clostridium perfringens type D epsilon toxin
  publication-title: J. Comp. Pathol.
  doi: 10.1016/0021-9975(84)90024-0
– volume: 7
  start-page: 11
  year: 2017
  ident: 10.1016/j.isci.2019.04.016_bib65
  article-title: Oral multiple sclerosis drugs inhibit the in vitro growth of epsilon toxin producing gut bacterium, Clostridium perfringens
  publication-title: Front. Cell Infect. Microbiol.
  doi: 10.3389/fcimb.2017.00011
– volume: 34
  start-page: 11929
  year: 2014
  ident: 10.1016/j.isci.2019.04.016_bib84
  article-title: An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex
  publication-title: J. Neurosci.
  doi: 10.1523/JNEUROSCI.1860-14.2014
– volume: 66
  start-page: 2501
  year: 1998
  ident: 10.1016/j.isci.2019.04.016_bib45
  article-title: Neurotoxicity of Clostridium perfringens epsilon-toxin for the rat hippocampus via the glutamatergic system
  publication-title: Infect. Immun.
  doi: 10.1128/IAI.66.6.2501-2508.1998
– volume: 144
  start-page: 333
  issue: Pt 2
  year: 1998
  ident: 10.1016/j.isci.2019.04.016_bib55
  article-title: Production of a non-toxic site-directed mutant of Clostridium perfringens epsilon-toxin which induces protective immunity in mice
  publication-title: Microbiology
  doi: 10.1099/00221287-144-2-333
– volume: 277
  start-page: 39463
  year: 2002
  ident: 10.1016/j.isci.2019.04.016_bib47
  article-title: Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M206731200
– volume: 166
  start-page: 731
  year: 2004
  ident: 10.1016/j.isci.2019.04.016_bib67
  article-title: The raft-associated protein MAL is required for maintenance of proper axon–glia interactions in the central nervous system
  publication-title: J. Cell Biol.
  doi: 10.1083/jcb.200406092
– volume: 14
  start-page: 322
  year: 2017
  ident: 10.1016/j.isci.2019.04.016_bib30
  article-title: Zebrafish as a screening model for testing the permeability of blood-brain barrier to small molecules
  publication-title: Zebrafish
  doi: 10.1089/zeb.2016.1392
– volume: 19
  start-page: 27
  year: 1986
  ident: 10.1016/j.isci.2019.04.016_bib51
  article-title: A review of the sheep-multiple sclerosis connection
  publication-title: Med. Hypotheses
  doi: 10.1016/0306-9877(86)90134-9
– volume: 11
  start-page: 32
  year: 2017
  ident: 10.1016/j.isci.2019.04.016_bib32
  article-title: Novel Zebrafish EAE model: a quick in vivo screen for multiple sclerosis
  publication-title: Mult. Scler. Relat. Disord.
  doi: 10.1016/j.msard.2016.11.010
– volume: 276
  start-page: 13778
  year: 2001
  ident: 10.1016/j.isci.2019.04.016_bib46
  article-title: Cleavage of a C-terminal peptide is essential for heptamerization of Clostridium perfringens epsilon-toxin in the synaptosomal membrane
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.M011527200
– volume: 50
  start-page: 530
  year: 2007
  ident: 10.1016/j.isci.2019.04.016_bib71
  article-title: Distribution of Clostridium perfringens epsilon toxin in the brains of acutely intoxicated mice and its effect upon glial cells
  publication-title: Toxicon
  doi: 10.1016/j.toxicon.2007.04.025
– volume: 63
  start-page: 177
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib59
  article-title: Zebrafish as a model to investigate CNS myelination
  publication-title: Glia
  doi: 10.1002/glia.22755
– volume: 8
  start-page: e77548
  year: 2013
  ident: 10.1016/j.isci.2019.04.016_bib22
  article-title: Functional characterisation of the maturation of the blood-brain barrier in larval zebrafish
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0077548
– volume: 1
  start-page: 41
  year: 2002
  ident: 10.1016/j.isci.2019.04.016_bib56
  article-title: Zebrafish: a preclinical model for drug screening
  publication-title: Assay Drug Dev. Technol.
  doi: 10.1089/154065802761001293
– volume: 29
  start-page: 211
  year: 1991
  ident: 10.1016/j.isci.2019.04.016_bib52
  article-title: Distribution of labeled Clostridium perfringens epsilon toxin in mice
  publication-title: Toxicon
  doi: 10.1016/0041-0101(91)90105-Z
– volume: 30
  start-page: 275
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib15
  article-title: Clostridium perfringens epsilon toxin is cytotoxic for human renal tubular epithelial cells
  publication-title: Hum. Exp. Toxicol.
  doi: 10.1177/0960327110371700
– volume: 81
  start-page: 219
  year: 2003
  ident: 10.1016/j.isci.2019.04.016_bib19
  article-title: Pathogenesis of brain damage produced in sheep by Clostridium perfringens type D epsilon toxin: a review
  publication-title: Aust. Vet. J.
  doi: 10.1111/j.1751-0813.2003.tb11474.x
– volume: 439
  start-page: 497
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib61
  article-title: MAL, but not MAL2, expression promotes the formation of cholesterol-dependent membrane domains that recruit apical proteins
  publication-title: Biochem. J.
  doi: 10.1042/BJ20110803
– volume: 10
  start-page: 1315
  year: 2004
  ident: 10.1016/j.isci.2019.04.016_bib43
  article-title: Fulminant and fatal gas gangrene of the stomach in a healthy live liver donor
  publication-title: Liver Transpl.
  doi: 10.1002/lt.20227
– volume: 60
  start-page: 1237
  year: 1992
  ident: 10.1016/j.isci.2019.04.016_bib53
  article-title: High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain
  publication-title: Infect. Immun.
  doi: 10.1128/iai.60.3.1237-1240.1992
– volume: 8
  start-page: 1114
  year: 2013
  ident: 10.1016/j.isci.2019.04.016_bib72
  article-title: Evaluation of the pathogenesis and treatment of Mycobacterium marinum infection in zebrafish
  publication-title: Nat. Protoc.
  doi: 10.1038/nprot.2013.068
– volume: 85
  start-page: 461
  year: 1975
  ident: 10.1016/j.isci.2019.04.016_bib48
  article-title: Vascular leakage produced in the brains of mice by Clostridium welchii type D toxin
  publication-title: J. Comp. Pathol.
  doi: 10.1016/0021-9975(75)90034-1
– volume: 11
  start-page: 797
  year: 2004
  ident: 10.1016/j.isci.2019.04.016_bib10
  article-title: Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin
  publication-title: Nat. Struct. Mol. Biol.
  doi: 10.1038/nsmb804
– volume: 268
  start-page: 385
  year: 1955
  ident: 10.1016/j.isci.2019.04.016_bib31
  article-title: Recovery of Clostridium welchii type D from man
  publication-title: Lancet
  doi: 10.1016/S0140-6736(55)91276-9
– volume: 23
  start-page: 1354
  year: 2012
  ident: 10.1016/j.isci.2019.04.016_bib85
  article-title: MAL facilitates the incorporation of exocytic uroplakin-delivering vesicles into the apical membrane of urothelial umbrella cells
  publication-title: Mol. Biol. Cell
  doi: 10.1091/mbc.e11-09-0823
– volume: 75
  start-page: 1785
  year: 2007
  ident: 10.1016/j.isci.2019.04.016_bib42
  article-title: Functional analysis of neutralizing antibodies against Clostridium perfringens epsilon-toxin
  publication-title: Infect. Immun.
  doi: 10.1128/IAI.01643-06
– volume: 50
  start-page: 10564
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib60
  article-title: Water oxidation by mononuclear ruthenium complexes with TPA-based ligands
  publication-title: Inorg. Chem.
  doi: 10.1021/ic200050g
– volume: 186
  start-page: 6345
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib4
  article-title: MAL protein controls protein sorting at the supramolecular activation cluster of human T lymphocytes
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.1003771
– volume: 105
  start-page: 2439
  year: 2008
  ident: 10.1016/j.isci.2019.04.016_bib8
  article-title: Anthrax lethal toxin induces cell death-independent permeability in zebrafish vasculature
  publication-title: Proc. Natl. Acad. Sci. U S A
  doi: 10.1073/pnas.0712195105
– volume: 5
  start-page: 155
  year: 2003
  ident: 10.1016/j.isci.2019.04.016_bib58
  article-title: Clostridium perfringens epsilon toxin rapidly decreases membrane barrier permeability of polarized MDCK cells
  publication-title: Cell Microbiol.
  doi: 10.1046/j.1462-5822.2003.00262.x
– volume: 75
  start-page: 619
  year: 2008
  ident: 10.1016/j.isci.2019.04.016_bib28
  article-title: Functional and developmental analysis of the blood-brain barrier in zebrafish
  publication-title: Brain Res. Bull.
  doi: 10.1016/j.brainresbull.2007.10.043
– volume: 60
  start-page: 102
  year: 1992
  ident: 10.1016/j.isci.2019.04.016_bib26
  article-title: Cloning and nucleotide sequencing of the Clostridium perfringens epsilon-toxin gene and its expression in Escherichia coli
  publication-title: Infect Immun.
  doi: 10.1128/iai.60.1.102-110.1992
– volume: 6
  start-page: e22053
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib62
  article-title: Evidence for a prepore stage in the action of Clostridium perfringens epsilon toxin
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0022053
– volume: 41
  start-page: 27
  year: 2016
  ident: 10.1016/j.isci.2019.04.016_bib23
  article-title: New insights into Clostridium perfringens epsilon toxin activation and action on the brain during enterotoxemia
  publication-title: Anaerobe
  doi: 10.1016/j.anaerobe.2016.06.006
– volume: 10
  start-page: 135
  year: 2004
  ident: 10.1016/j.isci.2019.04.016_bib77
  article-title: Diagnosis of Clostridium perfringens intestinal infections in sheep and goats
  publication-title: Anaerobe
  doi: 10.1016/j.anaerobe.2003.08.005
– volume: 278
  start-page: 4589
  year: 2011
  ident: 10.1016/j.isci.2019.04.016_bib7
  article-title: Molecular basis of toxicity of Clostridium perfringens epsilon toxin
  publication-title: FEBS J.
  doi: 10.1111/j.1742-4658.2011.08140.x
– volume: 22
  start-page: 403
  year: 2012
  ident: 10.1016/j.isci.2019.04.016_bib73
  article-title: Death receptors DR6 and TROY regulate brain vascular development
  publication-title: Dev. Cell
  doi: 10.1016/j.devcel.2011.11.018
– volume: 22
  start-page: 650
  year: 2013
  ident: 10.1016/j.isci.2019.04.016_bib6
  article-title: Clostridium perfringens epsilon toxin H149A mutant as a platform for receptor binding studies
  publication-title: Protein Sci.
  doi: 10.1002/pro.2250
– volume: 82
  start-page: 70
  year: 2007
  ident: 10.1016/j.isci.2019.04.016_bib29
  article-title: Zebrafish: an emerging model system for human disease and drug discovery
  publication-title: Clin. Pharmacol. Ther.
  doi: 10.1038/sj.clpt.6100223
– volume: 127
  start-page: 379
  year: 2008
  ident: 10.1016/j.isci.2019.04.016_bib16
  article-title: Lethal effects of Clostridium perfringens epsilon toxin are potentiated by alpha and perfringolysin-O toxins in a mouse model
  publication-title: Vet. Microbiol.
  doi: 10.1016/j.vetmic.2007.09.013
– volume: 7
  start-page: 37
  issue: 4
  year: 2018
  ident: 10.1016/j.isci.2019.04.016_bib36
  article-title: . A novel panel of rabbit monoclonal antibodies and their diverse applications including inhibition of Clostridium perfringens epsilon toxin oligomerization
  publication-title: Antibodies
  doi: 10.3390/antib7040037
– volume: 90
  start-page: 826
  year: 1965
  ident: 10.1016/j.isci.2019.04.016_bib49
  article-title: Isolation of Clostridium perfringens Type D from a case of gas gangrene
  publication-title: J. Bacteriol.
  doi: 10.1128/jb.90.3.826-826.1965
– volume: 248
  start-page: 307
  year: 2002
  ident: 10.1016/j.isci.2019.04.016_bib34
  article-title: In vivo imaging of embryonic vascular development using transgenic zebrafish
  publication-title: Dev. Biol.
  doi: 10.1006/dbio.2002.0711
– volume: 1848
  start-page: 797
  year: 2015
  ident: 10.1016/j.isci.2019.04.016_bib40
  article-title: Interaction of Clostridium perfringens epsilon-toxin with biological and model membranes: a putative protein receptor in cells
  publication-title: Biochim. Biophys. Acta
  doi: 10.1016/j.bbamem.2014.11.028
– volume: 25
  start-page: 653
  year: 2018
  ident: 10.1016/j.isci.2019.04.016_bib80
  article-title: Evidence of Clostridium perfringens epsilon toxin associated with multiple sclerosis
  publication-title: Mult. Scler.
  doi: 10.1177/1352458518767327
– volume: 143
  start-page: 1328
  year: 2016
  ident: 10.1016/j.isci.2019.04.016_bib3
  article-title: Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish
  publication-title: Development
– volume: 10
  start-page: 76
  year: 2010
  ident: 10.1016/j.isci.2019.04.016_bib82
  article-title: A novel transgenic zebrafish model for blood-brain and blood-retinal barrier development
  publication-title: BMC Dev. Biol.
  doi: 10.1186/1471-213X-10-76
– volume: 131
  start-page: 14
  year: 2008
  ident: 10.1016/j.isci.2019.04.016_bib12
  article-title: Binding of epsilon-toxin from Clostridium perfringens in the nervous system
  publication-title: Vet. Microbiol.
  doi: 10.1016/j.vetmic.2008.02.015
– volume: 169
  start-page: 72
  year: 2001
  ident: 10.1016/j.isci.2019.04.016_bib86
  article-title: Clostridium perfringens prototoxin-induced alteration of endothelial barrier antigen (EBA) immunoreactivity at the blood-brain barrier (BBB)
  publication-title: Exp. Neurol.
  doi: 10.1006/exnr.2001.7652
– volume: 179
  start-page: 6480
  year: 1997
  ident: 10.1016/j.isci.2019.04.016_bib57
  article-title: Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex
  publication-title: J. Bacteriol.
  doi: 10.1128/jb.179.20.6480-6487.1997
SSID ssj0002002496
Score 2.1645288
Snippet Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein...
Clostridium perfringens epsilon toxin (ETX) is hypothesized to mediate blood-brain barrier (BBB) permeability by binding to the myelin and lymphocyte protein...
SourceID doaj
pubmedcentral
proquest
pubmed
crossref
elsevier
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 39
SubjectTerms Model Organism
Molecular Mechanism of Behavior
Pathogenic Organism
Vascular Remodeling
Title Clostridium perfringens Epsilon Toxin Compromises the Blood-Brain Barrier in a Humanized Zebrafish Model
URI https://dx.doi.org/10.1016/j.isci.2019.04.016
https://www.ncbi.nlm.nih.gov/pubmed/31030181
https://www.proquest.com/docview/2216769781
https://pubmed.ncbi.nlm.nih.gov/PMC6487375
https://doaj.org/article/d559d06e4735453092ec67a885d9b724
Volume 15
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1ba9swFBYjT30ZHe3WrBdU2Nsws2zr9tiUhlDYnlIoexGyLsQhs0OcQNmvn47shKSF9GVvRvJNOkfSsfWd70Pom_TGljbjSeopfKA4lsiclgk1xvrCSZ97yHf--YtNnorHZ_q8J_UFmLCOHrjruB82hLw2ZQ4kcguapzJzhnEtBLWy5FlkAg1r3t7H1DxurwEVXlSWo4AJCq7ZZ8x04C7IeAVcl4w8pyB2vrcqRfL-g8XpbfD5GkO5tyiNT9HHPprEd10rPqEPrj5Ds_tFA2octtr8wUsXXC8mULX4YdlWi6bG0-alqjHMBKsmmNm1OESBeBQh7COQjMAjvQIlOxwONY7_-au_zuLfsMvsq3aGQUJtcY6exg_T-0nSCyokBnQLEm4zb1wW5hUO-bZeaOqNJI6WxFPvM8mkJ8TQlAmSa6qDGYXw3HBDvNRhJH9Gg7qp3QXCrBAE8mqZcEVRAuMOAyq_NNc5K3NbDBHZdqgyPds4iF4s1BZWNldgBAVGUGmhQtEQfd9ds-y4No6ePQI77c4EnuxYELxH9d6j3vOeIaJbK6s-5OhCiXCr6ujDb7cuoYKhYJNF167ZtCrLCKCGuSBD9KVzkd0rRk03AjX8wHkO2nBYU1ezyPkd-pvnnH79H42-RCfQlA4DcYUG69XGXYfQal3exFH0DwZGHwo
linkProvider Directory of Open Access Journals
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Clostridium+perfringens+Epsilon+Toxin+Compromises+the+Blood-Brain+Barrier+in+a+Humanized+Zebrafish+Model&rft.jtitle=iScience&rft.au=Adler%2C+Drew&rft.au=Linden%2C+Jennifer+R&rft.au=Shetty%2C+Samantha+V&rft.au=Ma%2C+Yinghua&rft.date=2019-05-31&rft.eissn=2589-0042&rft.volume=15&rft.spage=39&rft_id=info:doi/10.1016%2Fj.isci.2019.04.016&rft_id=info%3Apmid%2F31030181&rft.externalDocID=31030181
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2589-0042&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2589-0042&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2589-0042&client=summon