The TLR4 adaptor TRAM controls the phagocytosis of Gram-negative bacteria by interacting with the Rab11-family interacting protein 2

Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed on the surface of macrophages and recognizes Gram-negative bacteria. Moreover, TLR4 has been suggested to play a role in the phagocytosis of...

Full description

Saved in:
Bibliographic Details
Published inPLoS pathogens Vol. 15; no. 3; p. e1007684
Main Authors Skjesol, Astrid, Yurchenko, Mariia, Bösl, Korbinian, Gravastrand, Caroline, Nilsen, Kaja Elisabeth, Grøvdal, Lene Melsæther, Agliano, Federica, Patane, Francesco, Lentini, Germana, Kim, Hera, Teti, Giuseppe, Kumar Sharma, Aditya, Kandasamy, Richard K., Sporsheim, Bjørnar, Starheim, Kristian K., Golenbock, Douglas T., Stenmark, Harald, McCaffrey, Mary, Espevik, Terje, Husebye, Harald
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.03.2019
Public Library of Science (PLoS)
Subjects
Actin
Activation
Adapters
Adaptor Proteins, Signal Transducing - metabolism
Adaptor Proteins, Signal Transducing - physiology
Animals
Bacteria
Biology and Life Sciences
Cancer
Carrier Proteins - metabolism
Carrier Proteins - physiology
cdc42 GTP-Binding Protein
Cdc42 protein
Cellular signal transduction
Cytological research
E coli
Endocytosis
Endosomes
Escherichia coli
Escherichia coli - pathogenicity
Funding
G proteins
Gram-negative bacteria
HEK293 Cells
Hospitals
Humans
Immune system
Immunology
Inflammation
Interferon Regulatory Factor-3
Light rail transit
Lipopolysaccharides
Macrophages
Macrophages - immunology
Macrophages - metabolism
Medical research
Medicine
Medicine and Health Sciences
Membrane Proteins - metabolism
Membrane Proteins - physiology
Mice
Mice, Inbred C57BL
Microorganisms
Monocytes
Myeloid Differentiation Factor 88
Phagocytes
Phagocytosis
Phagocytosis - physiology
Physiological aspects
Primary Cell Culture
Protein Transport
Protein-protein interactions
Proteins
rab GTP-Binding Proteins
rac1 GTP-Binding Protein
Rac1 protein
Research and Analysis Methods
Signal Transduction
Software
Staphylococcus aureus
Staphylococcus aureus - pathogenicity
Staphylococcus aureus infections
THP-1 Cells
TLR4
TLR4 protein
Toll-Like Receptor 4 - metabolism
Toll-like receptors
Norway
Italy
Online AccessGet full text

Cover

Abstract Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed on the surface of macrophages and recognizes Gram-negative bacteria. Moreover, TLR4 has been suggested to play a role in the phagocytosis of Gram-negative bacteria, but the mechanisms remain unclear. Here we have used primary human macrophages and engineered THP-1 monocytes to show that the TLR4 sorting adapter, TRAM, is instrumental for phagocytosis of Escherichia coli as well as Staphylococcus aureus. We find that TRAM forms a complex with Rab11 family interacting protein 2 (FIP2) that is recruited to the phagocytic cups of E. coli. This promotes activation of the actin-regulatory GTPases Rac1 and Cdc42. Our results show that FIP2 guided TRAM recruitment orchestrates actin remodelling and IRF3 activation, two events that are both required for phagocytosis of Gram-negative bacteria.
AbstractList Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed on the surface of macrophages and recognizes Gram-negative bacteria. Moreover, TLR4 has been suggested to play a role in the phagocytosis of Gram-negative bacteria, but the mechanisms remain unclear. Here we have used primary human macrophages and engineered THP-1 monocytes to show that the TLR4 sorting adapter, TRAM, is instrumental for phagocytosis of Escherichia coli as well as Staphylococcus aureus. We find that TRAM forms a complex with Rab11 family interacting protein 2 (FIP2) that is recruited to the phagocytic cups of E. coli. This promotes activation of the actin-regulatory GTPases Rac1 and Cdc42. Our results show that FIP2 guided TRAM recruitment orchestrates actin remodelling and IRF3 activation, two events that are both required for phagocytosis of Gram-negative bacteria.
Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed on the surface of macrophages and recognizes Gram-negative bacteria. Moreover, TLR4 has been suggested to play a role in the phagocytosis of Gram-negative bacteria, but the mechanisms remain unclear. Here we have used primary human macrophages and engineered THP-1 monocytes to show that the TLR4 sorting adapter, TRAM, is instrumental for phagocytosis of Escherichia coli as well as Staphylococcus aureus . We find that TRAM forms a complex with Rab11 family interacting protein 2 (FIP2) that is recruited to the phagocytic cups of E . coli . This promotes activation of the actin-regulatory GTPases Rac1 and Cdc42. Our results show that FIP2 guided TRAM recruitment orchestrates actin remodelling and IRF3 activation, two events that are both required for phagocytosis of Gram-negative bacteria. The Gram-negative bacteria E . coli is the most common cause of severe human pathological conditions like sepsis. Sepsis is a clinical syndrome defined by pathological changes due to systemic inflammation, resulting in paralysis of adaptive T-cell immunity with IFN-β as a critical factor. TLR4 is a key sensing receptor of lipopolysaccharide on Gram-negative bacteria. Inflammatory signalling by TLR4 is initiated by the use of alternative pair of TIR-adapters, MAL-MyD88 or TRAM-TRIF. MAL-MyD88 signaling occurs mainly from the plasma membrane giving pro-inflammatory cytokines like TNF, while TRAM-TRIF signaling occurs from vacuoles like endosomes and phagosomes to give type I interferons like IFN-β. It has previously been shown that TLR4 can control phagocytosis and phagosomal maturation through MAL-MyD88 in mice, however, these data have been disputed and published before the role of TRAM was defined in the induction of IFN-β. A role for TRAM or TRIF in phagocytosis has not previously been reported. Here we describe a novel mechanism where TRAM and its binding partner Rab11-FIP2 control phagocytosis of E . coli and regulate IRF3 dependent production of IFN-β. The significance of these results is that we define Rab11-FIP2 as a potential target for modulation of TLR4-dependent signalling in different pathological states.
Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed on the surface of macrophages and recognizes Gram-negative bacteria. Moreover, TLR4 has been suggested to play a role in the phagocytosis of Gram-negative bacteria, but the mechanisms remain unclear. Here we have used primary human macrophages and engineered THP-1 monocytes to show that the TLR4 sorting adapter, TRAM, is instrumental for phagocytosis of Escherichia coli as well as Staphylococcus aureus. We find that TRAM forms a complex with Rab11 family interacting protein 2 (FIP2) that is recruited to the phagocytic cups of E. coli. This promotes activation of the actin-regulatory GTPases Rac1 and Cdc42. Our results show that FIP2 guided TRAM recruitment orchestrates actin remodelling and IRF3 activation, two events that are both required for phagocytosis of Gram-negative bacteria.Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed on the surface of macrophages and recognizes Gram-negative bacteria. Moreover, TLR4 has been suggested to play a role in the phagocytosis of Gram-negative bacteria, but the mechanisms remain unclear. Here we have used primary human macrophages and engineered THP-1 monocytes to show that the TLR4 sorting adapter, TRAM, is instrumental for phagocytosis of Escherichia coli as well as Staphylococcus aureus. We find that TRAM forms a complex with Rab11 family interacting protein 2 (FIP2) that is recruited to the phagocytic cups of E. coli. This promotes activation of the actin-regulatory GTPases Rac1 and Cdc42. Our results show that FIP2 guided TRAM recruitment orchestrates actin remodelling and IRF3 activation, two events that are both required for phagocytosis of Gram-negative bacteria.
Audience Academic
Author Lentini, Germana
Teti, Giuseppe
Kim, Hera
Stenmark, Harald
Kandasamy, Richard K.
Kumar Sharma, Aditya
Yurchenko, Mariia
Skjesol, Astrid
Sporsheim, Bjørnar
Nilsen, Kaja Elisabeth
Espevik, Terje
Husebye, Harald
Gravastrand, Caroline
Agliano, Federica
Grøvdal, Lene Melsæther
Starheim, Kristian K.
Golenbock, Douglas T.
Bösl, Korbinian
Patane, Francesco
McCaffrey, Mary
AuthorAffiliation 6 Molecular Cell Biology Laboratory, Biochemistry Department, Biosciences Institute, University College Cork, Cork, Ireland
4 Centre for Cancer Cell Reprogramming, Faculty of Medicine, University of Oslo, Oslo, Norway
1 Centre of Molecular Inflammation Research, Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway
3 Program in Innate Immunity, Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA, United States of America
2 Department of Clinical and Experimental Medicine, University of Messina, Messina, Italy
5 Department for Molecular Cell Biology, Institute for Cancer Research, Oslo University Hospital, Oslo Norway
7 The Central Norway Regional Health Authority, St. Olavs Hospital HF, Trondheim, Norway
University of Toronto, CANADA
AuthorAffiliation_xml – name: 1 Centre of Molecular Inflammation Research, Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway
– name: 4 Centre for Cancer Cell Reprogramming, Faculty of Medicine, University of Oslo, Oslo, Norway
– name: 6 Molecular Cell Biology Laboratory, Biochemistry Department, Biosciences Institute, University College Cork, Cork, Ireland
– name: 3 Program in Innate Immunity, Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, MA, United States of America
– name: 5 Department for Molecular Cell Biology, Institute for Cancer Research, Oslo University Hospital, Oslo Norway
– name: University of Toronto, CANADA
– name: 7 The Central Norway Regional Health Authority, St. Olavs Hospital HF, Trondheim, Norway
– name: 2 Department of Clinical and Experimental Medicine, University of Messina, Messina, Italy
Author_xml – sequence: 1
  givenname: Astrid
  surname: Skjesol
  fullname: Skjesol, Astrid
– sequence: 2
  givenname: Mariia
  orcidid: 0000-0002-0516-4747
  surname: Yurchenko
  fullname: Yurchenko, Mariia
– sequence: 3
  givenname: Korbinian
  orcidid: 0000-0003-0498-4273
  surname: Bösl
  fullname: Bösl, Korbinian
– sequence: 4
  givenname: Caroline
  orcidid: 0000-0002-6818-4139
  surname: Gravastrand
  fullname: Gravastrand, Caroline
– sequence: 5
  givenname: Kaja Elisabeth
  surname: Nilsen
  fullname: Nilsen, Kaja Elisabeth
– sequence: 6
  givenname: Lene Melsæther
  orcidid: 0000-0001-9148-6832
  surname: Grøvdal
  fullname: Grøvdal, Lene Melsæther
– sequence: 7
  givenname: Federica
  surname: Agliano
  fullname: Agliano, Federica
– sequence: 8
  givenname: Francesco
  orcidid: 0000-0003-2259-982X
  surname: Patane
  fullname: Patane, Francesco
– sequence: 9
  givenname: Germana
  surname: Lentini
  fullname: Lentini, Germana
– sequence: 10
  givenname: Hera
  surname: Kim
  fullname: Kim, Hera
– sequence: 11
  givenname: Giuseppe
  orcidid: 0000-0002-6315-8644
  surname: Teti
  fullname: Teti, Giuseppe
– sequence: 12
  givenname: Aditya
  surname: Kumar Sharma
  fullname: Kumar Sharma, Aditya
– sequence: 13
  givenname: Richard K.
  orcidid: 0000-0002-0894-1222
  surname: Kandasamy
  fullname: Kandasamy, Richard K.
– sequence: 14
  givenname: Bjørnar
  surname: Sporsheim
  fullname: Sporsheim, Bjørnar
– sequence: 15
  givenname: Kristian K.
  orcidid: 0000-0003-4598-1896
  surname: Starheim
  fullname: Starheim, Kristian K.
– sequence: 16
  givenname: Douglas T.
  surname: Golenbock
  fullname: Golenbock, Douglas T.
– sequence: 17
  givenname: Harald
  surname: Stenmark
  fullname: Stenmark, Harald
– sequence: 18
  givenname: Mary
  surname: McCaffrey
  fullname: McCaffrey, Mary
– sequence: 19
  givenname: Terje
  surname: Espevik
  fullname: Espevik, Terje
– sequence: 20
  givenname: Harald
  orcidid: 0000-0002-8828-1059
  surname: Husebye
  fullname: Husebye, Harald
BackLink https://www.ncbi.nlm.nih.gov/pubmed/30883606$$D View this record in MEDLINE/PubMed
BookMark eNqVk0Fv0zAUxyM0xLbCN0AQiQscUuzYSRwOSNUEo1IBqZSz9eI4qavUDrY76J0PjrulY5kmJORDHPv3f_b7-73z6EQbLaPoOUZTTAr8dmN2VkM37XvwU4xQkTP6KDrDWUaSghT05M78NDp3boMQxQTnT6JTghgjOcrPot-rtYxXiyWNoYbeGxuvlrPPsTDaW9O52Iftfg2tEXtvnHKxaeJLC9tEyxa8upJxBcJLqyCu9rHSYRr-lW7jn8qvr-VLqDBOGtiqbkz01nipdJw-jR430Dn5bPhOou8fP6wuPiWLr5fzi9kiETnLfCLKvKhznEpRY5oyggAoIUVaVTlBWVYSlOYI4RJVdSEygZumYgUtq6YumhILSSbRy5u4fWccHwx0PE0zjAllrAzE_IaoDWx4b9UW7J4bUPx6wdiWg_VKdJIjnFFKUI6RoLQQkjEpKAu5UpC0qJoQ6_1w2q7aylrIYCl0o6DjHa3WvDVXPKeEZSz_e11hlQuOcW0scIxYlvKCkvC4k-j1cIQ1P3bSeb5VTsiuAy3NLmSGS4qzkBsK6Kt76MP5D1QLIUWlGxNuJg5B-SxjiKWIhBqaRNMHqDBquVWhdGSjwvpI8GYkOJSX_OVb2DnH59-W_8F-GbMv7lp86-2xvgNAjxYa56xsbhGM-KGNji7wQxvxoY2C7N09mVA-lPuhK0B1_xb_AX5JIWs
CitedBy_id crossref_primary_10_4049_jimmunol_1900328
crossref_primary_10_3389_fvets_2022_1005899
crossref_primary_10_1016_j_intimp_2023_110327
crossref_primary_10_1111_jcmm_14529
crossref_primary_10_3389_fphar_2022_874197
crossref_primary_10_1126_sciadv_adg5128
crossref_primary_10_3390_biom11091319
crossref_primary_10_3389_fcimb_2020_592906
crossref_primary_10_1016_j_intimp_2021_107909
crossref_primary_10_1128_IAI_00809_20
crossref_primary_10_1007_s11030_021_10324_1
crossref_primary_10_1111_tra_12870
crossref_primary_10_1038_s41598_022_16214_2
crossref_primary_10_1155_2021_6646071
crossref_primary_10_3390_vaccines12101121
crossref_primary_10_1038_s41392_024_01980_4
crossref_primary_10_1369_0022155420930303
crossref_primary_10_26508_lsa_202302164
crossref_primary_10_1007_s00018_020_03656_y
crossref_primary_10_1080_10937404_2022_2124563
crossref_primary_10_1186_s12950_023_00367_6
crossref_primary_10_1016_j_vetmic_2024_110091
crossref_primary_10_1080_21505594_2021_1929037
crossref_primary_10_1016_j_molimm_2021_06_025
crossref_primary_10_1371_journal_ppat_1010908
crossref_primary_10_1107_S2053230X20009164
crossref_primary_10_1242_jcs_239194
crossref_primary_10_2147_CMAR_S257598
Cites_doi 10.1006/smim.2001.0331
10.1371/journal.ppat.1006556
10.1016/j.str.2006.06.010
10.1084/jem.20031023
10.1074/jbc.M206316200
10.1242/jcs.01280
10.1091/mbc.e03-09-0706
10.1007/978-3-642-59430-4_8
10.1038/cr.2008.65
10.1111/imr.12212
10.1089/omi.2011.0118
10.1016/j.cell.2006.03.047
10.1093/nar/29.9.e45
10.1074/jbc.M114.593426
10.1111/tra.12146
10.1126/science.282.5394.1717
10.1098/rstb.2000.0632
10.1111/j.1600-0854.2006.00528.x
10.1074/jbc.M107925200
10.1038/nrm2755
10.1016/j.molcel.2009.09.004
10.1126/science.282.5396.2085
10.1074/jbc.M104831200
10.1126/science.1096158
10.1371/journal.pone.0006529
10.1042/BST0371032
10.1002/ijc.29899
10.1016/j.it.2017.03.006
10.1242/jcs.078360
10.1038/ni.1727
10.1038/nature14359
10.4049/jimmunol.1402628
10.1016/j.jmb.2008.03.050
10.1074/jbc.274.19.13198
10.1091/mbc.e05-05-0466
10.1074/jbc.M109.034355
10.4049/jimmunol.1401605
10.1182/blood-2011-01-328906
10.1093/nar/gkv007
10.1016/j.immuni.2010.09.010
10.1016/j.immuni.2005.09.007
10.1007/s00011-007-6115-5
10.1038/nmeth.3252
10.1091/mbc.e14-05-0967
10.1038/35052055
10.1073/pnas.1222811110
10.1083/jcb.201707027
10.1038/ni1569
10.1042/BCJ20160992
10.1038/nri2079
ContentType Journal Article
Copyright COPYRIGHT 2019 Public Library of Science
2019 Skjesol et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
info:eu-repo/semantics/openAccess
2019 Skjesol et al 2019 Skjesol et al
Copyright_xml – notice: COPYRIGHT 2019 Public Library of Science
– notice: 2019 Skjesol et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: info:eu-repo/semantics/openAccess
– notice: 2019 Skjesol et al 2019 Skjesol et al
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
ISN
ISR
3V.
7QL
7U9
7X7
7XB
88E
8FE
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
AZQEC
BBNVY
BENPR
BHPHI
C1K
CCPQU
DWQXO
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7P
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PRINS
7X8
3HK
5PM
DOA
DOI 10.1371/journal.ppat.1007684
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Gale In Context: Canada
Gale In Context: Science
ProQuest Central (Corporate)
Bacteriology Abstracts (Microbiology B)
Virology and AIDS Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability (subscription)
ProQuest Central UK/Ireland
ProQuest Central Essentials
Biological Science Collection (subscription)
ProQuest Central
Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest One Community College
ProQuest Central Korea
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
ProQuest Biological Science Collection
ProQuest Health & Medical Collection
Medical Database
Biological Science Database
ProQuest Central Premium
ProQuest One Academic
Publicly Available Content Database
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic
ProQuest One Academic UKI Edition
ProQuest Central China
MEDLINE - Academic
NORA - Norwegian Open Research Archives
PubMed Central (Full Participant titles)
DOAJ Open Access Full Text
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
ProQuest One Academic Middle East (New)
ProQuest Central Essentials
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
SciTech Premium Collection
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central China
Environmental Sciences and Pollution Management
ProQuest Central
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
ProQuest Health & Medical Research Collection
Health Research Premium Collection
Health and Medicine Complete (Alumni Edition)
Natural Science Collection
ProQuest Central Korea
Bacteriology Abstracts (Microbiology B)
Health & Medical Research Collection
Biological Science Collection
AIDS and Cancer Research Abstracts
ProQuest Central (New)
ProQuest Medical Library (Alumni)
Virology and AIDS Abstracts
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
ProQuest SciTech Collection
ProQuest Hospital Collection (Alumni)
ProQuest Health & Medical Complete
ProQuest Medical Library
ProQuest One Academic UKI Edition
ProQuest One Academic
ProQuest One Academic (New)
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList MEDLINE



MEDLINE - Academic
Publicly Available Content Database
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  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
– sequence: 3
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
– sequence: 4
  dbid: BENPR
  name: ProQuest Central
  url: https://www.proquest.com/central
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
Medicine
DocumentTitleAlternate FIP2 uses TRAM to control phagocytosis of E. coli
EISSN 1553-7374
ExternalDocumentID 2251134889
oai_doaj_org_article_0154430610c447ce88ec48ab14ae47bf
PMC6438586
10852_74355
A580820341
30883606
10_1371_journal_ppat_1007684
Genre Research Support, Non-U.S. Gov't
Journal Article
GeographicLocations Norway
Italy
GeographicLocations_xml – name: Italy
– name: Norway
GrantInformation_xml – fundername: ;
  grantid: 46082500
– fundername: ;
  grantid: 80420223
– fundername: ;
  grantid: 50052400
– fundername: ;
  grantid: 223255/F50
– fundername: ;
  grantid: FRIMEDBIO 275876
GroupedDBID ---
123
29O
2WC
53G
5VS
7X7
88E
8FE
8FH
8FI
8FJ
AAFWJ
AAUCC
AAWOE
AAYXX
ABDBF
ABUWG
ACGFO
ACIHN
ACPRK
ACUHS
ADBBV
AEAQA
AENEX
AEUYN
AFKRA
AFPKN
AFRAH
AHMBA
ALMA_UNASSIGNED_HOLDINGS
AOIJS
B0M
BAWUL
BBNVY
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EAP
EAS
EBD
EMK
EMOBN
ESX
F5P
FPL
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAO
IHR
INH
INR
ISN
ISR
ITC
KQ8
LK8
M1P
M48
M7P
MM.
O5R
O5S
OK1
OVT
P2P
PGMZT
PHGZM
PHGZT
PIMPY
PQQKQ
PROAC
PSQYO
PV9
QF4
QN7
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
WOW
~8M
ADRAZ
CGR
CUY
CVF
ECM
EIF
H13
IPNFZ
NPM
PJZUB
PPXIY
PQGLB
RIG
WOQ
PMFND
3V.
7QL
7U9
7XB
8FK
AZQEC
C1K
DWQXO
GNUQQ
H94
K9.
PKEHL
PQEST
PQUKI
PRINS
7X8
3HK
AAPBV
ABPTK
M~E
N95
UMP
5PM
PUEGO
-
ADACO
BBAFP
ID FETCH-LOGICAL-c685t-c967d612ecd142830aa43372bb630559302600190bd7c5c1ffb8749bfd7f91ce3
IEDL.DBID M48
ISSN 1553-7374
1553-7366
IngestDate Fri Nov 26 17:52:08 EST 2021
Wed Aug 27 01:25:22 EDT 2025
Thu Aug 21 18:33:49 EDT 2025
Sat Apr 29 05:40:37 EDT 2023
Fri Jul 11 02:23:01 EDT 2025
Fri Jul 25 10:31:33 EDT 2025
Tue Jun 17 21:07:37 EDT 2025
Tue Jun 10 20:25:48 EDT 2025
Fri Jun 27 03:57:21 EDT 2025
Fri Jun 27 04:01:45 EDT 2025
Mon Jul 21 05:59:15 EDT 2025
Tue Jul 01 03:50:39 EDT 2025
Thu Apr 24 22:58:36 EDT 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 3
Language English
License This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c685t-c967d612ecd142830aa43372bb630559302600190bd7c5c1ffb8749bfd7f91ce3
Notes new_version
ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
content type line 23
NFR/223255
These authors are joint senior authors on this work.
The authors have declared that no competing interests exist.
ORCID 0000-0003-0498-4273
0000-0002-6818-4139
0000-0001-9148-6832
0000-0003-4598-1896
0000-0002-0894-1222
0000-0002-6315-8644
0000-0003-2259-982X
0000-0002-8828-1059
0000-0002-0516-4747
OpenAccessLink https://www.proquest.com/docview/2251134889?pq-origsite=%requestingapplication%
PMID 30883606
PQID 2251134889
PQPubID 1436335
ParticipantIDs plos_journals_2251134889
doaj_primary_oai_doaj_org_article_0154430610c447ce88ec48ab14ae47bf
pubmedcentral_primary_oai_pubmedcentral_nih_gov_6438586
cristin_nora_10852_74355
proquest_miscellaneous_2194151340
proquest_journals_2251134889
gale_infotracmisc_A580820341
gale_infotracacademiconefile_A580820341
gale_incontextgauss_ISR_A580820341
gale_incontextgauss_ISN_A580820341
pubmed_primary_30883606
crossref_primary_10_1371_journal_ppat_1007684
crossref_citationtrail_10_1371_journal_ppat_1007684
ProviderPackageCode CITATION
AAYXX
PublicationCentury 2000
PublicationDate 2019-03-01
PublicationDateYYYYMMDD 2019-03-01
PublicationDate_xml – month: 03
  year: 2019
  text: 2019-03-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS pathogens
PublicationTitleAlternate PLoS Pathog
PublicationYear 2019
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References DR Balce (ref34) 2011; 118
Y Chen (ref39) 2009; 35
RM Yates (ref32) 2005; 23
C Raiborg (ref47) 2015; 520
W Chen (ref29) 2008; 379
CP Horgan (ref12) 2009; 37
MW Pfaffl (ref49) 2001; 29
JM Blander (ref7) 2004; 304
BB Chu (ref13) 2009; 284
RM Yates (ref33) 2007; 8
DN Cullis (ref14) 2002; 277
J Stack (ref38) 2014; 193
ME Ritchie (ref52) 2015; 43
JC Kagan (ref18) 2008; 9
CJ Kirschning (ref36) 2002; 270
EK Park (ref43) 2007; 56
J Canton (ref35) 2014; 25
GC Yu (ref53) 2012; 16
M Zerial (ref11) 2001; 2
EM Palsson-McDermott (ref46) 2009; 10
E Seixas (ref8) 2018; 8
GH Fan (ref16) 2004; 15
M Nethe (ref40) 2010; 123
II Mechnikov (ref1) 1988; 10
M Yurchenko (ref44) 2018; 217
F Castellano (ref3) 2001; 13
A Hall (ref5) 2000; 355
K Funami (ref24) 2015; 195
SA Freeman (ref2) 2014; 262
CM Hales (ref26) 2001; 276
L Kong (ref9) 2008; 18
H Husebye (ref10) 2010; 33
E Campeau (ref48) 2009; 4
W Dong (ref42) 2016; 138
KA Fitzgerald (ref45) 2003; 198
HN Kovacic (ref41) 2001; 276
W Huber (ref51) 2015; 12
N Naslavsky (ref15) 2006; 17
NJ Nilsen (ref37) 2015; 290
AM Pauwels (ref30) 2017; 38
A Poltorak (ref6) 1998; 282
BD Grant (ref20) 2009; 10
Y Enokizono (ref23) 2013; 110
K Molleken (ref17) 2017; 13
JC Schafer (ref25) 2014; 15
WN Jagoe (ref21) 2006; 14
AJ Lindsay (ref50) 2004; 117
E Caron (ref4) 1998; 282
V Benard (ref27) 1999; 274
LA O'Neill (ref31) 2007; 7
JC Kagan (ref19) 2006; 125
DC Klein (ref22) 2015
S Bakshi (ref28) 2017; 474
References_xml – volume: 13
  start-page: 347
  issue: 6
  year: 2001
  ident: ref3
  article-title: Actin dynamics during phagocytosis
  publication-title: Semin Immunol
  doi: 10.1006/smim.2001.0331
– volume: 13
  start-page: e1006556
  issue: 8
  year: 2017
  ident: ref17
  article-title: Acquisition of Rab11 and Rab11-Fip2-A novel strategy for Chlamydia pneumoniae early survival
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.1006556
– volume: 14
  start-page: 1273
  issue: 8
  year: 2006
  ident: ref21
  article-title: Crystal structure of rab11 in complex with rab11 family interacting protein 2
  publication-title: Structure
  doi: 10.1016/j.str.2006.06.010
– volume: 198
  start-page: 1043
  issue: 7
  year: 2003
  ident: ref45
  article-title: LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF
  publication-title: The Journal of experimental medicine
  doi: 10.1084/jem.20031023
– volume: 277
  start-page: 49158
  issue: 51
  year: 2002
  ident: ref14
  article-title: Rab11-FIP2, an adaptor protein connecting cellular components involved in internalization and recycling of epidermal growth factor receptors
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M206316200
– volume: 117
  start-page: 4365
  issue: Pt 19
  year: 2004
  ident: ref50
  article-title: The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane
  publication-title: Journal of cell science
  doi: 10.1242/jcs.01280
– volume: 15
  start-page: 2456
  issue: 5
  year: 2004
  ident: ref16
  article-title: Rab11-family interacting protein 2 and myosin Vb are required for CXCR2 recycling and receptor-mediated chemotaxis
  publication-title: Molecular biology of the cell
  doi: 10.1091/mbc.e03-09-0706
– volume: 270
  start-page: 121
  year: 2002
  ident: ref36
  article-title: TLR2: Cellular sensor for microbial and endogenous molecular patterns
  publication-title: Curr Top Microbiol
  doi: 10.1007/978-3-642-59430-4_8
– volume: 18
  start-page: 745
  issue: 7
  year: 2008
  ident: ref9
  article-title: MyD88-independent activation of a novel actin-Cdc42/Rac pathway is required for Toll-like receptor-stimulated phagocytosis
  publication-title: Cell Res
  doi: 10.1038/cr.2008.65
– volume: 262
  start-page: 193
  issue: 1
  year: 2014
  ident: ref2
  article-title: Phagocytosis: receptors, signal integration, and the cytoskeleton
  publication-title: Immunol Rev
  doi: 10.1111/imr.12212
– volume: 16
  start-page: 284
  issue: 5
  year: 2012
  ident: ref53
  article-title: clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters
  publication-title: Omics
  doi: 10.1089/omi.2011.0118
– volume: 125
  start-page: 943
  issue: 5
  year: 2006
  ident: ref19
  article-title: Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling
  publication-title: Cell
  doi: 10.1016/j.cell.2006.03.047
– volume: 29
  start-page: e45
  issue: 9
  year: 2001
  ident: ref49
  article-title: A new mathematical model for relative quantification in real-time RT-PCR
  publication-title: Nucl Acids Res
  doi: 10.1093/nar/29.9.e45
– volume: 290
  start-page: 3209
  issue: 6
  year: 2015
  ident: ref37
  article-title: A Role for the Adaptor Proteins TRAM and TRIF in Toll-like Receptor 2 Signaling
  publication-title: Journal of Biological Chemistry
  doi: 10.1074/jbc.M114.593426
– volume: 15
  start-page: 292
  issue: 3
  year: 2014
  ident: ref25
  article-title: Rab11-FIP2 interaction with MYO5B regulates movement of Rab11a-containing recycling vesicles
  publication-title: Traffic
  doi: 10.1111/tra.12146
– volume: 282
  start-page: 1717
  issue: 5394
  year: 1998
  ident: ref4
  article-title: Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases
  publication-title: Science
  doi: 10.1126/science.282.5394.1717
– volume: 355
  start-page: 965
  issue: 1399
  year: 2000
  ident: ref5
  article-title: Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton
  publication-title: Philos T R Soc B
  doi: 10.1098/rstb.2000.0632
– volume: 8
  start-page: 241
  issue: 3
  year: 2007
  ident: ref33
  article-title: Macrophage activation downregulates the degradative capacity of the phagosome
  publication-title: Traffic
  doi: 10.1111/j.1600-0854.2006.00528.x
– volume: 276
  start-page: 45856
  issue: 49
  year: 2001
  ident: ref41
  article-title: Redox regulation of human Rac1 stability by the proteasome in human aortic endothelial cells
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M107925200
– volume: 10
  start-page: 597
  issue: 9
  year: 2009
  ident: ref20
  article-title: Pathways and mechanisms of endocytic recycling
  publication-title: Nature reviews Molecular cell biology
  doi: 10.1038/nrm2755
– volume: 35
  start-page: 841
  issue: 6
  year: 2009
  ident: ref39
  article-title: Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2009.09.004
– volume: 282
  start-page: 2085
  issue: 5396
  year: 1998
  ident: ref6
  article-title: Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene
  publication-title: Science
  doi: 10.1126/science.282.5396.2085
– volume: 276
  start-page: 39067
  issue: 42
  year: 2001
  ident: ref26
  article-title: Identification and characterization of a family of Rab11-interacting proteins
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M104831200
– volume: 304
  start-page: 1014
  issue: 5673
  year: 2004
  ident: ref7
  article-title: Regulation of phagosome maturation by signals from toll-like receptors
  publication-title: Science
  doi: 10.1126/science.1096158
– volume: 4
  start-page: e6529
  issue: 8
  year: 2009
  ident: ref48
  article-title: A versatile viral system for expression and depletion of proteins in mammalian cells
  publication-title: PloS one
  doi: 10.1371/journal.pone.0006529
– volume: 37
  start-page: 1032
  year: 2009
  ident: ref12
  article-title: The dynamic Rab11-FIPs
  publication-title: Biochemical Society transactions
  doi: 10.1042/BST0371032
– volume: 138
  start-page: 1680
  issue: 7
  year: 2016
  ident: ref42
  article-title: Rab11-FIP2 promotes the metastasis of gastric cancer cells
  publication-title: Int J Cancer
  doi: 10.1002/ijc.29899
– volume: 38
  start-page: 407
  issue: 6
  year: 2017
  ident: ref30
  article-title: Patterns, Receptors, and Signals: Regulation of Phagosome Maturation
  publication-title: Trends Immunol
  doi: 10.1016/j.it.2017.03.006
– volume: 123
  start-page: 4011
  issue: Pt 23
  year: 2010
  ident: ref40
  article-title: The role of ubiquitylation and degradation in RhoGTPase signalling
  publication-title: J Cell Sci
  doi: 10.1242/jcs.078360
– volume: 10
  start-page: 579
  issue: 6
  year: 2009
  ident: ref46
  article-title: TAG, a splice variant of the adaptor TRAM, negatively regulates the adaptor MyD88-independent TLR4 pathway
  publication-title: Nature immunology
  doi: 10.1038/ni.1727
– volume: 520
  start-page: 234
  issue: 7546
  year: 2015
  ident: ref47
  article-title: Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth
  publication-title: Nature
  doi: 10.1038/nature14359
– volume: 195
  start-page: 4456
  issue: 9
  year: 2015
  ident: ref24
  article-title: Identification of a Regulatory Acidic Motif as the Determinant of Membrane Localization of TICAM-2
  publication-title: J Immunol
  doi: 10.4049/jimmunol.1402628
– volume: 379
  start-page: 251
  issue: 2
  year: 2008
  ident: ref29
  article-title: Contribution of Ser386 and Ser396 to activation of interferon regulatory factor 3
  publication-title: J Mol Biol
  doi: 10.1016/j.jmb.2008.03.050
– volume: 274
  start-page: 13198
  issue: 19
  year: 1999
  ident: ref27
  article-title: Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases
  publication-title: J Biol Chem
  doi: 10.1074/jbc.274.19.13198
– volume: 17
  start-page: 163
  issue: 1
  year: 2006
  ident: ref15
  article-title: Interactions between EHD proteins and Rab11-FIP2: A role for EHD3 in early endosomal transport
  publication-title: Molecular biology of the cell
  doi: 10.1091/mbc.e05-05-0466
– volume: 284
  start-page: 22481
  issue: 33
  year: 2009
  ident: ref13
  article-title: Requirement of myosin Vb.Rab11a.Rab11-FIP2 complex in cholesterol-regulated translocation of NPC1L1 to the cell surface
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M109.034355
– volume: 193
  start-page: 6090
  issue: 12
  year: 2014
  ident: ref38
  article-title: TRAM Is Required for TLR2 Endosomal Signaling to Type I IFN Induction
  publication-title: Journal of Immunology
  doi: 10.4049/jimmunol.1401605
– volume: 118
  start-page: 4199
  issue: 15
  year: 2011
  ident: ref34
  article-title: Alternative activation of macrophages by IL-4 enhances the proteolytic capacity of their phagosomes through synergistic mechanisms
  publication-title: Blood
  doi: 10.1182/blood-2011-01-328906
– volume: 43
  start-page: e47
  issue: 7
  year: 2015
  ident: ref52
  article-title: limma powers differential expression analyses for RNA-sequencing and microarray studies
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkv007
– volume: 10
  start-page: 223
  issue: 1
  year: 1988
  ident: ref1
  article-title: Immunity in Infective Diseases, (Reprinted from Immunity in Infective Diseases, 1905)
  publication-title: Rev Infect Dis
– year: 2015
  ident: ref22
  article-title: CD14, TLR4 and TRAM Show Different Trafficking Dynamics During LPS Stimulation
  publication-title: Traffic
– volume: 33
  start-page: 583
  issue: 4
  year: 2010
  ident: ref10
  article-title: The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes
  publication-title: Immunity
  doi: 10.1016/j.immuni.2010.09.010
– volume: 23
  start-page: 409
  issue: 4
  year: 2005
  ident: ref32
  article-title: Phagosome maturation proceeds independently of stimulation of toll-like receptors 2 and 4
  publication-title: Immunity
  doi: 10.1016/j.immuni.2005.09.007
– volume: 56
  start-page: 45
  issue: 1
  year: 2007
  ident: ref43
  article-title: Optimized THP-1 differentiation is required for the detection of responses to weak stimuli
  publication-title: Inflamm Res
  doi: 10.1007/s00011-007-6115-5
– volume: 12
  start-page: 115
  issue: 2
  year: 2015
  ident: ref51
  article-title: Orchestrating high-throughput genomic analysis with Bioconductor
  publication-title: Nat Methods
  doi: 10.1038/nmeth.3252
– volume: 25
  start-page: 3330
  issue: 21
  year: 2014
  ident: ref35
  article-title: Contrasting phagosome pH regulation and maturation in human M1 and M2 macrophages
  publication-title: Molecular biology of the cell
  doi: 10.1091/mbc.e14-05-0967
– volume: 2
  start-page: 107
  issue: 2
  year: 2001
  ident: ref11
  article-title: Rab proteins as membrane organizers
  publication-title: Nature reviews Molecular cell biology
  doi: 10.1038/35052055
– volume: 110
  start-page: 19908
  issue: 49
  year: 2013
  ident: ref23
  article-title: Structures and interface mapping of the TIR domain-containing adaptor molecules involved in interferon signaling
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.1222811110
– volume: 217
  start-page: 1411
  issue: 4
  year: 2018
  ident: ref44
  article-title: SLAMF1 is required for TLR4-mediated TRAM-TRIF-dependent signaling in human macrophages
  publication-title: J Cell Biol
  doi: 10.1083/jcb.201707027
– volume: 9
  start-page: 361
  issue: 4
  year: 2008
  ident: ref18
  article-title: TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta
  publication-title: Nature immunology
  doi: 10.1038/ni1569
– volume: 474
  start-page: 1163
  issue: 7
  year: 2017
  ident: ref28
  article-title: Identification of TBK1 complexes required for the phosphorylation of IRF3 and the production of interferon beta
  publication-title: Biochem J
  doi: 10.1042/BCJ20160992
– volume: 8
  year: 2018
  ident: ref8
  article-title: Rab GTPase regulation of bacteria and protozoa phagocytosis occurs through the modulation of phagocytic receptor surface expression
  publication-title: Sci Rep-Uk
– volume: 7
  start-page: 353
  issue: 5
  year: 2007
  ident: ref31
  article-title: The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling
  publication-title: Nature reviews Immunology
  doi: 10.1038/nri2079
SSID ssj0041316
Score 2.4363205
Snippet Phagocytosis is a complex process that eliminates microbes and is performed by specialised cells such as macrophages. Toll-like receptor 4 (TLR4) is expressed...
SourceID plos
doaj
pubmedcentral
cristin
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1007684
SubjectTerms Actin
Activation
Adapters
Adaptor Proteins, Signal Transducing - metabolism
Adaptor Proteins, Signal Transducing - physiology
Animals
Bacteria
Biology and Life Sciences
Cancer
Carrier Proteins - metabolism
Carrier Proteins - physiology
cdc42 GTP-Binding Protein
Cdc42 protein
Cellular signal transduction
Cytological research
E coli
Endocytosis
Endosomes
Escherichia coli
Escherichia coli - pathogenicity
Funding
G proteins
Gram-negative bacteria
HEK293 Cells
Hospitals
Humans
Immune system
Immunology
Inflammation
Interferon Regulatory Factor-3
Light rail transit
Lipopolysaccharides
Macrophages
Macrophages - immunology
Macrophages - metabolism
Medical research
Medicine
Medicine and Health Sciences
Membrane Proteins - metabolism
Membrane Proteins - physiology
Mice
Mice, Inbred C57BL
Microorganisms
Monocytes
Myeloid Differentiation Factor 88
Phagocytes
Phagocytosis
Phagocytosis - physiology
Physiological aspects
Primary Cell Culture
Protein Transport
Protein-protein interactions
Proteins
rab GTP-Binding Proteins
rac1 GTP-Binding Protein
Rac1 protein
Research and Analysis Methods
Signal Transduction
Software
Staphylococcus aureus
Staphylococcus aureus - pathogenicity
Staphylococcus aureus infections
THP-1 Cells
TLR4
TLR4 protein
Toll-Like Receptor 4 - metabolism
Toll-like receptors
SummonAdditionalLinks – databaseName: DOAJ Open Access Full Text
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Nb9QwELXQSpW4IL43UJBBSJxCN7ETO8cFUQqiPSxbqTfLdpztSm0SNdnD3vnhzDjeVYOKeuEajyN5ZjJ-44zfEPIBtvhZmXEb51IXMU9NGRtp0jgxgmXSSMssnkOenuUn5_zHRXZxq9UX1oQN9MCD4o58lyzAtcnMci6sk9JZLrVJuHZcmAqjL-x5u2RqiMEQmX3TU2yKEwuW5-HSHBPJUbDRp7bVva8RyJHZ9MD6b6oebU-exX8fqyftVdPdBUT_rqe8tUEdPyaPArKk82FFT8gDVz8lB0Ovye0z8hscgi5_LjjVpW4h06bLxfyUhlL1jgIQpO2lXjV22zfduqNNRb_d6Ou4ditPDk7NQOysqdlSZJnw96vqFcWjXD99AfpK4uHIZCThySDWNU2fk_Pjr8svJ3FowRDbXGZ9bItclACCnC09NdtMa86YSI3JkSqsYEhJhtfRTSlsZpOqMlLwwlSlqIrEOvaCTOqmdlNCkVswS03quIUkzgrjypSXkJ9i4OCJi8g02EDV4P3IXJqlCgBOlkWE7YyibKAuxw4aV8r_jxOQwgw6VmhUFYwakXg_qx2oO-6R_4z23ssi8bZ_AO6ogjuq-9wxIu_RWxRSa9RYu7PSm65T33-dqXkmEW8BbPin0GIk9DEIVQ0s1upwXwK0iZRdI8nDkSQECDsanqLn7tbcqRTTSgaRu4CZO2--e_jdfhhfivV4tWs2IJMUgPxAahaRl4Pz7_XGYONikBdHRIw-i5FixyP1-tIzmwM8lpnMX_0PS7wmDwHcFkO94CGZ9Dcb9wYAZG_e-ljxBwAzahw
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Health & Medical Collection
  dbid: 7X7
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwhV1Lj9MwELagaBEXBMujgQUZhMTJbJM4sXNCBbEsiO6hdKW9RbbjdCstSWjaQ-_8cGYcNxC0wLWeRI3n4W_s8TeEvIIlflIk3LBUqozxSBdMSx2xUIs4kVqa2OA-5OwsPT3nny-SC7_h1vqyyn1MdIG6qA3ukR9HiIVjMLfsbfOdYdcoPF31LTRukltIXYZWLS76hAvis2t9iq1xmIjT1F-di0V47DX1pmnUxlUKpMhvemCcZ1WDRcpx-fcRe9Rc1e11cPTPqsrflqmTe-Sux5d02hnEfXLDVofkoOs4uTskt2f-LP0B-QEWQhdf5pyqQjWQetPFfDqjvna9pYAMaXOplrXZbep21dK6pB_X6hur7NKxhVPdMT0rqncUaSfchatqSXFv1z0-VzoMWbeHMpBw7BCrikYPyfnJh8X7U-Z7MjCTymTDTJaKAlCRNYXjapsoxeNYRFqnyB2WxchRhvfTdSFMYsKy1FLwTJeFKLPQ2PgRGVV1ZceEItlgEunIcgNZnRHaFhEvIGHFSMJDG5CxV0degTsglWkS5YB4kiQg8V4_ufFc5thS4yp3B3QCcppuunPUb-71GxDWP9V0XB7_kX-Hqu9lkYnb_VCvl7l37Nx1cYO8K5wYzoWxUlrDJUwvV5YLXQbkJRpOjlwbFRbzLNW2bfNPX8_yaSIRgAGO-KvQfCD02guVNXysUf4CBcwmcngNJI8GkhAxzGB4jEa8_-Y2_-Vb8OTesK8fftEP40uxQK-y9RZkwgygIEhNAvK484N-3mJYyWJIlAMiBh4ymNjhSLW6dFTngJdlItMn__5bT8kdwLFZVxp4REab9dY-A6y40c9dQPgJINRlOQ
  priority: 102
  providerName: ProQuest
Title The TLR4 adaptor TRAM controls the phagocytosis of Gram-negative bacteria by interacting with the Rab11-family interacting protein 2
URI https://www.ncbi.nlm.nih.gov/pubmed/30883606
https://www.proquest.com/docview/2251134889
https://www.proquest.com/docview/2194151340
http://hdl.handle.net/10852/74355
https://pubmed.ncbi.nlm.nih.gov/PMC6438586
https://doaj.org/article/0154430610c447ce88ec48ab14ae47bf
http://dx.doi.org/10.1371/journal.ppat.1007684
Volume 15
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwjV3db9MwELe2Tki8IL4bGJVBSDxlahIndh4Q6tDGQLRCpZX2FtmO01XqktC0En3nD-fOSSOCOsFrfI7ku_P5d_74HSFvYYkfpiHTbiRk7DJfpa4Sync9xYNQKKEDjfuQ40l0NWdfrsPrI7Kv2doosDqY2mE9qfl6dfbzx-4DTPj3tmoD9_adzspSbuypfyTYMTmBtYljTYMxa88VIGLbYqhYLMflQRQ1j-nu-guAYm3nWt5Ztiy7fxvDe-WqqA4B1L_vWf6xcF0-JA8axElHtYs8Ikcmf0zu1TUod0_IL3AUOvs6ZVSmsoQMnM6mozFtrrBXFAAiLW_kotC7TVEtK1pk9NNa3rq5WVjScKpqwmdJ1Y4i-4R9d5UvKG7x2u5TqTzPrbdSOhKWJGKZU_8pmV9ezD5euU1pBldHIty4Oo54CuDI6NRStg2lZEHAfaUipBCLA6Qqw2fqKuU61F6WKcFZrLKUZ7GnTfCM9PIiN31CkXMw9JVvmIbkTnNlUp-lkLdiQGGecUi_sUGSw6xARtPQTwD4hKFDgr1REt1QmmNljVViz-k4pDa1jhM0atIY1SFu26usKT3-IX-O9m5lkZDbfijWi6SZ34kt5gbplzfUjHFthDCaCVAvk4ZxlTnkDXpLgpQbOd7pWchtVSWfv0-SUSgQhwGcuFNo2hF61whlBQxWy-YdBWgTqbw6kqcdSQgcutPcR8_dj7lKfEw3A4joMfTce_Ph5tdtM_4U7-nlptiCjBcDIgSpoUOe187f6i2ABS2AfNkhvDMtOorttuTLG8t4DrBZhCJ68d9Df0nuA7KN68uCp6S3WW_NK0CPGzUgx_yaD8jJ-cXk23Rg92AGNkj8BhENb2A
linkProvider Scholars Portal
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV1Lj9MwELaWogUuCJZHCwsYBOIUtkmcODkgVB5Ly7Z7KF2pN6_tON1KSxKaVqh3fg-_kRknLQQtcNprPYkaz3jmG3v8DSHPIcR3k4BpJ4xk7DBPJY6KlOe4ivtBpCLta9yHHB2H_RP2aRpMd8iPzV0YLKvc-ETrqJNc4x75gYdY2Adzi98UXx3sGoWnq5sWGpVZHJn1N0jZyteD96DfF553-GHyru_UXQUcHUbB0tFxyBOI60Ynlm2sKyXzfe4pFSL7VewjyxbesFYJ14F201RFnMUqTXgau9r48N4r5CoE3i4me3y6TfAgHthWq9iKx-F-GNZX9XzuHtSW8aoo5NJWJoTIp7qr7UrOGkHR9g7YRohWcZ6XF8HfP6s4fwuLh7fIzRrP0l5lgLfJjsn2yG7V4XK9R66N6rP7O-Q7WCSdDMeMykQWkOrTybg3onWtfEkBidLiTM5yvV7m5bykeUo_LuQXJzMzy05OVcUsLalaU6S5sBe8shnFvWT7-Fgq13WqPZuGhGWjmGfUu0tOLkVb90gryzPTJhTJDQNPeYZpyCI1VybxWAIJMnou5poOadfqEBksP6RODTwBCCsIOsTf6EfomjsdW3icC3sgyCGHqqZboH5Frd8OcbZPFRV3yH_k36Lqt7LI_G1_yBczUTsSYbvGQZ7ndjVjXJsoMppFML1MGsZV2iHP0HAEcntkWDw0k6uyFIPPx6IXRAj4ALf8VWjcEHpZC6U5fKyW9YUNmE3kDGtI7jckwUPpxnAbjXjzzaX4tZbhyY1hXzz8dDuML8WCwMzkK5BxY4CeINXtkPvVOtjOmw-R04fEvEN4Y4U0JrY5ks3PLLU64PMoiMIH__5bT8j1_mQ0FMPB8dFDcgMwdFyVJe6T1nKxMo8Apy7VY-scKDm9bG_0E1oloRQ
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3NT9RAFJ_gEogXo_jBKupoNJ7Kbttppz0YAwKCwIaskHAbZ6bThQTbSpeYvftX-df53nS6WoN64tp507Tzvmfe_B4hr8DFD7OIaS9OZOqxQGWeSlTg-YqHUaISHWrchzwcxbsn7ONpdLpAfrR3YbCssrWJ1lBnpcY98kGAsXAI4pYOclcWcbS186766mEHKTxpbdtpNCKyb2bfIH2r3-5tAa9fB8HO9vH7Xc91GPB0nERTT6cxz8DHG51Z5LGhlCwMeaBUjEhYaYiIW3jbWmVcR9rPc5Vwlqo843nqaxPCe2-RRY5ZUY8sbm6PjsatHwDvYBuvYmMej4dx7C7uhdwfODlZryo5tXUKMaKrLmmr10XHRdpOAnN_0asuyvq6YPjPms7fnOTOXXLHRbd0oxHHe2TBFCtkqel3OVshy4fuJP8--Q7ySY8PxozKTFaQ-NPj8cYhdZXzNYW4lFZnclLq2bSsz2ta5vTDpfziFWZiscqpanCmJVUziqAX9rpXMaG4s2ynj6Xyfa_ZwelQWGyK84IGD8jJjfDrIekVZWFWCUWowyhQgWEackrNlckClkG6jHaM-aZPVh07RAHKiECqUSAg3oqiPglb_gjtkNSxoceFsMeDHDKqZrkF8lc4_vaJN59VNUgi_6HfRNbPaREH3D4oLyfCmRVhe8hB1ucPNWNcmyQxmiWwvEwaxlXeJy9RcAQifRSoMxN5Vddi79NIbEQJhn8QxfyVaNwheuOI8hJ-Vkt3fQNWExHEOpRrHUqwV7ozvIpC3P5zLX5pNsxsBfv64RfzYXwplgcWprwCGj-FQBSohn3yqNGD-bqF4EdDSNP7hHc0pLOw3ZHi_MwCrUO0nkRJ_Pjfn_WcLIMlEgd7o_0n5DYE1GlTo7hGetPLK_MUgtapeuasAyWfb9og_QRJfKav
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=The+TLR4+adaptor+TRAM+controls+the+phagocytosis+of+Gram-negative+bacteria+by+interacting+with+the+Rab11-family+interacting+protein+2&rft.jtitle=PLoS+pathogens&rft.au=Skjesol%2C+Astrid&rft.au=Yurchenko%2C+Mariia&rft.au=B%C3%B6sl%2C+Korbinian&rft.au=Gravastrand%2C+Caroline&rft.date=2019-03-01&rft.pub=Public+Library+of+Science&rft.issn=1553-7366&rft.volume=15&rft.issue=3&rft_id=info:doi/10.1371%2Fjournal.ppat.1007684&rft.externalDocID=A580820341
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1553-7374&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1553-7374&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1553-7374&client=summon