Exploiting a host-commensal interaction to promote intestinal barrier function and enteric pathogen tolerance

Commensal intestinal bacteria can prevent pathogenic infection; however, limited knowledge of the mechanisms by which individual bacterial species contribute to pathogen resistance has restricted their potential for therapeutic application. Here, we examined how colonization of mice with a human com...

Full description

Saved in:
Bibliographic Details
Published inScience immunology Vol. 1; no. 3
Main Authors Pedicord, Virginia A, Lockhart, Ainsley A K, Rangan, Kavita J, Craig, Jeffrey W, Loschko, Jakob, Rogoz, Aneta, Hang, Howard C, Mucida, Daniel
Format Journal Article
LanguageEnglish
Published United States 01.09.2016
Online AccessGet more information

Cover

Loading…
Abstract Commensal intestinal bacteria can prevent pathogenic infection; however, limited knowledge of the mechanisms by which individual bacterial species contribute to pathogen resistance has restricted their potential for therapeutic application. Here, we examined how colonization of mice with a human commensal protects against enteric infections. We show that improves host intestinal epithelial defense programs to limit serotype Typhimurium pathogenesis in multiple models of susceptibility. protection is mediated by a unique peptidoglycan hydrolase, SagA, and requires epithelial expression of pattern recognition receptor components and antimicrobial peptides. Ectopic expression of SagA in non-protective and probiotic bacteria is sufficient to enhance intestinal barrier function and confer resistance against Typhimurium and pathogenesis. These studies demonstrate that specific factors from commensal bacteria can be used to improve host barrier function and limit the pathogenesis of distinct enteric infections.
AbstractList Commensal intestinal bacteria can prevent pathogenic infection; however, limited knowledge of the mechanisms by which individual bacterial species contribute to pathogen resistance has restricted their potential for therapeutic application. Here, we examined how colonization of mice with a human commensal protects against enteric infections. We show that improves host intestinal epithelial defense programs to limit serotype Typhimurium pathogenesis in multiple models of susceptibility. protection is mediated by a unique peptidoglycan hydrolase, SagA, and requires epithelial expression of pattern recognition receptor components and antimicrobial peptides. Ectopic expression of SagA in non-protective and probiotic bacteria is sufficient to enhance intestinal barrier function and confer resistance against Typhimurium and pathogenesis. These studies demonstrate that specific factors from commensal bacteria can be used to improve host barrier function and limit the pathogenesis of distinct enteric infections.
Author Pedicord, Virginia A
Craig, Jeffrey W
Rogoz, Aneta
Rangan, Kavita J
Mucida, Daniel
Loschko, Jakob
Hang, Howard C
Lockhart, Ainsley A K
Author_xml – sequence: 1
  givenname: Virginia A
  surname: Pedicord
  fullname: Pedicord, Virginia A
  organization: Laboratory of Chemical Biology and Microbial Pathogenesis, The Rockefeller University, New York, NY, USA
– sequence: 2
  givenname: Ainsley A K
  surname: Lockhart
  fullname: Lockhart, Ainsley A K
  organization: Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA
– sequence: 3
  givenname: Kavita J
  surname: Rangan
  fullname: Rangan, Kavita J
  organization: Laboratory of Chemical Biology and Microbial Pathogenesis, The Rockefeller University, New York, NY, USA
– sequence: 4
  givenname: Jeffrey W
  surname: Craig
  fullname: Craig, Jeffrey W
  organization: Department of Pathology, Brigham & Women's Hospital, Boston, MA, USA
– sequence: 5
  givenname: Jakob
  surname: Loschko
  fullname: Loschko, Jakob
  organization: Laboratory of Molecular Immunology, The Rockefeller University, New York, NY, USA
– sequence: 6
  givenname: Aneta
  surname: Rogoz
  fullname: Rogoz, Aneta
  organization: Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA
– sequence: 7
  givenname: Howard C
  surname: Hang
  fullname: Hang, Howard C
  organization: Laboratory of Chemical Biology and Microbial Pathogenesis, The Rockefeller University, New York, NY, USA
– sequence: 8
  givenname: Daniel
  surname: Mucida
  fullname: Mucida, Daniel
  organization: Laboratory of Mucosal Immunology, The Rockefeller University, New York, NY, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28580440$$D View this record in MEDLINE/PubMed
BookMark eNpNj81KAzEUhYNUbK19AReSF5h6k2Yy6VJK_YGCG12X_LaRSTJkMqBv79QquDqXe8534FyjSUzRInRLYEkI5fe99j6EIaZ2KaVvmhW9QDPKGqjWjIvJv3uKFn3_AQBEUNJwdoWmVNQCGIMZCtvPrk2--HjAEh9TXyqdQrCxly32sdgsdfEp4pJwl1NIxf68-5EYE0rm7G3GbojnmIwG2xPmNe5kOaaDPbHt2BO1vUGXTra9XfzqHL0_bt82z9Xu9ell87CrNANaKlo7YzRlupakobKunVZarxU3FqThajRWYIFzcI5RpQUBtWocY9wIARroHN2de7tBBWv2XfZB5q_93276DXQEYyM
CitedBy_id crossref_primary_10_1111_nyas_14526
crossref_primary_10_3389_fmicb_2022_863407
crossref_primary_10_1093_procel_pwad016
crossref_primary_10_3390_nu15194241
crossref_primary_10_7554_eLife_95297_3
crossref_primary_10_7554_eLife_95297
crossref_primary_10_3389_fcimb_2021_716299
crossref_primary_10_1002_cti2_1095
crossref_primary_10_1002_ps_6769
crossref_primary_10_1093_ecco_jcc_jjaa065
crossref_primary_10_1016_j_chembiol_2022_11_001
crossref_primary_10_1016_j_ijfoodmicro_2024_110714
crossref_primary_10_1126_sciadv_abf0677
crossref_primary_10_1128_AEM_00844_21
crossref_primary_10_1021_acssynbio_2c00583
crossref_primary_10_1039_D3LC01027A
crossref_primary_10_7554_eLife_45343
crossref_primary_10_1021_acs_biochem_0c00755
crossref_primary_10_1126_science_aaf3552
crossref_primary_10_3390_foods13060874
crossref_primary_10_1126_science_abo2366
crossref_primary_10_3390_cancers14153563
crossref_primary_10_1111_imcb_12798
crossref_primary_10_3389_fmicb_2022_1071255
crossref_primary_10_1038_s41589_022_01122_3
crossref_primary_10_1016_j_coi_2019_11_004
crossref_primary_10_1016_j_tibs_2017_08_005
crossref_primary_10_1016_j_neo_2022_100818
crossref_primary_10_1186_s13099_018_0259_4
crossref_primary_10_3390_ijms25105405
crossref_primary_10_1002_cbic_202200693
crossref_primary_10_3389_fbioe_2020_00558
crossref_primary_10_1128_mBio_02587_19
crossref_primary_10_1002_imt2_196
crossref_primary_10_1016_j_cell_2023_12_014
crossref_primary_10_1038_s41551_019_0397_0
crossref_primary_10_2478_am_2023_0014
crossref_primary_10_3390_pathogens7030057
crossref_primary_10_1016_j_psj_2019_12_046
crossref_primary_10_1002_cbic_201900535
crossref_primary_10_3389_fimmu_2019_01107
crossref_primary_10_1021_acs_biochem_1c00758
crossref_primary_10_1111_imm_13117
crossref_primary_10_3389_fimmu_2021_708472
crossref_primary_10_3389_fcimb_2021_638014
crossref_primary_10_1016_j_chemosphere_2021_131120
crossref_primary_10_1016_j_chom_2023_08_002
crossref_primary_10_1039_C9FO01651A
crossref_primary_10_1039_D2FO03467K
crossref_primary_10_1021_acschembio_0c00618
crossref_primary_10_1126_science_abc9113
crossref_primary_10_1186_s12864_023_09945_7
crossref_primary_10_1021_acschembio_8b01038
crossref_primary_10_1146_annurev_micro_090816_093549
crossref_primary_10_1021_acs_biochem_2c00120
crossref_primary_10_1016_j_scitotenv_2020_137382
crossref_primary_10_3390_jcm11071916
crossref_primary_10_4049_jimmunol_2100215
crossref_primary_10_3390_antibiotics11070857
crossref_primary_10_1016_j_jare_2023_03_008
ContentType Journal Article
DBID NPM
DOI 10.1126/sciimmunol.aai7732
DatabaseName PubMed
DatabaseTitle PubMed
DatabaseTitleList PubMed
Database_xml – sequence: 1
  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 no_fulltext_linktorsrc
Discipline Biology
EISSN 2470-9468
ExternalDocumentID 28580440
Genre Journal Article
GrantInformation_xml – fundername: NIGMS NIH HHS
  grantid: R01 GM103593
GroupedDBID 0R~
53G
ACGFS
AJGZS
ALMA_UNASSIGNED_HOLDINGS
BCGUY
BKF
C45
EBS
EJD
NPM
O9-
OGROG
OVD
RHI
TEORI
ID FETCH-LOGICAL-c402t-25fddc24c5a172a55fcbcc9b6de0ad6b4c530e0660ff42bc810b37f446d880c02
ISSN 2470-9468
IngestDate Thu May 23 23:23:29 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 3
Language English
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c402t-25fddc24c5a172a55fcbcc9b6de0ad6b4c530e0660ff42bc810b37f446d880c02
OpenAccessLink https://europepmc.org/articles/pmc5453653?pdf=render
PMID 28580440
ParticipantIDs pubmed_primary_28580440
PublicationCentury 2000
PublicationDate 2016-09-01
PublicationDateYYYYMMDD 2016-09-01
PublicationDate_xml – month: 09
  year: 2016
  text: 2016-09-01
  day: 01
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Science immunology
PublicationTitleAlternate Sci Immunol
PublicationYear 2016
References 22424233 - Cell. 2012 Mar 16;148(6):1258-70
11303279 - Clin Infect Dis. 2001 May 1;32(9):1384-5
21831747 - Benef Microbes. 2010 Mar;1(1):11-29
26777404 - Cell. 2016 Jan 28;164(3):378-91
20182457 - Nat Rev Immunol. 2010 Mar;10(3):159-69
19930635 - Gut Pathog. 2009 Nov 23;1(1):19
24096337 - Nat Rev Immunol. 2013 Nov;13(11):790-801
24958710 - Infect Immun. 2014 Sep;82(9):3753-63
19812981 - Curr Top Microbiol Immunol. 2009;337:93-127
20098461 - Nat Rev Immunol. 2010 Feb;10 (2):131-44
21962867 - Int J Food Microbiol. 2011 Dec 2;151(2):125-40
22582016 - Science. 2012 Jun 8;336(6086):1325-9
22162005 - Inflamm Bowel Dis. 2012 Aug;18(8):1434-46
18509436 - Nature. 2008 May 29;453(7195):620-5
23115039 - Infect Immun. 2013 Jan;81(1):259-70
12933846 - Infect Immun. 2003 Sep;71(9):5033-41
25088769 - Immunity. 2014 Aug 21;41(2):311-24
24016187 - Annu Rev Genet. 2013;47:377-404
19343057 - Nat Rev Immunol. 2009 May;9(5):313-23
12427955 - Microbiology. 2002 Nov;148(Pt 11):3651-60
22896700 - J Biol Chem. 2012 Oct 5;287(41):34844-55
25714160 - N Engl J Med. 2015 Feb 26;372(9):825-34
27708039 - Science. 2016 Sep 23;353(6306):1434-1437
21321077 - Infect Immun. 2011 Apr;79(4):1536-45
23442379 - J Anim Sci Biotechnol. 2013 Feb 25;4(1):5
8124710 - Cell. 1994 Feb 25;76(4):717-24
21270894 - Nature. 2011 Jan 27;469(7331):543-7
20198339 - Int J Oncol. 2010 Apr;36(4):941-53
27025632 - Antibiotics (Basel). 2015 Sep 24;4(4):411-23
20382864 - Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7722-7
20207762 - J Bacteriol. 2010 May;192(9):2469-70
25417164 - Cell. 2014 Nov 6;159(4):896-910
15692051 - Science. 2005 Feb 4;307(5710):731-4
20731667 - Cell Microbiol. 2010 Oct;12(10):1389-97
24995874 - Annu Rev Microbiol. 2014;68:217-35
22177113 - Curr Opin Microbiol. 2012 Feb;15(1):57-62
18524406 - Int J Food Microbiol. 2008 Jul 31;125(3):286-92
22224764 - Annu Rev Immunol. 2012;30:759-95
25242213 - Mol Immunol. 2015 Feb;63(2):193-202
18724361 - Nature. 2008 Oct 9;455(7214):804-7
26853748 - Cell Metab. 2016 Mar 8;23 (3):413-26
23842501 - Nature. 2013 Aug 8;500(7461):232-6
26176396 - N Engl J Med. 2015 Jul 16;373(3):287-8
23828891 - Science. 2013 Aug 2;341(6145):569-73
19364837 - Infect Immun. 2009 Jul;77(7):2635-42
26195303 - Annu Rev Microbiol. 2015;69:145-66
21694778 - PLoS One. 2011;6(6):e20749
20615996 - Proc Natl Acad Sci U S A. 2011 Mar 15;108 Suppl 1:4659-65
19235151 - Curr Protoc Microbiol. 2009 Feb;Chapter 9:Unit9A.1
23435982 - J Bacteriol. 2013 May;195(9):2004-10
16000463 - J Clin Microbiol. 2005 Jul;43(7):3380-9
12704158 - Infect Immun. 2003 May;71(5):2839-58
23511135 - J Trauma Acute Care Surg. 2013 Apr;74(4):983-89; discussion 989-90
21803916 - Appl Environ Microbiol. 2011 Sep;77(18):6495-501
19159975 - Curr Microbiol. 2009 May;58(5):464-71
27541692 - PLoS Biol. 2016 Aug 19;14(8):e1002533
21219177 - Annu Rev Immunol. 2011;29:415-45
16869830 - Cell Microbiol. 2006 Dec;8(12):1946-57
23955152 - Nature. 2013 Sep 19;501(7467):426-9
25337874 - Nature. 2015 Jan 8;517(7533):205-8
23922847 - PLoS One. 2013 Jul 29;8(7):e69901
26822608 - Science. 2016 Feb 26;351(6276):933-9
21998396 - Science. 2011 Oct 14;334(6053):255-8
24315484 - Cell. 2013 Dec 19;155(7):1451-63
16362887 - J Infect Dis. 2006 Jan 15;193(2):231-40
27022930 - PLoS Pathog. 2016 Mar 29;12(3):e1005530
24345802 - Mucosal Immunol. 2014 Jul;7(4):939-47
19174417 - Gut. 2009 Jun;58(6):771-6
23932219 - Lancet. 2013 Oct 12;382(9900):1249-57
17616592 - J Bacteriol. 2007 Oct;189(19):6763-72
25607457 - Immunity. 2015 Jan 20;42(1):28-39
16922084 - Curr Top Microbiol Immunol. 2006;308:1-18
References_xml
SSID ssj0001821764
Score 2.3117328
Snippet Commensal intestinal bacteria can prevent pathogenic infection; however, limited knowledge of the mechanisms by which individual bacterial species contribute...
SourceID pubmed
SourceType Index Database
Title Exploiting a host-commensal interaction to promote intestinal barrier function and enteric pathogen tolerance
URI https://www.ncbi.nlm.nih.gov/pubmed/28580440
Volume 1
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9NAEF6lICQuiDeUgvbADTmy12t7c6wqqopHD6hFvVWzr2CJOFFkkODv8Ec7-3KcKIjHxYp25fVjPs_OTOabIeQ1NDmgpaCyotHooJRSZICGdSZNAcwWRQ2lYyN_PK_PLvm7q-pqMvk1ylr61sup-rmXV_I_UsUxlKtjyf6DZIdFcQB_o3zxiBLG41_J2CfQtT5xGd44ukaGV1mgY-oraThucWgEjvblyqfdGT-MX7WzQSWsfbs6t7X1KSvZleh0yfWuU_ESL4znfjXrARrRjE0aoXXskq3AvGv9oWK-_Od2PW8d62tAyQfUvl8gsISO284FzFEzDZHWT9DNQ0D2PXxve9j8Z3WyhnY-Yp6FvMAUrijqIR8rajXGmzyb8dBLZ2r2jCW1PEJfuV_Zp_aU8WGnAG3ThHDpSPqrhRc_E5Vw_bX_PLtTgDtNHZCDRjgleh4DQj6MJ9Cn80XKhofYpmbt3JsrPh3X23FkvEFzcZ_ci54IPQ6wekAmpntI7oTepD8ekcUGXBToNrjoCFy0X9IILroBF43goglcFMFFI7hoAhcdwPWYXJ6-vTg5y2JvjkzxnPUZq6zWinFVAZrAUFVWSaVmstYmB11LnChzg_Zsbi1nUokil2VjOa817hgqZ0_IrW7ZmWeEltrgIlq60od8JkphmGZ4biFsgbuNfU6ehvd0vQoFWK7TGzz87cwLcncDviNy2-IXb16i-djLV16AN9cFddU
link.rule.ids 786
linkProvider National Library of Medicine
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=Exploiting+a+host-commensal+interaction+to+promote+intestinal+barrier+function+and+enteric+pathogen+tolerance&rft.jtitle=Science+immunology&rft.au=Pedicord%2C+Virginia+A&rft.au=Lockhart%2C+Ainsley+A+K&rft.au=Rangan%2C+Kavita+J&rft.au=Craig%2C+Jeffrey+W&rft.date=2016-09-01&rft.issn=2470-9468&rft.eissn=2470-9468&rft.volume=1&rft.issue=3&rft_id=info:doi/10.1126%2Fsciimmunol.aai7732&rft_id=info%3Apmid%2F28580440&rft_id=info%3Apmid%2F28580440&rft.externalDocID=28580440
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2470-9468&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2470-9468&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2470-9468&client=summon