Literature DB >> 25144609

Commensal-pathogen interactions in the intestinal tract: lactobacilli promote infection with, and are promoted by, helminth parasites.

Lisa A Reynolds1, Katherine A Smith2, Kara J Filbey2, Yvonne Harcus2, James P Hewitson2, Stephen A Redpath3, Yanet Valdez4, María J Yebra5, B Brett Finlay6, Rick M Maizels2.   

Abstract

The intestinal microbiota are pivotal in determining the developmental, metabolic and immunological status of the mammalian host. However, the intestinal tract may also accommodate pathogenic organisms, including helminth parasites which are highly prevalent in most tropical countries. Both microbes and helminths must evade or manipulate the host immune system to reside in the intestinal environment, yet whether they influence each other's persistence in the host remains unknown. We now show that abundance of Lactobacillus bacteria correlates positively with infection with the mouse intestinal nematode parasite, Heligmosomoides polygyrus, as well as with heightened regulatory T cell (Treg) and Th17 responses. Moreover, H. polygyrus raises Lactobacillus species abundance in the duodenum of C57BL/6 mice, which are highly susceptible to H. polygyrus infection, but not in BALB/c mice, which are relatively resistant. Sequencing of samples at the bacterial gyrB locus identified the principal Lactobacillus species as L. taiwanensis, a previously characterized rodent commensal. Experimental administration of L. taiwanensis to BALB/c mice elevates regulatory T cell frequencies and results in greater helminth establishment, demonstrating a causal relationship in which commensal bacteria promote infection with an intestinal parasite and implicating a bacterially-induced expansion of Tregs as a mechanism of greater helminth susceptibility. The discovery of this tripartite interaction between host, bacteria and parasite has important implications for both antibiotic and anthelmintic use in endemic human populations.

Entities:  

Keywords:  Commensal; Duodenum; Lactobacillus; Microbiota; Nematode; Th17; Treg

Mesh:

Year:  2014        PMID: 25144609      PMCID: PMC4822684          DOI: 10.4161/gmic.32155

Source DB:  PubMed          Journal:  Gut Microbes        ISSN: 1949-0976


  58 in total

Review 1.  Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota.

Authors:  Karen Smith; Kathy D McCoy; Andrew J Macpherson
Journal:  Semin Immunol       Date:  2006-11-21       Impact factor: 11.130

2.  Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice.

Authors:  Paul Forsythe; Mark D Inman; John Bienenstock
Journal:  Am J Respir Crit Care Med       Date:  2007-01-04       Impact factor: 21.405

3.  Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis.

Authors:  Aurélien Trompette; Eva S Gollwitzer; Koshika Yadava; Anke K Sichelstiel; Norbert Sprenger; Catherine Ngom-Bru; Carine Blanchard; Tobias Junt; Laurent P Nicod; Nicola L Harris; Benjamin J Marsland
Journal:  Nat Med       Date:  2014-01-05       Impact factor: 53.440

4.  Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes.

Authors:  A H Franks; H J Harmsen; G C Raangs; G J Jansen; F Schut; G W Welling
Journal:  Appl Environ Microbiol       Date:  1998-09       Impact factor: 4.792

5.  Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses.

Authors:  Timothy W Hand; Liliane M Dos Santos; Nicolas Bouladoux; Michael J Molloy; Antonio J Pagán; Marion Pepper; Craig L Maynard; Charles O Elson; Yasmine Belkaid
Journal:  Science       Date:  2012-08-23       Impact factor: 47.728

6.  Suppression of type 2 immunity and allergic airway inflammation by secreted products of the helminth Heligmosomoides polygyrus.

Authors:  Henry J McSorley; Mary T O'Gorman; Natalie Blair; Tara E Sutherland; Kara J Filbey; Rick M Maizels
Journal:  Eur J Immunol       Date:  2012-08-08       Impact factor: 5.532

Review 7.  Interactions between the microbiota and the immune system.

Authors:  Lora V Hooper; Dan R Littman; Andrew J Macpherson
Journal:  Science       Date:  2012-06-06       Impact factor: 47.728

8.  Proteomic analysis of secretory products from the model gastrointestinal nematode Heligmosomoides polygyrus reveals dominance of venom allergen-like (VAL) proteins.

Authors:  James P Hewitson; Yvonne Harcus; Janice Murray; Maaike van Agtmaal; Kara J Filbey; John R Grainger; Stephen Bridgett; Mark L Blaxter; Peter D Ashton; David A Ashford; Rachel S Curwen; R Alan Wilson; Adam A Dowle; Rick M Maizels
Journal:  J Proteomics       Date:  2011-06-29       Impact factor: 4.044

9.  Parasite-induced TH1 cells and intestinal dysbiosis cooperate in IFN-γ-dependent elimination of Paneth cells.

Authors:  Megan Raetz; Sun-Hee Hwang; Cara L Wilhelm; Donna Kirkland; Alicia Benson; Carolyn R Sturge; Julie Mirpuri; Shipra Vaishnava; Baidong Hou; Anthony L Defranco; Christopher J Gilpin; Lora V Hooper; Felix Yarovinsky
Journal:  Nat Immunol       Date:  2012-12-23       Impact factor: 25.606

10.  Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation.

Authors:  Nicholas Arpaia; Clarissa Campbell; Xiying Fan; Stanislav Dikiy; Joris van der Veeken; Paul deRoos; Hui Liu; Justin R Cross; Klaus Pfeffer; Paul J Coffer; Alexander Y Rudensky
Journal:  Nature       Date:  2013-11-13       Impact factor: 49.962

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  93 in total

1.  Role of coaggregation in the pathogenicity and prolonged colonisation of Vibrio cholerae.

Authors:  Yien Shin Toh; Soo Ling Yeoh; Ivan Kok Seng Yap; Cindy Shuan Ju Teh; Thin Thin Win; Kwai Lin Thong; Chun Wie Chong
Journal:  Med Microbiol Immunol       Date:  2019-07-01       Impact factor: 3.402

Review 2.  Helminths and intestinal barrier function.

Authors:  Derek M McKay; Adam Shute; Fernando Lopes
Journal:  Tissue Barriers       Date:  2017-01-02

Review 3.  Metabolites: deciphering the molecular language between DCs and their environment.

Authors:  Lucía Minarrieta; Peyman Ghorbani; Tim Sparwasser; Luciana Berod
Journal:  Semin Immunopathol       Date:  2016-12-05       Impact factor: 9.623

4.  Worm expulsion is independent of alterations in composition of the colonic bacteria that occur during experimental Hymenolepis diminuta-infection in mice.

Authors:  Adam Shute; Arthur Wang; Timothy S Jayme; Marc Strous; Kathy D McCoy; Andre G Buret; Derek M McKay
Journal:  Gut Microbes       Date:  2020-01-13

Review 5.  Cohabitation in the Intestine: Interactions among Helminth Parasites, Bacterial Microbiota, and Host Immunity.

Authors:  Lisa A Reynolds; B Brett Finlay; Rick M Maizels
Journal:  J Immunol       Date:  2015-11-01       Impact factor: 5.422

6.  The gut microbiota response to helminth infection depends on host sex and genotype.

Authors:  Fei Ling; Natalie Steinel; Jesse Weber; Lei Ma; Chris Smith; Decio Correa; Bin Zhu; Daniel Bolnick; Gaoxue Wang
Journal:  ISME J       Date:  2020-01-31       Impact factor: 10.302

Review 7.  Nematodes and human therapeutic trials for inflammatory disease.

Authors:  D E Elliott; J V Weinstock
Journal:  Parasite Immunol       Date:  2017-04-18       Impact factor: 2.280

8.  Enteric Helminths Promote Salmonella Coinfection by Altering the Intestinal Metabolome.

Authors:  Lisa A Reynolds; Stephen A Redpath; Sophie Yurist-Doutsch; Navkiran Gill; Eric M Brown; Joris van der Heijden; Tara P Brosschot; Jun Han; Natalie C Marshall; Sarah E Woodward; Yanet Valdez; Christoph H Borchers; Georgia Perona-Wright; B Brett Finlay
Journal:  J Infect Dis       Date:  2017-04-15       Impact factor: 5.226

9.  Specific Gut and Salivary Microbiota Patterns Are Linked With Different Cognitive Testing Strategies in Minimal Hepatic Encephalopathy.

Authors:  Jasmohan S Bajaj; Andrew Fagan; Melanie B White; James B Wade; Phillip B Hylemon; Douglas M Heuman; Michael Fuchs; Binu V John; Chathur Acharya; Masoumeh Sikaroodi; Patrick M Gillevet
Journal:  Am J Gastroenterol       Date:  2019-07       Impact factor: 10.864

Review 10.  Gut microorganisms as promising targets for the management of type 2 diabetes.

Authors:  Nathalie M Delzenne; Patrice D Cani; Amandine Everard; Audrey M Neyrinck; Laure B Bindels
Journal:  Diabetologia       Date:  2015-07-31       Impact factor: 10.122

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