User menu

A gut pathobiont synergizes with the microbiota to instigate inflammatory disease marked by immunoreactivity against other symbionts but not itself.

Bibliographic reference Gomes-Neto, João Carlos ; Kittana, Hatem ; Mantz, Sara ; Segura Munoz, Rafael R ; Schmaltz, Robert J ; et. al. A gut pathobiont synergizes with the microbiota to instigate inflammatory disease marked by immunoreactivity against other symbionts but not itself.. In: Scientific Reports, Vol. 7, p. 17707 (2017)
Permanent URL http://hdl.handle.net/2078.1/191934
  1. Huttenhower Curtis, Kostic Aleksandar D., Xavier Ramnik J., Inflammatory Bowel Disease as a Model for Translating the Microbiome, 10.1016/j.immuni.2014.05.013
  2. Sartor R. Balfour, Microbial Influences in Inflammatory Bowel Diseases, 10.1053/j.gastro.2007.11.059
  3. Frank D. N., St. Amand A. L., Feldman R. A., Boedeker E. C., Harpaz N., Pace N. R., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases, 10.1073/pnas.0706625104
  4. Gevers Dirk, Kugathasan Subra, Denson Lee A., Vázquez-Baeza Yoshiki, Van Treuren Will, Ren Boyu, Schwager Emma, Knights Dan, Song Se Jin, Yassour Moran, Morgan Xochitl C., Kostic Aleksandar D., Luo Chengwei, González Antonio, McDonald Daniel, Haberman Yael, Walters Thomas, Baker Susan, Rosh Joel, Stephens Michael, Heyman Melvin, Markowitz James, Baldassano Robert, Griffiths Anne, Sylvester Francisco, Mack David, Kim Sandra, Crandall Wallace, Hyams Jeffrey, Huttenhower Curtis, Knight Rob, Xavier Ramnik J., The Treatment-Naive Microbiome in New-Onset Crohn’s Disease, 10.1016/j.chom.2014.02.005
  5. Chow Janet, Tang Haiqing, Mazmanian Sarkis K, Pathobionts of the gastrointestinal microbiota and inflammatory disease, 10.1016/j.coi.2011.07.010
  6. Round June L., Mazmanian Sarkis K., The gut microbiota shapes intestinal immune responses during health and disease, 10.1038/nri2515
  7. Winter Sebastian E., Bäumler Andreas J., Why related bacterial species bloom simultaneously in the gut: principles underlying the ‘Like will to like’ concept : Principles of ‘Like will to like’, 10.1111/cmi.12245
  8. Winter Sebastian E, Bäumler Andreas J, Dysbiosis in the inflamed intestine : Chance favors the prepared microbe, 10.4161/gmic.27129
  9. Garrett Wendy S., Gallini Carey A., Yatsunenko Tanya, Michaud Monia, DuBois Andrea, Delaney Mary L., Punit Shivesh, Karlsson Maria, Bry Lynn, Glickman Jonathan N., Gordon Jeffrey I., Onderdonk Andrew B., Glimcher Laurie H., Enterobacteriaceae Act in Concert with the Gut Microbiota to Induce Spontaneous and Maternally Transmitted Colitis, 10.1016/j.chom.2010.08.004
  10. Garrett Wendy S., Lord Graham M., Punit Shivesh, Lugo-Villarino Geanncarlo, Mazmanian Sarkis K., Ito Susumu, Glickman Jonathan N., Glimcher Laurie H., Communicable Ulcerative Colitis Induced by T-bet Deficiency in the Innate Immune System, 10.1016/j.cell.2007.08.017
  11. Chassaing Benoit, Koren Omry, Carvalho Frederic A, Ley Ruth E, Gewirtz Andrew T, AIEC pathobiont instigates chronic colitis in susceptible hosts by altering microbiota composition, 10.1136/gutjnl-2013-304909
  12. Elinav Eran, Strowig Till, Kau Andrew L., Henao-Mejia Jorge, Thaiss Christoph A., Booth Carmen J., Peaper David R., Bertin John, Eisenbarth Stephanie C., Gordon Jeffrey I., Flavell Richard A., NLRP6 Inflammasome Regulates Colonic Microbial Ecology and Risk for Colitis, 10.1016/j.cell.2011.04.022
  13. Seo Sang-Uk, Kamada Nobuhiko, Muñoz-Planillo Raúl, Kim Yun-Gi, Kim Donghyun, Koizumi Yukiko, Hasegawa Mizuho, Himpsl Stephanie D., Browne Hilary P., Lawley Trevor D., Mobley Harry L.T., Inohara Naohiro, Núñez Gabriel, Distinct Commensals Induce Interleukin-1β via NLRP3 Inflammasome in Inflammatory Monocytes to Promote Intestinal Inflammation in Response to Injury, 10.1016/j.immuni.2015.03.004
  14. Devkota, S. et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature 487, 104–108 (2012).
  15. Zhang, Q. et al. Accelerated dysbiosis of gut microbiota during aggravation of DSS-induced colitis by a butyrate-producing bacterium. Sci Rep 6, 27572 (2016).
  16. Bloom Seth M., Bijanki Vinieth N., Nava Gerardo M., Sun Lulu, Malvin Nicole P., Donermeyer David L., Dunne W. Michael, Allen Paul M., Stappenbeck Thaddeus S., Commensal Bacteroides Species Induce Colitis in Host-Genotype-Specific Fashion in a Mouse Model of Inflammatory Bowel Disease, 10.1016/j.chom.2011.04.009
  17. Chow Janet, Mazmanian Sarkis K., A Pathobiont of the Microbiota Balances Host Colonization and Intestinal Inflammation, 10.1016/j.chom.2010.03.004
  18. Liu Zhiping, Ramer-Tait Amanda E., Henderson Abigail L., Demirkale Cumhur Yusuf, Nettleton Dan, Wang Chong, Hostetter Jesse M., Jergens Albert E., Wannemuehler Michael J., Helicobacter bilis Colonization Enhances Susceptibility to Typhlocolitis Following an Inflammatory Trigger, 10.1007/s10620-011-1701-3
  19. Fox, J. G. et al. Helicobacter bilis sp. nov., a novel Helicobacter species isolated from bile, livers, and intestines of aged, inbred mice. J Clin Microbiol 33, 445–454 (1995).
  20. Maggio-Price Lillian, Bielefeldt-Ohmann Helle, Treuting Piper, Iritani Brian M., Zeng Weiping, Nicks Andrea, Tsang Mark, Shows Donna, Morrissey Phil, Viney Joanne L., Dual Infection with Helicobacter bilis and Helicobacter hepaticus in P-Glycoprotein-Deficient mdr1a−/− Mice Results in Colitis that Progresses to Dysplasia, 10.1016/s0002-9440(10)62489-3
  21. Maggio-Price Lillian, Shows Donna, Waggie Kim, Burich Andrew, Zeng Weiping, Escobar Sabine, Morrissey Phil, Viney Joanne L., Helicobacter bilis Infection Accelerates and H. hepaticus Infection Delays the Development of Colitis in Multiple Drug Resistance-Deficient (mdr1a−/−) Mice, 10.1016/s0002-9440(10)64894-8
  22. Maxwell Joseph R., Zhang Yu, Brown William A., Smith Carole L., Byrne Fergus R., Fiorino Mike, Stevens Erin, Bigler Jeannette, Davis John A., Rottman James B., Budelsky Alison L., Symons Antony, Towne Jennifer E., Differential Roles for Interleukin-23 and Interleukin-17 in Intestinal Immunoregulation, 10.1016/j.immuni.2015.08.019
  23. Shomer, N. H., Dangler, C. A., Schrenzel, M. D. & Fox, J. G. Helicobacter bilis-induced inflammatory bowel disease in scid mice with defined flora. Infect Immun 65, 4858–4864 (1997).
  24. Khor Bernard, Gardet Agnès, Xavier Ramnik J., Genetics and pathogenesis of inflammatory bowel disease, 10.1038/nature10209
  25. Sartor R Balfour, Mechanisms of Disease: pathogenesis of Crohn's disease and ulcerative colitis, 10.1038/ncpgasthep0528
  26. Maloy Kevin J., Powrie Fiona, Intestinal homeostasis and its breakdown in inflammatory bowel disease, 10.1038/nature10208
  27. Lupp Claudia, Robertson Marilyn L., Wickham Mark E., Sekirov Inna, Champion Olivia L., Gaynor Erin C., Finlay B. Brett, Host-Mediated Inflammation Disrupts the Intestinal Microbiota and Promotes the Overgrowth of Enterobacteriaceae, 10.1016/j.chom.2007.08.002
  28. Papa Eliseo, Docktor Michael, Smillie Christopher, Weber Sarah, Preheim Sarah P., Gevers Dirk, Giannoukos Georgia, Ciulla Dawn, Tabbaa Diana, Ingram Jay, Schauer David B., Ward Doyle V., Korzenik Joshua R., Xavier Ramnik J., Bousvaros Athos, Alm Eric J., Non-Invasive Mapping of the Gastrointestinal Microbiota Identifies Children with Inflammatory Bowel Disease, 10.1371/journal.pone.0039242
  29. Mukhopadhya Indrani, Hansen Richard, El-Omar Emad M., Hold Georgina L., IBD—what role do Proteobacteria play?, 10.1038/nrgastro.2012.14
  30. Haines D. C., Gorelick P. L., Battles J. K., Pike K. M., Anderson R. J., Fox J. G., Taylor N. S., Shen Z., Dewhirst F. E., Anver M. R., Ward J. M., Inflammatory Large Bowel Disease in Immunodeficient Rats Naturally and Experimentally Infected with Helicobacter bilis, 10.1177/030098589803500305
  31. Carvalho Frederic A., Koren Omry, Goodrich Julia K., Johansson Malin E.V., Nalbantoglu Ilke, Aitken Jesse D., Su Yueju, Chassaing Benoit, Walters William A., González Antonio, Clemente Jose C., Cullender Tyler C., Barnich Nicolas, Darfeuille-Michaud Arlette, Vijay-Kumar Matam, Knight Rob, Ley Ruth E., Gewirtz Andrew T., Transient Inability to Manage Proteobacteria Promotes Chronic Gut Inflammation in TLR5-Deficient Mice, 10.1016/j.chom.2012.07.004
  32. Yang Ines, Eibach Daniel, Kops Friederike, Brenneke Birgit, Woltemate Sabrina, Schulze Jessika, Bleich André, Gruber Achim D., Muthupalani Sureshkumar, Fox James G., Josenhans Christine, Suerbaum Sebastian, Intestinal Microbiota Composition of Interleukin-10 Deficient C57BL/6J Mice and Susceptibility to Helicobacter hepaticus-Induced Colitis, 10.1371/journal.pone.0070783
  33. Nagalingam Nabeetha A, Robinson Courtney J, Bergin Ingrid L, Eaton Kathryn A, Huffnagle Gary B, Young Vincent B, The effects of intestinal microbial community structure on disease manifestation in IL-10-/- mice infected with Helicobacter hepaticus, 10.1186/2049-2618-1-15
  34. Dieleman L. A., Arends A., Tonkonogy S. L., Goerres M. S., Craft D. W., Grenther W., Sellon R. K., Balish E., Sartor R. B., Helicobacter hepaticus Does Not Induce or Potentiate Colitis in Interleukin-10-Deficient Mice, 10.1128/iai.68.9.5107-5113.2000
  35. Contractor, N. V. et al. Lymphoid hyperplasia, autoimmunity, and compromised intestinal intraepithelial lymphocyte development in colitis-free gnotobiotic IL-2-deficient mice. J Immunol 160, 385–394 (1998).
  36. Dianda, L. et al. T cell receptor-alpha beta-deficient mice fail to develop colitis in the absence of a microbial environment. Am J Pathol 150, 91–97 (1997).
  37. Sellon, R. K. et al. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect Immun 66, 5224–5231 (1998).
  38. Kim Sandra C., Tonkonogy Susan L., Karrasch Thomas, Jobin Christian, Sartor Balfour R., Dual-association of gnotobiotic Il-10−/− mice with 2 nonpathogenic commensal bacteria induces aggressive pancolitis : , 10.1002/ibd.20246
  39. Cong Yingzi, Brandwein Steven L., McCabe Robert P., Lazenby A., Birkenmeier Edward H., Sundberg John P., Elson Charles O., CD4+T Cells Reactive to Enteric Bacterial Antigens in Spontaneously Colitic C3H/HeJBir Mice: Increased T Helper Cell Type 1 Response and Ability to Transfer Disease, 10.1084/jem.187.6.855
  40. Littman Dan R., Rudensky Alexander Y., Th17 and Regulatory T Cells in Mediating and Restraining Inflammation, 10.1016/j.cell.2010.02.021
  41. Hand T. W., Dos Santos L. M., Bouladoux N., Molloy M. J., Pagan A. J., Pepper M., Maynard C. L., Elson C. O., Belkaid Y., Acute Gastrointestinal Infection Induces Long-Lived Microbiota-Specific T Cell Responses, 10.1126/science.1220961
  42. Belkaid Yasmine, Hand Timothy W., Role of the Microbiota in Immunity and Inflammation, 10.1016/j.cell.2014.03.011
  43. Cong Y., Weaver C. T., Lazenby A., Elson C. O., Colitis Induced by Enteric Bacterial Antigen-Specific CD4+ T Cells Requires CD40-CD40 Ligand Interactions for a Sustained Increase in Mucosal IL-12, 10.4049/jimmunol.165.4.2173
  44. Lodes Michael J., Cong Yingzi, Elson Charles O., Mohamath Raodoh, Landers Carol J., Targan Stephan R., Fort Madeline, Hershberg Robert M., Bacterial flagellin is a dominant antigen in Crohn disease, 10.1172/jci200420295
  45. Brimnes Jens, Reimann Jörg, Nissen Mogens H., Claesson Mogens H., Enteric bacterial antigens activate CD4+ T cells fromscid mice with inflammatory bowel disease, 10.1002/1521-4141(200101)31:1<23::aid-immu23>3.0.co;2-2
  46. Ivanov Ivaylo I., Atarashi Koji, Manel Nicolas, Brodie Eoin L., Shima Tatsuichiro, Karaoz Ulas, Wei Dongguang, Goldfarb Katherine C., Santee Clark A., Lynch Susan V., Tanoue Takeshi, Imaoka Akemi, Itoh Kikuji, Takeda Kiyoshi, Umesaki Yoshinori, Honda Kenya, Littman Dan R., Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria, 10.1016/j.cell.2009.09.033
  47. Eun C. S., Mishima Y., Wohlgemuth S., Liu B., Bower M., Carroll I. M., Sartor R. B., Induction of Bacterial Antigen-Specific Colitis by a Simplified Human Microbiota Consortium in Gnotobiotic Interleukin-10-/- Mice, 10.1128/iai.01513-13
  48. Kullberg M. C., Andersen J. F., Gorelick P. L., Caspar P., Suerbaum S., Fox J. G., Cheever A. W., Jankovic D., Sher A., Induction of colitis by a CD4+ T cell clone specific for a bacterial epitope, 10.1073/pnas.2534546100
  49. Palm Noah W., de Zoete Marcel R., Cullen Thomas W., Barry Natasha A., Stefanowski Jonathan, Hao Liming, Degnan Patrick H., Hu Jianzhong, Peter Inga, Zhang Wei, Ruggiero Elizabeth, Cho Judy H., Goodman Andrew L., Flavell Richard A., Immunoglobulin A Coating Identifies Colitogenic Bacteria in Inflammatory Bowel Disease, 10.1016/j.cell.2014.08.006
  50. Chai, J. N. et al. Helicobacter species are potent drivers of colonic T cell responses in homeostasis and inflammation. Sci Immunol 2 (2017).
  51. Jergens A. E, Wilson-Welder J. H, Dorn A., Henderson A., Liu Z., Evans R. B, Hostetter J., Wannemuehler M. J, Helicobacter bilis triggers persistent immune reactivity to antigens derived from the commensal bacteria in gnotobiotic C3H/HeN mice, 10.1136/gut.2006.099242
  52. Dewhirst, F. E. et al. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 65, 3287–3292 (1999).
  53. Wymore Brand Meghan, Wannemuehler Michael J., Phillips Gregory J., Proctor Alexandra, Overstreet Anne-Marie, Jergens Albert E., Orcutt Roger P., Fox James G., The Altered Schaedler Flora: Continued Applications of a Defined Murine Microbial Community, 10.1093/ilar/ilv012
  54. Gomes-Neto João Carlos, Mantz Sara, Held Kyler, Sinha Rohita, Segura Munoz Rafael R., Schmaltz Robert, Benson Andrew K., Walter Jens, Ramer-Tait Amanda E., A real-time PCR assay for accurate quantification of the individual members of the Altered Schaedler Flora microbiota in gnotobiotic mice, 10.1016/j.mimet.2017.02.003
  55. Martinez I., Wallace G., Zhang C., Legge R., Benson A. K., Carr T. P., Moriyama E. N., Walter J., Diet-Induced Metabolic Improvements in a Hamster Model of Hypercholesterolemia Are Strongly Linked to Alterations of the Gut Microbiota, 10.1128/aem.00380-09
  56. Jergens Albert E., Dorn Andrea, Wilson Jenny, Dingbaum Krystal, Henderson Abigail, Liu Zhiping, Hostetter Jesse, Evans Richard B., Wannemuehler Michael J., Induction of differential immune reactivity to members of the flora of gnotobiotic mice following colonization with Helicobacter bilis or Brachyspira hyodysenteriae, 10.1016/j.micinf.2006.01.019
  57. Ramer-Tait Amanda E., Petersen Christine A., Jones Douglas E., IL-2 limits IL-12 enhanced lymphocyte proliferation during Leishmania amazonensis infection, 10.1016/j.cellimm.2011.03.016
  58. Ramer A. E., Vanloubbeeck Y. F., Jones D. E., Antigen-Responsive CD4+ T Cells from C3H Mice Chronically Infected with Leishmania amazonensis Are Impaired in the Transition to an Effector Phenotype, 10.1128/iai.74.3.1547-1554.2006
  59. Jones D. E., Buxbaum L. U., Scott P., IL-4-Independent Inhibition of IL-12 Responsiveness During Leishmania amazonensis Infection, 10.4049/jimmunol.165.1.364