B cells as a critical node in the microbiota-host immune system network

Immunological Reviews

Volumn 260, Issue 1, 2014, Pages 50-66

  Slack, Emma ^a   Balmer, Maria L ^b,d   Macpherson, Andrew J ^c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

B lymphocytes; Gut associated lymphoid tissue; IgA; Innate immunity; Intestinal barrier; Microbiota

Indexed keywords

HISTONE DEACETYLASE; IMMUNOGLOBULIN G; MUCIN; SECRETORY IMMUNOGLOBULIN; SHORT CHAIN FATTY ACID; TOLL LIKE RECEPTOR 5; FATTY ACID; IMMUNOGLOBULIN A;

ADAPTIVE IMMUNITY; ANTIBODY PRODUCTION; ANTIGEN BINDING; AUTOPHAGY; B LYMPHOCYTE; BACTERICIDAL ACTIVITY; CELLULAR IMMUNITY; ENDOPLASMIC RETICULUM STRESS; EPITHELIUM CELL; GLYCOSYLATION; HELPER CELL; HOST; HUMAN; HYBRIDOMA CELL LINE; IMMUNE DEFICIENCY; IMMUNE EVASION; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOGLOBULIN A DEFICIENCY; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; INTESTINE MUCOSA; MESENTERY LYMPH NODE; MICROBIAL DIVERSITY; MICROENVIRONMENT; MONONUCLEAR PHAGOCYTE; MUCOSAL IMMUNITY; MUCUS SECRETION; NONHUMAN; NUTRIENT AVAILABILITY; PRIORITY JOURNAL; REVIEW; SYMBIOSIS; VACCINATION; ANIMAL; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; MICROFLORA; MUCUS; PEYER PATCH; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; TUMOR MICROENVIRONMENT;

ANIMALS; AUTOPHAGY; B-LYMPHOCYTE SUBSETS; CELLULAR MICROENVIRONMENT; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS; HISTONE DEACETYLASES; HOST-PATHOGEN INTERACTIONS; HUMANS; IGA DEFICIENCY; IMMUNE SYSTEM; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; IMMUNOLOGIC DEFICIENCY SYNDROMES; INTESTINAL MUCOSA; INTESTINES; MICROBIOTA; MUCUS; PEYER'S PATCHES; SYMBIOSIS; T-LYMPHOCYTE SUBSETS;

EID: 84902590970     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12179     Document Type: Review

References (189)

1. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI. Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 2008;6:776-788.
2. Whitman WB, Coleman DC, Wiebe WJ. Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 1998;95:6578-6583.
3. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007;449:819-826.
4. Collado MC, Cernada M, Bauerl C, Vento M, Perez-Martinez G. Microbial ecology and host-microbiota interactions during early life stages. Gut Microbes 2012;3:352-365.
5. Suzuki K, et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci USA 2004;101:1981-1986.
6. Elinav E, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011;145:745-757.
7. Germain RN, Meier-Schellersheim M, Nita-Lazar A, Fraser ID. Systems biology in immunology: a computational modeling perspective. Annu Rev Immunol 2011;29:527-585.
8. Nakaya HI, Pulendran B. Systems vaccinology: its promise and challenge for HIV vaccine development. Curr Opin HIV AIDS 2011;7:24-31.
9. Danilova N. The evolution of adaptive immunity. Adv Exp Med Biol 2012;738:218-235.
10. Sun Y, Wei Z, Li N, Zhao Y. A comparative overview of immunoglobulin genes and the generation of their diversity in tetrapods. Dev Comp Immunol 2013;39:103-109.
11. Rath T, et al. The immunologic functions of the neonatal Fc receptor for IgG. J Clin Immunol 2012;33(Suppl):S9-S17.
12. Sunyer JO. Fishing for mammalian paradigms in the teleost immune system. Nat Immunol 2013;14:320-326.
13. Zhang YA, et al. IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol 2010;11:827-835.
14. Harriman GR, et al. Targeted deletion of the IgA constant region in mice leads to IgA deficiency with alterations in expression of other immunoglobulin isotypes. J Immunol 1999;162:2521-2529.
15. Mbawuike IN, Pacheco S, Acuna CL, Switzer KC, Zhang YX, Harriman GR. Mucosal immunity to influenza without IgA: an IgA knockout mouse model. J Immunol 1999;162:2530-2537.
16. Jorgensen GH, et al. Clinical symptoms in adults with selective IgA deficiency: a case-control study. J Clin Immunol 2013;33:742-747.
17. Mazanec MB, Kaetzel CS, Lamm ME, Fletcher D, Nedrud JG. Intracellular neutralization of virus by immunoglobulin A antibodies. Proc Natl Acad Sci USA 1992;89:6901-6905.
18. O'Neal CM, Harriman GR, Conner ME. Protection of the villus epithelial cells of the small intestine from rotavirus infection does not require immunoglobulin A. J Virol 2000;74:4102-4109.
19. Young GR, Eksmond U, Salcedo R, Alexopoulou L, Stoye JP, Kassiotis G. Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 2012;491:774-778.
20. Burns JW, Krishnaney AA, Vo PT, Rouse RV, Anderson LJ, Greenberg HB. Analyses of homologous rotavirus infection in the mouse model. Virology 1995;207:143-153.
21. Sait LC, et al. Secretory antibodies reduce systemic antibody responses against the gastrointestinal commensal flora. Int Immunol 2007;19:257-265.
22. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004;303:1662-1665.
23. Endt K, et al. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog 2010;6:e1001097.
24. Bollinger RR, Everett ML, Palestrant D, Love SD, Lin SS, Parker W. Human secretory immunoglobulin A may contribute to biofilm formation in the gut. Immunology 2003;109:580-587.
25. Fagarasan S, Muramatsu M, Suzuki K, Nagaoka H, Hiai H, Honjo T. Critical roles of activation-induced cytidine deaminase in the homeostasis of gut flora. Science 2002;298:1424-1427.
26. Uren TK, Wijburg OL, Simmons C, Johansen FE, Brandtzaeg P, Strugnell RA. Vaccine-induced protection against gastrointestinal bacterial infections in the absence of secretory antibodies. Eur J Immunol 2005;35:180-188.
27. Greenberg HB, Estes MK. Rotaviruses: from pathogenesis to vaccination. Gastroenterology 2009;136:1939-1951.
28. Alpan O, Rudomen G, Matzinger P. The role of dendritic cells, B cells, and M cells in gut-oriented immune responses. J Immunol 2001;166:4843-4852.
29. Corthesy B. Roundtrip ticket for secretory IgA: role in mucosal homeostasis? J Immunol 2007;178:27-32.
30. Shimada S, et al. Generation of polymeric immunoglobulin receptor-deficient mouse with marked reduction of secretory IgA. J Immunol 1999;163:5367-5373.
31. Rochereau N, et al. Dectin-1 is essential for reverse transcytosis of glycosylated SIgA-antigen complexes by intestinal M cells. PLoS Biol 2013;11:e1001658.
32. Ng KM, et al. Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 2013;502:96-99.
33. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol 2008;1:11-22.
34. Schluter J, Foster KR. The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol 2012;10:e1001424.
35. Hamze M, Desmetz C, Guglielmi P. B cell-derived cytokines in disease. Eur Cytokine Netw 2013;24:20-26.
36. Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S. IL-10, producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol 2013;178:735-743.
37. Montecino-Rodriguez E, Dorshkind K. B-1 B cell development in the fetus and adult. Immunity 2012;36:13-21.
38. Gao J, et al. Novel functions of murine B1 cells: active phagocytic and microbicidal abilities. Eur J Immunol 2012;42:982-992.
39. Fritz JH, et al. Acquisition of a multifunctional IgA+ plasma cell phenotype in the gut. Nature 2012;481:199-203.
40. Liu Y, et al. Gene-targeted B-deficient mice reveal a critical role for B cells in the CD4 T cell response. Int Immunol 1995;7:1353-1362.
41. van Essen D, Dullforce P, Brocker T, Gray D. Cellular interactions involved in Th cell memory. J Immunol 2000;165:3640-3646.
42. Akirav EM, Xu Y, Ruddle NH. Resident B cells regulate thymic expression of myelin oligodendrocyte glycoprotein. J Neuroimmunol 2011;235:33-39.
43. Golovkina TV, Shlomchik M, Hannum L, Chervonsky A. Organogenic role of B lymphocytes in mucosal immunity. Science 1999;286:1965-1968.
44. Goodman AL, et al. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 2009;6:279-289.
45. Slack E, et al. Innate and adaptive iimmunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009;325:617-620.
46. Macpherson AJ, et al. IgA B cell and IgA antibody production in the absence of mu and delta heavy chain expression early in B cell ontongeny. Nat Immunol 2001;2:625-631.
47. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 2007;19:59-69.
48. Peterson DA, McNulty NP, Guruge JL, Gordon JI. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2007;2:328-339.
49. Kramer DR, Cebra JJ. Early appearance of "natural" mucosal IgA responses and germinal centers in suckling mice developing in the absence of maternal antibodies. J Immunol 1995;154:2051-2062.
50. Harris N, et al. Mechanisms of neonatal mucosal antibody protection. J Immunol 2006;177:6256-6262.
51. Klaasen HL, Koopman JP, Poelma FG, Beynen AC. Intestinal, segmented, filamentous bacteria. FEMS Microbiol Rev 1992;8:165-180.
52. Maruya M, Kawamoto S, Kato LM, Fagarasan S. Impaired selection of IgA and intestinal dysbiosis associated with PD-1-deficiency. Gut Microbes 2013;4:165-171.
53. David LA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2013;505:559-563.
54. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. Diversity, stability and resilience of the human gut microbiota. Nature 2012;489:220-230.
55. Hammarstrom L, Vorechovsky I, Webster D. Selective IgA deficiency (SIgAD) and common variable immunodeficiency (CVID). Clin Exp Immunol 2000;120:225-231.
56. Goldstein MF, Goldstein AL, Dunsky EH, Dvorin DJ, Belecanech GA, Shamir K. Pediatric selective IgM immunodeficiency. Clin Dev Immunol 2008;2008:624850.
57. Husby S, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition guidelines for the diagnosis of coeliac disease. J Ped Gastroenterol Nutr 2012;54:136-160.
58. Singh K, Chang C, Gershwin ME. IgA deficiency and autoimmunity. Autoimmunity Rev 2014;13:163-177.
59. Furst DE, et al. Updated consensus statement on biological agents for the treatment of rheumatic diseases, 2012. Ann Rheum Dis 2012;72 (Suppl):ii2-ii34.
60. Rawlings DJ, Witte ON. Bruton's tyrosine kinase is a key regulator in B-cell development. Immunol Rev 1994;138:105-119.
61. Lopez-Granados E, Perez de Diego R, Ferreira Cerdon A, Fonton Casariego G, Garcia Rodriguez MC. A genotype-phenotype correlation study in a group of 54 patients with X-linked agammaglobulinemia. J Allergy Clin Immunol 2005;116:690-697.
62. Hendriks RW, Bredius RGM, Pike-Overzet K, Staal FJT. Biology and novel treatment options for XLA, the most common monogenetic immunodeficiency in man. Exp Opin Ther Targets 2014;15:1003-1021.
63. Ariganello P, et al. Relapsing Campylobacter jejuni systemic infections in a child with X-linked agammaglobulinemia. Case Rep Pediatr 2013;2013:735108.
64. Jirapongsananuruk O, et al. Recurrent Campylobacter lari bacteremia in X-linked agammaglobulinemia: a case report and review. Asian Pac J Allergy Immunol 2006;24:171-174.
65. Van der Hilst JC, Smits BW, van der Meer JW. Hypogammaglobulinaemia: cumulative experience in 49 patients in a tertiary care institution. Neth J Med 2002;60:140-147.
66. Cuccherini B, et al. Bacteremia and skin/bone infections in two patients with X-linked agammaglobulinemia caused by an unusual organism related to flexispira/helicobacter species. Clin Immunol 2000;97:121-129.
67. Mangla A, et al. Pleiotropic consequences of Bruton tyrosine kinase deficiency in myeloid lineages lead to poor inflammatory responses. Blood 2004;104:1191-1197.
68. Chapel H, et al. Common variable immunodeficiency disorders: division into distinct clinical phenotypes. Blood 2008;112:277-286.
69. Resnick ES, Cunningham-Rundles C. The many faces of the clinical picture of common variable immune deficiency. Curr Opin Allergy Clin Immunol 2012;12:595-601.
70. Nenci A, et al. Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007;446:557-561.
71. Thorpe JE, Baughman RP, Frame PT, Wesseler TA, Staneck JL. Bronchoalveolar lavage for diagnosing acute bacterial pneumonia. J Infect Dis 1987;155:855-861.
72. Notarangelo LD. Primary immunodeficiencies. J Allergy Clin Immunol 2010;125:S182-S194.
73. Ley RE, et al. Evolution of mammals and their gut microbes. Science 2008;320:1647-1651.
74. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 2010;330:1768-1773.
75. Hongoh Y. Diversity and genomes of uncultured microbial symbionts in the termite gut. Biosci Biotechnol Biochem 2010;74:1145-1151.
76. Muegge BD, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 2011;332:970-974.
77. Soave O, Brand CD. Coprophagy in animals: a review. Cornell Vet 1991;81:357-364.
78. Ouwerkerk JP, de Vos WM, Belzer C. Glycobiome: bacteria and mucus at the epithelial interface. Best Pract Res Clin Gastroenterol 2013;27:25-38.
79. Vaishnava S, et al. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011;334:255-258.
80. Liu JZ, et al. Zinc Sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 2012;11:227-239.
81. van der Waaij LA, Limburg PC, Mesander G, van der Waaij D. In vivo IgA coating of anaerobic bacteria in human faeces. Gut 1996;38:348-354.
82. Macpherson AJ, Gatto D, Sainsbury E, Harriman GR, Hengartner H, Zinkernagel RM. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 2000;288:2222-2226.
83. Mathias A, Corthesy B. N-Glycans on secretory component: mediators of the interaction between secretory IgA and gram-positive commensals sustaining intestinal homeostasis. Gut Microbes 2011;2:287-293.
84. Caselli M, Cassol F, Gentili V, Di Luca D. Genome sequences of segmented filamentous bacteria in animals: implications for human research. Gut Microbes 2012;3:401-405.
85. Kuwahara T, et al. The lifestyle of the segmented filamentous bacterium: a non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing. DNA Res 2011;18:291-303.
86. Pamp SJ, Harrington ED, Quake SR, Relman DA, Blainey PC. Single-cell sequencing provides clues about the host interactions of segmented filamentous bacteria (SFB). Genome Res 2012;22:1107-1119.
87. Prakash T, et al. Complete genome sequences of rat and mouse segmented filamentous bacteria, a potent inducer of th17 cell differentiation. Cell Host Microbe 2011;10:273-284.
88. Sczesnak A, et al. The genome of th17 cell-inducing segmented filamentous bacteria reveals extensive auxotrophy and adaptations to the intestinal environment. Cell Host Microbe 2011;10:260-272.
89. Winter SE, Lopez CA, Baumler AJ. The dynamics of gut-associated microbial communities during inflammation. EMBO Rep 2013;14:319-327.
90. Stecher B, Hardt WD. Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 2010;14:82-91.
91. Mumy KL, McCormick BA. The role of neutrophils in the event of intestinal inflammation. Curr Opin Pharmacol 2009;9:697-701.
92. Stecher B, et al. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 2010;6:e1000711.
93. Maier L, et al. Microbiota-derived hydrogen fuels Salmonella Typhimurium Invasion of the gut ecosystem. Cell Host Microbe 2014;14:641-651.
94. Stecher B, Berry D, Loy A. Colonization resistance and microbial ecophysiology: using gnotobiotic mouse models and single-cell technology to explore the intestinal jungle. FEMS Microbiol Rev 2013;37:793-829.
95. Molloy MJ, et al. Intraluminal containment of commensal outgrowth in the gut during infection-induced dysbiosis. Cell Host Microbe 2013;14:318-328.
96. Garrett WS, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 2010;8:292-300.
97. Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 2001;413:639-643.
98. Grainger JR, et al. Inflammatory monocytes regulate pathologic responses to commensals during acute gastrointestinal infection. Nat Med 2013;19:713-721.
99. Berry D, et al. Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc Natl Acad Sci USA 2013;110:4720-4725.
100. Lindner C, et al. Age, microbiota, and T cells shape diverse individual IgA repertoires in the intestine. J Exp Med 2012;209:365-377.
101. Duerkop BA, Hooper LV. Resident viruses and their interactions with the immune system. Nat Immunol 2013;14:654-659.
102. Minot S, et al. The human gut virome: inter-individual variation and dynamic response to diet. Genome Res 2011;21:1616-1625.
103. Schulz O, Pabst O. Antigen sampling in the small intestine. Trends Immunol 2012;34:155-161.
104. Shan M, et al. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 2013;342:447-453.
105. Johansson MEV, Sjovall H, Hansson GC. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol 2013;10:352-361.
106. Kashyap PC, et al. Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proc Natl Acad Sci USA 2013;110:17059-17064.
107. Van der Sluis M, et al. Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 2006;131:117-129.
108. An G, et al. Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med 2007;204:1417-1429.
109. Velcich A, et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 2002;295:1726-1729.
110. Johansson MEV, et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 2013;63:281-291.
111. Lamont JT. Mucus: the front line of intestinal mucosal defense. Ann N Y Acad Sci 1992;664:190-201.
112. Ermund A, Schotte A, Johansson MEV, Gustafsson JK, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. I. Gastrointestinal mucus layers have different properties depending on location as well as over the Peyer's patches. Am J Physiol 2013;305:G341-G347.
113. Rodriguez-Pineiro AM, et al. Studies of mucus in mouse stomach, small intestine, and colon. II. Gastrointestinal mucus proteome reveals Muc2 and Muc5ac accompanied by a set of core proteins. Am J Physiol 2013;305:G348-G356.
114. Holmen Larsson JM, Thomsson KA, Rodriguez-Pineiro AM, Karlsson H, Hansson GC. Studies of mucus in mouse stomach, small intestine, and colon. III. Gastrointestinal Muc5ac and Muc2 mucin O-glycan patterns reveal a regiospecific distribution. Am J Physiol 2013;305:G357-G363.
115. Rawls JF, Mahowald MA, Ley RE, Gordon JI. Reciprocal gut microbiota transplants from zebrafish and mice to germ-free recipients reveal host habitat selection. Cell 2006;127:423-433.
116. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA 2014;111:2247-2252.
117. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004;118:229-241.
118. Natividad JM, et al. Commensal and probiotic bacteria influence intestinal barrier function and susceptibility to colitis in Nod1-/-; Nod2-/- mice. Inflamm Bowel Dis 2011;18:1434-1446.
119. Bjarnason I, Macpherson AJ, Hollander D. Intestinal permeability: an overview. Gastroenterology 1995;108:1566-1581.
120. Rechkemmer G, Ronnau K, von Engelhardt W. Fermentation of polysaccharides and absorption of short chain fatty acids in the mammalian hindgut. Comp Biochem Physiol A Comp Physiol 1988;90:563-568.
121. Alenghat T, et al. Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature 2013;504:153-157.
122. Donohoe DR, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab 2011;13:517-526.
123. Roediger WE. Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 1980;21:793-798.
124. Roediger WE. Utilization of nutrients by isolated epithelial cells of the rat colon. Gastroenterology 1982;83:424-429.
125. Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt WD. Comparison of Salmonella serovar typhmurium colitis in streptomycin pretreated and germfree mice. Infect Immun 2005;73:3228-3241.
126. Furusawa Y, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 2013;504:446-450.
127. Smith PM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013;341:569-573.
128. Trompette A, et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014;20:159-166.
129. Wichmann A, et al. Microbial modulation of energy availability in the colon regulates intestinal transit. Cell Host Microbe 2013;14:582-590.
130. Maslowski KM, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009;461:1282-1286.
131. Hatzi K, et al. A hybrid mechanism of action for BCL6 in B cells defined by formation of functionally distinct complexes at enhancers and promoters. Cell Rep 2013;4:578-588.
132. Gardet A, Xavier RJ. Common alleles that influence autophagy and the risk for inflammatory bowel disease. Curr Opin Immunol 2012;24:522-529.
133. Adolph TE, et al. Paneth cells as a site of origin for intestinal inflammation. Nature 2013;503:272-276.
134. Conway KL, et al. ATG5 regulates plasma cell differentiation. Autophagy 2013;9:528-537.
135. Pengo N, et al. Plasma cells require autophagy for sustainable immunoglobulin production. Nat Immunol 2013;14:298-305.
136. Yilmaz OH, et al. mTORC1 in the Paneth cell niche couples intestinal stem-cell function to calorie intake. Nature 2012;486:490-495.
137. Hodin CM, et al. Starvation compromises paneth cells. Am J Pathol 2011;179:2885-2893.
138. Cording S, et al. The intestinal micro-environment imprints stromal cells to promote efficient Treg induction in gut-draining lymph nodes. Mucosal Immunol 2014;7:359-368.
139. Pearson C, Uhlig HH, Powrie F. Lymphoid microenvironments and innate lymphoid cells in the gut. Trends Immunol 2012;33:289-296.
140. Coombes JL, et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007;204:1757-1764.
141. Worthington JJ, Czajkowska BI, Melton AC, Travis MA. Intestinal dendritic cells specialize to activate transforming growth factor-beta and induce Foxp3+ regulatory T cells via integrin alphavbeta8. Gastroenterology 2011;141:1802-1812.
142. Suzuki K, et al. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010;33:71-83.
143. Tezuka H, et al. Prominent role for plasmacytoid dendritic cells in mucosal T cell-independent IgA induction. Immunity 2011;34:247-257.
144. Castigli E, et al. TACI and BAFF-R mediate isotype switching in B cells. J Exp Med 2005;201:35-39.
145. Obata T, et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc Natl Acad Sci USA 2010;107:7419-7424.
146. Macpherson AJ, McCoy KD. Stratification and compartmentalisation of immunoglobulin responses to commensal intestinal microbes. Semin Immunol 2013;25:358-363.
147. Banks TA, et al. Lymphotoxin-alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J Immunol 1995;155:1685-1693.
148. Koni PA, Sacca R, Lawton P, Browning JL, Ruddle NH, Flavell RA. Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity 1997;6:491-500.
149. Kruglov AA, et al. Nonredundant function of soluble LTalpha3 produced by innate lymphoid cells in intestinal homeostasis. Science 2013;342:1243-1246.
150. Lochner M, et al. Microbiota-induced tertiary lymphoid tissues aggravate inflammatory disease in the absence of RORO≥t and LTi cells. J Exp Med 2011;208:125-134.
151. Heidegger S, et al. TLR activation excludes circulating naive CD8+ T cells from gut-associated lymphoid organs in mice. J Immunol 2013;190:5313-5320.
152. Hand TW, et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 2012;337:1553-1556.
153. Diehl GE, et al. Microbiota restricts trafficking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature 2013;494:116-120.
154. Farache J, et al. Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 2013;38:581-595.
155. Hapfelmeier S, et al. Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. J Exp Med 2008;205:437-450.
156. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci USA 2008;105:20858-20863.
157. Larsson E, et al. Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut 2012;61:1124-1131.
158. Cullender TC, et al. Innate and adaptive immunity interact to quench microbiome flagellar motility in the gut. Cell Host Microbe 2013;14:571-581.
159. Vijay-Kumar M, et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 2010;328:228-231.
160. Lopez-Yglesias AH, et al. Flagellin induces antibody responses through a TLR5- and inflammasome-independent pathway. J Immunol 2014;192:1587-1596.
161. Bailly-Bechet M, Benecke A, Hardt WD, Lanza V, Sturm A, Zecchina R. An externally modulated, noise-driven switch for the regulation of SPI1 in Salmonella enterica serovar Typhimurium. J Math Biol 2010;63:637-662.
162. Hawn TR, et al. A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease. J Exp Med 2003;198:1563-1572.
163. Parkes M, Cortes A, van Heel DA, Brown MA. Genetic insights into common pathways and complex relationships among immune-mediated diseases. Nat Rev Genet 2013;14:661-673.
164. Kathrani A, House A, Catchpole B, Murphy A, Werling D, Allenspach K. Breed-independent toll-like receptor 5 polymorphisms show association with canine inflammatory bowel disease. Tiss Antigens 2011;78:94-101.
165. Ubeda C, et al. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J Exp Med 2012;209:1445-1456.
166. Ko HJ, et al. Innate immunity mediated by MyD88 signal is not essential for induction of lipopolysaccharide-specific B cell responses but is indispensable for protection against Salmonella enterica serovar Typhimurium infection. J Immunol 2009;182:2305-2312.
167. Hirota K, et al. Plasticity of TH17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat Immunol 2013;14:372-379.
168. Tsuji M, et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009;323:1488-1492.
169. Zheng SG, Wang J, Horwitz DA. Cutting edge: Foxp3+CD4+CD25+ regulatory T cells induced by IL-2 and TGF-beta are resistant to Th17 conversion by IL-6. J Immunol 2008;180:7112-7116.
170. Yang XO, et al. Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 2008;29:44-56.
171. Xu LL, Kitani A, Fuss I, Strober W. Cutting edge: regulatory T cells induce CD4(+)CD25(-)Foxp3(-) T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta. J Immunol 2007;178:6725-6729.
172. Lycke N, Holmgren J. Intestinal mucosal memory and presence of memory cells in lamina propria and Peyer's patches in mice 2 years after oral immunization with cholera toxin. Scand J Immunol 1986;23:611-616.
173. Hapfelmeier S, et al. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 2010;328:1705-1709.
174. Cong Y, Feng T, Fujihashi K, Schoeb TR, Elson CO. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc Natl Acad Sci USA 2009;106:19256-19261.
175. Gaboriau-Routhiau V, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009;31:677-689.
176. Ishikawa H, et al. Effect of intestinal microbiota on the induction of regulatory CD25+ CD4+ T cells. Clin Exp Immunol 2008;153:127-135.
177. Ivanov II, et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 2008;4:337-349.
178. O'Mahony C, et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 2008;4:e1000112.
179. Geuking MB, et al. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 2011;34:794-806.
180. Snel J, et al. Interactions between gut-associated lymphoid tissue and colonization levels of indigenous, segmented, filamentous bacteria in the small intestine of mice. Can J Microbiol 1998;44:1177-1182.
181. Talham GL, Jiang HQ, Bos NA, Cebra JJ. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 1999;67:1992-2000.
182. Atarashi K, et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008;455:808-812.
183. Cahenzli J, Koller Y, Wyss M, Geuking MB, McCoy KD. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe 2013;14:559-570.
184. Pang T. Vaccination in the Third World. Contemporary issues. C R Acad Sci III 1999;322:995-997.
185. Armah GE, et al. Immunogenicity of the pentavalent rotavirus vaccine in African Infants. Vaccine 2012;30(Suppl 1):A86-A93.
186. Fraser A, Paul M, Goldberg E, Acosta CJ, Leibovici L. Typhoid fever vaccines: systematic review and meta-analysis of randomised controlled trials. Vaccine 2007;25:7848-7857.
187. Michetti P, Mahan MJ, Slauch JM, Mekalanos JJ, Neutra MR. Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect Immun 1992;60:1786-1792.
188. Scribano ML, Prantera C. Use of antibiotics in the treatment of Crohn's disease. World J Gastroenterol 2013;19:648-653.
189. Osorio F, et al. DC activated via dectin-1 convert Treg into IL-17 producers. Eur J Immunol 2008;38:3274-3281.