Roles of B-1 and B-2 cells in innate and acquired IgA-mediated immunity

Immunological Reviews

Volumn 237, Issue 1, 2010, Pages 180-190

  Suzuki, Keiichiro ^a   Maruya, Mikako ^a   Kawamoto, Shimpei ^a,b   Fagarasan, Sidonia ^a  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

AID; B 1 cells; bacteria; IgA; T dependent; T independent

Indexed keywords

CD11B ANTIGEN; CD23 ANTIGEN; CD45 ANTIGEN; CD5 ANTIGEN; CD9 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR5; COLLAGENASE 3; CXCL13 CHEMOKINE; GELATINASE B; IMMUNOGLOBULIN A; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 7; LYMPHOCYTE SURFACE MARKER; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MUCOSAL ADDRESSIN CELL ADHESION MOLECULE 1; RETINOIC ACID; THYMIC STROMAL LYMPHOPOIETIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR PAX5; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1;

ANTIGEN SPECIFICITY; B 1 CELL; B 2 CELL; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL MIGRATION; CELL RENEWAL; CELLULAR DISTRIBUTION; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNOGLOBULIN PRODUCTION; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; LYMPHOID PROGENITOR CELL; MICROBIAL COMMUNITY; NONHUMAN; PERITONEAL CAVITY; PERITONEUM; PRE B LYMPHOCYTE; PRIORITY JOURNAL; RETINOL DEFICIENCY; REVIEW; SPLEEN; VIRUS INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; B-LYMPHOCYTE SUBSETS; B-LYMPHOCYTES; HUMANS; IMMUNITY, INNATE; IMMUNOGLOBULIN A;

EID: 77955863142     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2010.00941.x     Document Type: Review

References (126)

1. Sonnenburg JL, Angenent LT, Gordon JI. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine? Nat Immunol 2004 5:569 573.
2. Hooper LV, Gordon JI. Commensal host-bacterial relationships in the gut. Science 2001 292:1115 1118.
3. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science 2005 307:1915 1920.
4. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006 124:837 848.
5. Cebra JJ. Influences of microbiota on intestinal immune system development. Am J Clin Nutr 1999 69:1046S 1051S.
6. Macpherson AJ, Harris NL. Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 2004 4:478 485.
7. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005 122:107 118.
8. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol 2008 1:11 22.
9. Fagarasan S, Kawamoto S, Kanagawa O, Suzuki K. Adaptive immune regulation in the gut: T cell-dependent and T cell-independent IgA synthesis. Annu Rev Immunol 2010 28:243 273.
10. Cerutti A, Rescigno M. The biology of intestinal immunoglobulin A responses. Immunity 2008 28:740 750.
11. Kantor AB, Herzenberg LA. Origin of murine B cell lineages. Annu Rev Immunol 1993 11:501 538.
12. Hardy RR, Hayakawa K. B cell development pathways. Annu Rev Immunol 2001 19:595 621.
13. Martin F, Kearney JF. B1 cells: similarities and differences with other B cell subsets. Curr Opin Immunol 2001 13:195 201.
14. Won WJ, Kearney JF. CD9 is a unique marker for marginal zone B cells, B1 cells, and plasma cells in mice. J Immunol 2002 168:5605 5611.
15. Ha SA, et al. Regulation of B1 cell migration by signals through Toll-like receptors. J Exp Med 2006 203:2541 2550.
16. Berberich S, Forster R, Pabst O. The peritoneal micromilieu commits B cells to home to body cavities and the small intestine. Blood 2007 109:4627 4634.
17. Tumang JR, Hastings WD, Bai C, Rothstein TL. Peritoneal and splenic B-1 cells are separable by phenotypic, functional, and transcriptomic characteristics. Eur J Immunol 2004 34:2158 2167.
18. Hastings WD, Tumang JR, Behrens TW, Rothstein TL. Peritoneal B-2 cells comprise a distinct B-2 cell population with B-1b-like characteristics. Eur J Immunol 2006 36:1114 1123.
19. Stoermann B, Kretschmer K, Duber S, Weiss S. B-1a cells are imprinted by the microenvironment in spleen and peritoneum. Eur J Immunol 2007 37:1613 1620.
20. Berland R, Wortis HH. Origins and functions of B-1 cells with notes on the role of CD5. Annu Rev Immunol 2002 20:253 300.
21. Hardy RR, Carmack CE, Shinton SA, Riblet RJ, Hayakawa K. A single VH gene is utilized predominantly in anti-BrMRBC hybridomas derived from purified Ly-1 B cells. Definition of the VH11 family. J Immunol 1989 142:3643 3651.
22. Casali P, Burastero SE, Nakamura M, Inghirami G, Notkins AL. Human lymphocytes making rheumatoid factor and antibody to ssDNA belong to Leu-1+ B-cell subset. Science 1987 236:77 81.
23. Hayakawa K, Carmack CE, Hyman R, Hardy RR. Natural autoantibodies to thymocytes: origin, VH genes, fine specificities, and the role of Thy-1 glycoprotein. J Exp Med 1990 172:869 878.
24. Hayakawa K, Hardy RR, Herzenberg LA. Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J Exp Med 1985 161:1554 1568.
25. Hardy RR, Hayakawa K. A developmental switch in B lymphopoiesis. Proc Natl Acad Sci USA 1991 88:11550 11554.
26. Herzenberg LA. B-1 cells: the lineage question revisited. Immunol Rev 2000 175:9 22.
27. Lam KP, Rajewsky K. B cell antigen receptor specificity and surface density together determine B-1 versus B-2 cell development. J Exp Med 1999 190:471 477.
28. Watanabe N, Nisitani S, Ikuta K, Suzuki M, Chiba T, Honjo T. Expression levels of B cell surface immunoglobulin regulate efficiency of allelic exclusion and size of autoreactive B-1 cell compartment. J Exp Med 1999 190:461 469.
29. Montecino-Rodriguez E, Leathers H, Dorshkind K. Identification of a B-1 B cell-specified progenitor. Nat Immunol 2006 7:293 301.
30. Herzenberg LA, Tung JW. B cell lineages: documented at last Nat Immunol 2006 7:225 226.
31. Astrakhan A, et al. Local increase in thymic stromal lymphopoietin induces systemic alterations in B cell development. Nat Immunol 2007 8:522 531.
32. Esplin BL, Welner RS, Zhang Q, Borghesi LA, Kincade PW. A differentiation pathway for B1 cells in adult bone marrow. Proc Natl Acad Sci USA 2009 106:5773 5778.
33. Chen X, Esplin BL, Garrett KP, Welner RS, Webb CF, Kincade PW. Retinoids accelerate B lineage lymphoid differentiation. J Immunol 2008 180:138 145.
34. Chen X, Welner RS, Kincade PW. A possible contribution of retinoids to regulation of fetal B lymphopoiesis. Eur J Immunol 2009 39:2515 2524.
35. Kantor AB, Stall AM, Adams S, Watanabe K, Herzenberg LA. De novo development and self-replenishment of B cells. Int Immunol 1995 7:55 68.
36. Karras JG, Wang Z, Huo L, Howard RG, Frank DA, Rothstein TL. Signal transducer and activator of transcription-3 (STAT3) is constitutively activated in normal, self-renewing B-1 cells but only inducibly expressed in conventional B lymphocytes. J Exp Med 1997 185:1035 1042.
37. Solvason N, et al. Cyclin D2 is essential for BCR-mediated proliferation and CD5 B cell development. Int Immunol 2000 12:631 638.
38. Mohamedali A, et al. Cyclin D2 controls B cell progenitor numbers. J Leukoc Biol 2003 74:1139 1143.
39. Hoffmann A, et al. Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population. Nat Immunol 2007 8:695 704.
40. Ding C, Liu Y, Wang Y, Park BK, Wang CY, Zheng P. Siglecg limits the size of B1a B cell lineage by down-regulating NFkappaB activation. PLoS ONE 2007 2:e997.
41. Jellusova J, Wellmann U, Amann K, Winkler TH, Nitschke L. CD22 x Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J Immunol 2010 184:3618 3627.
42. Wardemann H, Boehm T, Dear N, Carsetti R. B-1a B cells that link the innate and adaptive immune responses are lacking in the absence of the spleen. J Exp Med 2002 195:771 780.
43. Yang Y, Tung JW, Ghosn EE, Herzenberg LA. Division and differentiation of natural antibody-producing cells in mouse spleen. Proc Natl Acad Sci USA 2007 104:4542 4546.
44. Forster I, Vieira P, Rajewsky K. Flow cytometric analysis of cell proliferation dynamics in the B cell compartment of the mouse. Int Immunol 1989 1:321 331.
45. Kopf M, et al. IL-5-deficient mice have a developmental defect in CD5+ B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 1996 4:15 24.
46. Yoshida T, et al. Defective B-1 cell development and impaired immunity against Angiostrongylus cantonensis in IL-5R alpha-deficient mice. Immunity 1996 4:483 494.
47. Moro K, et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 2010 463:540 544.
48. Rangel-Moreno J, et al. Omental milky spots develop in the absence of lymphoid tissue-inducer cells and support B and T cell responses to peritoneal antigens. Immunity 2009 30:731 743.
49. Ansel KM, Harris RB, Cyster JG. CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 2002 16:67 76.
50. Arroyo AG, Yang JT, Rayburn H, Hynes RO. Differential requirements for alpha4 integrins during fetal and adult hematopoiesis. Cell 1996 85:997 1008.
51. Arroyo AG, et al. In vivo roles of integrins during leukocyte development and traffic: insights from the analysis of mice chimeric for alpha 5, alpha v, and alpha 4 integrins. J Immunol 2000 165:4667 4675.
52. Itakura A, et al. An hour after immunization peritoneal B-1 cells are activated to migrate to lymphoid organs where within 1 day they produce IgM antibodies that initiate elicitation of contact sensitivity. J Immunol 2005 175:7170 7178.
53. Choi YS, Baumgarth N. Dual role for B-1a cells in immunity to influenza virus infection. J Exp Med 2008 205:3053 3064.
54. Fagarasan S, et al. Alymphoplasia (aly)-type nuclear factor kappaB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J Exp Med 2000 191:1477 1486.
55. Kunisawa J, et al. Sphingosine 1-phosphate regulates peritoneal B-cell trafficking for subsequent intestinal IgA production. Blood 2007 109:3749 3756.
56. Kunisawa J, Gohda M, Kurashima Y, Ishikawa I, Higuchi M, Kiyono H. Sphingosine 1-phosphate-dependent trafficking of peritoneal B cells requires functional NFkappaB-inducing kinase in stromal cells. Blood 2008 111:4646 4652.
57. 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.
58. Stoel M, et al. Restricted IgA repertoire in both B-1 and B-2 cell-derived gut plasmablasts. J Immunol 2005 174:1046 1054.
59. Shimomura Y, et al. Regulatory role of B-1 B cells in chronic colitis. Int Immunol 2008 20:729 737.
60. Savitsky D, Calame K. B-1 B lymphocytes require Blimp-1 for immunoglobulin secretion. J Exp Med 2006 203:2305 2314.
61. Nixon JC, Ferrell S, Miner C, Oldham AL, Hochgeschwender U, Webb CF. Transgenic mice expressing dominant-negative bright exhibit defects in B1 B cells. J Immunol 2008 181:6913 6922.
62. Nishikawa S, Honda K, Vieira P, Yoshida H. Organogenesis of peripheral lymphoid organs. Immunol Rev 2003 195:72 80.
63. Randall TD, Carragher DM, Rangel-Moreno J. Development of secondary lymphoid organs. Annu Rev Immunol 2008 26:627 650.
64. Suzuki K, Fagarasan S. How host-bacterial interactions lead to IgA synthesis in the gut. Trends Immunol 2008 29:523 531.
65. Hamada H, et al. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J Immunol 2002 168:57 64.
66. Tsuji M, Suzuki K, Kinoshita K, Fagarasan S. Dynamic interactions between bacteria and immune cells leading to intestinal IgA synthesis. Semin Immunol 2008 20:59 66.
67. Bouskra D, et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008 456:507 510.
68. Fagarasan S, Muramatsu M, Suzuki K, Nagaoka H, Hiai H, Honjo T. Critical roles of activation-induced cytidine deaminase (AID) in the homeostasis of gut flora. Science 2002 298:1424 1427.
69. Lorenz RG, Chaplin DD, McDonald KG, McDonough JS, Newberry RD. Isolated lymphoid follicle formation is inducible and dependent upon lymphotoxin- sufficient B lymphocytes, lymphotoxin beta receptor, and TNF receptor I function. J Immunol 2003 170:5475 5482.
70. Pabst O, et al. Cryptopatches and isolated lymphoid follicles: dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur J Immunol 2005 35:98 107.
71. Muramatsu M, Kinoshita K, Fagarasan S, Yamada S, Shinkai Y, Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000 102:553 563.
72. Kang HS, et al. Signaling via LTbetaR on the lamina propria stromal cells of the gut is required for IgA production. Nat Immunol 2002 3:576 582.
73. Eberl G, Marmon S, Sunshine MJ, Rennert PD, Choi Y, Littman DR. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat Immunol 2004 5:64 73.
74. Tsuji M, et al. Requirement for lymphoid tissue-inducer cells in isolated follicle formation and T cell-independent immunoglobulin A generation in the gut. Immunity 2008 29:261 271.
75. McDonald KG, McDonough JS, Wang C, Kucharzik T, Williams IR, Newberry RD. CC chemokine receptor 6 expression by B lymphocytes is essential for the development of isolated lymphoid follicles. Am J Pathol 2007 170:1229 1240.
76. Muramatsu M, et al. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem 1999 274:18470 18476.
77. Casola S, et al. B cell receptor signal strength determines B cell fate. Nat Immunol 2004 5:317 327.
78. King C, Tangye SG, Mackay CR. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu Rev Immunol 2008 26:741 766.
79. 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.
80. Hardtke S, Ohl L, Forster R. Balanced expression of CXCR5 and CCR7 on follicular T helper cells determines their transient positioning to lymph node follicles and is essential for efficient B-cell help. Blood 2005 106:1924 1931.
81. Haynes NM, Allen CD, Lesley R, Ansel KM, Killeen N, Cyster JG. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J Immunol 2007 179:5099 5108.
82. Vinuesa CG, Tangye SG, Moser B, Mackay CR. Follicular B helper T cells in antibody responses and autoimmunity. Nat Rev Immunol 2005 5:853 865.
83. Suzuki K, Meek B, Doi Y, Honjo T, Fagarasan S. Two distinctive pathways for recruitment of naive and primed IgM+ B cells to the gut lamina propria. Proc Natl Acad Sci USA 2005 102:2482 2486.
84. Velazquez P, et al. Villous B cells of the small intestine are specialized for invariant NK T cell dependence. J Immunol 2008 180:4629 4638.
85. Cazac BB, Roes J. TGF-beta receptor controls B cell responsiveness and induction of IgA in vivo. Immunity 2000 13:443 451.
86. Borsutzky S, Cazac BB, Roes J, Guzman CA. TGF-beta receptor signaling is critical for mucosal IgA responses. J Immunol 2004 173:3305 3309.
87. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003 116:217 224.
88. Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 2007 26:579 591.
89. Pesu M, et al. T-cell-expressed proprotein convertase furin is essential for maintenance of peripheral immune tolerance. Nature 2008 455:246 250.
90. 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.
91. Travis MA, et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature 2007 449:361 365.
92. Gros MJ, Naquet P, Guinamard RR. Cell intrinsic TGF-beta 1 regulation of B cells. J Immunol 2008 180:8153 8158.
93. Suzuki K, et al. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010.
94. Iwasaki A, Kelsall BL. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 1999 190:229 239.
95. Sato A, Hashiguchi M, Toda E, Iwasaki A, Hachimura S, Kaminogawa S. CD11b+ Peyer's patch dendritic cells secrete IL-6 and induce IgA secretion from naive B cells. J Immunol 2003 171:3684 3690.
96. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004 21:527 538.
97. Mora JR, et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006 314:1157 1160.
98. Linterman MA, et al. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J Exp Med 2010 207:353 363.
99. Zotos D, et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell-intrinsic mechanism. J Exp Med 2010 207:365 378.
100. Dullaers M, et al. A T cell-dependent mechanism for the induction of human mucosal homing immunoglobulin A-secreting plasmablasts. Immunity 2009 30:120 129.
101. Tezuka H, et al. Regulation of IgA production by naturally occurring TNFiNOS-producing dendritic cells. Nature 2007 448:929 933.
102. Litinskiy MB, et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat Immunol 2002 3:822 829.
103. Xu W, et al. Epithelial cells trigger frontline immunoglobulin class switching through a pathway regulated by the inhibitor SLPI. Nat Immunol 2007 8:294 303.
104. He B, et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 2007 26:812 826.
105. Shang L, et al. Toll-like receptor signaling in small intestinal epithelium promotes B-cell recruitment and IgA production in lamina propria. Gastroenterology 2008 135:529 538.
106. 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.
107. Crouch EE, et al. Regulation of AID expression in the immune response. J Exp Med 2007 204:1145 1156.
108. Rescigno M, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001 2:361 367.
109. Niess JH, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005 307:254 258.
110. Bogunovic M, et al. Origin of the lamina propria dendritic cell network. Immunity 2009 31:513 525.
111. Schulz O, et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J Exp Med 2009 206:3101 3114.
112. Sun CM, et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 2007 204:1775 1785.
113. Uematsu S, et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 2008 9:769 776.
114. Varol C, et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 2009 31:502 512.
115. Iliev ID, Mileti E, Matteoli G, Chieppa M, Rescigno M. Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol 2009 2:340 350.
116. Brandtzaeg P. Induction of secretory immunity and memory at mucosal surfaces. Vaccine 2007 25:5467 5484.
117. Harris NL, et al. Mechanisms of neonatal mucosal antibody protection. J Immunol 2006 177:6256 6262.
118. Macpherson AJ, Uhr T. Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004 303:1662 1665.
119. Slack E, et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009 325:617 620.
120. Rey J, Garin N, Spertini F, Corthesy B. Targeting of secretory IgA to Peyer's patch dendritic and T cells after transport by intestinal M cells. J Immunol 2004 172:3026 3033.
121. Suzuki K, et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci USA 2004 101:1981 1986.
122. Salzman NH, et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010 11:76 83.
123. 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.
124. Ivanov II, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009 139:485 498.
125. Doreau A, et al. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat Immunol 2009 10:778 785.
126. 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.