Impaired selection of IgA and intestinal dysbiosis associated with PD-1-deficiency

Gut Microbes

Volumn 4, Issue 2, 2013, Pages 165-171

  Maruya, Mikako ^a   Kawamoto, Shimpei ^a   Kato, Lucia M ^a   Fagarasan, Sidonia ^a  

^a RIKEN YOKOHAMA INSTITUTE   (Japan)

Author keywords

Germinal center; Gut; IgA; Microbiota; PD 1; TFH

Indexed keywords

ANTIBIOTIC AGENT; CHEMOKINE RECEPTOR CXCR5; IMMUNOGLOBULIN A; INTERLEUKIN 21; PROGRAMMED DEATH 1 RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ARTICLE; CELL EXPANSION; CELL SELECTION; CYTOKINE PRODUCTION; ENTEROPATHY; GERMINAL CENTER; HUMAN; INTESTINE DYSBIOSIS; MICROBIAL COMMUNITY; NONHUMAN; PEYER PATCH; PROTEIN DEFICIENCY; SOMATIC HYPERMUTATION; T LYMPHOCYTE;

GERMINAL CENTER; GUT; IGA; MICROBIOTA; PD-1; TFH;

ANIMALS; ANTIGENS, DIFFERENTIATION; B-LYMPHOCYTES; GASTROINTESTINAL TRACT; GERMINAL CENTER; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; METAGENOME; MICE; MICE, KNOCKOUT; PEYER'S PATCHES; T-LYMPHOCYTES;

EID: 84874694349     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.23595     Document Type: Article

References (35)

1. Sutherland DB, Fagarasan S. IgA synthesis: a form of functional immune adaptation extending beyond gut. Curr Opin Immunol 2012; 24:261-268;PMID:22503962; http://dx.doi.org/10.1016/j.coi.2012.03.005.
2. 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; PMID:20192805; http://dx.doi.org/10.1146/annurev-immunol-030409-101314.
3. Strugnell RA, Wijburg OL. The role of secretory antibodies in infection immunity. Nat Rev Microbiol 2010; 8:656-667; PMID:20694027; http://dx.doi. org/10.1038/nrmicro2384.
4. Suzuki K, Kawamoto S, Maruya M, Fagarasan S. GALT: organization and dynamics leading to IgA synthesis. Adv Immunol 2010; 107:153-185;PMID:21034974; http://dx.doi.org/10.1016/B978- 0-12-381300-8.00006-X.
5. 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; PMID:12434060; http://dx.doi.org/10.1126/science.1077336.
6. Wei M, Shinkura R, Doi Y, Maruya M, Fagarasan S, Honjo T. Mice carrying a knock-in mutation of Aicda resulting in a defect in somatic hypermutation have impaired gut homeostasis and compromised mucosal defense. Nat Immunol 2011; 12:264-270; PMID:21258321; http://dx.doi.org/10.1038/ni.1991.
7. Jacob J, Kelsoe G, Rajewsky K, Weiss U. Intraclonal generation of antibody mutants in germinal centres. Nature 1991; 354:389-392; PMID:1956400; http://dx.doi.org/10.1038/354389a0.
8. 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; PMID:11007474; http://dx.doi.org/10.1016/S0092-8674(00)00078-7.
9. 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; PMID:17911595.
10. Okazaki T, Honjo T. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol 2006; 27:195-201; PMID:16500147; http://dx.doi. org/10.1016/j.it.2006.02.001.
11. Shimatani K, Nakashima Y, Hattori M, Hamazaki Y, Minato N. PD-1+ memory phenotype CD4+ T cells expressing C/EBPalpha underlie T cell immunode- pression in senescence and leukemia. Proc Natl Acad Sci U S A 2009; 106:15807-15812; PMID:19805226; http://dx.doi.org/10.1073/pnas.0908805106.
12. Okazaki T, Okazaki IM, Wang J, Sugiura D, Nakaki F, Yoshida T, et al. PD-1 and LAG-3 inhibitory co-receptors act synergistically to prevent autoimmunity in mice. J Exp Med 2011; 208:395-407; PMID:21300912; http://dx.doi.org/10.1084/jem.20100466.
13. Kawamoto S, Tran TH, Maruya M, Suzuki K, Doi Y, Tsutsui Y, et al. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science 2012; 336:485-489; PMID:22539724; http://dx.doi.org/10.1126/science.1217718.
14. Riley JL. PD-1 signaling in primary T cells. Immunol Rev 2009; 229:114-125; PMID:19426218; http://d x.doi.org/10.1111/j.1600-065X.2009.00767.x.
15. Good-Jacobson KL, Szumilas CG, Chen L, Sharpe AH, Tomayko MM, Shlomchik MJ. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat Immunol 2010; 11:535-542; PMID:20453843; http://dx.doi. org/10.1038/ni.1877.
16. Allen CD, Okada T, Cyster JG. Germinal-center organization and cellular dynamics. Immunity 2007; 27:190-202;PMID:17723214; http://dx.doi.org/10.1016/j.immuni.2007.07.0 09.
17. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011; 469:543-547; PMID:21270894; http://dx.doi.org/10.1038/nature09646.
18. Obata T, Goto Y, Kunisawa J, Sato S, Sakamoto M, Setoyama H, et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis. Proc Natl Acad Sci U S A 2010; 107:7419-424; PMID:20360558; http://dx.doi.org/10.1073/pnas.1001061107.
19. Sonnenberg GF, Monticelli LA, Alenghat T, Fung TC, Hutnick NA, Kunisawa J, et al. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria. Science 2012; 336:1321-1325PMID:22674331; http://dx.doi. org/10.1126/science.1222551.
20. Arthur JC, Perez-Chanona E, Mühlbauer M, Tomkovich S, Uronis JM, Fan TJ, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012; 338:120-123; PMID:22903521; http://dx.doi.org/10.1126/science.1224820.
21. De Palma G, Nadal I, Medina M, Donat E, Ribes- Koninckx C, Calabuig M, et al. Intestinal dysbiosis and reduced immunoglobulin-coated bacteria associated with coeliac disease in children. BMC Microbiol 2010; 10:63; PMID:20181275; http:// dx.doi.org/10.1186/1471-2180-10-63.
22. Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145:745-757; PMID:21565393; http://dx.doi.org/10.1016/j.cell.2011.04.022.
23. Suzuki K, Maruya M, Kawamoto S, Sitnik K, Kitamura H, Agace W W, et al. Suzuki K, Meek B, Doi Y, Muramatsu M, Chiba T, Honjo T, et al. Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci U S A 2004; 101:1981-1986; PMID:14766966; http://dx.doi.org/10.1073/pnas.0307317101.
24. Suzuki K, Maruya M, Kawamoto S, Sitnik K, Kitamura H, Agace WW, et al. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 2010; 33:71-83; PMID:20643338; http://dx.doi.org/10.1016/j.immuni.2010.07.003.
25. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol 2011; 29:621-663; PMID:21314428; http://dx.doi.org/10.1146/annurev-immunol-031210-101400.
26. Okada T, Moriyama S, Kitano M. Differentiation of germinal center B cells and follicular helper T cells as viewed by tracking Bcl6 expression dynamics. Immunol Rev 2012; 247:120-132; PMI D:22500836; ht t p: //dx.doi.org/10.1111/j.160 0-065X.2012.01120.x.
27. Ozaki K, Spolski R, Ettinger R, Kim HP, Wang G, Qi CF, et al. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J Immunol 2004; 173:5361-5371; PM I D:1549 4 4 82.
28. Zotos D, Coquet JM, Zhang Y, Light A, D'Costa K, Kallies A, 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; PMID:20142430; http://dx.doi.org/10.1084/ jem.20091777.
29. Allen CD, Okada T, Tang HL, Cyster JG. Imaging of germinal center selection events during affinity maturation. Science 2007; 315:528-531; PMID:17185562; http://dx.doi.org/10.1126/science.1136736.
30. Victora GD, Schwickert TA, Fooksman DR, Kamphorst AO, Meyer-Hermann M, Dustin ML, et al. Germinal center dynamics revealed by multiphoton microscopy with a photoactivatable fluorescent reporter. Cell 2010; 143:592-605;PMID:21074050; http: //dx.doi.org/10.1016/j.cell.2010.10.032.
31. Tsuji M, Komatsu N, Kawamoto S, Suzuki K, Kanagawa O, Honjo T, et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009; 323:1488-1492; PMID:19286559; http://dx.doi.org/10.1126/science.1169152.
32. Slack E, Hapfelmeier S, Stecher B, Velykoredko Y, Stoel M, Lawson MA, et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009; 325:617-620; PMID:19644121; http://dx.doi.org/10.1126/science.117 2 747.
33. Wang N, Shen N, Vyse TJ, Anand V, Gunnarson I, Sturfelt G, et al. Selective IgA deficiency in autoimmune diseases. Mol Med 2011; 17:1383-1396; PMID: 21826374.
34. Aytekin C, Tuygun N, Gokce S, Dogu F, Ikinciogullari A. Selective IgA deficiency: clinical and laboratory features of 118 children in Turkey. J Clin Immunol 2012; 32:961-6; PMID:22547079; http: //dx.doi.org/10.1007/s10875-012-9702-3.
35. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010; 32:815-827; PMID:20620945; http: //dx.doi.org /10.1016/j.immuni.2010.06.001.