Resident enteric microbiota and CD8+ T cells shape the abundance of marginal zone B cells

European Journal of Immunology

Volumn 38, Issue 12, 2008, Pages 3411-3425

  Wei, Bo ^a   Su, Thomas T ^a   Dalwadi, Harnisha ^a   Stephan, Robert P ^b   Fujiwara, Daisuke ^a   Huang, Tiffany T ^a   Brewer, Sarah ^a   Chen, Lindy ^a   Arditi, Moshe ^c   Borneman, James ^d   Rawlings, David J ^e   Braun, Jonathan ^a,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

Animal models; B cell development; CD8 T cells; Enteric microbiota

Indexed keywords

HLA B ANTIGEN; T LYMPHOCYTE RECEPTOR; PROLIFERATION REGULATORY FACTORS, HUMAN URINE; PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; C57BL 6 MOUSE; CD8+ T LYMPHOCYTE; CELL SHAPE; CELLULAR IMMUNITY; CONTROLLED STUDY; CROSS REACTION; ENTEROBACTERIACEAE; FEMALE; GENE MUTATION; INNATE IMMUNITY; INTESTINE FLORA; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOCYTE FUNCTION; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MOUSE; NONHUMAN; POPULATION ABUNDANCE; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; IMMUNOLOGY; MICROBIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL MOVEMENT; CELL SHAPE; MICE; MICE, INBRED C57BL; PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 59749098602     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838432     Document Type: Article

References (64)

1. Savage, D. C., Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 1977. 31: 107-133.
2. Conway, P. L., Microbial ecology of the human large intestine, in: Gibson, G. R. (Ed.), Human Colonic Bacteria: Role in Nutrition, Physiology, and Pathology, CRC Press, Boca Raton 1995, pp. 1-24.
3. Mackie, R. I., Sghir, A. and Gaskins, H. R., Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 1999. 69: 1035S-1045S.
4. Ley, R. E., Peterson, D. A. and Gordon, J. I., Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 2006. 124: 837-848.
5. Janeway, C. A., Jr., How the immune system works to protect the host from infection: A personal view. Proc. Natl. Acad. Sci. USA 2001. 98: 7461-7468.
6. Garrett, W. S., Lord, G. M., Punit, S., Lugo-Villarino, G., Mazmanian, S. K., Ito, S., Glickman, J. N. and Glimcher, L. H., Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007. 131: 33-45.
7. Bendelac, A., Bonneville, M. and Kearney, J. F., Autoreactivity by design: Innate B and T lymphocytes. Nat. Rev. Immunol. 2001. 1: 177-186.
8. Cariappa, A., Tang, M., Parng, C., Nebelitskiy, E., Carroll, M., Georgopoulos, K. and Pillai, S., The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 2001. 14: 603-615.
9. Martin, F., Kearney, J. F., Positive selection from newly formed to marginal zone B cells depends on the rate of clonal production, CD19, and btk. Immunity 2000. 12: 39-49.
10. Scupham, A. J., Presley, L. L., Wei, B., Bent, E., Griffith, N., McPherson, M., Zhu, F. et al., Abundant and diverse fungal microbiota in the murine intestine. Appl. Environ. Microbiol. 2006. 72: 793-801.
11. + T cells and resident microbiota. J. Immunol. 2008. 180: 5843-5852.
12. high T cells to SCID recipients. J. Immunol. 1997. 158: 3464-3473.
13. Srivastava, B., Quinn, W. J., III, Hazard, K., Erikson, J. and Allman, D., Characterization of marginal zone B cell precursors. J. Exp. Med. 2005. 202: 1225-1234.
14. Huang, T., Wei, B., Velazquez, P., Borneman, J. and Braun, J., Commensal microbiota alter the abundance and TCR responsiveness of splenic naive CD4(+) T lymphocytes. Clin. Immunol. 2005. 117: 221-230.
15. Martin, F., Oliver, A. M. and Kearney, J. F., Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001. 14: 617-629.
16. Ansel, K. M., Harris, R. B. and Cyster, J. G., CXCL13 is required for B1 cell homing, natural antibody production, and body cavity immunity. Immunity 2002. 16: 67-76.
17. Kumararatne, D. S. and MacLennan, I. C. M., The origin of marginal-zone cells. Adv. Exp. Med. Biol. 1982. 149: 83-90.
18. high B cells: A population of mixed origin. Eur. J. Immunol. 1999. 29: 3285-3294.
19. Takeuchi, O., Hoshino, K., Kawai, T., Sanjo, H., Takada, H., Ogawa, T., Takeda, K. and Akira, S., Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999. 11: 443-451.
20. Kawai, T., Adachi, O., Ogawa, T., Takeda, K. and Akira, S., Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999. 11: 115-122.
21. Horng, T., Barton, G. M., Flavell, R. A. and Medzhitov, R., The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 2002. 420: 329-333.
22. Hoebe, K., Du, X., Georgel, P., Janssen, E., Tabeta, K., Kim, S. O., Goode, J. et al., Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 2003. 424: 743-748.
23. Martin, F. and Kearney, J. F., Marginal-zone B cells. Nat. Rev. Immunol. 2002. 2: 323-335.
24. Nell, L. J., Kastner, D. L. and Rich, R. R., Qa-1-associated antigens. III. Distribution of Qa-1 region antigens on lymphoid subpopulations. J. Immunol. 1980. 125: 2597-2603.
25. Lo, W. F., Woods, A. S., DeCloux, A., Cotter, R. J., Metcalf, E. S. and Soloski, M. J., Molecular mimicry mediated by MHC class Ib molecules after infection with gram-negative pathogens. Nat. Med. 2000. 6: 215-218.
26. Humphrey, J. H. and Grennan, D., Different macrophage populations distinguished by means of fluorescent polysaccharides. Recognition and properties of marginal-zone macrophages. Eur. J. Immunol. 1981. 11: 221-228.
27. Amlot, P. L., Grennan, D. and Humphrey, J. H., Splenic dependence of the antibody response to thymus-independent (TI-2) antigens. Eur. J. Immunol. 1985. 15: 508-512.
28. Honda, K., Sakaguchi, S., Nakajima, C., Watanabe, A., Yanai, H., Matsumoto, M., Ohteki, T. et al., Selective contribution of IFN-alpha,beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. USA 2003. 100: 10872-10877.
29. Bealmear, P. M., Mirand, E. A. and Holtermann, O. A., Miscellaneous immune defects in gnotobiotic and SPF mice. Prog. Clin. Biol. Res. 1983. 132C: 423-432.
30. Ouwehand, W. H., Isolauri, E. and Salminen, S., The role of the intestinal microflora for the development of the immune system in early childhood. Eur. J. Nutr. 2002. 41: I32-I37.
31. Casola, S., Otipoby, K. L., Alimzhanov, M., Humme, S., Uyttersprot, N., Kutok, J. L., Carroll, M. C. and Rajewsky, K., B cell receptor signal strength determines B cell fate. Nat. Immunol. 2004. 5: 317-327.
32. Shikina, T., Hiroi, T., Iwatani, K., Jang, M. H., Fukuyama, S., Tamura, M., Kubo, T. et al., IgA class switch occurs in the organized nasopharynx- and gut-associated lymphoid tissue, but not in the diffuse lamina propria of airways and gut. J. Immunol. 2004. 172: 6259-6264.
33. Lorenz, R. G., Chaplin, D. D., McDonald, K. G., McDonough, J. S. and Newberry, R. D., 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.
34. Suzuki, K., Meek, B., Doi, Y., Honjo, T. and 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.
35. Bos, N. A., Cebra, J. J. and Kroese, F. G., B-1 cells and the intestinal microflora. Curr. Top. Microbiol. Immunol. 2000. 252: 211-220.
36. Sarma-Rupavtarm, R. B., Ge, Z., Schauer, D. B., Fox, J. G. and Polz, M. F., Spatial distribution and stability of the eight microbial species of the altered schaedler flora in the mouse gastrointestinal tract. Appl. Environ. Microbiol. 2004. 70: 2791-2800.
37. + T cells in immunity to Salmonella infection and the involvement of MHC class Ib molecules. J. Immunol. 1999. 162: 5398-5406.
38. Lo, W. F., Dunn, C. D., Ong, H., Metcalf, E. S. and Soloski, M. J., Bacterial and host factors involved in the major histocompatibility complex class Ib-restricted presentation of Salmonella Hsp 60: Novel pathway. Infect. Immun. 2004. 72: 2843-2849.
39. Ludewig, B., Bonilla, W. V., Dumrese, T., Odermatt, B., Zinkernagel, R. M. and Hengartner, H., Perforin-independent regulation of dendritic cell homeostasis by CD8(+) T cells in vivo: Implications for adaptive immunotherapy. Eur. J. Immunol. 2001. 31: 1772-1779.
40. + T cells in vivo. Proc. Natl. Acad. Sci. USA 2006. 103: 147-152.
41. + T cells enter reactive lymph nodes and kill dendritic cells. Nat. Immunol. 2007. 8: 743-752.
42. Wu, D., Xing, G. W., Poles, M. A., Horowitz, A., Kinjo, Y., Sullivan, B., Bodmer-Narkevitch, V. et al., Bacterial glycolipids and analogs as antigens for CD1d-restricted NKT cells. Proc. Natl. Acad. Sci. USA 2005. 102: 1351-1356.
43. Mattner, J., Debord, K. L., Ismail, N., Goff, R. D., Cantu, C., III, Zhou, D., Saint-Mezard, P. et al., Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 2005. 434: 525-529.
44. Treiner, E., Duban, L., Bahram, S., Radosavljevic, M., Wanner, V., Tilloy, F., Affaticati, P. et al., Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature 2003. 422: 164-169.
45. Kawachi, I., Maldonado, J., Strader, C. and Gilfillan, S., MR1-restricted Vα19i mucosal-associated invariant T cells are innate T cells in the gut lamina propria that provide a rapid and diverse cytokine response. J. Immunol. 2006. 176: 1618-1627.
46. Hansen, T. H., Huang, S., Arnold, P. L. and Fremont, D. H., Patterns of nonclassical MHC antigen presentation. Nat. Immunol. 2007. 8: 563-568.
47. Bonasio, R., Scimone, M. L., Schaerli, P., Grabie, N., Lichtman, A. H. and von Andrian, U. H., Clonal deletion of thymocytes by circulating dendritic cells homing to the thymus. Nat. Immunol. 2006. 7: 1092-1100.
48. Ostman, S., Rask, C., Wold, A. E., Hultkrantz, S. and Telemo, E., Impaired regulatory T cell function in germ-free mice. Eur. J. Immunol. 2006. 36: 2336-2346.
49. Min, B., Thornton, A., Caucheteux, S. M., Younes, S. A., Oh, K., Hu-Li, J. and Paul, W. E., Gut flora antigens are not important in the maintenance of regulatory T cell heterogeneity and homeostasis. Eur. J. Immunol. 2007. 37: 1916-1923.
50. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O. and Kasper, D. L., An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005. 122: 107-118.
51. McClellan, K. B., Gangappa, S., Speck, S. H. and Virgin, H. W., Antibody-independent control of gamma-herpesvirus latency via B cell induction of anti-viral T cell responses. PLoS Pathog 2006. 2: E58.
52. Homann, D., Tishon, A., Berger, D. P., Weigle, W. O., von Herrath, M. G. and Oldstone, M. B., Evidence for an underlying CD4 helper and CD8 T-cell defect in B-cell-deficient mice: Failure to clear persistent virus infection after adoptive immunotherapy with virus-specific memory cells from muMT/muMT mice. J. Virol. 1998. 72: 9208-9216.
53. Chang, C. and Miller, J. F., Campylobacter jejuni colonization of mice with limited enteric flora. Infect. Immun. 2006. 74: 5261-5271.
54. + T in the protective regulation of systemic inflammation. Clin. Immunol. 2008. 127:303-312.
55. + regulatory T cells in the lamina propria of patients with inflammatory bowel disease. J. Immunol. 2005. 174: 5814-5822.
56. Lin, Q., Dong, C. and Cooper, M. D., Impairment of T and B cell development by treatment with a type I interferon. J. Exp. Med. 1998. 187: 79-87.
57. Meraz, M. A., White, J. M., Sheehan, K. C., Bach, E. A., Rodig, S. J., Dighe, A. S., Kaplan, D. H. et al., Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 1996. 84: 431-442.
58. Fung-Leung, W. P., Schilham, M. W., Rahemtulla, A., Kundig, T. M., Vollenweider, M., Potter, J., van Ewijk, W. and Mak, T. W., CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell 1991. 65: 443-449.
59. van den Broek, M. E., Kagi, D., Ossendorp, F., Toes, R., Vamvakas, S., Lutz, W. K., Melief, C. J. et al., Decreased tumor surveillance in perforindeficient mice. J. Exp. Med. 1996. 184: 1781-1790.
60. Dalwadi, H., Wei, B., Schrage, M., Spicher, K., Birnbaumer, L., Su, T. T., Rawlings, D. J. and Braun, J., B cell developmental requirement for the Gài2 gene. J. Immunol. 2003. 170: 1707-1715.
61. Davies, A., Kalb, S., Liang, B., Aldrich, C. J., Lemonnier, F. A., Jiang, H., Cotter, R. and Soloski, M. J., A peptide from heat shock protein 60 is the dominant peptide bound to Qa-1 in the absence of the MHC class Ia leader sequence peptide Qdm. J. Immunol. 2003. 170: 5027-5033.
62. Su, T. T. and Rawlings, D. J., Transitional B lymphocyte subsets operate as distinct checkpoints in murine splenic B cell development. J. Immunol. 2002. 168: 2101-2110.
63. Dalwadi, H., Wei, B., Kronenberg, M., Sutton, C. L. and Braun, J., The Crohn's disease-associated bacterial protein 12 is a novel enteric T cell superantigen. Immunity 2001. 15: 149-158.
64. - 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. J. Exp. Med. 1998. 187: 855-864.