Insulinoma-released exosomes activate autoreactive marginal zone-like B cells that expand endogenously in prediabetic NOD mice

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2588-2597

  Bashratyan, Roman ^a   Sheng, Huiming ^a   Regn, Danielle ^a   Rahman, M Jubayer ^a   Dai, Yang D ^a  

^a TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

Author keywords

Autoimmunity; Autoreactive B cells; Exosomes; NOD; Type 1 diabetes (T1D)

Indexed keywords

CHEMOKINE; CYTOKINE; MYELOID DIFFERENTIATION FACTOR 88; TACROLIMUS; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE RELEASE; EXOSOME; IMPAIRED GLUCOSE TOLERANCE; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; INSULINOMA; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PRIORITY JOURNAL;

AUTOIMMUNITY; AUTOREACTIVE B CELLS; EXOSOMES; NOD; TYPE 1 DIABETES (T1D);

ANIMALS; AUTOANTIGENS; B-LYMPHOCYTES; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DISEASE SUSCEPTIBILITY; EXOSOMES; IMMUNOGLOBULINS; INFLAMMATION MEDIATORS; INSULIN; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED NOD; MYELOID DIFFERENTIATION FACTOR 88; PRECURSOR CELLS, B-LYMPHOID; SIGNAL TRANSDUCTION; TACROLIMUS; TOLL-LIKE RECEPTORS;

EID: 84885816903     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343376     Document Type: Article

References (46)

1. Sercarz, E. E., Driver clones and determinant spreading. J. Autoimmun. 2000. 14: 275-277.
2. Nakayama, M., Abiru, N., Moriyama, H., Babaya, N., Liu, E., Miao, D., Yu, L. et al., Prime role for an insulin epitope in the development of type 1 diabetes in NOD mice. Nature 2005. 435: 220-223.
3. Pugliese, A., Brown, D., Garza, D., Murchison, D., Zeller, M., Redondo, M., Diez J. et al., Self-antigen-presenting cells expressing diabetes-associated autoantigens exist in both thymus and peripheral lymphoid organs. J. Clin. Invest. 2001. 107: 555-564.
4. Gotter, J., Brors, B., Hergenhahn, M. and Kyewski, B., Medullary epithelial cells of the human thymus express a highly diverse selection of tissue-specific genes colocalized in chromosomal clusters. J. Exp. Med. 2004. 199: 155-166.
5. Quinn, A., McInerney, B., Reich, E. P., Kim, O., Jensen, K. P. and Sercarz, E. E., Regulatory and effector CD4 T cells in nonobese diabetic mice recognize overlapping determinants on glutamic acid decarboxylase and use distinct V beta genes. J. Immunol. 2001. 166: 2982-2991.
6. Stadinski, B. D., Zhang, L., Crawford, F., Marrack, P., Eisenbarth, G. S. and Kappler, J. W., Diabetogenic T cells recognize insulin bound to IAg7 in an unexpected, weakly binding register. Proc. Natl. Acad. Sci. USA 2010. 107: 10978-10983.
7. Mohan, J. F., Petzold, S. J. and Unanue, E. R., Register shifting of an insulin peptide-MHC complex allows diabetogenic T cells to escape thymic deletion. J. Exp. Med. 2011. 208: 2375-2383.
8. Mannering, S. I., Harrison, L. C., Williamson, N. A., Morris, J. S., Thearle, D. J., Jensen, K. P., Kay, T. W. et al., The insulin A-chain epitope recognized by human T cells is posttranslationally modified. J. Exp. Med. 2005. 202: 1191-1197.
9. Wicker, L. S., Clark, J., Fraser, H. I., Garner, V. E., Gonzalez-Munoz, A., Healy, B., Howlett, S. et al., Type 1 diabetes genes and pathways shared by humans and NOD mice. J. Autoimmun. 2005. 25 (Suppl): 29-33.
10. Trudeau, J. D., Dutz, J. P., Arany, E., Hill, D. J., Fieldus, W. E. and Finegood, D. T., Neonatal beta-cell apoptosis: a trigger for autoimmune diabetes? Diabetes 2000. 49: 1-7.
11. Diana, J., Simoni, Y., Furio, L., Beaudoin, L., Agerberth, B., Barrat, F. and Lehuen, A., Crosstalk between neutrophils, B-1a cells and plasmacytoid dendritic cells initiates autoimmune diabetes. Nat. Med. 2013. 19: 65-73.
12. Winer, S., Tsui, H., Lau, A., Song, A., Li, X., Cheung, R. K., Sampson, A. et al., Autoimmune islet destruction in spontaneous type 1 diabetes is not beta-cell exclusive. Nat. Med. 2003. 9: 198-205.
13. Thery, C., Ostrowski, M. and Segura, E., Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009. 9: 581-593.
14. Zitvogel, L., Regnault, A., Lozier, A., Wolfers, J., Flament, C., Tenza, D., Ricciardi-Castagnoli, P. et al., Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med. 1998. 4: 594-600.
15. Chen, W., Wang, J., Shao, C., Liu, S., Yu, Y., Wang, Q. and Cao, X., Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells. Eur. J. Immunol. 2006. 36: 1598-1607.
16. Xiang, X., Poliakov, A., Liu, C., Liu, Y., Deng, Z. B., Wang, J., Cheng, Z. et al., Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer 2009. 124: 2621-2633.
17. Wieckowski, E. U., Visus, C., Szajnik, M., Szczepanski, M. J., Storkus, W. J. and Whiteside, T. L., Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J. Immunol. 2009. 183: 3720-3730.
18. Sheng, H., Hassanali, S., Nugent, C., Wen, L., Hamilton-Williams, E., Dias, P. and Dai, Y. D., Insulinoma-released exosomes or microparticles are immunostimulatory and can activate autoreactive T cells spontaneously developed in nonobese diabetic mice. J. Immunol. 2011. 187: 1591-1600.
19. Klein, U., Rajewsky, K. and Kuppers, R., Human immunoglobulin (Ig)M+IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 1998. 188: 1679-1689.
20. Marino, E., Batten, M., Groom, J., Walters, S., Liuwantara, D., Mackay, F. and Grey, S. T., Marginal-zone B-cells of nonobese diabetic mice expand with diabetes onset, invade the pancreatic lymph nodes, and present autoantigen to diabetogenic T-cells. Diabetes 2008. 57: 395-404.
21. Tabeta, K., Hoebe, K., Janssen, E. M., Du, X., Georgel, P., Crozat, K., Mudd, S. et al., The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 2006. 7: 156-164.
22. Kono, D. H., Haraldsson, M. K., Lawson, B. R., Pollard, K. M., Koh, Y. T., Du, X., Arnold, C. N. et al., Endosomal TLR signaling is required for anti-nucleic acid and rheumatoid factor autoantibodies in lupus. Proc. Natl. Acad. Sci. USA 2009. 106: 12061-12066.
23. Woodward, E. J. and Thomas, J. W., Multiple germline kappa light chains generate anti-insulin B cells in nonobese diabetic mice. J. Immunol. 2005. 175: 1073-1079.
24. Wicker, L. S., Boltz, R. C., Jr., Matt, V., Nichols, E. A., Peterson, L. B. and Sigal, N. H., Suppression of B cell activation by cyclosporin A, FK506 and rapamycin. Eur. J. Immunol. 1990. 20: 2277-2283.
25. Quintana, F. J. and Cohen, I. R., The natural autoantibody repertoire and autoimmune disease. Biomed. Pharmacother. 2004. 58: 276-281.
26. Corte-Real, J., Duarte, N., Tavares, L. and Penha-Goncalves, C., Autoimmunity triggers in the NOD mouse: a role for natural auto-antibody reactivities in type 1 diabetes. Ann. NY Acad. Sci. 2009. 1173: 442-448.
27. Bendelac, A., Bonneville, M. and Kearney, J. F., Autoreactivity by design: innate B and T lymphocytes. Nat. Rev. Immunol. 2001. 1: 177-186.
28. Rolf, J., Motta, V., Duarte, N., Lundholm, M., Berntman, E., Bergman, M. L., Sorokin, L. et al., The enlarged population of marginal zone/CD1d(high) B lymphocytes in nonobese diabetic mice maps to diabetes susceptibility region Idd11. J. Immunol. 2005. 174: 4821-4827.
29. Attanavanich, K. and Kearney, J. F., Marginal zone, but not follicular B cells, are potent activators of naive CD4 T cells. J. Immunol. 2004. 172: 803-811.
30. Link, A., Zabel, F., Schnetzler, Y., Titz, A., Brombacher, F. and Bachmann, M. F., Innate immunity mediates follicular transport of particulate but not soluble protein antigen. J. Immunol. 2012. 188: 3724-3733.
31. Busconi, L., Bauer, J. W., Tumang, J. R., Laws, A., Perkins-Mesires, K., Tabor, A. S., Lau, C. et al., Functional outcome of B cell activation by chromatin immune complex engagement of the B cell receptor and TLR9. J. Immunol. 2007. 179: 7397-7405.
32. Barr, T. A., Brown, S., Ryan, G., Zhao, J. and Gray, D., TLR-mediated stimulation of APC: distinct cytokine responses of B cells and dendritic cells. Eur. J. Immunol. 2007. 37: 3040-3053.
33. Barr, T. A., Shen, P., Brown, S., Lampropoulou, V., Roch, T., Lawrie, S., Fan, B. et al., B cell depletion therapy ameliorates autoimmune disease through ablation of IL-6-producing B cells. J. Exp. Med. 209: 1001-1010.
34. Chen, X., Martin, F., Forbush, K. A., Perlmutter, R. M. and Kearney, J. F., Evidence for selection of a population of multi-reactive B cells into the splenic marginal zone. Int. Immunol. 1997. 9: 27-41.
35. Kanayama, N., Cascalho, M. and Ohmori, H., Analysis of marginal zone B cell development in the mouse with limited B cell diversity: role of the antigen receptor signals in the recruitment of B cells to the marginal zone. J. Immunol. 2005. 174: 1438-1445.
36. Nakayama, M., Castoe, T., Sosinowski, T., He, X., Johnson, K., Haskins, K., Vignali, D. A. et al., Germline TRAV5D-4 T-cell receptor sequence targets a primary insulin peptide of NOD mice. Diabetes 2012. 61: 857-865.
37. Abiru, N., Yu, L., Miao, D., Maniatis, A. K., Liu, E., Moriyama, H. and Eisenbarth, G. S., Transient insulin autoantibody expression independent of development of diabetes: comparison of NOD and NOR strains. J. Autoimmun. 2001. 17: 1-6.
38. Fu, W., Wojtkiewicz, G., Weissleder, R., Benoist, C. and Mathis, D., Early window of diabetes determinism in NOD mice, dependent on the complement receptor CRIg, identified by noninvasive imaging. Nat. Immunol. 2012. 13: 361-368.
39. Wang, G. J., Liu, Y., Qin, A., Shah, S. V., Deng, Z. B., Xiang, X., Cheng, Z. et al., Thymus exosomes-like particles induce regulatory T cells. J. Immunol. 2008. 181: 5242-5248.
40. Qazi, K. R., Gehrmann, U., Domange Jordo, E., Karlsson, M. C. and Gabrielsson, S., Antigen-loaded exosomes alone induce Th1-type memory through a B-cell-dependent mechanism. Blood 2009. 113: 2673-2683.
41. Vallhov, H., Gutzeit, C., Johansson, S. M., Nagy, N., Paul, M., Li, Q., Friend, S. et al., Exosomes containing glycoprotein 350 released by EBV-transformed B cells selectively target B cells through CD21 and block EBV infection in vitro. J. Immunol. 2011. 186: 73-82.
42. Chalmin, F., Ladoire, S., Mignot, G., Vincent, J., Bruchard, M., Remy-Martin, J. P., Boireau, W. et al., Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J. Clin. Invest. 2010. 120: 457-471.
43. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P. et al., Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008. 319: 1244-1247.
44. Shaw, P. X., Goodyear, C. S., Chang, M. K., Witztum, J. L. and Silverman, G. J., The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neo-antigens and apoptotic cells. J. Immunol. 2003. 170: 6151-6157.
45. Matyas, G. R., Wieczorek, L., Beck, Z., Ochsenbauer-Jambor, C., Kappes, J. C., Michael, N. L., Polonis V. R. et al., Neutralizing antibodies induced by liposomal HIV-1 glycoprotein 41 peptide simultaneously bind to both the 2F5 or 4E10 epitope and lipid epitopes. AIDS 2009. 23: 2069-2077.
46. Miyazaki, J., Araki, K., Yamato, E., Ikegami, H., Asano, T., Shibasaki, Y., Oka, Y. et al., Establishment of a pancreatic beta cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 1990. 127: 126-132.