A new paradigm for an old story: The role of regulatory B cells in cancer

Frontiers in Immunology

Volumn 3, Issue JUL, 2012, Pages

  Biragyn, Arya ^a   Lee Chang, Catalina ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84871947021     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00206     Document Type: Article

References (59)

1. Aklilu, M., Stadler, W. M., Markiewicz, M., Vogelzang, N. J., Mahowald, M., Johnson, M., and Gajewski, T. F. (2004). Depletion of normal B cells with rituximab as an adjunct to IL-2 therapy for renal cell carcinoma and melanoma. Ann. Oncol. 15, 1109-1114.
2. Ammirante, M., Luo, J. L., Grivennikov, S., Nedospasov, S., and Karin, M. (2010). B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 464, 302-305.
3. Balabanian, K., Foussat, A., Bouchet-Delbos, L., Couderc, J., Krzysiek, R., Amara, A., Baleux, F., Portier, A., Galanaud, P., and Emilie, D. (2002). Interleukin-10 modulates the sensitivity of peritoneal B lymphocytes to chemokines with opposite effects on stromal cell-derived factor-1 and B-lymphocyte chemoattractant. Blood 99, 427-436.
4. Blair, P. A., Norena, L. Y., Flores-Borja, F., Rawlings, D. J., Isenberg, D. A., Ehrenstein, M. R., and Mauri, C. (2010). CD19(+) CD24(hi) CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic Lupus Erythematosus patients. Immunity 32, 129-140.
5. Bouaziz, J. D., Yanaba, K., Venturi, G. M., Wang, Y., Tisch, R. M., Poe, J. C., and Tedder, T. F. (2007). Therapeutic B cell depletion impairs adaptive and autoreactive CD4+ T cell activation in mice. Proc. Natl. Acad. Sci. U.S.A. 104, 20878-20883.
6. Brodt, P., and Gordon, J. (1978). Anti-tumor immunity in B lymphocyte-deprived mice. I. Immunity to a chemically induced tumor. J. Immunol. 121, 359-362.
7. Brodt, P., and Gordon, J. (1982). Natural resistance mechanisms may play a role in protection against chemical carcinogenesis. Cancer Immunol. Immunother. 13, 125-127.
8. Brummel, R., and Lenert, P. (2005). Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J. Immunol. 174, 2429-2434.
9. Byrne, S. N., and Halliday, G. M. (2005). B cells activated in lymph nodes in response to ultraviolet irradiation or by interleukin-10 inhibit dendritic cell induction of immunity. J. Invest. Dermatol. 124, 570-578.
10. Candolfi, M., Curtin, J. F., Yagiz, K., Assi, H., Wibowo, M. K., Alzadeh, G. E., Foulad, D., Muhammad, A. K., Salehi, S., Keech, N., Puntel, M., Liu, C., Sanderson, N. R., Kroeger, K. M., Dunn, R., Martins, G., Lowenstein, P. R., and Castro, M. G. (2011). B cells are critical to T-cell-mediated antitumor immunity induced by a combined immune-stimulatory/conditionally cytotoxic therapy for glioblastoma. Neoplasia 13, 947-960.
11. Dass, S., Vital, E. M., and Emery, P. (2007). Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum. 56, 2715-2718.
12. de Visser, K. E., Korets, L. V., and Coussens, L. M. (2005). De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7, 411-423.
13. Ding, Q., Yeung, M., Camirand, G., Zeng, Q., Akiba, H., Yagita, H., Chalasani, G., Sayegh, M. H., Najafian, N., and Rothstein, D. M. (2011). Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J. Clin. Invest. 121, 3645-3656.
14. Evans, J. G., Chavez-Rueda, K. A., Eddaoudi, A., Meyer-Bahlburg, A., Rawlings, D. J., Ehrenstein, M. R., and Mauri, C. (2007). Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. 178, 7868-7878.
15. Fommer, F., Heinen, T. J., Wunderlich, F. T., Yogev, N., Buch, T., Roers, A., Bettelli, E., Müller, W., Anderton, S. M., and Waisman, A. (2008). Tolerance without clonal expansion: self-antigen-expressing B cells program self-reactive T cells for future deletion. J. Immunol. 181, 5748-5759.
16. Fuchs, E. J., and Matzinger, P. (1992). B cells turn off virgin but not memory T cells. Science 258, 1156-1159.
17. Gary-Gouy, H., Harriague, J., Bismuth, G., Platzer, C., Schmitt, C., and Dalloul, A. H. (2002). Human CD5 promotes B-cell survival through stimulation of autocrine IL-10 production. Blood 100, 4537-4543.
18. Goetz, M., Atreya, R., Ghalibafian, M., Galle, P. R., and Neurath, M. F. (2007). Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm. Bowel Dis. 13, 1365-1368.
19. Gray, M., Miles, K., Salter, D., Gray, D., and Savill, J. (2007). Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc. Natl. Acad. Sci. U.S.A. 104, 14080-14085.
20. Horikawa, M., Minard-Colin, V., Matsushita, T., and Tedder, T. F. (2011). Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice. J. Clin. Invest. 121, 4268-4280.
21. Hussain, S., and Delovitch, T. L. (2007). Intravenous transfusion of BCR-activated B cells protects NOD mice from type 1 diabetes in an IL-10-dependent manner. J. Immunol. 179, 7225-7232.
22. Inoue, S., Leitner, W. W., Golding, B., and Scott, D. (2006). Inhibitory effects of B cells on antitumor immunity. Cancer Res. 66, 7741-7747.
23. Iwata, Y., Matsushita, T., Horikawa, M., Dilillo, D. J., Yanaba, K., Venturi, G. M., Szabolcs, P. M., Bernstein, S. H., Magro, C. M., Williams, A. D., Hall, R. P., St Clair, E. W., and Tedder, T. F. (2011). Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117, 530-541.
24. Kessel, A., Haj, T., Peri, R., Snir, A., Melamed, D., Sabo, E., and Toubi, E. (2012). Human CD19(+) CD25(high) B regulatory cells suppress proliferation of CD4(+) T cells and enhance Foxp3 and CTLA-4 expression in T-regulatory cells. Autoimmun. Rev. 11, 670-677.
25. Lampropoulou, V., Hoehlig, K., Roch, T., Neves, P., Calderon Gomez, E., Sweenie, C. H., Hao, Y., Freitas, A. A., Steinhoff, U., Anderton, S. M., and Fillatreau, S. (2008). TLR-activated B cells suppress T cell-mediated autoimmunity. J. Immunol. 180, 4763-4773.
26. Lanzavecchia, A. (1985). Antigen-specific interaction between T and B cells. Nature 314, 537-539.
27. Lenert, P., Brummel, R., Field, E. H., and Ashman, R. F. (2005). TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J. Clin. Immunol. 25, 29-40.
28. Matsushita, T., Yanaba, K., Bouaziz, J. D., Fujimoto, M., and Tedder, T. F. (2008). Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118, 3420-3430.
29. Mielke, F., Schneider-Obermeyer, J., and Dorner, T. (2008). Onset of psoriasis with psoriatic arthropathy during rituximab treatment of non-Hodgkin lymphoma. Ann. Rheum. Dis. 67, 1056-1057.
30. Mizoguchi, A., Mizoguchi, E., Smith, R. N., Preffer, F. I., and Bhan, A. K. (1997). Suppressive role of B cells in chronic colitis of T cell receptor alpha mutant mice. J. Exp. Med. 186, 1749-1756.
31. Mizoguchi, A., Mizoguchi, E., Takedatsu, H., Blumberg, R. S., and Bhan, A. K. (2002). Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16, 219-230.
32. Monach, P. A., Schreiber, H., and Rowley, D. A. (1993). CD4+ and B lymphocytes in transplantation immunity. II. Augmented rejection of tumor allografts by mice lacking B cells. Transplantation 55, 1356-1361.
33. Morris, A., and Moller, G. (1968). Regulation of cellular antibody synthesis effect of adoptively transferred antibody-producing spleen cells on cellular antibody synthesis. J. Immunol. 101, 439-445.
34. Newell, K. A., Asare, A., Kirk, A. D., Gisler, T. D., Bourcier, K., Suthanthiran, M., Burlingham, W. J., Marks, W. H., Sanz, I., Lechler, R. I., Hernandez-Fuentes, M. P., Turka, L. A., Seyfert-Margolis, V. L., and Immune Tolerance Network ST507 Study Group. (2010). Identification of a B cell signature associated with renal transplant tolerance in humans. J. Clin. Invest. 120, 1836-1847.
35. O'Garra, A., and Howard, M. (1992). Cytokines and Ly-1 (B1) B cells. Int. Rev. Immunol. 8, 219-234.
36. Olkhanud, P. B., Baatar, D., Bodogai, M., Hakim, F., Gress, R., Anderson, R. L., Deng, J., Xu, M., Briest, S., and Biragyn, A. (2009). Breast cancer lung metastasis requires expression of chemokine receptor CCR4 and regulatory T cells. Cancer Res. 69, 5996-6004.
37. Olkhanud, P. B., Damdinsuren, B., Bodogai, M., Gress, R. E., Sen, R., Wejksza, K., Malchinkhuu, E., Wersto, R. P., and Biragyn, A. (2011). Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4 T cells to T-regulatory cells. Cancer Res. 71, 3505-3515.
38. Pallier, A., Hillion, S., Danger, R., Giral, M., Racape, M., Degauque, N., Dugast, E., Ashton-Chess, J., Pettré, S., Lozano, J. J., Bataille, R., Devys, A., Cesbron-Gautier, A., Braudeau, C., Larrose, C., Soulillou, J. P., and Brouard, S. (2010). Patients with drug-free long-term graft function display increased numbers of peripheral B cells with a memory and inhibitory phenotype. Kidney Int. 78, 503-513.
39. Parekh, V. V., Prasad, D. V., Banerjee, P. P., Joshi, B. N., Kumar, A., and Mishra, G. C. (2003). B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGF-beta 1. J. Immunol. 170, 5897-5911.
40. Pretscher, D., Distel, L. V., Grabenbauer, G. G., Wittlinger, M., Buettner, M., and Niedobitek, G. (2009). Distribution of immune cells in head and neck cancer: CD8+ T-cells and CD20+ B-cells in metastatic lymph nodes are associated with favourable outcome in patients with oro- and hypopharyngeal carcinoma. BMC Cancer 9, 292. doi: 10.1186/1471-2407-9-292
41. Qin, Z., Richter, G., Schuler, T., Ibe, S., Cao, X., and Blankenstein, T. (1998). B cells inhibit induction of T cell-dependent tumor immunity. Nat. Med. 4, 627-630.
42. Ravetch, J. V., and Bolland, S. (2001). IgG Fc receptors. Annu. Rev. Immunol. 19, 275-290.
43. Reichardt, P., Dornbach, B., Rong, S., Beissert, S., Gueler, F., Loser, K., and Gunzer, M. (2007). Naive B cells generate regulatory T cells in the presence of a mature immunologic synapse. Blood 110, 1519-1529.
44. Rowley, D. A., and Stach, R. M. (1998). B lymphocytes secreting IgG linked to latent transforming growth factor-beta prevent primary cytolytic T lymphocyte responses. Int. Immunol. 10, 355-363.
45. Sagoo, P., Perucha, E., Sawitzki, B., Tomiuk, S., Stephens, D. A., Miqueu, P., Chapman, S., Craciun, L., Sergeant, R., Brouard, S., Rovis, F., Jimenez, E., Ballow, A., Giral, M., Rebollo-Mesa, I., Le Moine, A., Braudeau, C., Hilton, R., Gerstmayer, B., Bourcier, K., Sharif, A., Krajewska, M., Lord, G. M., Roberts, I., Goldman, M., Wood, K. J., Newell, K., Seyfert-Margolis, V., Warrens, A. N., Janssen, U., Volk, H. D., Soulillou, J. P., Hernandez-Fuentes, M. P., and Lechler, R. I. (2010). Development of a cross-platform biomarker signature to detect renal transplant tolerance in humans. J. Clin. Invest. 120, 1848-1861.
46. Sayi, A., Kohler, E., Toller, I. M., Flavell, R. A., Muller, W., Roers, A., and Müller, A. (2011). TLR-2-activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J. Immunol. 186, 878-890.
47. Scapini, P., Lamagna, C., Hu, Y., Lee, K., Tang, Q., Defranco, A. L., and Lowell, C. A. (2011). B cell-derived IL-10 suppresses inflammatory disease in Lyn-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 108, E823-E832.
48. Schioppa, T., Moore, R., Thompson, R. G., Rosser, E. C., Kulbe, H., Nedospasov, S., Mauri, C., Coussens, L. M., and Balkwill, F. R. (2011). B regulatory cells and the tumor-promoting actions of TNF-alpha during squamous carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 108, 10662-10667.
49. Shimamura, T., Hashimoto, K., and Sasaki, S. (1982). Feedback suppression of the immune response in vivo. I. Immune B cells induce antigen-specific suppressor T cells. Cell. Immunol. 68, 104-113.
50. Sorrentino, R., Morello, S., Forte, G., Montinaro, A., de Vita, G., Luciano, A., Palma, G., Arra, C., Maiolino, P., Adcock, I. M., and Pinto, A. (2011). B cells contribute to the antitumor activity of CpG-oligodeoxynucleotide in a mouse model of metastatic lung carcinoma. Am. J. Respir. Crit. Care Med. 183, 1369-1379.
51. Stach, R. M., and Rowley, D. A. (1993). A first or dominant immunization. II. Induced immunoglobulin carries transforming growth factor beta and suppresses cytolytic T cell responses to unrelated alloantigens. J. Exp. Med. 178, 841-852.
52. Sun, J. B., Flach, C. F., Czerkinsky, C., and Holmgren, J. (2008). B lymphocytes promote expansion of regulatory T cells in oral tolerance: powerful induction by antigen coupled to cholera toxin B subunit. J. Immunol. 181, 8278-8287.
53. Townsend, M. J., Monroe, J. G., and Chan, A. C. (2010). B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol. Rev. 237, 264-283.
54. Tretter, T., Venigalla, R. K., Eckstein, V., Saffrich, R., Sertel, S., Ho, A. D., and Lorenz, H. M. (2008). Induction of CD4+ T-cell anergy and apoptosis by activated human B cells. Blood 112, 4555-4564.
55. Watt, V., Ronchese, F., and Ritchie, D. (2007). Resting B cells suppress tumor immunity via an MHC class-II dependent mechanism. J. Immunother. 30, 323-332.
56. Wolf, S. D., Dittel, B. N., Hardardottir, F., and Janeway, C. A. Jr. (1996). Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J. Exp. Med. 184, 2271-2278.
57. Yanaba, K., Bouaziz, J. D., Haas, K. M., Poe, J. C., Fujimoto, M., and Tedder, T. F. (2008). A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28, 639-650.
58. Zuniga, E., Rabinovich, G. A., Iglesias, M. M., and Gruppi, A. (2001). Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis. J. Leukoc. Biol. 70, 73-79.
59. Zusman, T., Lisansky, E., Arons, E., Anavi, R., Bonnerot, C., Sautes, C., Fridman, W. H., Witz, I. P., and Ran, M. (1996). Contribution of the intracellular domain of murine Fc-gamma receptor type IIB1 to its tumor-enhancing potential. Int. J. Cancer 68, 219-227.