Myeloid-derived suppressor cells promote B-cell production of IgA in a TNFR2-dependent manner

Cellular and Molecular Immunology

Volumn 14, Issue 7, 2017, Pages 597-606

  Xu, Xia ^a   Meng, Qinghong ^a   Erben, Ulrike ^b   Wang, Peigang ^a   Glauben, Rainer ^b   Kühl, Anja A ^b   Wu, Hao ^a   Ma, Chung Wah ^c   Hu, Minghua ^c   Wang, Yuanyuan ^c   Sun, Wei ^d   Jia, Junying ^a   Wu, Xinyi ^a   Chen, Wei ^d   Siegmund, Britta ^b   Qin, Zhihai ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c Infinitus Chinese Herbal Immunity Research Centre   (China)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

B cells; IgA; MDSCs; TNFR2

Indexed keywords

IMMUNOGLOBULIN A; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN ANTIBODY REACTION; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CELL CONTACT; COCULTURE; CONTROLLED STUDY; FEMALE; GERMINAL CENTER; IMMUNOREGULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID-DERIVED SUPPRESSOR CELL; NONHUMAN; PLASMA CELL; SPLEEN; TUMOR GROWTH; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL PROLIFERATION; LYMPHOCYTE ACTIVATION; METABOLISM;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CELL PROLIFERATION; IMMUNOGLOBULIN A; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; MICE, INBRED C57BL; MYELOID-DERIVED SUPPRESSOR CELLS; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; SPLEEN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 85021834703     PISSN: 16727681     EISSN: None     Source Type: Journal    
DOI: 10.1038/cmi.2015.103     Document Type: Article

References (51)

1. Youn JI, Gabrilovich DI. The biology of myeloid-derived suppressor cells: The blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 2010; 40: 2969-2975.
2. Jiang J, Wang Z, Li Z, Zhang J, Wang C, Xu X, et al. Early exposure of high-dose interleukin-4 to tumor stroma reverses myeloid cell-mediated T-cell suppression. Gene Ther 2010; 17: 991-999.
3. Zhao X, Rong L, Zhao X, Li X, Liu X, Deng J, et al. TNF signaling drives myeloid-derived suppressor cell accumulation. J Clin Invest 2012; 122: 4094-4104.
4. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9: 162-174.
5. Monach PA, Schreiber H, Rowley DA. CD4+ and B lymphocytes in transplantation immunity. II. Augmented rejection of tumor allografts by mice lacking B cells. Transplantation 1993; 55: 1356-1361.
6. Schultz KR, Klarnet JP, Gieni RS, HayGlass KT, Greenberg PD. The role of B cells for in vivo T cell responses to a Friend virus-induced leukemia. Science 1990; 249: 921-923.
7. Qin Z, Richter G, Schuler T, Ibe S, Cao X, Blankenstein T. B cells inhibit induction of T cell-dependent tumor immunity. Nat Med 1998; 4: 627-630.
8. de Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 2006; 6: 24-37.
9. Pabst O. New concepts in the generation and functions of IgA. Nat Rev Immunol 2012; 12: 821-832.
10. Woof JM, Kerr MA. The function of immunoglobulin A in immunity. J Pathol 2006; 208: 270-282.
11. 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.
12. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454: 436-444.
13. Fiers W. Tumor necrosis factor. Characterization at the molecular, cellular and in vivo level. FEBS Lett 1991; 285: 199-212.
14. Grell M, Douni E, Wajant H, Lohden M, Clauss M, Maxeiner B, et al. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor. Cell 1995; 83: 793-802.
15. Hu X, Li B, Li X, Zhao X, Wan L, Lin G, et al. Transmembrane TNFalpha promotes suppressive activities of myeloid-derived suppressor cells via TNFR2. J Immunol 2014; 192: 1320-1331.
16. Shalapour S, Font-Burgada J, Di Caro G, Zhong Z, Sanchez-Lopez E, Dhar D, et al. Immunosuppressive plasma cells impede T-cell-dependent immunogenic chemotherapy. Nature 2015; 521: 94-98.
17. Shu SY, Rosenberg SA. Adoptive immunotherapy of newly induced murine sarcomas. Cancer Res 1985; 45: 1657-1662.
18. Kusmartsev S, Cheng F, Yu B, Nefedova Y, Sotomayor E, Lush R, et al. All-trans-retinoic acid eliminates immature myeloid cells from tumorbearing mice and improves the effect of vaccination. Cancer Res 2003; 63: 4441-4449.
19. Nefedova Y, Fishman M, Sherman S, Wang X, Beg AA, Gabrilovich DI. Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells. Cancer Res 2007; 67: 11021-11028.
20. Kamata T, Nogaki F, Fagarasan S, Sakiyama T, Kobayashi I, Miyawaki S, et al. Increased frequency of surface IgA-positive plasma cells in the intestinal lamina propria and decreased IgA excretion in hyper IgA (HIGA) mice, a murine model of IgA nephropathy with hyperserum IgA. J Immunol 2000; 165: 1387-1394.
21. Wang W, Li Q, Zhang J, Wu H, Yin Y, Ge Q, et al. Hemokinin-1 activates the MAPK pathway and enhances B cell proliferation and antibody production. J Immunol 2010; 184: 3590-3597.
22. Defrance T, Vanbervliet B, Briere F, Durand I, Rousset F, Banchereau J. Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J Exp Med 1992; 175: 671-682.
23. Crook KR, Jin M, Weeks MF, Rampersad RR, Baldi RM, Glekas AS, et al. Myeloid-derived suppressor cells regulate T cell and B cell responses during autoimmune disease. J Leukoc Biol 2015; 97: 573-582.
24. Green KA, Cook WJ, Green WR. Myeloid-derived suppressor cells in murine retrovirus-induced AIDS inhibit T-A nd B-cell responses in vitro that are used to define the immunodeficiency. J Virol 2013; 87: 2058-2071.
25. Jordan MB, Mills DM, Kappler J, Marrack P, Cambier JC. Promotion of B cell immune responses via an alum-induced myeloid cell population. Science 2004; 304: 1808-1810.
26. Zhang X. Regulatory functions of innate-like B cells. Cell Mol Immunol 2013; 10: 113-121.
27. Kaminski DA, Stavnezer J. Enhanced IgA class switching in marginal zone and B1 B cells relative to follicular/B2 B cells. J Immunol 2006; 177: 6025-6029.
28. Baumgarth N. The double life of a B-1 cell: Self-reactivity selects for protective effector functions. Nat Rev Immunol 2011; 11: 34-46.
29. Rosado MM, Aranburu A, Capolunghi F, Giorda E, Cascioli S, Cenci F, et al. From the fetal liver to spleen and gut: The highway to natural antibody. Mucosal Immunol 2009; 2: 351-361.
30. Cerutti A, Rescigno M. The biology of intestinal immunoglobulin A responses. Immunity 2008; 28: 740-750.
31. Ho HC, Ng MH, Kwan HC. Factors affecting serum IgA antibody to Epstein-Barr viral capsid antigens in nasopharyngeal carcinoma. Br J Cancer 1978; 37: 356-362.
32. Kosunen TU, Seppala K, Sarna S, Aromaa A, Knekt P, Virtamo J, et al. Association of Helicobacter pylori IgA antibodies with the risk of peptic ulcer disease and gastric cancer. World J Gastroenterol 2005; 11: 6871-6874.
33. Deture FA, Deardourff SL, Kaufman HE, Centifanto YM. A comparison of serum immunoglobulins from patients with nonneoplastic prostates and prostatic carcinoma. J Urol 1978; 120: 435-437.
34. Baseler MW, Maxim PE, Veltri RW. Circulating IgA immune complexes in head and neck cancer, nasopharyngeal carcinoma, lung cancer, colon cancer. Cancer 1987; 59: 1727-1731.
35. Ludvigsson JF, Neovius M, Hammarstrom L. Association between IgA deficiency & other autoimmune conditions: A population-based matched cohort study. J Clin Immunol 2014; 34: 444-451.
36. DiLillo DJ, Yanaba K, Tedder TF. B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: Therapeutic B cell depletion enhances B16 melanoma growth in mice. J Immunol 2010; 184: 4006-4016.
37. Kumashiro R, Shiraishi M, Sugimachi K, Hiramoto Y, Tamada R, Okamura T, et al. Bidirectional effects of splenectomy on the growth of syngeneic tumor in mice. Jpn J Surg 1984; 14: 167-173.
38. Palladino MA, Bahjat FR, Theodorakis EA, Moldawer LL. Anti-TNFalpha therapies: The next generation. Nat Rev Drug Discov 2003; 2: 736-746.
39. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, dendritic cells. Science 2010; 327: 656-661.
40. Naude PJ, den Boer JA, Luiten PG, Eisel UL. Tumor necrosis factor receptor cross-talk. FEBS J 2011; 278: 888-898.
41. Pasparakis M, Alexopoulou L, Episkopou V, Kollias G. Immune and inflammatory responses in TNF alpha-deficient mice: A critical requirement for TNF alpha in the formation of primary B cell follicles, follicular dendritic cell networks and germinal centers, in the maturation of the humoral immune response. J Exp Med 1996; 184: 1397-1411.
42. Tumanov AV, Grivennikov SI, Kruglov AA, Shebzukhov YV, Koroleva EP, Piao Y, et al. Cellular source and molecular form of TNF specify its distinct functions in organization of secondary lymphoid organs. Blood 2010; 116: 3456-3464.
43. Ruuls SR, Hoek RM, Ngo VN, McNeil T, Lucian LA, Janatpour MJ, et al. Membrane-bound TNF supports secondary lymphoid organ structure but is subservient to secreted TNF in driving autoimmune inflammation. Immunity 2001; 15: 533-543.
44. Eissner G, Kolch W, Scheurich P. Ligands working as receptors: Reverse signaling by members of the TNF superfamily enhance the plasticity of the immune system. Cytokine Growth Factor Rev 2004; 15: 353-366.
45. Horiuchi T, Mitoma H, Harashima S, Tsukamoto H, Shimoda T. Transmembrane TNF-alpha: Structure, function and interaction with anti-TNF agents. Rheumatology (Oxford) 2010; 49: 1215-1228.
46. Qin Z, Kruger-Krasagakes S, Kunzendorf U, Hock H, Diamantstein T, Blankenstein T. Expression of tumor necrosis factor by different tumor cell lines results either in tumor suppression or augmented metastasis. J Exp Med 1993; 178: 355-360.
47. Zhao X, Mohaupt M, Jiang J, Liu S, Li B, Qin Z. Tumor necrosis factor receptor 2-mediated tumor suppression is nitric oxide dependent and involves angiostasis. Cancer Res 2007; 67: 4443-4450.
48. Moore RJ, Owens DM, Stamp G, Arnott C, Burke F, East N, et al. Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med 1999; 5: 828-831.
49. Scott KA, Moore RJ, Arnott CH, East N, Thompson RG, Scallon BJ, et al. An anti-tumor necrosis factor-alpha antibody inhibits the development of experimental skin tumors. Mol Cancer Ther 2003; 2: 445-451.
50. Harrison ML, Obermueller E, Maisey NR, Hoare S, Edmonds K, Li NF, et al. Tumor necrosis factor alpha as a new target for renal cell carcinoma: Two sequential phase II trials of infliximab at standard and high dose. J Clin Oncol 2007; 25: 4542-4549.
51. Rosenblum H, Amital H. Anti-TNF therapy: Safety aspects of taking the risk. Autoimmun Rev 2011; 10: 563-568.