Elevated IL-17 produced by TH17 cells promotes myeloma cell growth and inhibits immune function in multiple myeloma

Blood

Volumn 115, Issue 26, 2010, Pages 5385-5392

  Prabhala, Rao H ^a,b   Pelluru, Dheeraj ^a   Fulciniti, Mariateresa ^a   Prabhala, Harsha K ^c   Nanjappa, Puru ^a   Song, Weihua ^a   Pai, Christine ^a   Amin, Samir ^a   Tai, Yu Tzu ^a   Richardson, Paul G ^a   Ghobrial, Irene M ^a   Treon, Steven P ^a   Daley, John F ^a   Anderson, Kenneth C ^a,b   Kutok, Jeffery L ^b   Munshi, Nikhil C ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD ANALYSIS; BONE MARROW; BONE MARROW CELL; CANCER GROWTH; CANCER PATIENT; CELL ADHESION; CELL POLARITY; COLONY FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN TISSUE; IN VIVO STUDY; MALE; MOUSE; MULTIPLE MYELOMA; MYELOMA CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; STROMA CELL; TH1 CELL; TH17 CELL; TUMOR IMMUNITY; TUMOR XENOGRAFT; ANIMAL; CELL PROLIFERATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HELPER CELL; IMMUNOLOGY; MONONUCLEAR CELL; MOUSE MUTANT;

ANIMALS; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERLEUKIN-17; LEUKOCYTES, MONONUCLEAR; MALE; MICE; MICE, SCID; MULTIPLE MYELOMA; RECEPTORS, INTERLEUKIN-17; T-LYMPHOCYTES, HELPER-INDUCER; TH1 CELLS;

EID: 77955862810     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-10-246660     Document Type: Article

References (50)

1. Munshi NC. Immunoregulatory mechanisms in multiple myeloma. Hematol Oncol Clin North Am. 1997;11(1):51-69.
2. Raitakari M, Brown RD, Gibson J, Joshua DE. T cells in myeloma. Hematol Oncol. 2003;21(1):33-42.
3. Mariani S, Coscia M, Even J, et al. Severe and long-lasting disruption of T-cell receptor diversity in human myeloma after high-dose chemotherapy and autologous peripheral blood progenitor cell infusion. Br J Haematol. 2001;113(4):1051-1059. (Pubitemid 32634776)
4. Maecker B, Anderson KS, von Bergwelt-Baildon MS, et al. Viral antigen-specific CD8+ T-cell responses are impaired in multiple myeloma. Br J Haematol. 2003;121(6):842-848.
5. Moss P, Gillespie G, Frodsham P, Bell J, Reyburn H. Clonal populations of CD4+ and CD8+ T cells in patients with multiple myeloma and paraproteinemia. Blood. 1996;87(8):3297-3306. (Pubitemid 26115360)
6. Sze DM, Giesajtis G, Brown RD, et al. Clonal cytotoxic T cells are expanded in myeloma and reside in the CD8(+)CD57(+)CD28(-) compartment. Blood. 2001;98(9):2817-2827.
7. Hayashi T, Hideshima T, Akiyama M, et al. Ex vivo induction of multiple myeloma-specific cytotoxic T lymphocytes. Blood. 2003;102(4):1435-1442.
8. Massaia M, Bianchi A, Attisano C, et al. Detection of hyperreactive T cells in multiple myeloma by multivalent cross-linking of the CD3/TCR complex. Blood. 1991;78(7):1770-1780.
9. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986;136(7):2348-2357.
10. Mangan PR, Harrington LE, O'Quinn DB, et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature. 2006;441(7090):231-234.
11. Ivanov II, McKenzie BS, Zhou L, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell. 2006;126(6):1121-1133. (Pubitemid 44380299)
12. H17 and regulatory T cells. Nature. 2006;441(7090):235-238.
13. H17-cell-mediated autoimmunity to environmental toxins. Nature. 2008;453(7191):106-109.
14. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol. 2007;8(9):942-949.
15. Wilson NJ, Boniface K, Chan JR, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol. 2007;8(9):950-957.
16. Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity. 2004;21(2):241-254. (Pubitemid 39094053)
17. Zheng Y, Valdez PA, Danilenko DM, et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med. 2008;14(3):282-289.
18. Aujla SJ, Chan YR, Zheng M, et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med. 2008;14(3):275-281.
19. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity. 2005;22(3):285-294. (Pubitemid 40387471)
20. Michel ML, Mendes-da-Cruz D, Keller AC, et al. Critical role of ROR-gammat in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc Natl Acad Sci U S A. 2008;105(50):19845-19850.
21. Hymowitz SG, Filvaroff EH, Yin JP, et al. IL-17s adopt a cystine knot fold: structure and activity of a novel cytokine, IL-17F, and implications for receptor binding. EMBO J. 2001;20(19):5332-5341.
22. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity. 2004;21(4):467-476.
23. Yao Z, Fanslow WC, Seldin MF, et al. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity. 1995;3(6):811-821.
24. Fossiez F, Djossou O, Chomarat P, et al. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med. 1996;183(6):2593-2603.
25. Kao CY, Huang F, Chen Y, et al. Up-regulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-kappaB-dependent signaling pathway. J Immunol. 2005;175(10):6676-6685. (Pubitemid 41598911)
26. Khader SA, Bell GK, Pearl JE, et al. IL-23 and IL-17 in the establishment of protective pulmonary CD4 T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol. 2007;8(4):369-377.
27. Rifas L, Arackal S. T cells regulate the expression of matrix metalloproteinase in human osteoblasts via a dual mitogen-activated protein kinase mechanism. Arthritis Rheum. 2003;48(4):993-1001.
28. Chizzolini C, Chicheportiche R, Alvarez M, et al. Prostaglandin E2 synergistically with interleukin-23 favors human Th17 expansion. Blood. 2008;112(9):3696-3703.
29. Sonderegger I, Iezzi G, Maier R, Schmitz N, Kurrer M, Kopf M. GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. J Exp Med. 2008;205(10):2281-2294.
30. LeibundGut-Landmann S, Gross O, Robinson MJ, et al. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol. 2007;8(6):630-638.
31. van Beelen AJ, Zelinkova Z, Taanman-Kueter EW, et al. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells. Immunity. 2007;27(4):660-669. (Pubitemid 47615504)
32. Kano S, Sato K, Morishita Y, et al. The contribution of transcription factor IRF1 to the interferon-gamma-interleukin 12 signaling axis and TH1 versus TH-17 differentiation of CD4+ T cells. Nat Immunol. 2008;9(1):34-41.
33. de Beaucoudrey L, Puel A, Filipe-Santos O, et al. Mutations in STAT3 and IL12RB1 impair the development of human IL-17-producing T cells. J Exp Med. 2008;205(7):1543-1550.
34. Chen Z, Laurence A, Kanno Y, et al. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci U S A. 2006;103(21):8137-8142. (Pubitemid 43801065)
35. Hideshima T, Mitsiades C, Tonon G, Richardson PG, Anderson KC. Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets. Nat Rev Cancer. 2007;7(8):585-598.
36. Brown LM, Gridley G, Check D, Landgren O. Risk of multiple myeloma and monoclonal gammopathy of undetermined significance among white and black male United States veterans with prior autoimmune, infectious, inflammatory, and allergic disorders. Blood. 2008;111(7):3388-3394.
37. Tai YT, Podar K, Catley L, et al. Insulin-like growth factor-1 induces adhesion and migration in human multiple myeloma cells via activation of beta1-integrin and phosphatidylinositol 3′-kinase/AKT signaling. Cancer Res. 2003;63(18):5850-5858. (Pubitemid 37187484)
38. Ikeda H, Hideshima T, Fulciniti M, et al. The monoclonal antibody nBT062 conjugated to cytotoxic Maytansinoids has selective cytotoxicity against CD138-positive multiple myeloma cells in vitro and in vivo. Clin Cancer Res. 2009;15(12):4028-4037.
39. Annunziato F, Cosmi L, Liotta F, Maggi E, Romagnani S. Type 17 T helper cells-origins, features and possible roles in rheumatic disease. Nat Rev Rheumatol. 2009;5(6):325-331.
40. Pernis AB. Th17 cells in rheumatoid arthritis and systemic lupus erythematosus. J Intern Med. 2009;265(6):644-652.
41. Munshi NC, Mitsiades CS, Richardson PG, Anderson KC. Does maintenance therapy with thalidomide benefit patients with multiple myeloma? Nat Clin Pract Oncol. 2007;4(7):394-395. (Pubitemid 47039687)
42. Dhodapkar KM, Barbuto S, Matthews P, et al. Dendritic cells mediate the induction of polyfunctional human IL17-producing cells (Th17-1 cells) enriched in the bone marrow of patients with myeloma. Blood. 2008;112(7):2878-2885.
43. Miyahara Y, Odunsi K, Chen W, Peng G, Matsuzaki J, Wang RF. Generation and regulation of human CD4 IL-17-producing T cells in ovarian cancer. Proc Natl Acad Sci U S A. 2008;105(40):15505-15510.
44. Kottke T, Sanchez-Perez L, Diaz RM, et al. Induction of hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer. Cancer Res. 2007;67(24):11970-11979.
45. Martin-Orozco N, Muranski P, Chung Y, et al. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity. 2009;31(5):787-98.
46. Kryczek I, Banerjee M, Cheng P, et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood. 2009;114(6):1141-9.
47. Alexandrakis MG, Pappa CA, Miyakis S, et al. Serum interleukin-17 and its relationship to angiogenic factors in multiple myeloma. Eur J Intern Med. 2006;17(6):412-416. (Pubitemid 44572138)
48. Oteri G, Allegra A, Bellomo G, et al. Reduced serum levels of Interleukin 17 in patients with osteonecrosis of the jaw and in multiple myeloma subjects after bis-phosphonates administration. Cytokine. 2008;43(2):103-104.
49. Langowski JL, Zhang X, Wu L, et al. IL-23 promotes tumor incidence and growth. Nature. 2006;442(7101):461-465. (Pubitemid 44264796)
50. Brenne AT, Ro TB, Waage A, Sundan A, Borset M, Hjorth-Hansen H. Interleukin-21 is a growth and survival factor for human myeloma cells. Blood. 2002;99(10):3756-3762.