Dendritic cells mediate the induction of polyfunctional human IL17-producing cells (Th17-1 cells) enriched in the bone marrow of patients with myeloma

Blood

Volumn 112, Issue 7, 2008, Pages 2878-2885

  Dhodapkar, Kavita M ^a   Barbuto, Scott ^a   Matthews, Phillip ^a   Kukreja, Anjli ^a   Mazumder, Amitabha ^b   Vesole, David ^b   Jagannath, Sundar ^b   Dhodapkar, Madhav V ^a,c,d  

^a ROCKEFELLER UNIVERSITY   (United States)

^b ST VINCENT S COMPREHENSIVE CANCER CENTER   (United States)

^c YALE UNIVERSITY   (United States)

^d YALE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; EPITOPE;

ADULT; AGED; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL EXPANSION; CELL INFILTRATION; CELL MATURATION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; GAMMOPATHY; HUMAN; HUMAN CELL; MALE; MONOCLONAL IMMUNOGLOBULINEMIA; MONOCYTE; MYELOMA; PHENOTYPE; PRIORITY JOURNAL; TH17 CELL; BIOSYNTHESIS; BONE MARROW; CELL PROLIFERATION; CELL SEPARATION; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MIDDLE AGED; MULTIPLE MYELOMA; PATHOLOGY; TUMOR CELL LINE;

AGED; APOPTOSIS; BONE MARROW; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SEPARATION; DENDRITIC CELLS; EPITOPES; FEMALE; HUMANS; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MONOCYTES; MULTIPLE MYELOMA; PHENOTYPE; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 53449089919     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-03-143222     Document Type: Article

References (68)

1. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature. 2007;449:419-426.
2. Gutcher I, Becher B. APC-derived cytokines and Tcell polarization in autoimmune inflammation. J Clin Invest. 2007;117:1119-1127.
3. Chen Z, O'Shea JJ. Th17 cells: a new fate for differentiating helperTcells. Immunol Res. 2008;41: 87-102.
4. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med. 2007; 13: 139-145.
5. Cua DJ, Sherlock J, Chen Y, et al. lnterleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 2003;421:744-748.
6. Yen D, Cheung J, Scheerens H, et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17and IL-6. J Clin Invest. 2006;116:1310-1316.
7. Cho ML, Kang JW, Moon YM, et al. STAT3 and NF-kappaB signal pathway is required for IL-23-mediated IL-17 production in spontaneous arthritis animal model IL-1 receptor antagonist-deficient mice. J Immunol. 2006;176:5652-5661.
8. Nakae S, Saijo S, Horai R, Sudo K, Mori S, Iwakura Y. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci U S A. 2003; 100:5986-5990.
9. Komiyama Y, Nakae S, Matsuki T, et al. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol. 2006;177:566-573.
10. Nakae S, Nambu A, Sudo K, Iwakura Y. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol. 2003; 171:6173-6177.
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;126:1121-1133.
12. Laurence A, Tato CM, Davidson TS, et al. lnterleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity. 2007;26:371-381.
13. Yang XO, Panopoulos AD, Nurieva R, et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem. 2007; 282:9358-9363.
14. Mathur AN, Chang HC, Zisoulis DG, et al. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J Immunol. 2007;178:4901-4907.
15. Nurieva R, Yang XO, Martinez G, et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature. 2007;448:480-483.
16. Korn T, Bettelli E, Gao W, et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature. 2007;448:484-487.
17. Zhou L, Ivanov II, Spolski R, et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol. 2007;8:967-974.
18. Laurence A. O'Shea JJ. TH-17 differentiation: of mice and men. Nature Immunology. 2007;8:903-905.
19. Chen Z, Tato CM, Muul L, Laurence A, O'Shea JJ. Distinct regulation of interleukin-17 in human T helper lymphocytes. Arthritis Rheum. 2007;56: 2936-2946.
20. Acosta-Rodriguez EV, Napolitani G, LanzavecchiaA, Sallusto F. Interleukins 1 beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol. 2007;8:942-949.
21. Acosta-Rodriguez EV, Rivino L, Geginat J, et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol. 2007;8:639-646.
22. Evans HG, Suddason T, Jackson I, Taams LS, Lord GM. Optimal induction of T helper 17 cells in humans requires T cell receptor ligation in the context of Toll-like receptor-activated monocytes. Proc Natl Acad Sci U S A. 2007;104:17034-17039.
23. Annunziato F, Cosmi L, Santarlasci V, et al. Phenotypic and functional features of human Th17 cells. J Exp Med. 2007;204:1849-1861.
24. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol. 2007;25:821-852.
25. Amadi-Obi A, Yu CR, Liu X, et al. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat Med. 2007;13:711-718.
26. 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;27:660-669.
27. Chen X, Vodanovic-Jankovic S, Johnson B, Keller M, Komorowski R, Drobyski WR. Absence of regulatory T-cell control of TH1 and TH17 cells is responsible for the autoimmune-mediated pathology in chronic graft-versus-host disease. Blood. 2007;110:3804-3813.
28. Kryczek I, Wei S, Vatan L, et al. Cutting edge: opposite effects of IL-1 and IL-2 on the regulation of IL-17+ Tcell pool IL-1 subverts IL-2-mediated suppression. J Immunol. 2007;179:1423-1426.
29. Kryczek I, Wei S, Zou L, et al. Cutting edge: Th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment. J Immunol. 2007;178:6730-6733.
30. Leibundgut-Landmann S, Gross O, Robinson MJ, et al. Syk- and GARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol. 2007;8: 630-638.
31. Bailey SL, Schreiner B, McMahon EJ, Miller SD. CNS myeloid DCs presenting endogenous myelin peptides 'preferentially' polarize CD4+ T(H)-17 cells in relapsing EAE. Nat Immunol. 2007;8:172-180.
32. Dhodapkar KM, Krasovsky J, Williamson B, Dhodapkar MV. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J Exp Med. 2002;195:125-133.
33. Dhodapkar MV, Krasovsky J, Olson K. T cells from the tumor microenvironment of patients with progressive myeloma can generate strong, tumor-specific cytolytic responses to autologous, tumor-loaded dendritic cells. Proc Natl Acad Sci U S A. 2002;99:13009-13013.
34. Banerjee D, Dhodapkar MV, Matayeva E, Steinman RM, Dhodapkar K. Expansion of FOXP3high regulatory T cells by human dendritic cells (DCs) in vitro and after DC injection of cytokine matured DCs in myeloma patients. Blood. 2006;108:2655-2661.
35. Dhodapkar KM, Banerjee D, Connolly J, et al. Selective blockade of the inhibitory Fc{gamma} receptor (Fc{gamma}RIIB) in human dendritic cells and monocytes induces a type I interferon response program. J Exp Med. 2007;204:1359-1369.
36. Ehrlich LA, Roodman GD. The role of immune cells and inflammatory cytokines in Paget's disease and multiple myeloma. Immunol Rev. 2005; 208:252-266.
37. Dhodapkar KM, Kaufman JL, Ehlers M, et al. Selective blockade of inhibitory Fc gamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibodycoated tumor cells. Proc Natl Acad Sci U S A. 2005;102:2910-2915.
38. Bettelli E, Korn T, Kuchroo VK. Th17: the third member of the effector Tcell trilogy. Curr Opin Immunol. 2007;19:652-657.
39. Palucka AK, Ueno H, Fay JW, Banchereau J. Taming cancer by inducing immunity via dendritic cells. Immunol Rev. 2007;220:129-150.
40. Yang XO, Pappu BP, Nurieva R, et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors RORalpha and RORgamma. Immunity. 2008;28:29-39.
41. Gocke AR, Cravens PD, Ben LH, et al. T-bet regulates the fate of Th1 and Th17 lymphocytes in autoimmunity. J Immunol. 2007;178:1341-1348.
42. Harris TJ, Grosso JF, Yen HR, et al. Cutting edge: an in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol. 2007;179:4313-4317.
43. Iwamoto S, Iwai S, Tsujiyama K, et al. TNF-alpha drives human CD14+ monocytes to differentiate into CD70+ dendritic cells evoking Th1 and Th17 responses. J Immunol. 2007;179:1449-1457.
44. 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;17:412-416.
45. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity. 2008;28:454-467.
46. Sato K, Suematsu A, Okamoto K, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med. 2006;203:2673-2682.
47. Kotake S, Udagawa N, Takahashi N, et al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest. 1999;103:1345-1352.
48. van den Berg WB, van Lent PL, Joosten LA, Abdollahi-Roodsaz S, Koenders Ml. Amplifying elements of arthritis and joint destruction. Ann Rheum Dis. 2007;66:iii45-iii48.
49. Coury F, Annels N, Rivollier A, et al. Langerhans cell histiocytosis reveals a new IL-17A-dependent pathway of dendritic cell fusion. Nat Med. 2008; 14:81-87.
50. Rivollier A, Mazzorana M, Tebib J, et al. Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood. 2004:104:4029-4037.
51. Noonan K, Matsui W, Serafini P, et al. Activated marrow-infiltrating lymphocytes effectively target plasma cells and their clonogenic precursors. Cancer Res. 2005;65:2026-2034.
52. Dhodapkar MV, Krasovsky J, Osman K, Geller MD. Vigorous premalignancy-specific effector T cell response in the bone marrow of patients with monoclonal gammopathy. J Exp Med. 2003; 198:1753-1757.
53. Said JW, Rettig MR, Heppner K, et al. Localization of Kaposi's sarcoma-associated herpesvirus in bone marrow biopsy samples from patients with multiple myeloma. Blood. 1997;90:4278-4282.
54. Bahlis NJ, King AM, Kolonias D, et al. CD28-mediated regulation of multiple myeloma cell proliferation and survival. Blood. 2007;109:5002-5010.
55. Chauhan D, Bharti A, Raje N, et al. Detection of Kaposi's sarcoma herpesvirus DN A sequences in multiple myeloma bone marrow stromal cells. Blood. 1999;93:1482-1486.
56. Kukreja A, Hutchinson A, Dhodapkar K, et al. Enhancement of clonogenicity of human multiple myeloma by dendritic cells. J Exp Med. 2006;203: 1859-1865.
57. Giuliani N, Lisignoli G, Tagliaferri S, et al. Macrophage inflammatory protein (MIP)-3a/CCL20 and its receptor CCR6 are overexpressed in the bone microenvironment and involved in osteoclast formation in multiple myeloma patients [abstract]. Blood. 2007;110:1028a.
58. Kimura A, Naka T, Kishimoto T. IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc Natl Acad Sci U S A. 2007;104:12099-12104.
59. Andrade F, Casciola-Rosen L, Rosen A. Apoptosis in systemic lupus erythematosus. Clinical implications. Rheum Dis Clin North Am. 2000;26: 215-227.
60. Kim S, Elkon KB, Ma X. Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity. 2004; 21:643-653.
61. Kano S, Sato K, Morishita Y, et al. The contribution of transcription factor IRF1 to the interferongamma-interleukin 12 signaling axis and T(H)1 versus T(H)-17 differentiation of CD4(+) T cells. Nat Immunol. 2008;9:34-41.
62. ZelanteT, DeLuca A, Bonifazi P, et al. IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol. 2007;37:2695-2706.
63. Huang W, Na L, Fidel PL, Schwarzenberger P. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J Infect Dis. 2004;190:624-631.
64. Lo CH, Lee SC, Wu PY, et al. Antitumor and antimetastatic activity of IL-23. J Immunol. 2003;171:600-607.
65. Hu J, Yuan X, Belladonna ML, et al. Induction of potent antitumor immunity by intratumoral injection of interleukin 23-transduced dendritic cells. Cancer Res. 2006;66:8887-8896.
66. Langowski JL, Kastelein RA, Oft M. Swords into plowshares: IL-23 repurposes tumor immune surveillance. Trends Immunol. 2007;28:207-212.
67. 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;67:11970-11979.
68. Zaba LC, Cardinale I, Gilleaudeau P, et al. Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med. 2007;204:3183-3194.