SOCS3 transactivation by PPARγ prevents IL-17-driven cancer growth

Cancer Research

Volumn 73, Issue 12, 2013, Pages 3578-3590

  Berger, Hélène ^a,b   V́egran, Fréd́erique ^a,b   Chikh, Madijd ^a,b   Gilardi, Federica ^e   Ladoire, Sylvain ^a,b,c   Bugaut, Hél̀ene ^a,b   Mignot, Grégoire ^a,b   Chalmin, Fanny ^a,b   Bruchard, Mélanie ^a,b   Deranger̀e, Valentin ^a,b   Chevriaux, Angélique ^a,b,c   Réb́e, Cédric ^a,b,c   Ryffel, Bernhard ^d,h   Pot, Caroline ^f,g   Hichami, Aziz ^a,b   Desvergne, Béatrice ^e   Ghiringhelli, François ^a,b,c   Apetoh, Lionel ^a,b,c  

^a Chu   (France)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c CENTRE GEORGES FRANÇOIS LECLERC   (France)

^d Molecular Immunology   (France)

^e UNIVERSITY OF LAUSANNE   (Switzerland)

^f GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^g UNIVERSITY OF GENEVA   (Switzerland)

^h UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

DOCOSAHEXAENOIC ACID; INTERLEUKIN 17; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMALL INTERFERING RNA; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BREAST ADENOCARCINOMA; CANCER GROWTH; CANCER INHIBITION; CANCER PREVENTION; CARCINOMA CELL; CD4+ T LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIET; FATTY ACID ANALYSIS; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; MELANOMA; MELANOMA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOCS3 GENE; TH17 CELL; TRANSACTIVATION;

ANIMALS; BLOTTING, WESTERN; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE, TUMOR; DIET; DOCOSAHEXAENOIC ACIDS; FEMALE; INTERLEUKIN-17; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; PPAR GAMMA; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TH17 CELLS; TRANSCRIPTIONAL ACTIVATION; TUMOR BURDEN;

EID: 84879103089     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4018     Document Type: Article

References (50)

1. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13: 1050-9. (Pubitemid 47517504)
2. Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med 2009; 15:1170-8.
3. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454:436-44.
4. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009;27:485-517.
5. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006; 126:1121-33. (Pubitemid 44380299)
6. Harris TJ, Grosso JF, Yen HR, Xin H, Kortylewski M, Albesiano E, et al. Cutting edge: an in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. J Immunol 2007; 179:4313-7.
7. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, et al. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem 2007;282:9358-63. (Pubitemid 47104613)
8. Wang L, Yi T, Kortylewski M, Pardoll DM, Zeng D, Yu H. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 2009;206:1457-64.
9. Bang HO, Dyerberg J, Nielsen AB. Plasma lipid and lipoprotein pattern in Greenlandic West-coast Eskimos. Lancet 1971;1:1143-5.
10. Bang HO, Dyerberg J, Sinclair HM. The composition of the Eskimo food in north western Greenland. Am J Clin Nutr 1980;33:2657-61. (Pubitemid 11172006)
11. Finocchiaro C, Segre O, Fadda M, Monge T, Scigliano M, Schena M, et al. Effect of n-3 fatty acids on patients with advanced lung cancer: a double-blind, placebo-controlled study. Br J Nutr 2012; 108:327-33.
12. Li H, Ruan XZ, Powis SH, Fernando R, Mon WY, Wheeler DC, et al. EPA and DHA reduce LPS-induced inflammation responses in HK-2 cells: evidence for a PPAR-gamma-dependent mechanism. Kidney Int 2005; 67:867-74. (Pubitemid 41623311)
13. Siddiqui RA, Harvey KA, Xu Z, Bammerlin EM, Walker C, Altenburg JD. Docosahexaenoic acid: a natural powerful adjuvant that improves efficacy for anticancer treatment with no adverse effects. Biofactors 2011;37:399-412.
14. + T cells. J Exp Med 2008;205:1381-93.
15. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I, et al. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002;17:375-87. (Pubitemid 35279557)
16. Nadra K, Quignodon L, Sardella C, Joye E, Mucciolo A, Chrast R, et al. PPARgamma in placental angiogenesis. Endocrinology 2010;151: 4969-81.
17. Nadra K, Anghel SI, Joye E, Tan NS, Basu-Modak S, Trono D, et al. Differentiation of trophoblast giant cells and their metabolic functions are dependent on peroxisome proliferator-activated receptor beta/delta. Mol Cell Biol 2006;26:3266-81.
18. Triboulot C, Hichami A, Denys A, Khan NA. Dietary (n-3) polyunsaturated fatty acids exert antihypertensive effects by modulating calcium signaling in T cells of rats. J Nutr 2001;131:2364-9. (Pubitemid 32851882)
19. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959;37:911-7.
20. Pace-Asciak CR. One-step rapid extractive methylation of plasma nonesterified fatty acids for gas chromatographic analysis. J Lipid Res 1989;30:451-4. (Pubitemid 19082074)
21. Almallah YZ, El-Tahir A, Heys SD, Richardson S, Eremin O. Distal procto-colitis and n-3 polyunsaturated fatty acids: the mechanism (s) of natural cytotoxicity inhibition. Eur J Clin Invest 2000;30: 58-65. (Pubitemid 30071858)
22. Kong W, Yen JH, Ganea D. Docosahexaenoic acid prevents dendritic cell maturation, inhibits antigen-specific Th1/Th17 differentiation and suppresses experimental autoimmune encephalomyelitis. Brain Behav Immun 2011;25:872-82.
23. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 2005;201:233-40. (Pubitemid 40189432)
24. Chen Z, Laurence A, Kanno Y, Pacher-Zavisin M, Zhu BM, Tato C, et al. Selective regulatory function of Socs3 in the formation of IL-17-secreting T cells. Proc Natl Acad Sci U S A 2006;103:8137-42. (Pubitemid 43801065)
25. Durant L, Watford WT, Ramos HL, Laurence A, Vahedi G, Wei L, et al. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 2010;32:605-15.
26. Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, et al. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 2010;142:687-98.
27. Yu JH, Kim KH, Kim H. SOCS 3 and PPAR-gamma ligands inhibit the expression of IL-6 and TGF-beta1 by regulating JAK2/STAT3 signaling in pancreas. Int J Biochem Cell Biol 2008;40:677-88. (Pubitemid 351297741)
28. Park EJ, Park SY, Joe EH, Jou I. 15d-PGJ2 and rosiglitazone suppress Janus kinase-STAT inflammatory signaling through induction of suppressor of cytokine signaling 1 (SOCS1) and SOCS3 in glia. J Biol Chem 2003;278:14747-52. (Pubitemid 36799798)
29. Molinari R, D'Eliseo D, Manzi L, Zolla L, Velotti F, Merendino N. The n3-polyunsaturated fatty acid docosahexaenoic acid induces immunogenic cell death in human cancer cell lines via pre-apoptotic calreticulin exposure. Cancer Immunol Immunother 2011;60:1503-7.
30. Nam JS, Terabe M, Kang MJ, Chae H, Voong N, Yang YA, et al. Transforming growth factor beta subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res 2008;68:3915-23.
31. Garcia de G, Boyano D, Smith-Zubiaga I, Alvarez A, Canton I, Canavate L. Involvement of interleukin-6 in the biology and metastatic activity of B16F10 melanoma cells. Eur Cytokine Netw 1998;9:187-92.
32. Bunt SK, Yang L, Sinha P, Clements VK, Leips J, Ostrand-Rosenberg S. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res 2007;67:10019-26. (Pubitemid 47621253)
33. Numasaki M, Fukushi J, Ono M, Narula SK, Zavodny PJ, Kudo T, et al. Interleukin-17 promotes angiogenesis and tumor growth. Blood 2003;101:2620-7. (Pubitemid 36857622)
34. Yki-Jarvinen H. Thiazolidinediones. N Engl J Med 2004;351:1106-18.
35. Shibata N, Kawaguchi-Niida M, Yamamoto T, Toi S, Hirano A, Kobayashi M. Effects of the PPARgamma activator pioglitazone on p38 MAP kinase and IkappaBalpha in the spinal cord of a transgenic mouse model of amyotrophic lateral sclerosis. Neuropathology 2008;28:387-98. (Pubitemid 351798977)
36. Klotz L, Burgdorf S, Dani I, Saijo K, Flossdorf J, Hucke S, et al. The nuclear receptor PPAR gamma selectively inhibits Th17 differentiation in a T cell-intrinsic fashion and suppresses CNS autoimmunity. J Exp Med 2009;206:2079-89.
37. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-17.
38. Belluzzi A, Boschi S, Brignola C, Munarini A, Cariani G, Miglio F. Polyunsaturated fatty acids and inflammatory bowel disease. Am J Clin Nutr 2000;71:339S-42S. (Pubitemid 30046138)
39. Almallah YZ, Ewen SW, El-Tahir A, Mowat NA, Brunt PW, Sinclair TS, et al. Distal proctocolitis and n-3 polyunsaturated fatty acids (n-3 PUFAs): the mucosal effect in situ. J Clin Immunol 2000;20:68-76. (Pubitemid 30210109)
40. Nieto N, Torres MI, Rios A, Gil A. Dietary polyunsaturated fatty acids improve histological and biochemical alterations in rats with experimental ulcerative colitis. J Nutr 2002;132:11-9. (Pubitemid 34042448)
41. Shimizu T, Igarashi J, Ohtuka Y, Oguchi S, Kaneko K, Yamashiro Y. Effects of n-3 polyunsaturated fatty acids and vitamin E on colonic mucosal leukotriene generation, lipid peroxidation, and microcirculation in rats with experimental colitis. Digestion 2001;63:49-54. (Pubitemid 32098459)
42. Fradet V, Cheng I, Casey G, Witte JS. Dietary omega-3 fatty acids, cyclooxygenase-2 genetic variation, and aggressive prostate cancer risk. Clin Cancer Res 2009;15:2559-66.
43. Thiebaut AC, Chajes V, Gerber M, Boutron-Ruault MC, Joulin V, Lenoir G, et al. Dietary intakes of omega-6 and omega-3 polyunsaturated fatty acids and the risk of breast cancer. Int J Cancer 2009;124:924-31.
44. Bougnoux P, Hajjaji N, Ferrasson MN, Giraudeau B, Couet C, Le Floch O. Improving outcome of chemotherapy of metastatic breast cancer by docosahexaenoic acid: a phase II trial. Br J Cancer 2009;101:1978-85.
45. Kryczek I, Zhao E, Liu Y, Wang Y, Vatan L, Szeliga W, et al. Human TH17 cells are long-lived effector memory cells. Sci Transl Med 2011;3:104ra0.
46. Muranski P, Borman ZA, Kerkar SP, Klebanoff CA, Ji Y, Sanchez-Perez L, et al. Th17 cells are long lived and retain a stem cell-like molecular signature. Immunity 2011;35:972-85.
47. Zhang JP, Yan J, Xu J, Pang XH, Chen MS, Li L, et al. Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients. J Hepatol 2009;50:980-9.
48. Chen X, Wan J, Liu J, Xie W, Diao X, Xu J, et al. Increased IL-17-producing cells correlate with poor survival and lymphangiogenesis in NSCLC patients. Lung Cancer 2010;69:348-54.
49. Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer. Cancer Res 2011;71:1263-71.
50. Liu J, Duan Y, Cheng X, Chen X, Xie W, Long H, et al. IL-17 is associated with poor prognosis and promotes angiogenesis via stimulating VEGF production of cancer cells in colorectal carcinoma. Biochem Biophys Res Commun 2011;407:348-54.