IL-23 suppresses innate immune response independently of IL-17A during carcinogenesis and metastasis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 18, 2010, Pages 8328-8333

  Teng, Michele W L ^a,b   Andrews, Daniel M ^a   McLaughlin, Nicole ^a   Von Scheidt, Bianca ^a   Ngiow, Shin Foong ^a,b   Möller, Andreas ^a,b   Hill, Geoffrey R ^c   Iwakura, Yoichiro ^d   Oft, Martin ^e   Smyth, Mark J ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF TOKYO   (Japan)

^e MERCK RESEARCH LABORATORIES   (United States)

Author keywords

IL 2; Inflammation; Innate immunity; NK cell; Tumor

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 23P19; PERFORIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; B LYMPHOCYTE; CANCER INCIDENCE; CARCINOGENESIS; CD8+ T LYMPHOCYTE; COLON ADENOCARCINOMA; DENDRITIC CELL; EXPERIMENTAL MODEL; FIBROSARCOMA; IMMUNE RESPONSE; IMMUNOTHERAPY; LUNG METASTASIS; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SKIN PAPILLOMA; T LYMPHOCYTE;

ANIMALS; CELL LINE, TUMOR; FEMALE; IMMUNITY, INNATE; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-2; INTERLEUKIN-23 SUBUNIT P19; KILLER CELLS, NATURAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIUM; NEOPLASM METASTASIS; NEOPLASMS; PERFORIN;

MUS;

EID: 77952402724     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1003251107     Document Type: Article

References (42)

1. Trinchieri G, Pflanz S, Kastelein RA (2003) The IL-12 family of heterodimeric cytokines: New players in the regulation of T cell responses. Immunity 19:641-644. (Pubitemid 37490789)
2. Trinchieri G (2003) Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 3:133-146. (Pubitemid 37328691)
3. Oppmann B, et al. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13:715-725.
4. Lyakh L, Trinchieri G, Provezza L, Carra G, Gerosa F (2008) Regulation of interleukin-12/interleukin-23 production and the T-helper 17 response in humans. Immunol Rev 226:112-131.
5. Presky DH, et al. (1996) A functional interleukin 12 receptor complex is composed of two beta-type cytokine receptor subunits. Proc Natl Acad Sci USA 93:14002-14007. (Pubitemid 26424235)
6. Parham C, et al. (2002) A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol 168:5699-5708. (Pubitemid 34556153)
7. McKenzie BS, Kastelein RA, Cua DJ (2006) Understanding the IL-23-IL-17 immune pathway. Trends Immunol 27:17-23.
8. Langrish CL, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201:233-240.
9. Kolls JK, Lindén A (2004) Interleukin-17 family members and inflammation. Immunity 21:467-476.
10. Yen D, et al. (2006) IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest 116:1310-1316.
11. Tesmer LA, Lundy SK, Sarkar S, Fox DA (2008) Th17 cells in human disease. Immunol Rev 223:87-113.
12. Luger D, et al. (2008) Either a Th17 or a Th1 effector response can drive autoimmunity: Conditions of disease induction affect dominant effector category. J Exp Med 205:799-810. (Pubitemid 351549879)
13. O'Connor RA, et al. (2008) Cutting edge: Th1 cells facilitate the entry of Th17 cells to the central nervous system during experimental autoimmune encephalomyelitis. J Immunol 181:3750-3754.
14. Haak S, et al. (2009) IL-17A and IL-17F do not contribute vitally to autoimmune neuroinflammation in mice. J Clin Invest 119:61-69.
15. Zhou L, Chong MM, Littman DR (2009) Plasticity of CD4+ T cell lineage differentiation. Immunity 30:646-655.
16. Langowski JL, et al. (2006) IL-23 promotes tumour incidence and growth. Nature 442:461-465.
17. Kortylewski M, et al. (2009) Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment. Cancer Cell 15:114-123.
18. Kryczek I, Wei S, Szeliga W, Vatan L, Zou W (2009) Endogenous IL-17 contributes to reduced tumor growth and metastasis. Blood 114:357-359.
19. Martin-Orozco N, et al. (2009) T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 31:787-798.
20. Wang L, et al. (2009) IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 206:1457-1464.
21. Wu S, et al. (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15:1016-1022.
22. Smyth MJ, et al. (1999) Perforin is a major contributor to NK cell control of tumor metastasis. J Immunol 162:6658-6662.
23. Smyth MJ, et al. (2004) NKG2D recognition and perforin effector function mediate effective cytokine immunotherapy of cancer. J Exp Med 200:1325-1335.
24. Moore RJ, et al. (1999) Mice deficient in tumor necrosis factor-alpha are resistant to skin carcinogenesis. Nat Med 5:828-831.
25. Swann JB, et al. (2008) Demonstration of inflammation-induced cancer and cancer immunoediting during primary tumorigenesis. Proc Natl Acad Sci USA 105:652-656.
26. Smyth MJ, et al. (2000) Differential tumor surveillance by natural killer (NK) and NKT cells. J Exp Med 191:661-668.
27. Koebel CM, et al. (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450:903-907.
28. Smyth MJ, Crowe NY, Godfrey DI (2001) NK cells and NKT cells collaborate in host protection from methylcholanthrene-induced fibrosarcoma. Int Immunol 13:459-463.
29. Girardi M, et al. (2001) Regulation of cutaneous malignancy by gammadelta T cells. Science 294:605-609. (Pubitemid 32999559)
30. Oppenheim DE, et al. (2005) Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 6:928-937.
31. Awasthi A, et al. (2009) Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol 182:5904-5908.
32. Cella M, et al. (2009) A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity. Nature 457:722-725.
33. Xiao M, et al. (2009) IFNgamma promotes papilloma development by up-regulating Th17-associated inflammation. Cancer Res 69:2010-2017.
34. Street SE, Cretney E, Smyth MJ (2001) Perforin and interferon-gamma activities independently control tumor initiation, growth, and metastasis. Blood 97:192-197. (Pubitemid 32061260)
35. Guia S, et al. (2008) A role for interleukin-12/23 in the maturation of human natural killer and CD56+ T cells in vivo. Blood 111:5008-5016.
36. Kaiga T, et al. (2007) Systemic administration of IL-23 induces potent antitumor immunity primarily mediated through Th1-type response in association with the endogenously expressed IL-12. J Immunol 178:7571-7580. (Pubitemid 46898026)
37. Overwijk WW, et al. (2006) Immunological and antitumor effects of IL-23 as a cancer vaccine adjuvant. J Immunol 176:5213-5222.
38. Shan BE, Hao JS, Li QX, Tagawa M (2006) Antitumor activity and immune enhancement of murine interleukin-23 expressed in murine colon carcinoma cells. Cell Mol Immunol 3:47-52.
39. Hu J, et al. (2006) Induction of potent antitumor immunity by intratumoral injection of interleukin 23-transduced dendritic cells. Cancer Res 66:8887-8896. (Pubitemid 44449207)
40. Yuan X, Hu J, Belladonna ML, Black KL, Yu JS (2006) Interleukin-23- expressing bone marrow-derived neural stem-like cells exhibit antitumor activity against intracranial glioma. Cancer Res 66:2630-2638.
41. Nakae S, et al. (2002) Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17:375-387. (Pubitemid 35279557)
42. Smyth MJ, Kelly JM, Baxter AG, Körner H, Sedgwick JD (1998) An essential role for tumor necrosis factor in natural killer cell-mediated tumor rejection in the peritoneum. J Exp Med 188:1611-1619. (Pubitemid 28516106)