A role for T-bet-mediated tumour immune surveillance in anti-IL-17A treatment of lung cancer

Nature Communications

Volumn 2, Issue 1, 2011, Pages

  Reppert, S ^a   Boross, I ^b   Koslowski, M ^b   Tureci O ^b   Koch, S ^a   Lehr, H A ^c   Finotto, S ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 23; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LEUKOCYTE ANTIGEN; NEUTRALIZING ANTIBODY; T BOX TRANSCRIPTION FACTOR; T BOX TRANSCRIPTION FACTOR TBX21; T-BOX TRANSCRIPTION FACTOR TBX21;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL SURVIVAL; CLINICAL ARTICLE; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOSURVEILLANCE; LUNG ADENOCARCINOMA; LUNG CANCER; MALE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; UPREGULATION; WILD TYPE; ADENOCARCINOMA; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; LUNG; LUNG TUMOR; METABOLISM; MIDDLE AGED; MOUSE; MOUSE MUTANT; PATHOLOGY;

ADENOCARCINOMA; ADMINISTRATION, INTRANASAL; ADULT; AGED; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIGENS, CD; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOLOGIC SURVEILLANCE; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-23; LUNG; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTES, REGULATORY;

EID: 84455203145     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1609     Document Type: Article

References (50)

1. Greenlee, R. T., Hill-Harmon, M. B., Murray, T. & Tun, M. Cancer statistics. CA Cancer J. Clin. 51, 15-36 (2001).
2. Travis, W. D., Travis, L. B. & Devesa, S. S. Lung cancer. Cancer 75, 191-202 (1995).
3. Lee, J. M. et al. Infammation in lung carcinogenesis: new targets for lung cancer chemoprevention and treatment. Crit. Rev. Oncol. Hematol. 66, 208-217 (2008).
4. Iwakura, Y., Ishigame, H., Saijo, S. & Nakae, S. Functional specialization of interleukin-17 family members. Immunity 34, 49-62 (2011).
5. Hu, Y., Shen, F., Crellin, N. K. & Ouyang, W. Te IL-17 pathway as a major therapeutic target in autoimmune diseases. Ann. NY Acad. Sci. 1217, 60-76 (2011).
6. Ciree, A. et al. Expression and activity of IL-17 in cutaneous T-cell lymphomas (mycosis fungoides and Sezary syndrome). Int. J. Cancer 112, 113-120 (2004). (Pubitemid 39249498)
7. Kato, T. et al. Expression of IL-17 mRNA in ovarian cancer. Biochem. Biophys. Res. Commun. 282, 735-738 (2001). (Pubitemid 32924619)
8. Folkman, J., Watson, K., Ingber, D. & Hanahan, D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature 339, 58-61 (1998).
9. Hanahan, D. & Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364 (1996). (Pubitemid 26272076)
10. Leek, R. D., Harris, A. L. & Lewis, C. E. Cytokine networks in solid human tumours: regulation of angiogenesis. J. Leukoc. Biol. 56, 423-435 (1994). (Pubitemid 24319901)
11. Arenberg, D. A. et al. Te role of CXC chemokines in the regulation of angiogenesis in non-small cell lung cancer. J Leukoc Biol 62, 554-562 (1997). (Pubitemid 27519764)
12. Fontanini, G. et al. Vascular endothelial growth factor is associated with neovascularization and infuences progression of non-small cell lung carcinoma. Clin. Cancer Res. 3, 861-865 (1997). (Pubitemid 27252933)
13. Tanaka, F. et al. Expression of angiopoietins and its clinical signifcance in non-small cell lung cancer. Cancer Res. 62, 7124-7129.
14. Arenberg, D. A. et al. Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice. J. Clin. Invest. 97, 2792-2802 (1996). (Pubitemid 26197092)
15. Arenberg, D. A. et al. Interferon-gamma-inducible protein 10 (IP-10) is an angiostatic factor that inhibits human non-small cell lung cancer (NSCLC) tumorigenesis and spontaneous metastases. J. Exp. Med. 184, 981-992 (1996).
16. Numasaki, M. et al. Interleukin-17 promotes angiogenesis and tumour growth. Blood 101, 2620-2627 (2003). (Pubitemid 36857622)
17. Unutmaz, D. RORC2:the master regulator of human T17 cell programming. Eur. J. Immunol. 39, 1452-1455 (2009).
18. Durrant, D. M., Gafen, S. L., Riesenfeld, E. P., Irvin, C. G. & Metzger, D. W. Development of allergen-induced airway infammation in the absence of T-bet regulation is dependent on IL-17. J. Immunol. 183, 5293-5300 (2009).
19. Dubinett, S. M. et al. Intratumoral interleukin-2 immunotherapy: activation of tumour-infltrating and splenic lymphocytes in vivo. Cancer Immunol. Immunother. 36, 156-162 (1993). (Pubitemid 23047713)
20. Werneck, M. B., Lugo-Villarino, G., Hwang, E. S., Cantor, H. & Glimcher, L. H. T-bet plays a key role in NK-mediated control of melanoma metastatic disease. J. Immunol. 180, 8004-8010 (2008).
21. Sauer, K. A. et al. Immunosurveillance of lung melanoma metastasis in EBI-3-defcient mice mediated by CD8+ T cells. J. Immunol. 181, 6148-6157 (2008).
22. Hofman, R. M. Te multiple uses of fuorescent proteins to visualize cancer in vivo. Nat. Rev. Cancer 5, 796-806 (2005).
23. Bertram, J. S. & Janik, P. Establishment of a cloned line of Lewis lung carcinoma cells adapted to cell culture. Cancer Lett. 11, 63-73 (1980). (Pubitemid 11198069)
24. Martin-Orozco, N. et al. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 31, 787-798 (2009).
25. He, D. et al. IL-17 promotes tumor development through the induction of tumor promoting microenvironments at tumor sites and myeloid-derived suppressor cells. J. Immunol. 184, 2281-2288 (2010).
26. Chae, W. J. et al. Ablation of IL17-A abrogates progression of spontaneous intestinal tumorigensis. Proc. Natl Acad. Sci. USA. 107, 5540-5544 (2010).
27. Wang, L. et al. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J. Exp. Med. 206, 1457-1464 (2009).
28. Bromberg, J. F. et al. Stat3 as an oncogene. Cell 98, 295-303 (1999). (Pubitemid 29380565)
29. Yu, H., Kortylewski, M. & Pardoll, D. Crosstalk between cancer and immune cells:role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 7, 41-51 (2007). (Pubitemid 46020826)
30. Colombo, M. P. & Piconese, S. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat. Rev. Cancer 7, 880-887 (2007). (Pubitemid 350006256)
31. Di Cesare, A., Di Meglio, P. & Nestle, F. O. Te IL-23/T17 axis in the immunopathogenesis of psoriasis. J. Invest. Dermatol. 129, 1339-1350 (2009).
32. Gyulveszi, G., Haak, S. & Becher, B. IL-23-driven encephalo-tropism and T17 polarization during CNS-infammation in vivo. Eur. J. Immunol. 39, 1864-1869 (2009).
33. Wakashin, H., Hirose, K., Iwamoto, I. & Nakajima, H. Role of IL-23-T17 cell axis in allergic airway infammation. Int. Arch. Allergy Immunol. 149(Suppl 1), 108-112 (2009).
34. Cornelissen, F., van Hamburg, J. P. & Lubberts, E. Te IL-12/IL-23 axis and its role in T17 cell development, pathology and plasticity in arthritis. Curr. Opin. Investig. Drugs 10, 452-462 (2009).
35. Weaver, C. T., Hatton, R. D., Mangan, P. R. & Harrington, L. E. IL-17 family cytokines and the expanding diversity of efector T cell lineages. Annu. Rev. Immunol. 25, 821-852 (2007). (Pubitemid 46697925)
36. Zhou, L., Chong, M. M. & Littman, D. R. Plasticity of CD4+ T cell lineage diferentiation. Immunity 30, 646-655 (2009).
37. Chen, Z., Laurence, A. & O'Shea, J. J. Signal transduction pathways and transcriptional regulation in the control of T17 diferentiation. Semin. Immunol. 19, 400-408 (2007).
38. Wang, X., Fu, X. & Hofman, R. M. A new patient like metastatic model of human lung cancer constructed orthotopically with intact tissue via thoracotomy in immuno-defcient mice. Int. J. Cancer 51, 992-995 (1992).
39. Hofman, R. M. Orthotopic metastatic mouse models for anticancer drug discovery and evaluation: a bridge to the clinic. Investig. New Drugs 17, 343-360 (1999).
40. Gocke, A. R. et al. T-bet regulates the fate of T1 and T17 lymphocytes in autoimmunity. J. Immunol. 178, 1341-1348 (2007). (Pubitemid 46154603)
41. Mangan, P. R. et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441, 231-234 (2006).
42. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M. & Stockinger, B. TGFbeta in the context of an infammatory cytokine milieu supports de novo diferentiation of IL-17-producing T cells. Immunity 24, 179-189 (2006). (Pubitemid 43214587)
43. Wang, R. F. Immune suppression by tumour-specifc CD4+ regulatory T-cells in cancer. Semin. Cancer Biol. 16, 73-79 (2006).
44. Wang, R. F. Regulatory T cells and innate immune regulation in tumour immunity. Springer Semin. Immunopathol. 28, 17-23 (2006).
45. Szabo, S. J. et al. A novel transcription factor, T-bet, directs T1 lineage commitment. Cell 100, 655-669 (2000).
46. Finotto, S. et al. Development of spontaneous airway changes consistent with human asthma in mice lacking T-bet. Science 295, 336-338 (2002). (Pubitemid 34074365)
47. Townsend, M. J. et al. Tbet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20, 477-494 (2004). (Pubitemid 38482125)
48. Szabo, S. J. et al. Distinct efects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8T cells. Science 295, 338-342 (2002). (Pubitemid 34074366)
49. Maxeiner, J. H. et al. A key regulatory role of the transcription factor NFATc2 in bronchial adenocarcinoma via CD8+ T lymphocytes. Cancer Res. 69, 3069-3076 (2009).
50. Sauer, K. A., Scholtes, P., Karwot, R. & Finotto, S. Isolation of CD4+ T cells from murine lungs: a method to analyze ongoing immune responses in the lung. Nat. Protoc. 1, 2870-2875 (2006).