Improved mouse models to assess tumour immunity and irAEs after combination cancer immunotherapies

Clinical and Translational Immunology

Volumn 3, Issue 8, 2014, Pages

  Liu, Jing ^a,b   Blake, Stephen J ^a   Smyth, Mark J ^a,b   Teng, Michele WL ^a,b  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84919964373     PISSN: None     EISSN: 20500068     Source Type: Journal    
DOI: 10.1038/cti.2014.18     Document Type: Review

References (68)

1. Couzin-Frankel J. Breakthrough of the year 2013. Cancer immunotherapy. Science (New York, N.Y.) 2013; 342: 1432–1433.
2. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369: 122–133.
3. Callahan MK, Wolchok JD. At the bedside: CTLA-4- and PD-1-blocking antibodies in cancer immunotherapy. J Leukoc Biol 2013; 94: 41–53.
4. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005; 353: 2654–2666.
5. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science (New York, N.Y.) 2006; 313: 1960–1964.
6. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 2011; 29: 610–618.
7. Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G et al. In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 2009; 27: 5944–5951.
8. Galon J, Angell HK, Bedognetti D, Marincola FM. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013; 39: 11–26.
9. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science (New York, N.Y.) 2011; 331: 1565–1570.
10. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646–674.
11. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29: 235–271.
12. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995; 182: 459–465.
13. Chen L. Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity. Nat Rev Immunol 2004; 4: 336–347.
14. Goldberg MV, Drake CG. LAG-3 in cancer immunotherapy. Curr Top Microbiol Immunol 2011; 344: 269–278.
15. Ngiow SF, Teng MW, Smyth MJ. Prospects for TIM3-targeted antitumor immunotherapy. Cancer Res 2011; 71: 6567–6571.
16. Gyorki DE, Callahan M, Wolchok JD, Ariyan CE. The delicate balance of melanoma immunotherapy. Clin Trans Immunol 2013; 2: e5.
17. Page DB, Postow MA, Callahan MK, Allison JP, Wolchok JD. Immune modulation in cancer with antibodies. Annu Rev Med 2014; 65: 185–202.
18. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711–723.
19. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366: 2443–2454.
20. Weber JS, Kähler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol 2012; 30: 2691–2697.
21. McDermott D, Haanen J, Chen T-T, Lorigan P, O'Day S, MDX010 Investigators. Efficacy and safety of ipilimumab in metastatic melanoma patients surviving more than 2 years following treatment in a phase III trial (MDX010-20). Ann Oncol 2013; 24: 2694–2698.
22. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014.
23. Phan GQ, Yang JC, Sherry RM, Hwu P, Topalian SL, Schwartzentruber DJ et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci USA 2003; 100: 8372–8377.
24. Feng Y, Roy A, Masson E, Chen T-T, Humphrey R, Weber JS. Exposure–response relationships of the efficacy and safety of ipilimumab in patients with advanced melanoma. Clin Cancer Res 2013; 19: 3977–3986.
25. Schadendorf D. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in metastatic or locally advanced, unresectable melanoma [abstract]. Eur Cancer Congress 2013; 2013: LBA24.
26. Yao S, Zhu Y, Chen L. Advances in targeting cell surface signalling molecules for immune modulation. Nat Rev Drug Discov 2013; 12: 130–146.
27. Vonderheide RH, Glennie MJ. Agonistic CD40 antibodies and cancer therapy. Clin Cancer Res 2013; 19: 1035–1043.
28. Gangadhar TC, Vonderheide RH. Mitigating the toxic effects of anticancer immunotherapy. Nat Rev Clin Oncol 2014; 11: 91–99.
29. Weinberg AD, Morris NP, Kovacsovics-Bankowski M, Urba WJ, Curti BD. Science gone translational: the OX40 agonist story. Immunol Rev 2011; 244: 218–231.
30. Li SY, Liu Y. Immunotherapy of melanoma with the immune costimulatory monoclonal antibodies targeting CD137. Clin Pharmacol 2013; 5 (Suppl 1): 47–53.
31. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbé C et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009; 15: 7412–7420.
32. Prieto PA, Yang JC, Sherry RM, Hughes MS, Kammula US, White DE et al. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin Cancer Res 2012; 18: 2039–2047.
33. Downey SG, Klapper JA, Smith FO, Yang JC, Sherry RM, Royal RE et al. Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin Cancer Res 2007; 13 (22 Pt 1): 6681–6688.
34. Ribas A, Hodi FS, Callahan M, Konto C, Wolchok J. Hepatotoxicity with combination of vemurafenib and ipilimumab. N Engl J Med 2013; 368: 1365–1366.
35. Bystryn JC, Rigel D, Friedman RJ, Kopf A. Prognostic significance of hypopigmentation in malignant melanoma. Arch Dermatol 1987; 123: 1053–1055.
36. Byrne KT, Cote AL, Zhang P, Steinberg SM, Guo Y, Allie R et al. Autoimmune melanocyte destruction is required for robust CD8+ memory T cell responses to mouse melanoma. J Clin Invest 2011; 121: 1797–1809.
37. Duhra P, Ilchyshyn A. Prolonged survival in metastatic malignant melanoma associated with vitiligo. Clin Exp Dermatol 1991; 16: 303–305.
38. Quaglino P, Marenco F, Osella-Abate S, Cappello N, Ortoncelli M, Salomone B et al. Vitiligo is an independent favourable prognostic factor in stage III and IV metastatic melanoma patients: results from a single-institution hospital-based observational cohort study. Ann Oncol 2010; 21: 409–414.
39. Pommier A, Audemard A, Durand A, Lengagne R, Delpoux A, Martin B et al. Inflammatory monocytes are potent antitumor effectors controlled by regulatory CD4+ T cells. Proc Natl Acad Sci USA 2013; 110: 13085–13090.
40. Dranoff G. Experimental mouse tumour models: what can be learnt about human cancer immunology? Nat Rev Immunol 2012; 12: 61–66.
41. DuPage M, Jacks T. Genetically engineered mouse models of cancer reveal new insights about the antitumor immune response. Curr Opin Immunol 2013; 25: 192–199.
42. Eyles J, Puaux AL, Wang X, Toh B, Prakash C, Hong M et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 2010; 120: 2030–2039.
43. Knight DA, Ngiow SF, Li M, Parmenter T, Mok S, Cass A et al. Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J Clin Invest 2013; 123: 1371–1381.
44. DuPage M, Cheung AF, Mazumdar C, Winslow MM, Bronson R, Schmidt LM et al. Endogenous T cell responses to antigens expressed in lung adenocarcinomas delay malignant tumor progression. Cancer Cell 2011; 19: 72–85.
45. DuPage M, Mazumdar C, Schmidt LM, Cheung AF, Jacks T. Expression of tumour-specific antigens underlies cancer immunoediting. Nature 2012; 482: 405–409.
46. Matsushita H, Vesely MD, Koboldt DC, Rickert CG, Uppaluri R, Magrini VJ et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 2012; 482: 400–404.
47. Devaud C, Westwood JA, John LB, Flynn JK, Paquet-Fifield S, Duong CP et al. Tissues in different anatomical sites can sculpt and vary the tumor microenvironment to affect responses to therapy. Mol Ther 2014; 22: 18–27.
48. Uno T, Takeda K, Kojima Y, Yoshizawa H, Akiba H, Mittler RS et al. Eradication of established tumors in mice by a combination antibody-based therapy. Nat Med 2006; 12: 693–698.
49. Iwama S, De Remigis A, Callahan MK, Slovin SF, Wolchok JD, Caturegli P. Pituitary expression of CTLA-4 mediates hypophysitis secondary to administration of CTLA-4 blocking antibody. Sci Transl Med 2014; 6: 230ra45.
50. Murphy JT, Burey AP, Beebe AM, Gu D, Presta LG, Merghoub T et al. Anaphylaxis caused by repetitive doses of a GITR agonist monoclonal antibody in mice. Blood 2014; 123: 2172–2180.
51. Teng MW, Ngiow SF, von Scheidt B, McLaughlin N, Sparwasser T, Smyth MJ. Conditional regulatory T-cell depletion releases adaptive immunity preventing carcinogenesis and suppressing established tumor growth. Cancer Res 2010; 70: 7800–7809.
52. Lahl K, Sparwasser T. In vivo depletion of FoxP3+ Tregs using the DEREG mouse model. Methods Mol Biol 2011; 707: 157–172.
53. Kim JM, Rasmussen JP, Rudensky AY. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat Immunol 2007; 8: 191–197.
54. Ngiow SF, von Scheidt B, Moller A, Smyth MJ, Teng MW. The interaction between murine melanoma and the immune system reveals that prolonged responses predispose for autoimmunity. Oncoimmunology 2013; 2: e23036.
55. Hemminki K, Liu X, Ji J, Sundquist J, Sundquist K. Autoimmune disease and subsequent digestive tract cancer by histology. Ann Oncol 2012; 23: 927–933.
56. Zhernakova A, van Diemen CC, Wijmenga C. Detecting shared pathogenesis from the shared genetics of immune-related diseases. Nat Rev Genet 2009; 10: 43–55.
57. Miska J, Bas E, Devarajan P, Chen Z. Autoimmunity-mediated antitumor immunity: tumor as an immunoprivileged self. Eur J Immunol 2012; 42: 2584–2596.
58. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet 2008; 371: 569–578.
59. Nicolucci A. Epidemiological aspects of neoplasms in diabetes. Acta Diabetol 2010; 47: 87–95.
60. Pelleymounter M, Cullen M, Baker M, Hecht R, Winters D, Boone T et al. Effects of the obese gene product on body weight regulation in ob/ob mice. Science (New York, N.Y.) 1995; 269: 540–543.
61. Yang JC, Hughes M, Kammula U, Royal R, Sherry RM, Topalian SL et al. Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis. J Immunother 2007; 30: 825–830.
62. Chung KY, Gore I, Fong L, Venook A, Beck SB, Dorazio P et al. Phase II study of the anti-cytotoxic T-lymphocyte-associated antigen 4 monoclonal antibody, tremelimumab, in patients with refractory metastatic colorectal cancer. J Clin Oncol 2010; 28: 3485–3490.
63. Ralph C, Elkord E, Burt DJ, O'Dwyer JF, Austin EB, Stern PL et al. Modulation of lymphocyte regulation for cancer therapy: a phase II trial of tremelimumab in advanced gastric and esophageal adenocarcinoma. Clin Cancer Res 2010; 16: 1662–1672.
64. Ribas A, Kefford R, Marshall MA, Punt CJ, Haanen JB, Marmol M et al. Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma. J Clin Oncol 2013; 31: 616–622.
65. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013; 369: 134–144.
66. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366: 2455–2465.
67. Herbst RS, Gordon MS, Fine GD, Sosman JA, Soria J, Hamid O et al. A study of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic tumors. J Clin Oncol 2013 31 (suppl): Abstract 3000).
68. Vonderheide RH, Flaherty KT, Khalil M, Stumacher MS, Bajor DL, Hutnick NA et al. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007; 25: 876–883.