Requirement for innate immunity and CD90 NK1.1 lymphocytes to treat established melanoma with chemo-immunotherapy

Cancer Immunology Research

Volumn 3, Issue 3, 2015, Pages 296-304

  Moskalenko, Marina ^a   Pan, Michael ^a   Fu, Yichun ^b   De Moll, Ellen H ^a   Hashimoto, Daigo ^a,c   Mortha, Arthur ^a   Leboeuf, Marylene ^a   Jayaraman, Padmini ^d   Bernardo, Sebastian ^a   Sikora, Andrew G ^d   Wolchok, Jedd ^e   Bhardwaj, Nina ^a   Merad, Miriam ^a   Saenger, Yvonne ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NewYork Presbyterian Hospital   (United States)

^c HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY TARGETING TYROSINASE RELATED PROTEIN 1; CYCLOPHOSPHAMIDE; DIFFERENTIATION ANTIGEN; F4/80 PROTEIN; FC RECEPTOR; INTERLEUKIN 2 RECEPTOR GAMMA; PROTEIN; THY 1 ANTIGEN; UNCLASSIFIED DRUG; KLRB1C PROTEIN, MOUSE; LY ANTIGEN; MONOCLONAL ANTIBODY; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY B; OXIDOREDUCTASE; TYROSINASE-RELATED PROTEIN-1;

ACTIVE IMMUNIZATION; ADAPTIVE IMMUNITY; ADD ON THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PREVENTION; CELL INFILTRATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; FEMALE; IMMUNE SYSTEM; IN VIVO STUDY; INNATE IMMUNITY; LONG TERM SURVIVAL; LOW DRUG DOSE; LYMPHOID CELL; MACROPHAGE; MELANOMA; MELANOMA B16; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PASSIVE IMMUNIZATION; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TREATMENT RESPONSE; WILD TYPE; ANIMAL; C57BL MOUSE; CD8+ T LYMPHOCYTE; IMMUNOLOGY; IMMUNOTHERAPY; KNOCKOUT MOUSE; MELANOMA, EXPERIMENTAL; METABOLISM; NATURAL KILLER CELL; TUMOR CELL LINE;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, LY; ANTIGENS, THY-1; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYCLOPHOSPHAMIDE; FEMALE; IMMUNITY, INNATE; IMMUNOTHERAPY; KILLER CELLS, NATURAL; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B; OXIDOREDUCTASES; RECEPTORS, IGG;

EID: 84962308492     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-14-0120     Document Type: Article

References (56)

1. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survivalwith ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
2. Hamid O, Robert C, Daud A, Hodi FS, Hwu W-J, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.
3. Hersh EM, O'Day SJ, Powderly J, Khan KD, Pavlick AC, Cranmer LD, et al. A phase II multicenter study of ipilimumab with or without dacarbazine in chemotherapy-naive patients with advanced melanoma. Invest New Drugs 2011;29:489-98.
4. Weber J, Hamid O, Amin A, O'Day S, Masson E, Goldberg SM, et al. Randomized phase I pharmacokinetic study of ipilimumab with or without oneoftwo different chemotherapy regimens in patients with untreated advanced melanoma. Cancer Immunity 2013;13:7.
5. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517-26.
6. Wolchok JD, Weber JS, Maio M, Neyns B, Harmankaya K, Chin K, et al. Four-year survival rates for patients with metastatic melanoma who received ipilimumab in phase II clinical trials. Ann Oncol 2013;24: 2174-80.
7. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 2001; 344:783-92.
8. Smith EL, Zamarin D, Lesokhin AM. Harnessing the immune system for cancer therapy. Curr Opin Oncol 2014;26:600-7.
9. Shuptrine CW, Surana R, Weiner LM. Monoclonal antibodies for the treatment of cancer. Sem Cancer Biol 2012;22:3-13.
10. Gajria D, Chandarlapaty S. HER2-amplified breast cancer: mechanisms of trastuzumab resistance and novel targeted therapies. Expert Rev Anticancer Ther 2011;11:263-75.
11. Abes R, Gelize E, Fridman WH, Teillaud JL. Long-lasting antitumor protection by anti-CD20 antibody through cellular immune response. Blood 2010;116:926-34.
12. Weng WK, Weng WK, Levy R. Immunoglobulin G Fc receptor polymorphisms do not correlate with response to chemotherapy or clinical course in patients with follicular lymphoma. Leuk Lymphoma 2009;50: 1494-500.
13. Nimmerjahn F, Ravetch JV. Antibodies, Fc receptors and cancer. Curr Opin Immunol 2007;19:239-45.
14. Weiner Louis M, Murray Joseph C, Shuptrine Casey W. Antibody-based immunotherapy of cancer. Cell 2012;148:1081-4.
15. Houghton AN The serological analysis of human cancer. Identification of differentiation antigens onmelanoma and melanocytes. Prog Clin Biol Res 1983;119:199-205.
16. Hara I, Takechi Y, Houghton AN. Implicating a role for immune recognition of self in tumor rejection: passive immunization against the brown locus protein. J Exp Med 1995;182:1609-14.
17. Takechi Y, Hara I, Naftzger C, Xu Y, Houghton AN. A melanosomal membrane protein is a cell surface target for melanoma therapy. Clin Cancer Res 1996;2:1837-42.
18. Welt S, Mattes MJ, Grando R, Thomson TM, Leonard RW, Zanzonico PB, et al. Monoclonal antibody to an intracellular antigen images human melanoma transplants in nu/nu mice. Proc Natl Acad Sci U S A 1987;84: 4200-4.
19. Clynes R, Takechi Y, Moroi Y, Houghton A, Ravetch JV. Fc receptors are required in passive and active immunity to melanoma. Proc Natl Acad Sci U S A 1998;95:652-6.
20. Shields JD, Kourtis IC, Tomei AA, Roberts JM, Swartz MA. Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 2010;328:749-52.
21. Hirschhorn-Cymerman D, Rizzuto GA, Merghoub T, Cohen AD, Avogadri F, Lesokhin AM, et al. OX40 engagement and chemotherapy combination provides potent antitumor immunity with concomitant regulatory T cell apoptosis. J Exp Med 2009;206: 1103-16.
22. Cao X, Shores EW, Hu-Li J, Anver MR, Kelsall BL, Russell SM, et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 1995;2:223-38.
23. + cells that can differentiate to APC, NK cells, and follicular cells but not T or B cells. Immunity 1997;7:493-504.
24. Spits H, Artis D, Colonna M, Diefenbach A, Di Santo JP, Eberl G, et al. Innate lymphoid cells - a proposal for uniform nomenclature. Nat Rev Immunol 2013;13:145-9.
25. Albert H, Collin M, Dudziak D, Ravetch JV, Nimmerjahn F. In vivo enzymatic modulation of IgG glycosylation inhibits autoimmune disease in an IgG subclass-dependent manner. Proc Natl Acad Sci USA 2008; 105:15005-9.
26. Parikh F, Duluc D, Imai N, Clark A, Misiukiewicz K, Bonomi M, et al. Chemo radiotherapy-induced upregulation of PD-1 antagonizes immunity to HPV-related oropharyngeal cancer. Cancer Res 2014;74:7205-16.
27. Spits H, Cupedo T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Ann Rev Immunol 2012;30: 647-75.
28. + T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005; 105:2862-8.
29. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 2011;71:4809-20.
30. Tabrizi MA, Tseng CM, Roskos LK. Elimination mechanisms of therapeutic monoclonal antibodies. Drug Discov Today 2006;11:81-8.
31. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 1994;76:519-29.
32. Weiner LM, Surana R, Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol 2010;10:317-27.
33. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992;68:869-77.
34. Dhodapkar KM, Kaufman JL, Ehlers M, Banerjee DK, Bonvini E, Koenig S, et al. Selective blockade of inhibitory Fcgamma receptor enables human dendritic cell maturation with IL-12p70 production and immunity to antibody-coated tumor cells. Proc Natl Acad Sci USA 2005;102:2910-5.
35. 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;195:125-33.
36. Diefenbach A, Colonna M, Koyasu S. Development, differentiation, and diversity of innate lymphoid cells. Immunity 2014;41:354-65.
37. Eisenring M, vom Berg J, Kristiansen G, Saller E, Becher B. IL-12 initiates tumor rejection via lymphoid tissue-inducer cells bearing the natural cytotoxicity receptor NKp46. Nat Immunol 2010;11:1030-8.
38. Walker JA, Barlow JL, McKenzie AN. Innate lymphoid cells - how did we miss them? Nat Rev Immunol 2013;13:75-87.
39. Bevaart L, Jansen MJ, van Vugt MJ, Verbeek JS, van de Winkel JG, Leusen JH. The high-affinity IgG receptor, Fcgamma R, plays a central role in antibody therapy of experimental melanoma. Cancer Res 2006;66: 1261-4.
40. Otten MA, van der Bij GJ, Verbeek SJ, Nimmerjahn F, Ravetch JV, Beelen RH, et al. Experimental antibody therapy of liver metastases reveals functional redundancy between Fc gamma RI and Fc gamma RIV. J Immunol 2008;181:6829-36.
41. Mortha A, Chudnovskiy A, Hashimoto D, Bogunovic M, Spencer SP, Belkaid Y, et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014;343:1249288.
42. Gul N, Babes L, Siegmund K, Korthouwer R, Bogels M, Braster R, et al. Macrophages eliminate circulating tumor cells after monoclonal antibody therapy. J Clin Invest 2014;124:812-23.
43. Nimmerjahn F, Lux A, Albert H, Woigk M, Lehmann C, Dudziak D, et al. Fcgamma RIV deletion reveals its central role for IgG2a and IgG2b activity in vivo. Proc Natl Acad Sci U S A 2010;107:19396-401.
44. Nimmerjahn F, Bruhns P, Horiuchi K, Ravetch JV. FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 2005;23:41-51.
45. Park S, Jiang Z, Mortenson ED, Deng L, Radkevich-Brown O, Yang X, et al. The therapeutic effect of anti-HER2/neu antibody depends on both innate and adaptive immunity. Cancer Cell 2010;18:160-70.
46. Taylor C, Hershman D, Shah N, Suciu-Foca N, Petrylak DP, Taub R, et al. Augmented HER-2 specific immunity during treatment with trastuzumab and chemotherapy. Clin Cancer Res 2007;13:5133-43.
47. Weber JS, Kudchadkar RR, Yu B, Gallenstein D, Horak CE, Inzunza HD, et al. Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or-naive melanoma. J Clin Oncol 2013;31: 4311-8.
48. Gajewski TF, Woo SR, Zha Y, Spaapen R, Zheng Y, Corrales L, et al. Cancer immunotherapy strategies based on overcoming barriers within the tumor microenvironment. Curr Opin Immunol 2013;25:268-76.
49. Jacobs JJ, Snackey C, Geld of AA, Characiejus D, Van Moorselaar RJ, Den Otter W. Inefficacy of therapeutic cancer vaccines and proposed improvements. Casus of prostate cancer. Anticancer Res 2014;34:2689-700.
50. Henney AM, Decker RS. Production of a factor by cultured human heart valves that is immunologically related to interleukin 1. Cardiovascular Res 1987;21:21-7.
51. Vonarbourg C, Diefenbach A. Multifaceted roles of interleukin-7 signaling for the development and function of innate lymphoid cells. Sem Immunol 2012;24:165-74.
52. Takatori H, Kanno Y, Watford WT, Tato CM, Weiss G, Ivanov II, et al. Lymphoid tissue inducer-like cells are an innate source of IL-17 and IL-22. J Exp Med 2009;206:35-41.
53. Pallasch CP, Leskov I, Braun CJ, Vorholt D, Drake A, Soto-Feliciano YM, et al. Sensitizing protective tumor microenvironments to antibody-mediated therapy. Cell 2014;156:590-602.
54. van Spriel AB, van Ojik HH, Bakker A, Jansen MJ, van de Winkel JG. Mac-1 (CD11b/CD18) is crucial for effective Fc receptor-mediated immunity to melanoma. Blood 2003;101:253-8.
55. Hazenberg MD, Spits H. Human innate lymphoid cells. Blood 2014; 124:700-9.
56. 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;369:122-33.