Rationale for targeting the immune system through checkpoint molecule blockade in the treatment of non-small-cell lung cancer

Annals of Oncology

Volumn 24, Issue 5, 2013, Pages 1170-1179

  Zielinski, C ^a,b   Knapp, S ^b,c   Mascaux, C ^d   Hirsch, F ^d  

^a Central European Cooperative Oncology Group Austria   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^d UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

CTLA 4 blockade; Immunomodulators; Ipilimumab; Non small cell lung cancer; Squamous histology

Indexed keywords

ANTINEOPLASTIC AGENT; CANCER VACCINE; CARBOPLATIN; CORTICOSTEROID; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; ETOPOSIDE; IPILIMUMAB; IXABEPILONE; NIVOLUMAB; PACLITAXEL; PLACEBO; PLATINUM COMPLEX; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN TYROSINE KINASE INHIBITOR; TAXANE DERIVATIVE;

ADVANCED CANCER; ANTIGEN SPECIFICITY; APOPTOSIS; CANCER CHEMOTHERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER IMMUNIZATION; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CASTRATION RESISTANT PROSTATE CANCER; CHEMOTHERAPY INDUCED EMESIS; COLITIS; COLORECTAL CANCER; DIARRHEA; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; DYSPNEA; ENTEROCOLITIS; FATIGUE; HEPATITIS; HUMAN; HYPOPHYSITIS; HYPOTHYROIDISM; IMMUNE DEFICIENCY; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOSURVEILLANCE; LUNG CARCINOGENESIS; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; MELANOMA; MONOTHERAPY; MULTIPLE CYCLE TREATMENT; NAUSEA; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; REVIEW; SOLID TUMOR; THYROIDITIS; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; VITILIGO;

EID: 84877149232     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mds647     Document Type: Review

References (81)

1. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008; 359: 1367-1380.
2. World Health Organization Cancer. http://www.who.int/mediacentre/factsheets/fs297/en/index.html. (16 November 2011, date last accessed).
3. American Cancer Society. Cancer facts & figures 2011. http://www.cancer.org/acs/groups/content/@epidemiologysurveilance/documents/document/acspc-029771.pdf. (17 November 2011, date last accessed).
4. Brodowicz T, Ciuleanu T, Crawford J et al. Third CECOG consensus on the systemic treatment of non-small-cell lung cancer. Ann Oncol 2012; 23: 1223-1229.
5. D'Addario G, Felip E, ESMO Guidelines Working Group. Non-small-cell lung cancer: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 2009; 20(Suppl 4): 68-70.
6. D'Addario G, Früh M, Reck M et al. Metastatic non-small-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010; 21(Suppl 5): v116-v119.
7. Goldstraw P, Ball D, Jett JR et al. Non-small-cell lung cancer. Lancet 2011; 378: 1727-1740.
8. Travis WD, Travis LB, Devesa SS. Lung cancer. Cancer 1995; 75(Suppl 1): 191-202.
9. National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology. Non-small cell lung cancer, version 2.2012. http://www.nccn.org/professionals/physician_gls/f_guidelines.asp#nscl. (26 July 26 2011, date last accessed).
10. Scagliotti G, Hanna N, Fossella F et al. The differential efficacy of pemetrexed according to NSCLC histology: a review of two phase III studies. Oncologist 2009; 14: 253-263.
11. Johnson DH, Fehrenbacher L, Novotny WF et al. Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. J Clin Oncol 2004; 22: 2184-2191.
12. Travis WB, Brambilla E, Noguchi M et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society: international multidisciplinary classification of lung adenocarcinoma: executive summary. Proc Am Thorac Soc 2011; 8(5): 381-385.
13. Choi DR, Lee DH, Choi CM et al. Erlotinib in first-line therapy for non-small cell lung cancer: a prospective phase II study. Anticancer Res 2011; 31: 3457-3462.
14. Shukuya T, Takahashi T, Kaira R et al. Efficacy of gefitinib for nonadenocarcinoma non-small-cell lung cancer patients harboring epidermal growth factor receptor mutations: a pooled analysis of published reports. Cancer Sci 2011; 102: 1032-1037.
15. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
16. Karabon L, Pawlak E, Tomkiewicz A et al. CTLA-4, CD28, and ICOS gene polymorphism associations with non-small-cell lung cancer. Hum Immunol 2011; 72: 947-954.
17. Zhang Y, Zhang J, Deng Y et al. Polymorphisms in the cytotoxic T-lymphocyte antigen 4 gene and cancer risk: a meta-analysis. Cancer 2011; 117: 4312-4324.
18. Topalian SL, Hodi FS, Brahmer JR et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366: 2443-2454.
19. Kim R, Emi M, Tanabe K. Cancer immunoediting from immune surveillance to immune escape. Immunology 2007; 121: 1-14.
20. Dranoff G. Cytokines in cancer pathogenesis and cancer therapy. Nat Rev Cancer 2004; 4: 11-22.
21. Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006; 90: 51-81.
22. Lee JC, Lee KM, Kim DW et al. Elevated TGF-ß1 and down-modulation of NKG2D underlies impaired NK cytotoxicity in cancer patients. J Immunol 2004; 172: 7335-7340.
23. Gancz D, Fishelson Z. Cancer resistance to complement-dependent cytotoxicity (CDC): problem-oriented research and development. Mol Immunol 2009; 46: 2794-2800.
24. Nagata S. Fas ligand and immune evasion. Nat Med 1996; 2: 1306-1307.
25. Schimmer AD. Inhibitor of apoptosis proteins: translating basic knowledge into clinical practice. Cancer Res 2004; 64: 7183-7190.
26. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 2006; 6: 295-307.
27. de Jong RA, Leffers N, Boezen HM et al. Presence of tumor-infiltrating lymphocytes is an independent prognostic factor in type I and II endometrial cancer. Gynecol Oncol 2009; 114: 105-110.
28. Leffers N, Gooden MJM, de Jong RA et al. Prognostic significance of tumorinfiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother 2009; 58: 449-459.
29. Zhuang X, Xia X, Wang C et al. A high number of CD8+ T cells infiltrated in NSCLC tissues is associated with a favorable prognosis. Appl Immunohistochem Mol Morphol 2010; 18: 24-28.
30. Petersen RP, Campa MJ, Sperlazza J et al. Tumor infiltrating FOXP3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer 2006; 107: 2866-2872.
31. Zamarron BF, Chen W. Dual roles of immune cells and their factors in cancer development and progression. Int J Biol Sci 2011; 7: 651-658.
32. Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 2007; 25: 267-296.
33. Mantovani A, Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 2010; 22: 231-237.
34. Dy GK, Adjei AA. Emerging therapeutic targets in non-small cell lung cancer. Proc Am Thorac Soc 2009; 6: 218-23.
35. Bremnes RM, Al-Shibli K, Donnem T et al. The role of tumor-infiltrating immune cells and chronic inflammation at the tumor site on cancer development, progression, and prognosis: emphasis on non-small cell lung cancer. J Thorac Oncol 2011; 6: 824-833.
36. Dieu-Nosjean MC, Antoine M, Danel C et al. Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008; 26: 4410-4417.
37. Hiraoka K, Miyamoto M, Cho Y et al. Concurrent infiltration by CD8+ T cells and CD4+ T cells is a favourable prognostic factor in non-small-cell lung carcinoma. Br J Cancer 2006; 94: 275-280.
38. Al-Shibli KI, Donnem T, Al-Saad S et al. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008; 14: 5220-5227.
39. Kawai O, Ishii G, Kubota K et al. Predominant infiltration of macrophages and CD8(+) T cells in cancer nests is a significant predictor of survival in stage IV nonsmall cell lung cancer. Cancer 2008; 113: 1387-1395.
40. Woo EY, Yeh H, Chu CS et al. Cutting edge: regulatory T-cells from lung cancer patients directly inhibit autologous T cell proliferation. J Immunology 2002; 168: 4272-4276.
41. Chen W, Jin W, Hardegen N et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 2003; 198: 1875-1886.
42. Walker MR, Kasprowicz DJ, Gersuk VH et al. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J Clin Invest 2003; 112: 1437-1443.
43. Sharma S, Yang SC, Zhu L et al. Tumor cyclooxygenase-2/prostaglandin E2-dependent promotion of FoxP3 expression and CD4+CD25+ T regulatory cell activities in lung cancer. Cancer Res 2005; 65: 5211-5220.
44. Wolf D, Wolf AM, Rumpold H et al. The expression of the regulatory T cellspecific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin Cancer Res 2005; 11: 8326-8331.
45. Rekhtman N, Ang DC, Sima CS et al. Immunohistochemical algorithm for differentiation of lung adenocarcinoma and squamous cell carcinoma based on large series of whole-tissue sections with validation in small specimens. Mod Pathol 2011; 24: 1348-1359.
46. Bolli M, Kocher T, Adamina M et al. Tissue microarray evaluation of melanoma antigen E (MAGE) tumor-associated antigen expression: potential indications for specific immunotherapy and prognostic relevance in squamous cell lung carcinoma. Ann Surg 2002; 236: 785-793.
47. Kim J-H, Zo JI, Nakayama H et al. Patient and tumor characteristics impacting on MAGE-A3 expression: screening data from the MAGRIT phase III trial. Presented at the 2011 World Congress of Lung Cancer; July 3-7, 2011; Amsterdam, Netherlands. Session MO21.
48. Yoshida N, Abe H, Ohkuri T et al. Expression of the MAGE-A4 and NY-ESO-1 cancer-testis antigens and T cell infiltration in non-small cell lung carcinoma and their prognostic significance. Int J Oncol 2006; 28: 1089-1098.
49. Kim SH, Lee S, Lee CH et al. Expression of cancer-testis antigens MAGE-A3/6 and NY-ESO-1 in non-small-cell lung carcinomas and their relationship with immune cell infiltration. Lung 2009; 187: 401-411.
50. Suzuki K, Kachala SS, Kadota K et al. Prognostic immune markers in non-small cell lung cancer. Clin Cancer Res 2011; 17: 524-5256.
51. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005; 5: 263-274.
52. Lipson EJ, Drake CG. Ipilimumab: an anti-CTLA-4 antibody for metastatic melanoma. Clin Cancer Res 2011; 17: 6958-6962.
53. Pentcheva-Hoang T, Corse E, Allison JP. Negative regulators of T-cell activation: potential targets for therapeutic intervention in cancer, autoimmune disease, and persistent infections. Immunol Rev 2009; 229: 67-87.
54. Nishimura H, Nose M, Hiai H et al. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999; 11: 141-151.
55. Okazaki T, Honjo T. PD-1 and PD-1 ligands: from discovery to clinical application. Int Immunol 2007; 19: 813-824.
56. Jin HT, Ahmed R, Okazaki T. Role of PD-1 in regulating T-cell immunity. Curr Top Microbiol Immunol 2011; 350: 17-37.
57. Salama AK, Hodi FS. Cytotoxic T-lymphocyte-associated antigen-4. Clin Cancer Res 2011; 17: 4622-4628.
58. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev 2008; 224: 166-182.
59. Fife BT, Guleria I, Gubbels Bupp M et al. Insulin-induced remission in new-onset NOD mice is maintained by the PD-1-PD-L1 pathway. J Exp Med 2006; 203: 2737-2747.
60. Tivol EA, Borriello F, Schweitzer AN et al. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995; 3: 541-547.
61. Song B, Liu Y, Liu J et al. CTLA-4 +49A>G polymorphism Is associated with advanced non-small cell lung cancer prognosis. Respiration 2011; 82: 439-444.
62. Holt GE, Podack ER, Raez LE. Immunotherapy as a strategy for the treatment of non-small-cell lung cancer. Therapy 2011; 8: 43-54.
63. Shepherd FA, Douillard JY, Blumenschein GR, Jr. Immunotherapy for non-small cell lung cancer: novel approaches to improve patient outcome. J Thorac Oncol 2011; 6: 1763-1773.
64. Peggs KS, Quezada SA, Chambers CA et al. Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med 2009; 206: 1717-1725.
65. Peggs KS, Quezada SA, Korman AJ et al. Principles and use of anti-CTLA4 antibody in human cancer immunotherapy. Curr Opin Immunol 2006; 18: 206-213.
66. Jure-Kunkel MN, Masters G, Girit E et al. Antitumor activity of anti-CTLA-4 monoclonal antibody (mAb) in combination with ixabepilone in preclinical tumor models. J Clin Oncol 2008; 26(20 suppl): Abstr 3048.
67. Masters G, Barreto L, Girit E et al. Antitumor activity of cytotoxic T-lymphocyte antigen-4 blockade alone or combined with paclitaxel, etoposide, or gemcitabine in murine models. Presented at the 24th Annual Meeting of the International Society for Biological Therapy of Cancer, Washington DC, USA; October 29-31, 2009. J Immunother 2009; 32: 994.
68. Yervoy™ (ipilimumab) [prescribing information]. Princeton, NJ: Bristol-Myers Squibb; 2011.
69. Hodi FS, O'Day SJ, McDermott DF et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010; 363: 711-723.
70. Robert C, Thomas L, Bondarenko I et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011; 364: 2517-2526.
71. Fong L, Small EJ. Anti-cytotoxic T-lymphocyte antigen-4antibody: the first in an emerging class of immunomodulatory antibodies for cancer treatment. J Clin Oncol 2008; 26: 5275-5283.
72. Wolchok JD, Hoos A, O'Day S et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009; 15: 7412-7420.
73. Hoos A, Ibrahim R, Korman A et al. Development of ipilimumab: contribution to a new paradigm for cancer immunotherapy. Semin Oncol 2010; 37: 533-546.
74. Hoos A, Eggermont AM, Janetzki S et al. Improved endpoints for cancer immunotherapy trials. J Natl Cancer Inst 2010; 102: 1388-1397.
75. Tesniere A, Apetoh L, Ghiringhelli F et al. Immunogenic cancer cell death: a keylock paradigm. Curr Opin Immunol 2008; 20: 504-511.
76. Ramakrishnan R, Assudani D, Nagaraj S et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest 2010; 120: 1111-1124.
77. Masters G, Barreto L, Girit E et al. Antitumor activity of cytotoxic T-lymphocyte antigen-4 blockade alone or combined with paclitaxel, etoposide or gemcitabine in murine models. J Immunother 2009; 32: 994.
78. Calabrò L, Danielli R, Sigalotti L et al. Clinical studies with anti-CTLA-4 antibodies in non-melanoma indications. Semin Oncol 2010; 37: 460-467.
79. Lynch TJ, Bondarenko I, Luft A et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol 2012; 30: 2046-2054.
80. Tomasini P, Khobta N, Greillier L et al. Ipilimumab: its potential in non-small cell lung cancer. Ther Adv Med Oncol 2012; 4: 43-50.
81. Lynch T, Bondarenko I, Luft A et al. Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in non-small cell lung cancer: analysis by baseline histology in a phase 2 trial. Presented at the 2011 World Congress of Lung Cancer; July 3-7; Amsterdam, Netherlands.