Immunotherapy in the treatment of non-small cell lung cancer

Lung Cancer

Volumn 85, Issue 2, 2014, Pages 101-109

  Sundar, Raghav ^a   Soong, Richie ^a,b   Cho, Byoung Chul ^c   Brahmer, Julie R ^d   Soo, Ross A ^a,b,e  

^a NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c Yonsei University College of Medicine   (South Korea)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

CTLA 4; Immunotherapy; Ipilimumab; Nivolumab; Non small cell lung cancer; PD L1

Indexed keywords

ADENOSINE A2A RECEPTOR; BIOLOGICAL MARKER; BMS 936559; BMS 986016; CD134 ANTIGEN; CD137 LIGAND; CD27 ANTIGEN; CD28 ANTIGEN; CD40 LIGAND; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DOCETAXEL; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INDUCIBLE T CELL COSTIMULATOR; IPILIMUMAB; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LAG3 PROTEIN; LIRILUMAB; MEDI 4736; MONOCLONAL ANTIBODY; MPDL 3280A; MSB 0010718C; NIVOLUMAB; PEMBROLIZUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN; TICILIMUMAB; TIM3 PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; PROTEIN BINDING; T LYMPHOCYTE RECEPTOR;

CANCER IMMUNOTHERAPY; DRUG RESPONSE; HUMAN; IMMUNE RESPONSE; LUNG NON SMALL CELL CANCER; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN INTERACTION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; ANIMAL; CARCINOMA, NON-SMALL-CELL LUNG; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LUNG NEOPLASMS; METABOLISM;

ANIMALS; ANTIBODIES, MONOCLONAL; CARCINOMA, NON-SMALL-CELL LUNG; CARRIER PROTEINS; COSTIMULATORY AND INHIBITORY T-CELL RECEPTORS; HUMANS; IMMUNOTHERAPY; LUNG NEOPLASMS; PROTEIN BINDING;

EID: 84904112296     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2014.05.005     Document Type: Review

References (104)

1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90.
2. Mok T.S., Wu Y.L., Thongprasert S., Yang C.H., Chu D.T., Saijo N., et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 2009, 361:947-957.
3. Pao W., Girard N. New driver mutations in non-small-cell lung cancer. Lancet Oncol 2011, 12:175-180.
4. Schiller J.H., Morgan-Ihrig C., Levitt M.L. Concomitant administration of interleukin-2 plus tumor necrosis factor in advanced non-small cell lung cancer. Am J Clin Oncol 1995, 18:47-51.
5. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
6. Einhorn L.H., Bond W.H., Hornback N., Joe B.T. Long-term results in combined-modality treatment of small cell carcinoma of the lung. Semin Oncol 1978, 5:309-313.
7. Jansen R.L., Slingerland R., Goey S.H., Franks C.R., Bolhuis R.L., Stoter G. Interleukin-2 and interferon-alpha in the treatment of patients with advanced non-small-cell lung cancer. J Immunother (1991) 1992, 12:70-73.
8. Butts C., Socinski M.A., Mitchell P.L., Thatcher N., Havel L., Krzakowski M., et al. Tecemotide (L-BLP25) versus placebo after chemoradiotherapy for stage III non-small-cell lung cancer (START): a randomised, double-blind, phase 3 trial. Lancet Oncol 2014, 15:59-68.
9. Giaccone G., Bazhenova L., Nemunaitis J., Juhasz E., Ramlau R., van den Heuvel M., et al. A phase III study of belagenpumatucel-L therapeutic tumor cell vaccine for non-small cell lung cancer. European Cancer Congress 2013, Abstract LBA 2.
10. Media release Investigational MAGE-A3 antigen-specific cancer immunotherapeutic does not meet first co-primary endpoints in MAGRIT, a phase III non-small cell lung cancer clinical trial 2014, (accessed 30.03.14). http://www.gsk.com/media/press-releases/2014/investigational-MAGE-A3-antigen-specific-cancer-immunotherapeutic-does-not-meet-first-co-primary-endpoints-in-MAGRIT.html.
11. Mellstedt H., Vansteenkiste J., Thatcher N. Vaccines for the treatment of non-small cell lung cancer: investigational approaches and clinical experience. Lung Cancer 2011, 73:11-17.
12. O'Day S.J., Hamid O., Urba W.J. Targeting cytotoxic T-lymphocyte antigen-4 (CTLA-4): a novel strategy for the treatment of melanoma and other malignancies. Cancer 2007, 110:2614-2627.
13. Keir M.E., Butte M.J., Freeman G.J., Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008, 26:677-704.
14. Nishimura H., Honjo T. PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol 2001, 22:265-268.
15. Roth C.G., Garner K., Eyck S.T., Boyiadzis M., Kane L.P., Craig F.E. TIM3 expression by leukemic and non-leukemic myeloblasts. Cytometry B Clin Cytom 2013, 84:167-172.
16. Wada J., Kanwar Y.S. Identification and characterization of galectin-9, a novel beta-galactoside-binding mammalian lectin. J Biol Chem 1997, 272:6078-6086.
17. Sega E.I., Leveson-Gower D.B., Florek M., Schneidawind D., Luong R.H., Negrin R.S. Role of lymphocyte activation gene-3 (lag-3) in conventional and regulatory T cell function in allogeneic transplantation. PLOS ONE 2014, 9:e86551.
18. Watanabe N., Gavrieli M., Sedy J.R., Yang J., Fallarino F., Loftin S.K., et al. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol 2003, 4:670-679.
19. Pasero C., Olive D. Interfering with coinhibitory molecules: BTLA/HVEM as new targets to enhance anti-tumor immunity. Immunol Lett 2013, 151:71-75.
20. Lee C.F., Lai H.L., Lee Y.C., Chien C.L., Chern Y. The A2A adenosine receptor is a dual coding gene: a novel mechanism of gene usage and signal transduction. J Biol Chem 2014, 289:1257-1270.
21. Sica G.L., Choi I.H., Zhu G., Tamada K., Wang S.D., Tamura H., et al. B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 2003, 18:849-861.
22. Kohrt H.E., Thielens A., Marabelle A., Sagiv-Barfi I., Sola C., Chanuc F., et al. Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies. Blood 2014, 123:678-686.
23. Farres M.N., Sabry M.K., Ahmed E.E., Elkady H.M., Mohamed N.A. OX40 ligand: a potential costimulatory molecule in atopic asthma. J Asthma 2014, [Epub ahead of print], PMID: 24580371.
24. Shao Z., Schwarz H. CD137 ligand, a member of the tumor necrosis factor family, regulates immune responses via reverse signal transduction. J Leukoc Biol 2011, 89:21-29.
25. Chatzigeorgiou A., Lyberi M., Chatzilymperis G., Nezos A., Kamper E. CD40/CD40L signaling and its implication in health and disease. Biofactors 2009, 35:474-483.
26. Viac J., Schmitt D., Claudy A. CD40 expression in epidermal tumors. Anticancer Res 1997, 17:569-572.
27. Prasad K.V., Ao Z., Yoon Y., Wu M.X., Rizk M., Jacquot S., et al. CD27, a member of the tumor necrosis factor receptor family, induces apoptosis and binds to Siva, a proapoptotic protein. Proc Natl Acad Sci U S A 1997, 94:6346-6351.
28. Nocentini G., Ronchetti S., Cuzzocrea S., Riccardi C. GITR/GITRL: more than an effector T cell co-stimulatory system. Eur J Immunol 2007, 37:1165-1169.
29. Yoshinaga S.K., Whoriskey J.S., Khare S.D., Sarmiento U., Guo J., Horan T., et al. T-cell co-stimulation through B7RP-1 and ICOS. Nature 1999, 402:827-832.
30. Woerly G., Roger N., Loiseau S., Dombrowicz D., Capron A., Capron M. Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon gamma): inhibition by immunoglobulin a complexes. J Exp Med 1999, 190:487-495.
31. Chambers C.A., Kuhns M.S., Egen J.G., Allison J.P. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu Rev Immunol 2001, 19:565-594.
32. Thompson C.B., Allison J.P. The emerging role of CTLA-4 as an immune attenuator. Immunity 1997, 7:445-450.
33. Waterhouse P., Penninger J.M., Timms E., Wakeham A., Shahinian A., Lee K.P., et al. Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 1995, 270:985-988.
34. Salvi S., Fontana V., Boccardo S., Merlo D.F., Margallo E., Laurent S., et al. Evaluation of CTLA-4 expression and relevance as a novel prognostic factor in patients with non-small cell lung cancer. Cancer Immunol Immunother 2012, 61:1463-1472.
35. Zheng H., Li Y., Wang X., Zhang X., Wang X. Expression and significance of gp96 and immune-related gene CTLA-4, CD8 in lung cancer tissues. Zhongguo Fei Ai Za Zhi 2010, 13:790-794.
36. Lynch T.J., Bondarenko I., Luft A., Serwatowski P., Barlesi F., Chacko R., 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.
37. Zatloukal P., Heo D.S., Park K., Kang J., Butts C., Bradford D., et al. Randomized phase II clinical trial comparing tremelimumab (CP-675,206) with best supportive care (BSC) following first-line platinum-based therapy in patients (pts) with advanced non-small cell lung cancer (NSCLC). J Clin Oncol 2009, 27. (suppl; abstr 15S, 8071).
38. Ahmadzadeh M., Johnson L.A., Heemskerk B., Wunderlich J.R., Dudley M.E., White D.E., et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 2009, 114:1537-1544.
39. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012, 366:2443-2454.
40. Brahmer J., Horn L., Antonia S., Spigel D., Gandhi L., Sequist L., et al. Nivolumab (anti-PD-1; BMS-936558; ONO-4538) in patients with non-small cell lung cancer (NSCLC): overall survival and long-term safety in a phase 1 trial. IASLC 15th World Conference on Lung Cancer 2013, Abstract MO18.03.
41. Antonia S., Grosso J., Horak C., Harbison C., Kurland J., Inzunza D., et al. Association of tumor PD-L1 expression and immune biomarkers with clinical activity in patients with non-small cell lung cancer treated with nivolumab. IASLC 15th World Conference on Lung Cancer 2013, Abstract P2.11-035.
42. Hamid O., Robert C., Daud A., Hodi F.S., Hwu W.J., Kefford R., et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013, 369:134-144.
43. Garon E., Balmanoukian A., Hamid O., Hui R., Gandhi L., Leighi N., et al. Preliminary clinical safety and activity of MK-3475 mono-therapy for the treatment of previously treated patients with non-small cell lung cancer. IASLC 15th World Conference on Lung Cancer 2013, Abstract MO18.02.
44. Dong H., Strome S.E., Salomao D.R., Tamura H., Hirano F., Flies D.B., et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002, 8:793-800.
45. Yang C.Y., Lin M.W., Chang Y.L., Wu C.T., Yang P.C. Programmed cell death-ligand 1 expression in surgically resected stage I pulmonary adenocarcinoma and its correlation with driver mutations and clinical outcomes. Eur J Cancer 2014, 50:1361-1369.
46. Velcheti V., Schalper K.A., Carvajal D.E., Anagnostou V.K., Syrigos K.N., Sznol M., et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest 2014, 94:107-116.
47. Chen Y.Y., Wang L.B., Zhu H.L., Li X.Y., Zhu Y.P., Yin Y.L., et al. Relationship between programmed death-ligand 1 and clinicopathological characteristics in non-small cell lung cancer patients. Chin Med Sci J 2013, 28:147-151.
48. Chen Y.B., Mu C.Y., Huang J.A. Clinical significance of programmed death-1 ligand-1 expression in patients with non-small cell lung cancer: a 5-year-follow-up study. Tumori 2012, 98:751-755.
49. Boland J.M., Kwon E.D., Harrington S.M., Wampfler J.A., Tang H., Yang P., et al. Tumor B7-H1 and B7-H3 expression in squamous cell carcinoma of the lung. Clin Lung Cancer 2013, 14:157-163.
50. Mu C.Y., Huang J.A., Chen Y., Chen C., Zhang X.G. High expression of PD-L1 in lung cancer may contribute to poor prognosis and tumor cells immune escape through suppressing tumor infiltrating dendritic cells maturation. Med Oncol 2011, 28:682-688.
51. Konishi J., Yamazaki K., Azuma M., Kinoshita I., Dosaka-Akita H., Nishimura M. B7-H1 expression on non-small cell lung cancer cells and its relationship with tumor-infiltrating lymphocytes and their PD-1 expression. Clin Cancer Res 2004, 10:5094-5100.
52. Velcheti V., Rimm D.L., Schalper K.A. Sarcomatoid lung carcinomas show high levels of programmed death ligand-1 (PD-L1). J Thorac Oncol 2013, 8:803-805.
53. Brahmer J.R., Tykodi S.S., Chow L.Q., Hwu W.J., Topalian S.L., 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.
54. Soria J., Cruz C., Bahleda R., Delord J., Horn L., Herbst R., et al. Clinical activity, safety and biomarkers of PD-L1 blockade in non-small cell lung cancer (NSCLC): additional analyses from a clinical study of the engineered antibody MPDL3280A (anti-PDL1). European Cancer Congress 2013, Abstract 3408.
55. Khleif S., Lutzky J., Segal N., Antonia S., Blake-Haskins A., Stewart R., et al. MEDI4736, an anti-PD-L1 antibody with modified Fc domain: preclinical evaluation and early clinical results from a phase 1 study in patients with advanced solid tumors. European Cancer Congress 2013, Abstract 802.
56. Monney L., Sabatos C.A., Gaglia J.L., Ryu A., Waldner H., Chernova T., et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 2002, 415:536-541.
57. Zhu C., Anderson A.C., Schubart A., Xiong H., Imitola J., Khoury S.J., et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 2005, 6:1245-1252.
58. Sabatos C.A., Chakravarti S., Cha E., Schubart A., Sanchez-Fueyo A., Zheng X.X., et al. Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat Immunol 2003, 4:1102-1110.
59. Sakuishi K., Apetoh L., Sullivan J.M., Blazar B.R., Kuchroo V.K., Anderson A.C. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 2010, 207:2187-2194.
60. Fourcade J., Sun Z., Benallaoua M., Guillaume P., Luescher I.F., Sander C., et al. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med 2010, 207:2175-2186.
61. Gao X., Zhu Y., Li G., Huang H., Zhang G., Wang F., et al. TIM-3 expression characterizes regulatory T cells in tumor tissues and is associated with lung cancer progression. PLoS ONE 2012, 7:e30676.
62. Zhuang X., Zhang X., Xia X., Zhang C., Liang X., Gao L., et al. Ectopic expression of TIM-3 in lung cancers: a potential independent prognostic factor for patients with NSCLC. Am J Clin Pathol 2012, 137:978-985.
63. Zhou Q., Munger M.E., Veenstra R.G., Weigel B.J., Hirashima M., Munn D.H., et al. Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood 2011, 117:4501-4510.
64. Ngiow S.F., von Scheidt B., Akiba H., Yagita H., Teng M.W., Smyth M.J. Anti-TIM3 antibody promotes T cell IFN-gamma-mediated antitumor immunity and suppresses established tumors. Cancer Res 2011, 71:3540-3551.
65. Huang C.T., Workman C.J., Flies D., Pan X., Marson A.L., Zhou G., et al. Role of LAG-3 in regulatory T cells. Immunity 2004, 21:503-513.
66. Gandhi M.K., Lambley E., Duraiswamy J., Dua U., Smith C., Elliott S., et al. Expression of LAG-3 by tumor-infiltrating lymphocytes is coincident with the suppression of latent membrane antigen-specific CD8+ T-cell function in Hodgkin lymphoma patients. Blood 2006, 108:2280-2289.
67. Freire J., Ajona D., de Biurrun G., Agorreta J., Segura V., Guruceaga E., et al. Silica-induced chronic inflammation promotes lung carcinogenesis in the context of an immunosuppressive microenvironment. Neoplasia 2013, 15:913-924.
68. Ruggeri L., Capanni M., Urbani E., Perruccio K., Shlomchik W.D., Tosti A., et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002, 295:2097-2100.
69. Romagne F., Andre P., Spee P., Zahn S., Anfossi N., Gauthier L., et al. Preclinical characterization of 1-7F9, a novel human anti-KIR receptor therapeutic antibody that augments natural killer-mediated killing of tumor cells. Blood 2009, 114:2667-2677.
70. Al Omar S., Middleton D., Marshall E., Porter D., Xinarianos G., Raji O., et al. Associations between genes for killer immunoglobulin-like receptors and their ligands in patients with solid tumors. Hum Immunol 2010, 71:976-981.
71. Gertner-Dardenne J., Fauriat C., Orlanducci F., Thibult M.L., Pastor S., Fitzgibbon J., et al. The co-receptor BTLA negatively regulates human Vgamma9Vdelta2 T-cell proliferation: a potential way of immune escape for lymphoma cells. Blood 2013, 122:922-931.
72. Paterson D.J., Jefferies W.A., Green J.R., Brandon M.R., Corthesy P., Puklavec M., et al. Antigens of activated rat T lymphocytes including a molecule of 50,000 Mr detected only on CD4 positive T blasts. Mol Immunol 1987, 24:1281-1290.
73. Gramaglia I., Weinberg A.D., Lemon M., Croft M. Ox-40 ligand: a potent costimulatory molecule for sustaining primary CD4 T cell responses. J Immunol 1998, 161:6510-6517.
74. Sugamura K., Ishii N., Weinberg A.D. Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat Rev Immunol 2004, 4:420-431.
75. Weinberg A.D., Rivera M.M., Prell R., Morris A., Ramstad T., Vetto J.T., et al. Engagement of the OX-40 receptor in vivo enhances antitumor immunity. J Immunol 2000, 164:2160-2169.
76. Morris A., Vetto J.T., Ramstad T., Funatake C.J., Choolun E., Entwisle C., et al. Induction of anti-mammary cancer immunity by engaging the OX-40 receptor in vivo. Breast Cancer Res Treat 2001, 67:71-80.
77. Ali S.A., Ahmad M., Lynam J., McLean C.S., Entwisle C., Loudon P., et al. Anti-tumour therapeutic efficacy of OX40L in murine tumour model. Vaccine 2004, 22:3585-3594.
78. Sadun R.E., Hsu W.E., Zhang N., Nien Y.C., Bergfeld S.A., Sabzevari H., et al. Fc-mOX40L fusion protein produces complete remission and enhanced survival in 2 murine tumor models. J Immunother 2008, 31:235-245.
79. Redmond W.L., Gough M.J., Weinberg A.D. Ligation of the OX40 co-stimulatory receptor reverses self-Ag and tumor-induced CD8 T-cell anergy in vivo. Eur J Immunol 2009, 39:2184-2194.
80. Curti B.D., Kovacsovics-Bankowski M., Morris N., Walker E., Chisholm L., Floyd K., et al. OX40 is a potent immune-stimulating target in late-stage cancer patients. Cancer Res 2013, 73:7189-7198.
81. Morris N.P., Peters C., Montler R., Hu H.M., Curti B.D., Urba W.J., et al. Development and characterization of recombinant human Fc:OX40L fusion protein linked via a coiled-coil trimerization domain. Mol Immunol 2007, 44:3112-3121.
82. Wilcox R.A., Flies D.B., Zhu G., Johnson A.J., Tamada K., Chapoval A.I., et al. Provision of antigen and CD137 signaling breaks immunological ignorance, promoting regression of poorly immunogenic tumors. J Clin Invest 2002, 109:651-659.
83. Ascierto P.A., Marincola F.M., Ribas A. Anti-CTLA4 monoclonal antibodies: the past and the future in clinical application. J Transl Med 2011, 9:196.
84. Sznol M., Hodi F.S., Margolin K., McDermott D.F., Ernstoff M.S., Kirkwood J.M., et al. Phase I study of BMS-663513, a fully human anti-CD137 agonist monoclonal antibody, in patients (pts) with advanced cancer (CA). J Clin Oncol 2008, 26. (suppl; abstr 3007).
85. Ronchetti S., Nocentini G., Riccardi C., Pandolfi P.P. Role of GITR in activation response of T lymphocytes. Blood 2002, 100:350-352.
86. Arnett S.O., Teillaud J.L., Wurch T., Reichert J.M., Dunlop C., Huber M. IBC's 21st annual antibody engineering and 8th annual antibody therapeutics international conferences and 2010 annual meeting of the antibody society. December 5-9, 2010, San Diego, CA, USA. MAbs 2011, 3:133-152.
87. Sabel M.S., Yamada M., Kawaguchi Y., Chen F.A., Takita H., Bankert R.B. CD40 expression on human lung cancer correlates with metastatic spread. Cancer Immunol Immunother 2000, 49:101-108.
88. von Scheidt B., Leung P.S., Yong M.C., Zhang Y., Towne J.E., Smyth M.J., et al. Combined anti-CD40 and anti-IL-23 monoclonal antibody therapy effectively suppresses tumor growth and metastases. Cancer Res 2014, 74:2412-2421.
89. Hutloff A., Dittrich A.M., Beier K.C., Eljaschewitsch B., Kraft R., Anagnostopoulos I., et al. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999, 397:263-266.
90. Suntharalingam G., Perry M.R., Ward S., Brett S.J., Castello-Cortes A., Brunner M.D., et al. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med 2006, 355:1018-1028.
91. Delbaldo C., Michiels S., Syz N., Soria J.C., Le Chevalier T., Pignon J.P. Benefits of adding a drug to a single-agent or a 2-agent chemotherapy regimen in advanced non-small-cell lung cancer: a meta-analysis. JAMA 2004, 292:470-484.
92. Herbst R.S., Prager D., Hermann R., Fehrenbacher L., Johnson B.E., Sandler A., et al. TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small-cell lung cancer. J Clin Oncol 2005, 23:5892-5899.
93. Hodi F.S., Butler M., Oble D.A., Seiden M.V., Haluska F.G., Kruse A., et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc Natl Acad Sci U S A 2008, 105:3005-3010.
94. Curran M.A., Montalvo W., Yagita H., Allison J.P. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc Natl Acad Sci USA 2010, 107:4275-4280.
95. Callahan M.K., Wolchok J.D., Allison J.P. Anti-CTLA-4 antibody therapy: immune monitoring during clinical development of a novel immunotherapy. Semin Oncol 2010, 37:473-484.
96. Berman D.M., Wolchok J., Weber J., Hamid O., O'Day S., Chasalow S.D. Association of peripheral blood absolute lymphocyte count (ALC) and clinical activity in patients (pts) with advanced melanoma treated with ipilimumab. J Clin Oncol 2009, 27. (suppl; abstr 3020).
97. Liakou C.I., Kamat A., Tang D.N., Chen H., Sun J., Troncoso P., et al. CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients. Proc Natl Acad Sci U S A 2008, 105:14987-14992.
98. Phan G.Q., Yang J.C., Sherry R.M., Hwu P., Topalian S.L., Schwartzentruber D.J., et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci U S A 2003, 100:8372-8377.
99. Maker A.V., Yang J.C., Sherry R.M., Topalian S.L., Kammula U.S., Royal R.E., et al. Intrapatient dose escalation of anti-CTLA-4 antibody in patients with metastatic melanoma. J Immunother 2006, 29:455-463.
100. Hamid O., Schmidt H., Nissan A., Ridolfi L., Aamdal S., Hansson J., et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J Transl Med 2011, 9:204.
101. Taube J.M., Anders R.A., Young G.D., Xu H., Sharma R., McMiller T.L., et al. Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape. Sci Transl Med 2012, 4:127ra37.
102. Eisenhauer E.A., Therasse P., Bogaerts J., Schwartz L.H., Sargent D., Ford R., et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009, 45:228-247.
103. Wolchok J.D., Hoos A., O'Day S., Weber J.S., Hamid O., Lebbe 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.
104. Oxnard G.R., Morris M.J., Hodi F.S., Baker L.H., Kris M.G., Venook A.P., et al. When progressive disease does not mean treatment failure: reconsidering the criteria for progression. J Natl Cancer Inst 2012, 104:1534-1541.