Oncology meets immunology: The cancer-immunity cycle

Immunity

Volumn 39, Issue 1, 2013, Pages 1-10

  Chen, Daniel S ^a,c   Mellman, Ira ^b,c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMP 224; ANTINEOPLASTIC AGENT; LAMBROLIZUMAB; MEDI 4736; MEMBRANE PROTEIN; MPDL 320 A; MPDL 3280A; NIVOLUMAB; PD L1 PROTEIN; PIDILIZUMAB; PROGRAMMED DEATH 1 RECEPTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ADOPTIVE IMMUNOTHERAPY; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTINEOPLASTIC ACTIVITY; AUTOIMMUNITY; CANCER CELL; CANCER GENETICS; CANCER IMMUNIZATION; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER THERAPY; CROSS PRESENTATION; HUMAN; INHIBITION KINETICS; LUNG CANCER; LYMPHOCYTE ACTIVATION; LYMPHOCYTE MIGRATION; LYMPHOCYTIC INFILTRATION; MELANOMA; MOLECULAR RECOGNITION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

CYTOKINES; HUMANS; IMMUNITY; IMMUNOTHERAPY; MODELS, IMMUNOLOGICAL; NEOPLASMS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT;

EID: 84880706152     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2013.07.012     Document Type: Review

References (84)

1. Boon T., Cerottini J.C., Van den Eynde B., van der Bruggen P., Van Pel A. Tumor antigens recognized by T lymphocytes. Annu. Rev. Immunol. 1994, 12:337-365.
2. Brahmer J.R., Drake C.G., Wollner I., Powderly J.D., Picus J., Sharfman W.H., Stankevich E., Pons A., Salay T.M., McMiller T.L., et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J.Clin. Oncol. 2010, 28:3167-3175.
3. Brahmer J.R., Horn L., Antonia S.J., Spigel D.R., Gandhi L., Sequist L.V., Sankar V., Ahlers C.M., Wigginton J.M., Kollia G., et al. Survival and long-term follow-up of the phase I trial of nivolumab (Anti-PD-1; BMS-936558; ONO-4538) in patients (pts) with previously treated advanced non-small cell lung cancer (NSCLC). J.Clin. Oncol. 2013, 31(suppl):8030.
4. Brestoff J.R., Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 2013, 14:676-684.
5. Bulgaru A.M., Mani S., Goel S., Perez-Soler R. Erlotinib (Tarceva): a promising drug targeting epidermal growth factor receptor tyrosine kinase. Expert Rev. Anticancer Ther. 2003, 3:269-279.
6. Chemnitz J.M., Parry R.V., Nichols K.E., June C.H., Riley J.L. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human Tcell stimulation, but only receptor ligation prevents Tcell activation. J.Immunol. 2004, 173:945-954.
7. Chen D.S., Irving B.A., Hodi F.S. Molecular pathways: next-generation immunotherapy-inhibiting programmed death-ligand 1 and programmed death-1. Clin. Cancer Res. 2012, 18:6580-6587.
8. Cho D.C., Sosman J.A., Sznol M., Gordon M.S., Hollebecque A., Hamid O., McDermott D.F., Delord J.-P., Rhee I.P., Mokatrin A., et al. Clinical activity, safety, and biomarkers of MPDL3280A, an engineered PD-L1 antibody in patients with metastatic renal cell carcinoma (mRCC). J.Clin. Oncol. 2013, 31(suppl):4505.
9. Corbière V., Chapiro J., Stroobant V., Ma W., Lurquin C., Lethé B., van Baren N., Van den Eynde B.J., Boon T., Coulie P.G. Antigen spreading contributes to MAGE vaccination-induced regression of melanoma metastases. Cancer Res. 2011, 71:1253-1262.
10. Davis M.M. Immunology taught by humans. Sci. Transl. Med. 2012, 4:117fs2.
11. Demaria S., Kawashima N., Yang A.M., Devitt M.L., Babb J.S., Allison J.P., Formenti S.C. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin. Cancer Res. 2005, 11:728-734.
12. Drake C.G., McDermott D.F., Sznol M., Choueiri T.K., Kluger H.M., Powderly J.D., Smith D.C., Sankar V., Gutierrez A.A., Wigginton J.M., et al. Survival, safety, and response duration results of nivolumab (Anti-PD-1; BMS-936558; ONO-4538) in a phase I trial in patients with previously treated metastatic renal cell carcinoma (mRCC): Long-term patient follow-up. J.Clin. Oncol. 2013, 31(suppl):4514.
13. Dunn G.P., Bruce A.T., Ikeda H., Old L.J., Schreiber R.D. Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 2002, 3:991-998.
14. Duraiswamy J., Kaluza K.M., Freeman G.J., Coukos G. Dual Blockade of PD-1 and CTLA-4 Combined with Tumor Vaccine Effectively Restores T-Cell Rejection Function in Tumors. Cancer Res. 2013, 73:3591-3603.
15. Ferguson T.A., Choi J., Green D.R. Armed response: how dying cells influence T-cell functions. Immunol. Rev. 2011, 241:77-88.
16. Francisco L.M., Sage P.T., Sharpe A.H. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 2010, 236:219-242.
17. Franciszkiewicz K., Boissonnas A., Boutet M., Combadière C., Mami-Chouaib F. Role of chemokines and chemokine receptors in shaping the effector phase of the antitumor immune response. Cancer Res. 2012, 72:6325-6332.
18. Franciszkiewicz K., Le Floc'h A., Boutet M., Vergnon I., Schmitt A., Mami-Chouaib F. CD103 or LFA-1 engagement at the immune synapse between cytotoxic Tcells and tumor cells promotes maturation and regulates T-cell effector functions. Cancer Res. 2013, 73:617-628.
19. Gajewski T.F. Cancer immunotherapy. Mol. Oncol. 2012, 6:242-250.
20. Gajewski T.F., Fuertes M., Spaapen R., Zheng Y., Kline J. Molecular profiling to identify relevant immune resistance mechanisms in the tumor microenvironment. Curr. Opin. Immunol. 2011, 23:286-292.
21. Gajewski T.F., Woo S.R., Zha Y., Spaapen R., Zheng Y., Corrales L., Spranger S. Cancer immunotherapy strategies based on overcoming barriers within the tumor microenvironment. Curr. Opin. Immunol. 2013, 25:268-276.
22. Galon J., Angell H.K., Bedognetti D., Marincola F. The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013, 39:11-26. this issue.
23. Ge Y., Xi H., Ju S., Zhang X. Blockade of PD-1/PD-L1 immune checkpoint during DC vaccination induces potent protective immunity against breast cancer in hu-SCID mice. Cancer Lett. 2013, 336:253-259.
24. Goding S.R., Wilson K.A., Xie Y., Harris K.M., Baxi A., Akpinarli A., Fulton A., Tamada K., Strome S.E., Antony P.A. Restoring immune function of tumor-specific CD4+ Tcells during recurrence of melanoma. J.Immunol. 2013, 190:4899-4909.
25. Greaves P., Gribben J.G. The role of B7 family molecules in hematologic malignancy. Blood 2013, 121:734-744.
26. Grosso J., Horak C.E., Inzunza D., Cardona D.M., Simon J.S., Gupta A.K., Sankar V., Park J.-S., Kollia G., Taube J.M., et al. Association of tumor PD-L1 expression and immune biomarkers with clinical activity in patients (pts) with advanced solid tumors treated with nivolumab (anti-PD-1; BMS-936558; ONO-4538). J.Clin. Oncol. 2013, 31(suppl):3016.
27. Grupp S.A., Kalos M., Barrett D., Aplenc R., Porter D.L., Rheingold S.R., Teachey D.T., Chew A., Hauck B., Wright J.F., et al. Chimeric antigen receptor-modified Tcells for acute lymphoid leukemia. N.Engl. J. Med. 2013, 368:1509-1518.
28. Hamid O., Robert C., Daud A., Hodi F.S., Hwu W.J., Kefford R., Wolchok J.D., Hersey P., Joseph R.W., Weber J.S., et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N.Engl. J. Med. 2013, Published online June 2, 2013. 10.1056/NEJMoa1305133.
29. Hamid O., Sosman J.A., Lawrence D.P., Sullivan R.J., Ibrahim N., Kluger H.M., Boasberg P.D., Flaherty K., Hwu P., Ballinger M., et al. Clinical activity, safety, and biomarkers of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic melanoma (mM). J.Clin. Oncol. 2013, 31(suppl):9010.
30. Heo J., Reid T., Ruo L., Breitbach C.J., Rose S., Bloomston M., Cho M., Lim H.Y., Chung H.C., Kim C.W., et al. Randomized dose-finding clinical trial of oncolytic immunotherapeutic vaccinia JX-594 in liver cancer. Nat. Med. 2013, 19:329-336.
31. Herbst R.S., Gordon M.S., Fine G.D., Sosman J.A., Soria J.-C., Hamid O., Powderly J.D., Burris H.A., Mokatrin A., Kowanetz M., 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):3000.
32. Hiniker S.M., Chen D.S., Reddy S., Chang D.T., Jones J.C., Mollick J.A., Swetter S.M., Knox S.J. A systemic complete response of metastatic melanoma to local radiation and immunotherapy. Transl Oncol 2012, 5:404-407.
33. Hodi F.S., O'Day S.J., McDermott D.F., Weber R.W., Sosman J.A., Haanen J.B., Gonzalez R., Robert C., Schadendorf D., Hassel J.C., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N.Engl. J. Med. 2010, 363:711-723.
34. Huang T., Karsy M., Zhuge J., Zhong M., Liu D. B-Raf and the inhibitors: from bench to bedside. J Hematol Oncol 2013, 6:30-38.
35. Isaacs J.D., Wing M.G., Greenwood J.D., Hazleman B.L., Hale G., Waldmann H. A therapeutic human IgG4 monoclonal antibody that depletes target cells in humans. Clin. Exp. Immunol. 1996, 106:427-433.
36. Jacobs J.F., Nierkens S., Figdor C.G., de Vries I.J., Adema G.J. Regulatory Tcells in melanoma: the final hurdle towards effective immunotherapy?. Lancet Oncol. 2012, 13:e32-e42.
37. James B.R., Tomanek-Chalkley A., Askeland E.J., Kucaba T., Griffith T.S., Norian L.A. Diet-induced obesity alters dendritic cell function in the presence and absence of tumor growth. J.Immunol. 2012, 189:1311-1321.
38. Kalos M., June C.H. Adoptive Tcell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 2013, 39:49-60. this issue.
39. Karan D., Van Veldhuizen P. Combination immunotherapy with prostate GVAX and ipilimumab: safety and toxicity. Immunotherapy 2012, 4:577-580.
40. Kasuga K. Comprehensive analysis of MHC ligands in clinical material by immunoaffinity-mass spectrometry. Methods Mol. Biol. 2013, 1023:203-218.
41. Kochenderfer J.N., Rosenberg S.A. Treating B-cell cancer with Tcells expressing anti-CD19 chimeric antigen receptors. Nat Rev Clin Oncol 2013, 10:267-276.
42. Kruit W.H., Suciu S., Dreno B., Mortier L., Robert C., Chiarion-Sileni V., Maio M., Testori A., Dorval T., Grob J.J., et al. Selection of immunostimulant AS15 for active immunization with MAGE-A3 protein: results of a randomized phase II study of the European Organisation for Research and Treatment of Cancer Melanoma Group in metastatic melanoma. J.Clin. Oncol. 2013, 31:2413-2420.
43. Lin Y.L., Meng Y., Jiang W., Roux B. Explaining why Gleevec is a specific and potent inhibitor of Abl kinase. Proc. Natl. Acad. Sci. USA 2013, 110:1664-1669.
44. Lippitz B.E. Cytokine patterns in patients with cancer: a systematic review. Lancet Oncol. 2013, 14:e218-e228.
45. Liu C., Peng W., Xu C., Lou Y., Zhang M., Wargo J.A., Chen J.Q., Li H.S., Watowich S.S., Yang Y., et al. BRAF inhibition increases tumor infiltration by Tcells and enhances the antitumor activity of adoptive immunotherapy in mice. Clin. Cancer Res. 2013, 19:393-403.
46. Madan R.A., Mohebtash M., Arlen P.M., Vergati M., Rauckhorst M., Steinberg S.M., Tsang K.Y., Poole D.J., Parnes H.L., Wright J.J., et al. Ipilimumab and a poxviral vaccine targeting prostate-specific antigen in metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial. Lancet Oncol. 2012, 13:501-508.
47. Mellman I., Coukos G., Dranoff G. Cancer immunotherapy comes of age. Nature 2011, 480:480-489.
48. Motz G.T., Coukos G. Deciphering and Reversing Tumor Immune Suppression. Immunity 2013, 39:61-73. this issue.
49. Mullard A. New checkpoint inhibitors ride the immunotherapy tsunami. Nat. Rev. Drug Discov. 2013, 12:489-492.
50. Ott P.A., Henry T., Baranda S.J., Frleta D., Manches O., Bogunovic D., Bhardwaj N. Inhibition of both BRAF and MEK in BRAF(V600E) mutant melanoma restores compromised dendritic cell (DC) function while having differential direct effects on DC properties. Cancer Immunol. Immunother. 2013, 62:811-822.
51. Palucka K., Banchereau J. Dendritic-cell-based therapeutic cancer vaccines. Immunity 2013, 39:38-48. this issue.
52. Parry R.V., Chemnitz J.M., Frauwirth K.A., Lanfranco A.R., Braunstein I., Kobayashi S.V., Linsley P.S., Thompson C.B., Riley J.L. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol. Cell. Biol. 2005, 25:9543-9553.
53. Patnaik A., Kang S.P., Tolcher A.W., Rasco D.W., Papadopoulos K.P., Beeram M., Drengler R., Chen C., Smith L., Perez C., et al. Phase I study of MK-3475 (anti-PD-1 monoclonal antibody) in patients with advanced solid tumors. J.Clin. Oncol. 2012, 30(suppl):2512.
54. Peng W., Liu C., Xu C., Lou Y., Chen J., Yang Y., Yagita H., Overwijk W.W., Lizée G., Radvanyi L., Hwu P. PD-1 blockade enhances T-cell migration to tumors by elevating IFN-γ inducible chemokines. Cancer Res. 2012, 72:5209-5218.
55. Postow M.A., Callahan M.K., Barker C.A., Yamada Y., Yuan J., Kitano S., Mu Z., Rasalan T., Adamow M., Ritter E., et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N.Engl. J. Med. 2012, 366:925-931.
56. Powderly J.D., Koeppen H., Hodi F.S., Sosman J.A., Gettlinger S.N., Desai R., Tabernero J., Soria J.-C., Hamid O., Fine G.D., et al. Biomarkers and associations with the clinical activity of PD-L1 blockade in a MPDL3280A study. J.Clin. Oncol. 2013, 31(suppl):3001.
57. Predina J., Eruslanov E., Judy B., Kapoor V., Cheng G., Wang L.C., Sun J., Moon E.K., Fridlender Z.G., Albelda S., Singhal S. Changes in the local tumor microenvironment in recurrent cancers may explain the failure of vaccines after surgery. Proc. Natl. Acad. Sci. USA 2013, 110:E415-E424.
58. Qureshi O.S., Zheng Y., Nakamura K., Attridge K., Manzotti C., Schmidt E.M., Baker J., Jeffery L.E., Kaur S., Briggs Z., et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science 2011, 332:600-603.
59. Rammensee H.G., Weinschenk T., Gouttefangeas C., Stevanović S. Towards patient-specific tumor antigen selection for vaccination. Immunol. Rev. 2002, 188:164-176.
60. Riella L.V., Paterson A.M., Sharpe A.H., Chandraker A. Role of the PD-1 pathway in the immune response. Am. J. Transplant. 2012, 12:2575-2587.
61. Rotem-Yehudar R., Rodionov G., Landes S. CT-011, a humanized monoclonal antibody, interacts with the PD-1 receptor and modulates survival and trafficking signals in effector/memory T lymphocytes. Proc. Am. Assoc. Cancer Res. 2009, Apr 18-22 Abstract 2410.
62. Rothman J., Paterson Y. Live-attenuated Listeria-based immunotherapy. Expert Rev. Vaccines 2013, 12:493-504.
63. Rothschild S.I., Gautschi O. Crizotinib in the Treatment of Non-Small-Cell Lung Cancer. Clin. Lung Cancer 2013, Published online June 19, 2013. 10.1016/j.cllc.2013.04.006.
64. Segal N.H., Parsons D.W., Peggs K.S., Velculescu V., Kinzler K.W., Vogelstein B., Allison J.P. Epitope landscape in breast and colorectal cancer. Cancer Res. 2008, 68:889-892.
65. Smothers F., Hoos A., Langermann S., Marshall S., May R., Fleming M. AMP-224, A fusion Protein That Targets PD-1. Ann. Oncol. 2013, 24(suppl):i7-i17.
66. So T., Lee S.W., Croft M. Tumor necrosis factor/tumor necrosis factor receptor family members that positively regulate immunity. Int. J. Hematol. 2006, 83:1-11.
67. Spigel D.R., Gettinger S.N., Horn L., Herbst R.S., Gandhi L., Gordon M.S., Cruz C., Conkling P., Cassier P.A., Antonia S.J., et al. Clinical activity, safety and biomarkers of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic non-small cell lung cancer (NSCLC). J.Clin. Oncol. 2013, 31(suppl):8008.
68. Stagg J., Loi S., Divisekera U., Ngiow S.F., Duret H., Yagita H., Teng M.W., Smyth M.J. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc. Natl. Acad. Sci. USA 2011, 108:7142-7147.
69. Stewart R.A., Morrow M., Chodorge M., Marcus D., Boyle M., Mulgrew K., Hammond S., Wang S., Alimzhanov M., Robbins P., et al. Delivering effective blockade of immunosupression to enhance tumour rejection: Monoclonal antibody discovery and preclinical development. Cancer Res. 2011, 71(Suppl):LB-158.
70. Sznol M., Kluger H.M., Hodi F.S., McDermott D.F., Carvajal R.D., Lawrence D.P., Topalian S.L., Atkins M.B., Powderly J.D., Sharfman W.H., et al. Survival and long-term follow-up of safety and response in patients (pts) with advanced melanoma (MEL) in a phase I trial of nivolumab (anti-PD-1; BMS-936558; ONO-4538). J.Clin. Oncol. 2013, 31(suppl):CRA9006.
71. Tabernero J., Powderly J.D., Hamid O., Gordon M.S., Fisher G.A., Braiteh F.S., Garbo L.E., Fine G.D., Kowanetz M., McCall B., et al. Clinical activity, safety, and biomarkers of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic CRC, gastric cancer (GC), SCCHN, or other tumors. J.Clin. Oncol. 2013, 31(suppl):3622.
72. Tian T., Olson S., Whitacre J.M., Harding A. The origins of cancer robustness and evolvability. Integr Biol (Camb) 2011, 3:17-30.
73. Topalian S.L., Drake C.G., Pardoll D.M. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr. Opin. Immunol. 2012, 24:207-212.
74. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N.Engl. J. Med. 2012, 366:2443-2454.
75. Topalian S.L., Sznol M., Brahmer J.R., McDermott D.F., Smith D.C., Gettinger S.N., Taube J.M., Drake C.G., Pardoll D.M., Powderly J.D., et al. Nivolumab (anti-PD-1; BMS-936558; ONO-4538) in patients with advanced solid tumors: Survival and long-term safety in a phase I trial. J.Clin. Oncol. 2013, 31(suppl):3002.
76. van den Boorn J.G., Hartmann G. Turning tumors into vaccines: Co-opting the Innate Immune System. Immunity 2013, 39:27-37. this issue.
77. Vanneman M., Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat. Rev. Cancer 2012, 12:237-251.
78. Vansteenkiste J., Zielinski M., Linder A., Dahabreh J., Gonzalez E.E., Malinowski W., Lopez-Brea M., Vanakesa T., Jassem J., Kalofonos H., et al. Adjuvant MAGE-A3 immunotherapy in resected non-small-cell lung cancer: Phase II randomized study results. J.Clin. Oncol. 2013, 31:2396-2403.
79. Wang L., Qian J., Lu Y., Li H., Bao H., He D., Liu Z., Zheng Y., He J., Li Y., et al. Immune evasion evasion of mantle cell lymphoma: expression of B7-H1 leads to inhibited T-cell response to and killing of tumor cells. Haematologica 2013, Published online March 18, 2013. 10.3324/haematol.2012.071340.
80. West E.E., Jin H.T., Rasheed A.U., Penaloza-Macmaster P., Ha S.J., Tan W.G., Youngblood B., Freeman G.J., Smith K.A., Ahmed R. PD-L1 blockade synergizes with IL-2 therapy in reinvigorating exhausted Tcells. J.Clin. Invest. 2013, 123:2604-2615.
81. Westin J., Chu F., Fayad L., Kwak L.W., Fowler N.H., Romaguera J., Hagemeister F.B., Fanale M., Samaniego F., Allen R., et al. Phase II Safety and Efficacy Study of CT-011, a Humanized anti-PD-1 Monoclonal Antibody, in Combination with Rituximab in Patients with Relapsed Follicular Lymphoma. Blood 2012, 120:793.
82. Wolchok J.D., Kluger H., Callahan M.K., Postow M.A., Rizvi N.A., Lesokhin A.M., Segal N.H., Ariyan C.E., Gordon R.A., Reed K., et al. Nivolumab plus ipilimumab in advanced melanoma. N.Engl. J. Med. 2013.
83. Xu X., Ye L., Araki K., Ahmed R. mTOR, linking metabolism and immunity. Semin. Immunol. 2012, 24:429-435.
84. Zitvogel L., Galluzzi L., Smyth M.J., Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 2013, 39:74-88. this issue.