Understanding the function and dysfunction of the immune system in lung cancer: the role of immune checkpoints

Cancer Biology and Medicine

Volumn 12, Issue 2, 2015, Pages 79-86

  Karachaliou, Niki ^a   Cao, Maria Gonzalez ^a   Teixidó, Cristina ^b   Viteri, Santiago ^a   Morales Espinosa, Daniela ^a   Santarpia, Mariacarmela ^c   Rosell, Rafael ^a,b,d,e,f  

^a INSTITUT UNIVERSITARI DEXEUS   (Spain)

^b Pangaea Biotech   (Spain)

^c UNIVERSITY OF MESSINA   (Italy)

^d HOSPITAL UNIVERSITARI GERMANS TRIAS I PUJOL   (Spain)

^e Molecular Oncology Research (MORe) Foundation   (Spain)

^f Germans Trias i Pujol Health Sciences Institute and Hospital Campus Can   (China)

Author keywords

Immune checkpoint; Immunotherapy; Lung cancer; Program death 1 (PD 1); Program death ligand 1 (PD L1)

Indexed keywords

ANTINEOPLASTIC AGENT; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERFERON; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; NEOANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; STAT3 PROTEIN; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER THERAPY; CARCINOGENESIS; CLINICAL EFFECTIVENESS; CLINICAL PRACTICE; HUMAN; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LUNG CANCER; MULTICENTER STUDY (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR SUPPRESSOR GENE;

EID: 84937545889     PISSN: 20953941     EISSN: None     Source Type: Journal    
DOI: 10.7497/j.issn.2095-3941.2015.0029     Document Type: Review

References (69)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014;64:9-29.
2. Rosell R, Bivona TG, Karachaliou N. Genetics and biomarkers in personalisation of lung cancer treatment. Lancet 2013;382:720-731.
3. Rosell R, Karachaliou N, Wolf J, Ou SH. ALK and ROS1 nonsmall- cell lung cancer: two molecular subgroups sensitive to targeted therapy. Lancet Respir Med 2014;2:966-968.
4. Rosell R. Dynamic Evolution of ALK Positive Non-Small Cell Lung Cancers and Management of Associated Brain Metastases [podcast]. J Clin Oncol 2015. [Epub ahead of print].
5. Kilinc MO, Gu T, Harden JL, Virtuoso LP, Egilmez NK. Central role of tumor-associated CD8+ T effector/memory cells in restoring systemic antitumor immunity. J Immunol 2009;182:4217-4225.
6. 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.
7. Luckheeram RV, Zhou R, Verma AD, Xia B. CD4+T cells: differentiation and functions. Clin Dev Immunol 2012;2012:925135.
8. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263-274.
9. Kryczek I, Wei S, Gong W, Shu X, Szeliga W, Vatan L, et al. Cutting edge: IFN-gamma enables APC to promote memory Th17 and abate Th1 cell development. J Immunol 2008;181:5842-5846.
10. Gershon RK, Kondo K. Infectious immunological tolerance. Immunology 1971;21:903-914.
11. Gershon RK, Kondo K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 1970;18:723-737.
12. Berendt MJ, North RJ. T-cell-mediated suppression of antitumor immunity. An explanation for progressive growth of an immunogenic tumor. J Exp Med 1980;151:69-80.
13. Bursuker I, North RJ. Generation and decay of the immune response to a progressive fibrosarcoma. II. Failure to demonstrate postexcision immunity after the onset of T cell-mediated suppression of immunity. J Exp Med 1984;159:1312-1321.
14. North RJ, Bursuker I. Generation and decay of the immune response to a progressive fibrosarcoma. I. Ly-1+2- suppressor T cells down-regulate the generation of Ly-1-2+ effector T cells. J Exp Med 1984;159:1295-1311.
15. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-1164.
16. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-1061.
17. Heikkinen T, Jävinen A. The common cold. Lancet 2003;361:51-59.
18. Greenwald RJ, Freeman GJ, Sharpe AH. The B7 family revisited. Annu Rev Immunol 2005;23:515-548.
19. Townsend SE, Allison JP. Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science 1993;259:368-370.
20. Riley JL, June CH. The CD28 family: a T-cell rheostat for therapeutic control of T-cell activation. Blood 2005;105:13-21.
21. Nirschl CJ, Drake CG. Molecular pathways: coexpression of immune checkpoint molecules: signaling pathways and implications for cancer immunotherapy. Clin Cancer Res 2013;19:4917-4924.
22. Ngiow SF, von Scheidt B, Akiba H, Yagita H, Teng MW, Smyth MJ. Anti-TIM3 antibody promotes T cell IFN-γ-mediated antitumor immunity and suppresses established tumors. Cancer Res 2011;71:3540-3551.
23. Wang L, Rubinstein R, Lines JL, Wasiuk A, Ahonen C, Guo Y, et al. VISTA, a novel mouse Ig superfamily ligand that negatively regulates T cell responses. J Exp Med 2011;208:577-592.
24. Chemnitz JM, Parry RV, Nichols KE, June CH, Riley JL. SHP- 1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J Immunol 2004;173:945-954.
25. Yokosuka T, Takamatsu M, Kobayashi-Imanishi W, Hashimoto-Tane A, Azuma M, Saito T. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 2012;209:1201-1217.
26. Su JC, Chiang HC, Tseng PH, Tai WT, Hsu CY, Li YS, et al. RFX- 1-dependent activation of SHP-1 inhibits STAT3 signaling in hepatocellular carcinoma cells. Carcinogenesis 2014;35:2807-2814.
27. Tang TL, Freeman RM Jr, O'Reilly AM, Neel BG, Sokol SY. The SH2-containing protein-tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell 1995;80:473-483.
28. Bennett AM, Hausdorff SF, O'Reilly AM, Freeman RM, Neel BG. Multiple requirements for SHPTP2 in epidermal growth factormediated cell cycle progression. Mol Cell Biol 1996;16:1189-1202.
29. Lehmann U, Schmitz J, Weissenbach M, Sobota RM, Hortner M, Friederichs K, et al. SHP2 and SOCS3 contribute to Tyr-759- dependent attenuation of interleukin-6 signaling through gp130. J Biol Chem 2003;278:661-671.
30. 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.
31. Sharma P, Allison JP. The future of immune checkpoint therapy. Science. 2015;348:56-61.
32. Freedman LR, Cerottini JC, Brunner KT. In vivo studies of the role of cytotoxic T cells in tumor allograft immunity. J Immunol 1972;109:1371-1378.
33. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12:298-306.
34. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol 2004;22:329-360.
35. Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE, 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.
36. Wang QJ, Hanada K, Robbins PF, Li YF, Yang JC. Distinctive features of the differentiated phenotype and infiltration of tumorreactive lymphocytes in clear cell renal cell carcinoma. Cancer Res 2012;72:6119-6129.
37. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002;8:793-800.
38. Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med 2007;13:84-88.
39. Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7- H1). Proc Natl Acad Sci U S A 2008;105:20852-20857.
40. Liu J, Hamrouni A, Wolowiec D, Coiteux V, Kuliczkowski K, Hetuin D, et al. Plasma cells from multiple myeloma patients express B7-H1 (PD-L1) and increase expression after stimulation with IFN-{gamma} and TLR ligands via a MyD88-, TRAF6-, and MEK-dependent pathway. Blood 2007;110:296-304.
41. Taube JM, Anders RA, Young GD, Xu H, Sharma R, McMiller TL, 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.
42. Ghebeh H, Tulbah A, Mohammed S, Elkum N, Bin Amer SM, Al-Tweigeri T, et al. Expression of B7-H1 in breast cancer patients is strongly associated with high proliferative Ki-67-expressing tumor cells. Int J Cancer 2007;121:751-758.
43. Zhu J, Chen L, Zou L, Yang P, Wu R, Mao Y, et al. MiR-20b, -21, and -130b inhibit PTEN expression resulting in B7-H1 over-expression in advanced colorectal cancer. Hum Immunol 2014;75:348-353.
44. Yamamoto R, Nishikori M, Tashima M, Sakai T, Ichinohe T, Takaori-Kondo A, et al. B7-H1 expression is regulated by MEK/ ERK signaling pathway in anaplastic large cell lymphoma and Hodgkin lymphoma. Cancer Sci 2009;100:2093-2100.
45. Hirahara K, Ghoreschi K, Yang XP, Takahashi H, Laurence A, Vahedi G, et al. Interleukin-27 priming of T cells controls IL-17 production in trans via induction of the ligand PD-L1. Immunity 2012;36:1017-1030.
46. 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.
47. Mu CY, Huang JA, Chen Y, Chen C, Zhang XG. 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.
48. Wöfle SJ, Strebovsky J, Bartz H, Sär A, Arnold C, Kaiser C, et al. PD-L1 expression on tolerogenic APCs is controlled by STAT-3. Eur J Immunol 2011;41:413-424.
49. Pivarcsi A, Müller A, Hippe A, Rieker J, van Lierop A, Steinhoff M, et al. Tumor immune escape by the loss of homeostatic chemokine expression. Proc Natl Acad Sci U S A 2007;104:19055-19060.
50. Xu C, Fillmore CM, Koyama S, Wu H, Zhao Y, Chen Z, et al. Loss of Lkb1 and Pten leads to lung squamous cell carcinoma with elevated PD-L1 expression. Cancer Cell 2014;25:590-604.
51. Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov 2013;3:1355-1363.
52. D'Incecco A, Andreozzi M, Ludovini V, Rossi E, Capodanno A, Landi L, et al. PD-1 and PD-L1 expression in molecularly selected non-small-cell lung cancer patients. Br J Cancer 2015;112:95-102.
53. Azuma K, Ota K, Kawahara A, Hattori S, Iwama E, Harada T, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol 2014;25:1935-1940.
54. Zhang Y, Wang L, Li Y, Pan Y, Wang R, Hu H, et al. Protein expression of programmed death 1 ligand 1 and ligand 2 independently predict poor prognosis in surgically resected lung adenocarcinoma. Onco Targets Ther 2014;7:567-573.
55. Gainor JF, Sequist LV, Shaw AT, Azzoli CG, Piotrowska Z, Huynh T, et al. Clinical correlation and frequency of programmed death ligand-1 (PD-L1) expression in EGFR-mutant and ALKrearranged non-small cell lung cancer (NSCLC). J Clin Oncol 2015;33:abstr 8012.
56. 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;364:2517-2526.
57. Schadendorf D, Hodi FS, Robert C, Weber JS, Margolin K, Hamid O, et al. Pooled Analysis of Long-Term Survival Data From Phase II and Phase III Trials of Ipilimumab in Unresectable or Metastatic Melanoma. J Clin Oncol 2015;33:1889-1894.
58. 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.
59. Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 2015;372:320-330.
60. Paz-Ares L, Horn L, Borghaei H, Spigel DR, Steins M, Ready N, et al. Phase III, randomized trial (CheckMate 057) of nivolumab (NIVO) versus docetaxel (DOC) in advanced non-squamous cell (non-SQ) non-small cell lung cancer (NSCLC). J Clin Oncol 2015;33:abstr LBA109.
61. Brahmer J, Reckamp KL, Baas P, Crinò L, Eberhardt WE, Poddubskaya E, et al. Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer. N Engl J Med 2015. [Epub ahead of print].
62. Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 2014;515:568-571.
63. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014;515:563-567.
64. 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.
65. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature 2013;500:415-421.
66. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 2015;348:124-128.
67. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014;371:2189-2199.
68. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science 2015;348:69-74.
69. Schumacher TN, Kesmir C, van Buuren MM. Biomarkers in cancer immunotherapy. Cancer Cell 2015;27:12-14.