PD-L1 expression in lung cancer

Journal of Thoracic Oncology

Volumn 11, Issue 7, 2016, Pages 964-975

  Yu, Hui ^a   Boyle, Theresa A ^a,b,c   Zhou, Caicun ^d   Rimm, David L ^e   Hirsch, Fred R ^a,b  

^a UNIVERSITY OF COLORADO CANCER CENTER   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^d SHANGHAI PULMONARY HOSPITAL   (China)

^e YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biomarker; Immunotherapy; Lung cancer; PD L1

Indexed keywords

ANTINEOPLASTIC AGENT; ATEZOLIZUMAB; AVELUMAB; DURVALUMAB; MONOCLONAL ANTIBODY; NIVOLUMAB; PEMBROLIZUMAB; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; BIOLOGICAL MARKER; CD274 PROTEIN, HUMAN;

CANCER CHEMOTHERAPY; CANCER DIAGNOSIS; CANCER RISK; CELLS BY BODY ANATOMY; CLINICAL TRIAL (TOPIC); COMPARATIVE STUDY; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; GENETIC HETEROGENEITY; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG CANCER; PATIENT CARE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK ASSESSMENT; RISK FACTOR; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; IMMUNOLOGY; IMMUNOTHERAPY; LUNG NEOPLASMS; MOUSE;

ANIMALS; ANTIGENS, CD274; BIOMARKERS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOTHERAPY; LUNG NEOPLASMS; MICE;

EID: 84978238160     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1016/j.jtho.2016.04.014     Document Type: Review

References (81)

1. 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.
2. Brahmer J, Reckamp KL, Baas P, et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 2015;373:123-135.
3. Borghaei H, Paz-Ares L, Horn L, et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 2015;373:1627-1639.
4. Garon EB, Rizvi NA, Hui R, et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 2015;372:2018-2028.
5. Brahmer JR, Tykodi SS, Chow LQ, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366:2455-2465.
6. Freeman GJ, Long AJ, Iwai Y, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med. 2000;192:1027-1034.
7. Dong H, Strome SE, Salomao DR, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8:793-800.
8. Dong H, Zhu G, Tamada K, et al. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med. 1999;5:1365-1369.
9. Hamid O, Robert C, Daud A, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med. 2013;369:134-144.
10. Brahmer JR, Drake CG, Wollner I, 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.
11. Thompson RH, Kuntz SM, Leibovich BC, et al. Tumor B7-H1 is associated with poor prognosis in renal cell carcinoma patients with long-term follow-up. Cancer Res. 2006;66:3381-3385.
12. Motzer RJ, Rini BI, McDermott DF, et al. Nivolumab for metastatic renal cell carcinoma: results of a randomized phase II trial. J Clin Oncol. 2015;33:1430-1437.
13. Robert C, Long GV, Brady B, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372:320-330.
14. Mahoney KM, Atkins MB. Prognostic and predictive markers for the new immunotherapies. Oncology (Williston Park). 2014;28(suppl 3):39-48.
15. Kim MY, Koh J, Kim S, et al. Clinicopathological analysis of PD-L1 and PD-L2 expression in pulmonary squamous cell carcinoma: comparison with tumor-infiltrating T cells and the status of oncogenic drivers. Lung Cancer. 2015;88:24-33.
16. Schmidt LH, Kummel A, Gorlich D, et al. PD-1 and PD-L1 expression in NSCLC indicate a favorable prognosis in defined subgroups. PLoS One. 2015;10:e0136023.
17. Tang Y, Fang W, Zhang Y, et al. The association between PD-L1 and EGFR status and the prognostic value of PD-L1 in advanced non-small cell lung cancer patients treated with EGFR-TKIs. Oncotarget. 2015;6:14209-14219.
18. Taube JM, Anders RA, Young GD, 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.
19. Badoual C, Hans S, Merillon N, et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-associated head and neck cancer. Cancer Res. 2013;73:128-138.
20. Rizvi NA, Mazieres J, Planchard D, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol. 2015;16: 257-265.
21. Gettinger SN, Horn L, Gandhi L, et al. Overall survival and long-term safety of nivolumab (anti-programmed death 1 antibody, BMS-936558, ONO-4538) in patients with previously treated advanced non-small-cell lung cancer. J Clin Oncol. 2015;33:2004-2012.
22. Gettinger SN. First-line monotherapy with nivolumab (NIVO; antiprogrammed death-1 [PD-1]) in advanced non-small cell lung cancer (NSCLC): safety, efficacy and correlation of outcomes with PD-1 ligand (PD-L1) expression [abstract]. J Clin Oncol. 2015;33(suppl): 8025.
23. Rizvi NA, Shepherd FA, Antonia SJ, et al. First-line monotherapy with nivolumab (anti-PD-1; BMS-936558, ONO-4538) in advanced non-small cell lung cancer (NSCLC): safety, efficacy, and correlation of outcomes with PD-L1 status. Int J Radiat Oncol Biol Phys. 2014;90:S31.
24. Antonia SJ, Goldman J, Chow LQ, et al. Safety and efficacy of first-line nivolumab (anti-PD-1; BMS-936558, ONO-4538) and ipilimumab in non-small cell lung cancer (NSCLC). Int J Radiat Oncol Biol Phys. 2014;90: S32-S33.
25. Ramalingam SS, Panchard D, et al. Phase II study of nivolumab (Anti-PD-1 BMS-936558, ONO-4538) in patients with advanced, refractory squamous non-small cell lung cancer [abstract]. Int J Rad Oncol Biol Phys. 2014;90:LB2.
26. Herbst RS, Baas P, Kim D-W, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1 positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomized controlled trial. Lancet. 2016;387: 1540-1550.
27. Herbst RS, Soria JC, Kowanetz M, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515: 563-567.
28. Spira AI, Park K, Mazieres J, et al. Efficacy, safety and predictive biomarker results from a randomized phase II study comparing MPDL3280A vs docetaxel in 2L/3L NSCLC (POPLAR) [abstract]. J Clin Oncol. 2015;33(suppl):8010.
29. Spigel DR, Chaft JE, Gettinger SN, et al. Clinical activity and safety from a phase II study (FIR) of MPDL3280A (anti-PD-L1) in PD-L1-selected patients with non-small cell lung cancer (NSCLC) [abstract]. J Clin Oncol. 2015;33(suppl):8028.
30. Horn L, Spigel DR, Gettinger SN, et al. Clinical activity, safety and predictive biomarkers of the engineered antibody MPDL3280A (anti-PDL1) in non-small cell lung cancer (NSCLC): update from a phase 1a study [abstract]. J Clin Oncol. 2015;33(suppl):8029.
31. Liu SV, Powderly JD, Camidge DR, et al. Safety and efficacy of MPDL3280A (anti-PDL1) in combination with platinum-based doublet chemotherapy in patients with advanced non-small cell lung cancer (NSCLC) [abstract]. J Clin Oncol. 2015;33(suppl):8030.
32. Rebelatto M, Mistry A, Sabalos C, et al. Development of a PD-L1 companion diagnostic assay for treatment with MEDI4736 in NSCLC and SCCHN patients [abstract]. J Clin Oncol. 2015;33(suppl):8033.
33. Gulley JL, Spigel D, Kelly K, et al. Avelumab (MSB0010718C), an anti-PD-L1 antibody, in advanced NSCLC patients: a phase 1b, open-label expansion trial in patients progressing after platinum-based chemotherapy [abstract]. J Clin Oncol. 2015;33(suppl):8034.
34. Zhang J, Gao J, Li Y, et al. Circulating PD-L1 in NSCLC patients and the correlation between the level of PD-L1 expression and the clinical characteristics. Thorac Cancer. 2015;6:534-538.
35. Lin C, Chen X, Li M, et al. Programmed death-ligand 1 expression predicts tyrosine kinase inhibitor response and better prognosis in a cohort of patients with epidermal growth factor receptor mutation-positive lung adenocarcinoma. Clin Lung Cancer. 2015;16: e25-e35.
36. Zhang Y, Wang L, Li Y, 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.
37. Azuma K, Ota K, Kawahara A, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol. 2014;25:1935-1940.
38. Yang CY, Lin MW, Chang YL, et al. 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.
39. Velcheti V, Schalper KA, Carvajal DE, et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest. 2014;94:107-116.
40. Chen YB, Mu CY, Huang JA. 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.
41. Schultheis AM, Scheel AH, Ozretic L, et al. PD-L1 expression in small cell neuroendocrine carcinomas. Eur J Cancer. 2015;51:421-426.
42. Ishii H, Azuma K, Kawahara A, et al. Significance of programmed cell death-ligand 1 expression and its association with survival in patients with small cell lung cancer. J Thorac Oncol. 2015;10:426-430.
43. Komiya T, Madan R. PD-L1 expression in small cell lung cancer. Eur J Cancer. 2015;51:1853-1855.
44. Hirsch FR, McElhinny A, Stanforth D, et al. PD-L1 IHC assays for lung cancer: results from phase I of the Blueprint PD-L1 Assay Comparison Project. Paper presented at: AACR Annual Meeting; April 19, 2016; New Orleans, LA.
45. Ott PA, Elez Fernandez ME, Hiret S, et al. Pembrolizumab (MK-3475) in patients (pts) with extensive-stage small cell lung cancer (SCLC): preliminary safety and efficacy results from Keynote-028 [abstract]. J Clin Oncol. 2015;33(suppl):7502.
46. Powles T, Eder JP, Fine GD, et al. MPDL3280A (anti-PDL1) treatment leads to clinical activity in metastatic bladder cancer. Nature. 2014;515:558-562.
47. McDermott DF, Sosman JA, Sznol M, et al. Atezolizumab, an anti-programmed death-ligand 1 antibody, in metastatic renal cell carcinoma: long-term safety, clinical activity, and immune correlates from a phase Ia study. J Clin Oncol. 2016;34:833-842.
48. McLaughlin J, Han G, Schalper KA, et al. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol. 2015;2:1-9.
49. Sharpe AH, Wherry EJ, Ahmed R, et al. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat Immunol. 2007;8: 239-245.
50. Spranger S, Spaapen RM, Zha Y, et al. Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Sci Transl Med. 2013;5:200ra116.
51. Tumeh PC, Harview CL, Yearley JH, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515:568-571.
52. Kerr KM, Tsao MS, Nicholson AG, et al. Programmed death-ligand 1 immunohistochemistry in lung cancer: in what state is this art? J Thorac Oncol. 2015;10: 985-989.
53. Gerdes MJ, Sevinsky CJ, Sood A, et al. Highly multiplexed single-cell analysis of formalin-fixed, paraffinembedded cancer tissue. Proc Natl Acad Sci U S A. 2013;110:11982-11987.
54. Wistuba II. Assessment of immune cells in tumor biopsies as a biomarker [abstract]. 2015 WCLC meeting, Abstract MS21.03. http://library.iaslc.org/search-speaker?search-speaker=24778. Accessed May 20, 2016.
55. McLaughlin JF, Schalper K, Carvajal-Hausdorf DE, et al. Domain-specific PD-L1 protein measurement in nonsmall cell lung cancer (NSCLC) [abstract]. J Clin Oncol. 2014;32(suppl):8064.
56. Taube JM, Klein A, Brahmer JR, et al. Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res. 2014;20:5064-5074.
57. Akbay EA, Koyama S, Carretero J, et al. Activation of the PD-1 pathway contributes to immune escape in EGFRdriven lung tumors. Cancer Discov. 2013;3:1355-1363.
58. Thompson RH, Gillett MD, Cheville JC, et al. Costimulatory molecule B7-H1 in primary and metastatic clear cell renal cell carcinoma. Cancer. 2005;104:2084-2091.
59. Thompson RH, Gillett MD, Cheville JC, et al. Costimulatory B7-H1 in renal cell carcinoma patients: Indicator of tumor aggressiveness and potential therapeutic target. Proc Natl Acad Sci U S A. 2004;101:17174-17179.
60. Mu CY, Huang JA, Chen Y, et al. 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.
61. Phillips T, Simmons P, Inzunza HD, et al. Development of an automated PD-L1 immunohistochemistry (IHC) assay for non-small cell lung cancer. Appl Immunohistochem Mol Morphol. 2015;23:541-549.
62. Bigelow E, Bever KM, Xu H, et al. Immunohistochemical staining of B7-H1 (PD-L1) on paraffin-embedded slides of pancreatic adenocarcinoma tissue [abstract]. J Vis Exp. 2013;71:4059.
63. Soliman H, Khalil F, Antonia S, et al. PD-L1 expression is increased in a subset of basal type breast cancer cells. PLoS One. 2014;9:e88557.
64. Wolff AC, Hammond ME, Hicks DG, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update [abstract]. J Clin Oncol. 2013;31(suppl):3997-4013.
65. Wolff AC, Hammond ME, Hicks DG, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. Arch Pathol Lab Med. 2014;138: 241-256.
66. Marti AM, Martinez P, Navarro A, et al. Concordance of PD-L1 expression by different immunohistochemistry (IHC) definitions and in situ hybridization (ISH) in squamous cell carcinoma (SCC) of the lung [abstract]. J Clin Oncol. 2014;32(suppl):7569.
67. Twa DD, Chan FC, Ben-Neriah S, et al. Genomic rearrangements involving programmed death ligands are recurrent in primary mediastinal large B-cell lymphoma. Blood. 2014;123:2062-2065.
68. Hellman MD, Creelan BC, Woo K, et al. Smoking history and response to nivolumab in patients with advanced NSCLCs. Ann Oncol. 2014;25(suppl 4):iv426-iv470.
69. Rizvi NA, Hellmann MD, Snyder A, et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 2015;348:124-128.
70. Le DT, Uram JN, Wang H, et al. PD-1 Blockade in tumors with mismatch-repair deficiency. N Engl J Med. 2015;372:2509-2520.
71. Rosenberg JE, Hoffman-Censits J, Powles T, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial [e-pub ahead of print]. Lancet. doi: 10.1016/S0140-6736 (16)00561-4, accessed May 20, 2016.
72. Rudd CE, Taylor A, Schneider H. CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev. 2009;229:12-26.
73. Wing K, Onishi Y, Prieto-Martin P, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 2008;322:271-275.
74. Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373:23-34.
75. Latchman Y, Wood CR, Chernova T, et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol. 2001;2:261-268.
76. Youngnak P1, Kozono Y, Kozono H, et al. Differential binding propeties of B7-H1 and B7-DC to programmed death-1. Biochem Biophys Res Commun. 2003;307:672-677.
77. Yamazaki T, Akiba H, Iwai H, et al. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol. 2002;169:5538-5545.
78. Shin SJ, Jeon YK, Kim PJ, et al. Clinicopathologic analysis of PD-L1 and PD-L2 expression in renal cell carcinoma: association with oncogenic proteins status. Ann Surg Oncol. 2016;23:694-702.
79. Kim S, Kim MY, Koh J, et al. Programmed death-1 ligand 1 and 2 are highly expressed in pleomorphic carcinomas of the lung: comparison of sarcomatous and carcinomatous areas. Eur J Cancer. 2015;51:2698-2707.
80. Calles A, Liao X, Sholl LM, et al. Expression of PD-1 and its ligands, PD-L1 and PD-L2, in smokers and never smokers with KRAS-mutant lung cancer. J Thorac Oncol. 2015;10:1726-1735.
81. Champiat S, Ileana E, Giaccone G, et al. Incorporating immune-checkpoint inhibitors into systemic therapy of NSCLC. J Thorac Oncol. 2014;9:144-153.