Assessing PDL-1 and PD-1 in Non–Small Cell Lung Cancer: A Novel Immunoscore Approach

Clinical Lung Cancer

Volumn 18, Issue 2, 2017, Pages 220-233.e8

  Paulsen, Erna Elise ^a,b   Kilvaer, Thomas K ^a,b   Khanehkenari, Mehrdad Rakaee ^b   Al Saad, Samer ^a   Hald, Sigurd M ^b   Andersen, Sigve ^a,b   Richardsen, Elin ^a,b   Ness, Nora ^b   Busund, Lill Tove ^a,b   Bremnes, Roy M ^a,b   Donnem, Tom ^a,b  

^a UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Immune checkpoints; Lymph node metastasis; PD; Prognostic; TNM stage I

Indexed keywords

PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; ANTIGEN ANTIBODY COMPLEX; CD274 PROTEIN, HUMAN; PDCD1 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CANCER TISSUE; CELL DENSITY; CELL INFILTRATION; DISEASE FREE SURVIVAL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOSCORE; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; NON SMALL CELL LUNG CANCER; OVERALL SURVIVAL; PRIMARY TUMOR; TISSUE MICROARRAY; ADENOCARCINOMA; ANTIGEN ANTIBODY COMPLEX; ENZYME IMMUNOASSAY; FOLLOW UP; IMMUNOLOGY; LARGE CELL CARCINOMA; LUNG TUMOR; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; RETROSPECTIVE STUDY; SECONDARY; SQUAMOUS CELL CARCINOMA; SURVIVAL RATE; TUMOR ASSOCIATED LEUKOCYTE; VERY ELDERLY;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANTIGEN-ANTIBODY COMPLEX; ANTIGENS, CD274; BIOMARKERS, TUMOR; CARCINOMA, LARGE CELL; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; LYMPHATIC METASTASIS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; NEOPLASM STAGING; PROGNOSIS; PROGRAMMED CELL DEATH 1 RECEPTOR; RETROSPECTIVE STUDIES; SURVIVAL RATE; TISSUE ARRAY ANALYSIS;

EID: 85006134968     PISSN: 15257304     EISSN: 19380690     Source Type: Journal    
DOI: 10.1016/j.cllc.2016.09.009     Document Type: Article

References (54)

1. 1 Goldstraw, P., Crowley, J., Chansky, K., et al. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2 (2007), 706–714.
2. 2 Fridman, W.H., Pages, F., Sautes-Fridman, C., Galon, J., The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12 (2012), 298–306.
3. 3 Bremnes, R.M., Busund, L.T., Kilvaer, T.L., et al. The role of tumor-infiltrating lymphocytes in development, progression, and prognosis of non-small cell lung cancer. J Thorac Oncol 11 (2016), 789–800.
4. 4 Angell, H., Galon, J., From the immune contexture to the Immunoscore: the role of prognostic and predictive immune markers in cancer. Curr Opin Immunol 25 (2013), 261–267.
5. 5 Salgado, R., Denkert, C., Demaria, S., et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol 26 (2015), 259–271.
6. 6 Donnem, T., Hald, S.M., Paulsen, E.E., et al. Stromal CD8+ T-cell density—a promising supplement to TNM staging in non-small cell lung cancer. Clin Cancer Res 21 (2015), 2635–2643.
7. 7 Donnem, T., Kilvaer, T.K., Andersen, S., et al. Strategies for clinical implementation of TNM-Immunoscore in resected nonsmall-cell lung cancer. Ann Oncol 27 (2016), 225–232.
8. 8 Paulsen, E.E., Kilvaer, T., Khanehkenari, M.R., et al. CD45RO(+) memory T lymphocytes—a candidate marker for TNM-Immunoscore in squamous non-small cell lung cancer. Neoplasia 17 (2015), 839–848.
9. 9 Pardoll, D.M., The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12 (2012), 252–264.
10. 10 Keir, M.E., Butte, M.J., Freeman, G.J., Sharpe, A.H., PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 26 (2008), 677–704.
11. 11 Sanmamed, M.F., Chen, L., Inducible expression of B7-H1 (PD-L1) and its selective role in tumor site immune modulation. Cancer J 20 (2014), 256–261.
12. 12 Anagnostou, V.K., Brahmer, J.R., Cancer immunotherapy: a future paradigm shift in the treatment of non-small cell lung cancer. Clin Cancer Res 21 (2015), 976–984.
13. 13 Garon, E.B., Rizvi, N.A., Hui, R., et al. Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med 372 (2015), 2018–2028.
14. 14 Borghaei, H., Paz-Ares, L., Horn, L., et al. Nivolumab versus docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med 373 (2015), 1627–1639.
15. 15 Herbst, R.S., 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 randomised controlled trial. Lancet 387 (2016), 1540–1550.
16. 16 Fehrenbacher, L., Spira, A., Ballinger, M., et al. Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): a multicentre, open-label, phase 2 randomised controlled trial. Lancet 387 (2016), 1837–1846.
17. 17 Patel, S.P., Kurzrock, R., PD-L1 expression as a predictive biomarker in cancer immunotherapy. Mol Cancer Ther 14 (2015), 847–856.
18. 18 Brahmer, J., Reckamp, K.L., Baas, P., et al. Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 373 (2015), 123–135.
19. 19 Zhou, Z.J., Zhan, P., Song, Y., PD-L1 over-expression and survival in patients with non-small cell lung cancer: a meta-analysis. Transl Lung Cancer Res 4 (2015), 203–208.
20. 20 McLaughlin, J., Han, G., Schalper, K.A., et al. Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol 2 (2016), 46–54.
21. 21 Rami-Porta, R., Chansky, K., Goldstraw, P., Updated lung cancer staging system. Future Oncol 5 (2009), 1545–1553.
22. 22 Travis, W.D., Brambilla, E., Muller-Hermelink, H.K., Harris, C.C., World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Lung, Pleura and Heart. 2004, IARC Press, Lyon.
23. 23 Travis, W.D., Brambilla, E., Van Schil, P., et al. Paradigm shifts in lung cancer as defined in the new IASLC/ATS/ERS lung adenocarcinoma classification. Eur Respir J 38 (2011), 239–243.
24. 24 McShane, L.M., Altman, D.G., Sauerbrei, W., et al. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 97 (2005), 1180–1184.
25. 25 Donnem, T., Al-Saad, S., Al-Shibli, K., et al. Inverse prognostic impact of angiogenic marker expression in tumor cells versus stromal cells in non small cell lung cancer. Clin Cancer Res 13 (2007), 6649–6657.
26. 26 Kerr, K.M., Tsao, M.S., Nicholson, A.G., et al. Programmed death-ligand 1 immunohistochemistry in lung cancer: in what state is this art?. J Thorac Oncol 10 (2015), 985–989.
27. 27 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 6 (2015), 14209–14219.
28. 28 Sheng, J., Fang, W., Yu, J., et al. Expression of programmed death ligand-1 on tumor cells varies pre and post chemotherapy in non-small cell lung cancer. Sci Rep, 6, 2016, 20090.
29. 29 Schmidt, L.H., Kummel, A., Gorlich, D., et al. PD-1 and PD-L1 expression in NSCLC indicate a favorable prognosis in defined subgroups. PLoS One, 10, 2015, e0136023.
30. 30 Koh, J., Go, H., Keam, B., et al. Clinicopathologic analysis of programmed cell death-1 and programmed cell death-ligand 1 and 2 expressions in pulmonary adenocarcinoma: comparison with histology and driver oncogenic alteration status. Mod Pathol 28 (2015), 1154–1166.
31. 31 Kim, M.Y., Koh, J., Kim, S., Go, H., Jeon, Y.K., Chung, D.H., 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 88 (2015), 24–33.
32. 32 Mahoney, K.M., Sun, H., Liao, X., et al. PD-L1 antibodies to its cytoplasmic domain most clearly delineate cell membranes in immunohistochemical staining of tumor cells. Cancer Immunol Res 3 (2015), 1308–1315.
33. 33 Topalian, S.L., Hodi, F.S., Brahmer, J.R., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366 (2012), 2443–2454.
34. 34 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 28 (2011), 682–688.
35. 35 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 98 (2012), 751–755.
36. 36 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 25 (2014), 1935–1940.
37. 37 Mao, Y., Li, W., Chen, K., et al. B7-H1 and B7-H3 are independent predictors of poor prognosis in patients with non-small cell lung cancer. Oncotarget 6 (2015), 3452–3461.
38. 38 Velcheti, V., Schalper, K.A., Carvajal, D.E., et al. Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest 94 (2014), 107–116.
39. 39 Cooper, W.A., Tran, T., Vilain, R.E., et al. PD-L1 expression is a favorable prognostic factor in early stage non-small cell carcinoma. Lung Cancer 89 (2015), 181–188.
40. 40 D'Incecco, A., Andreozzi, M., Ludovini, V., et al. PD-1 and PD-L1 expression in molecularly selected non-small-cell lung cancer patients. Br J Cancer 112 (2015), 95–102.
41. 41 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 16 (2015), e25–e35.
42. 42 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 10 (2004), 5094–5100.
43. 43 Boland, J.M., Kwon, E.D., Harrington, S.M., et al. Tumor B7-H1 and B7-H3 expression in squamous cell carcinoma of the lung. Clin Lung Cancer 14 (2013), 157–163.
44. 44 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 50 (2014), 1361–1369.
45. 45 Zhong, A., Xing, Y., Pan, X., Shi, M., Xu, H., Prognostic value of programmed cell death-ligand 1 expression in patients with non-small-cell lung cancer: evidence from an updated meta-analysis. Onco Targets Ther 8 (2015), 3595–3601.
46. 46 Rizvi, N.A., Hellmann, M.D., Snyder, A., et al. Cancer immunology: mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348 (2015), 124–128.
47. 47 Akbay, E.A., Koyama, S., Carretero, J., et al. Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov 3 (2013), 1355–1363.
48. 48 Ilie, M., Long-Mira, E., Bence, C., et al. Comparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: a potential issue for anti-PD-L1 therapeutic strategies. Ann Oncol 27 (2016), 147–153.
49. 49 Calles, A., Liao, X., Sholl, L.M., 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 10 (2015), 1726–1735.
50. 50 Herbst, R.S., Soria, J.C., Kowanetz, M., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515 (2014), 563–567.
51. 51 Taube, J.M., Klein, A., Brahmer, J.R., 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 20 (2014), 5064–5074.
52. 52 Muller, P., Rothschild, S.I., Arnold, W., et al. Metastatic spread in patients with non-small cell lung cancer is associated with a reduced density of tumor-infiltrating T cells. Cancer Immunol Immunother 65 (2016), 1–11.
53. 53 Viguier, M., Lemaitre, F., Verola, O., et al. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J Immunol 173 (2004), 1444–1453.
54. 54 Heeren, A.M., Koster, B.D., Samuels, S., et al. High and interrelated rates of PD-L1+CD14+ antigen-presenting cells and regulatory T cells mark the microenvironment of metastatic lymph nodes from patients with cervical cancer. Cancer Immunol Res 3 (2015), 48–58.