Biomarkers in early-stage non-small-cell lung cancer: Current concepts and future directions

Journal of Thoracic Oncology

Volumn 9, Issue 11, 2014, Pages 1609-1617

  Burotto, Mauricio ^a   Thomas, Anish ^a   Subramaniam, Deepa ^b   Giaccone, Giuseppe ^b   Rajan, Arun ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biomarkers; Early stage lung cancer; Lung cancer; Predictive; Prognostic

Indexed keywords

BIOLOGICAL MARKER; BRCA1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; K RAS PROTEIN; PROTEIN P53; RIBONUCLEOTIDE REDUCTASE; TUMOR MARKER;

CANCER ADJUVANT THERAPY; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER PROGNOSIS; HUMAN; IMMUNE SYSTEM; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; REVIEW; RNA METHYLATION; TUMOR ASSOCIATED LEUKOCYTE; LUNG TUMOR; METABOLISM; PROGNOSIS;

BIOMARKERS, TUMOR; CARCINOMA, NON-SMALL-CELL LUNG; HUMANS; LUNG NEOPLASMS; PROGNOSIS;

EID: 84925723349     PISSN: 15560864     EISSN: 15561380     Source Type: Journal    
DOI: 10.1097/JTO.0000000000000302     Document Type: Review

References (82)

1. Howlader N, Noone AM, Krapcho M, et al. (eds). SEER Cancer Statistics Review, 1975-2011. National Cancer Institute. Bethesda, MD. Available at http://seer.cancer.gov/csr/1975-2011/. Accessed April 2014.
2. Früh M, Rolland E, Pignon JP, et al. Pooled analysis of the effect of age on adjuvant cisplatin-based chemotherapy for completely resected non-small-cell lung cancer. J Clin Oncol 2008;26:3573-3581.
3. Arriagada R, Auperin A, Burdett S, et al. Adjuvant chemotherapy, with or without postoperative radiotherapy, in operable non-small-cell lung cancer: two meta-analyses of individual patient data. Lancet 2010;375:1267-1277.
4. Howlader N, Noone AM, Krapcho M, et al. SEER Cancer Statistics Review. Bethesda, MD: National Cancer Institute, 2012.
5. Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365:395-409.
6. Arriagada R, Bergman B, Dunant A, et al. Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N Engl J Med 2004;350:351-360.
7. Douillard JY, Rosell R, De Lena M, et al. Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol 2006;7:719-727.
8. Pignon JP, Tribodet H, Scagliotti GV, et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol 2008;26:3552-3559.
9. Buyse M, Sargent DJ, Grothey A, et al. Biomarkers and surrogate end points - the challenge of statistical validation. Nat Rev Clin Oncol 2010;7:309-317.
10. Group EBCTC: Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005;365:1687-1717.
11. Mogi A, Kuwano H. TP53 mutations in nonsmall cell lung cancer. J Biomed Biotechnol 2011;2011:583929.
12. Oscier DG, Gardiner AC, Mould SJ, et al. Multivariate analysis of prognostic factors in CLL: clinical stage, IGVH gene mutational status, and loss or mutation of the p53 gene are independent prognostic factors. Blood 2002;100:1177-1184.
13. Abudu A, Mangham DC, Reynolds GM, et al. Overexpression of p53 protein in primary Ewing's sarcoma of bone: relationship to tumour stage, response and prognosis. Br J Cancer 1999;79:1185-1189.
14. Graziano SL, Gu L, Wang X, et al. Prognostic significance of mucin and p53 expression in stage IB non-small cell lung cancer: a laboratory companion study to CALGB 9633. J Thorac Oncol 2010;5:810-817.
15. Mitsudomi T, Hamajima N, Ogawa M, et al. Prognostic significance of p53 alterations in patients with non-small cell lung cancer: a meta-analysis. Clin Cancer Res 2000;6:4055-4063.
16. Rodenhuis S, van de Wetering ML, Mooi WJ, et al. Mutational activation of the K-ras oncogene. A possible pathogenetic factor in adenocarcinoma of the lung. N Engl J Med 1987;317:929-935.
17. Rodenhuis S, Slebos RJ, Boot AJ, et al. Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res 1988;48:5738-5741.
18. Rosell R, Li S, Skacel Z, et al. Prognostic impact of mutated K-ras gene in surgically resected non-small cell lung cancer patients. Oncogene 1993;8:2407-2412.
19. Vega F, Iniesta P, Caldes T, et al. Association of K-ras codon 12 transversions with short survival in non-small cell lung cancer. Int J Oncol 1996;9:1307-1311.
20. Slebos RJ, Kibbelaar RE, Dalesio O, et al. K-ras oncogene activation as a prognostic marker in adenocarcinoma of the lung. N Engl J Med 1990;323:561-565.
21. Huncharek M, Muscat J, Geschwind JF. K-ras oncogene mutation as a prognostic marker in non-small cell lung cancer: a combined analysis of 881 cases. Carcinogenesis 1999;20:1507-1510.
22. Roberts PJ, Stinchcombe TE. KRAS mutation: should we test for it, and does it matter? J Clin Oncol 2013;31:1112-1121.
23. Shepherd FA, Domerg C, Hainaut P, et al. Pooled analysis of the prognostic and predictive effects of KRAS mutation status and KRAS mutation subtype in early-stage resected non-small-cell lung cancer in four trials of adjuvant chemotherapy. J Clin Oncol 2013;31:2173-2181.
24. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008;359:1367-1380.
25. Rusch V, Klimstra D, Venkatraman E, et al. Overexpression of the epidermal growth factor receptor and its ligand transforming growth factor alpha is frequent in resectable non-small cell lung cancer but does not predict tumor progression. Clin Cancer Res 1997;3:515-522.
26. Sonobe M, Nakagawa M, Takenaka K, et al. Influence of epidermal growth factor receptor (EGFR) gene mutations on the expression of EGFR, phosphoryl-Akt, and phosphoryl-MAPK, and on the prognosis of patients with non-small cell lung cancer. J Surg Oncol 2007;95:63-69.
27. Sonobe M, Kobayashi M, Ishikawa M, et al. Impact of KRAS and EGFR gene mutations on recurrence and survival in patients with surgically resected lung adenocarcinomas. Ann Surg Oncol 2012;19(Suppl 3):S347-S354.
28. Liu WS, Zhao LJ, Pang QS, et al. Prognostic value of epidermal growth factor receptor mutations in resected lung adenocarcinomas. Med Oncol 2014;31:771.
29. D'Angelo SP, Janjigian YY, Ahye N, et al. Distinct clinical course of EGFR-mutant resected lung cancers: results of testing of 1118 surgical specimens and effects of adjuvant gefitinib and erlotinib. J Thorac Oncol 2012;7:1815-1822.
30. Heinmöller P, Gross C, Beyser K, et al. HER2 status in non-small cell lung cancer: results from patient screening for enrollment to a phase II study of herceptin. Clin Cancer Res 2003;9:5238-5243.
31. Stephens P, Hunter C, Bignell G, et al. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature 2004;431:525-526.
32. Brabender J, Danenberg KD, Metzger R, et al. Epidermal growth factor receptor and HER2-neu mRNA expression in non-small cell lung cancer is correlated with survival. Clin Cancer Res 2001;7:1850-1855.
33. Takenaka M, Hanagiri T, Shinohara S, et al. The prognostic significance of HER2 overexpression in non-small cell lung cancer. Anticancer Res 2011;31:4631-4636.
34. Korrapati V, Gaffney M, Larsson LG, et al. Effect of HER2/neu expression on survival in non-small-cell lung cancer. Clin Lung Cancer 2001;2:216-219.
35. Xia Q, Zhu Z, Wang J, et al. Expression and association of HER2 with prognosis in early-stage (T1-T2N0M0) non-small cell lung cancer. Tumour Biol 2012;33:1719-1725.
36. Mazieres J, Peters S, Lepage B, et al. Lung cancer that harbors a HER2 mutation: epidemiologic characteristics and therapeutic perspectives. J Clin Oncol 2013;31:1997-2003.
37. Li L, Elledge SJ, Peterson CA, et al. Specific association between the human DNA repair proteins XPA and ERCC1. Proc Natl Acad Sci U S A 1994;91:5012-5016.
38. Simon GR, Sharma S, Cantor A, et al. ERCC1 expression is a predictor of survival in resected patients with non-small cell lung cancer. Chest 2005;127:978-983.
39. Olaussen KA, Dunant A, Fouret P, et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N Engl J Med 2006;355:983-991.
40. Zheng Z, Chen T, Li X, et al. DNA synthesis and repair genes RRM1 and ERCC1 in lung cancer. N Engl J Med 2007;356:800-808.
41. Friboulet L, Olaussen KA, Pignon JP, et al. ERCC1 isoform expression and DNA repair in non-small-cell lung cancer. N Engl J Med 2013;368:1101-1110.
42. Davidson JD, Ma L, Flagella M, et al. An increase in the expression of ribonucleotide reductase large subunit 1 is associated with gemcitabine resistance in non-small cell lung cancer cell lines. Cancer Res 2004;64:3761-3766.
43. Bepler G, Sharma S, Cantor A, et al. RRM1 and PTEN as prognostic parameters for overall and disease-free survival in patients with non-small-cell lung cancer. J Clin Oncol 2004;22:1878-1885.
44. Bepler G, Zinner RG, Moon J, et al. A phase 2 cooperative group adjuvant trial using a biomarker-based decision algorithm in patients with stage I non-small cell lung cancer (SWOG-0720, NCT00792701). Cancer 2014;doi: 10.1002/cncr.28714 [Epub ahead of print].
45. Foulkes WD. Inherited susceptibility to common cancers. N Engl J Med 2008;359:2143-2153.
46. Lee MN, Tseng RC, Hsu HS, et al. Epigenetic inactivation of the chromosomal stability control genes BRCA1, BRCA2, and XRCC5 in non-small cell lung cancer. Clin Cancer Res 2007;13:832-838.
47. Marsit CJ, Liu M, Nelson HH, et al. Inactivation of the Fanconi anemia/BRCA pathway in lung and oral cancers: implications for treatment and survival. Oncogene 2004;23:1000-1004.
48. Rosell R, Skrzypski M, Jassem E, et al. BRCA1: a novel prognostic factor in resected non-small-cell lung cancer. PLoS One 2007;2:e1129.
49. Sanchez JM, Cobo M, Arrabal R, et al. Pilot SCAT trial: Spanish customized adjuvant chemotherapy (CT) based on BRCA1 mRNA expression levels (l) in resected stage II-IIIA non-small cell lung cancer (NSCLC) patients (p). J Clin Oncol 2012;30.
50. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-723.
51. Kantoff PW, Higano CS, Shore ND, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 2010;363:411-422.
52. 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.
53. Jadus MR, Natividad J, Mai A, et al. Lung cancer: a classic example of tumor escape and progression while providing opportunities for immunological intervention. Clin Dev Immunol 2012;2012:160724.
54. Suzuki K, Kachala SS, Kadota K, et al. Prognostic immune markers in non-small cell lung cancer. Clin Cancer Res 2011;17:5247-5256.
55. Ruffini E, Asioli S, Filosso PL, et al. Clinical significance of tumorinfiltrating lymphocytes in lung neoplasms. Ann Thorac Surg 2009;87:365-371.
56. Wakabayashi O, Yamazaki K, Oizumi S, et al. CD4+ T cells in cancer stroma, not CD8+ T cells in cancer cell nests, are associated with favorable prognosis in human non-small cell lung cancers. Cancer Sci 2003;94:1003-1009.
57. Al-Shibli KI, Donnem T, Al-Saad S, et al. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008;14:5220-5227.
58. deLeeuw RJ, Kost SE, Kakal JA, et al. The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 2012;18:3022-3029.
59. Shimizu K, Nakata M, Hirami Y, et al. Tumor-infiltrating Foxp3+ regulatory T cells are correlated with cyclooxygenase-2 expression and are associated with recurrence in resected non-small cell lung cancer. J Thorac Oncol 2010;5:585-590.
60. Suzuki K, Kadota K, Sima CS, et al. Clinical impact of immune microenvironment in stage I lung adenocarcinoma: tumor interleukin-12 receptor β2 (IL-12Rβ2), IL-7R, and stromal FoxP3/CD3 ratio are independent predictors of recurrence. J Clin Oncol 2013;31:490-498.
61. Melero I, Hervas-Stubbs S, Glennie M, et al. Immunostimulatory monoclonal antibodies for cancer therapy. Nat Rev Cancer 2007;7:95-106.
62. Salvi S, Fontana V, Boccardo 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.
63. 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.
64. Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res 2013;19:5300-5309.
65. 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.
66. Antonia SJ, Grosso JF, Horak CE, 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 (anti-PD-1; BMS-936558; ONO-4538). J Thorac Oncol 2013;8(suppl 2):Abstract P2.11-035.
67. Gettinger S, Shepherd F, Antonia SJ, et al. First-line nivolumab (anti-PD-1; BMS-936558, ONO-4538) monotherapy in advanced NSCLC: Safety, efficacy, and correlation of outcomes with PD-L1 status. J Clin Oncol 2014;32:5s.
68. 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.
69. Paik S, Shak S, Tang G, et al. A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 2004;351:2817-2826.
70. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 2000;403:503-511.
71. Chen HY, Yu SL, Chen CH, et al. A five-gene signature and clinical outcome in non-small-cell lung cancer. N Engl J Med 2007;356:11-20.
72. Lau SK, Boutros PC, Pintilie M, et al. Three-gene prognostic classifier for early-stage non small-cell lung cancer. J Clin Oncol 2007;25:5562-5569.
73. Subramanian J, Simon R. Gene expression-based prognostic signatures in lung cancer: ready for clinical use? J Natl Cancer Inst 2010;102:464-474.
74. Kratz JR, He J, Van Den Eeden SK, et al. A practical molecular assay to predict survival in resected non-squamous, non-small-cell lung cancer: development and international validation studies. Lancet 2012;379:823-832.
75. Brock MV, Hooker CM, Ota-Machida E, et al. DNA methylation markers and early recurrence in stage I lung cancer. N Engl J Med 2008;358:1118-1128.
76. Sandoval J, Mendez-Gonzalez J, Nadal E, et al. A prognostic DNA methylation signature for stage I non-small-cell lung cancer. J Clin Oncol 2013;31:4140-4147.
77. Boeri M, Pastorino U, Sozzi G. Role of microRNAs in lung cancer: microRNA signatures in cancer prognosis. Cancer J 2012;18:268-274.
78. Landi MT, Zhao Y, Rotunno M, et al. MicroRNA expression differentiates histology and predicts survival of lung cancer. Clin Cancer Res 2010;16:430-441.
79. Donnem T, Fenton CG, Lonvik K, et al. MicroRNA signatures in tumor tissue related to angiogenesis in non-small cell lung cancer. PLoS One 2012;7:e29671.
80. Zhu CQ, Ding K, Strumpf D, et al. Prognostic and predictive gene signature for adjuvant chemotherapy in resected non-small-cell lung cancer. J Clin Oncol 2010;28:4417-4424.
81. Subramanian J, Simon R. What should physicians look for in evaluating prognostic gene-expression signatures? Nat Rev Clin Oncol 2010;7:327-334.
82. Yanagisawa K, Tomida S, Shimada Y, et al. A 25-signal proteomic signature and outcome for patients with resected non-small-cell lung cancer. J Natl Cancer Inst 2007;99:858-867.