Profiling cancer testis antigens in non–small-cell lung cancer

JCI Insight

Volumn 1, Issue 10, 2019, Pages

  Djureinovic, Dijana ^a   Hallström, Björn M ^b   Horie, Masafumi ^c   Margareta Mattsson, Johanna Sofia ^a   Fleur, Linnea La ^a   Fagerberg, Linn ^b   Brunnström, Hans ^d   Lindskog, Cecilia ^a   Madjar, Katrin ^e   Rahnenführer, Jörg ^e   Ekman, Simon ^f   Ståhle, Elisabeth ^f   Koyi, Hirsh ^f   Brandén, Eva ^f   Edlund, Karolina ^e   Hengstler, Jan G ^e   Lambe, Mats ^a   Saito, Akira ^c   Botling, Johan ^a   Pontén, Fredrik ^a   Uhlén, Mathias ^b   Micke, Patrick ^a   more..

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^c UNIVERSITY OF TOKYO   (Japan)

^d Regional Laboratories Region Skåne ^*  (Sweden)

^e TU DORTMUND UNIVERSITY   (Germany)

^f UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER TESTIS ANTIGEN; TRANSCRIPTOME; TUMOR MARKER;

AGED; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CANCER TISSUE; CLUSTER ANALYSIS; COHORT ANALYSIS; CXORF67 GENE; FEMALE; GENE; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC FINGERPRINTING; GENETIC IDENTIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MOLECULAR GENETICS; NON SMALL CELL LUNG CANCER; PROTEIN EXPRESSION; PROTEIN METHYLATION; REGULATORY MECHANISM; RNA SEQUENCE; TGIF2LX GENE; TISSUE SPECIFICITY; TKTL1 GENE; VCX GENE;

EID: 85071293611     PISSN: None     EISSN: 23793708     Source Type: Journal    
DOI: 10.1172/jci.insight.86837     Document Type: Article

References (78)

1. Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature. 2014;511(7511):543–550.
2. Clinical Lung Cancer Genome Project (CLCGP), Network Genomic Medicine (NGM). A genomics-based classification of human lung tumors. Sci Transl Med. 2013;5(209):209ra153.
3. Pao W, Girard N. New driver mutations in non-small-cell lung cancer. Lancet Oncol. 2011;12(2):175–180.
4. Kwak EL, et al. Anaplastic lymphoma kinase inhibition in non-small-cell lung cancer. N Engl J Med. 2010;363(18):1693–1703.
5. Laurent-Puig P, Lievre A, Blons H. Mutations and response to epidermal growth factor receptor inhibitors. Clin Cancer Res. 2009;15(4):1133–1139.
6. Yang Y. Cancer immunotherapy: harnessing the immune system to battle cancer. J Clin Invest. 2015;125(9):3335–3337.
7. Rosenberg SA, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res. 2011;17(13):4550–4557.
8. Chen L, Han X. Anti-PD-1/PD-L1 therapy of human cancer: past, present, and future. J Clin Invest. 2015;125(9):3384–3391.
9. Anagnostou VK, Brahmer JR. Cancer immunotherapy: a future paradigm shift in the treatment of non-small cell lung cancer. Clin Cancer Res. 2015;21(5):976–984.
10. Madureira P, de Mello RA, de Vasconcelos A, Zhang Y. Immunotherapy for lung cancer: for whom the bell tolls?. Tumour Biol. 2015;36(3):1411–1422.
11. Melief CJ, van Hall T, Arens R, Ossendorp F, van der Burg SH. Therapeutic cancer vaccines. J Clin Invest. 2015;125(9):3401–3412.
12. Cohen CJ, et al. Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes. J Clin Invest. 2015;125(10):3981–3991.
13. Gubin MM, Artyomov MN, Mardis ER, Schreiber RD. Tumor neoantigens: building a framework for personalized cancer immunotherapy. J Clin Invest. 2015;125(9):3413–3421.
14. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015;348(6230):69–74.
15. Caballero OL, Chen YT. Cancer/testis (CT) antigens: potential targets for immunotherapy. Cancer Sci. 2009;100(11):2014–2021.
16. Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer. 2005;5(8):615–625.
17. Knuth A, Danowski B, Oettgen HF, Old LJ. T-cell-mediated cytotoxicity against autologous malignant melanoma: analysis with interleukin 2-dependent T-cell cultures. Proc Natl Acad Sci U S A. 1984;81(11):3511–3515.
18. Sahin U, et al. Human neoplasms elicit multiple specific immune responses in the autologous host. Proc Natl Acad Sci U S A. 1995;92(25):11810–11813.
19. Hunt JS. Stranger in a strange land. Immunol Rev. 2006;213:36–47.
20. Janitz M, et al. Analysis of mRNA for class I HLA on human gametogenic cells. Mol Reprod Dev. 1994;38(2):231–237.
21. Almeida LG, et al. CTdatabase: a knowledge-base of high-throughput and curated data on cancer-testis antigens. Nucleic Acids Res. 2009;37(Database issue):D816–D819.
22. Grunwald C, et al. Expression of multiple epigenetically regulated cancer/germline genes in nonsmall cell lung cancer. Int J Cancer. 2006;118(10):2522–2528.
23. Gure AO, et al. Cancer-testis genes are coordinately expressed and are markers of poor outcome in non-small cell lung cancer. Clin Cancer Res. 2005;11(22):8055–8062.
24. Shigematsu Y, et al. Clinical significance of cancer/testis antigens expression in patients with non-small cell lung cancer. Lung Cancer. 2010;68(1):105–110.
25. Tajima K, et al. Expression of cancer/testis (CT) antigens in lung cancer. Lung Cancer. 2003;42(1):23–33.
26. Bhattacharjee A, et al. Classification of human lung carcinomas by mRNA expression profiling reveals distinct adenocarcinoma subclasses. Proc Natl Acad Sci U S A. 2001;98(24):13790–13795.
27. Botling J, et al. Biomarker discovery in non-small cell lung cancer: integrating gene expression profiling, meta-analysis, and tissue microarray validation. Clin Cancer Res. 2013;19(1):194–204.
28. Uhlen M, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.
29. GTEx Consortium. Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science. 2015;348(6235):648–660.
30. Carson MJ, Doose JM, Melchior B, Schmid CD, Ploix CC. CNS immune privilege: hiding in plain sight. Immunol Rev. 2006;213:48–65.
31. Fritz P, Coy JF, Mürdter TE, Ott G, Alscher MD, Friedel G. TKTL-1 expression in lung cancer. Pathol Res Pract. 2012;208(4):203–209.
32. Ousati Ashtiani Z, et al. Association of TGIFLX/Y mRNA expression with prostate cancer. Med Oncol. 2009;26(1):73–77.
33. Taguchi A, et al. A search for novel cancer/testis antigens in lung cancer identifies VCX/Y genes, expanding the repertoire of potential immunotherapeutic targets. Cancer Res. 2014;74(17):4694–4705.
34. Melloni G, et al. Prognostic significance of cancer-testis gene expression in resected non-small cell lung cancer patients. Oncol Rep. 2004;12(1):145–151.
35. Rousseaux S, et al. Ectopic activation of germline and placental genes identifies aggressive metastasis-prone lung cancers. Sci Transl Med. 2013;5(186):186ra66.
36. Djureinovic D, et al. The human testis-specific proteome defined by transcriptomics and antibody-based profiling. Mol Hum Reprod. 2014;20(6):476–488.
37. Lindskog C, et al. The lung-specific proteome defined by integration of transcriptomics and antibody-based profiling. FASEB J. 2014;28(12):5184–5196.
38. Pou J, et al. Tissue factor pathway inhibitor 2 is induced by thrombin in human macrophages. Biochim Biophys Acta. 2011;1813(6):1254–1260.
39. Schmidt J, Weijdegård B, Mikkelsen AL, Lindenberg S, Nilsson L, Brännström M. Differential expression of inflammation-related genes in the ovarian stroma and granulosa cells of PCOS women. Mol Hum Reprod. 2014;20(1):49–58.
40. Karanikas V, et al. Co-expression patterns of tumor-associated antigen genes by non-small cell lung carcinomas: implications for immunotherapy. Cancer Biol Ther. 2008;7(3):345–352.
41. Lin C, et al. Cancer/testis antigen CSAGE is concurrently expressed with MAGE in chondrosarcoma. Gene. 2002;285(1–2):269–278.
42. De Smet C, De Backer O, Faraoni I, Lurquin C, Brasseur F, Boon T. The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc Natl Acad Sci U S A. 1996;93(14):7149–7153.
43. Kim R, Kulkarni P, Hannenhalli S. Derepression of cancer/testis antigens in cancer is associated with distinct patterns of DNA hypomethylation. BMC Cancer. 2013;13:144.
44. Gjerstorff MF, Andersen MH, Ditzel HJ. Oncogenic cancer/testis antigens: prime candidates for immunotherapy. Oncotarget. 2015;6(18):15772–15787.
45. van der Bruggen P, et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 1991;254(5038):1643–1647.
46. Scanlan MJ, et al. Identification of cancer/testis genes by database mining and mRNA expression analysis. Int J Cancer. 2002;98(4):485–492.
47. Vansteenkiste JF, et al. MAGRIT, a double-blind, randomized, placebo-controlled phase iii study to assess the efficacy of the recmage-A3 + AS15 cancer immunotherapeutic as adjuvant therapy in patients with resected mage-A3-positive non-small cell lung cancer (NSCLC). Ann Oncol. 2014;25(suppl 4):iv409.
48. Dutoit V, et al. Multiepitope CD8(+) T cell response to a NY-ESO-1 peptide vaccine results in imprecise tumor targeting. J Clin Invest. 2002;110(12):1813–1822.
49. Kissick HT, Sanda MG. The role of active vaccination in cancer immunotherapy: lessons from clinical trials. Curr Opin Immunol. 2015;35:15–22.
50. Nardelli-Haefliger D, Dudda JC, Romero P. Vaccination route matters for mucosal tumors. Sci Transl Med. 2013;5(172):172fs4.
51. Sasada T, Yamada A, Noguchi M, Itoh K. Personalized peptide vaccine for treatment of advanced cancer. Curr Med Chem. 2014;21(21):2332–2345.
52. Morse MA, Lyerly HK. Checkpoint blockade in combination with cancer vaccines. Vaccine. 2015;33(51):7377–7385.
53. Chen YT, et al. Identification of cancer/testis-antigen genes by massively parallel signature sequencing. Proc Natl Acad Sci U S A. 2005;102(22):7940–7945.
54. Sugita M, et al. Combined use of oligonucleotide and tissue microarrays identifies cancer/testis antigens as biomarkers in lung carcinoma. Cancer Res. 2002;62(14):3971–3979.
55. John T, et al. The role of cancer-testis antigens as predictive and prognostic markers in non-small cell lung cancer. PLoS ONE. 2013;8(7):e67876.
56. Lindskog C, Edlund K, Mattsson JS, Micke P. Immunohistochemistry-based prognostic biomarkers in NSCLC: novel findings on the road to clinical use?. Expert Rev Mol Diagn. 2015;15(4):471–490.
57. Simon RM, Hayes DF. Use of archived specimens in evaluation of prognostic and predictive biomarkers. J Natl Cancer Inst. 2009;101(21):1446–1452.
58. Subramanian J, Simon R. Gene expression-based prognostic signatures in lung cancer: ready for clinical use? J Natl Cancer Inst. 2010;102(7):464–474.
59. Travis W, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology And Genetics: Tumors Of The Lung, Pleura, Thymus And Heart. Vol. 1. Lyon, France: IARC; 2004.
60. Travis WD, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society: international multidisciplinary classification of lung adenocarcinoma: executive summary. Proc Am Thorac Soc. 2011;8(5):381–385.
61. Flicek P, et al. Ensembl 2012. Nucleic Acids Res. 2012;40(Database issue):D84–D90.
62. Trapnell C, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511–515.
63. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–930.
64. Kampf C, Olsson I, Ryberg U, Sjostedt E, Ponten F. Production of tissue microarrays, immunohistochemistry staining and digi-talization within the human protein atlas. J Vis Exp. 2012;(63).
65. Glazer CA, et al. Integrative discovery of epigenetically derepressed cancer testis antigens in NSCLC. PLoS ONE. 2009;4(12):e8189.
66. Jiao Y, Widschwendter M, Teschendorff AE. A systems-level integrative framework for genome-wide DNA methylation and gene expression data identifies differential gene expression modules under epigenetic control. Bioinformatics. 2014;30(16):2360–2366.
67. Klein JP, Moeschberger ML. Survival Analysis: Techniques For Censored And Truncated Data. 2nd ed. New York, New York, USA: Springer; 2003.
68. Therneau TM, Grambsch PM. Modeling Survival Data: Extending the Cox Model. New York, New York, USA: Springer; 2000.
69. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11(10):R106.
70. Zwiener I, Frisch B, Binder H. Transforming RNA-Seq data to improve the performance of prognostic gene signatures. PLoS ONE. 2014;9(1):e85150.
71. Benjamini Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57:289–300.
72. Schwarzer G. Meta: general package for meta-analysis. Version: 4.3-0. 2015.
73. Xie Y, et al. Robust gene expression signature from formalin-fixed paraffin-embedded samples predicts prognosis of non-small-cell lung cancer patients. Clin Cancer Res. 2011;17(17):5705–5714.
74. Okayama H, et al. Identification of genes upregulated in ALK-positive and EGFR/KRAS/ALK-negative lung adenocarcinomas. Cancer Res. 2012;72(1):100–111.
75. Hou J, et al. Gene expression-based classification of non-small cell lung carcinomas and survival prediction. PLoS ONE. 2010;5(4):e10312.
76. Bild AH, et al. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature. 2006;439(7074):353–357.
77. Der SD, et al. Validation of a histology-independent prognostic gene signature for early-stage, non-small-cell lung cancer including stage IA patients. J Thorac Oncol. 2014;9(1):59–64.
78. McCall MN, Bolstad BM, Irizarry RA. Frozen robust multiarray analysis (fRMA). Biostatistics. 2010;11(2):242–253.