Epigenetic inactivation of microRNA-34b/c predicts poor disease-free survival in early-stage lung adenocarcinoma

Clinical Cancer Research

Volumn 19, Issue 24, 2013, Pages 6842-6852

  Nadal, Ernest ^a   Chen, Guoan ^a   Gallegos, Marc ^b   Lin, Lin ^a   Ferrer Torres, Daysha ^a   Truini, Anna ^a   Wang, Zhuwen ^a   Lin, Jules ^a   Reddy, Rishindra M ^a   Llatjos, Roger ^b   Escobar, Ignacio ^b   Moya, Juan ^b   Chang, Andrew C ^a   Cardenal, Felipe ^b   Capellà, Gabriel ^b   Beer, David G ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b CATALAN INSTITUTE OF ONCOLOGY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MICRORNA; MICRORNA 34B; MICRORNA 34C; PROTEIN P53; UNCLASSIFIED DRUG;

AGED; APOPTOSIS; ARTICLE; CANCER STAGING; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; DEMETHYLATION; DISEASE FREE SURVIVAL; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE MUTATION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; METHYLATION; OVERALL SURVIVAL; PHENOTYPE; PREDICTION; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN METHYLATION;

ADENOCARCINOMA; ADULT; AGED; APOPTOSIS; CELL PROLIFERATION; DISEASE-FREE SURVIVAL; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; LUNG NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; PROMOTER REGIONS, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84890710331     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-0736     Document Type: Article

References (50)

1. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, Boyle P. Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 2007;18:581-92. (Pubitemid 46359643)
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29.
3. Youlden DR, Cramb SM, Baade PD. The International Epidemiology of Lung Cancer: geographical distribution and secular trends. J Thorac Oncol 2008;3:819-31.
4. Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med 2008;359:1367-80.
5. Fruh M, Rolland E, Pignon JP, Seymour L, Ding K, Tribodet H, 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;26:3573-81.
6. Group NM-aC Arriagada R, Auperin A, Burdett S, Higgins JP, Johnson DH, et al. Adjuvant chemotherapy, with or without postoperative radiotherapy, in operable non-small-cell lung cancer: two meta-anal-yses of individual patient data. Lancet 2010;375:1267-77.
7. Ludwig JA, Weinstein JN. Biomarkers in cancer staging, prognosis and treatment selection. Nat Rev 2005;5:845-56. (Pubitemid 41746029)
8. Mascaux C, Iannino N, Martin B, Paesmans M, Berghmans T, Dusart M, et al. The role of RAS oncogene in survival of patients with lung cancer: a systematic review of the literature with meta-analysis. Br J Cancer 2005;92:131-9. (Pubitemid 40188446)
9. Steels E, Paesmans M, Berghmans T, Branle F, Lemaitre F, Mascaux C, et al. Role of p53 as a prognostic factor for survival in lung cancer: a systematic review of the literature with a meta-analysis. Eur Respir J 2001;18:705-19. (Pubitemid 33040631)
10. Shedden K, Taylor JM, Enkemann SA, Tsao MS, Yeatman TJ, Gerald WL, et al. Gene expression-based survival prediction in lung adenocar-cinoma: a multi-site, blinded validation study. Nat Med 2008;14:822-7.
11. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009;10:704-14.
12. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 2006;6:259-69.
13. Hammond SM. MicroRNAs as tumor suppressors. Nat Genet 2007;39:582-3. (Pubitemid 46676097)
14. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007;447: 1130-4. (Pubitemid 47014436)
15. Wei CL, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T, et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006;124:207-19. (Pubitemid 43069320)
16. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D, et al. A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 2008;105:13556-61.
17. Corney DC, Hwang CI, Matoso A, Vogt M, Flesken-Nikitin A, Godwin AK, et al. Frequent downregulation of miR-34 family in human ovarian cancers. Clin Cancer Res 2010;16:1119-28.
18. Suzuki H, Yamamoto E, Nojima M, Kai M, Yamano HO, Yoshikawa K, et al. Methylation-associated silencing of microRNA-34b/c in gastric cancer and its involvement in an epigenetic field defect. Carcinogen-esis 2010;31:2066-73.
19. Vogt M, Munding J, Gruner M, Liffers ST, Verdoodt B, Hauk J, et al. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 2011;458:313-22.
20. Kubo T, Toyooka S, Tsukuda K, Sakaguchi M, Fukazawa T, Soh J, et al. Epigenetic silencing of microRNA-34b/c plays an important role in the pathogenesis of malignant pleural mesothelioma. Clin Cancer Res 2011;17:4965-74.
21. Toyota M, Suzuki H, Sasaki Y, Maruyama R, Imai K, Shinomura Y, et al. Epigenetic silencing of microRNA-34b/c and B-cell translocation gene 4 is associated with CpG island methylation in colorectal cancer. Cancer Res 2008;68:4123-32.
22. Wang Z, Chen Z, Gao Y, Li N, Li B, Tan F, et al. DNA hypermethylation of microRNA-34b/c has prognostic value for stage non-small cell lung cancer. Cancer Biol Ther 2011;11:490-6.
23. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol 2007;17:1298-307. (Pubitemid 47176893)
24. Tanaka N, Toyooka S, Soh J, Kubo T, Yamamoto H, Maki Y, et al. Frequent methylation and oncogenic role of microRNA-34b/c in small-cell lung cancer. Lung Cancer 2012;76:32-8.
25. Curado MP, Edwards B, Shin HR, Storm H, Ferlay J, Heanue M, et al. Cancer Incidence in Five Continents, Vol. IX, Lyon, France, International Agency for Research on Cancer (IARC) Scientific Publication 160, 2007.
26. Petitjean A, Mathe E, Kato S, Ishioka C, Tavtigian SV, Hainaut P, et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat 2007;28:622-9. (Pubitemid 46744292)
27. Bamford S, Dawson E, Forbes S, Clements J, Pettett R, Dogan A, et al. The COSMIC (Catalogue of Somatic Mutations in Cancer) database and website. Br J Cancer 2004;91:355-8. (Pubitemid 39037083)
28. Frigola J, Song J, Stirzaker C, Hinshelwood RA, Peinado MA, Clark SJ. Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nat Genet 2006;38: 540-9.
29. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009;4:e6816.
30. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 2012;13:134.
31. Voortman J, Goto A, Mendiboure J, Sohn JJ, Schetter AJ, Saito M, et al. MicroRNA expression and clinical outcomes in patients treated with adjuvant chemotherapy after complete resection of non-small cell lung carcinoma. Cancer Res 2010;70: 8288-98.
32. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
33. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435:834-8. (Pubitemid 40839735)
34. Kumar MS, Lu J, Mercer KL, Golub TR, Jacks T. Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet 2007;39:673-7. (Pubitemid 46676103)
35. Zhang L, Volinia S, Bonome T, Calin GA, Greshock J, Yang N, et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc Natl Acad Sci USA 2008;105: 7004-9. (Pubitemid 351754520)
36. Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med 2005;353:1793-801. (Pubitemid 41549891)
37. Saini HK, Griffiths-Jones S, Enright AJ. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci USA 2007;104:17719-24. (Pubitemid 350210901)
38. Aguda BD, Kim Y, Piper-Hunter MG, Friedman A, Marsh CB. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci USA 2008;105:19678-83.
39. Heller G, Weinzierl M, Noll C, Babinsky V, Ziegler B, Altenberger C, et al. Genome-wide miRNA expression profiling identifies miR-9-3 and miR-193a as targets for DNA methylation in non-small cell lung cancers. Clin Cancer Res 2012;18:1619-29.
40. Baer C, Claus R, Plass C. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Res 2013;73:473-7.
41. Concepcion CP, Han YC, Mu P, Bonetti C, Yao E, D'Andrea A, et al. Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet 2012;8:e1002797.
42. Mascaux C, Laes JF, Anthoine G, Haller A, Ninane V, Burny A, et al. Evolution of microRNA expression during human bronchial squamous carcinogenesis. Eur Respir J 2009;33:352-9.
43. Landi MT, Zhao Y, Rotunno M, Koshiol J, Liu H, Bergen AW, et al. MicroRNA expression differentiates histology and predicts survival of lung cancer. Clin Cancer Res 2010;16:430-41.
44. Corney DC, Flesken-Nikitin A, Godwin AK, Wang W, Nikitin AY. MicroRNA-34b and MicroRNA-34c are targets of p53 and cooperate in control of cell proliferation and adhesion-independent growth. Cancer Res 2007;67:8433-8. (Pubitemid 47437414)
45. Chim CS, Wan TS, Wong KY, Fung TK, Drexler HG, Wong KF. Methylation of miR-34a, miR-34b/c, miR-124-1 and miR-203 in Ph-negative myeloproliferative neoplasms. J Transl Med 2011; 9:197.
46. Bryant JL, Britson J, Balko JM, Willian M, Timmons R, Frolov A, et al. A microRNA gene expression signature predicts response to erlotinib in epithelial cancer cell lines and targets EMT. Br J Cancer 2012;106: 148-56.
47. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011;12:861-74.
48. Juergens RA, Wrangle J, Vendetti FP, Murphy SC, Zhao M, Coleman B, et al. Combination epigenetic therapy has efficacy in patients with refractory advanced non-small cell lung cancer. Cancer Discov 2011;1:598-607.
49. Wiggins JF, Ruffino L, Kelnar K, Omotola M, Patrawala L, Brown D, et al. Development of a lung cancer therapeutic based on the tumor suppressor microRNA-34. Cancer Res 2010;70: 5923-30.
50. Kasinski AL, Slack FJ. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 2011;11:849-64.