Methylation of an intronic region regulates miR-199a in testicular tumor malignancy

Oncogene

Volumn 30, Issue 31, 2011, Pages 3404-3415

  Cheung, H H ^a,b   Davis, A J ^a   Lee, T L ^a   Pang, A L ^a   Nagrani, S ^a   Rennert, O M ^a   Chan, W Y ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

intronic methylation; malignancy; miR 199a; PODXL; testicular tumor

Indexed keywords

DYNAMIN III; MICROR 199A; MICRORNA; PODOCALYXIN; PODOCALYXIN LIKE PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER INVASION; CELL MIGRATION; CHROMOSOME 1Q; CORRELATION ANALYSIS; DNA METHYLATION; EMBRYO; EMBRYONAL CARCINOMA; EPIGENETICS; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; MALE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA METHYLATION; TESTIS; TESTIS TUMOR;

ANIMALS; CARCINOMA; CELL LINE, TUMOR; CELL MOVEMENT; DNA METHYLATION; DYNAMIN III; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRONS; LIVER NEOPLASMS; LUNG NEOPLASMS; MALE; MICE; MICRORNAS; NEOPLASM INVASIVENESS; SIALOGLYCOPROTEINS; TESTICULAR NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79961168175     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.60     Document Type: Article

References (45)

1. Aleman A, Cebrian V, Alvarez M, Lopez V, Orenes E, Lopez-Serra L et al. (2008). Identification of PMF1 methylation in association with bladder cancer progression. Clin Cancer Res 14: 8236-8243.
2. Andrews PW, Damjanov I, Simon D, Banting GS, Carlin C, Dracopoli NC et al. (1984). Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab Invest 50: 147-162. (Pubitemid 14199076)
3. Casey G, Neville PJ, Liu X, Plummer SJ, Cicek MS, Krumroy LM et al. (2006). Podocalyxin variants and risk of prostate cancer and tumor aggressiveness. Hum Mol Genet 15: 735-741. (Pubitemid 43264698)
4. Chakrabarty A, Tranguch S, Daikoku T, Jensen K, Furneaux H, Dey SK. (2007). MicroRNA regulation of cyclooxygenase-2 during embryo implantation. Proc Natl Acad Sci USA 104: 15144-15149. (Pubitemid 47619608)
5. Chen R, Alvero AB, Silasi DA, Kelly MG, Fest S, Visintin I et al. (2008). Regulation of IKKbeta by miR-199a affects NF-kappaB activity in ovarian cancer cells. Oncogene 27: 4712-4723.
6. Cheung HH, Lee TL, Davis AJ, Taft DH, Rennert OM, Chan WY. (2010). Genome-wide DNA methylation profiling reveals novel epigenetically regulated genes and non-coding RNAs in human testicular cancer. Br J Cancer 102: 419-427.
7. Cheung HH, Lee TL, Rennert OM, Chan WY. (2009). DNA methylation of cancer genome. Birth Defects Res C Embryo Today 87: 335-350.
8. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Blake C, Shibata D et al. (2000). MethyLight: a high-throughput assay to measure DNA methylation. Nucleic Acids Res 28: E32.
9. Esquela-Kerscher A, Slack FJ. (2006). Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6: 259-269.
10. Fornari F, Milazzo M, Chieco P, Negrini M, Calin GA, Grazi GL et al. (2010). MiR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 70: 5184-5193.
11. Friedman LM, Dror AA, Mor E, Tenne T, Toren G, Satoh T et al. (2009). MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc Natl Acad Sci USA 106: 7915-7920.
12. Godwin JG, Ge X, Stephan K, Jurisch A, Tullius SG, Iacomini J. (2010). Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci USA 107: 14339-14344.
13. Hayatsu N, Kaneko MK, Mishima K, Nishikawa R, Matsutani M, Price JE et al. (2008). Podocalyxin expression in malignant astrocytic tumors. Biochem Biophys Res Commun 374: 394-398.
14. He L, Hannon GJ. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531. (Pubitemid 38868508)
15. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S et al. (2008). The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10: 202-210. (Pubitemid 351194050)
16. Ichimi T, Enokida H, Okuno Y, Kunimoto R, Chiyomaru T, Kawamoto K et al. (2009). Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer 125: 345-352.
17. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P et al. (2007). MicroRNA signatures in human ovarian cancer. Cancer Res 67: 8699-8707. (Pubitemid 47437445)
18. Jones PA, Takai D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293: 1068-1070. (Pubitemid 32758075)
19. Kim S, Lee UJ, Kim MN, Lee EJ, Kim JY, Lee MY et al. (2008). MicroRNA miR-199a* regulates the MET proto-oncogene and the downstream extracellular signal-regulated kinase 2 (ERK2). J Biol Chem 283: 18158-18166.
20. Koch LK, Zhou H, Ellinger J, Biermann K, Holler T, von Rucker A et al. (2008). Stem cell marker expression in small cell lung carcinoma and developing lung tissue. Hum Pathol 39: 1597-1605.
21. Lee DY, Shatseva T, Jeyapalan Z, Du WW, Deng Z, Yang BB. (2009). A 30-untranslated region (30UTR) induces organ adhesion by regulating miR-199a* functions. PLoS One 4: e4527.
22. Lee JW, Choi CH, Choi JJ, Park YA, Kim SJ, Hwang SY et al. (2008). Altered MicroRNA expression in cervical carcinomas. Clin Cancer Res 14: 2535-2542.
23. Li LC, Zhao H, Nakajima K, Oh BR, Ribeiro Filho LA, Carroll P et al. (2001). Methylation of the E-cadherin gene promoter correlates with progression of prostate cancer. J Urol 166: 705-709. (Pubitemid 32652304)
24. Li Y, Tabatabai ZL, Lee TL, Hatakeyama S, Ohyama C, Chan WY et al. (2007). The Y-encoded TSPY protein: a significant marker potentially plays a role in the pathogenesis of testicular germ cell tumors. Hum Pathol 38: 1470-1481. (Pubitemid 47418969)
25. Lin EA, Kong L, Bai XH, Luan Y, Liu CJ. (2009). miR-199a, a bone morphogenic protein 2-responsive MicroRNA, regulates chondrogenesis via direct targeting to Smad1. J Biol Chem 284: 11326-11335.
26. Lujambio A, Calin GA, Villanueva A, Ropero S, Sanchez-Cespedes M, Blanco D et al. (2008). A microRNA DNA methylation signature for human cancer metastasis. Proc Natl Acad Sci USA 105: 13556-13561.
27. Nam EJ, Yoon H, Kim SW, Kim H, Kim YT, Kim JH et al. (2008). MicroRNA expression profiles in serous ovarian carcinoma. Clin Cancer Res 14: 2690-2695.
28. Netto GJ, Nakai Y, Nakayama M, Jadallah S, Toubaji A, Nonomura N et al. (2008). Global DNA hypomethylation in intratubular germ cell neoplasia and seminoma, but not in nonseminomatous male germ cell tumors. Mod Pathol 21: 1337-1344.
29. Pang AL, Peacock S, Johnson W, Bear DH, Rennert OM, Chan WY. (2009). Cloning, characterization, and expression analysis of the novel acetyltransferase retrogene Ard1b in the mouse. Biol Reprod 81: 302-309.
30. Peltier HJ, Latham GJ. (2008). Normalization of microRNA expression levels in quantitative RT-PCR assays: identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA 14: 844-852. (Pubitemid 351574906)
31. Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J et al. (2009). Downregulation of miR-199a derepresses hypoxia-inducible factor-1alpha and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res 104: 879-886.
32. Sahai E. (2005). Mechanisms of cancer cell invasion. Curr Opin Genet Dev 15: 87-96. (Pubitemid 40127636)
33. Santhakumar D, Forster T, Laqtom NN, Fragkoudis R, Dickinson P, Abreu-Goodger C et al. (2010). Combined agonist-antagonist genome-wide functional screening identifies broadly active antiviral microRNAs. Proc Natl Acad Sci USA 107: 13830-13835.
34. Schopperle WM, Kershaw DB, DeWolf WC. (2003). Human embryonal carcinoma tumor antigen, Gp200/GCTM-2, is podoca-lyxin. Biochem Biophys Res Commun 300: 285-290. (Pubitemid 38375807)
35. Singal R, Ferris R, Little JA, Wang SZ, Ginder GD. (1997). Methylation of the minimal promoter of an embryonic globin gene silences transcription in primary erythroid cells. Proc Natl Acad Sci USA 94: 13724-13729. (Pubitemid 28009650)
36. Smiraglia DJ, Szymanska J, Kraggerud SM, Lothe RA, Peltomaki P, Plass C. (2002). Distinct epigenetic phenotypes in seminomatous and nonseminomatous testicular germ cell tumors. Oncogene 21: 3909-3916. (Pubitemid 34620859)
37. Somasiri A, Nielsen JS, Makretsov N, McCoy ML, Prentice L, Gilks CB et al. (2004). Overexpression of the anti-adhesin podocalyxin is an independent predictor of breast cancer progression. Cancer Res 64: 5068-5073. (Pubitemid 39006520)
38. Takeda T, Go WY, Orlando RA, Farquhar MG. (2000). Expression of podocalyxin inhibits cell-cell adhesion and modifies junctional properties in Madin-Darby canine kidney cells. Mol Biol Cell 11: 3219-3232. (Pubitemid 32107095)
39. Tsai WC, Hsu PW, Lai TC, Chau GY, Lin CW, Chen CM et al. (2009). MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology 49: 1571-1582.
40. Tsai ZY, Singh S, Yu SL, Kao LP, Chen BZ, Ho BC et al. (2010). Identification of microRNAs regulated by activin A in human embryonic stem cells. J Cell Biochem 109: 93-102.
41. Ueda T, Volinia S, Okumura H, Shimizu M, Taccioli C, Rossi S et al. (2009). Relation between microRNA expression and progression and prognosis of gastric cancer: a microRNA expression analysis. Lancet Oncol 11: 136-146.
42. Watts GS, Futscher BW, Holtan N, Degeest K, Domann FE, Rose SL. (2008). DNA methylation changes in ovarian cancer are cumulative with disease progression and identify tumor stage. BMC Med Genomics 1: 47.
43. Worley LA, Long MD, Onken MD, Harbour JW. (2008). Micro-RNAs associated with metastasis in uveal melanoma identified by multiplexed microarray profiling. Melanoma Res 18: 184-190. (Pubitemid 351684663)
44. Yin G, Chen R, Alvero AB, Fu HH, Holmberg J, Glackin C et al. (2010). TWISTing stemness, inflammation and proliferation of epithelial ovarian cancer cells through MIR199A2/214. Oncogene 29: 3545-3553.
45. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. (2008). MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18: 350-359. (Pubitemid 351333899)