Hypomethylation of retrotransposable elements correlates with genomic instability in non-small cell lung cancer

International Journal of Cancer

Volumn 124, Issue 1, 2009, Pages 81-87

  Daskalos, Alexandros ^a   Nikolaidis, Georgios ^a   Xinarianos, George ^a   Savvari, Paraskevi ^b   Cassidy, Adrian ^a   Zakopoulou, Roubini ^a,b   Kotsinas, Athanasios ^b   Gorgoulis, Vassilis ^b   Field, John K ^a   Liloglou, Triantafillos ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Alu; Genomic instability; Hypomethylation; LINE 1; Lung cancer

Indexed keywords

5 AZA 2' DEOXYCYTIDINE;

ADULT; AGED; ALU SEQUENCE; ARTICLE; CANCER CELL CULTURE; CHROMOSOME 13Q; CHROMOSOME 17P; CHROMOSOME 3P; CHROMOSOME 5Q; CHROMOSOME 9P; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION; FEMALE; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG NON SMALL CELL CANCER; MALE; MICROSATELLITE MARKER; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PYROSEQUENCING; RETROPOSON; GENETICS; HUMAN GENOME; LONG INTERSPERSED REPEAT; LUNG TUMOR; MIDDLE AGED; PATHOLOGY; TUMOR CELL LINE;

AGED; AGED, 80 AND OVER; ALU ELEMENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DNA METHYLATION; FEMALE; GENOME, HUMAN; GENOMIC INSTABILITY; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; LUNG NEOPLASMS; MALE; MIDDLE AGED; RETROELEMENTS;

EID: 58149399844     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23849     Document Type: Article

References (50)

1. Babushok DV, Kazazian HH, Jr. Progress in understanding the biology of the human mutagen LINE-1. Hum Mutat 2007;28:527-39.
2. Kazazian HH, Jr. Mobile elements: drivers of genome evolution. Science 2004;303:1626-32.
3. Sassaman DM, Dombroski BA, Moran JV, Kimberland ML, Naas TP, DeBerardinis RJ, Gabriel A, Swergold GD, Kazazian HH, Jr. Many human L1 elements are capable of retrotransposition. Nat Genet 1997;16:37-43.
4. Ostertag EM, Kazazian HH, Jr. Biology of mammalian L1 retrotransposons. Annu Rev Genet 2001;35:501-38.
5. Yang N, Kazazian HH, Jr. L1 retrotransposition is suppressed by endogenously encoded small interfering RNAs in human cultured cells. Nat Struct Mol Biol 2006;13:763-71.
6. Soifer HS, Rossi JJ. Small interfering RNAs to the rescue: blocking L1 retrotransposition. Nat Struct Mol Biol 2006;13:758-9.
7. Schulz WA. L1 retrotransposons in human cancers. J Biomed Biotechnol 2006;2006:83672.
8. Gilbert N, Lutz-Prigge S, Moran JV. Genomic deletions created upon LINE-1 retrotransposition. Cell 2002;110:315-25.
9. Symer DE, Connelly C, Szak ST, Caputo EM, Cost GJ, Parmigiani G, Boeke JD. Human l1 retrotransposition is associated with genetic instability in vivo. Cell 2002;110:327-38.
10. Kazazian HH, Jr, Goodier JL. LINE drive. retrotransposition and genome instability. Cell 2002;110:277-80.
11. Dewannieux M, Esnault C, Heidmann T. LINE-mediated retrotransposition of marked Alu sequences. Nat Genet 2003;35:41-8.
12. Mighell AJ, Markham AF, Robinson PA. Alu sequences. FEBS Lett 1997;417:1-5.
13. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene 2002;21:5400-13.
14. Suter CM, Martin DI, Ward RL. Hypomethylation of L1 retrotransposons in colorectal cancer and adjacent normal tissue. Int J Colorectal Dis 2004;19:95-101.
15. Chalitchagorn K, Shuangshoti S, Hourpai N, Kongruttanachok N, Tangkijvanich P, Thong-ngam D, Voravud N, Sriuranpong V, Mutirangura A. Distinctive pattern of LINE-1 methylation level in normal tissues and the association with carcinogenesis. Oncogene 2004;23: 8841-6.
16. Cho NY, Kim BH, Choi M, Yoo EJ, Moon KC, Cho YM, Kim D, Kang GH. Hypermethylation of CpG island loci and hypomethylation of LINE-1 and Alu repeats in prostate adenocarcinoma and their relationship to clinicopathological features. J Pathol 2007;211:269-77.
17. Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim Biophys Acta 2007;1775:138-62.
18. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M, Laird PW. Analysis of repetitive element DNA methylation by methylight. Nucleic Acids Res 2005;33:6823-36.
19. Choi IS, Estecio MR, Nagano Y, Kim do H, White JA, Yao JC, Issa JP, Rashid A. Hypomethylation of LINE-1 and Alu in well-differentiated neuroendocrine tumors (pancreatic endocrine tumors and carcinoid tumors). Mod Pathol 2007;20:802-10.
20. Ehrlich M, Woods CB, Yu MC, Dubeau L, Yang F, Campan M, Weisenberger DJ, Long T, Youn B, Fiala ES, Laird PW. Quantitative analysis of associations between DNA hypermethylation, hypomethylation, and DNMT RNA levels in ovarian tumors. Oncogene 2006;25:2636-45.
21. Gaudet F, Hodgson JG, Eden A, Jackson-Grusby L, Dausman J, Gray JW, Leonhardt H, Jaenisch R. Induction of tumors in mice by genomic hypomethylation. Science 2003;300:489-92.
22. Eden A, Gaudet F, Waghmare A, Jaenisch R. Chromosomal instability and tumors promoted by DNA hypomethylation. Science 2003;300:455.
23. Belgnaoui SM, Gosden RG, Semmes OJ, Haoudi A. Human LINE-1 retrotransposon induces DNA damage and apoptosis in cancer cells. Cancer Cell Int 2006;6:13.
24. Sato M, Shames DS, Gazdar AF, Minna JD. A translational view of the molecular pathogenesis of lung cancer. J Thorac Oncol 2007;2:327-43.
25. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, Cantor CR, Field JK, van den Boom D. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci USA 2005;102:15785-90.
26. Ehrich M, Field JK, Liloglou T, Xinarianos G, Oeth P, Nelson MR, Cantor CR, van den Boom D. Cytosine methylation profiles as a molecular marker in non-small cell lung cancer. Cancer Res 2006;66:10911-18.
27. Field JK, Liloglou T, Warrak S, Burger M, Becker E, Berlin K, Nimmrich I, Maier S. Methylation discriminators in NSCLC identified by a microarray based approach. Int J Oncol 2005;27:105-11.
28. Shames DS, Girard L, Gao B, Sato M, Lewis CM, Shivapurkar N, Jiang A, Perou CM, Kim YH, Pollack JR, Fong KM, Lam CL, et al. A genome-wide screen for promoter methylation in lung cancer identifies novel methylation markers for multiple malignancies. PLoS Med 2006;3:e486.
29. Liloglou T, Maloney P, Xinarianos G, Fear S, Field JK. Sensitivity and limitations of high throughput fluorescent microsatellite analysis for the detection of allelic imbalance: application in lung tumors. Int J Oncol 2000;16:5-14.
30. Liloglou T, Maloney P, Xinarianos G, Hulbert M, Walshaw MJ, Gosney JR, Turnbull L, Field JK. Cancer-specific genomic instability in bronchial lavage: a molecular tool for lung cancer detection. Cancer Res 2001;61:1624-8.
31. Roman-Gomez J, Jimenez-Velasco A, Agirre X, Cervantes F, Sanchez J, Garate L, Barrios M, Castillejo JA, Navarro G, Colomer D, Prosper F, Heiniger A, et al. Promoter hypomethylation of the LINE-1 retrotransposable elements activates sense/antisense transcription and marks the progression of chronic myeloid leukemia. Oncogene 2005;24:7213-23.
32. Wallace MR, Andersen LB, Saulino AM, Gregory PE, Glover TW, Collins FS. A de novo Alu insertion results in neurofibromatosis type 1. Nature 1991;353:864-6.
33. Rauch T, Wang Z, Zhang X, Zhong X, Wu X, Lau SK, Kernstine KH, Riggs AD, Pfeifer GP. Homeobox gene methylation in lung cancer studied by genome-wide analysis with a microarray-based methylated CpG island recovery assay. Proc Natl Acad Sci USA 2007;104:5527-32.
34. Rauch TA, Zhong X, Wu X, et al. High-resolution mapping of DNA hypermethylation and hypomethylation in lung cancer. Proc Natl Acad Sci USA 2008;105:252-7.
35. Estecio MR, Gharibyan V, Shen L, Ibrahim AE, Doshi K, He R, Jelinek J, Yang AS, Yan PS, Huang TH, Tajara EH, Issa JP. LINE-1 hypomethylation in cancer is highly variable and inversely correlated with microsatellite instability. PLoS ONE 2007;2:e399.
36. Lin CS, Goldthwait DA, Samols D. Identification of Alu transposition in human lung carcinoma cells. Cell 1988;54:153-9.
37. Kubo S, Seleme MC, Soifer HS, Perez JL, Moran JV, Kazazian HH, Jr, Kasahara N. L1 retrotransposition in nondividing and primary human somatic cells. Proc Natl Acad Sci USA 2006;103:8036-41.
38. Morrish TA, Garcia-Perez JL, Stamato TD, Taccioli GE, Sekiguchi J, Moran JV. Endonuclease-independent LINE-1 retrotransposition at mammalian telomeres. Nature 2007;446:208-12.
39. Bratthauer GL, Cardiff RD, Fanning TG. Expression of LINE-1 retrotransposons in human breast cancer. Cancer 1994;73:2333-6.
40. Florl AR, Lower R, Schmitz-Drager BJ, Schulz WA. DNA methylation and expression of LINE-1 and HERV-K provirus sequences in urothelial and renal cell carcinomas. Br J Cancer 1999;80:1312-21.
41. Muckenfuss H, Hamdorf M, Held U, Perkovic M, Lower J, Cichutek K, Flory E, Schumann GG, Münk C. APOBEC3 proteins inhibit human LINE-1 retrotransposition. J Biol Chem 2006;281:22161-72.
42. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ, Heidmann T, Schwartz O. APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 2005;433:430-3.
43. Goodier JL, Zhang L, Vetter MR, Kazazian HH, Jr. LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex. Mol Cell Biol 2007;27:6469-83.
44. Rodriguez J, Vives L, Jordà M, Morales C, Muñoz M, Vendrell E, Peinado MA. Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res 2008;36:770-84.
45. Lyko F, Brown R. DNA methyltransferase inhibitors and the development of epigenetic cancer therapies. J Natl Cancer Inst 2005;97:1498-506.
46. Issa JP. DNA methylation as a therapeutic target in cancer. Clin Cancer Res 2007;13:1634-7.
47. Appleton K, Mackay HJ, Judson I, Plumb JA, McCormick C, Strathdee G, Lee C, Barrett S, Reade S, Jadayel D, Tang A, Bellenger K, et al. Phase I and pharmacodynamic trial of the DNA methyltransferase inhibitor decitabine and carboplatin in solid tumors. J Clin Oncol 2007;25:4603-9.
48. Oki Y, Jelinek J, Shen L, Kantarjian HM, Issa JP. Induction of hypomethylation and molecular response after decitabine therapy in patients with chronic myelomonocytic leukemia. Blood 2008;111:2382-4.
49. Glasspool RM, Teodoridis JM, Brown R. Epigenetics as a mechanism driving polygenic clinical drug resistance. Br J Cancer 2006;94:1087-92.
50. Ehrlich M. The controversial denouement of vertebrate DNA methylation research. Biochemistry 2005;70:568-75.