LINE-1 retrotransposition events regulate gene expression after X-ray irradiation

DNA and Cell Biology

Volumn 31, Issue 9, 2012, Pages 1458-1467

  Banaz Yaşar, Ferya ^a   Gedik, Nilgün ^a   Karahan, Selda ^a   Diaz Carballo, David ^a   Bongartz, Birthe M ^a   Ergün, Süleyman ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2AX; PROTEIN P53;

ARTICLE; CELL CLONE; CELL PROLIFERATION; CELL PROTECTION; CELL STRAIN; CONTROLLED STUDY; DNA DAMAGE; DNA INTEGRATION; DNA STRAND BREAKAGE; DNA TRANSPOSITION; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INSERTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LONG INTERSPERSED NUCLEAR ELEMENT 1; LONG INTERSPERSED REPEAT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RADIATION DOSE; RETROPOSON; REVERSE TRANSCRIPTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE; X IRRADIATION;

CELL LINE; CELL PROLIFERATION; CLONE CELLS; DNA BREAKS, DOUBLE-STRANDED; DOSE-RESPONSE RELATIONSHIP, RADIATION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; PHOSPHORYLATION; TUMOR SUPPRESSOR PROTEIN P53; X-RAYS;

EID: 84865748132     PISSN: 10445498     EISSN: 15577430     Source Type: Journal    
DOI: 10.1089/dna.2012.1676     Document Type: Article

References (38)

1. Asakawa, J., Kuick, R., Kodaira, M., Nakamura, N., Katayama, H., Pierce, D., Funamoto, S., Preston, D., Satoh, C., Neel, J. V., and Hanash, S. (2004). A genome scanning approach to assess the genetic effects of radiation in mice and humans. Radiat Res 161, 380-390. (Pubitemid 40754234)
2. Banaz-Yasar, F., Lennartz, K., Winterhager, E., and Gellhaus, A. (2008). Radiation-induced bystander effects in malignant trophoblast cells are independent from gap junctional communication. J Cell Biochem 103, 149-161.
3. Banaz-Yasar, F., Steffen, G., Hauschild, J., Bongartz, B. M., Schumann, G. G., and Ergun, S. (2010). LINE-1 retrotransposition events affect endothelial proliferation and migration. Histochem Cell Biol 134, 581-589.
4. Belancio, V. P., Deininger, P. L., and Roy-Engel, A. M. (2009). LINE dancing in the human genome: transposable elements and disease. Genome Med 1, 97.
5. Belancio, V. P., Hedges, D. J., and Deininger, P. (2006). LINE-1 RNA splicing and influences on mammalian gene expression. Nucleic Acids Res 34, 1512-1521.
6. Belgnaoui, S. M., Gosden, R. G., Semmes, O. J., and Haoudi, A. (2006). Human LINE-1 retrotransposon induces DNA damage and apoptosis in cancer cells. Cancer Cell Int 6, 13.
7. Burma, S., Chen, B. P., Murphy, M., Kurimasa, A., and Chen, D. J. (2001). ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 276, 42462-42467.
8. Callahan, K. E., Hickman, A. B., Jones, C. E., Ghirlando, R., and Furano, A. V. (2012). Polymerization and nucleic acid-binding properties of human L1 ORF1 protein. Nucleic Acids Res 40, 813-827.
9. Cordaux, R., and Batzer, M. A. (2009). The impact of retrotransposons on human genome evolution. Nat Rev Genet 10, 691-703.
10. Dale, R., and Carabe-Fernandez, A. (2005). The radiobiology of conventional radiotherapy and its application to radionuclide therapy. Cancer Biother Radiopharm 20, 47-51. (Pubitemid 40478521)
11. Edgell, C. J., McDonald, C. C., and Graham, J. B. (1983). Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci U S A 80, 3734-3737. (Pubitemid 13063134)
12. El-Sawy, M., Kale, S. P., Dugan, C., Nguyen, T. Q., Belancio, V., Bruch, H., Roy-Engel, A. M., and Deininger, P. L. (2005). Nickel stimulates L1 retrotransposition by a post-transcriptional mechanism. J Mol Biol 354, 246-257. (Pubitemid 41579844)
13. Ergun, S., Buschmann, C., Heukeshoven, J., Dammann, K., Schnieders, F., Lauke, H., Chalajour, F., Kilic, N., Stratling, W. H., and Schumann, G. G. (2004). Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues. J Biol Chem 279, 27753-27763. (Pubitemid 38812617)
14. Farkash, E. A., Kao, G. D., Horman, S. R., and Prak, E. T. (2006). Gamma radiation increases endonuclease-dependent L1 retrotransposition in a cultured cell assay. Nucleic Acids Res 34, 1196-1204.
15. Faulkner, G. J., Kimura, Y., Daub, C. O., Wani, S., Plessy, C., Irvine, K. M., Schroder, K., Cloonan, N., Steptoe, A. L., Lassmann, T., Waki, K., Hornig, N., Arakawa, T., Takahashi, H., Kawai, J., Forrest, A. R., Suzuki, H., Hayashizaki, Y., Hume, D. A., Orlando, V., Grimmond, S. M., and Carninci, P. (2009). The regulated retrotransposon transcriptome of mammalian cells. Nat Genet 41, 563-571.
16. Feng, Q., Moran, J. V., Kazazian, H. H., Jr., and Boeke, J. D. (1996). Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87, 905-916. (Pubitemid 26404289)
17. Gasior, S. L., Roy-Engel, A. M., and Deininger, P. L. (2008). ERCC1/XPF limits L1 retrotransposition. DNA Repair (Amst) 7, 983-989.
18. Gasior, S. L., Wakeman, T. P., Xu, B., and Deininger, P. L. (2006). The human LINE-1 retrotransposon creates DNA doublestrand breaks. J Mol Biol 357, 1383-1393.
19. Haoudi, A., Semmes, O. J., Mason, J. M., and Cannon, R. E. (2004). Retrotransposition-competent human line-1 induces apoptosis in cancer cells with intact p53. J Biomed Biotechnol 2004, 185-194. (Pubitemid 40128954)
20. Harris, C. R., Dewan, A., Zupnick, A., Normart, R., Gabriel, A., Prives, C., Levine, A. J., and Hoh, J. (2009). p53 responsive elements in human retrotransposons. Oncogene 28, 3857-3865.
21. Kale, S. P., Moore, L., Deininger, P. L., and Roy-Engel, A. M. (2005). Heavy metals stimulate human LINE-1 retrotransposition. Int J Environ Res Public Health 2, 14-23. (Pubitemid 40973381)
22. Kazazian, H. H., Jr. (2004). Mobile elements: drivers of genome evolution. Science 303, 1626-1632. (Pubitemid 38338313)
23. Kirilyuk, A., Tolstonog, G. V., Damert, A., Held, U., Hahn, S., Lower, R., Buschmann, C., Horn, A. V., Traub, P., and Schumann, G. G. (2008). Functional endogenous LINE-1 retrotransposons are expressed and mobilized in rat chloroleukemia cells. Nucleic Acids Res 36, 648-665. (Pubitemid 351250455)
24. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., Fitz Hugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., Le Vine, R., McEwan, P., McKernan, K., Meldrim, J., Mesirov, J. P., Miranda, C., Morris, W., Naylor, J., Raymond, C., Rosetti, M., Santos, R., Sheridan, A., Sougnez, C., Stange-Thomann, N., Stojanovic, N., Subramanian, A., Wyman, D., Rogers, J., Sulston, J., Ainscough, R., Beck, S., Bentley, D., Burton, J., Clee, C., Carter, N., Coulson, A., Deadman, R., Deloukas, P., Dunham, A., Dunham, I., Durbin, R., French, L., Grafham, D., Gregory, S., Hubbard, T., Humphray, S., Hunt, A., Jones, M., Lloyd, C., McMurray, A., Matthews, L., Mercer, S., Milne, S., Mullikin, J. C., Mungall, A., Plumb, R., Ross, M., Shownkeen, R., Sims, S., Waterston, R. H., Wilson, R. K., Hillier, L. W., McPherson, J. D., Marra, M. A., Mardis, E. R., Fulton, L. A., Chinwalla, A. T., Pepin, K. H., Gish, W. R., Chissoe, S. L., Wendl, M. C., Delehaunty, K. D., Miner, T. L., Delehaunty, A., Kramer, J. B., Cook, L. L., Fulton, R. S., Johnson, D. L., Minx, P. J., Clifton, S. W., Hawkins, T., Branscomb, E., Predki, P., Richardson, P., Wenning, S., Slezak, T., Doggett, N., Cheng, J. F., Olsen, A., Lucas, S., Elkin, C., Uberbacher, E., Frazier, M., et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860-921. (Pubitemid 32165345)
25. Lane, D. P. (1992). Cancer. p53, guardian of the genome. Nature 358, 15-16.
26. Luan, D. D., and Eickbush, T. H. (1996). Downstream 28S gene sequences on the RNA template affect the choice of primer and the accuracy of initiation by the R2 reverse transcriptase. Mol Cell Biol 16, 4726-4734. (Pubitemid 26272126)
27. McClintock, B. (1956). Controlling elements and the gene. Cold Spring Harb Symp Quant Biol 21, 197-216.
28. Meyer, T. J., Srikanta, D., Conlin, E. M., and Batzer, M. A. (2010). Heads or tails: L1 insertion-associated 5' homopolymeric sequences. Mob DNA 1, 7.
29. Moran, J. V., Holmes, S. E., Naas, T. P., DeBerardinis, R. J., Boeke, J. D., and Kazazian, H. H., Jr. (1996). High frequency retrotransposition in cultured mammalian cells. Cell 87, 917-927. (Pubitemid 26404290)
30. Oricchio, E., Sciamanna, I., Beraldi, R., Tolstonog, G. V., Schumann, G. G., and Spadafora, C. (2007). Distinct roles for LINE-1 and HERV-K retroelements in cell proliferation, differentiation and tumor progression. Oncogene 26, 4226-4233. (Pubitemid 46975802)
31. Rangwala, S. H., and Kazazian, H. H., Jr. (2009). The L1 retrotransposition assay: a retrospective and toolkit. Methods 49, 219-226.
32. Rogakou, E. P., Boon, C., Redon, C., and Bonner, W. M. (1999). Megabase chromatin domains involved in DNA doublestrand breaks in vivo. J Cell Biol 146, 905-916.
33. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S., and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273, 5858-5868. (Pubitemid 28124064)
34. Rogakou, E. P., and Sekeri-Pataryas, K. E. (1999). Histone variants of H2A and H3 families are regulated during in vitro aging in the same manner as during differentiation. Exp Gerontol 34, 741-754. (Pubitemid 29430130)
35. Sassaman, D. M., Dombroski, B. A., Moran, J. V., Kimberland, M. L., Naas, T. P., DeBerardinis, R. J., Gabriel, A., Swergold, G. D., and Kazazian, H. H., Jr. (1997) Many human L1 elements are capable of retrotransposition. Nat Genet 16, 37-43. (Pubitemid 27198154)
36. Schulz, W. A. (2006). L1 retrotransposons in human cancers. J Biomed Biotechnol 2006, 83672.
37. Sciamanna, I., Landriscina, M., Pittoggi, C., Quirino, M., Mearelli, C., Beraldi, R., Mattei, E., Serafino, A., Cassano, A., Sinibaldi-Vallebona, P., Garaci, E., Barone, C., and Spadafora, C. (2005) Inhibition of endogenous reverse transcriptase antagonizes human tumor growth. Oncogene 24, 3923-3931. (Pubitemid 40896404)
38. Servomaa, K., and Rytomaa, T. (1990). UV light and ionizing radiations cause programmed death of rat chloroleukaemia cells by inducing retropositions of a mobile DNA element (L1Rn). Int J Radiat Biol 57, 331-343. (Pubitemid 20088859)