Nickel stimulates L1 retrotransposition by a post-transcriptional mechanism

Journal of Molecular Biology

Volumn 354, Issue 2, 2005, Pages 246-257

  El Sawy, Mohammed ^a   Kale, Shubha P ^b   Dugan, Christine ^a   Nguyen, Thuc Quyen ^b   Belancio, Victoria ^a   Bruch, Heather ^a   Roy Engel, Astrid M ^a   Deininger, Prescott L ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b XAVIER UNIVERSITY OF LOUISIANA   (United States)

Author keywords

DNA repair; Genetic instability; L1; Nickel; Retroelement

Indexed keywords

COBALT CHLORIDE; ENVIRONMENTAL POISON; HEAVY METAL; MAGNESIUM CHLORIDE; NICKEL CHLORIDE; TOXIC SUBSTANCE;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DNA DAMAGE; DNA NICK TRANSLATION; DNA REPAIR; DRUG EFFECT; FEMALE; GENETIC DAMAGE; GENETIC STABILITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RETROPOSON; STIMULATION;

ANIMALIA;

EID: 27644569729     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.09.050     Document Type: Article

References (71)

1. E.S. Lander, L.M. Linton, B. Birren, C. Nusbaum, M.C. Zody, and J. Baldwin Initial sequencing and analysis of the human genome. International Human Genome Sequencing Consortium Nature 409 2001 860 921
2. J.M. Chen, P.D. Stenson, D.N. Cooper, and C. Ferec A systematic analysis of LINE-1 endonuclease-dependent retrotranspositional events causing human genetic disease Hum. Genet. 117 2005 411 427
3. F. Gaudet, W.M. Rideout III, A. Meissner, J. Dausman, H. Leonhardt, and R. Jaenisch Dnmt1 expression in pre- and postimplantation embryogenesis and the maintenance of IAP silencing Mol. Cell Biol. 24 2004 1640 1648
4. F. Yu, N. Zingler, G. Schumann, and W.H. Stratling Methyl-CpG-binding protein 2 represses LINE-1 expression and retrotransposition but not Alu transcription Nucl. Acids Res. 29 2001 4493 4501
5. J. Huang, T. Fan, Q. Yan, H. Zhu, S. Fox, and H.J. Issaq Lsh, an epigenetic guardian of repetitive elements Nucl. Acids Res. 32 2004 5019 5028
6. D. Bourc'his, and T.H. Bestor Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L Nature 431 2004 96 99
7. P. Capy, G. Gasperi, C. Biemont, and C. Bazin Stress and transposable elements: co-evolution or useful parasites? Heredity 85 2000 101 106
8. K.P. Lu, L.M. Hallberg, J. Tomlinson, and K.S. Ramos Benzo(a)pyrene activates L1Md retrotransposon and inhibits DNA repair in vascular smooth muscle cells Mutat. Res. 454 2000 35 44
9. J.D. Boeke LINEs and Alus-the polyA connection Nature Genet. 16 1997 6 7
10. C. Esnault, J. Maestre, and T. Heidmann Human LINE retrotransposons generate processed pseudogenes Nature Genet. 24 2000 363 367
11. M. Dewannieux, C. Esnault, and T. Heidmann LINE-mediated retrotransposition of marked Alu sequences Nature Genet. 35 2003 41 48
12. G. Grimaldi, J. Skowronski, and M.F. Singer Defining the beginning and end of KpnI family segments EMBO J. 3 1984 1753 1759
13. B. Brouha, J. Schustak, R.M. Badge, S. Lutz-Prigge, A.H. Farley, J.V. Moran, and H.H. Kazazian Jr L1s account for the bulk of retrotransposition in the human population Proc. Natl Acad. Sci. USA 100 2003 5280 5285
14. H.H.J. Kazazian Mobile elements and disease Curr. Opin. Genet. Dev. 8 1998 343 350
15. X. Li, W.A. Scaringe, K.A. Hill, S. Roberts, A. Mengos, and D. Careri Frequency of recent retrotransposition events in the human factor IX gene Hum. Mutat. 17 2001 511 519
16. P.L. Deininger, and M.A. Batzer Alu repeats and human disease Mol. Genet. Metab. 67 1999 183 193
17. E.M. Ostertag, and H.H. Kazazian Jr Twin priming: a proposed mechanism for the creation of inversions in L1 retrotransposition Genome Res. 11 2001 2059 2065
18. B.A. Dombroski, S.L. Mathias, E. Nanthakumar, A.F. Scott, and H.H. Kazazian Isolation of an active human transposable element Science 254 1991 1805 1810
19. S.E. Holmes, B.A. Dombroski, C.M. Krebs, C.D. Boehm, and H.H. Kazazian Jr A new retrotransposable human L1 element from the LRE2 locus on chromosome 1q produces a chimaeric insertion Nature Genet. 7 1994 143 148
20. J.V. Moran, S.E. Holmes, T.P. Naas, R.J. DeBerardinis, J.D. Boeke, and H.H. Kazazian Jr Jr High frequency retrotransposition in cultured mammalian cells Cell 87 1996 917 927
21. M.L. Kimberland, V. Divoky, J. Prchal, U. Schwahn, W. Berger, and H.H. Kazazian Jr Full-length human L1 insertions retain the capacity for high frequency retrotransposition in cultured cells Hum. Mol. Genet. 8 1999 1557 1560
22. S.A. Trelogan, and S.L. Martin Tightly regulated, developmentally specific expression of the first open reading frame from LINE-1 during mouse embryogenesis Proc. Natl Acad. Sci. USA 92 1995 1520 1524
23. S. Ergun, C. Buschmann, J. Heukeshoven, K. Dammann, F. Schnieders, and H. Lauke Cell type-specific expression of LINE-1 open reading frames 1 and 2 in fetal and adult human tissues J. Biol. Chem. 279 2004 27753 27763
24. A.R. Muotri, V.T. Chu, M.C. Marchetto, W. Deng, J.V. Moran, and F.H. Gage Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition Nature 435 2005 903 910
25. M.F. Singer, V. Krek, J.P. McMillan, G.D. Swergold, and R.E. Thayer LINE-1: a human transposable element Gene 135 1993 183 188
26. J. Skowronski, T.G. Fanning, and M.F. Singer Unit-length line-1 transcripts in human teratocarcinoma cells Mol. Cell Biol. 8 1988 1385 1397
27. H.L. Asch, E. Eliacin, T.G. Fanning, J.L. Connolly, G. Bratthauer, and B.B. Asch Comparative expression of the LINE-1 p40 protein in human breast carcinomas and normal breast tissues Oncol. Res. 8 1996 239 247
28. G.L. Bratthauer, R.D. Cardiff, and T.G. Fanning Expression of LINE-1 retrotransposons in human breast cancer Cancer 73 1994 2333 2336
29. G.L. Bratthauer, and T.G. Fanning Active LINE-1 retrotransposons in human testicular cancer Oncogene 7 1992 507 510
30. T.P. Naas, R.J. DeBerardinis, J.V. Moran, E.M. Ostertag, S.F. Kingsmore, and M.F. Seldin An actively retrotransposing, novel subfamily of mouse L1 elements EMBO J. 17 1998 590 597
31. T.A. Morrish, N. Gilbert, J.S. Myers, B.J. Vincent, T.D. Stamato, and G.E. Taccioli DNA repair mediated by endonuclease-independent LINE-1 retrotransposition Nature Genet. 31 2002 159 165
32. J.S. Han, and J.D. Boeke A highly active synthetic mammalian retrotransposon Nature 429 2004 314 318
33. V. Perepelitsa-Belancio, and P. Deininger RNA truncation by premature polyadenylation attenuates human mobile element activity Nature Genet. 35 2003 363 366
34. T.H. Eickbush Repair by retrotransposition Nature Genet. 31 2002 126 127
35. S.P. Kale, L. Moore, P.L. Deininger, and A.M. Roy-Engel Heavy metals stimulate human LINE-1 retrotransposition Int. J. Environ. Res. Public Health 2 2005 84 90
36. N.A. Elghany, M.C. Schumacher, M.L. Slattery, D.W. West, and J.S. Lee Occupation, cadmium exposure, and prostate cancer Epidemiology 1 1990 107 115
37. M.P. Waalkes, S. Rehm, C.W. Riggs, R.M. Bare, D.E. Devor, and L.A. Poirier Cadmium carcinogenesis in male Wistar [Crl:(WI)BR] rats: dose-response analysis of effects of zinc on tumor induction in the prostate, in the testes, and at the injection site Cancer Res. 49 1989 4282 4288
38. S. Takenaka, H. Oldiges, H. Konig, D. Hochrainer, and G. Oberdorster Carcinogenicity of cadmium chloride aerosols in W rats J. Natl Cancer Inst. 70 1983 367 373
39. F.W. Sunderman Jr, R.M. Maenza, S.M. Hopfer, J.M. Mitchell, P.R. Allpass, and I. Damjanov Induction of renal cancers in rats by intrarenal injection of nickel subsulfide J. Environ. Pathol. Toxicol. 2 1979 1511 1527
40. A.V. Saknyn′, and V.A. Blokhin Development of malignant tumors in rats under the influence of nickel-containing aerosols Vopr. Onkol. 24 1978 44 48
41. I.A.R.C. Meeting of the IARC working group on beryllium, cadmium, mercury and exposures in the glass manufacturing industry Scand. J. Work Environ. Health 19 1993 360 363
42. C.B. Klein, K. Frenkel, and M. Costa The role of oxidative processes in metal carcinogenesis Chem. Res. Toxicol. 4 1991 592 604
43. K.S. Kasprzak Possible role of oxidative damage in metal-induced carcinogenesis Cancer Invest. 13 1995 411 430
44. S. Kawanishi, Y. Hiraku, M. Murata, and S. Oikawa The role of metals in site-specific DNA damage with reference to carcinogenesis(1,2) Free Radic. Biol. Med. 32 2002 822 832
45. H. Cangul, L. Broday, K. Salnikow, J. Sutherland, W. Peng, and Q. Zhang Molecular mechanisms of nickel carcinogenesis Toxicol. Letters 127 2002 69 75
46. R. Kowara, A. Karaczyn, R.Y.S. Cheng, K. Salnikow, and K.S. Kasprzak Microarray analysis of altered gene expression in murine fibroblasts transformed by nickel(II) to nickel(II)-resistant malignant phenotype Toxicol. Appl. Pharmacol. 205 2005 1 10
47. T. Zhou, X. Jia, R.E. Chapin, R.R. Maronpot, M.W. Harris, and J. Liu Cadmium at a non-toxic dose alters gene expression in mouse testes Toxicol. Letters 154 2004 191 200
48. A. Hartwig, and D. Beyersmann Enhancement of UV-induced mutagenesis and sister-chromatid exchanges by nickel ions in V79 cells: evidence for inhibition of DNA repair Mutat. Res. 217 1989 65 73
49. A. Hartwig, and T. Schwerdtle Interactions by carcinogenic metal compounds with DNA repair processes: toxicological implications Toxicol. Letters 127 2002 47 54
50. J.V. Moran, R.J. DeBerardinis, and H.H. Kazazian Jr Exon shuffling by L1 retrotransposition Science 283 1999 1530 1534
51. J.D. Freeman, N.L. Goodchild, and D.L. Mager A modified indicator gene for selection of retrotransposition events in mammalian cells Biotechniques 17 1994 46 48 see also pages 49, 52
52. A. Hartwig, M. Asmuss, I. Ehleben, U. Herzer, D. Kostelac, and A. Pelzer Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms Environ. Health Perspect. 110 2002 797 799
53. K. Nordlind, and A. Henze Investigation of ability of the metal allergens cobalt chloride, nickel sulfate and potassium dichromate to give a mitogenic response in human thymocytes Int. Arch. Allergy Appl. Immunol. 75 1984 330 332
54. K. Wozniak, and J. Blasiak Free radicals-mediated induction of oxidized DNA bases and DNA-protein cross-links by nickel chloride Mutat. Res. 514 2002 233 243
55. K. Danadevi, R. Rozati, B. Saleha Banu, and P. Grover In vivo genotoxic effect of nickel chloride in mice leukocytes using comet assay Food Chem. Toxicol. 42 2004 751 757
56. K.S. Kasprzak, F.W. Sunderman Jr, and K. Salnikow Nickel carcinogenesis Mutat. Res. 533 2003 67 97
57. S. Ali, S.K. Jain, M. Abdulla, and M. Athar Paraquat induced DNA damage by reactive oxygen species Biochem. Mol. Biol. Int. 39 1996 63 67
58. A. Hartwig, L.H. Mullenders, R. Schlepegrell, U. Kasten, and D. Beyersmann Nickel (II) interferes with the incision step in nucleotide excision repair in mammalian cells Cancer Res. 54 1994 4045 4051
59. K.S. Kasprzak, B.A. Diwan, and J.M. Rice Iron accelerates while magnesium inhibits nickel-induced carcinogenesis in the rat kidney Toxicology 90 1994 129 140
60. G.D. Swergold Identification, characterization, and cell specificity of a human LINE-1 promoter Mol. Cell Biol. 10 1990 6718 6729
61. W. Wei, N. Gilbert, S.L. Ooi, J.F. Lawler, E.M. Ostertag, and H.H. Kazazian Human L1 Retrotransposition: cis preference versus trans complementation Mol. Cell Biol. 21 2001 1429 1439
62. D.D. Luan, and T.H. Eickbush RNA template requirements for target DNA-primed reverse transcription by the R2 retrotransposable element Mol. Cell Biol. 15 1995 3882 3891
63. Q. Feng, J.V. Moran, H.H. Kazazian Jr, and J.D. Boeke Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition Cell 87 1996 905 916
64. D. Takai, Y. Yagi, N. Habib, T. Sugimura, and T. Ushijima Hypomethylation of LINE1 retrotransposon in human hepatocellular carcinomas, but not in surrounding liver cirrhosis Jpn. J. Clin. Oncol. 30 2000 306 309
65. K. Hata, and Y. Sakaki Identification of critical CpG sites for repression of L1 transcription by DNA methylation Gene 189 1997 227 234
66. D. Beyersmann Effects of carcinogenic metals on gene expression Toxicol. Letters 127 2002 63 68
67. S. Lisby, L.H. Hansen, T. Menn, and O. Baadsgaard Nickel-induced proliferation of both memory and naive T cells in patch test-negative individuals Clin. Expt. Immunol. 117 1999 217 222
68. M. Hartmann, and A. Hartwig Disturbance of DNA damage recognition after UV-irradiation by nickel(II) and cadmium(II) in mammalian cells Carcinogenesis 19 1998 617 621
69. U. Kasten, L.H. Mullenders, and A. Hartwig Cobalt (II) inhibits the incision and the polymerization step of nucleotide excision repair in human fibroblasts Mutat. Res. 383 1997 81 89
70. H.H. Kazazian Jr Genetics. L1 retrotransposons shape the mammalian genome Science 289 2000 1152 1153
71. N. Gilbert, S. Lutz-Prigge, and J.V. Moran Genomic deletions created upon LINE-1 retrotransposition Cell 110 2002 315 325