Multiple fates of L1 retrotransposition intermediates in cultured human cells

Molecular and Cellular Biology

Volumn 25, Issue 17, 2005, Pages 7780-7795

  Gilbert, Nicolas ^a,b   Lutz, Sheila ^a   Morrish, Tammy A ^a   Moran, John V ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RNA DIRECTED DNA POLYMERASE; SMALL NUCLEAR RNA;

ARTICLE; BASE MISPAIRING; CELL CULTURE; CELL TRANSFORMATION; CHIMERA; CHROMOSOME DELETION; CHROMOSOME DUPLICATION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA INTEGRATION; DNA REPAIR; GENE REARRANGEMENT; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HELA CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; LONG INTERSPERSED REPEAT; PRIORITY JOURNAL; RETROPOSON; RNA TRANSPORT;

CELLS, CULTURED; CONSENSUS SEQUENCE; DNA, COMPLEMENTARY; GENETIC ENGINEERING; GENOME, HUMAN; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MODELS, GENETIC; MUTAGENESIS, INSERTIONAL; MUTATION; NUCLEOTIDES; SUBSTRATE SPECIFICITY; TRANSLOCATION, GENETIC;

EID: 23844510228     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.17.7780-7795.2005     Document Type: Article

References (77)

1. Altschul, S. F., T. L. Madden, A. A. Schafler, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Athanikar, J. N., R. M. Badge, and J. V. Moran. 2004. A YY1-binding site is required for accurate human LINE-1 transcription initiation. Nucleic Acids Res. 32:3846-3855.
3. Bibillo, A., and T. H. Eickbush. 2002. High processivity of the reverse transcriptase from a non-long terminal repeat retrotransposon. J. Biol. Chem. 277:34836-34845.
4. Boeke, J. D. 2003. The unusual phylogenetic distribution of retrotransposons: a hypothesis. Genome Res. 13:1975-1983.
5. Boissinot, S., P. Chevret, and A. V. Furano. 2000. L1 (LINE-1) retrotransposon evolution and amplification in recent human history. Mol. Biol. Evol. 17:915-928.
6. Brouha, B., J. Schustak, R. M. Badge, S. Lutz-Prigge, A. H. Farley, J. V. Moran, and H. H. Kazazian, Jr. 2003. Hot L1s account for the bulk of retrotransposition in the human population. Proc. Natl. Acad. Sci. USA 100:5280-5285.
7. Buzdin, A., E. Gogvadze, E. Kovalskaya, P. Volchkov, S. Ustyugova, A. Illarionova, A. Fushan, T. Vinogradova, and E. Sverdlov. 2003. The human genome contains many types of chimeric retrogenes generated through in vivo RNA recombination. Nucleic Acids Res. 31:4385-4390.
8. Buzdin, A., S. Ustyugova, E. Gogvadze, T. Vinogradova, Y. Lebedev, and E. Sverdlov. 2002. A new family of chimeric retrotranscripts formed by a full copy of U6 small nuclear RNA fused to the 3′ terminus of L1. Genomics 80:402-406.
9. Carroll, M. L., A. M. Roy-Engel, S. V. Nguyen, A. H. Salem, E. Vogel, B. Vincent, J. Myers, Z. Ahmad, L. Nguyen, M. Sammarco, W. S. Watkins, J. Henke, W. Makalowski, L. B. Jorde, P. L. Deininger, and M. A. Batzer. 2001. Large-scale analysis of the Alu Ya5 and Yb8 subfamilies and their contribution to human genomic diversity. J. Mol. Biol. 311:17-40.
10. Cost, G. J., and J. D. Boeke. 1998. Targeting of human retrotransposon integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. Biochemistry 37:18081-18093.
11. Cost, G. J., Q. Feng, A. Jacquier, and J. D. Boeke. 2002. Human L1 element target-primed reverse transcription in vitro. EMBO J. 21:5899-5910.
12. Dickson, L., S. Connell, H. R. Huang, R. M. Henke, L. Liu, and P. S. Perlman. 2004. Abortive transposition by a group II intron in yeast mitochondria. Genetics 168:77-87.
13. Dombroski, B. A., S. L. Mathias, E. Nanthakumar, A. F. Scott, and H. H. Kazazian, Jr. 1991. Isolation of an active human transposable element. Science 254:1805-1808.
14. Dombroski, B. A., A. F. Scott, and H. H. Kazazian, Jr. 1993. Two additional potential retrotransposons isolated from a human L1 subfamily that contains an active retrotransposable element. Proc. Natl. Acad. Sci. USA 90:6513-6517.
15. Ergun, S., C. Buschmann, J. Heukeshoven, K. Dammann, F. Schnieders, H. Lauke, F. Chalajour, N. Kilic, W. H. Stratling, and G. G. Schumann. 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.
16. Eskes, R., L. Liu, H. Ma, M. Y. Chao, L. Dickson, A. M. Lambowitz, and P. S. Perlman. 2000. Multiple homing pathways used by yeast mitochondrial group II introns. Mol. Cell. Biol. 20:8432-8446.
17. Fanning, T., and M. Singer. 1987. The LINE-1 DNA sequences in four mammalian orders predict proteins that conserve homologies to retrovirus proteins. Nucleic Acids Res. 15:2251-2260.
18. Farley, A. H., E. T. Luning Prak, and H. H. Kazazian, Jr. 2004. More active human L1 retrotransposons produce longer insertions. Nucleic Acids Res. 32:502-510.
19. Feng, Q., J. V. Moran, H. H. Kazazian, Jr., and J. D. Boeke. 1996. Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition. Cell 87:905-916.
20. Garvey, S. M., C. Rajan, A. P. Lerner, W. N. Frankel, and G. A. Cox. 2002. The muscular dystrophy with myositis (mdm) mouse mutation disrupts a skeletal muscle-specific domain of titin. Genomics 79:146-149.
21. Gilbert, N., S. Lutz-Prigge, and J. V. Moran. 2002. Genomic deletions created upon LINE-1 retrotransposition. Cell 110:315-325.
22. Goodier, J. L., E. M. Ostertag, K. A. Engleka, M. C. Seleme, and H. H. Kazazian, Jr. 2004. A potential role for the nucleolus in L1 retrotransposition. Hum. Mol. Genet. 13:1041-1048.
23. Gorbunova, V., and A. A. Levy. 1997. Non-homologous DNA end joining in plant cells is associated with deletions and filler DNA insertions. Nucleic Acids Res. 25:4650-4657.
24. Gorbunova, V. V., and A. A. Levy. 1999. How plants make ends meet: DNA double-strand break repair. Trends Plant Sci. 4:263-269.
25. Grimaldi, G., J. Skowronski, and M. F. Singer. 1984. Defining the beginning and end of Kpn1 family segments. EMBO J. 3:1753-1759.
26. Haas, N. B., J. M. Grabowski, J. North, J. V. Moran, H. H. Kazazian, and J. B. Burch. 2001. Subfamilies of CRl non-LTR retrotransposons have different 5′UTR sequences but are otherwise conserved. Gene 265:175-183.
27. Harris, R. S., A. M. Sheehy, H. M. Craig, M. H. Malim, and M. S. Neuberger. 2003. DNA deamination: not just a trigger for antibody diversification but also a mechanism for defense against retroviruses. Nat. Immunol. 4:641-643.
28. Hayakawa, T., Y. Satta, P. Cagneux, A. Varki, and N. Takahata. 2001. Alu-mediated inactivation of the human CMP- N-acetylneuraminic acid hydroxylase gene. Proc. Natl. Acad. Sci. USA 98:11399-11404.
29. Hayward, B. E., M. Zavanelli, and A. V. Furano. 1997. Recombination creates novel L1 (LINE-1) elements in Rattus norvegiens. Genetics 146:641-654.
30. Hohjoh, H., and M. F. Singer. 1996. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J. 15:630-639.
31. Hohjoh, H., and M. F. Singer. 1997. Sequence-specific single-strand RNA binding protein encoded by the human LINE-1 retrotransposon. EMBO J. 16:6034-6043.
32. Holmes, S. E., B. A. Dombroski, C. M. Krebs, C. D. Boehm, and H. H. Kazazian, Jr. 1994. A new retrotransposable human L1 element from the LRE2 locus on chromosome 1q produces a chimaeric insertion. Nat. Genet. 7:143-148.
33. Holmes, S. E., M. F. Singer, and G. D. Swergold. 1992. Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element. J. Biol. Chem. 267:19765-19768.
34. Hutchison, C. A., S. C. Hardies, D. D. Loeb, W. R. Shehee, and M. H. Edgell. 1989. LINEs and related retroposons: long interspersed repeated sequences in the eucaryotic genome, p. 593-617. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. ASM Press, Washington, D.C.
35. Inoue, H., H. Nojima, and H. Okayama. 1990. High efficiency transformation of Escherichia coli with plasmids. Gene 96:23-28.
36. Jurka, J. 1997. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc. Natl. Acad. Sci. USA 94:1872-1877.
37. Kass, D. H., M. A. Batzer, and P. L. Deininger. 1995. Gene conversion as a secondary mechanism of short interspersed element (SINE) evolution. Mol. Cell. Biol. 15:19-25.
38. Kent, W. J. 2002. BLAT - the BLAST-like alignment tool. Genome Res. 12:656-664.
39. Kimberland, M. L., V. Divoky, J. Prchal, U. Schwahn, W. Berger, and H. H. Kazazian, Jr. 1999. Full-length human L1 insertions retain the capacity for high frequency retrotransposition in cultured cells. Hum. Mol. Genet. 8:1557-1560.
40. Kirik, A., S. Salomon, and H. Puchta. 2000. Species-specific double-strand break repair and genome evolution in plants. EMBO J. 19:5562-5566.
41. Kojima, T., K. Nakajima, and K. Mikoshiba. 2000. The disabled 1 gene is disrupted by a replacement with L1 fragment in yotari mice. Brain Res. Mol. Brain Res. 75:121-127.
42. Kutsche, K., B. Ressler, H. G. Katzera, U. Orth, G. Gillessen-Kaesbach, S. Morlot, E. Schwinger, and A. Gal. 2002. Characterization of breakpoint sequences of five rearrangements in L1CAM and ABCD1 (ALD) genes. Hum. Mutat. 19:526-535.
43. Lander, E. S., L. M. Linton, B. Birren, C. Nusbaum, M. C. Zody, J. Baldwin, K. Devon, K. Dewar, M. Doyle, W. FitzHugh, R. Funke, D. Gage, K. Harris, A. Heaford, J. Howland, L. Kann, J. Lehoczky, R. LeVine, P. McEwan, K. McKernan, J. Meldrim, J. P. Mesirov, C. Miranda, W. Morris, J. Naylor, C. Raymond, M. Rosetti, R. Santos, A. Sheridan, C. Sougnez, N. Stange-Thomann, N. Stojanovic, A. Subramanian, D. Wyman, J. Rogers, J. Sulston, R. Ainscough, S. Beck, D. Bentley, J. Burton, C. Clee, N. Carter, A. Coulson, R. Deadman, P. Deloukas, A. Dunham, I. Dunham, R. Durbin, L. French, D. Grafham, S. Gregory, T. Hubbard, S. Humphray, A. Hunt, M. Jones, C. Lloyd, A. McMurray, L. Matthews, S. Mercer, S. Milne, J. C. Mullikin, A. Mungall, R. Plumb, M. Ross, R. Shownkeen, S. Sims, R. H. Waterston, R. K. Wilson, L. W. Hillier, J. D. McPherson, M. A. Marra, E. R. Mardis, L. A. Fulton, A. T. Chinwalla, K. H. Pepin, W. R. Gish, S. L. Chissoe, M. C. Wendl, K. D. Delehaunty, T. L. Miner, A. Delehaunty, J. B. Kramer, L. L. Cook, R. S. Fulton, D. L. Johnson, P. J. Minx, S. W. Clifton, T. Hawkins, E. Branscomb, P. Predki, P. Richardson, S. Wenning, T. Slezak, N. Doggett, J. F. Cheng, A. Olsen, S. Lucas, C. Elkin, E. Uberbacher, M. Frazier, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
44. Liang, F., M. Han, P. J. Romanienko, and M. Jasin. 1998. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA 95:5172-5177.
45. Lin, Y., and A. S. Waldman. 2001. Capture of DNA sequences at double-strand breaks in mammalian chromosomes. Genetics 158:1665-1674.
46. Lin, Y., and A. S. Waldman. 2001. Promiscuous patching of broken chromosomes in mammalian cells with extrachromosomal DNA. Nucleic Acids Res. 29:3975-3981.
47. Luan, D. D., M. H. Korman, J. L. Jakubczak, and T. H. Eickbush. 1993. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595-605.
48. Lutz, S. M., B. J. Vincent, H. H. Kazazian, Jr., M. A. Batzer, and J. V. Moran. 2003. Allelic heterogeneity in LINE-1 retrotransposition activity. Am. J. Hum. Genet. 73:1431-1437.
49. Martin, S. L., and F. D. Bushman. 2001. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol. Cell. Biol. 21:467-475.
50. Martin, S. L., W.-L. P. Li, A. V. Furano, and S. Boissinot. The structures of mouse and human L1 elements reflect their insertion mechanism. Mol. Genet. Genomics, in press.
51. Mathias, S. L., A. F. Scott, H. H. Kazazian, Jr., J. D. Boeke, and A. Gabriel. 1991. Reverse transcriptase encoded by a human transposable element. Science 254:1808-1810.
52. Moran, J. V., R. J. DeBerardinis, and H. H. Kazazian, Jr. 1999. Exon shuffling by L1 retrotransposition. Science 283:1530-1534.
53. Moran, J. V., and N. Gilbert. 2002. Mammalian LINE-1 retrotransposons and related elements, p. 836-869. In A. Lambowitz (ed.), Mobile DNA II. ASM Press, Washington, D.C.
54. Moran, J. V., S. E. Holmes, T. P. Naas, R. J. DeBerardinis, J. D. Boeke, and H. H. Kazazian, Jr. 1996. High frequency retrotransposition in cultured mammalian cells. Cell 87:917-927.
55. Moran, J. V., S. Zimmerly, R. Eskes, J. C. Kennell, A. M. Lambowitz, R. A. Butow, and P. S. Perlman. 1995. Mobile group II introns of yeast mitochondrial DNA are novel site-specific retroelements. Mol. Cell. Biol. 15:2828-2838.
56. Morrish, T. A., N. Gilbert, J. S. Myers, B. J. Vincent, T. D. Stamato, G. E. Taccioli, M. A. Batzer, and J. V. Moran. 2002. DNA repair mediated by endomiclease-independent LINE-1 retrotransposition. Nat. Genet. 31:159-165.
57. Nassif, N., J. Penney, S. Pal, W. R. Engels, and G. B. Gloor. 1994. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14:1613-1625.
58. Ostertag, E. M., and H. H. Kazazian, Jr. 2001. Twin priming: a proposed mechanism for the creation of inversions in L1 retrotransposition. Genome Res. 11:2059-2065.
59. Paques, F., W. Y. Leung, and J. E. Haber. 1998. Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol. Cell. Biol. 18:2045-2054.
60. Salem, A. H., G. E. Kilroy, W. S. Watkins, L. B. Jorde, and M. A. Batzer. 2003. Recently integrated AIu elements and human genomic diversity. Mol. Biol. Evol. 20:1349-1361.
61. Sargent, R. G., M. A. Brenneman, and J. H. Wilson. 1997. Repair of site-specific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell. Biol. 17:267-277.
62. Sargent, R. G., J. L. Meservy, B. D. Perkins, A. E. Kilburn, Z. Intody, G. M. Adair, R. S. Nairn, and J. H. Wilson. 2000. Role of the nucleotide excision repair gene ERCC1 in formation of recombination-dependent rearrangements in mammalian cells. Nucleic Acids Res. 28:3771-3778.
63. Sassaman, D. M., B. A. Dombroski, J. V. Moran, M. L. Kimberland, T. P. Naas, R. J. DeBerardinis, A. Gabriel, G. D. Swergold, and H. H. Kazazian, Jr. 1997. Many human L1 elements are capable of retrotransposition. Nat. Genet. 16:37-43.
64. Saxton, J. A., and S. L. Martin. 1998. Recombination between subtypes creates a mosaic lineage of LINE-1 that is expressed and actively retrotransposing in the mouse genome. J. Mol. Biol. 280:611-622.
65. Schwarz-Sommer, Z., L. Leclerq, E. Goebel, and H. Saedler. 1987. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 6:3873-3880.
66. Scott, A. F., B. J. Schmeckpeper, M. Abdelrazik, C. T. Comey, B. O'Hara, J. P. Rossiter, T. Cooley, P. Heath, K. D. Smith, and L. Margolet. 1987. Origin of the human L1 elements: proposed progenitor genes deduced from a consensus DNA sequence. Genomics 1:113-125.
67. Segal, Y., B. Peissel, A. Renieri, M. de Marchi, A. Ballabio, Y. Pei, and J. Zhou. 1999. LINE-1 elements at the sites of molecular rearrangements in Alport syndrome-diffuse leiomyomatosis. Am. J. Hum. Genet. 64:62-69.
68. Skowronski, J., T. G. Fanning, and M. F. Singer. 1988. Unit-length Line-1 transcripts in human teratocarcinoma cells. Mol. Cell. Biol. 8:1385-1397.
69. Smit, A. F. 1996. The origin of interspersed repeats in the human genome. Curr. Opin. Genet. Dev. 6:743-748.
70. Su, L. K., G. Steinbach, J. C. Sawyer, M. Hindi, P. A. Ward, and P. M. Lynch. 2000. Genomic rearrangements of the APC tumor-suppressor gene in familial adenomatous polyposis. Hum. Genet. 106:101-107.
71. Sugawara, N., and J. E. Haber. 1992. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12:563-575.
72. Symer, D. E., C. Connelly, S. T. Szak, E. M. Caputo, G. J. Cost, G. Parmigiani, and J. D. Boeke. 2002. Human L1 retrotransposition is associated with genetic instability in vivo. Cell 110:327-338.
73. Tang, X., Y. Nakata, H. O. Li, M. Zhang, H. Gao, A. Fujita, O. Sakatsume, T. Ohta, and K. Yokoyama. 1994. The optimization of preparations of competent cells for transformation of E. coli. Nucleic Acids Res. 22:2857-2858.
74. Voliva, C. F., S. L. Martin, C. A. Hutchison III, and M. H. Edgell. 1984. Dispersal process associated with the L1 family of interspersed repetitive DNA sequences. J. Mol. Biol. 178:795-813.
75. Wang, T., I. Lerer, Z. Gueta, M. Sagi, L. Kadouri, T. Peretz, and D. Abeliovich. 2001. A deletion/insertion mutation in the BRCA2 gene in a breast cancer family, a possible role of the Alu-polyA tail in the evolution of the deletion. Genes Chromosomes Cancer 31:91-95.
76. Wei, W., T. A. Morrish, R. S. Alisch, and J. V. Moran. 2000. A transient assay reveals that cultured human cells can accommodate multiple LINE-1 retrotransposition events. Anal. Biochem. 284:435-438.
77. Zhong, J., and A. M. Lambowitz. 2003. Group II intron mobility using nascent strands at DNA replication forks to prime reverse transcription. EMBO J. 22:4555-4565.