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Journal of Biomedicine and Biotechnology
Volume 2006, Article ID 45621, 6 pages
http://dx.doi.org/10.1155/JBB/2006/45621
Mini-Review Article

The ORF1 Protein Encoded by LINE-1: Structure and Function During L1 Retrotransposition

Department of Cell and Developmental Biology, School of Medicine, University of Colorado, Fitzsimons Campus, PO Box 6511, Mail Stop 8108, Aurora, CO 80045, USA

Received 17 September 2005; Revised 10 December 2005; Accepted 13 December 2005

Copyright © 2006 Sandra L. Martin. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. T H Eickbush and H S Malik, “Origins and evolution of retrotransposons,” in Mobile DNA II, N L Craig, R Craigie, M Gellert, and A M Lambowitz, Eds., pp. 1111–1144, American Society of Microbiology Press, Washington, DC, 2002. View at Google Scholar
  2. A V Furano, “The biological properties and evolutionary dynamics of mammalian LINE-1 retrotransposons,” Progress in Nucleic Acid Research and Molecular Biology, vol. 64, pp. 255–294, 2000. View at Google Scholar
  3. J V Moran and N Gilbert, “Mammalian LINE-1 retrotransposons and related elements,” in Mobile DNA II, N L Craig, R Craigie, M Gellert, and A M Lambowitz, Eds., pp. 836–869, American Society of Microbiology Press, Washington, DC, 2002. View at Google Scholar
  4. Q Feng, J V Moran, H H Jr Kazazian, and J D Boeke, “Human L1 retrotransposon encodes a conserved endonuclease required for retrotransposition,” Cell, vol. 87, no. 5, pp. 905–916, 1996. View at Publisher · View at Google Scholar
  5. J V Moran, S E Holmes, T P Naas, R J DeBerardinis, J D Boeke, and H H Jr Kazazian, “High frequency retrotransposition in cultured mammalian cells,” Cell, vol. 87, no. 5, pp. 917–927, 1996. View at Publisher · View at Google Scholar
  6. M Hattori, S Kuhara, O Takenaka, and Y Sakaki, “L1 family of repetitive DNA sequences in primates may be derived from a sequence encoding a reverse transcriptase-related protein,” Nature, vol. 321, no. 6070, pp. 625–628, 1986. View at Publisher · View at Google Scholar
  7. D D Loeb, R W Padgett, S C Hardies et al., “The sequence of a large L1Md element reveals a tandemly repeated 5' end and several features found in retrotransposons,” Molecular and Cellular Biology, vol. 6, no. 1, pp. 168–182, 1986. View at Google Scholar
  8. S L Mathias, A F Scott, H H Jr Kazazian, J D Boeke, and A Gabriel, “Reverse transcriptase encoded by a human transposable element,” Science, vol. 254, no. 5039, pp. 1808–1810, 1991. View at Publisher · View at Google Scholar
  9. H Hohjoh and M F Singer, “Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA,” The EMBO Journal, vol. 15, no. 3, pp. 630–639, 1996. View at Google Scholar
  10. D D Duvernell and B J Turner, “Swimmer 1, a new low-copy-number LINE family in teleost genomes with sequence similarity to mammalian L1,” Molecular Biology and Evolution, vol. 15, no. 12, pp. 1791–1793, 1998. View at Google Scholar
  11. A Lupas, M Van Dyke, and J Stock, “Predicting coiled coils from protein sequences,” Science, vol. 252, no. 5010, pp. 1162–1164, 1991. View at Publisher · View at Google Scholar
  12. C Notredame, D G Higgins, and J Heringa, “T-Coffee: a novel method for fast and accurate multiple sequence alignment,” Journal of Molecular Biology, vol. 302, no. 1, pp. 205–217, 2000. View at Publisher · View at Google Scholar
  13. R J DeBerardinis, J L Goodier, E M Ostertag, and H H Jr Kazazian, “Rapid amplification of a retrotransposon subfamily is evolving the mouse genome,” Nature Genetics, vol. 20, no. 3, pp. 288–290, 1998. View at Publisher · View at Google Scholar
  14. T P Naas, R J DeBerardinis, J V Moran et al., “An actively retrotransposing, novel subfamily of mouse L1 elements,” The EMBO Journal, vol. 17, no. 2, pp. 590–597, 1998. View at Publisher · View at Google Scholar
  15. U Schwahn, S Lenzner, J Dong et al., “Positional cloning of the gene for X-linked retinitis pigmentosa 2,” Nature Genetics, vol. 19, no. 4, pp. 327–332, 1998. View at Publisher · View at Google Scholar
  16. G W Demers, M J Matunis, and R C Hardison, “The L1 family of long interspersed repetitive DNA in rabbits: sequence, copy number, conserved open reading frames, and similarity to keratin,” Journal of Molecular Evolution, vol. 29, no. 1, pp. 3–19, 1989. View at Publisher · View at Google Scholar
  17. S L Martin, D Branciforte, D Keller, and D L Bain, “Trimeric structure for an essential protein in L1 retrotransposition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 24, pp. 13815–13820, 2003. View at Publisher · View at Google Scholar
  18. S E Holmes, M F Singer, and G D Swergold, “Studies on p40, the leucine zipper motif-containing protein encoded by the first open reading frame of an active human LINE-1 transposable element,” The Journal of Biological Chemistry, vol. 267, no. 28, pp. 19765–19768, 1992. View at Google Scholar
  19. N B Adey, S A Schichman, C A III Hutchison, and M H Edgell, “Composite of A and F-type 5 terminal sequences defines a subfamily of mouse LINE-1 elements,” Journal of Molecular Biology, vol. 221, no. 2, pp. 367–373, 1991. View at Publisher · View at Google Scholar
  20. N B Adey, S A Schichman, D K Graham, S N Peterson, M H Edgell, and C A III Hutchison, “Rodent L1 evolution has been driven by a single dominant lineage that has repeatedly acquired new transcriptional regulatory sequences,” Molecular Biology and Evolution, vol. 11, no. 5, pp. 778–789, 1994. View at Google Scholar
  21. J A Saxton and S L Martin, “Recombination between subtypes creates a mosaic lineage of LINE-1 that is expressed and actively retrotransposing in the mouse genome,” Journal of Molecular Biology, vol. 280, no. 4, pp. 611–622, 1998. View at Publisher · View at Google Scholar
  22. B E Hayward, M Zavanelli, and A V Furano, “Recombination creates novel L1 (LINE-1) elements in Rattus norvegicus,” Genetics, vol. 146, no. 2, pp. 641–654, 1997. View at Google Scholar
  23. E L Cabot, B Angeletti, K Usdin, and A V Furano, “Rapid evolution of a young L1 (LINE-1) clade in recently speciated Rattus taxa,” Journal of Molecular Evolution, vol. 45, no. 4, pp. 412–423, 1997. View at Publisher · View at Google Scholar
  24. S Boissinot and A V Furano, “Adaptive evolution in LINE-1 retrotransposons,” Molecular Biology and Evolution, vol. 18, no. 12, pp. 2186–2194, 2001. View at Google Scholar
  25. J L Goodier, E M Ostertag, K Du, and H H Jr Kazazian, “A novel active L1 retrotransposon subfamily in the mouse,” Genome Research, vol. 11, no. 10, pp. 1677–1685, 2001. View at Publisher · View at Google Scholar
  26. M L Mears and C A III Hutchison, “The evolution of modern lineages of mouse L1 elements,” Journal of Molecular Evolution, vol. 52, no. 1, pp. 51–62, 2001. View at Google Scholar
  27. N L Craig, “Unity in transposition reactions,” Science, vol. 270, no. 5234, pp. 253–254, 1995. View at Publisher · View at Google Scholar
  28. D D Luan, M H Korman, J L Jakubczak, and T H Eickbush, “Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition,” Cell, vol. 72, no. 4, pp. 595–605, 1993. View at Publisher · View at Google Scholar
  29. G J Cost and J D Boeke, “Targeting of human retrotransposon integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure,” Biochemistry, vol. 37, no. 51, pp. 18081–18093, 1998. View at Publisher · View at Google Scholar
  30. T A Morrish, N Gilbert, J S Myers et al., “DNA repair mediated by endonuclease-independent LINE-1 retrotransposition,” Nature Genetics, vol. 31, no. 2, pp. 159–165, 2002. View at Publisher · View at Google Scholar
  31. J Kulkosky, K S Jones, R A Katz, J P Mack, and A M Skalka, “Residues critical for retroviral integrative recombination in a region that is highly conserved among retroviral/retrotransposon integrases and bacterial insertion sequence transposases,” Molecular and Cellular Biology, vol. 12, no. 5, pp. 2331–2338, 1992. View at Google Scholar
  32. D R Davies, L Mahnke Braam, W S Reznikoff, and I Rayment, “The three-dimensional structure of a Tn5 transposase-related protein determined to 2.9-Å resolution,” The Journal of Biological Chemistry, vol. 274, no. 17, pp. 11904–11913, 1999. View at Publisher · View at Google Scholar
  33. E M Ostertag, E TL Prak, R J DeBerardinis, J V Moran, and H H Jr Kazazian, “Determination of L1 retrotransposition kinetics in cultured cells,” Nucleic Acids Research, vol. 28, no. 6, pp. 1418–1423, 2000. View at Publisher · View at Google Scholar
  34. G J Cost, Q Feng, A Jacquier, and J D Boeke, “Human L1 element target-primed reverse transcription in vitro,” The EMBO Journal, vol. 21, no. 21, pp. 5899–5910, 2002. View at Publisher · View at Google Scholar
  35. H Hohjoh and M F Singer, “Sequence-specific single-strand RNA binding protein encoded by the human LINE-1 retrotransposon,” The EMBO Journal, vol. 16, no. 19, pp. 6034–6043, 1997. View at Publisher · View at Google Scholar
  36. S L Martin and F D Bushman, “Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon,” Molecular and Cellular Biology, vol. 21, no. 2, pp. 467–475, 2001. View at Publisher · View at Google Scholar
  37. M Dewannieux, C Esnault, and T Heidmann, “LINE-mediated retrotransposition of marked Alu sequences,” Nature Genetics, vol. 35, no. 1, pp. 41–48, 2003. View at Publisher · View at Google Scholar
  38. W Wei, N Gilbert, S L Ooi et al., “Human L1 retrotransposition: cis preference versus trans complementation,” Molecular and Cellular Biology, vol. 21, no. 4, pp. 1429–1439, 2001. View at Publisher · View at Google Scholar
  39. C Esnault, J Maestre, and T Heidmann, “Human LINE retrotransposons generate processed pseudogenes,” Nature Genetics, vol. 24, no. 4, pp. 363–367, 2000. View at Publisher · View at Google Scholar
  40. V O Kolosha and S L Martin, “In vitro properties of the first ORF protein from mouse LINE-1 support its role in ribonucleoprotein particle formation during retrotransposition,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 19, pp. 10155–10160, 1997. View at Publisher · View at Google Scholar
  41. S L Martin, J Li, and J A Weisz, “Deletion analysis defines distinct functional domains for protein-protein and nucleic acid interactions in the ORF1 protein of mouse LINE-1,” Journal of Molecular Biology, vol. 304, no. 1, pp. 11–20, 2000. View at Publisher · View at Google Scholar
  42. S L Martin, “Ribonucleoprotein particles with LINE-1 RNA in mouse embryonal carcinoma cells,” Molecular and Cellular Biology, vol. 11, no. 9, pp. 4804–4807, 1991. View at Google Scholar
  43. H Hohjoh and M F Singer, “Ribonuclease and high salt sensitivity of the ribonucleoprotein complex formed by the human LINE-1 retrotransposon,” Journal of Molecular Biology, vol. 271, no. 1, pp. 7–12, 1997. View at Publisher · View at Google Scholar
  44. D A Kulpa and J V Moran, “Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition,” Human Molecular Genetics, vol. 14, no. 21, pp. 3237–3248, 2005. View at Publisher · View at Google Scholar
  45. V O Kolosha and S L Martin, “High-affinity, non-sequence-specific RNA binding by the open reading frame 1 (ORF1) protein from long interspersed nuclear element 1 (LINE-1),” The Journal of Biological Chemistry, vol. 278, no. 10, pp. 8112–8117, 2003. View at Publisher · View at Google Scholar
  46. A Rein, L E Henderson, and J G Levin, “Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication,” Trends in Biochemical Sciences, vol. 23, no. 8, pp. 297–301, 1998. View at Publisher · View at Google Scholar
  47. M C Williams, I Rouzina, J R Wenner, R J Gorelick, K Musier-Forsyth, and V A Bloomfield, “Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 11, pp. 6121–6126, 2001. View at Publisher · View at Google Scholar
  48. A Dawson, E Hartswood, T Paterson, and D J Finnegan, “A LINE-like transposable element in Drosophila, the I factor, encodes a protein with properties similar to those of retroviral nucleocapsids,” The EMBO Journal, vol. 16, no. 14, pp. 4448–4455, 1997. View at Publisher · View at Google Scholar
  49. S L Martin, M Cruceanu, D Branciforte et al., “LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein,” Journal of Molecular Biology, vol. 348, no. 3, pp. 549–561, 2005. View at Publisher · View at Google Scholar
  50. J S Han and J D Boeke, “LINE-1 retrotransposons: modulators of quantity and quality of mammalian gene expression?” BioEssays, vol. 27, no. 8, pp. 775–784, 2005. View at Publisher · View at Google Scholar