Trimeric structure and flexibility of the L1ORF1 protein in human L1 retrotransposition

Nature Structural and Molecular Biology

Volumn 18, Issue 9, 2011, Pages 1006-1014

  Khazina, Elena ^a   Truffault, Vincent ^a   Büttner, Regina ^a   Schmidt, Steffen ^a   Coles, Murray ^a   Weichenrieder, Oliver ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN L1ORF1; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; GENETIC VARIABILITY; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN STRUCTURE; RETROPOSON;

CRYSTALLOGRAPHY, X-RAY; HUMANS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SUBSTRATE SPECIFICITY;

EID: 80052449321     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2097     Document Type: Article

References (43)

1. Goodier, J.L. & Kazazian, H.H. Jr. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135, 23-35 (2008).
2. Han, J.S. & Boeke, J.D. LINE-1 retrotransposons: modulators of quantity and quality of mammalian gene expression? Bioessays 27, 775-784 (2005). (Pubitemid 41297400)
3. Moran, J.V. & Gilbert, N. Mammalian LINE-1 retrotransposons and related elements. in Mobile DNA II Vol. 2 (eds. Craig, N.L., Craigie, R., Gellert, M. & Lambowitz, A.M.) 836-869 (ASM Press, 2002).
4. Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001). (Pubitemid 32165345)
5. Beck, C.R. et al. LINE-1 retrotransposition activity in human genomes. Cell 141, 1159-1170 (2010).
6. Ewing, A.D. & Kazazian, H.H. Jr. High-throughput sequencing reveals extensive variation in human-specific L1 content in individual human genomes. Genome Res. 20, 1262-1270 (2010).
7. Huang, C.R. et al. Mobile interspersed repeats are major structural variants in the human genome. Cell 141, 1171-1182 (2010).
8. Iskow, R.C. et al. Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141, 1253-1261 (2010).
9. Coufal, N.G. et al. L1 retrotransposition in human neural progenitor cells. Nature 460, 1127-1131 (2009).
10. Eickbush, T.H. & Malik, H.S. Origin and evolution of retrotransposons. in Mobile DNA II Vol. 2 (eds. Craig, N.L., Craigie, R., Gellert, M. & Lambowitz, A.M.) 1111-1144 (ASM Press, 2002).
11. Cost, G.J., Feng, Q., Jacquier, A. & Boeke, J.D. Human L1 element target-primed reverse transcription in vitro. EMBO J. 21, 5899-5910 (2002). (Pubitemid 35315287)
12. Luan, D.D., Korman, M.H., Jakubczak, J.L. & Eickbush, T.H. 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 (1993). (Pubitemid 23077747)
13. Khazina, E. & Weichenrieder, O. Non-LTR retrotransposons encode noncanonical RRM domains in their first open reading frame. Proc. Natl. Acad. Sci. USA 106, 731-736 (2009).
14. Moran, J.V. et al. High frequency retrotransposition in cultured mammalian cells. Cell 87, 917-927 (1996). (Pubitemid 26404290)
15. Hohjoh, H. & Singer, M.F. Cytoplasmic ribonucleoprotein complexes containing human LINE-1 protein and RNA. EMBO J. 15, 630-639 (1996). (Pubitemid 26044576)
16. Kulpa, D.A. & Moran, J.V. Ribonucleoprotein particle formation is necessary but not sufficient for LINE-1 retrotransposition. Hum. Mol. Genet. 14, 3237-3248 (2005). (Pubitemid 41631298)
17. Martin, S.L. Ribonucleoprotein particles with LINE-1 RNA in mouse embryonal carcinoma cells. Mol. Cell. Biol. 11, 4804-4807 (1991). (Pubitemid 21895879)
18. Goodier, J.L., Zhang, L., Vetter, M.R. & Kazazian, H.H. 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. 27, 6469-6483 (2007). (Pubitemid 47435752)
19. Soper, S.F. et al. Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 15, 285-297 (2008).
20. Hohjoh, H. & Singer, M.F. Sequence-specific single-strand RNA binding protein encoded by the human LINE-1 retrotransposon. EMBO J. 16, 6034-6043 (1997). (Pubitemid 27427298)
21. Kolosha, V.O. & Martin, S.L. In vitro properties of the first ORF protein from mouse LINE-1 support its role in ribonucleoprotein particle formation during retrotransposition. Proc. Natl. Acad. Sci. USA 94, 10155-10160 (1997). (Pubitemid 27407010)
22. Martin, S.L. & Bushman, F.D. Nucleic acid chaperone activity of the ORF1 protein from the mouse LINE-1 retrotransposon. Mol. Cell. Biol. 21, 467-475 (2001). (Pubitemid 32037367)
23. Wei, W. et al. Human L1 retrotransposition: cis preference versus trans complementation. Mol. Cell. Biol. 21, 1429-1439 (2001). (Pubitemid 32114989)
24. Basame, S. et al. Spatial assembly and RNA binding stoichiometry of a LINE-1 protein essential for retrotransposition. J. Mol. Biol. 357, 351-357 (2006). (Pubitemid 43292547)
25. Martin, S.L., Branciforte, D., Keller, D. & Bain, D.L. Trimeric structure for an essential protein in L1 retrotransposition. Proc. Natl. Acad. Sci. USA 100, 13815-13820 (2003). (Pubitemid 37499149)
26. Januszyk, K. et al. Identification and solution structure of a highly conserved C-terminal domain within ORF1p required for tetrotransposition of long interspersed nuclear element-1. J. Biol. Chem. 282, 24893-24904 (2007). (Pubitemid 47347512)
27. Chou, K.C. Prediction of tight turns and their types in proteins. Anal. Biochem. 286, 1-16 (2000).
28. Hartmann, M.D. et al. A coiled-coil motif that sequesters ions to the hydrophobic core. Proc. Natl. Acad. Sci. USA 106, 16950-16955 (2009).
29. Martin, S.L. et al. LINE-1 retrotransposition requires the nucleic acid chaperone activity of the ORF1 protein. J. Mol. Biol. 348, 549-561 (2005). (Pubitemid 40520490)
30. Martin, S.L. et al. A single amino acid substitution in ORF1 dramatically decreases L1 retrotransposition and provides insight into nucleic acid chaperone activity. Nucleic Acids Res. 36, 5845-5854 (2008).
31. Evans, J.D., Peddigari, S., Chaurasiya, K.R., Williams, M.C. & Martin, S.L. Paired mutations abolish and restore the balanced annealing and melting activities of ORF1p that are required for LINE-1 retrotransposition. Nucleic Acids Res. doi:10.1093/nar/gkr171 (26 March 2011).
32. Albertini, A.A., Schoehn, G., Weissenhorn, W. & Ruigrok, R.W. Structural aspects of rabies virus replication. Cell. Mol. Life Sci. 65, 282-294 (2008). (Pubitemid 351161483)
33. Raymond, D.D., Piper, M.E., Gerrard, S.R. & Smith, J.L. Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc. Natl. Acad. Sci. USA 107, 11769-11774 (2010).
34. Tawar, R.G. et al. Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326, 1279-1283 (2009).
35. Ye, Q., Krug, R.M. & Tao, Y.J. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444, 1078-1082 (2006). (Pubitemid 46018528)
36. Cost, G.J. & Boeke, J.D. Targeting of human retrotransposon integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. Biochemistry 37, 18081-18093 (1998). (Pubitemid 29023965)
37. Repanas, K. et al. Determinants for DNA target structure selectivity of the human LINE-1 retrotransposon endonuclease. Nucleic Acids Res. 35, 4914-4926 (2007). (Pubitemid 47250359)
38. Kapitonov, V.V. & Jurka, J. The esterase and PHD domains in CR1-like non-LTR retrotransposons. Mol. Biol. Evol. 20, 38-46 (2003). (Pubitemid 36077897)
39. Kammerer, R.A. et al. A conserved trimerization motif controls the topology of short coiled-coils. Proc. Natl. Acad. Sci. USA 102, 13891-13896 (2005). (Pubitemid 41377674)
40. Kobe, B., Center, R.J., Kemp, B.E. & Poumbourios, P. Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retroviral transmembrane proteins. Proc. Natl. Acad. Sci. USA 96, 4319-4324 (1999). (Pubitemid 29190334)
41. Weissenhorn, W., Dessen, A., Harrison, S.C., Skehel, J.J. & Wiley, D.C. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387, 426-430 (1997). (Pubitemid 27227210)
42. Chen, J., Skehel, J.J. & Wiley, D.C. N-and C-terminal residues combine in the fusion-pH influenza hemagglutinin HA(2) subunit to form an N cap that terminates the triple-stranded coiled coil. Proc. Natl. Acad. Sci. USA 96, 8967-8972 (1999). (Pubitemid 29374691)
43. Müller, M., Weigand, J.E., Weichenrieder, O. & Suess, B. Thermodynamic characterization of an engineered tetracycline-binding riboswitch. Nucleic Acids Res. 34, 2607-2617 (2006). (Pubitemid 43985625)