Ty3 reverse transcriptase complexed with an RNA-DNA hybrid shows structural and functional asymmetry

Nature Structural and Molecular Biology

Volumn 21, Issue 4, 2014, Pages 389-396

  Nowak, Elzbieta ^a   Miller, Jennifer T ^b   Bona, Marion K ^b   Studnicka, Justyna ^a   Szczepanowski, Roman H ^a   Jurkowski, Jakub ^a   Le Grice, Stuart F J ^b   Nowotny, Marcin ^a  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b Laboratory of Cancer Prevention   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; HOMODIMER; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE;

ALPHA CHAIN; ARCHITECTURE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; DNA PURIFICATION; DNA RNA HYBRIDIZATION; DNA STRUCTURE; DNA SYNTHESIS; ENZYME ACTIVITY; GENE REPLICATION; LONG TERMINAL REPEAT; PRIORITY JOURNAL; RETROPOSON; RNA PURIFICATION; RNA STRUCTURE; SACCHAROMYCES CEREVISIAE; CATALYSIS; ENZYME PURIFICATION; NONHUMAN;

SACCHAROMYCES CEREVISIAE;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; RETROELEMENTS; RIBONUCLEASE H; RNA-DIRECTED DNA POLYMERASE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84897991198     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2785     Document Type: Article

References (45)

1. Cordaux, R. & Batzer, M.A. The impact of retrotransposons on human genome evolution. Nat. Rev. Genet. 10, 691-703 (2009
2. Lander, E.S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860-921 (2001
3. SanMiguel, P., Gaut, B.S., Tikhonov, A., Nakajima, Y. & Bennetzen, J.L. The paleontology of intergene retrotransposons of maize. Nat. Genet. 20, 43-45 (1998
4. Malik, H.S., Henikoff, S. & Eickbush, T.H. Poised for contagion: Evolutionary origins of the infectious abilities of invertebrate retroviruses. Genome Res. 10, 1307-1318 (2000
5. Llorens, C. et al. The Gypsy Database (GyDB) of mobile genetic elements: Release 2.0. Nucleic Acids Res. 39, D70-D74 (2011
6. Sandmeyer, S.B., Aye, M. & Menees, T.M. Ty3: A position-specific, gypsylike element in Saccharomyces cerevisiae. in Mobile DNA II (eds. Craig, N.L., Craigie, R., Gellert, M. & Lambowitz, A.M.) 663-682 (ASM Press, Washington, DC, 2002
7. Bibillo, A., Lener, D., Klarmann, G.J. & Le Grice, S.F. Functional roles of carboxylate residues comprising the DNA polymerase active site triad of Ty3 reverse transcriptase. Nucleic Acids Res. 33, 171-181 (2005
8. Bibillo, A., Lener, D., Tewari, A. & Le Grice, S.F. Interaction of the Ty3 reverse transcriptase thumb subdomain with template-primer. J. Biol. Chem. 280, 30282-30290 (2005
9. Lener, D., Budihas, S.R. & Le Grice, S.F. Mutating conserved residues in the ribonuclease H domain of Ty3 reverse transcriptase affects specialized cleavage events. J. Biol. Chem. 277, 26486-26495 (2002
10. Brinson, R.G et al. Probing anomalous structural features in polypurine tract-containing RNA-DNA hybrids with neomycin B. Biochemistry 48, 6988-6997 (2009
11. Dash, C., Marino, J.P. & Le Grice, S.F. Examining Ty3 polypurine tract structure and function by nucleoside analog interference. J. Biol. Chem. 281, 2773-2783 (2006
12. Rausch, J.W. et al. Interaction of p55 reverse transcriptase from the Saccharomyces cerevisiae retrotransposon Ty3 with conformationally distinct nucleic acid duplexes. J. Biol. Chem. 275, 13879-13887 (2000
13. Turner, K.B. et al. SHAMS: Combining chemical modification of RNA with mass spectrometry to examine polypurine tract-containing RNA/DNA hybrids. RNA 15, 1605-1613 (2009
14. Yi-Brunozzi, H.Y., Brabazon, D.M., Lener, D., Le Grice, S.F. & Marino, J.P. A ribose sugar conformational switch in the LTR-retrotransposon Ty3 polypurine tract-containing RNA/DNA hybrid. J. Am. Chem. Soc. 127, 16344-16345 (2005
15. Yi-Brunozzi, H.Y. et al. High-resolution NMR analysis of the conformations of native and base analog substituted retroviral and LTR-retrotransposon PPT primers. Chem. Biol. 15, 254-262 (2008
16. Huang, H., Chopra, R., Verdine, G.L. & Harrison, S.C. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: Implications for drug resistance. Science 282, 1669-1675 (1998
17. Lapkouski, M., Tian, L., Miller, J.T., Le Grice, S.F. & Yang, W. Complexes of HIV-1 RT, NNRTI and RNA/DNA hybrid reveal a structure compatible with RNA degradation. Nat. Struct. Mol. Biol. 20, 230-236 (2013
18. Malik, H.S. & Eickbush, T.H. Phylogenetic analysis of ribonuclease H domains suggests a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res. 11, 1187-1197 (2001
19. Kirchner, J. & Sandmeyer, S.B. Ty3 integrase mutants defective in reverse transcription or 3'-end processing of extrachromosomal Ty3 DNA. J. Virol. 70, 4737-4747 (1996
20. Wilhelm, M., Heyman, T., Friant, S. & Wilhelm, F.X. Heterogeneous terminal structure of Ty1 and Ty3 reverse transcripts. Nucleic Acids Res. 25, 2161-2166 (1997
21. Wilhelm, M., Uzun, O., Mules, E.H., Gabriel, A. & Wilhelm, F.X. Polypurine tract formation by Ty1 RNase H. J. Biol. Chem. 276, 47695-47701 (2001
22. Nymark-McMahon, M.H., Beliakova-Bethell, N.S., Darlix, J.L., Le Grice, S.F. & Sandmeyer, S.B. Ty3 integrase is required for initiation of reverse transcription. J. Virol. 76, 2804-2816 (2002
23. Nowak, E. et al. Structural analysis of monomeric retroviral reverse transcriptase in complex with an RNA/DNA hybrid. Nucleic Acids Res. 41, 3874-3887 (2013
24. Kohlstaedt, L.A., Wang, J., Friedman, J.M., Rice, P.A. & Steitz, T.A. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256, 1783-1790 (1992
25. Mous, J., Heimer, E.P. & Le Grice, S.F. Processing protease and reverse transcriptase from human immunodeficiency virus type I polyprotein in Escherichia coli. J. Virol. 62, 1433-1436 (1988
26. Nowotny, M. Retroviral integrase superfamily: The structural perspective. EMBO Rep. 10, 144-151 (2009
27. Nowotny, M., Gaidamakov, S.A., Crouch, R.J. & Yang, W. Crystal structures of RNase H bound to an RNA/DNA hybrid: Substrate specificity and metal-dependent catalysis. Cell 121, 1005-1016 (2005
28. Nowotny, M. et al. Structure of human RNase H1 complexed with an RNA/DNA hybrid: Insight into HIV reverse transcription. Mol. Cell 28, 264-276 (2007
29. Najmudin, S. et al. Crystal structures of an N-Terminal fragment from Moloney murine leukemia virus reverse transcriptase complexed with nucleic acid: Functional implications for template-primer binding to the fingers domain. J. Mol. Biol. 296, 613-632 (2000
30. Boyer, P.L., Ferris, A.L. & Hughes, S.H. Cassette mutagenesis of the reverse transcriptase of human immunodeficiency virus type 1. J. Virol. 66, 1031-1039 (1992
31. Kim, B. et al. New human immunodeficiency virus, type 1 reverse transcriptase (HIV-1 RT) mutants with increased fidelity of DNA synthesis. Accuracy, template binding, and processivity. J. Biol. Chem. 274, 27666-27673 (1999
32. Sarafianos, S.G. et al. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J. 20, 1449-1461 (2001
33. Beard, W.A. et al. Structure/function studies of human immunodeficiency virus type 1 reverse transcriptase. Alanine scanning mutagenesis of an alpha-helix in the thumb subdomain. J. Biol. Chem. 269, 28091-28097 (1994
34. Bebenek, K. et al. Reduced frameshift fidelity and processivity of HIV-1 reverse transcriptase mutants containing alanine substitutions in helix H of the thumb subdomain. J. Biol. Chem. 270, 19516-19523 (1995
35. Bebenek, K. et al. A minor groove binding track in reverse transcriptase. Nat. Struct. Biol. 4, 194-197 (1997
36. Powell, M.D. et al. Residues in the aH and aI helices of the HIV-1 reverse transcriptase thumb subdomain required for the specificity of RNase H-catalyzed removal of the polypurine tract primer. J. Biol. Chem. 274, 19885-19893 (1999
37. North, T.W., Cronn, R.C., Remington, K.M., Tandberg, R.T. & Judd, R.C. Characterization of reverse transcriptase from feline immunodeficiency virus. J. Biol. Chem. 265, 5121-5128 (1990
38. Thomas, D.A. & Furman, P.A. Purification and kinetic characterization of equine infectious anemia virus reverse transcriptase. Biochem. Biophys. Res. Commun. 180, 1365-1371 (1991
39. Rausch, J.W. & Le Grice, S.F. 'Binding, bending and bonding': Polypurine tract-primed initiation of plus-strand DNA synthesis in human immunodeficiency virus. Int. J. Biochem. Cell Biol. 36, 1752-1766 (2004
40. Swapna, L.S., Srikeerthana, K. & Srinivasan, N. Extent of structural asymmetry in homodimeric proteins: Prevalence and relevance. PLoS ONE 7, e36688 (2012
41. Karplus, P.A. & Diederichs, K. Linking crystallographic model and data quality. Science 336, 1030-1033 (2012
42. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010
43. Afonine, P.V., Grosse-Kunstleve, R.W. & Adams, P.D. The Phenix refinement framework. CCP4 Newsl. 42, contribution 8 (2005
44. Emsley, P. & Cowtan, K. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004
45. Schuck, P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619 (2000.