The removal of RNA primers from DNA synthesized by the reverse transcriptase of the retrotransposon Tf1 Is stimulated by Tf1 integrase

Journal of Virology

Volumn 86, Issue 11, 2012, Pages 6222-6230

  Herzig, Eytan ^a   Voronin, Nickolay ^a   Hizi, Amnon ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; INTEGRASE; PRIMER RNA; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; TF1 INTEGRASE; UNCLASSIFIED DRUG; MUTANT PROTEIN; RNA; RNA PRIMERS;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA STRAND; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INDUCTION; ENZYME REGULATION; ENZYME SUBSTRATE COMPLEX; HUMAN IMMUNODEFICIENCY VIRUS; MURINE LEUKEMIA VIRUS; MUTAGENESIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FOLDING; RETROPOSON; REVERSE TRANSCRIPTION; ZINC FINGER MOTIF; ENZYMOLOGY; GENETICS; METABOLISM; MISSENSE MUTATION;

HUMAN IMMUNODEFICIENCY VIRUS; MURINE LEUKEMIA VIRUS;

DNA, COMPLEMENTARY; HIV; INTEGRASES; LEUKEMIA VIRUS, MURINE; MUTANT PROTEINS; MUTATION, MISSENSE; RETROELEMENTS; RIBONUCLEASE H; RNA; RNA-DIRECTED DNA POLYMERASE;

EID: 84863599760     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00009-12     Document Type: Article

References (41)

1. Atwood-Moore A, Ejebe K, Levin HL. 2005. Specific recognition and cleavage of the plus-strand primer by reverse transcriptase. J. Virol. 79: 14863-14875.
2. Atwood-Moore A, Yan K, Judson RL, Levin HL. 2006. The self primer of the long terminal repeat retrotransposon Tf1 is not removed during reverse transcription. J. Virol. 80:8267-8270.
3. Atwood A, Choi J, Levin HL. 1998. The application of a homologous recombination assay revealed amino acid residues in an LTRretrotransposon that were critical for integration. J. Virol. 72:1324-1333.
4. Avidan O, Loya S, Tonjes RR, Sevilya Z, Hizi A. 2003. Expression and characterization of a recombinant novel reverse transcriptase of a porcine endogenous retrovirus. Virology 307:341-357.
5. Bushman FD, Engelman A, Palmer I, Wingfield P, Craigie R. 1993. Domains of the integrase protein of human immunodeficiency virus type 1 responsible for polynucleotidyl transfer and zinc binding. Proc. Natl. Acad. Sci. U. S. A. 90:3428-3432.
6. Butler M, Goodwin T, Simpson M, Singh M, Poulter R. 2001. Vertebrate LTR retrotransposons of the Tf1/sushi group. J. Mol. Evol. 52:260-274.
7. Champoux JJ, Schultz SJ. 2009. Ribonuclease H: properties, substrate specificity and roles in retroviral reverse transcription. FEBS J. 276:1506-1516.
8. Coffin JM, Hughes SH, Varmus HE. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
9. Craig NL, Craigie R, Gellert M, Lambowitz AM. 2002. Mobile DNA II. ASM Press, Washington, DC.
10. Craigie R. 2001. HIV integrase, a brief overview from chemistry to therapeutics. J. Biol. Chem. 276:23213-23216.
11. Dobard CW, Briones MS, Chow SA. 2007. Molecular mechanisms by which human immunodeficiency virus type 1 integrase stimulates the early steps of reverse transcription. J. Virol. 81:10037-10046.
12. Hare S, Gupta SS, Valkov E, Engelman A, Cherepanov P. 2010. Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 464:232-236.
13. Havecker ER, Gao X, Voytas DF. 2004. The diversity of LTR retrotransposons. Genome Biol. 5:225.
14. Herschhorn A, Hizi A. 2010. Retroviral reverse transcriptases. Cell. Mol. Life Sci. 67:2717-2747.
15. Herschhorn A, Oz-Gleenberg I, Hizi A. 2008. Quantitative analysis of the interactions between HIV-1 integrase and retroviral reverse transcriptases. Biochem. J. 412:163-170.
16. Hizi A. 2008. The reverse transcriptase of the Tf1 retrotransposon has a specific novel activity for generating theRNAself-primer that is functional in cDNA synthesis. J. Virol. 82:10906-10910.
17. Hizi A, Herschhorn A. 2008. Retroviral reverse transcriptases (other than those of HIV-1 and murine leukemia virus): a comparison of their molecular and biochemical properties. Virus Res. 134:203-220.
18. Hizi A, Hughes SH. 1988. Expression in Escherichia coli of a Moloney murine leukemia virus reverse transcriptase whose structure closely resembles the viral enzyme. Gene 66:319-323.
19. Hizi A, Leis JP, Joklik WK. 1977. RNA-dependent DNA polymerase of avian sarcoma virus B77. II. Comparison of the catalytic properties of the alpha, beta2, and alphabeta enzyme forms. J. Biol. Chem. 252:2290-2295.
20. Hizi A, Levin HL. 2005. The integrase of the long terminal repeatretrotransposon tf1 has a chromodomain that modulates integrase activities. J. Biol. Chem. 280:39086-39094.
21. Hizi A, McGill C, Hughes SH. 1988. Expression of soluble, enzymatically active, human immunodeficiency virus reverse transcriptase in Escherichia coli and analysis of mutants. Proc. Natl. Acad. Sci. U. S. A. 85:1218-1222.
22. Hizi A, Tal R, Shaharabany M, Loya S. 1991. Catalytic properties of the reverse transcriptases of human immunodeficiency viruses type 1 and type J. Biol. Chem. 266:6230-6239.
23. Hu SC, Court DL, Zweig M, Levin JG. 1986. Murine leukemia virus pol gene products: analysis with antisera generated against reverse transcriptase and endonuclease fusion proteins expressed in Escherichia coli. J. Virol. 60:267-274.
24. Jaskolski M, Alexandratos JN, Bujacz G, Wlodawer A. 2009. Piecing together the structure of retroviral integrase, an important target in AIDS therapy. FEBS J. 276:2926-2946.
25. Kirshenboim N, Hayouka Z, Friedler A, Hizi A. 2007. Expression and characterization of a novel reverse transcriptase of the LTR retrotransposon Tf1. Virology 366:263-276.
26. Le Grice SF. 2003. "In the beginning": initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42:14349-14355.
27. Levin HL. 1995. A novel mechanism of self-primed reverse transcription defines a new family of retroelements. Mol. Cell. Biol. 15:3310-3317.
28. Levin HL. 1996. An unusual mechanism of self-primed reverse transcription requires the RNase H domain of reverse transcriptase to cleave an RNA duplex. Mol. Cell. Biol. 16:5645-5654.
29. Lin JH, Levin HL. 1997. A complex structure in the mRNA of Tf1 is recognized and cleaved to generate the primer of reverse transcription. Genes Dev. 11:270-285.
30. Lin JH, Levin HL. 1997. Self-primed reverse transcription is a mechanism shared by several LTR-containing retrotransposons. RNA 3:952-953.
31. Malik HS, Eickbush TH. 1999. Modular evolution of the integrase domain in the Ty3/Gypsy class of LTR retrotransposons. J. Virol. 73:5186-5190.
32. Nymark-McMahon MH, Beliakova-Bethell NS, Darlix JL, Le Grice SF, Sandmeyer SB. 2002. Ty3 integrase is required for initiation of reverse transcription. J. Virol. 76:2804-2816.
33. Oz Gleenberg I, Herschhorn A, Goldgur Y, Hizi A. 2007. Inhibition of human immunodeficiency virus type-1 reverse transcriptase by a novel peptide derived from the viral integrase. Arch. Biochem. Biophys. 458: 202-212.
34. Oz Gleenberg I, Avidan O, Goldgur Y, Herschhorn A, Hizi A. 2005. Peptides derived from the reverse transcriptase of human immunodeficiency virus type 1 as novel inhibitors of the viral integrase. J. Biol. Chem. 280:21987-21996.
35. Oz I, Avidan O, Hizi A. 2002. Inhibition of the integrases of human immunodeficiency viruses type 1 and type 2 by reverse transcriptases. Biochem. J. 361:557-566.
36. Schultz SJ, Zhang M, Champoux JJ. 2003. Specific cleavages by RNase H facilitate initiation of plus-strand RNA synthesis by Moloney murine leukemia virus. J. Virol. 77:5275-5285.
37. Sevilya Z, Loya S, Hughes SH, Hizi A. 2001. The ribonuclease H activity of the reverse transcriptases of human immunodeficiency viruses type 1 and type 2 is affected by the thumb subdomain of the small protein subunits. J. Mol. Biol. 311:957-971.
38. Skalka AM, Goff SP. 1993. Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Steele SJ, Levin HL. 1998. A map of interactions between the proteins of a retrotransposon. J. Virol. 72:9318-9322.
40. Wilhelm M, Wilhelm FX. 2005. Role of integrase in reverse transcription of the Saccharomyces cerevisiae retrotransposon Ty1. Eukaryot. Cell 4:1057-1065.
41. Wilkinson TA, et al. 2009. Identifying and characterizing a functional HIV-1 reverse transcriptase-binding site on integrase. J. Biol. Chem. 284: 7931-7939.