Nucleocapsid protein annealing of a primer-template enhances (+)-strand DNA synthesis and fidelity by HIV-1 reverse transcriptase

Journal of Molecular Biology

Volumn 415, Issue 5, 2012, Pages 866-880

  Kim, Jiae ^a   Roberts, Anne ^a,c   Yuan, Hua ^b   Xiong, Yong ^b   Anderson, Karen S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

^c WESTERN CONNECTICUT STATE UNIVERSITY   (United States)

Author keywords

HIV 1 nucleocapsid protein; HIV 1 reverse transcriptase; nucleocapsid facilitated annealing; transient kinetics

Indexed keywords

NUCLEOCAPSID PROTEIN; NUCLEOTIDE; PRIMER DNA; RNA DIRECTED DNA POLYMERASE; VIRUS DNA; ZINC FINGER PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA SYNTHESIS; DNA TEMPLATE; HEAT; PRIORITY JOURNAL; PROTEIN ANNEALING; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION; STEADY STATE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84862776728     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.12.034     Document Type: Article

References (54)

1. Darlix J.L., Garrido J.L., Morellet N., Mely Y., and de Rocquigny H. Properties, functions, and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus Adv. Pharmacol. 55 2007 299 346
2. Haseltine W.A. Molecular biology of the human immunodeficiency virus type 1 FASEB J. 5 1991 2349 2360 (Pubitemid 21905782)
3. Gorelick R.J., Chabot D.J., Rein A., Henderson L.E., and Arthur L.O. The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent J. Virol. 67 1993 4027 4036 (Pubitemid 23180727)
4. Sakaguchi K., Zambrano N., Baldwin E.T., Shapiro B.A., Erickson J.W., and Omichinski J.G. Identification of a binding site for the human immunodeficiency virus type 1 nucleocapsid protein Proc. Natl Acad. Sci. USA 90 1993 5219 5223 (Pubitemid 23183009)
5. South T.L., Blake P.R., Hare D.R., and Summers M.F. C-terminal retroviral-type zinc finger domain from the HIV-1 nucleocapsid protein is structurally similar to the N-terminal zinc finger domain Biochemistry 30 1991 6342 6349
6. Houzet L., Morichaud Z., Didierlaurent L., Muriaux D., Darlix J.L., and Mougel M. Nucleocapsid mutations turn HIV-1 into a DNA-containing virus Nucleic Acids Res. 36 2008 2311 2319 (Pubitemid 351567004)
7. You J.C., and McHenry C.S. Human immunodeficiency virus nucleocapsid protein accelerates strand transfer of the terminally redundant sequences involved in reverse transcription J. Biol. Chem. 269 1994 31491 31495 (Pubitemid 24379506)
8. Remy E., de Rocquigny H., Petitjean P., Muriaux D., Theilleux V., Paoletti J., and Roques B.P. The annealing of tRNA3Lys to human immunodeficiency virus type 1 primer binding site is critically dependent on the NCp7 zinc fingers structure J. Biol. Chem. 273 1998 4819 4822 (Pubitemid 28108627)
9. Levin J.G., Guo J., Rouzina I., and Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism Prog. Nucleic Acid Res. Mol. Biol. 80 2005 217 286 (Pubitemid 43574891)
10. Auxilien S., Keith G., Le Grice S.F., and Darlix J.L. Role of post-transcriptional modifications of primer tRNALys,3 in the fidelity and efficacy of plus strand DNA transfer during HIV-1 reverse transcription J. Biol. Chem. 274 1999 4412 4420
11. Bampi C., Jacquenet S., Lener D., Decimo D., and Darlix J.L. The chaperoning and assistance roles of the HIV-1 nucleocapsid protein in proviral DNA synthesis and maintenance Int. J. Biochem. Cell Biol. 36 2004 1668 1686 (Pubitemid 38748527)
12. Thomas J.A., and Gorelick R.J. Nucleocapsid protein function in early infection processes Virus Res. 134 2008 39 63
13. Levin J.G., Mitra M., Mascarenhas A., and Musier-Forsyth K. Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription RNA Biol. 7 2010 754 774
14. Ji X., Klarmann G.J., and Preston B.D. Effect of human immunodeficiency virus type 1 (HIV-1) nucleocapsid protein on HIV-1 reverse transcriptase activity in vitro Biochemistry 35 1996 132 143 (Pubitemid 26036416)
15. DeStefano J.J. Interaction of human immunodeficiency virus nucleocapsid protein with a structure mimicking a replication intermediate. Effects on stability, reverse transcriptase binding, and strand transfer J. Biol. Chem. 271 1996 16350 16356
16. Rodriguez-Rodriguez L., Tsuchihashi Z., Fuentes G.M., Bambara R.A., and Fay P.J. Influence of human immunodeficiency virus nucleocapsid protein on synthesis and strand transfer by the reverse transcriptase in vitro J. Biol. Chem. 270 1995 15005 15011
17. Peliska J.A., Balasubramanian S., Giedroc D.P., and Benkovic S.J. Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity Biochemistry 33 1994 13817 13823 (Pubitemid 24381946)
18. Tanchou V., Gabus C., Rogemond V., and Darlix J.L. Formation of stable and functional HIV-1 nucleoprotein complexes in vitro J. Mol. Biol. 252 1995 563 571
19. Grohmann D., Godet J., Mely Y., Darlix J.L., and Restle T. HIV-1 nucleocapsid traps reverse transcriptase on nucleic acid substrates Biochemistry 46 2008 12230 12240
20. Mougel M., Houzet L., and Darlix J.L. When is it time for reverse transcription to start and go? Retrovirology 6 2009 24
21. Post K., Kankia B., Gopalakrishnan S., Yang V., Cramer E., and Saladores P. Fidelity of plus-strand priming requires the nucleic acid chaperone activity of HIV-1 nucleocapsid protein Nucleic Acids Res. 37 2009 1755 1766
22. Jacob D.T., and DeStefano J.J. A new role for HIV nucleocapsid protein in modulating the specificity of plus strand priming Virology 378 2008 385 396
23. Didierlaurent L., Houzet L., Morichaud Z., Darlix J.L., and Mougel M. The conserved N-terminal basic residues and zinc-finger motifs of HIV-1 nucleocapsid restrict the viral cDNA synthesis during virus formation and maturation Nucleic Acids Res. 36 2008 4745 4753
24. Iwatani Y., Rosen A.E., Guo J., Musier-Forsyth K., and Levin J.G. Efficient initiation of HIV-1 reverse transcription in vitro. Requirement for RNA sequences downstream of the primer binding site abrogated by nucleocapsid protein-dependent primer-template interactions J. Biol. Chem. 278 2003 14185 14195 (Pubitemid 36799966)
25. Egele C., Schaub E., Ramalanjaona N., Piemont E., Ficheux D., and Roques B. HIV-1 nucleocapsid protein binds to the viral DNA initiation sequences and chaperones their kissing interactions J. Mol. Biol. 342 2004 453 466 (Pubitemid 39149750)
26. Egele C., Schaub E., Piemont E., de Rocquigny H., and Mely Y. Investigation by fluorescence correlation spectroscopy of the chaperoning interactions of HIV-1 nucleocapsid protein with the viral DNA initiation sequences C. R. Biol. 328 2005 1041 1051 (Pubitemid 41824040)
27. Li X., Quan Y., Arts E.J., Li Z., Preston B.D., and de Rocquigny H. Human immunodeficiency virus type 1 nucleocapsid protein (NCp7) directs specific initiation of minus-strand DNA synthesis primed by human tRNA(Lys3) in vitro: studies of viral RNA molecules mutated in regions that flank the primer binding site J. Virol. 70 1996 4996 5004 (Pubitemid 26240669)
28. Lener D., Tanchou V., Roques B.P., Le Grice S.F., and Darlix J.L. Involvement of HIV-I nucleocapsid protein in the recruitment of reverse transcriptase into nucleoprotein complexes formed in vitro J. Biol. Chem. 273 1998 33781 33786 (Pubitemid 29005769)
29. Druillennec S., Caneparo A., de Rocquigny H., and Roques B.P. Evidence of interactions between the nucleocapsid protein NCp7 and the reverse transcriptase of HIV-1 J. Biol. Chem. 274 1999 11283 11288
30. Kati W.M., Johnson K.A., Jerva L.F., and Anderson K.S. Mechanism and fidelity of HIV reverse transcriptase J. Biol. Chem. 267 1992 25988 25997 (Pubitemid 23014006)
31. You J.C., and McHenry C.S. HIV nucleocapsid protein. Expression in Escherichia coli, purification, and characterization J. Biol. Chem. 268 1993 16519 16527 (Pubitemid 23229960)
32. Lener D., Benarous R., and Calogero R.A. Use of a constrain phage displayed-peptide library for the isolation of peptides binding to HIV-1 nucleocapsid protein (NCp7) FEBS Lett. 361 1995 85 88
33. Divita G., Restle T., and Goody R.S. Characterization of the dimerization process of HIV-1 reverse transcriptase heterodimer using intrinsic protein fluorescence FEBS Lett. 324 1993 153 158 (Pubitemid 23170405)
34. Thrall S.H., Reinstein J., Wohrl B.M., and Goody R.S. Evaluation of human immunodeficiency virus type 1 reverse transcriptase primer tRNA binding by fluorescence spectroscopy: specificity and comparison to primer/template binding Biochemistry 35 1996 4609 4618 (Pubitemid 26113523)
35. Feng J.Y., and Anderson K.S. Mechanistic studies comparing the incorporation of (+) and (-) isomers of 3TCTP by HIV-1 reverse transcriptase Biochemistry 38 1999 55 63 (Pubitemid 29035670)
36. Chen Y., Balakrishnan M., Roques B.P., Fay P.J., and Bambara R.A. Mechanism of minus strand strong stop transfer in HIV-1 reverse transcription J. Biol. Chem. 278 2003 8006 8017 (Pubitemid 36800539)
37. Gao L., Balakrishnan M., Roques B.P., and Bambara R.A. Insights into the multiple roles of pausing in HIV-1 reverse transcriptase-promoted strand transfers J. Biol. Chem. 282 2007 6222 6231 (Pubitemid 47100814)
38. Vartanian J.P., Plikat U., Henry M., Mahieux R., Guillemot L., Meyerhans A., and Wain-Hobson S. HIV genetic variation is directed and restricted by DNA precursor availability J. Mol. Biol. 270 1997 139 151 (Pubitemid 27296676)
39. Traut T.W. Physiological concentrations of purines and pyrimidines Mol. Cell. Biochem. 140 1994 1 22 (Pubitemid 24379884)
40. Muriaux D., and Darlix J.L. Properties and functions of the nucleocapsid protein in virus assembly RNA Biol. 7 2010 744 753
41. Godet J., and Mely Y. Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein RNA Biol. 7 2010 687 699
42. Cen S., Khorchid A., Gabor J., Rong L., Wainberg M.A., and Kleiman L. Roles of Pr55(gag) and NCp7 in tRNA(3)(Lys) genomic placement and the initiation step of reverse transcription in human immunodeficiency virus type 1 J. Virol. 74 2000 10796 10800
43. Hargittai M.R., Mangla A.T., Gorelick R.J., and Musier-Forsyth K. HIV-1 nucleocapsid protein zinc finger structures induce tRNA(Lys,3) structural changes but are not critical for primer/template annealing J. Mol. Biol. 312 2001 985 997 (Pubitemid 32980320)
44. Tisne C., Roques B.P., and Dardel F. Heteronuclear NMR studies of the interaction of tRNA(Lys)3 with HIV-1 nucleocapsid protein J. Mol. Biol. 306 2001 443 454 (Pubitemid 33027714)
45. Cruceanu M., Gorelick R.J., Musier-Forsyth K., Rouzina I., and Williams M.C. Rapid kinetics of protein-nucleic acid interaction is a major component of HIV-1 nucleocapsid protein's nucleic acid chaperone function J. Mol. Biol. 363 2006 867 877 (Pubitemid 44573231)
46. Darlix J.L., Godet J., Ivanyi-Nagy R., Fosse P., Mauffret O., and Mely Y. Flexible nature and specific functions of the HIV-1 nucleocapsid protein J. Mol. Biol. 410 2011 565 581
47. Druillennec S., Dong C.Z., Escaich S., Gresh N., Bousseau A., Roques B.P., and Fournie-Zaluski M.C. A mimic of HIV-1 nucleocapsid protein impairs reverse transcription and displays antiviral activity Proc. Natl Acad. Sci. USA 96 1999 4886 4891 (Pubitemid 29214505)
48. Miller Jenkins L.M., Hara T., Durell S.R., Hayashi R., Inman J.K., and Piquemal J.P. Specificity of acyl transfer from 2-mercaptobenzamide thioesters to the HIV-1 nucleocapsid protein J. Am. Chem. Soc. 129 2007 11067 11078 (Pubitemid 47435710)
49. Morellet N., Jullian N., De Rocquigny H., Maigret B., Darlix J.L., and Roques B.P. Determination of the structure of the nucleocapsid protein NCp7 from the human immunodeficiency virus type 1 by 1H NMR EMBO J. 11 1992 3059 3065
50. Amarasinghe G.K., De Guzman R.N., Turner R.B., Chancellor K.J., Wu Z.R., and Summers M.F. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition J. Mol. Biol. 301 2000 491 511
51. Summers M.F., Henderson L.E., Chance M.R., Bess J.W. Jr, South T.L., and Blake P.R. Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1 Protein Sci. 1 1992 563 574 (Pubitemid 23009191)
52. Kerr S.G., and Anderson K.S. RNA dependent DNA replication fidelity of HIV-1 reverse transcriptase: evidence of discrimination between DNA and RNA substrates Biochemistry 36 1997 14056 14063 (Pubitemid 27509840)
53. Anderson K.S., Sikorski J.A., and Johnson K.A. Evaluation of 5-enolpyruvoylshikimate-3-phosphate synthase substrate and inhibitor binding by stopped-flow and equilibrium fluorescence measurements Biochemistry 27 1988 1604 1610
54. Anderson K.S., Sikorski J.A., and Johnson K.A. Evaluation of 5-enolpyruvoylshikimate-3-phosphate synthase substrate and inhibitor binding by stopped-flow and equilibrium fluorescence measurements Biochemistry 27 1988 1604 1610