Role of capsid sequence and immature nucleocapsid proteins p9 and p15 in Human Immunodeficiency Virus type 1 genomic RNA dimerization

Virology

Volumn 385, Issue 1, 2009, Pages 233-244

  Kafaie, Jafar ^a,b   Dolatshahi, Marjan ^b   Ajamian, Lara ^a,b   Song, Rujun ^a,b   Mouland, Andrew J ^a,b   Rouiller, Isabelle ^b   Laughrea, Michael ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Capsid protein; Cores; Electron microscopy; HIV 1; Nucleocapsid protein; RNA dimerization

Indexed keywords

CAPSID PROTEIN; GAG PROTEIN; GENOMIC RNA; NUCLEOCAPSID PROTEIN; NUCLEOCAPSID PROTEIN P15; NUCLEOCAPSID PROTEIN P9; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; DIMERIZATION; ELECTRON MICROSCOPY; GENETIC TRANSFECTION; HELA CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTATION; NORTHERN BLOTTING; PLASMID; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; VIRION; VIRUS CAPSID; VIRUS ISOLATION; VIRUS REPLICATION;

DIMERIZATION; HELA CELLS; HIV INFECTIONS; HIV PROTEASE; HIV-1; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; NUCLEOCAPSID PROTEINS; RNA, VIRAL; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 60349097509     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.11.028     Document Type: Article

References (78)

1. Babé L.M., Rosé J., and Craik C.S. Trans-dominant inhibitory human immunodeficiency virus type 1 protease monomers prevent protease activation and virion maturation. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10069-10073
2. Bampi C., Bibillo A., Wendeler M., Divita G., Gorelick R.J., Le Grice S.F.J., and Darlix J.-L. Nucleotide excision repair and template-independent addition by HIV-1 reverse transcriptase in the presence of nucleocapsid protein. J. Biol. Chem. 281 (2006) 11736-11743
3. Benjamin J., Ganser-Pornillos B.K., Tivol W.F., Sundquist W.I., and Jensen G.J. Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J. Mol. Biol. 346 (2005) 577-588
4. Berthet-Colominas C., Monaco S., Novelli A., Sibai G., Mallet F., and Cusack S. Head-to-tail dimers and interdomain flexibility revealed by the crystal structure of HIV-1 capsid protein (p24) complexed with a monoclonal antibody Fab. EMBO J. 18 (1999) 1124-1136
5. Briggs J.A.G., Wilk T., Welker R., Krausslich H.-G., and Fuller S.D. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J. 22 (2003) 1707-1715
6. Briggs J.A.G., Simon M.N., Gross I., Krausslich H.G., and Fuller S.D. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11 (2004) 672-675
7. Cameron C.E., Ghosh M., Le Grice S.F.J., and Benkovic S.J. Mutations in HIV reverse transcriptase which alter RNase H activity and decrease strand transfer efficiency are suppressed by HIV nucleocapsid protein. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 6700-6705
8. Carrillo A., Stewart K.D., Sham H.L., Norbeck D.W., Kohlbrenner W.E., Leonard J.M., Kempf D.J., and Molla A. In vitro selection and characterization of human immunodeficiency virus type 1 variants with increased resistance to ABT-378, a novel protease inhibitor. J. Virol. 72 (1998) 7532-7541
9. Chassagne J., Verrelle P., Dionet C., Clavel F., Barre-Sinoussi F., Chermann J.C., Montagnier L., Gluckman J.C., and Klatzmann D. A monoclonal antibody against LAV gag precursor: use for viral protein analysis and antigenic expression in infected cells. J. Immunol. 136 (1986) 1442-1445
10. Chen N., Morag A., Almog N., Blumenzweig I., Dreazin O., and Kotler M. Extended nucleocapsid protein is cleaved from the Gag-Pol precursor of human immunodeficiency virus type 1. J. Gen.Virol. 82 (2001) 581-590
11. Cimarelli A., Sandin S., Hoglund S., and Luban J. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interactions with RNA. J. Virol. 74 (2000) 3046-3057
12. Cimarelli A., Sandin S., Hoglund S., and Luban J. Rescue of multiple viral functions by a second-site suppressor of a human inmunodeficiency virus type 1 nucleocapsid mutation. J. Virol. 74 (2000) 4273-4283
13. Cimarelli A., and Luban J. Context-dependent phenotype of a human immunodeficiency virus type 1 nucleocapsid mutation. J. Virol. 75 (2001) 7193-7197
14. Coren L.V., Thomas J.A., Chertova E., Sowder II R.C., Gagliardi T.D., Gorelick R.J., and Ott D.E. Mutational analysis of the C-terminal Gag cleavage sites in human immunodeficiency virus type 1. J. Virol. 81 (2007) 10047-10054
15. Croteau G., Doyon L., Thibeault D., McKercher G., Pilote L., and Lamarre D. Impaired fitness of human immunodeficiency virus type 1 variants with high-level resistance to protease inhibitors. J. Virol. 71 (1997) 1089-1096
16. Cruceanu M., Urbaneja M.A., Hixson C.V., Johnson D.G., Datta S.A., Fivash M.J., Stephen A.G., Fisher R.J., Gorelick R.J., Casas-Finet J.R., Rein A., Rouzina I., and Williams M.C. Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucl. Acids Res. 34 (2006) 593-605
17. 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
18. Davies D.R. The structure and function of the aspartic proteinases. Ann. Rev. Biophys. Biophys. Chem. 19 (1990) 189-215
19. DiIanni C., Davis L., Holloway M., Herber W.K., Darke P.L., Kohl N.E., and Dixon R.A. Characterization of an active single polypeptide form of the human immunodeficiency virus type 1 protease. J. Biol. Chem. 265 (1990) 17348-17354
20. Doyon L., Croteau G., Thibeault D., Poulin F., Pilote L., and Lamarre D. Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors. J. Virol. 70 (1996) 3763-3769
21. Dorfman T., Bukovsky A., Ohagen A., Hoglund S., and Gottlinger H.G. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68 (1994) 8180-8187
22. Dubouchet J., Adrian M., Chang J.J., Homo J.C., Lepault J., McDowall A.W., and Schultz P. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21 (1988) 129-228
23. Dulude D., Baril M., and Brakier-Gingras L. Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1. Nucleic Acids Res. 30 (2002) 5094-5102
24. Erickson-Viitanen S., Manfredi J., Viitanen P., Tribe D.E., Tritch R., Hutchison III C.A., Loeb D.D., and Swanstrom R. Cleavage of HIV-1 gag polyprotein synthesized in vitro: sequential cleavage by the viral protease. AIDS Res. Hum. Retroviruses 5 (1989) 577-591
25. Ganser-Pornillos B.K., Cheng A., and Yeager M. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 131 (2007) 70-79
26. Gottlinger H.G., Sodroski J.G., and Haseltine W.A. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 5781-5785
27. Gowda S.D., Stein B.S., and Engleman E.G. Identification of protein intermediates in the processing of the p55 HIV-1 gag precursor in cells infected with recombinant vaccinia virus. J. Biol. Chem. 264 (1989) 8459-8462
28. Harada S., Koyanagi Y., and Yamamoto N. Infection of HTLV III/LAV in HTLV-I-carrying cells MT-2 and MT-4 and application in a plaque assay. Science 229 (1985) 563-566
29. Henderson L.E., Bowers M.A., Sowder II R.C., Serabyn S.A., Johnson D.G., Bess J.J., Arthur L.O., Bryant D.K., and Fenselau C. Gag proteins of the highly replicative MN strain of human immunodeficiency virus type 1: posttranslational modifications, proteolytic processings, and complete amino acid sequences. J. Virol. 66 (1992) 1856-1865
30. Herskowitz I. Functional inactivation of genes by dominant negative mutations. Nature 329 (1987) 219-222
31. Kafaie J., Song R., Abrahamyan L., Mouland A.J., and Laughrea M. Mapping of nucleocapsid residues important for HIV-1 genomic RNA dimerization and packaging. Virology 375 (2008) 592-610
32. 2 symmetry-based HIV protease inhibitor, A77003, irreversibly inhibits infectivity of HIV-1 in vitro. AIDS Res. Hum. Retroviruses 10 (1994) 735-743
33. Kaplan A.H., and Swanstrom R. Human immunodeficiency virus type 1 Gag proteins are processed in two cellular compartments. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 4528-4532
34. Kaplan A.H., Zack J.A., Knigge M., Paul D.A., Kempf D.J., Norbeck D.W., and Swanstrom R. Partial inhibition of the human immunodeficiency virus type 1 protease results in aberrant virus assembly and the formation of noninfectious particles. J.Virol. 67 (1993) 4050-4055
35. Konvalinka J., Litterst M.A., Welker R., Kottler H., Rippmann F., Heuser A.M., and Kräusslich H.G. An active-site mutation in the human immunodeficiency virus type 1 proteinase (PR) causes reduced PR activity and loss of PR-mediated cytotoxicity without apparent effect on virus maturation and infectivity. J. Virol. 69 (1995) 7180-7186
36. Kräusslich H.G. Human immunodeficiency virus proteinase dimer as component of the viral polyprotein prevents particle assembly and viral infectivity. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 3213-3217
37. Laughrea M., and Jetté L. Kissing-loop model of HIV-1 genome dimerization: HIV-1 RNAs can assume alternative dimeric forms and all sequences upstream or downstream of hairpin 248-271 are dispensable for dimer formation. Biochemistry 35 (1996) 1589-1598
38. Laughrea M., Jetté L., Mak J., Kleiman L., Liang C., and Wainberg M.A. Mutations in the kissing-loop hairpin of human immunodeficiency virus type 1 reduce viral infectivity as well as genomic RNA packaging and dimerization. J. Virol. 71 (1997) 3397-3406
39. Laughrea M., Shen N., Jetté L., Darlix J.-L., Kleiman L., and Wainberg M.A. Role of distal zinc finger of nucleocapsid protein in genomic RNA dimerization of human immunodeficiency viryus type 1; no role for the palindrome crowning the R-U5 hairpin. Virology 281 (2001) 109-116
40. Lener D., Tanchou V., Roques B.P., Le Grice S.F.J., and Darlix J.-L. Involvement of HIV-1 nucleocapsid protein in the recruitment of reverse transcriptase into nucleoprotein complexes formed in vitro. J. Biol. Chem. 273 (1998) 33781-33786
41. 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
42. Ludtke J.J., Sebestyen M.G., and Wolff J.A. The effect of cell division on the cellular dynamics of microinjected DNA and dextran. Mol. Ther. 5 (2002) 579-588
43. Mammano F., Petit S.C., and Clavel F. Resistance-associated loss of viral fitness in human immunodeficiency virus type 1: phenotypic analysis of protease and gag coevolution in protease inhibitor-treated patients. J. Virol. 72 (1998) 7632-7637
44. Mervis R.J., Ahmad N., Lillehoj E.P., Raum M.G., Salazar F.H., Chan H.W., and Venkatesan S. The gag gene products of human immunodeficiency virus type 1: alignment within the gag open reading frame, identification of posttranslational modifications, and evidence for alternative gag precursors. J. Virol. 62 (1988) 3993-4002
45. Mirambeau G., Lyonnais S., Coulaud D., Hameau L., Lafosse S., Jeusset J., Justome A., Delain E., Gorelick E.J., and Le Cam E. Transmission electron microscopy reveals an optimal HIV-1 nucleocapsid aggregation with single-stranded nucleic acids and the mature HIV-1 nucleocapsid protein. J. Mol. Biol. 364 (2006) 496-511
46. Moore M.D., Fu W., Soheilian F., Nagashima K., Ptak R.G., Pathak V.K., and Hu W.-S. Suboptimal inhibition of protease activity in human immunodeficiency virus type 1: effects on virion morphogenesis and RNA maturation. Virology 379 (2008) 152-160
47. Mortuza G.B., Haire L.F., Stevens A., Smerdon S.J., Stoye J., and Taylor I.A. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature 431 (2004) 481-485
48. Pettit S.C., Moody M.D., Wehbie R.S., Kaplan A.H., Nantermet P.V., Klein C.A., and Swanstrom R. The p2 domain of human immunodeficiency virus type 1 Gag regulates sequential proteolytic processing and is required to produce fully infectious virions. J. Virol. 68 (1994) 8017-8027
49. Pettit S.C., Henderson G.J., Schiffer C.A., and Swanstrom R. Replacement of the P1 amino acid of human immunodeficiency virus type 1 Gag processing sites can inhibit or enhance the rate of cleavage by the viral protease. J. Virol. 76 (2002) 10226-10233
50. Pettit S.C., Everitt L.E., Choudhury S., Dunn B.M., and Kaplan A.H. Initial cleavage of the human immunodeficiency virus type 1 GagPol precursor by its activated protease occurs by an intramolecular mechanism. J. Virol. 78 (2004) 8477-8485
51. Poon D.T.K., Wu J., and Aldovini A. Charged amino acid residues of human immunodeficiency virus type 1 nucleocapsid p7 protein involved in RNA packaging and infectivity. J. Virol. 70 (1996) 6607-6616
52. Reicin A.S., Ohagen A., Yin L., Hoglund S., and Goff S.P. The role of Gag in human immunodeficiency virus type 1 virion morphogenesis and early steps of the viral life cycle. J. Virol. 70 (1996) 8645-8652
53. Rose R.B., Craik C.S., Douglas N.L., and Stroud R.M. Three-dimensional structures of HIV-1 and SIV protease product complexes. Biochemistry 35 (1996) 12933-12944
54. Rose R.E., Gong Y.-F., Greytok J.A., Bechtold C.M., Terry B.J., Robinson B.S., Alam M., Colonno R.J., and Lin P.-F. Human immunodeficiency virus type 1 viral background plays a major role in development of resistance to protease inhibitors. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 1648-1653
55. Rosé J.R., Babé L.M., and Craik C.S. Defining the level of human immunodeficiency virus type 1 (HIV-1) protease activity required for HIV-1 particle maturation and infectivity. J. Virol. 69 (1995) 2751-2758
56. Schock H.B., Garsky V.M., and Kuo L.C. Mutational anatomy of an HIV-1 protease variant conferring cross-resistance to protease inhibitors in clinical trials. Compensatory modulations of binding and activity. J. Biol Chem. 271 (1996) 31957-31963
57. Schwartz M.D., Fiore D., and Panganiban A.T. Distinct functions and requirements for the Cys-His boxes of the human immunodeficiency virus type 1 nucleocapsid protein during RNA encapsidation and replication. J. Virol. 71 (1997) 9295-9305
58. Shehu-Xhilaga M., Kraeusslich H.G., Pettit S., Swanstrom R., Lee J.Y., Marshall J.A., Crowe S.M., and Mak J. Proteolytic processing at the p2/nucleocapsid cleavage site is critical for human immunodeficiency virus type 1 RNA dimer maturation. J. Virol. 75 (2001) 9156-9164
59. Sheng N., and Erickson-Viitanen S. Cleavage of p15 protein in vitro by human immunodeficiency virus type 1 protease is RNA dependent. J. Virol. 68 (1994) 6207-6214
60. Sheng N., Pettit S.C., Tritch R.J., Ozturk D.H., Rayner M.M., Swanstrom R., and Erickson-Viitanen S. Determinants of the human immunodeficiency virus type 1 p15NC-RNA interaction that affect enhanced cleavage by the viral protease. J. Virol. 71 (1997) 5723-5732
61. Song R., Kafaie J., Yang L., and Laughrea M. HIV-1 Viral RNA is selected in the form of monomers that dimerize in a three-step protease-dependent process; the DIS of stem-loop 1 initiates viral RNA dimerization. J. Mol. Biol. 371 (2007) 1084-1098
62. Song R., Kafaie J., and Laughrea M. Role of the 5′ TAR stem-loop and the U5-AUG duplex in dimerization of HIV-1 genomic RNA. Biochemistry 47 (2008) 3283-3293
63. Spiegel, M.R., 1961. Theory and problems of statistics. Schaum's outline series, McGraw Hill.
64. Tang S., Murakami T., Agresta B.E., Campbell S., Freed E.O., and Levin J.G. Human immunodeficiency virus type 1 N-terminal capsid mutants that exhibit aberrant core morphology and are blocked in initiation of reverse transcription in infected cells. J. Virol. 75 (2001) 9366-9537
65. Thomas J.A., and Gorelick R.J. Nucleocapsid protein function in early infection processes. Virus Res. 134 (2008) 39-63
66. Tozser J., Blaha I., Copeland T.D., Wondrak E.M., and Oroszlan S. Comparison of the HIV-1 and HIV-2 proteinases using oligopeptide substrates representing cleavage sites in Gag and Gag-Pol polyproteins. FEBS Lett. 281 (1991) 77-80
67. Tseng W.-C., Haselton F.R., and Giorgio T.D. Transfection by cationic liposomes using simultaneously single cell measurements of plasmid delivery and transgene expression. J. Biol. Chem. 272 (1997) 25641-25647
68. Vaughan E.E., DeGiulio J.V., and Dean D.A. Intracellular trafficking of plasmids for gene therapy: mechanisms of cytoplasmic movement and nuclear import. Curr. Gene Ther. 6 (2006) 671-681
69. Veronese F.D., Rahman R., Copeland T.D., Oroszlan S., Gallo R.C., and Sarngadharan M.G. Immunological and chemical analysis of p6, the carboxyl-terminal fragment of HIV p15. AIDS Res. Hum. Retroviruses 3 (1987) 253-264
70. Von Schwedler U.K., Stemmler T.L., Klishko V.Y., Li S., Albertine K.H., Davis D.R., and Sundquist W.I. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17 (1998) 1555-1568
71. Von Schwedler U.K., Stray K.M., Garrus J.E., and Sundquist W.I. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77 (2003) 5439-5450
72. Wang S.-W., and Aldovini A. RNA incorporation is critical for retroviral particle integrity after cell membrane assembly of Gag complexes. J. Virol. 76 (2002) 11853-11865
73. Wang C.-T., and Barklis E. Assembly, processing and infectivity of human immunodeficiency virus type 1 gag mutants. J. Virol. 67 (1993) 4264-4273
74. Wang S.-W., Noonan K., and Aldovini A. Nucleocapsid-RNA interactions are esssential to structural stability but not to assembly of retroviruses. J. Virol. 78 (2004) 716-723
75. Wondrak E.M., Louis J.M., de Rocquigny H., Chermann J.-C., and Roques B.P. The gag precursor contains a specific HIV-1 protease cleavage site between the NC (p7) and p1 proteins. FEBS Lett. 333 (1993) 21-24
76. Yu X.-F., Matsuda Z., Yu Q.-C., and Essex M. Role of the C terminus Gag protein in human immunodeficiency virus type 1 virion assembly and maturation. J. Gen. Virol. 76 (1995) 3171-3179
77. Zhang Y.-M., Imamichi H., Imamichi T., Lane H.C., Fallon J., Vasudevachari M.B., and Salzman N.P. Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its gag substrate cleavages sites. J. Virol. 71 (1997) 6662-6670
78. Zybarth G., Krausslich H.-G., Partin K., and Carter C. Proteolytic activity of novel human immunodeficiency virus type 1 proteinase proteins from a precursor with a blocking mutation at the N-terminus of the PR domain. J. Virol. 68 (1994) 240-250