Comparing capsid assembly of primate lentiviruses and hepatitis B virus using cell-free systems

Virology

Volumn 333, Issue 1, 2005, Pages 114-123

  Lingappa, Jaisri R ^a   Newman, Michael A ^a   Klein, Kevin C ^a   Dooher, Julia E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Assembly; Capsid; Cell free system; Gag; Hepatitis B virus; Hepatitis C virus; HIV; Human immunodeficiency virus; Myristoylation; Simian immunodeficiency virus; Targeting

Indexed keywords

CAPSID PROTEIN; CELL EXTRACT; VIRUS PROTEIN;

ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; HEPATITIS B VIRUS; LENTIVIRINAE; MICROBIAL DIVERSITY; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN SYNTHESIS; PROTEIN TARGETING; STATISTICAL SIGNIFICANCE; VIRUS ASSEMBLY; VIRUS CAPSID;

EUKARYOTA; HEPATITIS B VIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS; MIRIDAE; PRIMATES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 13544270914     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virol.2004.12.024     Document Type: Article

References (59)

1. C.S. Adamson, and I.M. Jones The molecular basis of HIV capsid assembly-five years of progress Rev. Med. Virol. 14 2 2004 107 121
2. R. Berkowitz, J. Fisher, and S.P. Goff RNA packaging Curr. Top Microbiol. Immunol. 214 1996 177 218
3. J.A. Briggs, M.N. Simon, I. Gross, H.G. Krausslich, S.D. Fuller, V.M. Vogt, and M.C. Johnson The stoichiometry of Gag protein in HIV-1 Nat. Struct. Mol. Biol. 11 7 2004 672 675
4. M. Bryant, and L. Ratner Myristoylation-dependent replication and assembly of human immunodeficiency virus 1 Proc. Natl. Acad. Sci. U.S.A. 87 2 1990 523 527
5. S. Campbell, and A. Rein In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain J. Virol. 73 3 1999 2270 2279
6. S. Campbell, and V.M. Vogt Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1 J. Virol. 69 10 1995 6487 6497
7. P. Ceres, and A. Zlotnick Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids Biochemistry 41 39 2002 11525 11531
8. G. Choi, S. Park, B. Choi, S. Hong, J. Lee, E. Hunter, and S.S. Rhee Identification of a cytoplasmic targeting/retention signal in a retroviral Gag polyprotein J. Virol. 73 7 1999 5431 5437
9. A. Cimarelli, S. Sandin, S. Hoglund, and J. Luban Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA J. Virol. 74 7 2000 3046 3057
10. J.E. Dooher, and J.R. Lingappa Cell-free capsid assembly of primate lentiviruses from three different lineages J. Med. Primatol. 33 5-6 2004 272 280
11. J.E. Dooher, and J.R. Lingappa Conservation of a step-wise, energy-sensitive pathway involving HP68 for assembly of primate lentiviral capsids in cells J. Virol. 78 4 2004 1645 1656
12. J.E. Dooher, M. Pineda, J. Overbaugh, and J.R. Lingappa Characterization of virus infectivity and cell-free capsid assembly of SIVmneCL8 J. Med. Primatol. 33 5-6 2004 262 271
13. R.J. Ellis Macromolecular crowding: an important but neglected aspect of the intracellular environment Curr. Opin. Struct. Biol. 11 1 2001 114 119
14. A.H. Erickson, and G. Blobel Cell-free translation of messenger RNA in a wheat germ system Methods Enzymol. 96 1983 38 50
15. E.O. Freed HIV-1 gag proteins: diverse functions in the virus life cycle Virology 251 1 1998 1 15
16. E.O. Freed, J.M. Orenstein, A.J. Buckler-White, and M.A. Martin Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production J. Virol. 68 8 1994 5311 5320
17. D. Ganem, and A.M. Prince Hepatitis B virus infection-natural history and clinical consequences N. Engl. J. Med. 350 11 2004 1118 1129
18. P.D. Garcia, J.H. Ou, W.J. Rutter, and P. Walter Targeting of the hepatitis B virus precore protein to the endoplasmic reticulum membrane: after signal peptide cleavage translocation can be aborted and the product released into the cytoplasm J. Cell Biol. 106 4 1988 1093 1104
19. L. Garnier, J.B. Bowzard, and J.W. Wills Recent advances and remaining problems in HIV assembly AIDS 12 Suppl. A 1998 S5 S16
20. D. Gheysen, E. Jacobs, F. de Foresta, C. Thiriart, M. Francotte, D. Thines, and M. De Wilde Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells Cell 59 1 1989 103 112
21. H.G. Gottlinger, J.G. Sodroski, and W.A. Haseltine 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 15 1989 5781 5785
22. B.H. Hahn, G.M. Shaw, K.M. De Cock, and P.M. Sharp AIDS as a zoonosis: scientific and public health implications Science 287 5453 2000 607 614
23. R.O. Heuckeroth, D.A. Towler, S.P. Adams, L. Glaser, and J.I. Gordon 11-(Ethylthio)undecanoic acid. A myristic acid analogue of altered hydrophobicity which is functional for peptide N-myristoylation with wheat germ and yeast acyltransferase J. Biol. Chem. 263 5 1988 2127 2133
24. J. Hu, and C. Seeger Hsp90 is required for the activity of a hepatitis B virus reverse transcriptase Proc. Natl. Acad. Sci. U.S.A. 93 3 1996 1060 1064
25. J. Hu, D.O. Toft, and C. Seeger Hepadnavirus assembly and reverse transcription require a multi- component chaperone complex which is incorporated into nucleocapsids EMBO J. 16 1 1997 59 68
26. M. Kann, B. Sodeik, A. Vlachou, W.H. Gerlich, and A. Helenius Phosphorylation-dependent binding of hepatitis B virus core particles to the nuclear pore complex J. Cell Biol. 145 1 1999 45 55
27. K.C. Klein, S.J. Polyak, and J.R. Lingappa Unique features of Hepatitis C Virus capsid formation revealed by de novo cell-free assembly J. Virol. 78 17 2004 9257 9269
28. Klein, K.C., Dellos, S.R., Lingappa, J.R., submitted for publication. Identification of residues in the hepatitic C virus core protein that are critical for capsid assembly in a free-cell system. Submitted for publication
29. P.P. Lee, and M.L. Linial Efficient particle formation can occur if the matrix domain of human immunodeficiency virus type 1 Gag is substituted by a myristoylation signal J. Virol. 68 10 1994 6644 6654
30. Lingappa, J.R., Lingappa, V.R., in press. Recent insights in biological regulation from cell-free protein synthesizing systems. Mt. Sinai J. Med. (in press).
31. J.R. Lingappa, R.L. Martin, M.L. Wong, D. Ganem, W.J. Welch, and V.R. Lingappa A eukaryotic cytosolic chaperonin is associated with a high molecular weight intermediate in the assembly of hepatitis B virus capsid, a multimeric particle J. Cell Biol. 125 1 1994 99 111
32. J.R. Lingappa, R.L. Hill, M.L. Wong, and R.S. Hegde A multistep, ATP-dependent pathway for assembly of human immunodeficiency virus capsids in a cell-free system J. Cell Biol. 136 3 1997 567 581
33. H. Mabit, K.M. Breiner, A. Knaust, B. Zachmann-Brand, and H. Schaller Signals for bidirectional nucleocytoplasmic transport in the duck hepatitis B virus capsid protein J. Virol. 75 4 2001 1968 1977
34. D.A. Melton, P.A. Krieg, M.R. Rebagliati, T. Maniatis, K. Zinn, and M.R. Green Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter Nucleic Acids Res. 12 18 1984 7035 7056
35. Y. Morikawa, S. Hinata, H. Tomoda, T. Goto, M. Nakai, C. Aizawa, H. Tanaka, and S. Omura Complete inhibition of human immunodeficiency virus Gag myristoylation is necessary for inhibition of particle budding J. Biol. Chem. 271 5 1996 2868 2873
36. M. Nassal Hepatitis B virus morphogenesis Curr. Top. Microbiol. Immunol. 214 1996 297 337
37. M. Nassal Hepatitis B virus replication: novel roles for virus-host interactions Intervirology 42 2-3 1999 100 116
38. A. Ono, and E.O. Freed Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus J. Virol. 73 5 1999 4136 4144
39. A. Ono, and E.O. Freed Plasma membrane rafts play a critical role in HIV-1 assembly and release Proc. Natl. Acad. Sci. U.S.A. 98 24 2001 13925 13930
40. A. Ono, M. Huang, and E.O. Freed Characterization of human immunodeficiency virus type 1 matrix revertants: effects on virus assembly, Gag processing, and Env incorporation into virions J. Virol. 71 6 1997 4409 4418
41. A. Ono, D. Demirov, and E.O. Freed Relationship between human immunodeficiency virus type 1 Gag multimerization and membrane binding J. Virol. 74 11 2000 5142 5150
42. J.C. Paillart, and H.G. Gottlinger Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of gag membrane targeting J. Virol. 73 4 1999 2604 2612
43. R. Pal, M.S. Reitz Jr., E. Tschachler, R.C. Gallo, M.G. Sarngadharan, and F.D. Veronese Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly AIDS Res. Hum. Retroviruses 6 6 1990 721 730
44. D. Perez-Caballero, T. Hatziioannou, J. Martin-Serrano, and P.D. Bieniasz Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on gag precursor-membrane interactions J. Virol. 78 17 2004 9560 9563
45. B. Rabe, A. Vlachou, N. Pante, A. Helenius, and M. Kann Nuclear import of hepatitis B virus capsids and release of the viral genome Proc. Natl. Acad. Sci. U.S.A. 100 17 2003 9849 9854
46. S.S. Rhee, and E. Hunter Myristoylation is required for intracellular transport but not for assembly of D-type retrovirus capsids J. Virol. 61 4 1987 1045 1053
47. M. Sakalian, and E. Hunter Separate assembly and transport domains within the Gag precursor of Mason-Pfizer monkey virus J. Virol. 73 10 1999 8073 8082
48. M. Sakalian, S.D. Parker, R.A. Weldon Jr., and E. Hunter Synthesis and assembly of retrovirus Gag precursors into immature capsids in vitro J. Virol. 70 6 1996 3706 3715
49. S. Sandefur, R.M. Smith, V. Varthakavi, and P. Spearman Mapping and characterization of the N-terminal I domain of human immunodeficiency virus type 1 Pr55(Gag) J. Virol. 74 16 2000 7238 7249
50. M. Seifer, S. Zhou, and D.N. Standring A micromolar pool of antigenically distinct precursors is required to initiate cooperative assembly of hepatitis B virus capsids in Xenopus oocytes J. Virol. 67 1 1993 249 257
51. J.N. Sfakianos, R.A. LaCasse, and E. Hunter The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell Traffic 4 10 2003 660 670
52. P. Spearman, and L. Ratner Human immunodeficiency virus type 1 capsid formation in reticulocyte lysates J. Virol. 70 11 1996 8187 8194
53. P. Spearman, J.J. Wang, N. Vander Heyden, and L. Ratner Identification of human immunodeficiency virus type 1 Gag protein domains essential to membrane binding and particle assembly J. Virol. 68 5 1994 3232 3242
54. D.A. Towler, J.I. Gordon, S.P. Adams, and L. Glaser The biology and enzymology of eukaryotic protein acylation Annu. Rev. Biochem. 57 1988 69 99
55. P. Walter, and G. Blobel Purification of a membrane-associated protein complex required for protein translocation across the endoplasmic reticulum Proc. Natl. Acad. Sci. U.S.A. 77 12 1980 7112 7116
56. X. Yuan, X. Yu, T.H. Lee, and M. Essex Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor J. Virol. 67 11 1993 6387 6394
57. S. Zhou, S.Q. Yang, and D.N. Standring Characterization of hepatitis B virus capsid particle assembly in Xenopus oocytes J. Virol. 66 5 1992 3086 3092
58. W. Zhou, L.J. Parent, J.W. Wills, and M.D. Resh Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids J. Virol. 68 4 1994 2556 2569
59. C. Zimmerman, K.C. Klein, P.K. Kiser, A.R.S. Singh, B.L. Firestein, S.C. Riba, and J.R. Lingappa Identification of a host protein essential for assembly of immature HIV-1 capsids Nature 415 2002 88 92