Dominant negative inhibition of human immunodeficiency virus particle production by the nonmyristoylated form of Gag

Journal of Virology

Volumn 82, Issue 9, 2008, Pages 4384-4399

  Kawada, Shigeo ^a,d   Goto, Toshiyuki ^b   Haraguchi, Hiyori ^a   Ono, Akira ^c   Morikawa, Yuko ^a  

^a KITASATO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS; MYRISTYLATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; VIRION; VIRUS NUCLEOCAPSID; VIRUS PARTICLE;

CELL MEMBRANE; ENDOSOMES; GENE PRODUCTS, GAG; HELA CELLS; HIV; HUMANS; MICROSCOPY, ELECTRON; MYRISTIC ACID; SEQUENCE DELETION; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 42449108655     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01953-07     Document Type: Article

References (72)

1. Adachi, A., S. Koenig, H. E. Gendelman, D. Daugherty, S. Gattoni-Celli, A. S. Fauci, and M. A. Martin. 1987. Productive, persistent infection of human colorectal cell lines with human immunodeficiency virus. J. Virol. 61:209-213.
2. Aloia, R. C., H. Tian, and F. C. Jensen. 1993. Lipid composition and fluidity of the human immunodeficiency virus envelope and host cell plasma membranes. Proc. Natl. Acad. Sci. USA 90:5181-5185.
3. Amara, A., and D. R. Littman. 2003. After Hrs with HIV. J. Cell Biol. 162:371-375.
4. Andrawiss, M., Y. Takeuchi, L. Hewlett, and M. Collins. 2003. Murine leukemia virus particle assembly quantitated by fluorescence microscopy: role of Gag-Gag interactions and membrane association. J. Virol. 77:11651-11660.
5. Basyuk, E., T. Galli, M. Mougel, J. M. Blanchard, M. Sitbon, and E. Bertrand. 2003. Retroviral genomic RNAs are transported to the plasma membrane by endosomal vesicles. Dev. Cell 5:161-174.
6. Berkowitz, R. D., J. Luban, and S. P. Goff. 1993. Specific binding of human immunodeficiency virus type 1 Gag polyprotein and nucleocapsid protein to viral RNAs detected by RNA mobility shift assays. J. Virol. 67:7190-7200.
7. Borsetti, A., A. Ohagen, and H. G. Göttlinger. 1998. The C-terminal half of the human immunodeficiency virus type 1 Gag precursor is sufficient for efficient particle assembly. J. Virol. 72:9313-9317.
8. Brown, D. A., and E. London. 1998. Structure and origin of ordered lipid domains in biological membranes. J. Membr. Biol. 164:103-114.
9. Brügger, B., B. Glass, P. Haberkant, I. Leibrecht, F. T. Wieland, and H. G. Krausslich. 2006. The HIV lipidome: a raft with an unusual composition. Proc. Natl. Acad. Sci. USA 103:2641-2646.
10. Bryant, M., and L. Ratner. 1990. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. USA 87:523-527.
11. Bryant, M. L., R. O. Heuckeroth, J. T. Kimata, L. Ratner, and J. I. Gordon. 1989. Replication of human immunodeficiency virus 1 and Moloney murine leukemia virus is inhibited by different heteroatom-containing analogs of myristic acid. Proc. Natl. Acad. Sci. USA 86:8655-8659.
12. Burniston, M. T., A. Cimarelli, J. Colgan, S. P. Curtis, and J. Luban. 1999. Human immunodeficiency virus type 1 Gag polyprotein multimerization requires the nucleocapsid domain and RNA and is promoted by the capsid-dimer interface and the basic region of matrix protein. J. Virol. 73:8527-8540.
13. Dannull, J., A. Surovoy, G. Jung, and K. Moelling. 1994. Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J. 13:1525-1533.
14. Demirov, D. G., A. Ono, J. M. Orenstein, and E. O. Freed. 2002. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. USA 99:955-960.
15. Demirov, D. G., J. M. Orenstein, and E. O. Freed. 2002. The late domain of human immunodeficiency virus type 1 p6 promotes virus release in a cell type-dependent manner. J. Virol. 76:105-117.
16. Deneka, M., A. Pelchen-Matthews, R. Byland, E. Ruiz-Mateos, and M. Marsh. 2007. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J. Cell Biol. 177:329-341.
17. Dong, X., H. Li, A. Derdowski, L. Ding, A. Burnett, X. Chen, T. R. Peters, T. S. Dermody, E. Woodruff, J. J. Wang, and P. Spearman. 2005. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 120:663-674.
18. Dorfman, T., A. Bukovsky, A. Öhagen, S. Höglund, and H. G. Göttlinger. 1994. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68:8180-8187.
19. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32:257-283.
20. Gamble, T. R., F. F. Vajdos, S. Yoo, D. K. Worthylake, M. Houseweart, W. I. Sundquist, and C. P. Hill. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285-1294.
21. Gamble, T. R., S. Yoo, F. F. Vajdos, U. K. von Schwedler, D. K. Worthylake, H. Wang, J. P. McCutcheon, W. I. Sundquist, and C. P. Hill. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278:849-853.
22. Garnis, J. E., U. K. von Schwedler, O. W. Pornillos, S. G. Morham, K. H. Zavitz, H. E. Wang, D. A. Wettstein, K. M. Stray, M. Cote, R. L. Rich, D. G. Myszka, and W. I. Sundquist. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
23. Gheysen, D., E. Jacobs, F. de Foresta, C. Thiriart, M. Francotte, D. Thines, and M. De Wilde. 1989. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 59:103-112.
24. Göttlinger, H. G., T. Dorfman, J. G. Sodroski, and W. A. Haseltine. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. USA 88:3195-3199.
25. Göttlinger, H. G., J. G. Sodroski, and W. A. Haseltine. 1989. Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 86:5781-5785.
26. Grigorov, B., F. Arcanger, P. Roingeard, J. L. Darlix, and D. Muriaux. 2006. Assembly of infectious HIV-1 in human epithelial and T-lymphoblastic cell lines. J. Mol. Biol. 359:848-862.
27. Hancock, J. F. 2006. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7:456-462.
28. Harila, K., I. Prior, M. Sjoberg, A. Salminen, J. Hinkula, and M. Suomalainen. 2006. Vpu and Tsg101 regulate intracellular targeting of the human immunodeficiency virus type 1 core protein precursor Pr55gag. J. Virol. 80:3765-3772.
29. gag associates with membrane domains that are largely resistant to Brij98 but sensitive to Triton X-100. J. Virol. 77:4805-4817.
30. Huang, M., J. M. Orenstein, M. A. Martin, and E. O. Freed. 1995. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
31. Jouvenet, N., S. J. Neil, C. Bess, M. C. Johnson, C. A. Virgen, S. M. Simon, and P. D. Bieniasz. 2006. Plasma membrane is the site of productive HIV-1 particle assembly. PLoS Biol. 4:e435.
32. Langner, C. A., J. K. Lodge, S. J. Travis, J. E. Caldwell, T. Lu, Q. Li, M. L. Bryant, B. Devadas, G. W. Gokel, G. S. Kobayashi, and J. I. Gordon. 1992. 4-oxatetradecanoic acid is fungicidal for Cryptococcus neoformans and inhibits replication of human immunodeficiency virus I. J. Biol. Chem. 267:17159-17169.
33. Lichtenberg, D., F. M. Goni, and H. Heerklotz. 2005. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 30:430-436.
34. Lindwasser, O. W., and M. D. Resh. 2001. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75:7913-7924.
35. Lindwasser, O. W., and M. D. Resh. 2002. Myristoylation as a target for inhibiting HIV assembly: unsaturated fatty acids block viral budding. Proc. Natl. Acad. Sci. USA 99:13037-13042.
36. Martin-Serrano, J., T. Zang, and P. D. Bieniasz. 2001. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7:1313-1319.
37. Morikawa, Y., S. Hinata, H. Tomoda, T. Goto, M. Nakai, C. Aizawa, H. Tanaka, and S. Omura. 1996. Complete inhibition of human immunodeficiency virus Gag myristoylation is necessary for inhibition of particle budding. J. Biol. Chem. 271:2868-2873.
38. Munro, S. 2003. Lipid rafts: elusive or illusive? Cell 115:377-388.
39. Neil, S. J., S. W. Eastman, N. Jouvenet, and P. D. Bieniasz. 2006. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog. 2:e39.
40. Nelle, T. D., and J. W. Wills. 1996. A large region within the Rous sarcoma virus matrix protein is dispensable for budding and infectivity. J. Virol. 70:2269-2276.
41. Nguyen, D. G., A. Booth, S. J. Gould, and J. E. Hildreth. 2003. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J. Biol. Chem. 278:52347-52354.
42. Nguyen, D. H., and J. E. Hildreth. 2000. Evidence for budding of human immunodeficiency virus type 1 selectively from glycolipid-enriched membrane lipid rafts. J. Virol. 74:3264-3272.
43. Nydegger, S., M. Foti, A. Derdowski, P. Spearman, and M. Thali. 2003. HIV-1 egress is gated through late endosomal membranes. Traffic 4:902-910.
44. Ono, A., D. Demirov, and E. O. Freed. 2000. Relationship between human immunodeficiency virus type 1 Gag multimerization and membrane binding. J. Virol. 74:5142-5150.
45. Ono, A., and E. O. Freed. 1999. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J. Virol. 73:4136-4144.
46. Ono, A., and E. O. Freed. 2001. Plasma membrane rafts play a critical role in HIV-1 assembly and release. Proc. Natl. Acad. Sci. USA 98:13925-13930.
47. Ono, A., and E. O. Freed. 2004. Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J. Virol. 78:1552-1563.
48. Ono, A., J. M. Orenstein, and E. O. Freed. 2000. Role of the Gag matrix domain in targeting human immunodeficiency virus type 1 assembly. J. Virol. 74:2855-2866.
49. Ono, A., A. A. Waheed, A. Joshi, and E. O. Freed. 2005. Association of human immunodeficiency virus type 1 Gag with membrane does not require highly basic sequences in the nucleocapsid: use of a novel Gag multimerization assay. J. Virol. 79:14131-14140.
50. Ott, D. E., L. V. Coren, E. N. Chertova, T. D. Gagliardi, K. Nagashima, R. C. Sowder II, D. T. Poon, and R. J. Gorelick. 2003. Elimination of protease activity restores efficient virion production to a human immunodeficiency virus type 1 nucleocapsid deletion mutant. J. Virol. 77:5547-5556.
51. Paillart, J. C. and H. G. Göttlinger. 1999. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of gag membrane targeting. J. Virol. 73:2604-2612.
52. gag and is incorporated into viruslike particles. J. Virol. 66:6304-6313.
53. Pelchen-Matthews, A., B. Kramer, and M. Marsh. 2003. Infectious HIV-1 assembles in late endosomes in primary macrophages. J. Cell Biol. 162:443-455.
54. Perlman, M., and M. D. Resh. 2006. Identification of an intracellular trafficking and assembly pathway for HIV-1 gag. Traffic 6:731-745.
55. Raposo, G., M. Moore, D. Innes, R. Leijendekker, A. Leigh-Brown, P. Benaroch, and H. Geuze. 2002. Human macrophages accumulate HIV-1 particles in MHC II compartments. Traffic 3:718-729.
56. Reicin, A. S., S. Paik, R. D. Berkowitz, J. Luban, I. Lowy, and S. P. Goff. 1995. Linker insertion mutations in the human immunodeficiency virus type 1 gag gene: effects on virion particle assembly, release, and infectivity. J. Virol. 69:642-650.
57. Rein, A., M. R. McClure, N. R. Rice, R. B. Luftig, and A. M. Schultz. 1986. Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus. Proc. Natl. Acad. Sci. USA 83:7246-7250.
58. Saermark, T., A. Kleinschmidt, A. M. Wulff, H. Andreassen, A. Magee, and V. Erfie. 1991. Characterization of N-myristoyl transferase inhibitors and their effect on HIV release. AIDS 5:951-958.
59. Sakaguchi, K., N. Zambrano, E. T. Baldwin, B. A. Shapiro, J. W. Erickson, J. G. Omichinski, G. M. Clore, A. M. Gronenborn, and E. Appella. 1993. Identification of a binding site for the human immunodeficiency virus type 1 nucleocapsid protein. Proc. Natl. Acad. Sci. USA 90:5219-5223.
60. Gag. J. Virol. 72:2723-2732.
61. Sherer, N. M., M. J. Lehmann, L. F. Jimenez-Soto, A. Ingmundson, S. M. Horner, G. Cicchetti, P. G. Allen, M. Pypaert, J. M. Cunningham, and W. Mothes. 2003. Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4:785-801.
62. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
63. Stansell, E., E. Tytler, M. R. Walter, and E. Hunter. 2004. An early stage of Mason-Pfizer monkey virus budding is regulated by the hydrophobicity of the Gag matrix domain core. J. Virol. 78:5023-5031.
64. Tang, C., E. Loeliger, P. Luncsford, I. Kinde, D. Beckett, and M. F. Summers. 2004. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc. Natl. Acad. Sci. USA 101:517-522.
65. Tashiro, A., S. Shoji, and Y. Kubota. 1989. Antimyristoylation of the gag proteins in the human immunodeficiency virus-infected cells with N-myristoyl glycinal diethylacetal resulted in inhibition of virus production. Biochem. Biophys. Res. Commun. 165:1145-1154.
66. Gag. Proc. Natl. Acad. Sci. USA 98:7724-7729.
67. von Schwedler, U. K., T. L. Stemmler, V. Y. Klishko, S. Li, K. H. Albertine, D. R. Davis, and W. I. Sundquist. 1998. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17:1555-1568.
68. Wang, C. T., H. Y. Lai, and J. J. Li. 1998. Analysis of minimal human immunodeficiency virus type 1 gag coding sequences capable of virus-like particle assembly and release. J. Virol. 72:7950-7959.
69. Welsch, S., O. T. Keppler, A. Habermann, I. Allespach, J. Krijnse-Locker, and H. G. Krausslich. 2007. HIV-1 buds predominantly at the plasma membrane of primary human macrophages. PLoS Pathog. 3:e36.
70. Wills, J. W., C. E. Cameron, C. B. Wilson, Y. Xiang, R. P. Bennett, and J. Leis. 1994. An assembly domain of the Rous sarcoma virus Gag protein required late in budding. J. Virol. 68:6605-6618.
71. Zhou, W., L. J. Patent, J. W. Wills, and M. D. Resh. 1994. 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. 68:2556-2569.
72. Zhou, W., and M. D. Resh. 1996. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J. Virol. 70:8540-8548.