Cell-Type-Dependent Targeting of Human Immunodeficiency Virus Type 1 Assembly to the Plasma Membrane and the Multivesicular Body

Journal of Virology

Volumn 78, Issue 3, 2004, Pages 1552-1563

  Ono, Akira ^a,b   Freed, Eric O ^a,b  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; PROTEIN P6 GAG; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL MEMBRANE; CELL TYPE; CONTROLLED STUDY; ENDOSOME; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTRACELLULAR TRANSPORT; MACROPHAGE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; T LYMPHOCYTE; VIRUS ASSEMBLY; VIRUS PARTICLE; WILD TYPE;

ANTIGENS, CD; CELL MEMBRANE; CELLS, CULTURED; ENDOSOMES; GENE PRODUCTS, GAG; HELA CELLS; HIV-1; HUMANS; JURKAT CELLS; MACROPHAGES; MONOCYTES; MUTATION; ORGAN SPECIFICITY; PHOSPHOPROTEINS; PLATELET MEMBRANE GLYCOPROTEINS; VIRAL MATRIX PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 0347634393     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.3.1552-1563.2004     Document Type: Article

References (63)

1. Astarie-Dequeker, C., S. Carreno, C. Cougoule, and I. Maridonneau-Parini. 2002. The protein tyrosine kinase Hck is located on lysosomal vesicles that are physically and functionally distinct from CD63-positive lysosomes in human macrophages. J. Cell Sci. 115:81-89.
2. Babst, M., G. Odorizzi, E. J. Estepa, and S. D. Emr. 2000. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking. Traffic 1:248-258.
3. Chavrier, P., R. G. Parton, H. P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62:317-329.
4. Chen, B. K., I. Rousso, S. Shim, and P. S. Kim. 2001. Efficient assembly of an HIV-I/MLV Gag-chimeric virus in murine cells. Proc. Natl. Acad. Sci. USA 98:15239-15244.
5. Collman, R., N. F. Hassan, R. Walker, B. Godfrey, J. Cutilli, J. C. Hastings, H. Friedman, S. D. Douglas, and N. Nathanson. 1989. Infection of monocyte-derived macrophages with human immunodeficiency virus type 1 (HIV-1). Monocyte-tropic and lymphocyte-tropic strains of HIV-1 show distinctive patterns of replication in a panel of cell types. J. Exp. Med. 170:1149-1163.
6. 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.
7. 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.
8. Escola, J. M., M. J. Kleijmeer, W. Stoorvogel, J. M. Griffith, O. Yoshie, and H. J. Geuze. 1998. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273:20121-20127.
9. Facke, M., A. Janetzko, R. L. Shoeman, and H. G. Krausslich. 1993. A large deletion in the matrix domain of the human immunodeficiency virusgag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum. J. Virol. 67:4972-4980.
10. Fraile-Ramos, A., A. Pelchen-Matthews, T. N. Kledal, H. Browne, T. W. Schwartz, and M. Marsh. 2002. Localization of HCMV UL33 and US27 in endocytic compartments and viral membranes. Traffic 3:218-232.
11. Freed, E. O. 1998. HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251:1-15.
12. Freed, E. O. 2002. Viral late domains. J. Virol. 76:4679-4687.
13. Freed, E. O., E. L. Delwart, G. L. Buchschacher, Jr., and A. T. Panganiban. 1992. A mutation in the human immunodeficiency virus type I transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proc. Natl. Acad. Sci. USA 89:70-74.
14. Freed, E. O., G. Englund, and M. A. Martin. 1995. Role of the basic domain of human immunodeficiency virus type I matrix in macrophage infection. J. Virol. 69:3949-3954.
15. Freed, E. O., and M. A. Martin. 1994. Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type I envelope glycoprotein gp120. J. Virol. 68:2503-2512.
16. Freed, E. O., and M. A. Martin. 1995. Virion incorporation of envelope glycoproteins with long but not short cytoplasmic tails is blocked by specific, single amino acid substitutions in the human immunodeficiency virus type 1 matrix. J. Virol. 69:1984-1989.
17. Freed, E. O., J. M. Orenstein, A. J. Buckler-White, and M. A. Martin. 1994. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 68:5311-5320.
18. Gallina, A., G. Mantoan, G. Rindi, and G. Milanesi. 1994. Influence of MA internal sequences, but not of the myristylated N-terminus sequence, on the budding site of HIV-1 Gag protein. Biochem. Biophys. Res. Commun. 204:1031-1038.
19. Garrus, 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.
20. Gartner, S., P. Markovits, D. M. Markovitz, M. H. Kaplan, R. C. Gallo, and M. Popovic. 1986. The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233:215-219.
21. Gelderblom, H. R. 1991. Assembly and morphology of HIV: potential effect of structure on viral function. AIDS 5:617-637.
22. Gelderblom, H. R., M. Ozel, and G. Pauli. 1989. Morphogenesis and morphology of HIV. Structure-function relations. Arch. Virol. 106:1-13.
23. Goff, S. P. 2001. Retroviridae: the retroviruses and their replication, p. 1871-1940. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, Pa.
24. Hansen, M., L. Jelinek, S. Whiting, and E. Barklis. 1990. Transport and assembly of gag proteins into Moloney murine leukemia virus. J. Virol. 64:5306-5316.
25. Hermida-Matsumoto, L., and M. D. Resh. 2000. Localization of human immunodeficiency virus type I Gag and Env at the plasma membrane by confocal imaging. J. Virol. 74:8670-8679.
26. Hill, C. P., D. Worthylake, D. P. Bancroft, A. M. Christensen, and W. I. Sundquist. 1996. Crystal structures of the trimeric human immunodeficiency virus type I matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. USA 93:3099-3104.
27. Huang, M., J. M. Orenstein, M. A. Martin, and E. O. Freed. 1995. p6 Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
28. Katzmann, D. J., G. Odorizzi, and S. D. Emr. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905.
29. Kedzierska, K., and S. M. Crowe. 2002. The role of monocytes and macrophages in the pathogenesis of HIV-1 infection. Curr. Med. Chem. 9:1893-1903.
30. Kobayashi, T., E. Stang, K. S. Fang, P. de Moerloose, R. G. Parton, and J. Gruenberg. 1998. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392:193-197.
31. Koenig, S., H. E. Gendelman, J. M. Orenstein, M. C. Dal Canto, G. H. Pezeshkpour, M. Yungbluth, F. Janotta, A. Aksamit, M. A. Martin, and A. S. Fauci. 1986. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089-1093.
32. Kolesnikova, L., H. Bugany, H. D. Klenk, and S. Becker. 2002. VP40, the matrix protein of Marburg virus, is associated with membranes of the late endosomal compartment. J. Virol. 76:1825-1838.
33. Lee, P. P., and M. L. Linial. 1994. Efficient particle formation can occur if the matrix domain of human immunodeficiency virus type I Gag is substituted by a myristylation signal. J. Virol. 68:6644-6654.
34. 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.
35. Mariani, R., G. Rutter, M. E. Harris, T. J. Hope, H.-G. Kräusslich, and N. R. Landau. 2000. A block to human immunodeficiency virus type I assembly in murine cells. J. Virol. 74:3859-3870.
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. Meltzer, M. S., D. R. Skillman, P. J. Gomatos, D. C. Kalter, and H. E. Gendelman. 1990. Role of mononuclear phagocytes in the pathogenesis of human immunodeficiency virus infection. Annu. Rev. Immunol. 8:169-194.
38. 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.
39. Ono, A., M. Huang, and E. O. Freed. 1997. Characterization of human immunodeficiency virus type I matrix revertants: effects on virus assembly, Gag processing, and Env incorporation into virions. J. Virol. 71:4409-4418.
40. Ono, A., and M. Kawakita. 1994. Transport of envelope proteins of Sendai virus, HN and FO, is blocked at different steps by thapsigargin and other perturbants to intracellular Ca2+. J. Biochem. (Tokyo) 116:649-656.
41. Ono, A., J. M. Orenstein, and E. O. Freed. 2000. Role of the Gag matrix domain in targeting human immunodeficiency virus type I assembly. J. Virol. 74:2855-2866.
42. Orenstein, J. M., M. S. Meltzer, T. Phipps, and H. E. Gendelman. 1988. Cytoplasmic assembly and accumulation of human immunodeficiency virus types 1 and 2 in recombinant human colony-stimulating factor-I -treated human monocytes: an ultrastructural study. J. Virol. 62:2578-2586.
43. Patki, V., J. Virbasius, W. S. Lane, B. H. Toh, H. S. Shpetner, and S. Corvera. 1997. Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. USA 94:7326-7330.
44. 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.
45. Pornillas, O., J. E. Garrus, and W. I. Sundquist. 2002. Mechanisms of enveloped RNA virus budding. Trends Cell Biol. 12:569-579.
46. 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 compartmems. Traffic 3:718-729.
47. Reed, M., R. Mariani, L. Sheppard, K. Pekrun, N. R. Landau, and N. W. Soong. 2002. Chimeric human immunodeficiency virus type I containing murine leukemia virus matrix assembles in murine cells. J. Virol. 76:436-443.
48. Reil, H., A. A. Bukovsky, H. R. Gelderblom, and H. G. Gottlinger. 1998. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J. 17:2699-2708.
49. Scheifele, L. Z., J. D. Rhoads, and L. J. Parent. 2003. Specilicity of plasma membrane targeting by the Rous sarcoma virus Gag protein. J. Virol. 77:470-480.
50. Schubert, U., K. A. Clouse, and K. Strebel. 1995. Augmentation of virus secretion by the human immunodeficiency virus type I Vpu protein is cell type independent and occurs in cultured human primary macrophages and lymphocytes. J. Virol. 69:7699-7711.
51. Schubert, U., D. E. Ott, E. N. Chertova, R. Welker, U. Tessmer, M. F. Princiotta, J. R. Bennink, H. G. Krausslich, and J. W. Yewdell. 2000. Proteasome inhibition interferes with gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. Proc. Natl. Acad. Sci. USA 97:13057-13062.
52. Soneoka, Y., S. M. Kingsman, and A. J. Kingsman. 1997. Mutagenesis analysis of the murine leukemia virus matrix protein: identification of regions important for membrane localization and intracellular transport. J. Virol. 71:5549-5559.
53. Srinivasakumar, N., N. Chazal, C. Helga-Maria, S. Prasad, M. L. Hammarskjold, and D. Rekosh. 1997. The effect of viral regulatory protein expression on gene delivery by human immunodeficiency virus type 1 vectors produced in stable packaging cell lines. J. Virol. 71:5841-5848.
54. Stoorvogel, W., M. J. Kleijmeer, H. J. Geuze, and G. Raposo. 2002. The biogenesis and functions of exosomes. Traffic 3:321-330.
55. Swanstrom, R., and J. W. Wills. 1997. Synthesis, assembly, and processing of viral proteins, p. 263-334. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, N.Y.
56. Takenawa, T., and T. Itoh. 2001. Phosphoinositides, key molecules for regulation of actin cytoskeletal organization and membrane traffic from the plasma membrane. Biochim. Biophys. Acta 1533:190-206.
57. Toker, A. 2002. Phosphoinositides and signal transduction. Cell Mol. Life Sci. 59:761-779.
58. VerPlank, L., F. Bouamr, T. J. LaGrassa, B. Agresta, A. Kikonyogo, J. Leis, and C. A. Carter. 2001. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type I Pr55(Gag). Proc. Natl. Acad. Sci. USA 98:7724-7729.
59. Vitelli, R., M. Santillo, D. Lattero, M. Chiariello, M. Bifulco, C. B. Bruni, and C. Bucci. 1997. Role of the small GTPase Rab7 in the late endocytic pathway. J. Biol. Chem. 272:4391-4397.
60. 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.
61. Yee, J. K., T. Friedmann, and J. C. Burns. 1994. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 43:99-112.
62. Yuan, X., X. Yu, T. H. Lee, and M. Essex. 1993. Mutations in the N-terminal region of human immunodeficiency virus type I matrix protein block intracellular transport of the Gag precursor. J. Virol. 67:6387-6394.
63. Zhou, W., and M. D. Resh. 1996. Differential membrane binding of the human immunodeficiency virus type I matrix protein. J. Virol. 70:8540-8548.