Cleavage of the murine leukemia virus transmembrane Env protein by human immunodeficiency virus type 1 protease: Transdominant inhibition by matrix mutations

Journal of Virology

Volumn 72, Issue 12, 1998, Pages 9621-9627

  Kiernan, Rosemary E ^a,b   Freed, Eric O ^a  

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

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; MATRIX PROTEIN; MUTANT PROTEIN; PROTEINASE; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE FUSION; MURINE LEUKEMIA VIRUS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; VESICULAR STOMATITIS VIRUS; VIRION; VIRUS INFECTIVITY;

EID: 0031743807     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.12.9621-9627.1998     Document Type: Article

References (71)

1. Brody, B. A., S. S. Rhee, and E. Hunter. 1994. Postassembly cleavage of a retroviral glycoprotein cytoplasmic domain removes a necessary incorporation signal and activates fusion activity. J. Virol. 68:4620-4627.
2. Brody, B. A., S. S. Rhee, M. A. Sommerfelt, and E. Hunter. 1992. A viral protease-mediated cleavage of the transmembrane glycoprotein of Mason-Pfizer monkey virus can be suppressed by mutations within the matrix protein. Proc. Natl. Acad. Sci. USA 89:3443-3447.
3. Bryant, M., and L. Ratner. 1990. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. USA 87:523-527.
4. Casella, C. R., L. J. Raffini, and A. T. Panganiban. 1997. Pleiotropic mutations in the HIV-1 matrix protein that affect diverse steps in replication. Virology 228:294-306.
5. Christensen, A. M., M. A. Massiah, B. G. Turner, W. I. Sundquist, and M. F. Summers. 1996. Three-dimensional structure of the HTLV-II matrix protein and comparative analysis of matrix proteins from the different classes of pathogenic human retroviruses. J. Mol. Biol. 264:1117-1131.
6. Conte, M. R., M. Klikova, E. Hunter, T. Ruml, and S. Matthews. 1997. The three-dimensional solution structure of the matrix protein from the type D retrovirus, the Mason-Pfizer monkey virus, and implications for the morphology of retroviral assembly. EMBO J. 16:5819-5826.
7. Cosset, F. L., and S. J. Russell. 1996. Targeting retrovirus entry. Gene Ther. 3:946-956.
8. Crawford, S., and S. P. Goff. 1985. A deletion mutation in the 5′ part of the pol gene of Moloney murine leukemia virus blocks proteolytic processing of the Gag and Pol polyproteins. J. Virol. 53:899-907.
9. Dorfman, T., F. Mammano, W. A. Haseltine, and H. G. Gottlinger. 1994. Role of the matrix protein in the virion association of the human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 68:1689-1696.
10. Dubay, J. W., S. J. Roberts, B. H. Hahn, and E. Hunter. 1992. Truncation of the human immunodeficiency virus type 1 transmembrane glycoprotein cytoplasmic domain blocks virus infectivity. J. Virol. 66:6616-6625.
11. Earl, P. L., S. Koenig, and B. Moss. 1991. Biological and immunological properties of human immunodeficiency virus type 1 envelope glycoprotein: analysis of proteins with truncations and deletions expressed by recombinant vaccinia viruses. J. Virol. 65:31-41.
12. Facke, M., A. Janetzko, R. L. Shoeman, and H. G. Krausslich. 1993. A large deletion in the matrix domain of the human immunodeficiency virus gag gene redirects virus particle assembly from the plasma membrane to the endoplasmic reticulum. J. Virol. 67:4972-4980.
13. Freed, E. O. HIV-1 Gag proteins: diverse functions in the virus life cycle. Virology, in press.
14. Freed, E. O., E. L. Delwart, G. L. Buchschacher, Jr., and A. T. Panganiban. 1992. A mutation in the human immunodeficiency virus type 1 transmembrane glycoprotein gp41 dominantly interferes with fusion and infectivity. Proc. Natl. Acad. Sci. USA 89:70-74.
15. Freed, E. O., G. Englund, and M. A. Martin. 1995. Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J. Virol. 69:3949-3954.
16. Freed, E. O., and M. A. Martin. 1996. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70:341-351.
17. 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 1 envelope glycoprotein gp120. J. Virol. 68:2503-2512.
18. Freed, E. O., and M. A. Martin. 1995. The role of human immunodeficiency virus type 1 envelope glycoproteins in virus infection. J. Biol. Chem. 270: 23883-23886.
19. 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.
20. Freed, E. O., D. J. Myers, and R. Risser. 1989. Mutational analysis of the cleavage sequence of the human immunodeficiency virus type 1 envelope glycoprotein precursor gp160. J. Virol. 63:4670-4675.
21. 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.
22. 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.
23. Garnier, L., M. Ravallec, P. Blanchard, H. Chaabihi, J. P. Bossy, G. Devauchelle, A. Jestin, and M. Cerutti. 1995. Incorporation of pseudorabies virus gD into human immunodeficiency virus type 1 Gag particles produced in baculovirus-infected cells. J. Virol. 69:4060-4068.
24. Gottlinger, 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.
25. Gray, K. D., and M. J. Roth. 1993. Mutational analysis of the envelope gene of Moloney murine leukemia virus. J. Virol. 67:3489-3496.
26. Green, R. W., and J. H. Shaper. 1981. Physical and chemical properties of the major envelope glycoprotein gp85 from avian myeloblastosis virus. Biochim. Biophys. Acta 668:439-447.
27. He, J., and N. R. Landau. 1995. Use of a novel human immunodeficiency virus type 1 reporter virus expressing human placental alkaline phosphatase to detect an alternative viral receptor. J. Virol. 69:4587-4592.
28. Henderson, L. E., R. Sowder, T. D. Copeland, G. Smythers, and S. Oroszlan. 1984. Quantitative separation of murine leukemia virus proteins by reversed-phase high-pressure liquid chromatography reveals newly described gag and env cleavage products. J. Virol. 52:492-500.
29. 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 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. USA 93:3099-3104.
30. Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
31. Januszeski, M. M., P. M. Cannon, D. Chen, Y. Rozenberg, and W. F. Anderson. 1997. Functional analysis of the cytoplasmic tail of Moloney murine leukemia virus envelope protein. J. Virol. 71:3613-3619.
32. Johnston, P. B., J. W. Dubay, and E. Hunter. 1993. Truncations of the simian immunodeficiency virus transmembrane protein confer expanded virus host range by removing a block to virus entry into cells. J. Virol. 67:3077-3086.
33. Karshin, W. L., L. J. Arcement, R. B. Naso, and R. B. Arlinghaus. 1977. Common precursor for Rauscher leukemia virus gp69/71, p15(E), and p12(E). J. Virol. 23:787-798.
34. Katoh, I., Y. Yoshinaka, A. Rein, M. Shibuya, T. Odaka, and S. Oroszlan. 1985. Murine leukemia virus maturation: protease region required for conversion from "immature" to "mature" core form and for virus infectivity. Virology 145:280-292.
35. Kiernan, R., and E. O. Freed. Unpublished results.
36. Kiernan, R. E., A. Ono, G. Englund, and E. O. Freed. 1998. Role of matrix in an early postentry step in the human immunodeficiency virus type 1 life cycle. J. Virol. 72:4116-4126.
37. Kimpton, J., and M. Emerman. 1992. Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated β-galactosidase gene. J. Virol. 66: 2232-2239.
38. Landau, N. R., K. A. Page, and D. R. Littman. 1991. Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J. Virol. 65:162-169.
39. Lodge, R., L. Delamarre, J. P. Lalonde, J. Alvarado, D. A. Sanders, M. C. Dokhelar, E. A. Cohen, and G. Lemay. 1997. Two distinct oncornaviruses harbor an intracytoplasmic tyrosine-based basolateral targeting signal in their viral envelope glycoprotein. J. Virol. 71:5696-5702.
40. Lusso, P., F. di Marzo Veronese, B. Ensoli, G. Franchini, C. Jemma, S. E. DeRocco, V. S. Kalyanaraman, and R. C. Gallo. 1990. Expanded HIV-1 cellular tropism by phenotypic mixing with murine endogenous retroviruses. Science 247:848-852.
41. Mammano, F., E. Kondo, J. Sodroski, A. Bukovsky, and H. G. Gottlinger. 1995. Rescue of human immunodeficiency virus type 1 matrix protein mutants by envelope glycoproteins with short cytoplasmic domains. J. Virol. 69:3824-3830.
42. Matthews, S., M. Mikhailov, A. Burny, and P. Roy. 1996. The solution structure of the bovine leukaemia virus matrix protein and similarity with lentiviral matrix proteins. EMBO J. 15:3267-3674.
43. McDonnell, J. M., D. Fushman, S. M. Cahill, W. Zhou, A. Wolven, C. B. Wilson, T. D. Nelle, M. D. Resh, J. Wills, and D. Cowburn. 1998. Solution structure and dynamics of the bioactive retroviral M domain from Rous sarcoma virus. J. Mol. Biol. 279:921-928.
44. Mulligan, M. J., G. V. Yamshchikov, G. D. Ritter, Jr., F. Gao, M. J. Jin, C. D. Nail, C. P. Spies, B. H. Hahn, and R. W. Compans. 1992. Cytoplasmic domain truncation enhances fusion activity by the exterior glycoprotein complex of human immunodeficiency virus type 2 in selected cell types. J. Virol. 66:3971-3975.
45. Ono, A., M. Huang, and E. O. Freed. 1997. Characterization of human immunodeficiency virus type 1 matrix revertants: effects on virus assembly, Gag processing, and Env incorporation into virions. J. Virol. 71:4409-4418.
46. Page, K. A., N. R. Landau, and D. R. Littman. 1990. Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity. J. Virol. 64:5270-5276.
47. Pal, R., M. S. Reitz, Jr., E. Tschachler, R. C. Gallo, M. G. Sarngadharan, and F. D. Veronese. 1990. Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly. AIDS Res. Hum. Retroviruses 6:721-730.
48. Pinter, A., and E. Fleissner. 1977. The presence of disulfide-linked gp70-p15(E) complexes in AKR murine leukemia virus. Virology 83:417-422.
49. Pinter, A., W. J. Honnen, J. S. Tung, P. V. O'Donnell, and U. Hammerling. 1982. Structural domains of endogenous murine leukemia virus gp70s containing specific antigenic determinants defined by monoclonal antibodies. Virology 116:499-516.
50. Ragheb, J. A., and W. F. Anderson. 1994. pH-independent murine leukemia virus ecotropic envelope-mediated cell fusion: implications for the role of the R peptide and p12E TM in viral entry. J. Virol. 68:3220-3231.
51. Rao, Z., A. S. Belyaev, E. Fry, P. Roy, I. M. Jones, and D. I. Stuart. 1995. Crystal structure of SIV matrix antigen and implications for virus assembly. Nature 378:743-747.
52. Reicin, A. S., A. Ohagen, L. Yin, S. Hoglund, and S. P. Goff. 1996. The role of Gag in human immunodeficiency virus type 1 virion morphogenesis and early steps of the viral life cycle. J. Virol. 70:8645-8652.
53. 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.
54. Rein, A., J. Mirro, J. G. Haynes, S. M. Ernst, and K. Nagashima. 1994. Function of the cytoplasmic domain of a retroviral transmembrane protein: p15E-p2E cleavage activates the membrane fusion capability of the murine leukemia virus Env protein. J. Virol. 68:1773-1781.
55. Reiser, J., G. Harmison, S. Kluepfel-Stahl, R. O. Brady, S. Karlsson, and M. Schubert. 1996. Transduction of nondividing cells using pseudotyped defective high-titer HIV type 1 particles. Proc. Natl. Acad. Sci. USA 93:15266-15271.
56. Rice, N. R., L. E. Henderson, R. C. Sowder, T. D. Copeland, S. Oroszlan, and J. F. Edwards. 1990. Synthesis and processing of the transmembrane envelope protein of equine infectious anemia virus. J. Virol. 64:3770-3778.
57. Ritter, G. D., Jr., M. J. Mulligan, S. L. Lydy, and R. W. Compans. 1993. Cell fusion activity of the simian immunodeficiency virus envelope protein is modulated by the intracytoplasmic domain. Virology 197:255-264.
58. Schultz, A., and A. Rein. 1985. Maturation of murine leukemia virus env proteins in the absence of other viral proteins. Virology 145:335-339.
59. Sommerfelt, M. A., S. R. Petteway, Jr., G. B. Dreyer, and E. Hunter. 1992. Effect of retroviral proteinase inhibitors on Mason-Pfizer monkey virus maturation and transmembrane glycoprotein cleavage. J. Virol. 66:4220-4227.
60. Spector, D. H., E. Wade, D. A. Wright, V. Koval, C. Clark, D. Jaquish, and S. A. Spector. 1990. Human immunodeficiency virus pseudotypes with expanded cellular and species tropism. J. Virol. 64:2298-2308.
61. Sutcliffe, J. G., T. M. Shinnick, N. Green, F. T. Liu, H. L. Niman, and R. A. Lerner. 1980. Chemical synthesis of a polypeptide predicted from nucleotide sequence allows detection of a new retroviral gene product. Nature 287:801-805.
62. Wang, C. T., Y. Zhang, J. McDermott, and E. Barklis. 1993. Conditional infectivity of a human immunodeficiency virus matrix domain deletion mutant. J. Virol. 67:7067-7076.
63. Wilk, T., T. Pfeiffer, and V. Bosch. 1992. Retained in vitro infectivity and cytopathogenicity of HIV-1 despite truncation of the C-terminal tail of the env gene product. Virology 189:167-177.
64. Willey, R. L., J. S. Bonifacino, B. J. Potts, M. A. Martin, and R. D. Klausner. 1988. Biosynthesis, cleavage, and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. Proc. Natl. Acad. Sci. USA 85:9580-9584.
65. Yang, C., and R. W. Compans. 1996. Analysis of the cell fusion activities of chimeric simian immunodeficiency virus-murine leukemia virus envelope proteins: inhibitory effects of the R peptide. J. Virol. 70:248-254.
66. 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.
67. Yu, X., Q. C. Yu, T. H. Lee, and M. Essex. 1992. The C terminus of human immunodeficiency virus type 1 matrix protein is involved in early steps of the virus life cycle. J. Virol. 66:5667-5670.
68. Yu, X., X. Yuan, Z. Matsuda, T. H. Lee, and M. Essex. 1992. The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions. J. Virol. 66:4966-4971.
69. Yuan, X., X. Yu, T. H. Lee, and M. Essex. 1993. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor. J. Virol. 67:6387-6394.
70. Zhou, W., L. J. Parent, 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.
71. Zingler, K., and D. R. Littman. 1993. Truncation of the cytoplasmic domain of the simian immunodeficiency virus envelope glycoprotein increases env incorporation into particles and fusogenicity and infectivity. J. Virol. 67: 2824-2831.