Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1994 Aug;68(8):5311–5320. doi: 10.1128/jvi.68.8.5311-5320.1994

Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production.

E O Freed 1, J M Orenstein 1, A J Buckler-White 1, M A Martin 1
PMCID: PMC236481  PMID: 8035531

Abstract

The matrix protein of human immunodeficiency virus type 1 is encoded by the amino-terminal portion of the Gag precursor and is postulated to be involved in a variety of functions in the virus life cycle. To define domains and specific amino acid residues of the matrix protein that are involved in virus particle assembly, we introduced 35 amino acid substitution mutations in the human immunodeficiency virus type 1 matrix protein. Using reverse transcriptase and radioimmunoprecipitation analyses and transmission electron microscopy, we assessed the mutants for their ability to form virus particles and to function in the infection process. This study has identified several domains of the matrix protein in which single amino acid substitutions dramatically reduce the efficiency of virus particle production. These domains include the six amino-terminal residues of matrix, the region of matrix between amino acids 55 and 59, and the region between amino acids 84 and 95. Single amino acid substitutions in one of these domains (between matrix amino acids 84 and 88) result in a redirection of the majority of virus particle formation to sites within cytoplasmic vacuoles.

Full text

PDF
5311

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adachi A., Gendelman H. E., Koenig S., Folks T., Willey R., Rabson A., Martin M. A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol. 1986 Aug;59(2):284–291. doi: 10.1128/jvi.59.2.284-291.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blomberg J., Medstrand P. A sequence in the carboxyl terminus of the HIV-1 matrix protein is highly similar to sequences in membrane-associated proteins of other RNA viruses: possible functional implications. New Biol. 1990 Nov;2(11):1044–1046. [PubMed] [Google Scholar]
  3. Bryant M., Ratner L. Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc Natl Acad Sci U S A. 1990 Jan;87(2):523–527. doi: 10.1073/pnas.87.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bukrinskaya A. G., Vorkunova G. K., Tentsov YYu HIV-1 matrix protein p17 resides in cell nuclei in association with genomic RNA. AIDS Res Hum Retroviruses. 1992 Oct;8(10):1795–1801. doi: 10.1089/aid.1992.8.1795. [DOI] [PubMed] [Google Scholar]
  5. Bukrinsky M. I., Haggerty S., Dempsey M. P., Sharova N., Adzhubel A., Spitz L., Lewis P., Goldfarb D., Emerman M., Stevenson M. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature. 1993 Oct 14;365(6447):666–669. doi: 10.1038/365666a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chazal N., Carrière C., Gay B., Boulanger P. Phenotypic characterization of insertion mutants of the human immunodeficiency virus type 1 Gag precursor expressed in recombinant baculovirus-infected cells. J Virol. 1994 Jan;68(1):111–122. doi: 10.1128/jvi.68.1.111-122.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Copeland N. G., Jenkins N. A., Nexø B., Schultz A. M., Rein A., Mikkelsen T., Jørgensen P. Poorly expressed endogenous ecotropic provirus of DBA/2 mice encodes a mutant Pr65gag protein that is not myristylated. J Virol. 1988 Feb;62(2):479–487. doi: 10.1128/jvi.62.2.479-487.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cross F. R., Garber E. A., Pellman D., Hanafusa H. A short sequence in the p60src N terminus is required for p60src myristylation and membrane association and for cell transformation. Mol Cell Biol. 1984 Sep;4(9):1834–1842. doi: 10.1128/mcb.4.9.1834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Delchambre M., Gheysen D., Thines D., Thiriart C., Jacobs E., Verdin E., Horth M., Burny A., Bex F. The GAG precursor of simian immunodeficiency virus assembles into virus-like particles. EMBO J. 1989 Sep;8(9):2653–2660. doi: 10.1002/j.1460-2075.1989.tb08405.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Deminie C. A., Emerman M. Incorporation of human immunodeficiency virus type 1 Gag proteins into murine leukemia virus virions. J Virol. 1993 Nov;67(11):6499–6506. doi: 10.1128/jvi.67.11.6499-6506.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dorfman T., Mammano F., Haseltine W. A., Göttlinger H. G. Role of the matrix protein in the virion association of the human immunodeficiency virus type 1 envelope glycoprotein. J Virol. 1994 Mar;68(3):1689–1696. doi: 10.1128/jvi.68.3.1689-1696.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Edbauer C. A., Naso R. B. Cytoskeleton-associated Pr65gag and assembly of retrovirus temperature-sensitive mutants in chronically infected cells. Virology. 1984 Apr 30;134(2):389–397. doi: 10.1016/0042-6822(84)90306-4. [DOI] [PubMed] [Google Scholar]
  13. Freed E. O., Martin M. A. Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type 1 envelope glycoprotein gp120. J Virol. 1994 Apr;68(4):2503–2512. doi: 10.1128/jvi.68.4.2503-2512.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Freed E. O., Martin M. A. HIV-1 infection of non-dividing cells. Nature. 1994 May 12;369(6476):107–108. doi: 10.1038/369107b0. [DOI] [PubMed] [Google Scholar]
  15. Freed E. O., Risser R. The role of envelope glycoprotein processing in murine leukemia virus infection. J Virol. 1987 Sep;61(9):2852–2856. doi: 10.1128/jvi.61.9.2852-2856.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fricks C. E., Hogle J. M. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol. 1990 May;64(5):1934–1945. doi: 10.1128/jvi.64.5.1934-1945.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fäcke M., Janetzko A., Shoeman R. L., Kräusslich H. G. 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. 1993 Aug;67(8):4972–4980. doi: 10.1128/jvi.67.8.4972-4980.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gebhardt A., Bosch J. V., Ziemiecki A., Friis R. R. Rous sarcoma virus p19 and gp35 can be chemically crosslinked to high molecular weight complexes. An insight into virus assembly. J Mol Biol. 1984 Apr 5;174(2):297–317. doi: 10.1016/0022-2836(84)90340-1. [DOI] [PubMed] [Google Scholar]
  19. Gelderblom H. R. Assembly and morphology of HIV: potential effect of structure on viral function. AIDS. 1991 Jun;5(6):617–637. [PubMed] [Google Scholar]
  20. Gelderblom H. R., Ozel M., Pauli G. Morphogenesis and morphology of HIV. Structure-function relations. Arch Virol. 1989;106(1-2):1–13. doi: 10.1007/BF01311033. [DOI] [PubMed] [Google Scholar]
  21. Gheysen D., Jacobs E., de Foresta F., Thiriart C., Francotte M., Thines D., De Wilde M. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell. 1989 Oct 6;59(1):103–112. doi: 10.1016/0092-8674(89)90873-8. [DOI] [PubMed] [Google Scholar]
  22. Göttlinger H. G., Dorfman T., Sodroski J. G., Haseltine W. A. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3195–3199. doi: 10.1073/pnas.88.8.3195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Göttlinger H. G., Sodroski J. G., 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. 1989 Aug;86(15):5781–5785. doi: 10.1073/pnas.86.15.5781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Haffar O., Garrigues J., Travis B., Moran P., Zarling J., Hu S. L. Human immunodeficiency virus-like, nonreplicating, gag-env particles assemble in a recombinant vaccinia virus expression system. J Virol. 1990 Jun;64(6):2653–2659. doi: 10.1128/jvi.64.6.2653-2659.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hansen M., Jelinek L., Whiting S., Barklis E. Transport and assembly of gag proteins into Moloney murine leukemia virus. J Virol. 1990 Nov;64(11):5306–5316. doi: 10.1128/jvi.64.11.5306-5316.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hu S. L., Travis B. M., Garrigues J., Zarling J. M., Sridhar P., Dykers T., Eichberg J. W., Alpers C. Processing, assembly, and immunogenicity of human immunodeficiency virus core antigens expressed by recombinant vaccinia virus. Virology. 1990 Nov;179(1):321–329. doi: 10.1016/0042-6822(90)90300-g. [DOI] [PubMed] [Google Scholar]
  27. Jones T. A., Blaug G., Hansen M., Barklis E. Assembly of gag-beta-galactosidase proteins into retrovirus particles. J Virol. 1990 May;64(5):2265–2279. doi: 10.1128/jvi.64.5.2265-2279.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Jowett J. B., Hockley D. J., Nermut M. V., Jones I. M. Distinct signals in human immunodeficiency virus type 1 Pr55 necessary for RNA binding and particle formation. J Gen Virol. 1992 Dec;73(Pt 12):3079–3086. doi: 10.1099/0022-1317-73-12-3079. [DOI] [PubMed] [Google Scholar]
  29. Jørgensen E. C., Kjeldgaard N. O., Pedersen F. S., Jørgensen P. A nucleotide substitution in the gag N terminus of the endogenous ecotropic DBA/2 virus prevents Pr65gag myristylation and virus replication. J Virol. 1988 Sep;62(9):3217–3223. doi: 10.1128/jvi.62.9.3217-3223.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jørgensen E. C., Pedersen F. S., Jørgensen P. Matrix protein of Akv murine leukemia virus: genetic mapping of regions essential for particle formation. J Virol. 1992 Jul;66(7):4479–4487. doi: 10.1128/jvi.66.7.4479-4487.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kaplan A. H., Swanstrom R. Human immunodeficiency virus type 1 Gag proteins are processed in two cellular compartments. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4528–4532. doi: 10.1073/pnas.88.10.4528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Karacostas V., Nagashima K., Gonda M. A., Moss B. Human immunodeficiency virus-like particles produced by a vaccinia virus expression vector. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8964–8967. doi: 10.1073/pnas.86.22.8964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  34. Leis J., Baltimore D., Bishop J. M., Coffin J., Fleissner E., Goff S. P., Oroszlan S., Robinson H., Skalka A. M., Temin H. M. Standardized and simplified nomenclature for proteins common to all retroviruses. J Virol. 1988 May;62(5):1808–1809. doi: 10.1128/jvi.62.5.1808-1809.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Luo L., Li Y., Kang C. Y. Expression of gag precursor protein and secretion of virus-like gag particles of HIV-2 from recombinant baculovirus-infected insect cells. Virology. 1990 Dec;179(2):874–880. doi: 10.1016/0042-6822(90)90159-o. [DOI] [PubMed] [Google Scholar]
  36. Madisen L., Travis B., Hu S. L., Purchio A. F. Expression of the human immunodeficiency virus gag gene in insect cells. Virology. 1987 May;158(1):248–250. doi: 10.1016/0042-6822(87)90262-5. [DOI] [PubMed] [Google Scholar]
  37. Mergener K., Fäcke M., Welker R., Brinkmann V., Gelderblom H. R., Kräusslich H. G. Analysis of HIV particle formation using transient expression of subviral constructs in mammalian cells. Virology. 1992 Jan;186(1):25–39. doi: 10.1016/0042-6822(92)90058-w. [DOI] [PubMed] [Google Scholar]
  38. Montelaro R. C., Sullivan S. J., Bolognesi D. P. An analysis of type-C retrovirus polypeptides and their associations in the virion. Virology. 1978 Jan;84(1):19–31. doi: 10.1016/0042-6822(78)90215-5. [DOI] [PubMed] [Google Scholar]
  39. Orenstein J. M., Meltzer M. S., Phipps T., Gendelman H. E. Cytoplasmic assembly and accumulation of human immunodeficiency virus types 1 and 2 in recombinant human colony-stimulating factor-1-treated human monocytes: an ultrastructural study. J Virol. 1988 Aug;62(8):2578–2586. doi: 10.1128/jvi.62.8.2578-2586.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Pal R., Reitz M. S., Jr, Tschachler E., Gallo R. C., Sarngadharan M. G., Veronese F. D. Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly. AIDS Res Hum Retroviruses. 1990 Jun;6(6):721–730. doi: 10.1089/aid.1990.6.721. [DOI] [PubMed] [Google Scholar]
  41. Park J., Morrow C. D. Overexpression of the gag-pol precursor from human immunodeficiency virus type 1 proviral genomes results in efficient proteolytic processing in the absence of virion production. J Virol. 1991 Sep;65(9):5111–5117. doi: 10.1128/jvi.65.9.5111-5117.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pellman D., Garber E. A., Cross F. R., Hanafusa H. An N-terminal peptide from p60src can direct myristylation and plasma membrane localization when fused to heterologous proteins. 1985 Mar 28-Apr 3Nature. 314(6009):374–377. doi: 10.1038/314374a0. [DOI] [PubMed] [Google Scholar]
  43. Pellman D., Garber E. A., Cross F. R., Hanafusa H. Fine structural mapping of a critical NH2-terminal region of p60src. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1623–1627. doi: 10.1073/pnas.82.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Pepinsky R. B., Cappiello D., Wilkowski C., Vogt V. M. Chemical crosslinking of proteins in avian sarcoma and leukemia viruses. Virology. 1980 Apr 15;102(1):205–210. doi: 10.1016/0042-6822(80)90081-1. [DOI] [PubMed] [Google Scholar]
  45. Pepinsky R. B., Vogt V. M. Fine-structure analyses of lipid-protein and protein-protein interactions of gag protein p19 of the avian sarcoma and leukemia viruses by cyanogen bromide mapping. J Virol. 1984 Oct;52(1):145–153. doi: 10.1128/jvi.52.1.145-153.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Resh M. D., Ling H. P. Identification of a 32K plasma membrane protein that binds to the myristylated amino-terminal sequence of p60v-src. Nature. 1990 Jul 5;346(6279):84–86. doi: 10.1038/346084a0. [DOI] [PubMed] [Google Scholar]
  47. Rhee S. S., Hunter E. A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell. 1990 Oct 5;63(1):77–86. doi: 10.1016/0092-8674(90)90289-q. [DOI] [PubMed] [Google Scholar]
  48. Rhee S. S., Hunter E. Amino acid substitutions within the matrix protein of type D retroviruses affect assembly, transport and membrane association of a capsid. EMBO J. 1991 Mar;10(3):535–546. doi: 10.1002/j.1460-2075.1991.tb07980.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Rhee S. S., Hunter E. Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. J Virol. 1987 Apr;61(4):1045–1053. doi: 10.1128/jvi.61.4.1045-1053.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ross E. K., Buckler-White A. J., Rabson A. B., Englund G., Martin M. A. Contribution of NF-kappa B and Sp1 binding motifs to the replicative capacity of human immunodeficiency virus type 1: distinct patterns of viral growth are determined by T-cell types. J Virol. 1991 Aug;65(8):4350–4358. doi: 10.1128/jvi.65.8.4350-4358.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Ross E. K., Fuerst T. R., Orenstein J. M., O'Neill T., Martin M. A., Venkatesan S. Maturation of human immunodeficiency virus particles assembled from the gag precursor protein requires in situ processing by gag-pol protease. AIDS Res Hum Retroviruses. 1991 May;7(5):475–483. doi: 10.1089/aid.1991.7.475. [DOI] [PubMed] [Google Scholar]
  52. Rothman J. E. Polypeptide chain binding proteins: catalysts of protein folding and related processes in cells. Cell. 1989 Nov 17;59(4):591–601. doi: 10.1016/0092-8674(89)90005-6. [DOI] [PubMed] [Google Scholar]
  53. Royer M., Hong S. S., Gay B., Cerutti M., Boulanger P. Expression and extracellular release of human immunodeficiency virus type 1 Gag precursors by recombinant baculovirus-infected cells. J Virol. 1992 May;66(5):3230–3235. doi: 10.1128/jvi.66.5.3230-3235.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schultz A. M., Henderson L. E., Oroszlan S. Fatty acylation of proteins. Annu Rev Cell Biol. 1988;4:611–647. doi: 10.1146/annurev.cb.04.110188.003143. [DOI] [PubMed] [Google Scholar]
  55. Schultz A. M., Rein A. Unmyristylated Moloney murine leukemia virus Pr65gag is excluded from virus assembly and maturation events. J Virol. 1989 May;63(5):2370–2373. doi: 10.1128/jvi.63.5.2370-2373.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Shioda T., Shibuta H. Production of human immunodeficiency virus (HIV)-like particles from cells infected with recombinant vaccinia viruses carrying the gag gene of HIV. Virology. 1990 Mar;175(1):139–148. doi: 10.1016/0042-6822(90)90194-v. [DOI] [PubMed] [Google Scholar]
  57. Smith A. J., Cho M. I., Hammarskjöld M. L., Rekosh D. Human immunodeficiency virus type 1 Pr55gag and Pr160gag-pol expressed from a simian virus 40 late replacement vector are efficiently processed and assembled into viruslike particles. J Virol. 1990 Jun;64(6):2743–2750. doi: 10.1128/jvi.64.6.2743-2750.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Sompayrac L. M., Danna K. J. Efficient infection of monkey cells with DNA of simian virus 40. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7575–7578. doi: 10.1073/pnas.78.12.7575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Towler D. A., Gordon J. I., Adams S. P., Glaser L. The biology and enzymology of eukaryotic protein acylation. Annu Rev Biochem. 1988;57:69–99. doi: 10.1146/annurev.bi.57.070188.000441. [DOI] [PubMed] [Google Scholar]
  60. Vernon S. K., Murthy S., Wilhelm J., Chanda P. K., Kalyan N., Lee S. G., Hung P. P. Ultrastructural characterization of human immunodeficiency virus type 1 Gag-containing particles assembled in a recombinant adenovirus vector system. J Gen Virol. 1991 Jun;72(Pt 6):1243–1251. doi: 10.1099/0022-1317-72-6-1243. [DOI] [PubMed] [Google Scholar]
  61. Wachinger G., Nitschko H., Wachinger M., von der Helm K. The p17 stretch at the N terminus of the HIV1-gag precursor and the intracellular part of HIV1-env gp41 have heptad repeat regions in their sequences that could bind to each other in a coiled coil. Protein Seq Data Anal. 1991 Dec;4(6):375–376. [PubMed] [Google Scholar]
  62. Wang C. T., Barklis E. Assembly, processing, and infectivity of human immunodeficiency virus type 1 gag mutants. J Virol. 1993 Jul;67(7):4264–4273. doi: 10.1128/jvi.67.7.4264-4273.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Wang C. T., Zhang Y., McDermott J., Barklis E. Conditional infectivity of a human immunodeficiency virus matrix domain deletion mutant. J Virol. 1993 Dec;67(12):7067–7076. doi: 10.1128/jvi.67.12.7067-7076.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Weaver T. A., Panganiban A. T. N myristoylation of the spleen necrosis virus matrix protein is required for correct association of the Gag polyprotein with intracellular membranes and for particle formation. J Virol. 1990 Aug;64(8):3995–4001. doi: 10.1128/jvi.64.8.3995-4001.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Willey R. L., Bonifacino J. S., Potts B. J., Martin M. A., Klausner R. D. Biosynthesis, cleavage, and degradation of the human immunodeficiency virus 1 envelope glycoprotein gp160. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9580–9584. doi: 10.1073/pnas.85.24.9580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Willey R. L., Martin M. A., Peden K. W. Increase in soluble CD4 binding to and CD4-induced dissociation of gp120 from virions correlates with infectivity of human immunodeficiency virus type 1. J Virol. 1994 Feb;68(2):1029–1039. doi: 10.1128/jvi.68.2.1029-1039.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Willey R. L., Smith D. H., Lasky L. A., Theodore T. S., Earl P. L., Moss B., Capon D. J., Martin M. A. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J Virol. 1988 Jan;62(1):139–147. doi: 10.1128/jvi.62.1.139-147.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wills J. W., Craven R. C., Achacoso J. A. Creation and expression of myristylated forms of Rous sarcoma virus gag protein in mammalian cells. J Virol. 1989 Oct;63(10):4331–4343. doi: 10.1128/jvi.63.10.4331-4343.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wills J. W., Craven R. C. Form, function, and use of retroviral gag proteins. AIDS. 1991 Jun;5(6):639–654. doi: 10.1097/00002030-199106000-00002. [DOI] [PubMed] [Google Scholar]
  70. Wills J. W., Craven R. C., Weldon R. A., Jr, Nelle T. D., Erdie C. R. Suppression of retroviral MA deletions by the amino-terminal membrane-binding domain of p60src. J Virol. 1991 Jul;65(7):3804–3812. doi: 10.1128/jvi.65.7.3804-3812.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Yu X., Yu Q. C., Lee T. H., Essex M. The C terminus of human immunodeficiency virus type 1 matrix protein is involved in early steps of the virus life cycle. J Virol. 1992 Sep;66(9):5667–5670. doi: 10.1128/jvi.66.9.5667-5670.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Yu X., Yuan X., Matsuda Z., Lee T. H., Essex M. The matrix protein of human immunodeficiency virus type 1 is required for incorporation of viral envelope protein into mature virions. J Virol. 1992 Aug;66(8):4966–4971. doi: 10.1128/jvi.66.8.4966-4971.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Yuan X., Yu X., Lee T. H., Essex M. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor. J Virol. 1993 Nov;67(11):6387–6394. doi: 10.1128/jvi.67.11.6387-6394.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zhou W., Parent L. J., Wills J. W., Resh M. D. 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. 1994 Apr;68(4):2556–2569. doi: 10.1128/jvi.68.4.2556-2569.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES