Abstract
Mason-Pfizer monkey virus (M-PMV) is the prototype type D retrovirus which preassembles immature intracytoplasmic type A particles within the infected cell cytoplasm. Intracytoplasmic type A particles are composed of uncleaved polyprotein precursors which upon release are cleaved by the viral proteinase to their constituent mature proteins. This results in a morphological change in the virion described as maturation. We have investigated the role of the viral proteinase in virus maturation and infectivity by inhibiting the function of the enzyme through mutagenesis of the proteinase gene and by using peptide inhibitors originally designed to block human immunodeficiency virus type 1 proteinase activity. Mutation of the active-site aspartic acid, Asp-26, to asparagine abrogated the activity of the M-PMV proteinase but did not affect the assembly of noninfectious, immature virus particles. In mutant virions, the transmembrane glycoprotein (TM) of M-PMV, initially synthesized as a cell-associated gp22, is not cleaved to gp20, as is observed with wild-type virions. This demonstrates that the viral proteinase is responsible for this cleavage event. Hydroxyethylene isostere human immunodeficiency virus type 1 proteinase inhibitors were shown to block M-PMV proteinase cleavage of the TM glycoprotein and Gag-containing precursors in a dose-dependent manner. The TM cleavage event was more sensitive than cleavage of the Gag precursors to inhibition. The infectivity of treated particles was reduced significantly, but experiments showed that inhibition of precursor and TM cleavage may be at least partially reversible. These results demonstrate that the M-PMV aspartyl proteinase is activated in released virions and that the hydroxyethylene isostere proteinase inhibitors used in this study exhibit a broad spectrum of antiretroviral activity.
MeSH Terms
Animals
Cell Line
Endopeptidases/metabolism
Humans
Kinetics
Mason-Pfizer monkey virus/drug effects,growth & development,metabolism,ultrastructure
Membrane Glycoproteins/metabolism
Microscopy, Electron
Mutagenesis, Site-Directed
Precipitin Tests
Protease Inhibitors/pharmacology
Tumor Cells, Cultured
Viral Matrix Proteins/metabolism
Virus Replication
Chemicals
Membrane Glycoproteins
Protease Inhibitors
Viral Matrix Proteins
Endopeptidases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sommerfelt M A
Department of Microbiology, University of Alabama, Birmingham 35294.
Petteway S R
Dreyer G B
Hunter E
References (24)
24 references, click to expand
-
Rapid and efficient site-specific mutagenesis without phenotypic selection.
Proc Natl Acad Sci U S A. 1985 Jan;82(2):488-92
PMID: 3881765
-
Polypeptides of Mason-Pfizer monkey virus. I. Synthesis and processing of the gag-gene products.
Virology. 1984 Oct 30;138(2):260-75
PMID: 6333757
-
Inhibition of HIV-1 protease in infected T-lymphocytes by synthetic peptide analogues.
Nature. 1990 Jan 4;343(6253):90-2
PMID: 1688646
-
A synthetic HIV-1 protease inhibitor with antiviral activity arrests HIV-like particle maturation.
Science. 1990 Jan 26;247(4941):454-6
PMID: 2405486
-
Properties of avian retrovirus particles defective in viral protease.
J Virol. 1990 Oct;64(10):5076-92
PMID: 1697912
-
A new virus in a spontaneous mammary tumor of a rhesus monkey.
Cancer Res. 1970 Aug;30(8):2081-6
PMID: 4195910
-
Responses of infant rhesus monkeys to inoculation with Mason-Pfizer monkey virus materials.
J Natl Cancer Inst. 1975 Mar;54(3):651-8
PMID: 804565
-
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 U S A. 1992 Apr 15;89(8):3443-7
PMID: 1565636
-
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):4528-32
PMID: 2034693
-
Human immunodeficiency virus type 1 protease inhibitors irreversibly block infectivity of purified virions from chronically infected cells.
Antimicrob Agents Chemother. 1992 May;36(5):982-8
PMID: 1510424
-
Role of human immunodeficiency virus type 1-specific protease in core protein maturation and viral infectivity.
J Virol. 1989 Jun;63(6):2550-6
PMID: 2657099
-
Processing of in vitro-synthesized gag precursor proteins of human immunodeficiency virus (HIV) type 1 by HIV proteinase generated in Escherichia coli.
J Virol. 1988 Nov;62(11):4393-7
PMID: 3050149
-
Active human immunodeficiency virus protease is required for viral infectivity.
Proc Natl Acad Sci U S A. 1988 Jul;85(13):4686-90
PMID: 3290901
-
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):5781-5
PMID: 2788277
-
The protease and gag gene products of the human immunodeficiency virus: authentic cleavage and post-translational modification in an insect cell expression system.
Virology. 1989 May;170(1):107-16
PMID: 2655272
-
Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids.
J Virol. 1987 Apr;61(4):1045-53
PMID: 3493352
-
High-efficiency transformation of mammalian cells by plasmid DNA.
Mol Cell Biol. 1987 Aug;7(8):2745-52
PMID: 3670292
-
Immunodeficiency in rhesus monkeys associated with the original Mason-Pfizer monkey virus.
J Natl Cancer Inst. 1986 Oct;77(4):957-65
PMID: 3020302
-
HIV-1 protease specificity of peptide cleavage is sufficient for processing of gag and pol polyproteins.
Biochem Biophys Res Commun. 1988 Oct 14;156(1):297-303
PMID: 3052448
-
Viral proteinases.
Annu Rev Biochem. 1988;57:701-54
PMID: 3052288
-
Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus.
Cell. 1986 May 9;45(3):375-85
PMID: 2421920
-
Murine leukemia virus maturation: protease region required for conversion from "immature" to "mature" core form and for virus infectivity.
Virology. 1985 Sep;145(2):280-92
PMID: 2411050
-
Inhibition of human immunodeficiency virus 1 protease in vitro: rational design of substrate analogue inhibitors.
Proc Natl Acad Sci U S A. 1989 Dec;86(24):9752-6
PMID: 2690072
-
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. 1985 Mar;53(3):899-907
PMID: 3882995