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PMID: 2550669 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Creation and expression of myristylated forms of Rous sarcoma virus gag protein in mammalian cells.

Journal of virology ·Vol. 63 ·No. 10 ·1989-10-00 ·Pages 4331-43

Wills JW, Craven RC, Achacoso JA

Abstract

Rous sarcoma virus (RSV), a member of the avian sarcoma and leukosis family of retroviruses, has long been known to be capable of infecting and transforming mammalian cells; however, such transformed cells do not release virus particles. The RSV gag product (Pr76gag) produced in these cells is not released into the culture medium or proteolytically processed to release mature products. Thus, the behavior of Pr76gag in mammalian cells is much like that of mammalian retroviral Gag proteins which have been altered so as to block the addition of myristic acid at residue 2 (Gly). Because the RSV gag product does not possess a myristic acid addition site, we hypothesized that the creation of one by oligonucleotide-directed mutagenesis might permit particles to be released from mammalian cells. Two myristylated forms of Pr76 were created. In Pr76myr1, the first 10 amino acids have been exchanged for those of p60v-src, which are known to be sufficient for myristylation. In Pr76myr2, the Glu at the second residue has been substituted with Gly. The alleles encoding the modified and wild-type forms of Pr76 have been expressed at high levels in mammalian (CV-1) cells by using an SV40-based vector. Surprisingly, we have found that expression of high levels of the unmodified (wild-type) product, Pr76myr0, results in low levels of particle formation and precursor processing. This indicates that myristic acid is not the sole determinant for targeting. However, the addition of myristic acid to Pr76myr1 or Pr76myr2 resulted in a fivefold enhancement in Gag function. In all aspects examined, the behavior of myristylated Pr76 was identical to that of the authentic product produced in avian cells. We also show that processing is mediated by the gag-encoded protease and that removal of the amino terminus to create Pr76gagX results in an inability to form particles or be processed. This suggests that proper targeting is prerequisite for activation of the RSV protease in mammalian cells.

MeSH Terms
Animals Avian Sarcoma Viruses/metabolism Cell Line Enzyme Activation Gene Products, gag Genetic Vectors Mutation Myristic Acid Myristic Acids/metabolism Peptide Hydrolases/physiology Retroviridae Proteins/genetics,metabolism Transfection
Chemicals
Gene Products, gag Myristic Acids Retroviridae Proteins Myristic Acid Peptide Hydrolases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Wills J W
Department of Biochemistry and Molecular Biology, Louisiana State University Medical Center-Shreveport 71130-3932.
Craven R C
Achacoso J A
References (47)
47 references, click to expand
  1. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  2. Molecular modeling of the HIV-1 protease and its substrate binding site.
    Science. 1989 Feb 17;243(4893):928-31 PMID: 2537531
  3. The NH2-terminal sequence of the avian oncovirus gag precursor polyprotein (Pr76gag).
    Virology. 1978 Dec;91(2):423-33 PMID: 217156
  4. Biological techniques for avian sarcoma viruses.
    Methods Enzymol. 1979;58:379-93 PMID: 218076
  5. Transformation of NIH/3T3 mouse cells by DNA of Rous sarcoma virus.
    Cell. 1979 Aug;17(4):993-1002 PMID: 226269
  6. Identification of retrovirus matrix proteins by lipid-protein cross-linking.
    J Mol Biol. 1979 Jul 15;131(4):819-37 PMID: 229234
  7. Chemical crosslinking of proteins in avian sarcoma and leukemia viruses.
    Virology. 1980 Apr 15;102(1):205-10 PMID: 6245502
  8. Alignment of the peptides derived from acid-catalyzed cleavage of an aspartylprolyl bond in the major internal structural polypeptide of avian retroviruses.
    J Biol Chem. 1980 Jul 25;255(14):6962-5 PMID: 6248540
  9. Rous sarcoma virus precursor protein pr 76 is processed in avian sarcoma virus-transformed mammalian cells after fusion-injection of viral protein p 15.
    Virology. 1980 Oct 30;106(2):310-6 PMID: 6254253
  10. SV40-transformed simian cells support the replication of early SV40 mutants.
    Cell. 1981 Jan;23(1):175-82 PMID: 6260373
  11. Structure of viral DNA and RNA in mammalian cells infected with avian sarcoma virus.
    J Mol Biol. 1980 Nov 15;143(4):363-93 PMID: 6262515
  12. Restriction endonuclease and nucleotide sequence analyses of molecularly cloned unintegrated avian tumor virus DNA: structure of large terminal repeats in circle junctions.
    J Virol. 1982 Apr;42(1):346-51 PMID: 6283156
  13. Avian sarcoma virus gag precursor polypeptide is not processed in mammalian cells.
    J Virol. 1982 Nov;44(2):725-30 PMID: 6183452
  14. Cytoskeleton-associated Pr65gag and assembly of retrovirus temperature-sensitive mutants in chronically infected cells.
    Virology. 1984 Apr 30;134(2):389-97 PMID: 6336230
  15. Synthesis of avian RNA tumor virus structural proteins.
    Cold Spring Harb Symp Quant Biol. 1975;39 Pt 2:1067-75 PMID: 169008
  16. Generation of avian myeloblastosis virus structural proteins by proteolytic cleavage of a precursor polypeptide.
    J Mol Biol. 1975 Aug 15;96(3):471-93 PMID: 170408
  17. Complementation rescue of Rous sarcoma virus from transformed mammalian cells by polyethylene glycol-mediated cell fusion.
    J Virol. 1977 Jul;23(1):133-41 PMID: 196098
  18. High efficiency polyoma DNA transfection of chloroquine treated cells.
    Nucleic Acids Res. 1983 Mar 11;11(5):1295-308 PMID: 6298741
  19. Nucleotide sequence of Rous sarcoma virus.
    Cell. 1983 Mar;32(3):853-69 PMID: 6299578
  20. Myristyl amino-terminal acylation of murine retrovirus proteins: an unusual post-translational proteins modification.
    Proc Natl Acad Sci U S A. 1983 Jan;80(2):339-43 PMID: 6340098
  21. In vivo modification of retroviral gag gene-encoded polyproteins by myristic acid.
    J Virol. 1983 May;46(2):355-61 PMID: 6302307
  22. Alterations in the transport and processing of Rous sarcoma virus envelope glycoproteins mutated in the signal and anchor regions.
    J Cell Biochem. 1983;23(1-4):81-94 PMID: 6327741
  23. 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):145-53 PMID: 6090691
  24. Mutations of the Rous sarcoma virus env gene that affect the transport and subcellular location of the glycoprotein products.
    J Cell Biol. 1984 Dec;99(6):2011-23 PMID: 6094591
  25. Purification and chemical and immunological characterization of avian reticuloendotheliosis virus gag-gene-encoded structural proteins.
    Virology. 1985 Jan 30;140(2):289-312 PMID: 2982236
  26. An N-terminal peptide from p60src can direct myristylation and plasma membrane localization when fused to heterologous proteins.
    Nature. 1985 Mar 28-Apr 3;314(6009):374-7 PMID: 3920530
  27. Truncated gag-related proteins are produced by large deletion mutants of Rous sarcoma virus and form virus particles.
    J Virol. 1985 Jul;55(1):79-85 PMID: 2989562
  28. 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
  29. Primary structure of p19 species of avian sarcoma and leukemia viruses.
    J Virol. 1985 Oct;56(1):31-9 PMID: 2993659
  30. Fatty acylation of cellular proteins. Temporal and subcellular differences between palmitate and myristate acylation.
    J Biol Chem. 1986 Feb 15;261(5):2458-66 PMID: 3944142
  31. Amino-terminal deletion mutants of the Rous sarcoma virus glycoprotein do not block signal peptide cleavage but can block intracellular transport.
    J Cell Biol. 1986 Sep;103(3):829-38 PMID: 3017996
  32. Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus.
    Proc Natl Acad Sci U S A. 1986 Oct;83(19):7246-50 PMID: 3489936
  33. 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
  34. Expression of the Rous sarcoma virus env gene from a simian virus 40 late-region replacement vector: effects of upstream initiation codons.
    J Virol. 1987 Apr;61(4):1276-81 PMID: 3029425
  35. The covalent modification of eukaryotic proteins with lipid.
    J Cell Biol. 1987 Jun;104(6):1449-53 PMID: 3294853
  36. Efficient transformation by Prague A Rous sarcoma virus plasmid DNA requires the presence of cis-acting regions within the gag gene.
    J Virol. 1987 Nov;61(11):3401-9 PMID: 2822950
  37. Acylation of proteins with myristic acid occurs cotranslationally.
    Science. 1987 Nov 27;238(4831):1275-8 PMID: 3685978
  38. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Methods Enzymol. 1987;154:367-82 PMID: 3323813
  39. Standardized and simplified nomenclature for proteins common to all retroviruses.
    J Virol. 1988 May;62(5):1808-9 PMID: 3357211
  40. Activity of avian retroviral protease expressed in Escherichia coli.
    J Virol. 1988 Aug;62(8):2696-700 PMID: 2839695
  41. 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):3217-23 PMID: 2841473
  42. The biology and enzymology of eukaryotic protein acylation.
    Annu Rev Biochem. 1988;57:69-99 PMID: 3052287
  43. Viral proteinases.
    Annu Rev Biochem. 1988;57:701-54 PMID: 3052288
  44. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region.
    Cell. 1988 Nov 4;55(3):447-58 PMID: 2846182
  45. Fatty acylation of proteins.
    Annu Rev Cell Biol. 1988;4:611-47 PMID: 3058168
  46. Crystal structure of a retroviral protease proves relationship to aspartic protease family.
    Nature. 1989 Feb 9;337(6207):576-9 PMID: 2536902
  47. Mutants of SV40 with an altered small t protein are reduced in their ability to transform cells.
    Cell. 1978 May;14(1):79-88 PMID: 208777
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1989-10-00
Pages
4331-43
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC251050
Subset
IM
Grants
NCI NIH HHS · CA-47482 · United States
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