Production of Avian Leukosis Virus Particles in Mammalian Cells Can Be Mediated by the Interaction of the Human Immunodeficiency Virus Protein Rev and the Rev-responsive Element

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1995 Dec 5

PMID 8524879

Citations 20

Authors

G Nasioulas

S H Hughes

B K Felber

J M Whitcomb

Affiliations

Soon will be listed here.

Abstract

In human immunodeficiency virus type 1-infected cells, the efficient expression of viral proteins from unspliced and singly spliced RNAs is dependent on two factors: the presence in the cell of the viral protein Rev and the presence in the viral RNA of the Rev-responsive element (RRE). We show here that the HIV-1 Rev/RRE system can increase the expression of avian leukosis virus (ALV) structural proteins in mammalian cells (D-17 canine osteosarcoma) and promote the release of mature ALV virions from these cells. In this system, the Rev/RRE interaction appears to facilitate the export of full-length unspliced ALV RNA from the nucleus to the cytoplasm, allowing increased production of the ALV structural proteins. Gag protein is produced in the cytoplasm of the ALV-transfected cells even in the absence of a Rev/RRE interaction. However, a functional Rev/RRE interaction increases the amount of Gag present intracellularly and, more strikingly, results in the release of mature ALV particles into the supernatant. RCAS virus containing an RRE is replication-competent in chicken embryo fibroblasts; however, we have been unable to determine whether the particles produced in D-17 cells are as infectious as the particles produced in chicken embryo fibroblasts.

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References

Feinberg M, Jarrett R, Aldovini A, Gallo R, Wong-Staal F . HTLV-III expression and production involve complex regulation at the levels of splicing and translation of viral RNA. Cell. 1986; 46(6):807-17. DOI: 10.1016/0092-8674(86)90062-0. View

Schultz A, Oroszlan S . In vivo modification of retroviral gag gene-encoded polyproteins by myristic acid. J Virol. 1983; 46(2):355-61. PMC: 255136. DOI: 10.1128/JVI.46.2.355-361.1983. View

DE Wet J, Wood K, DeLuca M, Helinski D, Subramani S . Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987; 7(2):725-37. PMC: 365129. DOI: 10.1128/mcb.7.2.725-737.1987. View

Arrigo S, Yun M, Beemon K . cis-acting regulatory elements within gag genes of avian retroviruses. Mol Cell Biol. 1987; 7(1):388-97. PMC: 365080. DOI: 10.1128/mcb.7.1.388-397.1987. View

Stoltzfus C, Chang L, Cripe T, Turek L . Efficient transformation by Prague A Rous sarcoma virus plasmid DNA requires the presence of cis-acting regions within the gag gene. J Virol. 1987; 61(11):3401-9. PMC: 255935. DOI: 10.1128/JVI.61.11.3401-3409.1987. View

Malim M, HAUBER J, Le S, Maizel J, Cullen B . The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature. 1989; 338(6212):254-7. DOI: 10.1038/338254a0. View

Felber B, Cladaras C, Copeland T, Pavlakis G . rev protein of human immunodeficiency virus type 1 affects the stability and transport of the viral mRNA. Proc Natl Acad Sci U S A. 1989; 86(5):1495-9. PMC: 286723. DOI: 10.1073/pnas.86.5.1495. View

Stoltzfus C . Synthesis and processing of avian sarcoma retrovirus RNA. Adv Virus Res. 1988; 35:1-38. DOI: 10.1016/s0065-3527(08)60707-1. View

Hammarskjold M, Heimer J, Hammarskjold B, Sangwan I, Albert L, Rekosh D . Regulation of human immunodeficiency virus env expression by the rev gene product. J Virol. 1989; 63(5):1959-66. PMC: 250609. DOI: 10.1128/JVI.63.5.1959-1966.1989. View

10.

Emerman M, Vazeux R, Peden K . The rev gene product of the human immunodeficiency virus affects envelope-specific RNA localization. Cell. 1989; 57(7):1155-65. DOI: 10.1016/0092-8674(89)90053-6. View

11.

Wills J, Craven R, Achacoso J . Creation and expression of myristylated forms of Rous sarcoma virus gag protein in mammalian cells. J Virol. 1989; 63(10):4331-43. PMC: 251050. DOI: 10.1128/JVI.63.10.4331-4343.1989. View

12.

Chang D, Sharp P . Regulation by HIV Rev depends upon recognition of splice sites. Cell. 1989; 59(5):789-95. DOI: 10.1016/0092-8674(89)90602-8. View

13.

Heaphy S, Dingwall C, Ernberg I, Gait M, Green S, Karn J . HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell. 1990; 60(4):685-93. DOI: 10.1016/0092-8674(90)90671-z. View

14.

Mermer B, Felber B, Campbell M, Pavlakis G . Identification of trans-dominant HIV-1 rev protein mutants by direct transfer of bacterially produced proteins into human cells. Nucleic Acids Res. 1990; 18(8):2037-44. PMC: 330680. DOI: 10.1093/nar/18.8.2037. View

15.

Greene W . Regulation of HIV-1 gene expression. Annu Rev Immunol. 1990; 8:453-75. DOI: 10.1146/annurev.iy.08.040190.002321. View

16.

Viglianti G, Sharma P, Mullins J . Simian immunodeficiency virus displays complex patterns of RNA splicing. J Virol. 1990; 64(9):4207-16. PMC: 247885. DOI: 10.1128/JVI.64.9.4207-4216.1990. View

17.

Berberich S, Macias M, Zhang L, Turek L, Stoltzfus C . Comparison of Rous sarcoma virus RNA processing in chicken and mouse fibroblasts: evidence for double-spliced RNA in nonpermissive mouse cells. J Virol. 1990; 64(9):4313-20. PMC: 247898. DOI: 10.1128/JVI.64.9.4313-4320.1990. View

18.

Hughes S, Petropoulos C, Federspiel M, Sutrave P, Bradac J . Vectors and genes for improvement of animal strains. J Reprod Fertil Suppl. 1990; 41:39-49. View

19.

Schwartz S, Felber B, Fenyo E, Pavlakis G . Env and Vpu proteins of human immunodeficiency virus type 1 are produced from multiple bicistronic mRNAs. J Virol. 1990; 64(11):5448-56. PMC: 248596. DOI: 10.1128/JVI.64.11.5448-5456.1990. View

20.

Lu X, Heimer J, Rekosh D, Hammarskjold M . U1 small nuclear RNA plays a direct role in the formation of a rev-regulated human immunodeficiency virus env mRNA that remains unspliced. Proc Natl Acad Sci U S A. 1990; 87(19):7598-602. PMC: 54795. DOI: 10.1073/pnas.87.19.7598. View