Abstract
We have analyzed the roles of Gag protein nucleocapsid (NC) domains in the packaging or encapsidation of retroviral RNAs into virus particles. We found that mutation of both zinc finger motifs of the human immunodeficiency virus (HIV) NC domain reduced but did not eliminate encapsidation of the HIV viral RNA. However, the NC mutations also resulted in a three- to fourfold reduction in the specificity of RNA encapsidation, as determined by comparison of virus-associated genomic and spliced RNA levels. As a complementary approach, we replaced the NC domain of Moloney murine leukemia virus (M-MuLV) with that of HIV. Chimeric virus particles assembled efficiently, were of wild-type M-MuLV density, and cross-linked at NC cysteines. In encapsidation studies, wild-type M-MuLV precursor Gag (PrGag) proteins packaged M-MuLV transcripts more efficiently than HIV RNAs. In contrast, chimeric PrGag proteins possessing the HIV-1 NC domain in the context of the M-MuLV MA (matrix), p12, and CA (capsid) domains encapsidated HIV transcripts to a greater extent than M-MuLV transcripts. Our results support the notion that retroviral NC domains contribute toward both the efficiency and specificity of viral genomic RNA packaging.
MeSH Terms
Animals
Base Sequence
Capsid/isolation & purification,metabolism
Cell Line
Chlorocebus aethiops
Gene Products, gag/metabolism
HIV/metabolism
HIV-1/metabolism
Humans
Kidney
Kinetics
Molecular Sequence Data
Moloney murine leukemia virus/metabolism
Mutagenesis, Site-Directed
Oligodeoxyribonucleotides
Plasmids
RNA, Viral/isolation & purification,metabolism
Recombinant Proteins/metabolism
Restriction Mapping
Retroviridae/metabolism
Species Specificity
Substrate Specificity
Transcription, Genetic
Transfection
Viral Core Proteins/isolation & purification,metabolism
Zinc Fingers
Chemicals
Gene Products, gag
Oligodeoxyribonucleotides
RNA, Viral
Recombinant Proteins
Viral Core Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Zhang Y
Vollum Institute for Advanced Biomedical Research, Oregon Health Sciences University, Portland 97201-3098, USA.
Barklis E
References (27)
27 references, click to expand
-
Structural interactions between retroviral Gag proteins examined by cysteine cross-linking.
J Virol. 1995 Feb;69(2):1150-9
PMID: 7815493
-
Point mutants of Moloney murine leukemia virus that fail to package viral RNA: evidence for specific RNA recognition by a "zinc finger-like" protein sequence.
Proc Natl Acad Sci U S A. 1988 Nov;85(22):8420-4
PMID: 3141927
-
Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
Nature. 1970 Aug 15;227(5259):680-5
PMID: 5432063
-
A new technique for the assay of infectivity of human adenovirus 5 DNA.
Virology. 1973 Apr;52(2):456-67
PMID: 4705382
-
An avian oncovirus mutant (SE 21Q1b) deficient in genomic RNA: biological and biochemical characterization.
Cell. 1978 Dec;15(4):1371-81
PMID: 83199
-
Avian oncovirus mutant (SE21Q1b) deficient in genomic RNA: characterization of a deletion in the provirus.
J Virol. 1980 Nov;36(2):450-6
PMID: 6253670
-
Characterization of a Rous sarcoma virus mutant defective in packaging its own genomic RNA: biochemical properties of mutant TK15 and mutant-induced transformants.
J Virol. 1984 Jul;51(1):154-62
PMID: 6202881
-
Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus.
Cell. 1983 May;33(1):153-9
PMID: 6678608
-
The trans-activator gene of HTLV-III is essential for virus replication.
Nature. 1986 Mar 27-Apr 2;320(6060):367-71
PMID: 3007995
-
A conserved cis-acting sequence in the 5' leader of avian sarcoma virus RNA is required for packaging.
J Virol. 1986 Jul;59(1):163-7
PMID: 3012114
-
Human IL-3 (multi-CSF): identification by expression cloning of a novel hematopoietic growth factor related to murine IL-3.
Cell. 1986 Oct 10;47(1):3-10
PMID: 3489530
-
Chromosomal position or virus mutation permits retrovirus expression in embryonal carcinoma cells.
Cell. 1986 Nov 7;47(3):391-9
PMID: 3768959
-
Small finger protein of avian and murine retroviruses has nucleic acid annealing activity and positions the replication primer tRNA onto genomic RNA.
EMBO J. 1988 Jun;7(6):1777-83
PMID: 2458920
-
Efficient particle formation can occur if the matrix domain of human immunodeficiency virus type 1 Gag is substituted by a myristylation signal.
J Virol. 1994 Oct;68(10):6644-54
PMID: 7521919
-
Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions.
J Virol. 1989 Sep;63(9):4085-7
PMID: 2760989
-
Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus.
J Virol. 1990 May;64(5):1920-6
PMID: 2109098
-
Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA.
J Virol. 1990 Jul;64(7):3207-11
PMID: 2191147
-
Construction and use of a human immunodeficiency virus vector for analysis of virus infectivity.
J Virol. 1990 Nov;64(11):5270-6
PMID: 2214018
-
Specificity of Rous sarcoma virus nucleocapsid protein in genomic RNA packaging.
J Virol. 1992 Aug;66(8):4662-70
PMID: 1378506
-
Retrovirus-mediated insertion of expressed and non-expressed genes at identical chromosomal locations.
Nucleic Acids Res. 1993 May 25;21(10):2399-407
PMID: 8506135
-
Identification of a binding site for the human immunodeficiency virus type 1 nucleocapsid protein.
Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5219-23
PMID: 8506369
-
Assembly, processing, and infectivity of human immunodeficiency virus type 1 gag mutants.
J Virol. 1993 Jul;67(7):4264-73
PMID: 7685414
-
Functional chimeras of the Rous sarcoma virus and human immunodeficiency virus gag proteins.
J Virol. 1993 Nov;67(11):6487-98
PMID: 8411352
-
Conditional infectivity of a human immunodeficiency virus matrix domain deletion mutant.
J Virol. 1993 Dec;67(12):7067-76
PMID: 7693966
-
Specific binding of human immunodeficiency virus type 1 gag polyprotein and nucleocapsid protein to viral RNAs detected by RNA mobility shift assays.
J Virol. 1993 Dec;67(12):7190-200
PMID: 8230441
-
Assembly of HIV GAG-B-galactosidase fusion proteins into virus particles.
Virology. 1994 May 1;200(2):524-34
PMID: 8178440
-
Efficiency and selectivity of RNA packaging by Rous sarcoma virus Gag deletion mutants.
J Virol. 1994 Sep;68(9):5969-81
PMID: 8057473