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PMID: 8627803 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors.

Journal of virology ·Vol. 70 ·No. 5 ·1996-05-00 ·Pages 3227-34

Ferrari FK, Samulski T, Shenk T, Samulski RJ

Abstract

The ability of recombinant adeno-associated virus (AAV) to transduce cells with a marker gene in vitro was found to be substantially increased by the presence of adenovirus. Transfection experiments with adenovirus genomic DNA suggest that this increase is not facilitated by adenovirus-mediated viral uptake but is instead dependent on adenovirus gene expression. Using various adenovirus mutants, we were able to map this function to early-region E4 open reading frame 6. Plasmid expression of open reading frame 6 protein in cells infected with recombinant AAV increased transduction between 100- and 1,000-fold. The increase in transduction was not dependent on the recombinant AAV gene cassette but instead appeared to involve an immediate early step of the AAV life cycle. Chemical and physical agents that have been shown to induce helper-free replication of wild-type AAV were also able to stimulate recombinant AAV transduction, suggesting that the phenomenon might affect AAV DNA replication. Further experiments showed that viral uncoating was not affected and that the rate-limiting step involved synthesis of a second strand on the single-stranded genomic AAV DNA. These data suggest that the adenovirus E4 region, as well as chemical and physical agents, can play an essential role in an immediate-early step of the AAV life cycle, specifically in second-strand synthesis, and have important implications for the use of AAV vectors in gene therapy protocols.

MeSH Terms
Adenoviridae/genetics Cell Line DNA, Viral/biosynthesis,isolation & purification Dependovirus/genetics,physiology Gene Expression Genetic Vectors HeLa Cells Humans Kinetics Mutagenesis Open Reading Frames Plasmids Recombinant Proteins/analysis,biosynthesis Recombination, Genetic Transduction, Genetic Transfection Ultraviolet Rays X-Rays beta-Galactosidase/analysis,biosynthesis
Chemicals
DNA, Viral Recombinant Proteins beta-Galactosidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ferrari F K
Gene Therapy Center, University of North Carolina, Chapel Hill 27599, USA.
Samulski T
Shenk T
Samulski R J
References (39)
39 references, click to expand
  1. Evidence for a single-stranded adenovirus-associated virus genome: formation of a DNA density hybrid on release of viral DNA.
    Proc Natl Acad Sci U S A. 1969 Nov;64(3):863-9 PMID: 5264145
  2. Phenotypic correction of Fanconi anemia in human hematopoietic cells with a recombinant adeno-associated virus vector.
    J Clin Invest. 1994 Oct;94(4):1440-8 PMID: 7929819
  3. Enhancement of adenovirus plaque formation on HeLa cells by magnesium chloride.
    J Gen Virol. 1970 Dec;9(3):251-5 PMID: 5532241
  4. Characteristics of a human cell line transformed by DNA from human adenovirus type 5.
    J Gen Virol. 1977 Jul;36(1):59-74 PMID: 886304
  5. Isolation of adenovirus type 5 host range deletion mutants defective for transformation of rat embryo cells.
    Cell. 1979 Jul;17(3):683-9 PMID: 476833
  6. An adenovirus type 5 early gene function regulates expression of other early viral genes.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3665-9 PMID: 291030
  7. Nucleotide sequence of the inverted terminal repetition in adeno-associated virus DNA.
    J Virol. 1980 May;34(2):402-9 PMID: 6246271
  8. Integration of the adeno-associated virus genome into cellular DNA in latently infected human Detroit 6 cells.
    J Virol. 1980 Feb;33(2):739-48 PMID: 6251245
  9. Phenotypes of adenovirus-5 host-range mutants for early-mRNA synthesis.
    Cold Spring Harb Symp Quant Biol. 1980;44 Pt 1,:429-36 PMID: 6933039
  10. Proteins and messenger RNAs of the transforming region of wild-type and mutant adenoviruses.
    J Mol Biol. 1980 Sep 25;142(3):399-417 PMID: 7463479
  11. Characterization of an immunosuppressive parvovirus related to the minute virus of mice.
    J Virol. 1981 Apr;38(1):317-26 PMID: 6264106
  12. A cascade of adenovirus early functions is required for expression of adeno-associated virus.
    Cell. 1981 Nov;27(1 Pt 2):133-41 PMID: 6276019
  13. Cloning of adeno-associated virus into pBR322: rescue of intact virus from the recombinant plasmid in human cells.
    Proc Natl Acad Sci U S A. 1982 Mar;79(6):2077-81 PMID: 6281795
  14. Adenovirus VAI RNA is required for efficient translation of viral mRNAs at late times after infection.
    Cell. 1982 Dec;31(3 Pt 2):543-51 PMID: 6297772
  15. Properties of an adenovirus type 2 mutant, Ad2dl807, having a deletion near the right-hand genome terminus: failure to help AAV replication.
    Virology. 1983 Apr 30;126(2):505-16 PMID: 6305001
  16. Cloning of infectious adeno-associated virus genomes in bacterial plasmids.
    Gene. 1983 Jul;23(1):65-73 PMID: 6352411
  17. Rescue of adeno-associated virus from recombinant plasmids: gene correction within the terminal repeats of AAV.
    Cell. 1983 May;33(1):135-43 PMID: 6088052
  18. HeLa cell beta-tubulin gene transcription is stimulated by adenovirus 5 in parallel with viral early genes by an E1a-dependent mechanism.
    Mol Cell Biol. 1984 Dec;4(12):2792-801 PMID: 6527689
  19. Adenoviral early region 4 is required for efficient viral DNA replication and for late gene expression.
    J Virol. 1986 Mar;57(3):833-8 PMID: 3485200
  20. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos.
    EMBO J. 1986 Dec 1;5(12):3133-42 PMID: 3102226
  21. Replication of adeno-associated virus in synchronized cells without the addition of a helper virus.
    J Virol. 1987 Apr;61(4):972-81 PMID: 3029431
  22. A recombinant plasmid from which an infectious adeno-associated virus genome can be excised in vitro and its use to study viral replication.
    J Virol. 1987 Oct;61(10):3096-101 PMID: 3041032
  23. Adenovirus E1B 55-Mr polypeptide facilitates timely cytoplasmic accumulation of adeno-associated virus mRNAs.
    J Virol. 1988 Jan;62(1):206-10 PMID: 2824848
  24. DNA amplification of adeno-associated virus as a response to cellular genotoxic stress.
    Cancer Res. 1988 Jun 1;48(11):3123-9 PMID: 2835153
  25. Recombinant adeno-associated virus (rAAV)-mediated expression of a human gamma-globin gene in human progenitor-derived erythroid cells.
    Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10183-7 PMID: 7524085
  26. DNA-damaging agents greatly increase the transduction of nondividing cells by adeno-associated virus vectors.
    J Virol. 1994 Dec;68(12):8282-7 PMID: 7966621
  27. Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia.
    N Engl J Med. 1995 May 18;332(20):1317-22 PMID: 7715639
  28. DNA synthesis and topoisomerase inhibitors increase transduction by adeno-associated virus vectors.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5719-23 PMID: 7777575
  29. Replication of adeno-associated virus in cells irradiated with UV light at 254 nm.
    J Virol. 1989 Mar;63(3):1023-30 PMID: 2536816
  30. Adenovirus early region 4 encodes two gene products with redundant effects in lytic infection.
    J Virol. 1989 Jun;63(6):2605-15 PMID: 2724411
  31. Helper-free stocks of recombinant adeno-associated viruses: normal integration does not require viral gene expression.
    J Virol. 1989 Sep;63(9):3822-8 PMID: 2547998
  32. Site-specific integration by adeno-associated virus.
    Proc Natl Acad Sci U S A. 1990 Mar;87(6):2211-5 PMID: 2156265
  33. Targeted integration of adeno-associated virus (AAV) into human chromosome 19.
    EMBO J. 1991 Dec;10(12):3941-50 PMID: 1657596
  34. IFN increases class I MHC antigen expression on adenovirus-infected human cells without inducing resistance to natural killer cell killing.
    J Immunol. 1992 Oct 1;149(7):2372-7 PMID: 1382100
  35. Modulation of the cellular phenotype by integrated adeno-associated virus.
    Virology. 1992 Sep;190(1):316-29 PMID: 1326806
  36. Characterization of a preferred site on human chromosome 19q for integration of adeno-associated virus DNA by non-homologous recombination.
    EMBO J. 1992 Dec;11(13):5071-8 PMID: 1334463
  37. Deletion of the E4 region of the genome produces adenovirus DNA concatemers.
    Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):153-7 PMID: 8278357
  38. Recombinant adeno-associated virus-mediated gene transfer into hematopoietic progenitor cells.
    Blood. 1994 Sep 1;84(5):1492-500 PMID: 8068942
  39. Evidence for a single-stranded adenovirus-associated virus genome: isolation and separation of complementary single strands.
    J Virol. 1970 Jun;5(6):693-9 PMID: 5429749
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-05-00
Pages
3227-34
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190186
Subset
IM
Grants
NIDDK NIH HHS · DK42701 · United States
NHLBI NIH HHS · HL48327 · United States
NHLBI NIH HHS · HL51818 · United States
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