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Homologous Recombination in the Replicative Cycle of Adenoviruses and Its Relationship to DNA Replication

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The Molecular Repertoire of Adenoviruses II

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 199/2))

Abstract

The observation that adenovirus genomes can undergo genetic recombination is almost a quarter of a century old (Williams and Ustaçelebi 1971; Takemori 1972; Ensinger and Ginsberg 1972), yet despite its early discovery and its rapid exploitation as a tool for mapping mutations and for creating new genotypes (reviewed in Ginsberg and Young 1977; Young et al. 1984b), the mechanisms underlying it are not well understood at the molecular and biochemical levels. Such an understanding, however, can be expected to shed light not only on the specific features peculiar to adenovirus recombination itself, but also on the more general characteristics of the repair and recombinational capacities of the cell. These cellular aspects are of considerable current theoretical and practical interest, because of recent advances both in uncovering the molecular basis of genetic defects in DNA repair in mammalian cells and in the techniques of gene targeting by homologous recombination in order to investigate mammalian development and differentiation. As with many other fundamental biological phenomena, the study of adenovirus recombination can be expected to yield valuable insights into the normal capacities of the cell.

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References

  • Ahem KG, Wang K, Xu F-Y, Mathews CZ,Pearson GD (1991) Strands hybridize in postreplicative adenovirus overlap recombination. Proc Natl Acad Sci USA 88: 105–109

    Article  Google Scholar 

  • Anderson CW, Hardy MM, Dunn JJ, Klessig DF (1983) Independent, spontaneous mutants of adenovirus type 2-simian virus 40 hybrid Ad2+ND3 that grow efficiently in monkey cells possess identical mutations in the adenovirus type 2 DNA-binding gene. J Virol 48: 31–39

    PubMed  Google Scholar 

  • Barnes DE, Tomkinson AE, Lehmann AR, Webster ADB, Lindahl T (1992) Mutations in the DNA ligase I gene of an individual with immunodeficiencies and cellular hypersensitivity to DNA-damaging agents. Cell 69: 495–503

    Article  PubMed  CAS  Google Scholar 

  • Bennett KL, Pearson GD (1993) Sequence conversion during postreplicative adenovirus overlap recombination. Proc Natl Acad Sci USA 90: 1397–1401

    Article  PubMed  CAS  Google Scholar 

  • Berkner KL, Sharp PA (1983) Generation of adenovirus by transfection of plasmids. Nucleic Acids Res 11: 6003–6020

    Article  PubMed  CAS  Google Scholar 

  • Bodnar JW, Pearson GD (1980) Kinetics of adenovirus DNA replication. II Initiation of adenovirus DNA replication. Virology 105: 357–370

    Article  PubMed  CAS  Google Scholar 

  • Borts RH, Lichten M, Haber JE (1985) Analysis of meiosis-defective mutations in yeast by physical monitoring of recombination. Genetics 113: 551–567

    Google Scholar 

  • Carusi EA (1977) Evidence for blocked 5′ termini in human adenovirus DNA. Virology 76: 380–394

    Article  PubMed  CAS  Google Scholar 

  • Challberg MD, Kelly TJ Jr (1979) Adenovirus DNA replication in vitro. Proc Natl Acad Sci USA 76: 655–659

    Article  PubMed  CAS  Google Scholar 

  • Challberg MD, Kelly TJ Jr (1989) Animal virus DNA replication. Annu Rev Biochem 58: 671–717

    Article  PubMed  CAS  Google Scholar 

  • Cheng KC, Smith GR (1989) Distribution of Chi-stimulated recombinational exchanges and heteroduplex endpoints in phage lambda. Genetics 123: 5–17

    PubMed  CAS  Google Scholar 

  • Chinnadurai G, Chinnadurai S, Brusca J (1979) Physical mapping of a large plaque mutation of adenovirus type 2. J Virol 32: 623–628

    PubMed  CAS  Google Scholar 

  • Chroboczek J, Bieber F, Jacrot B (1992) The sequence of the genome of adenovirus type 5 and its comparison with the genome of adenovirus type 2. Virology 186: 280–285

    Article  PubMed  CAS  Google Scholar 

  • Detloff P, White MA, Petes TD (1992) Analysis of a gene conversion gradient at the HIS4 locus in Saccharomyces cerevisiae. Genetics 132: 113–123

    PubMed  CAS  Google Scholar 

  • Doerfler W (1981) DNA methylation—a regulatory signal in eukaryotic gene expression. J Gen Virol 57: 1–20

    Article  PubMed  CAS  Google Scholar 

  • Doermann AH (1953) The vegetative state in the life cycle of bacteriophage: evidence for its occurrence, and its genetic characterization. Cold Spring Harbor Symp Quant Biol 18: 3–11

    PubMed  CAS  Google Scholar 

  • Dunsworth-Browne M, Schell RE, Berk AJ (1980) Adenovirus terminal protein protects single stranded DNA from digestion by a cellular exonuclease. Nucleic Acids Res 8: 543–554

    Article  PubMed  CAS  Google Scholar 

  • Ensinger MJ, Ginsberg HS (1972) Selection and preliminary characterization of temperature-sensitive mutants of type 5 adenovirus. J Virol 10: 328–339

    PubMed  CAS  Google Scholar 

  • Epstein LH, Young CSH (1991) Adenovirus homologous recombination does not require expression of the immediate-early E1a gene. J Virol 65: 4475–4479

    PubMed  CAS  Google Scholar 

  • Fishel R, Lescoe MK, Rao MRS, Copeland NG, Jenkins NA, Garber J, Kane M, Kolodner R (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75: 1027–1038

    Article  PubMed  CAS  Google Scholar 

  • Fisher C, Parks RJ, Lauzon ML, Evans DH (1991) Heteroduplex DNA formation is associated with replication and recombination in poxvirus-infected cells. Genetics 129: 7–18

    PubMed  CAS  Google Scholar 

  • Flint SJ, Berget SM, Sharp PA (1976) Characterization of single-stranded viral DNA sequences present during replication of adenovirus types 2 and 5. Cell 9: 559–571

    Article  PubMed  CAS  Google Scholar 

  • Folger KR, Wong EA, Wahl G, Capecchi MR (1982) Patterns of integration of DNA microinjected into cultured mammalian cells: evidence for homologous recombination between injected plasmid DNA molecules. Mol Cell Biol 2: 1372–1387

    PubMed  CAS  Google Scholar 

  • Friedberg EC (1992) Xeroderma pigmentosum, Cockayne’s syndrome, helicases, and DNA repair: what’s the relationship? Cell 71: 887–889

    Article  PubMed  CAS  Google Scholar 

  • Frost E, Williams J (1978) Mapping temperature-sensitive and host range mutations of adenovirus type5 by marker rescue. Virology 91: 39–50

    Article  PubMed  CAS  Google Scholar 

  • Ginsberg HS, Young CSH (1977) The genetics of adenovirus. In: Fraenkel-Conrat H, Wagner RR (eds) Comprehensive virology, vol 9. Plenum, New York, pp 27–88

    Google Scholar 

  • Graham FL, Van der Eb AJ (1973) A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52: 456–467

    Article  PubMed  CAS  Google Scholar 

  • Haibert DN, Cutt JR, Shenk T (1986) Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J Virol 56: 250–257

    Google Scholar 

  • Hay RT, Stow ND, McDougall IM (1984) Replication of adenovirus mini-chromosomes. J Mol Biol 175: 493–510

    Article  PubMed  CAS  Google Scholar 

  • Hershey AD, Chase M (1951) Genetic recombination and heterozygosis in bacteriophage. Cold Spring Harbor Symp Quant Biol 16: 471–479

    PubMed  CAS  Google Scholar 

  • Holmes J, Clark S, Modrich P (1990) Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines. Proc Natl Acad Sci USA 87: 5837–5841

    Article  PubMed  CAS  Google Scholar 

  • Klessig DF, Grodzicker T (1979) Mutations that allow human Ad2 and Ad5 to express late genes in monkey cells map in the viral gene encoding the 72K DNA binding protein. Cell 17: 957–966

    Article  PubMed  CAS  Google Scholar 

  • Lewis JB, Anderson CW (1983) Proteins encoded near the adenovirus late messenger RNA leader segments. Virology 127: 112–123

    Article  PubMed  CAS  Google Scholar 

  • Lichten M, Goyon C, Schultes NP, Treco D, Szostak JW, Haber JE, Nicolas A (1990) Detection of heteroduplex DNA molecules among the products of Saccharomyces cerevisiae meiosis. Proc Natl Acad Sci USA 87: 7653–7657

    Article  PubMed  CAS  Google Scholar 

  • Mautner V, Mackay N (1984) Recombination in adenovirus: analysis of crossover sites in intertypic overlap recombinants. Virology 139: 43–52

    Article  PubMed  CAS  Google Scholar 

  • Meselson MS, Radding CM (1975) A general model for recombination. Proc Natl Acad Sci USA 72: 358–361

    Article  PubMed  CAS  Google Scholar 

  • Meyn MS (1993) High spontaneous intrachromosomal recombination rates in ataxia-telangiectasia. Science 260: 1327–1330

    Article  PubMed  CAS  Google Scholar 

  • Modrich P (1991) Mechanisms and biological effects of mismatch repair. Annu Rev Genet 25: 229–253

    Article  PubMed  CAS  Google Scholar 

  • Munz PL, Young CSH (1984) Polarity in adenovirus recombination. Virology 135: 503–514

    Article  PubMed  CAS  Google Scholar 

  • Munz PL, Young CSH (1987) The creation of adenovirus genomes with viable, stable, internal redundancies centered about the E2b region. Virology 158: 52–60

    Article  PubMed  CAS  Google Scholar 

  • Munz PL, Young CSH (1991) End-joining of DNA fragments in adenovirus transfection of human cells. Virology 183: 160–169

    Article  PubMed  CAS  Google Scholar 

  • Munz PI, Young C, Young CSH (1983) The genetic analysis of adenovirus recombination in triparental and superinfection crosses. Virology 126: 576–586

    Article  PubMed  CAS  Google Scholar 

  • Nicolas JC, Sarnow P, Girard M, Levine AJ (1983) Host range temperature-conditional mutants in the adenovirus DNA binding protein are defective in the assembly of infectious virus. Virology 126: 228–239

    Article  PubMed  CAS  Google Scholar 

  • Parsons R, Li G-M, Longley MJ, Fang W-H, Papadopoulos N, Jen J, de la Chapelle A, Kinzler KW, Vogelstein B, Modrich P(1993) Hypermutability and mismatch repair deficiency in RER+tumor cells. Cell 75: 1227–1236

    Article  PubMed  CAS  Google Scholar 

  • Pruzan R, Chatterjee PK, Flint SJ (1992) Specific transcription from the adenovirus E2E promoter by RNA polymerase III requires a subpopulation of TFIID. Nucleic Acids Res. 20: 5705–5712

    Article  PubMed  CAS  Google Scholar 

  • Puvion-Dutilleul F, Puvion E (1990a) Analysis by in situ hybridization and autoradiography of sites of replication and storage of single- and double-stranded adenovirus type 5 DNA in lytically infected HeLa cells. J Struct Biol 103: 280–289

    Article  CAS  Google Scholar 

  • Puvion-Dutilleul F, Puvion E (1990b) Replicating single-stranded adenovirus type 5 DNA molecules accumulate within well-delimited intranuclear areas of lytically infected HeLa cells. Eur J Cell Biol 52: 379–388

    CAS  Google Scholar 

  • Rainbow AJ (1991) Host cell reactivation of sunlamp-exposed adenovirus in fibroblasts from patients with Bloom’s syndrome, ataxia telangiectasia, and Huntington’s disease. Environ Mol Mutagen 17: 98–103

    Article  PubMed  CAS  Google Scholar 

  • Roberts RJ, Akusjärvi G, Aleström P, Gelinas RE, Gingeras TR, Sciaky D, Pettersson U (1986) A consensus sequence for the adenovirus-2 genome In: Doerfler W (ed) Adenovirus DNA. Martinus Nijhoff, Boston, pp 1–51

    Chapter  Google Scholar 

  • Roovers DJ, Young CSH, Vos HL, Sussenbach JS (1990) Physical mapping of two temperature-sensitive adenovirus mutants affected in the DNA polymerase and DNA binding protein. Virus Genes 4: 53–61

    Article  PubMed  CAS  Google Scholar 

  • Roth D, Wilson J (1988) Illegitimate recombination in mammalian cells. In: Kucherlapati R, Smith GR (eds) Genetic recombination. American Society for Microbiology, Washington DC, pp 621–653

    Google Scholar 

  • Soloway PD, Shenk T (1990) The adenovirus type 5 i-leader open reading frame functions in eis to reduce the half-life of L1 mRNAs. J Virol 64: 551–558

    PubMed  CAS  Google Scholar 

  • Sung P, Bailly V, Weber C, Thompson LH, Prakash L, Prakash S (1993) Human xeroderma pigmentosum group D gene encodes a DNA helicase. Nature 365: 852–855

    Article  PubMed  CAS  Google Scholar 

  • Symington JS, Lucher LA, Brackmann KH, Virtanen A, Pettersson U, Green M (1986) Biosynthesis of adenovirus type 2 i-leader protein. J Virol 57: 848–856

    PubMed  CAS  Google Scholar 

  • Takemori N (1972) Genetic studies with tumorigenic adenoviruses. III. Recombination in adenovirus type 12. Virology 47: 157–167

    Article  PubMed  CAS  Google Scholar 

  • Thomas DC, Roberts JD, Kunkel TA (1991) Heteroduplex repair in extracts of human HeLa cells. J Biol Chem 266: 3744–3751

    PubMed  CAS  Google Scholar 

  • Visconti N, Delbrück M (1953) The mechanism of genetic recombination in phage. Genetics 38: 5–33

    PubMed  CAS  Google Scholar 

  • Volkert FC, Young CSH (1983) The genetic analysis of recombination using adenovirus overlapping terminal DNA fragments. Virology 125: 175–193

    Article  PubMed  CAS  Google Scholar 

  • Volkert FC, Münz PL, Young CSH (1989) A genetic investigation of the mechanism of adenovirus marker rescue. Virology 173: 77–88

    Article  PubMed  CAS  Google Scholar 

  • Wang K, Pearson GD, (1985) Adenovirus sequences required for replication in vivo. Nucleic Acids Res 13: 5173–5187

    Article  PubMed  CAS  Google Scholar 

  • Wang K, Xu F-Y, Ahern KG, Pearson GD (1991) Inverted repeats direct repair of adenovirus mini-chromosome ends. Virology 183: 44–51

    Article  PubMed  CAS  Google Scholar 

  • Weinberg DH, Ketner G (1986) Adenoviral early region 4 is required for efficient viral DNA replication and for late gene expression. J Virol 57: 833–838

    PubMed  CAS  Google Scholar 

  • White E (1993) Regulation of apoptosis by the transforming genes of the DNA tumor virus adenovirus. Proc Soc Exp Biol Med 204: 30–39

    PubMed  CAS  Google Scholar 

  • Williams JF, Ustagelebi S (1971) Complementation and recombination with temperature-sensitive mutants of adenovirus type 5. J Gen virol 13: 345–348

    Article  PubMed  CAS  Google Scholar 

  • Williams JF, Young CSH, Austin PE (1974) Genetic analysis of human adenovirus type 5 in permissive and nonpermissive cells. Cold Spring Harbor Symp Quant Biol 39: 427–437

    Google Scholar 

  • Williams J, Grodzicker T, Sharp P, Sambrook S (1975) Adenovirus recombination: physical mapping of crossover events. Cell 4: 113–119

    Article  PubMed  CAS  Google Scholar 

  • Wold WSM, Gooding LR (1991) Region E3 of adenovirus: a cassette of genes involved in host immunosurveillance and virus-cell interactions. Virology 184: 1–8

    Article  PubMed  CAS  Google Scholar 

  • Wolgemuth DJ, Hsu M-T (1980) Visualization of genetic recombination intermediates of human adenovirus type 2 DNA from infected HeLa cells. Nature 287: 168–171

    Article  PubMed  CAS  Google Scholar 

  • Wolgemuth DJ, Hsu M-T (1981) DNA replication-mediated recombination of molecules of adenovirus 2 DNA. Proc Natl Acad Sci USA 78: 5076–5080

    Article  PubMed  CAS  Google Scholar 

  • Wood RD, Coverley D (1991) DNA excision repair in mammalian cell extracts. Bioessays 13: 447–453

    Article  PubMed  CAS  Google Scholar 

  • Young CSH, Fisher PB (1980) Adenovirus recombination in normal and repair-deficient human fibroblasts. Virology 100: 197–184

    Article  Google Scholar 

  • Young CSH, Silverstein SJ (1980) The kinetics of adenovirus recombination in homotypic and heterotypic genetic crosses. Virology 101: 503–515

    Article  PubMed  CAS  Google Scholar 

  • Young CSH, Williams JF (1975) Heat-stable variant of human adenovirus type 5: characterization and use in three-factor crosses. J virol 15: 1168–1175

    PubMed  CAS  Google Scholar 

  • Young CSH, Cachianes G, Münz P, Silverstein S (1984a) Replication and recombination in adenovirus-infected cells are temporally and functionally related. J Virol 51: 571–577

    CAS  Google Scholar 

  • Young CSH, ShenkT, Ginsberg HS (1984b) The genetic system In. Ginsberg HS (ed) The adenoviruses. Plenum, New York, pp 125–172

    Google Scholar 

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Young, C.S.H. (1995). Homologous Recombination in the Replicative Cycle of Adenoviruses and Its Relationship to DNA Replication. In: Doerfler, W., Böhm, P. (eds) The Molecular Repertoire of Adenoviruses II. Current Topics in Microbiology and Immunology, vol 199/2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79499-5_4

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