Initiation of Adenovirus DNA Replication: Detection of Covalent Complexes Between Nucleotide and the 80-kilodalton Terminal Protein

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1982 Jan 1

PMID 6896346

Citations 39

Authors

M D Challberg

J M Ostrove

T J Kelly Jr

Affiliations

Soon will be listed here.

Abstract

We have previously shown that the 5'-terminal deoxycytidine residue of each nascent adenovirus 5 DNA strand synthesized in vitro is covalently linked to the 80-kilodalton (kd) terminal protein precursor via a phosphodiester bond to a serine residue in the protein. When extracts prepared from adenovirus 5-infected cells are incubated with [alpha-33P]dCTP as the only added deoxynucleoside triphosphate, complexes consisting of nucleotide covalently linked to the 80-kd protein can be detected. The nucleotide moieties present in such complexes include d(pC) and d(pCpA), the 5'-terminal nucleotide and dinucleotide of adenovirus 5 DNA, respectively, as well as some longer oligonucleotides. The formation of these complexes requires the presence of adenovirus DNA containing the attached 55-kd terminal protein and ATP. Extracts from H5ts125-infected cells which are defective in DNA replication catalyze complex formation to the same extent as extracts prepared from wild-type infected cells; thus, the presence of the adenovirus-coded 72-kd DNA-binding protein is apparently not required. Most, if not all, of the 80-kd protein-nucleotide complexes that are formed are noncovalently bound to the input viral DNA. These observations are consistent with the protein-priming model for the initiation of adenovirus DNA replication.

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References

Green M, Pina M, Kimes R, Wensink P, MacHattie L, Thomas Jr C . Adenovirus DNA. I. Molecular weight and conformation. Proc Natl Acad Sci U S A. 1967; 57(5):1302-9. PMC: 224472. DOI: 10.1073/pnas.57.5.1302. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

Ensinger M, Ginsberg H . Selection and preliminary characterization of temperature-sensitive mutants of type 5 adenovirus. J Virol. 1972; 10(3):328-39. PMC: 356471. DOI: 10.1128/JVI.10.3.328-339.1972. View

van der Vliet P, Levine A . DNA-binding proteins specific for cells infected by adenovirus. Nat New Biol. 1973; 246(154):170-4. DOI: 10.1038/newbio246170a0. View

van der Vliet P, Levine A, Ensinger M, Ginsberg H . Thermolabile DNA binding proteins from cells infected with a temperature-sensitive mutant of adenovrius defective in viral DNA synthesis. J Virol. 1975; 15(2):348-54. PMC: 354459. DOI: 10.1128/JVI.15.2.348-354.1975. View

Vliet P, Sussenbach J . An adenovirus type 5 gene function required for initiation of viral DNA replication. Virology. 1975; 67(2):415-26. DOI: 10.1016/0042-6822(75)90443-2. View

Maxam A, Gilbert W . A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977; 74(2):560-4. PMC: 392330. DOI: 10.1073/pnas.74.2.560. View

van der Vliet P, Zandberg J, Jansz H . Evidence for a function of the adenovirus DNA-binding protein in initiation in DNA synthesis as well as in elongation of nascent DNA chains. Virology. 1977; 80(1):98-110. DOI: 10.1016/0042-6822(77)90383-x. View

Ginsberg H, LUNDHOLM U, Linne T . Adenovirus DNA-binding protein in cells infected with wild-type 5 adenovirus and two DNA-minus, temperature-sensitive mutants, H5ts125 and H5ts149. J Virol. 1977; 23(1):142-51. PMC: 515810. DOI: 10.1128/JVI.23.1.142-151.1977. View

10.

Rekosh D, Russell W, Bellet A, Robinson A . Identification of a protein linked to the ends of adenovirus DNA. Cell. 1977; 11(2):283-95. DOI: 10.1016/0092-8674(77)90045-9. View

11.

Lechner R, Kelly Jr T . The structure of replicating adenovirus 2 DNA molecules. Cell. 1977; 12(4):1007-20. DOI: 10.1016/0092-8674(77)90165-9. View

12.

Steenbergh P, Maat J, Van Ormondt H, Sussenbach J . The nucleotide sequence at the termini of adenovirus type 5 DNA. Nucleic Acids Res. 1977; 4(12):4371-89. PMC: 343247. DOI: 10.1093/nar/4.12.4371. View

13.

van der Vliet P, Keegstra W, Jansz H . Complex formation between the adenovirus type 5 DNA-binding protein and single-stranded DNA. Eur J Biochem. 1978; 86(2):389-98. DOI: 10.1111/j.1432-1033.1978.tb12321.x. View

14.

Winnacker E . Adenovirus DNA: structure and function of a novel replicon. Cell. 1978; 14(4):761-73. DOI: 10.1016/0092-8674(78)90332-x. View

15.

Horwitz M . Temperature-sensitive replication of H5ts125 adenovirus DNA in vitro. Proc Natl Acad Sci U S A. 1978; 75(9):4291-5. PMC: 336099. DOI: 10.1073/pnas.75.9.4291. View

16.

Challberg M, Kelly Jr T . Adenovirus DNA replication in vitro. Proc Natl Acad Sci U S A. 1979; 76(2):655-9. PMC: 383008. DOI: 10.1073/pnas.76.2.655. View

17.

Kaplan L, Ariga H, Hurwitz J, Horwitz M . Complementation of the temperature-sensitive defect in H5ts125 adenovirus DNA replication in vitro. Proc Natl Acad Sci U S A. 1979; 76(11):5534-8. PMC: 411683. DOI: 10.1073/pnas.76.11.5534. View

18.

Challberg M, Kelly Jr T . Adenovirus DNA replication in vitro: origin and direction of daughter strand synthesis. J Mol Biol. 1979; 135(4):999-1012. DOI: 10.1016/0022-2836(79)90524-2. View

19.

Schechter N, Davies W, Anderson C . Adenovirus coded deoxyribonucleic acid binding protein. Isolation, physical properties, and effects of proteolytic digestion. Biochemistry. 1980; 19(12):2802-10. DOI: 10.1021/bi00553a041. View

20.

Stillman B, Lewis J, Chow L, Mathews M, Smart J . Identification of the gene and mRNA for the adenovirus terminal protein precursor. Cell. 1981; 23(2):497-508. DOI: 10.1016/0092-8674(81)90145-8. View