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. 1973 Oct;12(4):808–818. doi: 10.1128/jvi.12.4.808-818.1973

Mechanism of Replication of Single-Stranded φX174 DNA VII. Circularization of the Progeny Viral Strand

Makoto Iwaya a, Shlomo Eisenberg a, Katalina Bartok a, David T Denhardt a,1
PMCID: PMC356698  PMID: 4591049

Abstract

Linear φX174 single-stranded DNA can be isolated from φX phage particles produced under various conditions. About half of the linear strands have a dGMP residue at the 5′ end, the remaining have roughly comparable amounts of dCMP, dTMP, and dAMP. The linear strands can be converted to covalently closed circular molecules by polynucleotide ligase, but only after they have been incubated with T4 DNA polymerase and deoxynucleoside triphosphates. Experiments with endonuclease R, the restriction enzyme from Haemophilus influenzae, indicated that the nucleotides incorporated into the DNA during this reaction were found predominantly in a limited region of the genome. The results suggest that the normal intermediate in single-stranded φX174 DNA synthesis may be a single-stranded linear molecule which is shorter than unit length and is intrinsically capable of circularization.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Denhardt D. T., Dressler D. H., Hathaway A. THE ABORTIVE REPLICATION OF PhiX174 DNA IN A RECOMBINATION-DEFICIENT MUTANT OF Escherichia coli. Proc Natl Acad Sci U S A. 1967 Mar;57(3):813–820. doi: 10.1073/pnas.57.3.813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Denhardt D. T., Sinsheimer R. L. The process of infection with bacteriophage phi-X174. 3. Phage maturation and lysis after synchronized infection. J Mol Biol. 1965 Jul;12(3):641–646. doi: 10.1016/s0022-2836(65)80318-7. [DOI] [PubMed] [Google Scholar]
  3. Dressler D. H., Denhardt D. T. Mechanism of replication of phi-X-174 single stranded DNA. Nature. 1968 Jul 27;219(5152):346–351. doi: 10.1038/219346a0. [DOI] [PubMed] [Google Scholar]
  4. Edgell M. H., Hutchison C. A., 3rd, Sclair M. Specific endonuclease R fragments of bacteriophage phiX174 deoxyribonucleic acid. J Virol. 1972 Apr;9(4):574–582. doi: 10.1128/jvi.9.4.574-582.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. FIERS W., SINSHEIMER R. L. The structure of the DNA of bacteriophage phi-X174. III. Ultracentrifugal evidence for a ring structure. J Mol Biol. 1962 Oct;5:424–434. doi: 10.1016/s0022-2836(62)80031-x. [DOI] [PubMed] [Google Scholar]
  6. Gilbert W., Dressler D. DNA replication: the rolling circle model. Cold Spring Harb Symp Quant Biol. 1968;33:473–484. doi: 10.1101/sqb.1968.033.01.055. [DOI] [PubMed] [Google Scholar]
  7. Glynn I. M., Chappell J. B. A simple method for the preparation of 32-P-labelled adenosine triphosphate of high specific activity. Biochem J. 1964 Jan;90(1):147–149. doi: 10.1042/bj0900147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goulian M., Lucas Z. J., Kornberg A. Enzymatic synthesis of deoxyribonucleic acid. XXV. Purification and properties of deoxyribonucleic acid polymerase induced by infection with phage T4. J Biol Chem. 1968 Feb 10;243(3):627–638. [PubMed] [Google Scholar]
  9. Hutchison C. A., 3rd, Sinsheimer R. L. The process of infection with bacteriophage phi-X174. X. Mutations in a phi-X Lysis gene. J Mol Biol. 1966 Jul;18(3):429–447. doi: 10.1016/s0022-2836(66)80035-9. [DOI] [PubMed] [Google Scholar]
  10. Iwaya M., Denhardt D. T. Mechanism of replication of phichi174 single-stranded DNA. V. Dispersive and conservative transfer of parental DNA into progeny DNA. J Mol Biol. 1973 Feb 19;73(3):291–305. doi: 10.1016/0022-2836(73)90343-4. [DOI] [PubMed] [Google Scholar]
  11. Iwaya M., Denhardt D. T. The mechanism of replication of phi X174 single-stranded DNA. II. The role of viral proteins. J Mol Biol. 1971 Apr 28;57(2):159–175. doi: 10.1016/0022-2836(71)90339-1. [DOI] [PubMed] [Google Scholar]
  12. Jovin T. M., Englund P. T., Bertsch L. L. Enzymatic synthesis of deoxyribonucleic acid. XXVI. Physical and chemical studies of a homogeneous deoxyribonucleic acid polymerase. J Biol Chem. 1969 Jun 10;244(11):2996–3008. [PubMed] [Google Scholar]
  13. Kato A. C., Bartok K., Fraser M. J., Denhardt D. T. Sensitivity of superhelical DNA to a single-strand specific endonuclease. Biochim Biophys Acta. 1973 Apr 21;308(7):68–78. doi: 10.1016/0005-2787(73)90123-8. [DOI] [PubMed] [Google Scholar]
  14. Knippers R., Razin A., Davis R., Sinsheimer R. L. The process of infection with Bacteriophage phi-X174. XXIX. In vivo studies on the synthesis of the single-stranded DNA of progeny phi-X174 bacteriophage. J Mol Biol. 1969 Oct 28;45(2):237–263. doi: 10.1016/0022-2836(69)90103-x. [DOI] [PubMed] [Google Scholar]
  15. Koczot F. J., Carter B. J., Garon C. F., Rose J. A. Self-complementarity of terminal sequences within plus or minus strands of adenovirus-associated virus DNA. Proc Natl Acad Sci U S A. 1973 Jan;70(1):215–219. doi: 10.1073/pnas.70.1.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lindqvist B. H., Sinsheimer R. L. The process of infection with bacteriophage phi X174. XVI. Synthesis of the replicative form and its relationship to viral single-stranded DNA synthesis. J Mol Biol. 1968 Mar 14;32(2):285–302. doi: 10.1016/0022-2836(68)90010-7. [DOI] [PubMed] [Google Scholar]
  17. Modrich P., Lehman I. R. Enzymatic characterization of a mutant of Escherichia coli with an altered DNA ligase. Proc Natl Acad Sci U S A. 1971 May;68(5):1002–1005. doi: 10.1073/pnas.68.5.1002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pauling C., Hamm L. Properties of a temperature-sensitive radiation-sensitive mutant of Escherichia coli. Proc Natl Acad Sci U S A. 1968 Aug;60(4):1495–1502. doi: 10.1073/pnas.60.4.1495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pauling C., Hamm L. Properties of a temperature-sensitive, radiation-sensitive mutant of Escherichia coli. II. DNA replication. Proc Natl Acad Sci U S A. 1969 Dec;64(4):1195–1202. doi: 10.1073/pnas.64.4.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Radloff R., Vinograd J. The absence of a non-nucleotide linker in polyoma and phiX174 DNA. Biochim Biophys Acta. 1971 Oct 14;247(2):207–219. doi: 10.1016/0005-2787(71)90671-x. [DOI] [PubMed] [Google Scholar]
  21. Richardson C. C. Phosphorylation of nucleic acid by an enzyme from T4 bacteriophage-infected Escherichia coli. Proc Natl Acad Sci U S A. 1965 Jul;54(1):158–165. doi: 10.1073/pnas.54.1.158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. STUDIER F. W. SEDIMENTATION STUDIES OF THE SIZE AND SHAPE OF DNA. J Mol Biol. 1965 Feb;11:373–390. doi: 10.1016/s0022-2836(65)80064-x. [DOI] [PubMed] [Google Scholar]
  23. Schaller H., Voss H., Gucker S. Structure of the DNA of bacteriophage fd. II. Isolation and characterization of a DNA fraction with double strand-like properties. J Mol Biol. 1969 Sep 28;44(3):445–458. doi: 10.1016/0022-2836(69)90372-6. [DOI] [PubMed] [Google Scholar]
  24. Schekman R. W., Iwaya M., Bromstrup K., Denhardt D. T. The mechanism of replication of phi X174 single-stranded DNA. 3. An enzymic study of the structure of the replicative form II DNA. J Mol Biol. 1971 Apr 28;57(2):177–199. doi: 10.1016/0022-2836(71)90340-8. [DOI] [PubMed] [Google Scholar]
  25. Schekman R. W., Ray D. S. Polynucleotide ligase and phiX174 single strand synthesis. Nat New Biol. 1971 Jun 9;231(23):170–173. doi: 10.1038/newbio231170a0. [DOI] [PubMed] [Google Scholar]
  26. Schröder C., Kaerner H. -C. Infectivity to Escherichia coli spheroplasts of linear phiX174 DNA strands derived from the replicative form (RFII) of phiX DNA. FEBS Lett. 1971 Nov 15;19(1):38–44. doi: 10.1016/0014-5793(71)80600-2. [DOI] [PubMed] [Google Scholar]
  27. Smith H. O., Wilcox K. W. A restriction enzyme from Hemophilus influenzae. I. Purification and general properties. J Mol Biol. 1970 Jul 28;51(2):379–391. doi: 10.1016/0022-2836(70)90149-x. [DOI] [PubMed] [Google Scholar]
  28. Symons R. H. Preparation of [alpha-32P]nucleoside and deoxynucleoside 5'-triphosphates from 32Pi and protected and unprotected nucleosides. Biochim Biophys Acta. 1969 Oct 22;190(2):548–550. doi: 10.1016/0005-2787(69)90105-1. [DOI] [PubMed] [Google Scholar]
  29. Weiss B., Jacquemin-Sablon A., Live T. R., Fareed G. C., Richardson C. C. Enzymatic breakage and joining of deoxyribonucleic acid. VI. Further purification and properties of polynucleotide ligase from Escherichia coli infected with bacteriophage T4. J Biol Chem. 1968 Sep 10;243(17):4543–4555. [PubMed] [Google Scholar]
  30. Weiss B., Live T. R., Richardson C. C. Enzymatic breakage and joining of deoxyribonucleic acid. V. End group labeling and analysis of deoxyribonucleic acid containing single straned breaks. J Biol Chem. 1968 Sep 10;243(17):4530–4542. [PubMed] [Google Scholar]

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