Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1973 Jan;70(1):205–209. doi: 10.1073/pnas.70.1.205

A Coat Protein of the Bacteriophage M13 Virion Participates in Membrane-Oriented Synthesis of DNA

S Michal Jazwinski 1, Roberto Marco 1, Arthur Kornberg 1
PMCID: PMC433216  PMID: 4567335

Abstract

Several molecules of a protein specified by gene 3 of M13 comprise a minor fraction of the phage coat and have been assigned a role in adsorption to the bacterial cell. We find that the gene-3 protein molecules of the virion are fully conserved in phage that have attached irreversibly to the host cell, and they form a complex with the phage DNA when it has been converted to a duplex replicative form. In cells infected at a restrictive temperature with a thermosensitive mutant in gene 3, there is no conversion of the phage DNA to the replicative form. Both the adsorbed phage and the complex of replicative form DNA with the gene-3 protein were isolated with the inner membrane fraction of the cell. We suggest that the gene-3 protein may perform an essential function in the synthesis of replicative form by linking the phage DNA to a cellular replicative system in or on the inner cell membrane.

Keywords: gene-3 protein, parental RF-gene-3 protein complex, cell inner membrane, ϕX174, fd and fl

Full text

PDF
209

Selected References

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

  1. Asbeck F., Beyreuther K., Köhler H., von Wettstein G., Braunitzer G. Virusproteine, IV. Die Konstitution des Hüllproteins des Phagen fd. Hoppe Seylers Z Physiol Chem. 1969 Sep;350(9):1047–1066. [PubMed] [Google Scholar]
  2. Brutlag D., Schekman R., Kornberg A. A possible role for RNA polymerase in the initiation of M13 DNA synthesis. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2826–2829. doi: 10.1073/pnas.68.11.2826. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Caro L. G., Schnös M. The attachment of the male-specific bacteriophage F1 to sensitive strains of Escherichia coli. Proc Natl Acad Sci U S A. 1966 Jul;56(1):126–132. doi: 10.1073/pnas.56.1.126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Forsheit A. B., Ray D. S. Replication of bacteriophage M13. VI. Attachment of M13 DNA to a fast-sedimenting host cell component. Virology. 1971 Mar;43(3):647–664. doi: 10.1016/0042-6822(71)90289-3. [DOI] [PubMed] [Google Scholar]
  5. Henry T. J., Brinton C. C., Jr Removal of the coat protein of bacteriophages M13 or fd from the exterior of the host after infection. Virology. 1971 Dec;46(3):754–763. doi: 10.1016/0042-6822(71)90077-8. [DOI] [PubMed] [Google Scholar]
  6. Henry T. J., Pratt D. The proteins of bacteriophage M13. Proc Natl Acad Sci U S A. 1969 Mar;62(3):800–807. doi: 10.1073/pnas.62.3.800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. JOVIN T., CHRAMBACH A., NAUGHTON M. A. AN APPARATUS FOR PREPARATIVE TEMPERATURE-REGULATED POLYACRYLAMIDE GEL ELECTROPHORESIS. Anal Biochem. 1964 Nov;9:351–369. doi: 10.1016/0003-2697(64)90192-7. [DOI] [PubMed] [Google Scholar]
  8. Kozak M., Nathans D. Fate of maturation protein during infection by coliphage MS2. Nat New Biol. 1971 Sep 15;234(50):209–211. doi: 10.1038/newbio234209a0. [DOI] [PubMed] [Google Scholar]
  9. Krahn P. M., O'Callaghan R. J., Paranchych W. Stages in phage R17 infection. VI. Injection of A protein and RNA into the host cell. Virology. 1972 Mar;47(3):628–637. doi: 10.1016/0042-6822(72)90552-1. [DOI] [PubMed] [Google Scholar]
  10. Marvin D. A., Hohn B. Filamentous bacterial viruses. Bacteriol Rev. 1969 Jun;33(2):172–209. doi: 10.1128/br.33.2.172-209.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Marvin D. A., Schaller H. The topology of DNA from the small filamentous bacteriophage fd. J Mol Biol. 1966 Jan;15(1):1–7. doi: 10.1016/s0022-2836(66)80204-8. [DOI] [PubMed] [Google Scholar]
  12. Newbold J. E., Sinsheimer R. L. The process of infection with bacteriophage phiX174. XXXII. Early steps in the infection process: attachment, eclipse and DNA penetration. J Mol Biol. 1970 Apr 14;49(1):49–66. doi: 10.1016/0022-2836(70)90375-x. [DOI] [PubMed] [Google Scholar]
  13. Osborn M. J., Gander J. E., Parisi E., Carson J. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem. 1972 Jun 25;247(12):3962–3972. [PubMed] [Google Scholar]
  14. Pratt D., Erdahl W. S. Genetic control of bacteriophage M13 DNA synthesis. J Mol Biol. 1968 Oct 14;37(1):181–200. doi: 10.1016/0022-2836(68)90082-x. [DOI] [PubMed] [Google Scholar]
  15. Pratt D., Tzagoloff H., Beaudoin J. Conditional lethal mutants of the small filamentous coliphage M13. II. Two genes for coat proteins. Virology. 1969 Sep;39(1):42–53. doi: 10.1016/0042-6822(69)90346-8. [DOI] [PubMed] [Google Scholar]
  16. Pratt D., Tzagoloff H., Erdahl W. S. Conditional lethal mutants of the small filamentous coliphage M13. I. Isolation, complementation, cell killing, time of cistron action. Virology. 1966 Nov;30(3):397–410. doi: 10.1016/0042-6822(66)90118-8. [DOI] [PubMed] [Google Scholar]
  17. Ray D. S., Schekman R. W. Replication of bacteriophage M13. I. Sedimentation analysis of crude lysates of M13-infected bacteria. Biochim Biophys Acta. 1969 Apr 22;179(2):398–407. [PubMed] [Google Scholar]
  18. SALIVAR W. O., TZAGOLOFF H., PRATT D. SOME PHYSICAL-CHEMICAL AND BIOLOGICAL PROPERTIES OF THE ROD-SHAPED COLIPHAGE M13. Virology. 1964 Nov;24:359–371. doi: 10.1016/0042-6822(64)90173-4. [DOI] [PubMed] [Google Scholar]
  19. Scandella C. J., Kornberg A. A membrane-bound phospholipase A1 purified from Escherichia coli. Biochemistry. 1971 Nov 23;10(24):4447–4456. doi: 10.1021/bi00800a015. [DOI] [PubMed] [Google Scholar]
  20. Schekman R., Wickner W., Westergaard O., Brutlag D., Geider K., Bertsch L. L., Kornberg A. Initiation of DNA synthesis: synthesis of phiX174 replicative form requires RNA synthesis resistant to rifampicin. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2691–2695. doi: 10.1073/pnas.69.9.2691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. TZAGOLOFF H., PRATT D. THE INITIAL STEPS IN INFECTION WITH COLIPHAGE M13. Virology. 1964 Nov;24:372–380. doi: 10.1016/0042-6822(64)90174-6. [DOI] [PubMed] [Google Scholar]
  22. Trenkner E., Bonhoeffer F., Gierer A. The fate of the protein component of bacteriophage fd during infection. Biochem Biophys Res Commun. 1967 Sep 27;28(6):932–939. doi: 10.1016/0006-291x(67)90069-1. [DOI] [PubMed] [Google Scholar]
  23. Tseng B. Y., Marvin D. A. Filamentous bacterial viruses. V. Asymmetric replication of fd duplex deoxyribonucleic acid. J Virol. 1972 Sep;10(3):371–383. doi: 10.1128/jvi.10.3.371-383.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Wickner W., Brutlag D., Schekman R., Kornberg A. RNA synthesis initiates in vitro conversion of M13 DNA to its replicative form. Proc Natl Acad Sci U S A. 1972 Apr;69(4):965–969. doi: 10.1073/pnas.69.4.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yamamoto K. R., Alberts B. M., Benzinger R., Lawhorne L., Treiber G. Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology. 1970 Mar;40(3):734–744. doi: 10.1016/0042-6822(70)90218-7. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES