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. 1989 Jun;86(11):3973–3977. doi: 10.1073/pnas.86.11.3973

Activation of prophage P4 by the P2 Cox protein and the sites of action of the Cox protein on the two phage genomes.

S Saha 1, E Haggård-Ljungquist 1, K Nordström 1
PMCID: PMC287370  PMID: 2657731

Abstract

Phage P2 induces the unrelated prophage P4. In this paper we show that this is due to the activation of the P4 late promoter PII by the P2 Cox protein. This is in contrast to the effects of Cox on P2, for which it is known from previous work that it acts as a repressor of the promoter Pc, which is responsible for expression of the immunity repressor C. The activator role of Cox was revealed by its effect on replication of P4 DNA and on the formation of chloramphenicol acetyltransferase when a promoterless cat gene was inserted downstream of the P4 PII promoter. DNase I protection studies revealed that the Cox protein binds to the repressor promoter Pc of phage P2 and to the promoter PII of phage P4. In the latter case the Cox protein binds upstream of the -35 region, in analogy to several other activators of promoters. A weak binding was found in the promoters Pe of phage P2 and Ple of phage P4. The Cox protein is a case of viral transactivation of the replication genes of one phage by a control protein of the other. However, the effects of the Cox protein are totally different in the two phages, repressive in one case and activating in the other.

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Selected References

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

  1. Alano P., Dehò G., Sironi G., Zangrossi S. Regulation of the plasmid state of the genetic element P4. Mol Gen Genet. 1986 Jun;203(3):445–450. doi: 10.1007/BF00422069. [DOI] [PubMed] [Google Scholar]
  2. Arya S. K., Guo C., Josephs S. F., Wong-Staal F. Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science. 1985 Jul 5;229(4708):69–73. doi: 10.1126/science.2990040. [DOI] [PubMed] [Google Scholar]
  3. BERTANI G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol. 1951 Sep;62(3):293–300. doi: 10.1128/jb.62.3.293-300.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barrett K. J., Gibbs W., Calendar R. A transcribing activity induced by satellite phage P4. Proc Natl Acad Sci U S A. 1972 Oct;69(10):2986–2990. doi: 10.1073/pnas.69.10.2986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berns K. I., Labow M. A. Parvovirus gene regulation. J Gen Virol. 1987 Mar;68(Pt 3):601–614. doi: 10.1099/0022-1317-68-3-601. [DOI] [PubMed] [Google Scholar]
  6. Bertani L. E. Genetic interaction between the nip1 mutation and genes affecting integration and excision in phage P2. Mol Gen Genet. 1980 Apr;178(1):91–99. doi: 10.1007/BF00267217. [DOI] [PubMed] [Google Scholar]
  7. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  8. Brosius J. Plasmid vectors for the selection of promoters. Gene. 1984 Feb;27(2):151–160. doi: 10.1016/0378-1119(84)90136-7. [DOI] [PubMed] [Google Scholar]
  9. Calendar R., Ljungquist E., Deho G., Usher D. C., Goldstein R., Youderian P., Sironi G., Six E. W. Lysogenization by satellite phage P4. Virology. 1981 Aug;113(1):20–38. doi: 10.1016/0042-6822(81)90133-1. [DOI] [PubMed] [Google Scholar]
  10. Dehó G., Zangrossi S., Ghisotti D., Sironi G. Alternative promoters in the development of bacteriophage plasmid P4. J Virol. 1988 May;62(5):1697–1704. doi: 10.1128/jvi.62.5.1697-1704.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Diana C., Dehò G., Geisselsoder J., Tinelli L., Goldstein R. Viral interference at the level of capsid size determination by satellite phage P4. J Mol Biol. 1978 Dec 15;126(3):433–445. doi: 10.1016/0022-2836(78)90050-5. [DOI] [PubMed] [Google Scholar]
  12. Felber B. K., Paskalis H., Kleinman-Ewing C., Wong-Staal F., Pavlakis G. N. The pX protein of HTLV-I is a transcriptional activator of its long terminal repeats. Science. 1985 Aug 16;229(4714):675–679. doi: 10.1126/science.2992082. [DOI] [PubMed] [Google Scholar]
  13. Geisselsoder J., Youdarian P., Dehò G., Chidambaram M., Goldstein R., Ljungquist E. Mutants of satellite virus P4 that cannot derepress their bacteriophage P2 helper. J Mol Biol. 1981 May 5;148(1):1–19. doi: 10.1016/0022-2836(81)90232-1. [DOI] [PubMed] [Google Scholar]
  14. Goosen N., van de Putte P. Role of ner protein in bacteriophage Mu transposition. J Bacteriol. 1986 Aug;167(2):503–507. doi: 10.1128/jb.167.2.503-507.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gottesman M. E., Adhya S., Das A. Transcription antitermination by bacteriophage lambda N gene product. J Mol Biol. 1980 Jun 15;140(1):57–75. doi: 10.1016/0022-2836(80)90356-3. [DOI] [PubMed] [Google Scholar]
  17. Heaphy S., Singh M., Gait M. J. Effect of single amino acid changes in the region of the adenylylation site of T4 RNA ligase. Biochemistry. 1987 Mar 24;26(6):1688–1696. doi: 10.1021/bi00380a030. [DOI] [PubMed] [Google Scholar]
  18. Larsen J. E., Gerdes K., Light J., Molin S. Low-copy-number plasmid-cloning vectors amplifiable by derepression of an inserted foreign promoter. Gene. 1984 Apr;28(1):45–54. doi: 10.1016/0378-1119(84)90086-6. [DOI] [PubMed] [Google Scholar]
  19. Lin C. S. Nucleotide sequence of the essential region of bacteriophage P4. Nucleic Acids Res. 1984 Nov 26;12(22):8667–8684. doi: 10.1093/nar/12.22.8667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lindahl G., Hirota Y., Jacob F. On the process of cellular division in Escherichia coli: replication of the bacterial chromosome under control of prophage P2. Proc Natl Acad Sci U S A. 1971 Oct;68(10):2407–2411. doi: 10.1073/pnas.68.10.2407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lindahl G., Sunshine M. Excision-deficient mutants of bacteriophage P2. Virology. 1972 Jul;49(1):180–187. doi: 10.1016/s0042-6822(72)80019-9. [DOI] [PubMed] [Google Scholar]
  22. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  23. Norrander J., Kempe T., Messing J. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene. 1983 Dec;26(1):101–106. doi: 10.1016/0378-1119(83)90040-9. [DOI] [PubMed] [Google Scholar]
  24. Ptashne M., Jeffrey A., Johnson A. D., Maurer R., Meyer B. J., Pabo C. O., Roberts T. M., Sauer R. T. How the lambda repressor and cro work. Cell. 1980 Jan;19(1):1–11. doi: 10.1016/0092-8674(80)90383-9. [DOI] [PubMed] [Google Scholar]
  25. Saha S., Haggård-Ljungquist E., Nordström K. The cox protein of bacteriophage P2 inhibits the formation of the repressor protein and autoregulates the early operon. EMBO J. 1987 Oct;6(10):3191–3199. doi: 10.1002/j.1460-2075.1987.tb02631.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Saha S., Lundqvist B., Haggård-Ljungquist E. Autoregulation of bacteriophage P2 repressor. EMBO J. 1987 Mar;6(3):809–814. doi: 10.1002/j.1460-2075.1987.tb04823.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shigesada K., Tsurushita N., Matsumoto Y., Imai M. Overproduction of transcription termination factor Rho in Escherichia coli. Gene. 1984 Jul-Aug;29(1-2):199–209. doi: 10.1016/0378-1119(84)90180-x. [DOI] [PubMed] [Google Scholar]
  28. Shore D., Dehò G., Tsipis J., Goldstein R. Determination of capsid size by satellite bacteriophage P4. Proc Natl Acad Sci U S A. 1978 Jan;75(1):400–404. doi: 10.1073/pnas.75.1.400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Six E. W., Klug C. A. Bacteriophage P4: a satellite virus depending on a helper such as prophage P2. Virology. 1973 Feb;51(2):327–344. doi: 10.1016/0042-6822(73)90432-7. [DOI] [PubMed] [Google Scholar]
  30. Six E. W., Lindqvist B. H. Mutual derepression in the P2-P4 bacteriophage system. Virology. 1978 Jun 15;87(2):217–230. doi: 10.1016/0042-6822(78)90127-7. [DOI] [PubMed] [Google Scholar]
  31. Sodroski J., Rosen C., Goh W. C., Haseltine W. A transcriptional activator protein encoded by the x-lor region of the human T-cell leukemia virus. Science. 1985 Jun 21;228(4706):1430–1434. doi: 10.1126/science.2990028. [DOI] [PubMed] [Google Scholar]
  32. Souza L., Calendar R., Six E. W., Lindqvist B. H. A transactivation mutant of satellite phage P4. Virology. 1977 Aug;81(1):81–90. doi: 10.1016/0042-6822(77)90060-5. [DOI] [PubMed] [Google Scholar]
  33. Sunshine M. G., Sauer B. A bacterial mutation blocking P2 phage late gene expression. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2770–2774. doi: 10.1073/pnas.72.7.2770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Thomas R. Control of development in temperate bacteriophages. 3. Which prophage genes are and which are not trans-activable in the presence of immunity? J Mol Biol. 1970 Apr 28;49(2):393–404. doi: 10.1016/0022-2836(70)90252-4. [DOI] [PubMed] [Google Scholar]

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