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
. 1985 Jan;82(1):29–33. doi: 10.1073/pnas.82.1.29

Thioredoxin is required for filamentous phage assembly.

M Russel, P Model
PMCID: PMC396964  PMID: 3881756

Abstract

Sequence comparisons show that the fip gene product of Escherichia coli, which is required for filamentous phage assembly, is thioredoxin. Thioredoxin serves as a cofactor for reductive processes in many cell types and is a constituent of phage T7 DNA polymerase. The fip-1 mutation makes filamentous phage and T7 growth temperature sensitive in cells that carry it. The lesion lies within a highly conserved thioredoxin active site. Thioredoxin reductase (NADPH), as well as thioredoxin, is required for efficient filamentous phage production. Mutant phages defective in phage gene I are particularly sensitive to perturbations in the fip-thioredoxin system. A speculative model is presented in which thioredoxin reductase, thioredoxin, and the gene I protein interact to drive an engine for filamentous phage assembly.

Full text

PDF

Images in this article

30Image
on p.30
30Image
on p.30

Selected References

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

  1. Adler S., Modrich P. T7-induced DNA polymerase. Requirement for thioredoxin sulfhydryl groups. J Biol Chem. 1983 Jun 10;258(11):6956–6962. [PubMed] [Google Scholar]
  2. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boeke J. D. One and two codon insertion mutants of bacteriophage f1. Mol Gen Genet. 1981;181(3):288–291. doi: 10.1007/BF00425599. [DOI] [PubMed] [Google Scholar]
  4. Boeke J. D., Russel M., Model P. Processing of filamentous phage pre-coat protein. Effect of sequence variations near the signal peptidase cleavage site. J Mol Biol. 1980 Dec 5;144(2):103–116. doi: 10.1016/0022-2836(80)90027-3. [DOI] [PubMed] [Google Scholar]
  5. Brown S., Albrechtsen B., Pedersen S., Klemm P. Localization and regulation of the structural gene for transcription-termination factor rho of Escherichia coli. J Mol Biol. 1982 Dec 5;162(2):283–298. doi: 10.1016/0022-2836(82)90527-7. [DOI] [PubMed] [Google Scholar]
  6. Chamberlin M. Isolation and characterization of prototrophic mutants of Escherichia coli unable to support the intracellular growth of T7. J Virol. 1974 Sep;14(3):509–516. doi: 10.1128/jvi.14.3.509-516.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fuchs J. Isolation of an Escherichia coli mutant deficient in thioredoxin reductase. J Bacteriol. 1977 Feb;129(2):967–972. doi: 10.1128/jb.129.2.967-972.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gorini L., Beckwith J. R. Suppression. Annu Rev Microbiol. 1966;20:401–422. doi: 10.1146/annurev.mi.20.100166.002153. [DOI] [PubMed] [Google Scholar]
  9. Grant R. A., Webster R. E. Minor protein content of the gene V protein/phage single-stranded DNA complex of the filamentous bacteriophage f1. Virology. 1984 Mar;133(2):315–328. doi: 10.1016/0042-6822(84)90398-2. [DOI] [PubMed] [Google Scholar]
  10. Grippo J. F., Tienrungroj W., Dahmer M. K., Housley P. R., Pratt W. B. Evidence that the endogenous heat-stable glucocorticoid receptor-activating factor is thioredoxin. J Biol Chem. 1983 Nov 25;258(22):13658–13664. [PubMed] [Google Scholar]
  11. Hill D. F., Petersen G. B. Nucleotide sequence of bacteriophage f1 DNA. J Virol. 1982 Oct;44(1):32–46. doi: 10.1128/jvi.44.1.32-46.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Holmgren A. Glutathione-dependent synthesis of deoxyribonucleotides. Characterization of the enzymatic mechanism of Escherichia coli glutaredoxin. J Biol Chem. 1979 May 10;254(9):3672–3678. [PubMed] [Google Scholar]
  13. Holmgren A. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2275–2279. doi: 10.1073/pnas.73.7.2275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Holmgren A., Kallis G. B., Nordström B. A mutant thioredoxin from Escherichia coli tsnC 7007 that is nonfunctional as subunit of phage T7 DNA polymerase. J Biol Chem. 1981 Mar 25;256(6):3118–3124. [PubMed] [Google Scholar]
  15. Holmgren A., Ohlsson I., Grankvist M. L. Thiroedoxin from Escherichia coli. Radioimmunological and enzymatic determinations in wild type cells and mutants defective in phage T7 DNA replication. J Biol Chem. 1978 Jan 25;253(2):430–436. [PubMed] [Google Scholar]
  16. Holmgren A. Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem. 1979 Oct 10;254(19):9627–9632. [PubMed] [Google Scholar]
  17. Holmgren A. Thioredoxin. 6. The amino acid sequence of the protein from escherichia coli B. Eur J Biochem. 1968 Dec 5;6(4):475–484. doi: 10.1111/j.1432-1033.1968.tb00470.x. [DOI] [PubMed] [Google Scholar]
  18. Hutcheson S. W., Buchanan B. B. Enzyme Regulation in Crassulacean Acid Metabolism Photosynthesis : Studies on Thioredoxin-Linked Enzymes of KalanchoE daigremontiana. Plant Physiol. 1983 Jul;72(3):877–885. doi: 10.1104/pp.72.3.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jacquot J. P., Gadal P., Nishizawa A. N., Yee B. C., Crawford N. A., Buchanan B. B. Enzyme regulation in C4 photosynthesis: mechanism of activation of NADP-malate dehydrogenase by reduced thioredoxin. Arch Biochem Biophys. 1984 Jan;228(1):170–178. doi: 10.1016/0003-9861(84)90058-4. [DOI] [PubMed] [Google Scholar]
  20. Lunn C. A., Pigiet V. P. Localization of thioredoxin from Escherichia coli in an osmotically sensitive compartment. J Biol Chem. 1982 Oct 10;257(19):11424–11430. [PubMed] [Google Scholar]
  21. Mark D. F., Chase J. W., Richardson C. C. Genetic mapping of trxA, a gene affecting thioredoxin in Escherichia coli K12. Mol Gen Genet. 1977 Oct 20;155(2):145–152. doi: 10.1007/BF00393153. [DOI] [PubMed] [Google Scholar]
  22. Mark D. F., Richardson C. C. Escherichia coli thioredoxin: a subunit of bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1976 Mar;73(3):780–784. doi: 10.1073/pnas.73.3.780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Martinez H. M. An efficient method for finding repeats in molecular sequences. Nucleic Acids Res. 1983 Jul 11;11(13):4629–4634. doi: 10.1093/nar/11.13.4629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Meng M., Hogenkamp H. P. Purification, characterization, and amino acid sequence of thioredoxin from Corynebacterium nephridii. J Biol Chem. 1981 Sep 10;256(17):9174–9182. [PubMed] [Google Scholar]
  25. Nygren H., Rozell B., Holmgren A., Hansson H. A. Immunoelectron microscopic localization of glutaredoxin and thioredoxin in Escherichia coli cells. FEBS Lett. 1981 Oct 12;133(1):145–150. doi: 10.1016/0014-5793(81)80492-9. [DOI] [PubMed] [Google Scholar]
  26. Russel M., Model P. A bacterial gene, fip, required for filamentous bacteriophage fl assembly. J Bacteriol. 1983 Jun;154(3):1064–1076. doi: 10.1128/jb.154.3.1064-1076.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Russel M., Model P. Characterization of the cloned fip gene and its product. J Bacteriol. 1984 Feb;157(2):526–532. doi: 10.1128/jb.157.2.526-532.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Russel M., Model P. Replacement of the fip gene of Escherichia coli by an inactive gene cloned on a plasmid. J Bacteriol. 1984 Sep;159(3):1034–1039. doi: 10.1128/jb.159.3.1034-1039.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tsang M. L., Schiff J. A. Assimilatory sulfate reduction in an Escherichia coli mutant lacking thioredoxin activity. J Bacteriol. 1978 Apr;134(1):131–138. doi: 10.1128/jb.134.1.131-138.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. WALLER J. P. THE NH2-TERMINAL RESIDUES OF THE PROTEINS FROM CELL-FREE EXTRACTS OF E. COLI. J Mol Biol. 1963 Nov;7:483–496. doi: 10.1016/s0022-2836(63)80096-0. [DOI] [PubMed] [Google Scholar]
  32. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Zinder N. D., Boeke J. D. The filamentous phage (Ff) as vectors for recombinant DNA--a review. Gene. 1982 Jul-Aug;19(1):1–10. doi: 10.1016/0378-1119(82)90183-4. [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