Nothing Special   »   [go: up one dir, main page]
Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Apr;173(8):2617–2624. doi: 10.1128/jb.173.8.2617-2624.1991

Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems.

J Perez-Casal 1, M G Caparon 1, J R Scott 1
PMCID: PMC207828  PMID: 1849511

Abstract

In the Streptococcus pyogenes M6 strain D471, an insertion of the conjugative transposon Tn916 into a region 2 kb upstream of the promoter of emm6 (the structural gene for the M protein) rendered the strain M negative (M. G. Caparon and J. R. Scott, Proc. Natl. Acad. Sci. USA 84:8677-8681, 1987). In the present work, we show that this insertion mutation, mry-1, is 244 bp upstream of an open reading frame encoding a protein we call Mry. This protein is visible on a gel after transcription and translation in vitro. We have developed a technique for complementation analysis in S. pyogenes and have used it to show that the wild-type mry gene is dominant to two mutant alleles. This dominance indicates that Mry acts in trans as a positive regulator of the emm6 gene. The translated DNA sequence of mry has two regions of similarity to the motif common to the receptor protein of two-component regulatory systems. In addition, the N terminus of Mry has two regions resembling a helix-turn-helix motif. Mry does not appear to be a global regulator of virulence determinants in the group A streptococcus because there is no effect of the mry-1 mutation on production of the hyaluronic acid capsule or streptokinase.

Full text

PDF
2617

Images in this article

2619Image
on p.2619
2621Image
on p.2621

Selected References

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

  1. Albright L. M., Huala E., Ausubel F. M. Prokaryotic signal transduction mediated by sensor and regulator protein pairs. Annu Rev Genet. 1989;23:311–336. doi: 10.1146/annurev.ge.23.120189.001523. [DOI] [PubMed] [Google Scholar]
  2. Aricó B., Miller J. F., Roy C., Stibitz S., Monack D., Falkow S., Gross R., Rappuoli R. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6671–6675. doi: 10.1073/pnas.86.17.6671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bartter T., Dascal A., Carroll K., Curley F. J. 'Toxic strep syndrome'. A manifestation of group A streptococcal infection. Arch Intern Med. 1988 Jun;148(6):1421–1424. doi: 10.1001/archinte.148.6.1421. [DOI] [PubMed] [Google Scholar]
  4. Björck L., Akesson P., Bohus M., Trojnar J., Abrahamson M., Olafsson I., Grubb A. Bacterial growth blocked by a synthetic peptide based on the structure of a human proteinase inhibitor. Nature. 1989 Jan 26;337(6205):385–386. doi: 10.1038/337385a0. [DOI] [PubMed] [Google Scholar]
  5. Caparon M. G., Scott J. R. Excision and insertion of the conjugative transposon Tn916 involves a novel recombination mechanism. Cell. 1989 Dec 22;59(6):1027–1034. doi: 10.1016/0092-8674(89)90759-9. [DOI] [PubMed] [Google Scholar]
  6. Chassy B. M. A gentle method for the lysis of oral streptococci. Biochem Biophys Res Commun. 1976 Jan 26;68(2):603–608. doi: 10.1016/0006-291x(76)91188-8. [DOI] [PubMed] [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fischetti V. A., Jones K. F., Scott J. R. Size variation of the M protein in group A streptococci. J Exp Med. 1985 Jun 1;161(6):1384–1401. doi: 10.1084/jem.161.6.1384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frey J., Krisch H. M. Omega mutagenesis in gram-negative bacteria: a selectable interposon which is strongly polar in a wide range of bacterial species. Gene. 1985;36(1-2):143–150. doi: 10.1016/0378-1119(85)90078-2. [DOI] [PubMed] [Google Scholar]
  10. Gold L., Pribnow D., Schneider T., Shinedling S., Singer B. S., Stormo G. Translational initiation in prokaryotes. Annu Rev Microbiol. 1981;35:365–403. doi: 10.1146/annurev.mi.35.100181.002053. [DOI] [PubMed] [Google Scholar]
  11. Gross R., Aricò B., Rappuoli R. Families of bacterial signal-transducing proteins. Mol Microbiol. 1989 Nov;3(11):1661–1667. doi: 10.1111/j.1365-2958.1989.tb00152.x. [DOI] [PubMed] [Google Scholar]
  12. Haanes-Fritz E., Kraus W., Burdett V., Dale J. B., Beachey E. H., Cleary P. Comparison of the leader sequences of four group A streptococcal M protein genes. Nucleic Acids Res. 1988 May 25;16(10):4667–4677. doi: 10.1093/nar/16.10.4667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harrison S. C., Aggarwal A. K. DNA recognition by proteins with the helix-turn-helix motif. Annu Rev Biochem. 1990;59:933–969. doi: 10.1146/annurev.bi.59.070190.004441. [DOI] [PubMed] [Google Scholar]
  14. Hollingshead S. K., Fischetti V. A., Scott J. R. Complete nucleotide sequence of type 6 M protein of the group A Streptococcus. Repetitive structure and membrane anchor. J Biol Chem. 1986 Feb 5;261(4):1677–1686. [PubMed] [Google Scholar]
  15. Jin S., Roitsch T., Ankenbauer R. G., Gordon M. P., Nester E. W. The VirA protein of Agrobacterium tumefaciens is autophosphorylated and is essential for vir gene regulation. J Bacteriol. 1990 Feb;172(2):525–530. doi: 10.1128/jb.172.2.525-530.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jones K. F., Manjula B. N., Johnston K. H., Hollingshead S. K., Scott J. R., Fischetti V. A. Location of variable and conserved epitopes among the multiple serotypes of streptococcal M protein. J Exp Med. 1985 Mar 1;161(3):623–628. doi: 10.1084/jem.161.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Malke H., Ferretti J. J. Streptokinase: cloning, expression, and excretion by Escherichia coli. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3557–3561. doi: 10.1073/pnas.81.11.3557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McLaughlin J. R., Murray C. L., Rabinowitz J. C. Unique features in the ribosome binding site sequence of the gram-positive Staphylococcus aureus beta-lactamase gene. J Biol Chem. 1981 Nov 10;256(21):11283–11291. [PubMed] [Google Scholar]
  19. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  20. Miller J. F., Mekalanos J. J., Falkow S. Coordinate regulation and sensory transduction in the control of bacterial virulence. Science. 1989 Feb 17;243(4893):916–922. doi: 10.1126/science.2537530. [DOI] [PubMed] [Google Scholar]
  21. Miller V. L., Taylor R. K., Mekalanos J. J. Cholera toxin transcriptional activator toxR is a transmembrane DNA binding protein. Cell. 1987 Jan 30;48(2):271–279. doi: 10.1016/0092-8674(87)90430-2. [DOI] [PubMed] [Google Scholar]
  22. Norgren M., Caparon M. G., Scott J. R. A method for allelic replacement that uses the conjugative transposon Tn916: deletion of the emm6.1 allele in Streptococcus pyogenes JRS4. Infect Immun. 1989 Dec;57(12):3846–3850. doi: 10.1128/iai.57.12.3846-3850.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Peng H. L., Novick R. P., Kreiswirth B., Kornblum J., Schlievert P. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol. 1988 Sep;170(9):4365–4372. doi: 10.1128/jb.170.9.4365-4372.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Powell B. S., Rogowsky P. M., Kado C. I. virG of Agrobacterium tumefaciens plasmid pTiC58 encodes a DNA-binding protein. Mol Microbiol. 1989 Mar;3(3):411–419. doi: 10.1111/j.1365-2958.1989.tb00186.x. [DOI] [PubMed] [Google Scholar]
  26. Robbins J. C., Spanier J. G., Jones S. J., Simpson W. J., Cleary P. P. Streptococcus pyogenes type 12 M protein gene regulation by upstream sequences. J Bacteriol. 1987 Dec;169(12):5633–5640. doi: 10.1128/jb.169.12.5633-5640.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Scott J. R. A turbid plaque-forming mutant of phage P1 that cannot lysogenize Escherichia coli. Virology. 1974 Dec;62(2):344–349. doi: 10.1016/0042-6822(74)90397-3. [DOI] [PubMed] [Google Scholar]
  29. Simpson W. J., LaPenta D., Chen C., Cleary P. P. Coregulation of type 12 M protein and streptococcal C5a peptidase genes in group A streptococci: evidence for a virulence regulon controlled by the virR locus. J Bacteriol. 1990 Feb;172(2):696–700. doi: 10.1128/jb.172.2.696-700.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Spanier J. G., Jones S. J., Cleary P. Small DNA deletions creating avirulence in Streptococcus pyogenes. Science. 1984 Aug 31;225(4665):935–938. doi: 10.1126/science.6089334. [DOI] [PubMed] [Google Scholar]
  31. Stevens D. L., Tanner M. H., Winship J., Swarts R., Ries K. M., Schlievert P. M., Kaplan E. Severe group A streptococcal infections associated with a toxic shock-like syndrome and scarlet fever toxin A. N Engl J Med. 1989 Jul 6;321(1):1–7. doi: 10.1056/NEJM198907063210101. [DOI] [PubMed] [Google Scholar]
  32. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Svensson M., Christensen P., Schalén D. Monoclonal opsonic mouse antibodies specific for streptococcal IgG Fc-receptor. J Med Microbiol. 1986 Nov;22(3):251–256. doi: 10.1099/00222615-22-3-251. [DOI] [PubMed] [Google Scholar]
  34. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  35. Trieu-Cuot P., Courvalin P. Nucleotide sequence of the Streptococcus faecalis plasmid gene encoding the 3'5"-aminoglycoside phosphotransferase type III. Gene. 1983 Sep;23(3):331–341. doi: 10.1016/0378-1119(83)90022-7. [DOI] [PubMed] [Google Scholar]
  36. WILSON A. T. The relative importance of the capsule and the M-antigen in determining colony form of group A streptococci. J Exp Med. 1959 Mar 1;109(3):257–270. doi: 10.1084/jem.109.3.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wexler D. E., Nelson R. D., Cleary P. P. Human neutrophil chemotactic response to group A streptococci: bacteria-mediated interference with complement-derived chemotactic factors. Infect Immun. 1983 Jan;39(1):239–246. doi: 10.1128/iai.39.1.239-246.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Whitnack E., Bisno A. L., Beachey E. H. Hyaluronate capsule prevents attachment of group A streptococci to mouse peritoneal macrophages. Infect Immun. 1981 Mar;31(3):985–991. doi: 10.1128/iai.31.3.985-991.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES