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
. 1983 Sep;80(18):5475–5479. doi: 10.1073/pnas.80.18.5475

Primary structure of streptococcal Pep M5 protein: Absence of extensive sequence repeats

Belur N Manjula 1, Sheenah M Mische 1, Vincent A Fischetti 1
PMCID: PMC384280  PMID: 16593365

Abstract

Extensive sequence repeats have been observed in a biologically active fragment of type 24 streptococcal M protein, namely Pep M24 [Beachey, E. H., Sayer, J. M. & Kang, A. H. (1978) Proc. Natl. Acad. Sci. USA 75, 3163-3167]. To determine whether such extensive repetition in sequence is a common characteristic of the antiphagocytic streptococcal M proteins, we have determined the sequences of the clostripain peptides of Pep M5, a biologically active fragment of the type 5 M protein that is analogous to Pep M24. These sequences, together with the amino-terminal sequence of the whole molecule, accounted for nearly two thirds of the Pep M5 molecule. However, extensive identical repeats of the kind observed in Pep M24 were not present in Pep M5. Preliminary study of the amino acid sequence analysis of the M protein from type 6 Streptococcus has also indicated the absence of sequence repeats within the regions of this molecule examined so far. These results suggest that extensive sequence repeats may not be a common characteristic of M-protein molecules. On the other hand, the seven-residue periodicity of the nonpolar residues, a characteristic of α-helical coiled-coil structures, appeared to extend over most of the Pep M5 molecule. This feature has been observed previously for the partial sequences of three M protein serotypes. Thus, the important element of the M-protein structure appears to be the seven-residue periodicity necessary for the maintenance of the coiled-coil structure rather than extensive identical amino acid sequence repeats.

Keywords: seven-residue periodicity, coiled-coil structure, antiphagocytic effect

Full text

PDF
5479

Selected References

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

  1. Beachey E. H., Seyer J. M., Kang A. H. Primary structure of protective antigens of type 24 streptococcal M protein. J Biol Chem. 1980 Jul 10;255(13):6284–6289. [PubMed] [Google Scholar]
  2. Beachey E. H., Seyer J. M., Kang A. H. Repeating covalent structure of streptococcal M protein. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3163–3167. doi: 10.1073/pnas.75.7.3163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Fischetti V. A., Gotschlich E. C., Siviglia G., Zabriskie J. B. Streptococcal M protein extracted by nonionic detergent. I. Properties of the antiphagocytic and type-specific molecules. J Exp Med. 1976 Jul 1;144(1):32–53. doi: 10.1084/jem.144.1.32. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fischetti V. A. Requirements for the opsonic activity of human IgG directed to type 6 group A streptococci: net basic charge and intact Fc region. J Immunol. 1983 Feb;130(2):896–902. [PubMed] [Google Scholar]
  5. Fischetti V. A. Streptococcal M protein extracted by nonionic detergent. III. Correlation between immunological cross-reactions and structural similarities with implications for antiphagocytosis. J Exp Med. 1978 Jun 1;147(6):1771–1778. doi: 10.1084/jem.147.6.1771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fox E. N. M proteins of group A streptococci. Bacteriol Rev. 1974 Mar;38(1):57–86. doi: 10.1128/br.38.1.57-86.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hodges R. S., Saund A. K., Chong P. C., St-Pierre S. A., Reid R. E. Synthetic model for two-stranded alpha-helical coiled-coils. Design, synthesis, and characterization of an 86-residue analog of tropomyosin. J Biol Chem. 1981 Feb 10;256(3):1214–1224. [PubMed] [Google Scholar]
  8. Hosein B., McCarty M., Fischetti V. A. Amino acid sequence and physicochemical similarities between streptococcal M protein and mammalian tropomyosin. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3765–3768. doi: 10.1073/pnas.76.8.3765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Klapper D. G., Wilde C. E., 3rd, Capra J. D. Automated amino acid sequence of small peptides utilizing Polybrene. Anal Biochem. 1978 Mar;85(1):126–131. doi: 10.1016/0003-2697(78)90282-8. [DOI] [PubMed] [Google Scholar]
  10. LANCEFIELD R. C. Current knowledge of type-specific M antigens of group A streptococci. J Immunol. 1962 Sep;89:307–313. [PubMed] [Google Scholar]
  11. Manjula B. N., Fischetti V. A. Studies on group A streptococcal M-proteins: purification of type 5 M-protein and comparison of its amino terminal sequence with two immunologically unrelated M-protein molecules. J Immunol. 1980 Jan;124(1):261–267. [PubMed] [Google Scholar]
  12. Manjula B. N., Fischetti V. A. Tropomyosin-like seven residue periodicity in three immunologically distinct streptococal M proteins and its implications for the antiphagocytic property of the molecule. J Exp Med. 1980 Mar 1;151(3):695–708. doi: 10.1084/jem.151.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McLachlan A. D., Karn J. Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature. 1982 Sep 16;299(5880):226–231. doi: 10.1038/299226a0. [DOI] [PubMed] [Google Scholar]
  14. Mitchell W. M. Cleavage at arginine residues by clostripain. Methods Enzymol. 1977;47:165–170. doi: 10.1016/0076-6879(77)47020-4. [DOI] [PubMed] [Google Scholar]
  15. Phillips G. N., Jr, Flicker P. F., Cohen C., Manjula B. N., Fischetti V. A. Streptococcal M protein: alpha-helical coiled-coil structure and arrangement on the cell surface. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4689–4693. doi: 10.1073/pnas.78.8.4689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Seyer J. M., Kang A. H., Beachey E. H. Primary structural similarities between types 5 and 24 M proteins of Streptococcus pyogenes. Biochem Biophys Res Commun. 1980 Jan 29;92(2):546–553. doi: 10.1016/0006-291x(80)90368-x. [DOI] [PubMed] [Google Scholar]
  17. Simpson R. J., Neuberger M. R., Liu T. Y. Complete amino acid analysis of proteins from a single hydrolysate. J Biol Chem. 1976 Apr 10;251(7):1936–1940. [PubMed] [Google Scholar]
  18. Swanson J., Hsu K. C., Gotschlich E. C. Electron microscopic studies on streptococci. I. M antigen. J Exp Med. 1969 Nov 1;130(5):1063–1091. doi: 10.1084/jem.130.5.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ward C. W., Dopheide T. A. Influenza virus haemagglutinin. Structural predictions suggest that the fibrillar appearance is due to the presence of a coiled-coil. Aust J Biol Sci. 1980 Aug;33(4):441–447. doi: 10.1071/bi9800441. [DOI] [PubMed] [Google Scholar]
  20. Zimmerman C. L., Appella E., Pisano J. J. Rapid analysis of amino acid phenylthiohydantoins by high-performance liquid chromatography. Anal Biochem. 1977 Feb;77(2):569–573. doi: 10.1016/0003-2697(77)90276-7. [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