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. 1991 Aug;59(8):2677–2685. doi: 10.1128/iai.59.8.2677-2685.1991

Sequence and structural analysis of surface protein antigen I/II (SpaA) of Streptococcus sobrinus.

R J LaPolla 1, J A Haron 1, C G Kelly 1, W R Taylor 1, C Bohart 1, M Hendricks 1, J P Pyati 1, R T Graff 1, J K Ma 1, T Lehner 1
PMCID: PMC258073  PMID: 1855987

Abstract

Streptococcal antigen I/II or the surface protein antigen A (SpaA) of Streptococcus sobrinus is an adhesin which mediates binding of the organism to tooth surfaces. The complete sequence of the gene which encodes SpaA has been determined. The gene consists of 4,584 bp and encodes a protein of 1,528 amino acid residues. The deduced amino acid sequence shows extensive homology with those of the cell surface adhesins from Streptococcus mutans serotypes c and f and from Streptococcus sanguis. Structural analysis of the N-terminal region (residues 50 to 550), which is rich in alanine and includes four tandem repeats of an 82-residue sequence, suggests that it adopts an alpha-helical coiled-coil conformation. Cell surface hydrophobicity may be associated with this region. The C-terminal region is more conserved and includes two tandem repeats of a 39-residue proline-rich sequence. A further proline-rich sequence in this region is predicted to span the cell wall. Although a hydrophobic sequence is present in the C-terminal region, it appears to be too short to span the cell membrane. Anchoring of SpaA in the cell membrane may therefore require some form of posttranslational modification or association with another membrane protein.

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Selected References

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

  1. Abiko Y., Hayakawa M., Aoki H., Saito S., Takiguchi H. Cloning of the gene for cell-surface protein antigen A from Streptococcus sobrinus (serotype d). Arch Oral Biol. 1989;34(7):571–575. doi: 10.1016/0003-9969(89)90096-4. [DOI] [PubMed] [Google Scholar]
  2. Acharya R., Fry E., Stuart D., Fox G., Rowlands D., Brown F. The three-dimensional structure of foot-and-mouth disease virus at 2.9 A resolution. Nature. 1989 Feb 23;337(6209):709–716. doi: 10.1038/337709a0. [DOI] [PubMed] [Google Scholar]
  3. Barlow D. J., Thornton J. M. Helix geometry in proteins. J Mol Biol. 1988 Jun 5;201(3):601–619. doi: 10.1016/0022-2836(88)90641-9. [DOI] [PubMed] [Google Scholar]
  4. Beighton D., Manji F., Baelum V., Fejerskov O., Johnson N. W., Wilton J. M. Associations between salivary levels of Streptococcus mutans, Streptococcus sobrinus, lactobacilli, and caries experience in Kenyan adolescents. J Dent Res. 1989 Aug;68(8):1242–1246. doi: 10.1177/00220345890680080601. [DOI] [PubMed] [Google Scholar]
  5. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [DOI] [PubMed] [Google Scholar]
  6. Cohen C., Parry D. A. Alpha-helical coiled coils and bundles: how to design an alpha-helical protein. Proteins. 1990;7(1):1–15. doi: 10.1002/prot.340070102. [DOI] [PubMed] [Google Scholar]
  7. Demuth D. R., Davis C. A., Corner A. M., Lamont R. J., Leboy P. S., Malamud D. Cloning and expression of a Streptococcus sanguis surface antigen that interacts with a human salivary agglutinin. Infect Immun. 1988 Sep;56(9):2484–2490. doi: 10.1128/iai.56.9.2484-2490.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Demuth D. R., Golub E. E., Malamud D. Streptococcal-host interactions. Structural and functional analysis of a Streptococcus sanguis receptor for a human salivary glycoprotein. J Biol Chem. 1990 May 5;265(13):7120–7126. [PubMed] [Google Scholar]
  9. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  10. Forester H., Hunter N., Knox K. W. Characteristics of a high molecular weight extracellular protein of Streptococcus mutans. J Gen Microbiol. 1983 Sep;129(9):2779–2788. doi: 10.1099/00221287-129-9-2779. [DOI] [PubMed] [Google Scholar]
  11. Freymann D. M., Metcalf P., Turner M., Wiley D. C. 6 A-resolution X-ray structure of a variable surface glycoprotein from Trypanosoma brucei. Nature. 1984 Sep 13;311(5982):167–169. doi: 10.1038/311167a0. [DOI] [PubMed] [Google Scholar]
  12. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  13. Gibbons R. J., Cohen L., Hay D. I. Strains of Streptococcus mutans and Streptococcus sobrinus attach to different pellicle receptors. Infect Immun. 1986 May;52(2):555–561. doi: 10.1128/iai.52.2.555-561.1986. [DOI] [PMC free article] [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. Holt R. G., Abiko Y., Saito S., Smorawinska M., Hansen J. B., Curtiss R., 3rd Streptococcus mutans genes that code for extracellular proteins in Escherichia coli K-12. Infect Immun. 1982 Oct;38(1):147–156. doi: 10.1128/iai.38.1.147-156.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jagusztyn-Krynicka E. K., Smorawinska M., Curtiss R., 3rd Expression of Streptococcus mutans aspartate-semialdehyde dehydrogenase gene cloned into plasmid pBR322. J Gen Microbiol. 1982 May;128(5):1135–1145. doi: 10.1099/00221287-128-5-1135. [DOI] [PubMed] [Google Scholar]
  17. Kelly C., Evans P., Bergmeier L., Lee S. F., Progulske-Fox A., Harris A. C., Aitken A., Bleiweis A. S., Lehner T. Sequence analysis of the cloned streptococcal cell surface antigen I/II. FEBS Lett. 1989 Nov 20;258(1):127–132. doi: 10.1016/0014-5793(89)81632-1. [DOI] [PubMed] [Google Scholar]
  18. Lee S. F., Progulske-Fox A., Bleiweis A. S. Molecular cloning and expression of a Streptococcus mutans major surface protein antigen, P1 (I/II), in Escherichia coli. Infect Immun. 1988 Aug;56(8):2114–2119. doi: 10.1128/iai.56.8.2114-2119.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lee S. F., Progulske-Fox A., Erdos G. W., Piacentini D. A., Ayakawa G. Y., Crowley P. J., Bleiweis A. S. Construction and characterization of isogenic mutants of Streptococcus mutans deficient in major surface protein antigen P1 (I/II). Infect Immun. 1989 Nov;57(11):3306–3313. doi: 10.1128/iai.57.11.3306-3313.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lehner T., Caldwell J., Smith R. Local passive immunization by monoclonal antibodies against streptococcal antigen I/II in the prevention of dental caries. Infect Immun. 1985 Dec;50(3):796–799. doi: 10.1128/iai.50.3.796-799.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lehner T., Haron J., Bergmeier L. A., Mehlert A., Beard R., Dodd M., Mielnik B., Moore S. Local oral immunization with synthetic peptides induces a dual mucosal IgG and salivary IgA antibody response and prevents colonization of Streptococcus mutans. Immunology. 1989 Jul;67(3):419–424. [PMC free article] [PubMed] [Google Scholar]
  22. Ma J. K., Hunjan M., Smith R., Lehner T. Specificity of monoclonal antibodies in local passive immunization against Streptococcus mutans. Clin Exp Immunol. 1989 Sep;77(3):331–337. [PMC free article] [PubMed] [Google Scholar]
  23. Ma J. K., Smith R., Lehner T. Use of monoclonal antibodies in local passive immunization to prevent colonization of human teeth by Streptococcus mutans. Infect Immun. 1987 May;55(5):1274–1278. doi: 10.1128/iai.55.5.1274-1278.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Maley F., Guarino D. U. Differential binding of sodium dodecyl sulfate to amino acids as evidenced by elution from Sephadex. Biochem Biophys Res Commun. 1977 Aug 22;77(4):1425–1430. doi: 10.1016/s0006-291x(77)80138-1. [DOI] [PubMed] [Google Scholar]
  25. Manjula B. N., Acharya A. S., Mische S. M., Fairwell T., Fischetti V. A. The complete amino acid sequence of a biologically active 197-residue fragment of M protein isolated from type 5 group A streptococci. J Biol Chem. 1984 Mar 25;259(6):3686–3693. [PubMed] [Google Scholar]
  26. McBride B. C., Song M., Krasse B., Olsson J. Biochemical and immunological differences between hydrophobic and hydrophilic strains of Streptococcus mutans. Infect Immun. 1984 Apr;44(1):68–75. doi: 10.1128/iai.44.1.68-75.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Michaelis S., Beckwith J. Mechanism of incorporation of cell envelope proteins in Escherichia coli. Annu Rev Microbiol. 1982;36:435–465. doi: 10.1146/annurev.mi.36.100182.002251. [DOI] [PubMed] [Google Scholar]
  28. Ogier J. A., Scholler M., Leproivre Y., Pini A., Sommer P., Klein J. P. Complete nucleotide sequence of the sr gene from Streptococcus mutans OMZ 175. FEMS Microbiol Lett. 1990 Mar 1;56(1-2):223–227. doi: 10.1016/0378-1097(90)90155-j. [DOI] [PubMed] [Google Scholar]
  29. Ogundipe J. O., Holt R. G. Molecular and immunochemical characterization of recombinant Escherichia coli containing the spaA gene region of Streptococcus sobrinus. Infect Immun. 1989 Jul;57(7):1906–1915. doi: 10.1128/iai.57.7.1906-1915.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Cloning of a surface protein antigen gene from serotype c Streptococcus mutans. Mol Microbiol. 1989 Feb;3(2):221–228. doi: 10.1111/j.1365-2958.1989.tb01811.x. [DOI] [PubMed] [Google Scholar]
  31. Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Molecular characterization of a surface protein antigen gene from serotype c Streptococcus mutans, implicated in dental caries. Mol Microbiol. 1989 May;3(5):673–678. doi: 10.1111/j.1365-2958.1989.tb00215.x. [DOI] [PubMed] [Google Scholar]
  32. Pancholi V., Fischetti V. A. Identification of an endogenous membrane anchor-cleaving enzyme for group A streptococcal M protein. Its implication for the attachment of surface proteins in gram-positive bacteria. J Exp Med. 1989 Dec 1;170(6):2119–2133. doi: 10.1084/jem.170.6.2119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pancholi V., Fischetti V. A. Isolation and characterization of the cell-associated region of group A streptococcal M6 protein. J Bacteriol. 1988 Jun;170(6):2618–2624. doi: 10.1128/jb.170.6.2618-2624.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Russell M. W., Bergmeier L. A., Zanders E. D., Lehner T. Protein antigens of Streptococcus mutans: purification and properties of a double antigen and its protease-resistant component. Infect Immun. 1980 May;28(2):486–493. doi: 10.1128/iai.28.2.486-493.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Russell M. W., Lehner T. Characterisation of antigens extracted from cells and culture fluids of Streptococcus mutans serotype c. Arch Oral Biol. 1978;23(1):7–15. doi: 10.1016/0003-9969(78)90047-x. [DOI] [PubMed] [Google Scholar]
  36. Russell M. W., Mansson-Rahemtulla B. Interaction between surface protein antigens of Streptococcus mutans and human salivary components. Oral Microbiol Immunol. 1989 Jun;4(2):106–111. doi: 10.1111/j.1399-302x.1989.tb00107.x. [DOI] [PubMed] [Google Scholar]
  37. Russell R. R. Wall-associated protein antigens of Streptococcus mutans. J Gen Microbiol. 1979 Sep;114(1):109–115. doi: 10.1099/00221287-114-1-109. [DOI] [PubMed] [Google Scholar]
  38. Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
  39. 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]
  40. Smith R., Lehner T., Beverley P. C. Characterization of monoclonal antibodies to Streptococcus mutans antigenic determinants I/II, I, II, and III and their serotype specificities. Infect Immun. 1984 Oct;46(1):168–175. doi: 10.1128/iai.46.1.168-175.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith R., Lehner T. Characterisation of monoclonal antibodies to common protein epitopes on the cell surface of Streptococcus mutans and Streptococcus sobrinus. Oral Microbiol Immunol. 1989 Sep;4(3):153–158. doi: 10.1111/j.1399-302x.1989.tb00243.x. [DOI] [PubMed] [Google Scholar]
  42. Sommer P., Bruyère T., Ogier J. A., Garnier J. M., Jeltsch J. M., Klein J. P. Cloning of the saliva-interacting protein gene from Streptococcus mutans. J Bacteriol. 1987 Nov;169(11):5167–5173. doi: 10.1128/jb.169.11.5167-5173.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Staffileno L. K., Hendricks M., LaPolla R., Bohart C., Van Hook P., Rosen J. I., Warner J., Hoey K., Wegemer D., Naso R. B. Cloning of the amino terminal nucleotides of the antigen I/II of Streptococcus sobrinus and the immune responses to the corresponding synthetic peptides. Arch Oral Biol. 1990;35 (Suppl):47S–52S. doi: 10.1016/0003-9969(90)90130-3. [DOI] [PubMed] [Google Scholar]
  44. Steinert P. M., Parry D. A. Intermediate filaments: conformity and diversity of expression and structure. Annu Rev Cell Biol. 1985;1:41–65. doi: 10.1146/annurev.cb.01.110185.000353. [DOI] [PubMed] [Google Scholar]
  45. Takahashi I., Okahashi N., Sasakawa C., Yoshikawa M., Hamada S., Koga T. Homology between surface protein antigen genes of Streptococcus sobrinus and Streptococcus mutans. FEBS Lett. 1989 Jun 5;249(2):383–388. doi: 10.1016/0014-5793(89)80664-7. [DOI] [PubMed] [Google Scholar]
  46. Taylor W. R. A flexible method to align large numbers of biological sequences. J Mol Evol. 1988 Dec;28(1-2):161–169. doi: 10.1007/BF02143508. [DOI] [PubMed] [Google Scholar]
  47. Weber P. C., Salemme F. R. Structural and functional diversity in 4-alpha-helical proteins. Nature. 1980 Sep 4;287(5777):82–84. doi: 10.1038/287082a0. [DOI] [PubMed] [Google Scholar]
  48. Weis W., Brown J. H., Cusack S., Paulson J. C., Skehel J. J., Wiley D. C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature. 1988 Jun 2;333(6172):426–431. doi: 10.1038/333426a0. [DOI] [PubMed] [Google Scholar]
  49. Wilson I. A., Skehel J. J., Wiley D. C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature. 1981 Jan 29;289(5796):366–373. doi: 10.1038/289366a0. [DOI] [PubMed] [Google Scholar]
  50. Winship P. R. An improved method for directly sequencing PCR amplified material using dimethyl sulphoxide. Nucleic Acids Res. 1989 Feb 11;17(3):1266–1266. doi: 10.1093/nar/17.3.1266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. de Jong W. W., Zweers A., Cohen L. H. Influence of single amino acid substitutions on electrophoretic mobility of sodium dodecyl sulfate-protein complexes. Biochem Biophys Res Commun. 1978 May 30;82(2):532–539. doi: 10.1016/0006-291x(78)90907-5. [DOI] [PubMed] [Google Scholar]

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