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. 1997 Dec;65(12):5157–5164. doi: 10.1128/iai.65.12.5157-5164.1997

Invasion of dentinal tubules by oral streptococci is associated with collagen recognition mediated by the antigen I/II family of polypeptides.

R M Love 1, M D McMillan 1, H F Jenkinson 1
PMCID: PMC175743  PMID: 9393810

Abstract

Cell surface proteins SspA and SspB in Streptococcus gordonii and SpaP in Streptococcus mutans are members of the antigen I/II family of polypeptides produced by oral streptococci. These proteins are adhesins and mediate species-specific binding of cells to a variety of host and bacterial receptors. Here we show that antigen I/II polypeptides are involved in the attachment of oral streptococci to collagen and that they also determine the ability of these bacteria to invade human root dentinal tubules. Wild-type S. gordonii DL1 (Challis) cells showed heavy invasion of tubules to a depth of approximately 200 microm, whereas the abilities of cells of isogenic mutant strains OB220 (sspA) and OB219 (sspA sspB) to invade were 50 and >90% reduced, respectively. Likewise, wild-type S. mutans NG8 cells invaded dentinal tubules, whereas cells of isogenic mutant strain 834 (spaP) did not. The invasive abilities of strains OB220 and OB219 were restored by heterologous expression of S. mutans SpaP polypeptide in these strains. The extents of tubule invasion by various wild-type and mutant strains correlated with their levels of adhesion to type I collagen, a major component of dentin. Furthermore, S. gordonii DL1 cells exhibited a growth response to collagen by forming long chains. This was not shown by ssp mutants but was restored by the expression of SpaP in these cells. The production of SspA polypeptide by S. gordonii DL1, but not production of SspB polypeptide by strain OB220 (sspA), was enhanced in the presence of collagen. These results are the first to demonstrate that antigen I/II family polypeptides bind collagen and mediate a morphological growth response of streptococci to collagen. These antigen I/II polypeptide activities are critical for intratubular growth of streptococci and thus for establishment of endodontic infections.

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Selected References

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  1. Akpata E. S., Blechman H. Bacterial invasion of pulpal dentin wall in vitro. J Dent Res. 1982 Feb;61(2):435–438. doi: 10.1177/00220345820610021401. [DOI] [PubMed] [Google Scholar]
  2. Baddour L. M. Virulence factors among gram-positive bacteria in experimental endocarditis. Infect Immun. 1994 Jun;62(6):2143–2148. doi: 10.1128/iai.62.6.2143-2148.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beighton D., Lynch E. Comparison of selected microflora of plaque and underlying carious dentine associated with primary root caries lesions. Caries Res. 1995;29(2):154–158. doi: 10.1159/000262058. [DOI] [PubMed] [Google Scholar]
  4. Bowden G. H., Ekstrand J., McNaughton B., Challacombe S. J. Association of selected bacteria with the lesions of root surface caries. Oral Microbiol Immunol. 1990 Dec;5(6):346–351. doi: 10.1111/j.1399-302x.1990.tb00439.x. [DOI] [PubMed] [Google Scholar]
  5. Brady L. J., Piacentini D. A., Crowley P. J., Bleiweis A. S. Identification of monoclonal antibody-binding domains within antigen P1 of Streptococcus mutans and cross-reactivity with related surface antigens of oral streptococci. Infect Immun. 1991 Dec;59(12):4425–4435. doi: 10.1128/iai.59.12.4425-4435.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dai X. F., Ten Cate A. R., Limeback H. The extent and distribution of intratubular collagen fibrils in human dentine. Arch Oral Biol. 1991;36(10):775–778. doi: 10.1016/0003-9969(91)90045-v. [DOI] [PubMed] [Google Scholar]
  7. Demuth D. R., Berthold P., Leboy P. S., Golub E. E., Davis C. A., Malamud D. Saliva-mediated aggregation of Enterococcus faecalis transformed with a Streptococcus sanguis gene encoding the SSP-5 surface antigen. Infect Immun. 1989 May;57(5):1470–1475. doi: 10.1128/iai.57.5.1470-1475.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Demuth D. R., Duan Y., Brooks W., Holmes A. R., McNab R., Jenkinson H. F. Tandem genes encode cell-surface polypeptides SspA and SspB which mediate adhesion of the oral bacterium Streptococcus gordonii to human and bacterial receptors. Mol Microbiol. 1996 Apr;20(2):403–413. doi: 10.1111/j.1365-2958.1996.tb02627.x. [DOI] [PubMed] [Google Scholar]
  9. Demuth D. R., Duan Y., Jenkinson H. F., McNab R., Gil S., Lamont R. J. Interruption of the Streptococcus gordonii M5 sspA/sspB intergenic region by an insertion sequence related to IS1167 of Streptococcus pneumoniae. Microbiology. 1997 Jun;143(Pt 6):2047–2055. doi: 10.1099/00221287-143-6-2047. [DOI] [PubMed] [Google Scholar]
  10. Erickson P. R., Herzberg M. C. Altered expression of the platelet aggregation-associated protein from Streptococcus sanguis after growth in the presence of collagen. Infect Immun. 1995 Mar;63(3):1084–1088. doi: 10.1128/iai.63.3.1084-1088.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Garberoglio R., Brännström M. Scanning electron microscopic investigation of human dentinal tubules. Arch Oral Biol. 1976;21(6):355–362. doi: 10.1016/s0003-9969(76)80003-9. [DOI] [PubMed] [Google Scholar]
  12. Gillaspy A. F., Patti J. M., Smeltzer M. S. Transcriptional regulation of the Staphylococcus aureus collagen adhesion gene, cna. Infect Immun. 1997 Apr;65(4):1536–1540. doi: 10.1128/iai.65.4.1536-1540.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Godon J. J., Pillidge C. J., Jury K., Shearman C. A., Gasson M. J. Molecular analysis of the Lactococcus lactis sex factor. Dev Biol Stand. 1995;85:423–430. [PubMed] [Google Scholar]
  14. Haapasalo M., Orstavik D. In vitro infection and disinfection of dentinal tubules. J Dent Res. 1987 Aug;66(8):1375–1379. doi: 10.1177/00220345870660081801. [DOI] [PubMed] [Google Scholar]
  15. Haisman R. J., Jenkinson H. F. Mutants of Streptococcus gordonii Challis over-producing glucosyltransferase. J Gen Microbiol. 1991 Mar;137(3):483–489. doi: 10.1099/00221287-137-3-483. [DOI] [PubMed] [Google Scholar]
  16. Hawkins B. W., Cannon R. D., Jenkinson H. F. Interactions of Actinomyces naeslundii strains T14V and ATCC 12104 with saliva, collagen and fibrinogen. Arch Oral Biol. 1993 Jun;38(6):533–535. doi: 10.1016/0003-9969(93)90191-n. [DOI] [PubMed] [Google Scholar]
  17. Herzberg M. C. Platelet-streptococcal interactions in endocarditis. Crit Rev Oral Biol Med. 1996;7(3):222–236. doi: 10.1177/10454411960070030201. [DOI] [PubMed] [Google Scholar]
  18. Homonylo-McGavin M. K., Lee S. F. Role of the C terminus in antigen P1 surface localization in Streptococcus mutans and two related cocci. J Bacteriol. 1996 Feb;178(3):801–807. doi: 10.1128/jb.178.3.801-807.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jenkinson H. F. Cell-surface proteins of Streptococcus sanguis associated with cell hydrophobicity and coaggregation properties. J Gen Microbiol. 1986 Jun;132(6):1575–1589. doi: 10.1099/00221287-132-6-1575. [DOI] [PubMed] [Google Scholar]
  20. Jenkinson H. F., Demuth D. R. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol. 1997 Jan;23(2):183–190. doi: 10.1046/j.1365-2958.1997.2021577.x. [DOI] [PubMed] [Google Scholar]
  21. Jenkinson H. F., Lamont R. J. Streptococcal adhesion and colonization. Crit Rev Oral Biol Med. 1997;8(2):175–200. doi: 10.1177/10454411970080020601. [DOI] [PubMed] [Google Scholar]
  22. Jenkinson H. F., Terry S. D., McNab R., Tannock G. W. Inactivation of the gene encoding surface protein SspA in Streptococcus gordonii DL1 affects cell interactions with human salivary agglutinin and oral actinomyces. Infect Immun. 1993 Aug;61(8):3199–3208. doi: 10.1128/iai.61.8.3199-3208.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kelly C. G., Todryk S., Kendal H. L., Munro G. H., Lehner T. T-cell, adhesion, and B-cell epitopes of the cell surface Streptococcus mutans protein antigen I/II. Infect Immun. 1995 Sep;63(9):3649–3658. doi: 10.1128/iai.63.9.3649-3658.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Koga T., Okahashi N., Takahashi I., Kanamoto T., Asakawa H., Iwaki M. Surface hydrophobicity, adherence, and aggregation of cell surface protein antigen mutants of Streptococcus mutans serotype c. Infect Immun. 1990 Feb;58(2):289–296. doi: 10.1128/iai.58.2.289-296.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kreft B., Marre R., Schramm U., Wirth R. Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells. Infect Immun. 1992 Jan;60(1):25–30. doi: 10.1128/iai.60.1.25-30.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Linde A. Dentin matrix proteins: composition and possible functions in calcification. Anat Rec. 1989 Jun;224(2):154–166. doi: 10.1002/ar.1092240206. [DOI] [PubMed] [Google Scholar]
  28. Liu T., Gibbons R. J. Binding of streptococci of the "mutans" group to type 1 collagen associated with apatitic surfaces. Oral Microbiol Immunol. 1990 Jun;5(3):131–136. doi: 10.1111/j.1399-302x.1990.tb00410.x. [DOI] [PubMed] [Google Scholar]
  29. Liu T., Gibbons R. J., Hay D. I., Skobe Z. Binding of Actinomyces viscosus to collagen: association with the type 1 fimbrial adhesin. Oral Microbiol Immunol. 1991 Feb;6(1):1–5. doi: 10.1111/j.1399-302x.1991.tb00443.x. [DOI] [PubMed] [Google Scholar]
  30. Love R. M. Bacterial penetration of the root canal of intact incisor teeth after a simulated traumatic injury. Endod Dent Traumatol. 1996 Dec;12(6):289–293. doi: 10.1111/j.1600-9657.1996.tb00529.x. [DOI] [PubMed] [Google Scholar]
  31. Love R. M., Chandler N. P., Jenkinson H. F. Penetration of smeared or nonsmeared dentine by Streptococcus gordonii. Int Endod J. 1996 Jan;29(1):2–12. doi: 10.1111/j.1365-2591.1996.tb01353.x. [DOI] [PubMed] [Google Scholar]
  32. Love R. M. Regional variation in root dentinal tubule infection by Streptococcus gordonii. J Endod. 1996 Jun;22(6):290–293. doi: 10.1016/S0099-2399(96)80261-5. [DOI] [PubMed] [Google Scholar]
  33. McGrady J. A., Butcher W. G., Beighton D., Switalski L. M. Specific and charge interactions mediate collagen recognition by oral lactobacilli. J Dent Res. 1995 Feb;74(2):649–657. doi: 10.1177/00220345950740020501. [DOI] [PubMed] [Google Scholar]
  34. McNab R., Holmes A. R., Clarke J. M., Tannock G. W., Jenkinson H. F. Cell surface polypeptide CshA mediates binding of Streptococcus gordonii to other oral bacteria and to immobilized fibronectin. Infect Immun. 1996 Oct;64(10):4204–4210. doi: 10.1128/iai.64.10.4204-4210.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Moisset A., Schatz N., Lepoivre Y., Amadio S., Wachsmann D., Schöller M., Klein J. P. Conservation of salivary glycoprotein-interacting and human immunoglobulin G-cross-reactive domains of antigen I/II in oral streptococci. Infect Immun. 1994 Jan;62(1):184–193. doi: 10.1128/iai.62.1.184-193.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. PAKULA R., WALCZAK W. On the nature of competence of transformable streptococci. J Gen Microbiol. 1963 Apr;31:125–133. doi: 10.1099/00221287-31-1-125. [DOI] [PubMed] [Google Scholar]
  37. Pashley D. H. Clinical considerations of microleakage. J Endod. 1990 Feb;16(2):70–77. doi: 10.1016/S0099-2399(06)81567-0. [DOI] [PubMed] [Google Scholar]
  38. Perez F., Rochd T., Lodter J. P., Calas P., Michel G. In vitro study of the penetration of three bacterial strains into root dentine. Oral Surg Oral Med Oral Pathol. 1993 Jul;76(1):97–103. doi: 10.1016/0030-4220(93)90302-k. [DOI] [PubMed] [Google Scholar]
  39. Peters L. B., Wesselink P. R., Moorer W. R. The fate and the role of bacteria left in root dentinal tubules. Int Endod J. 1995 Mar;28(2):95–99. doi: 10.1111/j.1365-2591.1995.tb00166.x. [DOI] [PubMed] [Google Scholar]
  40. Sommer P., Gleyzal C., Guerret S., Etienne J., Grimaud J. A. Induction of a putative laminin-binding protein of Streptococcus gordonii in human infective endocarditis. Infect Immun. 1992 Feb;60(2):360–365. doi: 10.1128/iai.60.2.360-365.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stark M., Kühn K. The properties of molecular fragments obtained on treating calfskin collagen with collagenase from Clostridium histolyticum. Eur J Biochem. 1968 Dec 5;6(4):534–541. doi: 10.1111/j.1432-1033.1968.tb00477.x. [DOI] [PubMed] [Google Scholar]
  42. Sundqvist G. Taxonomy, ecology, and pathogenicity of the root canal flora. Oral Surg Oral Med Oral Pathol. 1994 Oct;78(4):522–530. doi: 10.1016/0030-4220(94)90047-7. [DOI] [PubMed] [Google Scholar]
  43. Switalski L. M., Butcher W. G., Caufield P. C., Lantz M. S. Collagen mediates adhesion of Streptococcus mutans to human dentin. Infect Immun. 1993 Oct;61(10):4119–4125. doi: 10.1128/iai.61.10.4119-4125.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Visai L., Bozzini S., Raucci G., Toniolo A., Speziale P. Isolation and characterization of a novel collagen-binding protein from Streptococcus pyogenes strain 6414. J Biol Chem. 1995 Jan 6;270(1):347–353. doi: 10.1074/jbc.270.1.347. [DOI] [PubMed] [Google Scholar]

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