1887

Abstract

A major aetiological factor of dental caries is the pathology of the dental plaque biofilms. The amino acid -arginine (Arg) is found naturally in saliva as a free molecule or as a part of salivary peptides and proteins. Plaque bacteria metabolize Arg to produce alkali and neutralize glycolytic acids, promoting a less cariogenous oral microbiome. Here, we explored an alternative and complementary mechanism of action of Arg using atomic force microscopy. The nanomechanical properties of biofilm extracellular matrix were characterized under physiological buffer conditions. We report the effect of Arg on the adhesive behaviour and structural properties of extracellular polysaccharides in biofilms. High-resolution imaging of biofilm surfaces can reveal additional structural information on bacterial cells embedded within the surrounding extracellular matrix. A dense extracellular matrix was observed in biofilms without Arg compared to those grown in the presence of Arg. biofilms grown in the presence of Arg could influence the production and/or composition of extracellular membrane glucans and thereby affect their adhesion properties. Our results suggest that the presence of Arg in the oral cavity could influence the adhesion properties of to the tooth surface.

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2014-07-01
2020-01-17
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References

  1. Arce F. T., Carlson R., Monds J., Veeh R., Hu F. Z., Stewart P. S., Lal R., Ehrlich G. D., Avci R.. ( 2009;). Nanoscale structural and mechanical properties of nontypeable Haemophilus influenzae biofilms. J Bacteriol191:2512–2520 [CrossRef][PubMed]
    [Google Scholar]
  2. Binnig G., Quate C. F., Gerber C.. ( 1986;). Atomic force microscope. Phys Rev Lett56:930–933 [CrossRef][PubMed]
    [Google Scholar]
  3. Burne R. A., Marquis R. E.. ( 2000;). Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol Lett193:1–6 [CrossRef][PubMed]
    [Google Scholar]
  4. Busscher H. J., van de Belt-Gritter B., Dijkstra R. J., Norde W., Petersen F. C., Scheie A. A., van der Mei H. C.. ( 2007;). Intermolecular forces and enthalpies in the adhesion of Streptococcus mutans and an antigen I/II-deficient mutant to laminin films. J Bacteriol189:2988–2995 [CrossRef][PubMed]
    [Google Scholar]
  5. Cantore R., Petrou I., Lavender S., Santarpia P., Liu Z., Gittins E., Vandeven M., Cummins D., Sullivan R., Utgikar N.. ( 2013;). In situ clinical effects of new dentifrices containing 1.5% arginine and fluoride on enamel de- and remineralization and plaque metabolism. J Clin Dent24:A32–A44 [CrossRef][PubMed]
    [Google Scholar]
  6. Cross S. E., Kreth J., Zhu L., Qi F., Pelling A. E., Shi W., Gimzewski J. K.. ( 2006;). Atomic force microscopy study of the structure-function relationships of the biofilm-forming bacterium Streptococcus mutans . Nanotechnology17:S1–S7 [CrossRef][PubMed]
    [Google Scholar]
  7. Cross S. E., Kreth J., Zhu L., Sullivan R., Shi W., Qi F., Gimzewski J. K.. ( 2007;). Nanomechanical properties of glucans and associated cell-surface adhesion of Streptococcus mutans probed by atomic force microscopy under in situ conditions. Microbiology153:3124–3132 [CrossRef][PubMed]
    [Google Scholar]
  8. Dufrêne Y. F.. ( 2003;). Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology. Curr Opin Microbiol6:317–323 [CrossRef][PubMed]
    [Google Scholar]
  9. Dufrêne Y. F.. ( 2008;). Towards nanomicrobiology using atomic force microscopy. Nat Rev Microbiol6:674–680 [CrossRef][PubMed]
    [Google Scholar]
  10. Dupres V., Menozzi F. D., Locht C., Clare B. H., Abbott N. L., Cuenot S., Bompard C., Raze D., Dufrêne Y. F.. ( 2005;). Nanoscale mapping and functional analysis of individual adhesins on living bacteria. Nat Methods2:515–520 [CrossRef][PubMed]
    [Google Scholar]
  11. García-Godoy F., Hicks M. J.. ( 2008;). Maintaining the integrity of the enamel surface: the role of dental biofilm, saliva and preventive agents in enamel demineralization and remineralization. J Am Dent Assoc139:Suppl.25S–34S [CrossRef][PubMed]
    [Google Scholar]
  12. Harimawan A., Rajasekar A., Ting Y. P.. ( 2011;). Bacteria attachment to surfaces – AFM force spectroscopy and physicochemical analyses. J Colloid Interface Sci364:213–218 [CrossRef][PubMed]
    [Google Scholar]
  13. He J., Yarbrough D. K., Kreth J., Anderson M. H., Shi W., Eckert R.. ( 2010;). Systematic approach to optimizing specifically targeted antimicrobial peptides against Streptococcus mutans . Antimicrob Agents Chemother54:2143–2151 [CrossRef][PubMed]
    [Google Scholar]
  14. Hicks J., Garcia-Godoy F., Flaitz C.. ( 2003;). Biological factors in dental caries: role of saliva and dental plaque in the dynamic process of demineralization and remineralization (part 1). J Clin Pediatr Dent28:47–52[PubMed][CrossRef]
    [Google Scholar]
  15. Jeon J. G., Rosalen P. L., Falsetta M. L., Koo H.. ( 2011;). Natural products in caries research: current (limited) knowledge, challenges and future perspective. Caries Res45:243–263 [CrossRef][PubMed]
    [Google Scholar]
  16. Jorand F., Boué-Bigne F., Block J. C., Urbain V.. ( 1998;). Hydrophobic/hydrophilic properties of activated sludge exopolymeric substances. Water Sci Technol37:307–315 [CrossRef]
    [Google Scholar]
  17. Lang C., Böttner M., Holz C., Veen M., Ryser M., Reindl A., Pompejus M., Tanzer J. M.. ( 2010;). Specific Lactobacillus/Mutans Streptococcus co-aggregation. J Dent Res89:175–179 [CrossRef][PubMed]
    [Google Scholar]
  18. Lee Y. H., Zimmerman J. N., Custodio W., Xiao Y., Basiri T., Hatibovic-Kofman S., Siqueira W. L.. ( 2013;). Proteomic evaluation of acquired enamel pellicle during in vivo formation. PLoS ONE8:e67919 [CrossRef][PubMed]
    [Google Scholar]
  19. Li L., Finnegan M. B., Özkan S., Kim Y., Lillehoj P. B., Ho C.-M., Lux R., Mito R., Loewy Z., Shi W.. ( 2010;). In vitro study of biofilm formation and effectiveness of antimicrobial treatment on various dental material surfaces. Mol Oral Microbiol25:384–390 [CrossRef][PubMed]
    [Google Scholar]
  20. Liu B. H., Li K. L., Kang K.-L., Huang W.-K., Liao J.-D.. ( 2013;). In situ biosensing of the nanomechanical property and electrochemical spectroscopy of Streptococcus mutans-containing biofilms. J Phys D Appl Phys46:275401 [CrossRef]
    [Google Scholar]
  21. Loesche W. J.. ( 1986;). Role of Streptococcus mutans in human dental decay. Microbiol Rev50:353–380[PubMed]
    [Google Scholar]
  22. Loskill P., Zeitz C., Grandthyll S., Thewes N., Müller F., Bischoff M., Herrmann M., Jacobs K.. ( 2013;). Reduced adhesion of oral bacteria on hydroxyapatite by fluoride treatment. Langmuir29:5528–5533 [CrossRef][PubMed]
    [Google Scholar]
  23. Marsh P. D.. ( 1994;). Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res8:263–271[PubMed]
    [Google Scholar]
  24. Marsh P. D.. ( 2004;). Dental plaque as a microbial biofilm. Caries Res38:204–211 [CrossRef][PubMed]
    [Google Scholar]
  25. Marszalek P. E., Lu H., Li H. B., Carrion-Vazquez M., Oberhauser A. F., Schulten K., Fernandez J. M..( 1999;). Mechanical unfolding intermediates in titin modules. Nature402:100–103[CrossRef]
    [Google Scholar]
  26. Mei L., Busscher H. J., van der Mei H. C., Ren Y.. ( 2011;). Influence of surface roughness on streptococcal adhesion forces to composite resins. Dent Mater27:770–778 [CrossRef][PubMed]
    [Google Scholar]
  27. Morou-Bermudez E., Elias-Boneta A., Billings R. J., Burne R. A., Garcia-Rivas V., Brignoni-Nazario V., Suarez-Perez E.. ( 2011;). Urease activity in dental plaque and saliva of children during a three-year study period and its relationship with other caries risk factors. Arch Oral Biol56:1282–1289 [CrossRef][PubMed]
    [Google Scholar]
  28. Nascimento M. M., Gordan V. V., Garvan C. W., Browngardt C. M., Burne R. A.. ( 2009;). Correlations of oral bacterial arginine and urea catabolism with caries experience. Oral Microbiol Immunol24:89–95 [CrossRef][PubMed]
    [Google Scholar]
  29. Nascimento M. M., Liu Y., Kalra R., Perry S., Adewumi A., Xu X., Primosch R. E., Burne R. A.. ( 2013;). Oral arginine metabolism may decrease the risk for dental caries in children. J Dent Res92:604–608 [CrossRef][PubMed]
    [Google Scholar]
  30. Paes Leme A. F., Koo H., Bellato C. M., Bedi G., Cury J. A.. ( 2006;). The role of sucrose in cariogenic dental biofilm formation—new insight. J Dent Res85:878–887 [CrossRef][PubMed]
    [Google Scholar]
  31. Paster B. J., Boches S. K., Galvin J. L., Ericson R. E., Lau C. N., Levanos V. A., Sahasrabudhe A., Dewhirst F. E.. ( 2001;). Bacterial diversity in human subgingival plaque. J Bacteriol183:3770–3783 [CrossRef][PubMed]
    [Google Scholar]
  32. Pelling A. E., Li Y., Shi W., Gimzewski J. K.. ( 2005;). Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy. Proc Natl Acad Sci USA102:6484–6489 [CrossRef][PubMed]
    [Google Scholar]
  33. Qi F., Chen P., Caufield P. W.. ( 2001;). The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl Environ Microbiol67:15–21 [CrossRef][PubMed]
    [Google Scholar]
  34. Razatos A., Ong Y. L., Sharma M. M., Georgiou G.. ( 1998;). Molecular determinants of bacterial adhesion monitored by atomic force microscopy. Proc Natl Acad Sci USA95:11059–11064 [CrossRef][PubMed]
    [Google Scholar]
  35. Revsbech N. P.. ( 2005;). Analysis of microbial communities with electrochemical microsensors and microscale biosensors. Methods Enzymol397:147–166 [CrossRef][PubMed]
    [Google Scholar]
  36. Schilling K. M., Bowen W. H.. ( 1992;). Glucans synthesized in situ in experimental salivary pellicle function as specific binding sites for Streptococcus mutans . Infect Immun60:284–295[PubMed]
    [Google Scholar]
  37. Sharma S., Sen P., Mukhopadhyay S. N., Guha S. K.. ( 2003;). Microbicidal male contraceptive – Risug induced morpho structural damage in E. coli . Colloid Surfaces B32:43–50 [CrossRef]
    [Google Scholar]
  38. Sharma S., Cross S. E., Hsueh C., Wali R. P., Stieg A. Z., Gimzewski J. K.. ( 2010;). Nanocharacterization in dentistry. Int J Mol Sci11:2523–2545 [CrossRef][PubMed]
    [Google Scholar]
  39. Sharma S., Grintsevich E. E., Phillips M. L., Reisler E., Gimzewski J. K.. ( 2011;). Atomic force microscopy reveals drebrin induced remodeling of F-actin with subnanometer resolution. Nano Lett11:825–827 [CrossRef][PubMed]
    [Google Scholar]
  40. Sullivan R., Santarpia P., Lavender S., Gittins E., Liu Z., Anderson M. H., He J., Shi W., Eckert R.. ( 2011;). Clinical efficacy of a specifically targeted antimicrobial peptide mouth rinse: targeted elimination of Streptococcus mutans and prevention of demineralization. Caries Res45:415–428 [CrossRef][PubMed]
    [Google Scholar]
  41. Tabak L. A.. ( 2006;). In defense of the oral cavity: the protective role of the salivary secretions. Pediatr Dent28:110–117, discussion 192–198[PubMed]
    [Google Scholar]
  42. Thurnheer T., van der Ploeg J. R., Giertsen E., Guggenheim B.. ( 2006;). Effects of Streptococcus mutans gtfC deficiency on mixed oral biofilms in vitro. Caries Res40:163–171 [CrossRef][PubMed]
    [Google Scholar]
  43. VanWuyckhuyse B. C., Perinpanayagam H. E., Bevacqua D., Raubertas R. F., Billings R. J., Bowen W. H., Tabak L. A.. ( 1995;). Association of free arginine and lysine concentrations in human parotid saliva with caries experience. J Dent Res74:686–690 [CrossRef][PubMed]
    [Google Scholar]
  44. Vu B., Chen M., Crawford R. J., Ivanova E. P.. ( 2009;). Bacterial extracellular polysaccharides involved in biofilm formation. Molecules14:2535–2554 [CrossRef][PubMed]
    [Google Scholar]
  45. Xiao J., Koo H.. ( 2010;). Structural organization and dynamics of exopolysaccharide matrix and microcolonies formation by Streptococcus mutans in biofilms. J Appl Microbiol108:2103–2113[PubMed]
    [Google Scholar]
  46. Yakovenko O., Sharma S., Forero M., Tchesnokova V., Aprikian P., Kidd B., Mach A., Vogel V., Sokurenko E..& other authors ( 2008;). FimH forms catch bonds that are enhanced by mechanical force due to allosteric regulation. J Biol Chem283:11596–11605[CrossRef]
    [Google Scholar]
  47. Yamashita Y., Bowen W. H., Burne R. A., Kuramitsu H. K.. ( 1993;). Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infect Immun61:3811–3817[PubMed]
    [Google Scholar]
  48. Zero D. T., Fontana M., Martínez-Mier E. A., Ferreira-Zandoná A., Ando M., González-Cabezas C., Bayne S.. ( 2009;). The biology, prevention, diagnosis and treatment of dental caries: scientific advances in the United States. J Am Dent Assoc140:Suppl. 125S–34S [CrossRef][PubMed]
    [Google Scholar]
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