Caries Research

Original Paper

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Manganese Affects Streptococcus mutans Virulence Gene Expression

Arirachakaran P.a · Benjavongkulchai E.a · Luengpailin S.b · Ajdić D.c · Banas J.A.d

Author affiliations

aChulalongkorn University, Bangkok, and bKhon Kaen University, Khon Kaen, Thailand; cUniversity of Oklahoma Health Sciences Center, Oklahoma City, Okla., and dUniversity of Iowa College of Dentistry, Iowa City, Iowa, USA

Corresponding Author

Jeffrey A. Banas

University of Iowa College of Dentistry

Dows Institute for Research, Dental Science N 436

Iowa City, IA 52242 (USA)

Tel. +1 319 335 9911, Fax +1 319 335 8895, E-Mail Jeffrey-banas@uiowa.edu

Keywords: BiofilmManganeseStreptococcus mutans virulence

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Caries Res 2007;41:503–511
https://doi.org/10.1159/000110883

Abstract

Background/Aims: Studies of trace metals in drinking water and tooth enamel have suggested a caries-promoting potential for manganese (Mn). Additionally, Mn has been shown to be essential for the expression of mutans streptococci virulence factors such as the glucan-binding lectin (GBL) of Streptococcus sobrinus. The Streptococcus mutans glucan-binding protein (Gbp) GbpC is the functional analogue of the S. sobrinus GBL. S. mutans Gbps have been shown to contribute to biofilm architecture and virulence. This study was undertaken to examine the effects of Mn on the transcription of genes encoding S. mutans Gbps, including gbpC, along with other critical S. mutans virulence genes. Methods: Microarray analyses suggested the potential for an Mn effect on Gbp genes. Further investigation of the Mn effects on selected genes was undertaken by performing Northern blots, Western blots, and RT-PCR under conditions of planktonic and biofilm growth in Mn-depleted media or in media containing 50 µM Mn. Results: Mn resulted in increased expression of gbpC and gtfB, and decreased expression of wapA, in both planktonic and biofilm cultures. The expression levels of gbpA and gbpD were also decreased in the presence of Mn, but only in biofilms. The expression of gtfC was increased in the presence of Mn only in planktonic cultures. The spaP gene was expressed more highly in Mn-supplemented planktonic cultures but less in Mn-supplemented biofilms. Conclusion: Mn availability affects the expression of multiple S. mutans genes involved in adhesion and biofilm formation. Furthermore, these effects depend on the growth state of the organism.

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References

  1. Adkins BL, Losee FL: A study of the covariation of dental caries prevalence and multiple trace element content of water supplies. NY State Dent J 1970;36:618–622.
    External Resources
  2. Ajdić D, McShan WM, McLaughlin RE, Savić G, Chang J, Carson MB, Primeaux C, Tian R, Kenton S, Jia H, Lin S, Qian Y, Li S, Zhu H, Najar F, Lai H, White J, Roe BA, Ferretti JJ: Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci USA 2002;99:14434–14439.
    External Resources
  3. Aranha H, Evans SL, Arceneaux JE, Byers BR: Calcium modulation of growth of Streptococcus mutans. J Gen Microbiol 1986;132:2661–2663.
    External Resources
  4. Aranha H, Strachan RC, Arceneaux JE, Byers BR: Effect of trace metals on growth of Streptococcus mutans in a Teflon chemostat. Infect Immun 1982;35:456–460.
    External Resources
  5. Arirachakaran P, Luengpailin S, Banas JA, Mazurkiewicz JE, Benjavongkulchai E: Effects of manganese on Streptococcus mutans planktonic and biofilm growth. Caries Res 2007;41:497–502.
    External Resources
  6. Banas JA, Russell RR, Ferretti JJ: Sequence analysis of the gene for the glucan-binding protein of Streptococcus mutans Ingbritt. Infect Immun 1990;58:667–673.
    External Resources
  7. Banas JA, Vickerman MM: Glucan-binding proteins of the oral streptococci. Crit Rev Oral Biol Med 2003;14:89–99.
    External Resources
  8. Beighton D: The influence of manganese on carbohydrate metabolism and caries induction by Streptococcus mutans strain Ingbritt. Caries Res 1982;16:189–192.
    External Resources
  9. Beighton D: Manganese; in Curzon MEJ, Cutress TW (eds): Trace Elements and Dental Disease. Postgraduate Dental Handbook Series. Littleton, Wright, 1983, pp 237–244.
  10. Burne RA: Oral streptococci... products of their environment. J Dent Res 1998;77:445–452.
    External Resources
  11. Drake D, Taylor KG, Doyle RJ: Expression of the glucan-binding lectin of Streptococcus cricetus requires manganous ion. Infect Immun 1988;56:2205–2207.
    External Resources
  12. Fenno JC, Shaikh A, Spatafora G, Fives-Taylor P: The fimA locus of Streptococcus parasanguis encodes an ATP-binding membrane transport system. Mol Microbiol 1995;15:849–863.
    External Resources
  13. Gibbons RJ, Etherden I: Comparative hydrophobicities of oral bacteria and their adherence to salivary pellicles. Infect Immun 1983;41:1190–1196.
    External Resources
  14. Gilmore KS, Srinivas P, Akins DR, Hatter KL, Gilmore MS: Growth, development, and gene expression in a persistent Streptococcus gordonii biofilm. Infect Immun 2003;71:4759–4766.
    External Resources
  15. Glass RL, Rothman KJ, Espinal F, Velez H, Smith NJ: The prevalence of human dental caries and water-borne trace metals. Arch Oral Biol 1973;18:1099–1104.
    External Resources
  16. Hazlett KR, Mazurkiewicz JE, Banas JA: Inactivation of the gbpA gene of Streptococcus mutans alters structural and functional aspects of plaque biofilm which are compensated by recombination of the gtfB and gtfC genes. Infect Immun 1999;67:3909–3914.
    External Resources
  17. Hazlett KR, Michalek SM, Banas JA: Inactivation of the gbpA gene of Streptococcus mutans increases virulence and promotes in vivo accumulation of recombinations between the glucosyltransferase B and C genes. Infect Immun 1998;66:2180–2185.
    External Resources
  18. Jakubovics NS, Jenkinson HF: Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 2001;147:1709–1718.
    External Resources
  19. Johnston JW, Briles DE, Myers LE, Hollingshead SK: Mn2+-dependent regulation of multiple genes in Streptococcus pneumoniae through PsaR and the resultant impact on virulence. Infect Immun 2006;74:1171–1180.
    External Resources
  20. Kehres DG, Maguire ME: Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 2003;27:263–290.
    External Resources
  21. Kitten T, Munro CL, Michalek SM, Macrina FL: Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect Immun 2000;68:4441–4451.
    External Resources
  22. Landa AS, van der Mei HC, Busscher HJ: Detachment of linking film bacteria from enamel surfaces by oral rinses and penetration of sodium lauryl sulphate through an artificial oral biofilm. Adv Dent Res 1997;11:528–538.
    External Resources
  23. Lee SF, Progulske-Fox A, Erdos GW, Piacentini DA, Ayakawa GY, Crowley PJ, Bleiweis AS: Construction and characterization of isogenic mutants of Streptococcus mutans deficient in major surface protein antigen P1 (I/II). Infect Immun 1989;57:3306–3313.
    External Resources
  24. Liang L, Drake D, Doyle RJ: Stability of the glucan-binding lectin of oral streptococci. J Dent Res 1989;68:1677.
    External Resources
  25. Loesche WJ: Role of Streptococcus mutans in human dental decay. Microbiol Rev 1986;50:353–380.
    External Resources
  26. Lynch DJ, Fountain TL, Mazurkiewicz JE, Banas JA: Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol Lett 2007;268:158–165.
    External Resources
  27. Marsh PD: Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res 1994;8:263–271.
    External Resources
  28. Martin ME, Byers BR, Olson MOJ, Salin ML, Arceneaux JEL, Tolbert C: Streptococcus mutans superoxide dismutase that is active with either manganese or iron as a cofactor. J Biol Chem 1986;261:9361–9367.
    External Resources
  29. Matsumura M, Izumi T, Matsumoto M, Tsuji M, Fujiwara T, Ooshima T: The role of glucan-binding proteins in the cariogenicity of Streptococcus mutans. Microbiol Immunol 2003;47:213–215.
    External Resources
  30. Mattos-Graner RO, Jin S, King WF, Chen T, Smith DJ, Duncan MJ: Cloning of the Streptococcus mutans gene encoding glucan binding protein B and analysis of genetic diversity and protein production in clinical isolates. Infect Immun 2001;69:6931–6941.
    External Resources
  31. Mattos-Graner RO, Porter KA, Smith DJ, Hosogi Y, Duncan MJ: Functional analysis of glucan binding protein B from Streptococcus mutans. J Bacteriol 2006;188:3813–3825.
    External Resources
  32. Mattos-Graner RO, Smith DJ, King WF, Mayer MP: Water-insoluble glucan synthesis by mutans streptococcal strains correlates with caries incidence in 12- to 30-month-old children. J Dent Res 2000;79:1371–1377.
    External Resources
  33. Paik S, Brown A, Munro CL, Cornelissen CN, Kitten T: The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 2003;185:5967–5975.
    External Resources
  34. Papp-Wallace KM, Maguire ME: Manganese transport and the role of manganese in virulence. Annu Rev Microbiol 2006;60:187–209.
    External Resources
  35. Rolerson E, Swick A, Newlon L, Palmer C, Pan Y, Keeshan B, Spatafora G: The SloR/Dlg metalloregulator modulates Streptococcus mutans virulence gene expression. J Bacteriol 2006;188:5033–5044.
    External Resources
  36. Russell C, Coulter WA: Continuous monitoring of pH and Eh in bacterial plaque grown on a tooth in an artificial mouth. Appl Microbiol 1975;29:141–144.
    External Resources
  37. Sambrook J, Russell DW: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, Cold Spring Harbor Laboratory Press, 2001.
  38. Sato Y, Yamamoto Y, Kizaki H: Cloning and sequence analysis of the gbpC gene encoding a novel glucan-binding protein of Streptococcus mutans. Infect Immun 1997;65:668–675.
    External Resources
  39. Shah DS, Russell RR: A novel glucan-binding protein with lipase activity from the oral pathogen Streptococcus mutans. Microbiology 2004;150:1947–1956.
    External Resources
  40. Sulavik MC, Tardif G, Clewell DB: Identification of a gene, rgg, which regulates expression of glucosyltransferase and influences the Spp phenotype of Streptococcus gordonii Challis. J Bacteriol 1992;174:3577–3586.
    External Resources
  41. Terleckyj B, Shockman GD: Amino acid requirements of Streptococcus mutans and other oral streptococci. Infect Immun 1975;11:656–664.
    External Resources
  42. Vickerman MM, Jones GW: Sucrose-dependent accumulation of oral streptococci and their adhesion-defective mutants on saliva-coated hydroxyapatite. Oral Microbiol Immunol 1995;10:175–182.
    External Resources
  43. Vickerman MM, Minick PE: Genetic analysis of rgg-gtfG junctional region and its role in Streptococcus gordonii glucosyltransferase activity. Infect Immun 2002;70:1703–1714.
    External Resources
  44. Zaharik ML, Finlay BB: Mn2+ and bacterial pathogenesis. Frontiers Biosci 2004;9:1035–1042.
    External Resources

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: January 12, 2007
Accepted: August 14, 2007
Published online: November 08, 2007
Issue release date: November 2007

Number of Print Pages: 9
Number of Figures: 5
Number of Tables: 1

ISSN: 0008-6568 (Print)
eISSN: 1421-976X (Online)

For additional information: https://www.karger.com/CRE

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2007, Vol.41, No. 6

November 2007

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