1887

Abstract

Iron uptake, transport and storage in , the principal causative agent of human dental cavities, is unexplored despite early reports in the literature which predict a role for this trace metal in cariogenesis. Experiments in the authors’ laboratory revealed several iron-responsive proteins in , one of which reacted with a polyclonal antiserum directed against the FimA fimbrial adhesin from on Western blots. The results of Western blot and Northern hybridization experiments support an inverse relationship between iron availability and expression, and metal ion uptake experiments implicate FimA in Fe transport. Cloning of the homologue facilitated the construction of a knockout mutant which grew poorly in an iron-limiting medium relative to the wild-type progenitor strain, lending further support to a role for FimA in iron transport. The authors also identified and cloned a -like gene () located downstream of on the chromosome, and noted increased expression in a knockout mutant relative to wild-type on RNA spot blots and Western blots. The uptake of Fe, which was also significantly increased in this mutant, was compromised in a / double knockout. These findings are consistent with a role for Dlg in the iron-mediated regulation of , and possibly other iron transporters. Finally, the cariogenic potential of the and knockout mutants was not significantly different from that of the wild-type progenitor in a germ-free rat model.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-147-6-1599
2001-06-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/147/6/1471599a.html?itemId=/content/journal/micro/10.1099/00221287-147-6-1599&mimeType=html&fmt=ahah

References

  1. Adkins B. L., Losee F. L.. 1970; A study of covariation of dental caries prevalence and multiple trace element content of water supplies. N Y State Dent J36:618–622
    [Google Scholar]
  2. Aranha H., Strachan R. C., Arceneaux J., Byers B.. 1982; Effect of trace metals on growth of Streptococcus mutans in a teflon chemostat. Infect Immun35:456–460
    [Google Scholar]
  3. Archibald F.. 1983; Lactobacillus plantarum , an organism not requiring iron. FEMS Microbiol Lett19:29–32[CrossRef]
    [Google Scholar]
  4. Boyd J., Oza M. N., Murphy J.. 1990; Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent element ( dtxR ) from Corynebacterium diphtheriae. . Proc Natl Acad Sci USA87:5968–5972[CrossRef]
    [Google Scholar]
  5. Bullen J. J., Rogers H. J., Griffiths E.. 1978; Role of iron in bacterial infections. Curr Top Microbiol Immunol80:1–35
    [Google Scholar]
  6. Burnette-Curley D., Wells V., Viscount H., Munro C. L., Fenno J. C., Fives-Taylor P., Macrina F. L.. 1995; FimA, a major virulence factor associated with Streptococcus parasanguis endocarditis. Infect Immun63:4669–4674
    [Google Scholar]
  7. Butteron J., Stoebner J., Payne S., Calderwood S.. 1992; Cloning, sequencing, and transcriptional regulation of viuA , the gene encoding the ferric vibriobactin receptor in Vibrio cholerae. . J Bacteriol 174:3729–3738
    [Google Scholar]
  8. Cockayne A., Hill P. J., Powell N. B., Bishop K., Sims C., Williams P.. 1998; Molecular cloning of a 32 kilodalton lipoprotein component of a novel iron-regulated Staphylococcus epidermidis ABC tansporter. Infect Immun66:3767–3774
    [Google Scholar]
  9. Coish R. A., Sinton C. W.. 1992; Geochemistry of mafic dikes in the Adirondack mountains: implications for late Proterozoic continental rifting. Contrib Mineral Petrol110:500–514[CrossRef]
    [Google Scholar]
  10. Correia F. F., DiRienzo J. M., McKay T. L., Rosan B.. 1996; scbA from Streptococcus crista CC5A: an atypical member of the lraI gene family. Infect Immun64:2114–2121
    [Google Scholar]
  11. Dintilhac A., Claverys J. P.. 1997; The adc locus, which affects competence for genetic transformation in Streptococcus pneumoniae , encodes an ABC transporter with a putative lipoprotein homologous to a family of streptococcal adhesins. Res Microbiol148:119–131[CrossRef]
    [Google Scholar]
  12. Dintilhac A., Alloing G., Granadel C., Claverys J. P.. 1997; Competence and virulence of Streptococcus pneumoniae : AdcA and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol Microbiol25:727–739[CrossRef]
    [Google Scholar]
  13. Evans S., Arceneaux J., Byers B., Martin M., Aranha H.. 1986; Ferrous iron transport in Streptococcus mutans. . J Bacteriol168:1096–1099
    [Google Scholar]
  14. Federle M. J., McIver K. S., Scott J. R.. 1999; A response regulator that represses transcription of several virulence operons in the group A streptococcus. J Bacteriol181:3649–3657
    [Google Scholar]
  15. Fenno J. C., Shaikh A., Spatafora G., Fives-Taylor P.. 1995; The fimA locus of Streptococcus parasanguis encodes an ATP-binding membrane transport system. Mol Microbiol15:849–863[CrossRef]
    [Google Scholar]
  16. Finkelstein R., Sciortino C., McIntosh M.. 1983; Role of iron in microbe–host interactions. Rev Infect Dis5:S759–S777[CrossRef]
    [Google Scholar]
  17. Fleming T., Nahlika M., McIntosh M.. 1983; Regulation of enterobacteria iron transport in Escherichia coli : characterization of ent :: Mud(Apr lac ) operon fusions. J Bacteriol156:1171–1177
    [Google Scholar]
  18. Froeliger E. H., Fives-Taylor P.. 2000; Streptococcus parasanguis FimA does not contribute to adherence to SHA (abstract). J Dent Res79:337
    [Google Scholar]
  19. Ganeshkumar N., Hannam P. M., Kolenbrander P. E., McBride B. C.. 1991; Nucleotide sequence of a gene coding for a saliva-binding protein (SsaB) from Streptococcus sanguis 12 and possible role of the protein in coaggregation with Actinomyces. Infect Immun59:1093–1099
    [Google Scholar]
  20. Goodman S. D., Gao Q.. 2000; Characterization of the gtfB and gtfC promoters from Streptococcus mutans GS-5. Plasmid4:85–98
    [Google Scholar]
  21. Genco C., Desai P.. 1996; Iron acquisition in the pathogenic Neisseria. Trends. Microbiol4:185–191[CrossRef]
    [Google Scholar]
  22. Hardham J. M., Stamm L. V., Porcella S. F.. 7 other authors 1997; Identification and transcriptional analysis of a Treponema pallidum operon encoding a putative ABC transport system, an iron-activated repressor protein homolog, and a glycolytic pathway enzyme homolog. Gene197:47–64[CrossRef]
    [Google Scholar]
  23. Hennecke H.. 1990; Regulation of bacterial gene expression by metal–protein complexes. Mol Microbiol4:1621–1628[CrossRef]
    [Google Scholar]
  24. Husson M., Legrand D., Spik G., Leclerc H.. 1993; Iron acquisition by Helicobacter pylori : importance of human lactoferrin. Infect Immun61:2694–2697
    [Google Scholar]
  25. Janulcyk R., Pallon J., Björck L.. 1999; Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol344:596–606
    [Google Scholar]
  26. Keyes P.. 1958; Dental caries in the molar teeth of rats. II. A method for diagnosing and scoring several types of lesions simultaneously. J Dent Res37:1088–1099[CrossRef]
    [Google Scholar]
  27. Kitten T., Munro C. L., Michalek S. M., Macrina F. L.. 2000; Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect Immun68:4441–4451[CrossRef]
    [Google Scholar]
  28. Kolenbrander P. E., Andersen R. N., Ganeshkumar N.. 1994; Nucleotide sequence of the Streptococcus gordonii PK488 coaggregation adhesin gene, scaA , and ATP-binding cassette. Infect Immun62:4469–4480
    [Google Scholar]
  29. Kolenbrander P. E., Andersen R. N., Baker R. A., Jenkinson H. F.. 1998; The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol180:290–295
    [Google Scholar]
  30. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  31. Litwin C. M., Calderwood S. B.. 1993; Role of iron in regulation of virulence genes. Clin Microbiol Rev6:137–149
    [Google Scholar]
  32. Marmur J.. 1961; A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol3:208–218[CrossRef]
    [Google Scholar]
  33. Michalek S., McGhee J., Navia J.. 1975; Virulence of Streptococcus mutans : a sensitive method for evaluating cariogenicity in young gnotobiotic rats. Infect Immun12:69–75
    [Google Scholar]
  34. Nakayama K.. 1992; Nucleotide sequence of Streptococcus mutans superoxide dismutase gene and isolation of insertion mutants. J Bacteriol174:4928–4934
    [Google Scholar]
  35. Novak R., Braun J. S., Charpentier E., Tuomanen E.. 1998; Penicillin tolerance genes of Streptococcus pneuomoniae : the ABC-type manganese permease complex, Psa. Mol Microbiol29:1285–1296[CrossRef]
    [Google Scholar]
  36. Pohl E., Holmes R. K., Hol W. G. J.. 1999; Crystal structure of the iron-dependent regulator (IdeR) from Mycobacterium tuberculosis shows both metal binding sites fully occupied. J Mol Biol285:1145–1156[CrossRef]
    [Google Scholar]
  37. Posey J. E., Gherardini F. C.. 2000; Lack of a role for iron in the Lyme disease pathogen. Science288:1651–1653[CrossRef]
    [Google Scholar]
  38. Que Q., Helmann J. D.. 2000; Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheriae toxin repressor family of proteins. Mol Microbiol35:1454–1468
    [Google Scholar]
  39. Rigby P. W. J., Dieckman M., Phodes C., Berg P.. 1977; Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase. I. J Mol Biol113:237–251[CrossRef]
    [Google Scholar]
  40. Sambrook J., Fritsch E. F., Maniatis T.. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  41. Schiering N., Tao X., Zeng H., Murphy J., Petsko G., Ringe D.. 1995; Structures of the apo- and the metal ion-activated forms of the diphtheria tox repressor from Corynebacterium diphtheriae. . Proc Natl Acad Sci USA 92:9843–9850[CrossRef]
    [Google Scholar]
  42. Schmidt M.. 1997; Transcription of the Corynebacterium diphtheriae hmuO gene is regulated by iron and heme. Infect Immun65:4634–4641
    [Google Scholar]
  43. Schwyn B., Neilands J. B.. 1987; Universal chemical assay for the detection and determination of siderophores. Anal Biochem160:47–56[CrossRef]
    [Google Scholar]
  44. Southern E. M.. 1975; Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol98:503–517[CrossRef]
    [Google Scholar]
  45. Spatafora G., Moore M.. 1998; Growth of Streptococcus mutans in an iron-limiting medium. Methods Cell Sci20:217–221[CrossRef]
    [Google Scholar]
  46. Spatafora G., Rohrer K., Barnard D., Michalek S.. 1995; A Streptococcus mutans mutant that synthesizes elevated levels of intracellular polysaccharide is hypercariogenic in vivo. . Infect Immun63:2556–2563
    [Google Scholar]
  47. Spellerberg B., Rozdzinski E., Martin S., Weber-Heynemann J., Schnitzler N., Podbielski A., Lütticken R.. 1998; Lmb, a protein with similarities to the LraI adhesin family, mediates attachment of Streptococcus agalactiae to human laminin. Infect Immun67:871–878
    [Google Scholar]
  48. Tao X., Murphy J. R.. 1994; Iron, DtxR, and the regulation of diphtheria toxin expression. Mol Microbiol14:191–197[CrossRef]
    [Google Scholar]
  49. Terleckyj B., Willett N. P., Shockman G. D.. 1975; Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun11:649–655
    [Google Scholar]
  50. Viscount H. B., Munro C. L., Burnette-Curley D., Peterson D. L., Macrina F. L.. 1997; Immunization with FimA protects against Streptococcus parasanguis endocarditis in rats. Infect Immun65:994–1002
    [Google Scholar]
  51. Weinberg E. D.. 1978; Iron and infection. Microbiol Rev42:45–66
    [Google Scholar]
  52. Williams P., Griffiths E.. 1992; Bacterial transferrin receptors – structure, function, and contribution to virulence. Med Microbiol Immunol181:301–322
    [Google Scholar]
  53. Wooldridge K. G., Williams P. H.. 1993; Iron uptake mechanisms of pathogenic bacteria. FEMS Microbiol Rev12:325–348[CrossRef]
    [Google Scholar]
  54. Zimmerman L., Hantke K., Braun V.. 1984; Exogenous induction of the iron dicitrate transport system of Escherichia coli K-12. J Bacteriol159:271–277
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-147-6-1599
Loading
/content/journal/micro/10.1099/00221287-147-6-1599
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error