1887

Microbiology Society logo

Volume 158, Issue 12

Functional amyloid formation by Free

Abstract

Dental caries is a common infectious disease associated with acidogenic and aciduric bacteria, including . Organisms that cause cavities form recalcitrant biofilms, generate acids from dietary sugars and tolerate acid end products. It has recently been recognized that micro-organisms can produce functional amyloids that are integral to biofilm development. We now show that the cell-surface-localized adhesin P1 (antigen I/II, PAc) is an amyloid-forming protein. This conclusion is based on the defining properties of amyloids, including binding by the amyloidophilic dyes Congo red (CR) and Thioflavin T (ThT), visualization of amyloid fibres by transmission electron microscopy and the green birefringent properties of CR-stained protein aggregates when viewed under cross-polarized light. We provide evidence that amyloid is present in human dental plaque and is produced by both laboratory strains and clinical isolates of . We provide further evidence that amyloid formation is not limited to P1, since bacterial colonies without this adhesin demonstrate residual green birefringence. However, lacking sortase, the transpeptidase enzyme that mediates the covalent linkage of its substrates to the cell-wall peptidoglycan, including P1 and five other proteins, is not birefringent when stained with CR and does not form biofilms. Biofilm formation is inhibited when is cultured in the presence of known inhibitors of amyloid fibrillization, including CR, Thioflavin S and epigallocatechin-3-gallate, which also inhibited ThT uptake by extracellular proteins. Taken together, these results indicate that is an amyloid-forming organism and suggest that amyloidogenesis contributes to biofilm formation by this oral microbe.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.060855-0
2012-12-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/12/2903.html?itemId=/content/journal/micro/10.1099/mic.0.060855-0&mimeType=html&fmt=ahah

References

  1. Ahn S. J., Ahn S. J., Wen Z. T., Brady L. J., Burne R. A. ( 2008). Characteristics of biofilm formation by Streptococcus mutans in the presence of saliva. Infect Immun 76:4259–4268 [View Article][PubMed]
     [Google Scholar]
  2. Alteri C. J., Xicohténcatl-Cortes J., Hess S., Caballero-Olín G., Girón J. A., Friedman R. L. ( 2007). Mycobacterium tuberculosis produces pili during human infection. Proc Natl Acad Sci U S A 104:5145–5150 [View Article][PubMed]
     [Google Scholar]
  3. Ayakawa G. Y., Boushell L. W., Crowley P. J., Erdos G. W., McArthur W. P., Bleiweis A. S. ( 1987). Isolation and characterization of monoclonal antibodies specific for antigen P1, a major surface protein of mutans streptococci. Infect Immun 55:2759–2767[PubMed]
     [Google Scholar]
  4. Barnhart M. M., Chapman M. R. ( 2006). Curli biogenesis and function. Annu Rev Microbiol 60:131–147 [View Article][PubMed]
     [Google Scholar]
  5. Beg A. M., Jones M. N., Miller-Torbert T., Holt R. G. ( 2002). Binding of Streptococcus mutans to extracellular matrix molecules and fibrinogen. Biochem Biophys Res Commun 298:75–79 [View Article][PubMed]
     [Google Scholar]
  6. Bieler S., Estrada L., Lagos R., Baeza M., Castilla J., Soto C. ( 2005). Amyloid formation modulates the biological activity of a bacterial protein. J Biol Chem 280:26880–26885 [View Article][PubMed]
     [Google Scholar]
  7. Bouvet A., van de Rijn I., McCarty M. ( 1981). Nutritionally variant streptococci from patients with endocarditis: growth parameters in a semisynthetic medium and demonstration of a chromophore. J Bacteriol 146:1075–1082[PubMed]
     [Google Scholar]
  8. Brady L. J., Crowley P. J., Ma J. K., Kelly C., Lee S. F., Lehner T., Bleiweis A. S. ( 1991). Restriction fragment length polymorphisms and sequence variation within the spaP gene of Streptococcus mutans serotype c isolates. Infect Immun 59:1803–1810[PubMed]
     [Google Scholar]
  9. Brady L. J., Cvitkovitch D. G., Geric C. M., Addison M. N., Joyce J. C., Crowley P. J., Bleiweis A. S. ( 1998). Deletion of the central proline-rich repeat domain results in altered antigenicity and lack of surface expression of the Streptococcus mutans P1 adhesin molecule. Infect Immun 66:4274–4282[PubMed]
     [Google Scholar]
  10. Brady L. J., Maddocks S. E., Larson M. R., Forsgren N., Persson K., Deivanayagam C. C., Jenkinson H. F. ( 2010). The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Mol Microbiol 77:276–286 [View Article][PubMed]
     [Google Scholar]
  11. Broxmeyer L. ( 2002). Parkinson’s: another look. Med Hypotheses 59:373–377 [View Article][PubMed]
     [Google Scholar]
  12. Burne R. A., Ahn S. J., Wen Z. T., Zeng L., Lemos J. A., Abranches J., Nascimento M. ( 2009). Opportunities for disrupting cariogenic biofilms. Adv Dent Res 21:17–20 [View Article][PubMed]
     [Google Scholar]
  13. Butko P., Buford J. P., Goodwin J. S., Stroud P. A., McCormick C. L., Cannon G. C. ( 2001). Spectroscopic evidence for amyloid-like interfacial self-assembly of hydrophobin Sc3. Biochem Biophys Res Commun 280:212–215 [View Article][PubMed]
     [Google Scholar]
  14. Cegelski L., Pinkner J. S., Hammer N. D., Cusumano C. K., Hung C. S., Chorell E., Aberg V., Walker J. N., Seed P. C. & other authors ( 2009). Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 5:913–919 [View Article][PubMed]
     [Google Scholar]
  15. Chapman M. R., Robinson L. S., Pinkner J. S., Roth R., Heuser J., Hammar M., Normark S., Hultgren S. J. ( 2002). Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855 [View Article][PubMed]
     [Google Scholar]
  16. Chernoff Y. O. ( 2004). Amyloidogenic domains, prions and structural inheritance: rudiments of early life or recent acquisition?. Curr Opin Chem Biol 8:665–671 [View Article][PubMed]
     [Google Scholar]
  17. Claessen D., Rink R., de Jong W., Siebring J., de Vreugd P., Boersma F. G., Dijkhuizen L., Wosten H. A. ( 2003). A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17:1714–1726 [View Article][PubMed]
     [Google Scholar]
  18. Crowley P. J., Brady L. J., Michalek S. M., Bleiweis A. S. ( 1999). Virulence of a spaP mutant of Streptococcus mutans in a gnotobiotic rat model. Infect Immun 67:1201–1206[PubMed]
     [Google Scholar]
  19. DaSilva K. A., Shaw J. E., McLaurin J. ( 2010). Amyloid-beta fibrillogenesis: structural insight and therapeutic intervention. Exp Neurol 223:311–321 [View Article][PubMed]
     [Google Scholar]
  20. de Jong W., Wösten H. A., Dijkhuizen L., Claessen D. ( 2009). Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose. Mol Microbiol 73:1128–1140 [View Article][PubMed]
     [Google Scholar]
  21. de Vocht M. L., Reviakine I., Wösten H. A., Brisson A., Wessels J. G., Robillard G. T. ( 2000). Structural and functional role of the disulfide bridges in the hydrophobin SC3. J Biol Chem 275:28428–28432 [View Article][PubMed]
     [Google Scholar]
  22. Díaz-Corrales F. J., Colasante C., Contreras Q., Puig M., Serrano J. A., Hernández L., Beaman B. L. ( 2004). Nocardia otitidiscaviarum (GAM-5) induces parkinsonian-like alterations in mouse. Braz J Med Biol Res 37:539–548 [View Article][PubMed]
     [Google Scholar]
  23. Dueholm M. S., Petersen S. V., Sønderkær M., Larsen P., Christiansen G., Hein K. L., Enghild J. J., Nielsen J. L., Nielsen K. L. & other authors ( 2010). Functional amyloid in Pseudomonas . Mol Microbiol 77:1009–1020[PubMed]
     [Google Scholar]
  24. Ehrnhoefer D. E., Bieschke J., Boeddrich A., Herbst M., Masino L., Lurz R., Engemann S., Pastore A., Wanker E. E. ( 2008). EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat Struct Mol Biol 15:558–566 [View Article][PubMed]
     [Google Scholar]
  25. Ellefsen B., Holm-Pedersen P., Morse D. E., Schroll M., Andersen B. B., Waldemar G. ( 2008). Caries prevalence in older persons with and without dementia. J Am Geriatr Soc 56:59–67 [View Article][PubMed]
     [Google Scholar]
  26. Epstein E. A., Chapman M. R. ( 2008). Polymerizing the fibre between bacteria and host cells: the biogenesis of functional amyloid fibres. Cell Microbiol 10:1413–1420 [View Article][PubMed]
     [Google Scholar]
  27. Epstein E. A., Reizian M. A., Chapman M. R. ( 2009). Spatial clustering of the curlin secretion lipoprotein requires curli fiber assembly. J Bacteriol 191:608–615 [View Article][PubMed]
     [Google Scholar]
  28. Fowler D. M., Koulov A. V., Balch W. E., Kelly J. W. ( 2007). Functional amyloid – from bacteria to humans. Trends Biochem Sci 32:217–224 [View Article][PubMed]
     [Google Scholar]
  29. Garcia M. C., Lee J. T., Ramsook C. B., Alsteens D., Dufrêne Y. F., Lipke P. N. ( 2011). A role for amyloid in cell aggregation and biofilm formation. PLoS ONE 6:e17632 [View Article][PubMed]
     [Google Scholar]
  30. Gebbink M. F., Claessen D., Bouma B., Dijkhuizen L., Wösten H. A. ( 2005). Amyloids – a functional coat for microorganisms. Nat Rev Microbiol 3:333–341 [View Article][PubMed]
     [Google Scholar]
  31. Grelle G., Otto A., Lorenz M., Frank R. F., Wanker E. E., Bieschke J. ( 2011). Black tea theaflavins inhibit formation of toxic amyloid-β and α-synuclein fibrils. Biochemistry 50:10624–10636 [View Article][PubMed]
     [Google Scholar]
  32. Hammer N. D., Schmidt J. C., Chapman M. R. ( 2007). The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci U S A 104:12494–12499 [View Article][PubMed]
     [Google Scholar]
  33. Harper J. D., Lansbury P. T. Jr ( 1997). Models of amyloid seeding in Alzheimer’s disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins. Annu Rev Biochem 66:385–407 [View Article][PubMed]
     [Google Scholar]
  34. Heiser V., Scherzinger E., Boeddrich A., Nordhoff E., Lurz R., Schugardt N., Lehrach H., Wanker E. E. ( 2000). Inhibition of huntingtin fibrillogenesis by specific antibodies and small molecules: implications for Huntington’s disease therapy. Proc Natl Acad Sci U S A 97:6739–6744 [View Article][PubMed]
     [Google Scholar]
  35. Hett E. C., Hung D. T. ( 2009). Targeting multiple biofilm pathways. Chem Biol 16:1216–1218 [View Article][PubMed]
     [Google Scholar]
  36. Howie A. J., Brewer D. B., Howell D., Jones A. P. ( 2008). Physical basis of colors seen in Congo red-stained amyloid in polarized light. Lab Invest 88:232–242 [View Article][PubMed]
     [Google Scholar]
  37. Jenkinson H. F., Demuth D. R. ( 1997). Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol 23:183–190 [View Article][PubMed]
     [Google Scholar]
  38. Jin L. W., Claborn K. A., Kurimoto M., Geday M. A., Maezawa I., Sohraby F., Estrada M., Kaminksy W., Kahr B. ( 2003). Imaging linear birefringence and dichroism in cerebral amyloid pathologies. Proc Natl Acad Sci U S A 100:15294–15298 [View Article][PubMed]
     [Google Scholar]
  39. Klunk W. E., Jacob R. F., Mason R. P. ( 1999). Quantifying amyloid beta-peptide (Abeta) aggregation using the Congo red-Abeta (CR-abeta) spectrophotometric assay. Anal Biochem 266:66–76 [View Article][PubMed]
     [Google Scholar]
  40. Koga T., Asakawa H., Okahashi N., Hamada S. ( 1986). Sucrose-dependent cell adherence and cariogenicity of serotype c Streptococcus mutans . J Gen Microbiol 132:2873–2883[PubMed]
     [Google Scholar]
  41. Kolodkin-Gal I., Romero D., Cao S., Clardy J., Kolter R., Losick R. ( 2010). d-Amino acids trigger biofilm disassembly. Science 328:627–629 [View Article][PubMed]
     [Google Scholar]
  42. Kuner P., Bohrmann B., Tjernberg L. O., Näslund J., Huber G., Celenk S., Grüninger-Leitch F., Richards J. G., Jakob-Roetne R. & other authors ( 2000). Controlling polymerization of beta-amyloid and prion-derived peptides with synthetic small molecule ligands. J Biol Chem 275:1673–1678 [View Article][PubMed]
     [Google Scholar]
  43. Kwan A. H., Winefield R. D., Sunde M., Matthews J. M., Haverkamp R. G., Templeton M. D., Mackay J. P. ( 2006). Structural basis for rodlet assembly in fungal hydrophobins. Proc Natl Acad Sci U S A 103:3621–3626 [View Article][PubMed]
     [Google Scholar]
  44. Lam H., Oh D. C., Cava F., Takacs C. N., Clardy J., de Pedro M. A., Waldor M. K. ( 2009). d-Amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552–1555 [View Article][PubMed]
     [Google Scholar]
  45. Lamont R. J., El-Sabaeny A., Park Y., Cook G. S., Costerton J. W., Demuth D. R. ( 2002). Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology 148:1627–1636[PubMed]
     [Google Scholar]
  46. Larsen P., Nielsen J. L., Dueholm M. S., Wetzel R., Otzen D., Nielsen P. H. ( 2007). Amyloid adhesins are abundant in natural biofilms. Environ Microbiol 9:3077–3090 [View Article][PubMed]
     [Google Scholar]
  47. Larsen P., Nielsen J. L., Otzen D., Nielsen P. H. ( 2008). Amyloid-like adhesins produced by floc-forming and filamentous bacteria in activated sludge. Appl Environ Microbiol 74:1517–1526 [View Article][PubMed]
     [Google Scholar]
  48. Larson M. R., Rajashankar K. R., Patel M. H., Robinette R. A., Crowley P. J., Michalek S., Brady L. J., Deivanayagam C. ( 2010). Elongated fibrillar structure of a streptococcal adhesin assembled by the high-affinity association of alpha- and PPII-helices. Proc Natl Acad Sci U S A 107:5983–5988 [View Article][PubMed]
     [Google Scholar]
  49. Larson M. R., Rajashankar K. R., Crowley P. J., Kelly C., Mitchell T. J., Brady L. J., Deivanayagam C. ( 2011). Crystal structure of the C-terminal region of Streptococcus mutans antigen I/II and characterization of salivary agglutinin adherence domains. J Biol Chem 286:21657–21666 [View Article][PubMed]
     [Google Scholar]
  50. Lee S. F., Progulske-Fox A., Erdos G. W., Piacentini D. A., Ayakawa G. Y., Crowley P. J., Bleiweis A. S. ( 1989). Construction and characterization of isogenic mutants of Streptococcus mutans deficient in major surface protein antigen P1 (I/II). Infect Immun 57:3306–3313[PubMed]
     [Google Scholar]
  51. Lopez del Amo J. M., Fink U., Dasari M., Grelle G., Wanker E. E., Bieschke J., Reif B. ( 2012). Structural properties of EGCG-induced, nontoxic Alzheimer’s disease Aβ oligomers. J Mol Biol 421:517–524 [View Article][PubMed]
     [Google Scholar]
  52. Lundmark K., Westermark G. T., Nyström S., Murphy C. L., Solomon A., Westermark P. ( 2002). Transmissibility of systemic amyloidosis by a prion-like mechanism. Proc Natl Acad Sci U S A 99:6979–6984 [View Article][PubMed]
     [Google Scholar]
  53. Lundmark K., Westermark G. T., Olsén A., Westermark P. ( 2005). Protein fibrils in nature can enhance amyloid protein A amyloidosis in mice: cross-seeding as a disease mechanism. Proc Natl Acad Sci U S A 102:6098–6102 [View Article][PubMed]
     [Google Scholar]
  54. MacDonald A. B. ( 2006). Plaques of Alzheimer’s disease originate from cysts of Borrelia burgdorferi, the Lyme disease spirochete. Med Hypotheses 67:592–600 [View Article][PubMed]
     [Google Scholar]
  55. Mackay J. P., Matthews J. M., Winefield R. D., Mackay L. G., Haverkamp R. G., Templeton M. D. ( 2001). The hydrophobin EAS is largely unstructured in solution and functions by forming amyloid-like structures. Structure 9:83–91 [View Article][PubMed]
     [Google Scholar]
  56. Macrina F. L., Tobian J. A., Jones K. R., Evans R. P., Clewell D. B. ( 1982). A cloning vector able to replicate in Escherichia coli and Streptococcus sanguis . Gene 19:345–353 [View Article][PubMed]
     [Google Scholar]
  57. Maury C. P. ( 2009a). The emerging concept of functional amyloid. J Intern Med 265:329–334 [View Article][PubMed]
     [Google Scholar]
  58. Maury C. P. ( 2009b). Self-propagating β-sheet polypeptide structures as prebiotic informational molecular entities: the amyloid world. Orig Life Evol Biosph 39:141–150 [View Article][PubMed]
     [Google Scholar]
  59. McArthur W. P., Rhodin N. R., Seifert T. B., Oli M. W., Robinette R. A., Demuth D. R., Brady L. J. ( 2007). Characterization of epitopes recognized by anti-Streptococcus mutans P1 monoclonal antibodies. FEMS Immunol Med Microbiol 50:342–353 [View Article][PubMed]
     [Google Scholar]
  60. Miklossy J., Kis A., Radenovic A., Miller L., Forro L., Martins R., Reiss K., Darbinian N., Darekar P., Mihaly L. ( 2006). Beta-amyloid deposition and Alzheimer’s type changes induced by Borrelia spirochetes. Neurobiol Aging 27:228–236 [View Article][PubMed]
     [Google Scholar]
  61. Necula M., Kayed R., Milton S., Glabe C. G. ( 2007). Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J Biol Chem 282:10311–10324 [View Article][PubMed]
     [Google Scholar]
  62. Nilsson M. R. ( 2004). Techniques to study amyloid fibril formation in vitro . Methods 34:151–160 [View Article][PubMed]
     [Google Scholar]
  63. Nobbs A. H., Vajna R. M., Johnson J. R., Zhang Y., Erlandsen S. L., Oli M. W., Kreth J., Brady L. J., Herzberg M. C. ( 2007). Consequences of a sortase A mutation in Streptococcus gordonii . Microbiology 153:4088–4097 [View Article][PubMed]
     [Google Scholar]
  64. Nobbs A. H., Lamont R. J., Jenkinson H. F. ( 2009). Streptococcus adherence and colonization. Microbiol Mol Biol Rev 73:407–450 [View Article][PubMed]
     [Google Scholar]
  65. Nylander A., Forsgren N., Persson K. ( 2011). Structure of the C-terminal domain of the surface antigen SpaP from the caries pathogen Streptococcus mutans . Acta Crystallogr Sect F Struct Biol Cryst Commun 67:23–26 [View Article][PubMed]
     [Google Scholar]
  66. Otoo H. N., Lee K. G., Qiu W., Lipke P. N. ( 2008). Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot Cell 7:776–782 [View Article][PubMed]
     [Google Scholar]
  67. Otzen D., Nielsen P. H. ( 2008). We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65:910–927 [View Article][PubMed]
     [Google Scholar]
  68. Palmer S. R., Crowley P. J., Oli M. W., Ruelf M. A., Michalek S. M., Brady L. J. ( 2012). YidC1 and YidC2 are functionally distinct proteins involved in protein secretion, biofilm formation and cariogenicity of Streptococcus mutans . Microbiology 158:1702–1712 [View Article][PubMed]
     [Google Scholar]
  69. Porat Y., Abramowitz A., Gazit E. ( 2006). Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem Biol Drug Des 67:27–37 [View Article][PubMed]
     [Google Scholar]
  70. Ramsook C. B., Tan C., Garcia M. C., Fung R., Soybelman G., Henry R., Litewka A., O’Meally S., Otoo H. N. & other authors ( 2010). Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot Cell 9:393–404 [View Article][PubMed]
     [Google Scholar]
  71. Rauceo J. M., Gaur N. K., Lee K. G., Edwards J. E., Klotz S. A., Lipke P. N. ( 2004). Global cell surface conformational shift mediated by a Candida albicans adhesin. Infect Immun 72:4948–4955 [View Article][PubMed]
     [Google Scholar]
  72. Robinette R. A., Oli M. W., McArthur W. P., Brady L. J. ( 2011). A therapeutic anti-Streptococcus mutans monoclonal antibody used in human passive protection trials influences the adaptive immune response. Vaccine 29:6292–6300 [View Article][PubMed]
     [Google Scholar]
  73. Romero D., Aguilar C., Losick R., Kolter R. ( 2010). Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A 107:2230–2234 [View Article][PubMed]
     [Google Scholar]
  74. Romero D., Vlamakis H., Losick R., Kolter R. ( 2011). An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol 80:1155–1168 [View Article][PubMed]
     [Google Scholar]
  75. Römling U., Bian Z., Hammar M., Sierralta W. D., Normark S. ( 1998). Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180:722–731[PubMed]
     [Google Scholar]
  76. Saldaña Z., Xicohtencatl-Cortes J., Avelino F., Phillips A. D., Kaper J. B., Puente J. L., Girón J. A. ( 2009). Synergistic role of curli and cellulose in cell adherence and biofilm formation of attaching and effacing Escherichia coli and identification of Fis as a negative regulator of curli. Environ Microbiol 11:992–1006 [View Article][PubMed]
     [Google Scholar]
  77. Sato T., Hu J. P., Ohki K., Yamaura M., Washio J., Matsuyama J., Takahashi N. ( 2003). Identification of mutans streptococci by restriction fragment length polymorphism analysis of polymerase chain reaction-amplified 16S ribosomal RNA genes. Oral Microbiol Immunol 18:323–326 [View Article][PubMed]
     [Google Scholar]
  78. Sawyer E. B., Claessen D., Haas M., Hurgobin B., Gras S. L. ( 2011). The assembly of individual chaplin peptides from Streptomyces coelicolor into functional amyloid fibrils. PLoS ONE 6:e18839 [View Article][PubMed]
     [Google Scholar]
  79. Schaeken M. J., van der Hoeven J. S., Franken H. C. ( 1986). Comparative recovery of Streptococcus mutans on five isolation media, including a new simple selective medium. J Dent Res 65:906–908 [View Article][PubMed]
     [Google Scholar]
  80. Schwartz K., Syed A. K., Stephenson R. E., Rickard A. H., Boles B. R. ( 2012). Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog 8:e1002744 [View Article][PubMed]
     [Google Scholar]
  81. Sharp A., Crabb S. J., Johnson P. W., Hague A., Cutress R., Townsend P. A., Ganesan A., Packham G. ( 2009). Thioflavin S (NSC71948) interferes with Bcl-2-associated athanogene (BAG-1)-mediated protein–protein interactions. J Pharmacol Exp Ther 331:680–689 [View Article][PubMed]
     [Google Scholar]
  82. Shewmaker F., McGlinchey R. P., Thurber K. R., McPhie P., Dyda F., Tycko R., Wickner R. B. ( 2009). The functional curli amyloid is not based on in-register parallel β-sheet structure. J Biol Chem 284:25065–25076 [View Article][PubMed]
     [Google Scholar]
  83. Smith J. F., Knowles T. P., Dobson C. M., Macphee C. E., Welland M. E. ( 2006). Characterization of the nanoscale properties of individual amyloid fibrils. Proc Natl Acad Sci U S A 103:15806–15811 [View Article][PubMed]
     [Google Scholar]
  84. Takahashi N., Nyvad B. ( 2008). Caries ecology revisited: microbial dynamics and the caries process. Caries Res 42:409–418 [View Article][PubMed]
     [Google Scholar]
  85. Ton-That H., Marraffini L. A., Schneewind O. ( 2004). Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim Biophys Acta 1694:269–278 [View Article][PubMed]
     [Google Scholar]
  86. Troffer-Charlier N., Ogier J., Moras D., Cavarelli J. ( 2002). Crystal structure of the V-region of Streptococcus mutans antigen I/II at 2.4 Å resolution suggests a sugar preformed binding site. J Mol Biol 318:179–188 [View Article][PubMed]
     [Google Scholar]
  87. Wang X., Chapman M. R. ( 2008). Sequence determinants of bacterial amyloid formation. J Mol Biol 380:570–580 [View Article][PubMed]
     [Google Scholar]
  88. Zhou Y., Blanco L. P., Smith D. R., Chapman M. R. ( 2012). Bacterial amyloids. Methods Mol Biol 849:303–320 [View Article][PubMed]
     [Google Scholar]
  89. Zogaj X., Bokranz W., Nimtz M., Römling U. ( 2003). Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect Immun 71:4151–4158 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.060855-0
Loading
Functional amyloid formation by Streptococcus mutans
Microbiology 158, 2903 (2012); https://doi.org/10.1099/mic.0.060855-0
/content/journal/micro/10.1099/mic.0.060855-0
/content/journal/micro/10.1099/mic.0.060855-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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