A role for amyloid in cell aggregation and biofilm formation

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Garcia, Melissa C ^a   Lee, Janis T ^a   Ramsook, Caleen B ^a   Alsteens, David ^b   Dufrêne, Yves F ^b   Lipke, Peter N ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AMYLOID; CELL ADHESION MOLECULE; PEPTIDE; ALA1 PROTEIN, CANDIDA ALBICANS; CONGO RED; FUNGAL PROTEIN; MUTANT PROTEIN; NANOMATERIAL; POLYSTYRENE DERIVATIVE; THIAZOLE DERIVATIVE; THIOFLAVINE;

AMINO ACID SUBSTITUTION; ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL AGGREGATION; CELL SURFACE; CONTROLLED STUDY; FLUORESCENCE; GENETIC CONSERVATION; LIGAND BINDING; NONHUMAN; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; ADHESION; AMINO ACID SEQUENCE; ATOMIC FORCE MICROSCOPY; CHEMISTRY; CYTOLOGY; DRUG EFFECT; ENZYME SPECIFICITY; GENETICS; METABOLISM; MICROBIAL VIABILITY; MUTATION; PHYSIOLOGY; SOLUBILITY;

CANDIDA ALBICANS; SACCHAROMYCES CEREVISIAE;

ADHESIVENESS; AMINO ACID SEQUENCE; AMYLOID; BIOFILMS; CANDIDA ALBICANS; CELL ADHESION MOLECULES; CONGO RED; FLUORESCENCE; FUNGAL PROTEINS; MICROBIAL VIABILITY; MICROSCOPY, ATOMIC FORCE; MUTANT PROTEINS; MUTATION; NANOSTRUCTURES; PEPTIDES; POLYSTYRENES; SACCHAROMYCES CEREVISIAE; SOLUBILITY; SUBSTRATE SPECIFICITY; THIAZOLES;

EID: 79952425203     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017632     Document Type: Article

References (54)

1. Harriott MM, Noverr MC, (2009) Candida albicans and Staphylococcus aureus form polymicrobial biofilms: effects on antimicrobial resistance. Antimicrob Agents Chemother 53: 3914-3922.
2. Chandra J, Mukherjee PK, Leidich SD, Faddoul FF, Hoyer LL, et al. (2001) Antifungal resistance of candidal biofilms formed on denture acrylic in vitro. J Dent Res 80: 903-908.
3. Hawser SP, Douglas LJ, (1995) Resistance of Candida albicans biofilms to antifungal agents in vitro. Antimicrob Agents Chemother 39: 2128-2131.
4. Uppuluri P, Chaturvedi AK, Srinivasan A, Banerjee M, Ramasubramaniam AK, et al. (2010) Dispersion as an important step in the Candida albicans biofilm developmental cycle. PLoS Pathog 6: e1000828.
5. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, et al. (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183: 5385-5394.
6. Hoyer LL, Green CB, Oh SH, Zhao X, (2008) Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family-a sticky pursuit. Med Mycol 46: 1-15.
7. Sheppard DC, Yeaman MR, Welch WH, Phan QT, Fu Y, et al. (2004) Functional and structural diversity in the Als protein family of Candida albicans. J Biol Chem 279: 30480-30489.
8. Rauceo JM, Gaur NK, Lee KG, Edwards JE, Klotz SA, et al. (2004) Global cell surface conformational shift mediated by a Candida albicans adhesin. Infect Immun 72: 4948-4955.
9. Hoyer LL, Hecht JE, (2001) The ALS5 gene of Candida albicans and analysis of the Als5p N-terminal domain. Yeast 18: 49-60.
10. Otoo HN, Lee KG, Qiu W, Lipke PN, (2008) Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot Cell 7: 776-782.
11. Ramsook CB, Tan C, Garcia MC, Fung R, Soybelman G, et al. (2010) Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot Cell 9: 393-404.
12. Frank AT, Ramsook CB, Otoo HN, Tan C, Soybelman G, et al. (2010) Structure and function of glycosylated tandem repeats from Candida albicans Als adhesins. Eukaryot Cell 9: 405-414.
13. Rauceo JM, De Armond R, Otoo H, Kahn PC, Klotz SA, et al. (2006) Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot Cell 5: 1664-1673.
14. Dranginis AM, Rauceo JM, Coronado JE, Lipke PN, (2007) A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev 71: 282-294.
15. Nobile CJ, Schneider HA, Nett JE, Sheppard DC, Filler SG, et al. (2008) Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18: 1017-1024.
16. Klotz SA, Gaur NK, De Armond R, Sheppard D, Khardori N, et al. (2007) Candida albicans Als proteins mediate aggregation with bacteria and yeasts. Med Mycol 45: 363-370.
17. Nobbs AH, Vickerman MM, Jenkinson HF, (2010) Heterologous Expression of Candida albicans Cell Wall-Associated Adhesins in Saccharomyces cerevisiae Reveals Differential Specificities in Adherence and Biofilm Formation and in Binding Oral Streptococcus gordonii. Eukaryot Cell 9: 1622-1634.
18. Silverman RJ, Nobbs AH, Vickerman MM, Barbour ME, Jenkinson HF, (2010) Interaction of Candida albicans Cell-Wall Als3 Protein with Streptococcus gordonii SspB Adhesin Promotes Development of Mixed Species Communities. Infect Immun.
19. ten Cate JM, Klis FM, Pereira-Cenci T, Crielaard W, de Groot PW, (2009) Molecular and cellular mechanisms that lead to Candida biofilm formation. J Dent Res 88: 105-115.
20. Gaur NK, Klotz SA, Henderson RL, (1999) Overexpression of the Candida albicans ALA1 gene in Saccharomyces cerevisiae results in aggregation following attachment of yeast cells to extracellular matrix proteins, adherence properties similar to those of Candida albicans. Infect Immun 67: 6040-6047.
21. Gaur NK, Klotz SA, (2004) Accessibility of the peptide backbone of protein ligands is a key specificity determinant in Candida albicans SRS adherence. Microbiology 150: 277-284.
22. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, et al. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447: 453-457.
23. Jahn TR, Makin OS, Morris KL, Marshall KE, Tian P, et al. (2010) The common architecture of cross-beta amyloid. J Mol Biol 395: 717-727.
24. Chiti F, Webster P, Taddei N, Clark A, Stefani M, et al. (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc Natl Acad Sci U S A 96: 3590-3594.
25. Feng BY, Toyama BH, Wille H, Colby DW, Collins SR, et al. (2008) Small-molecule aggregates inhibit amyloid polymerization. Nat Chem Biol 4: 197-199.
26. Maezawa I, Hong HS, Liu R, Wu CY, Cheng RH, et al. (2008) Congo red and thioflavin-T analogs detect Abeta oligomers. J Neurochem 104: 457-468.
27. Inbar P, Yang J, (2006) Inhibiting protein-amyloid interactions with small molecules: a surface chemistry approach. Bioorg Med Chem Lett 16: 1076-1079.
28. Kim YS, Randolph TW, Manning MC, Stevens FJ, Carpenter JF, (2003) Congo red populates partially unfolded states of an amyloidogenic protein to enhance aggregation and amyloid fibril formation. J Biol Chem 278: 10842-10850.
29. Lorenzo A, Yankner BA, (1996) Amyloid fibril toxicity in Alzheimer's disease and diabetes. Ann N Y Acad Sci 777: 89-95.
30. Cegelski L, Pinkner JS, Hammer ND, Cusumano CK, Hung CS, et al. (2009) Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 5: 913-919.
31. 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.
32. Wang X, Hammer ND, Chapman MR, (2008) The molecular basis of functional bacterial amyloid polymerization and nucleation. J Biol Chem 283: 21530-21539.
33. Simkovsky R, King J, (2006) An elongated spine of buried core residues necessary for in vivo folding of the parallel beta-helix of P22 tailspike adhesin. Proc Natl Acad Sci U S A 103: 3575-3580.
34. de Jong W, Wosten HA, 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.
35. Alberti S, Halfmann R, King O, Kapila A, Lindquist S, (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137: 146-158.
36. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, et al. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325: 328-332.
37. Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, et al. (2006) Functional amyloid formation within mammalian tissue. PLoS Biol 4: e6.
38. Muller DJ, Helenius J, Alsteens D, Dufrene YF, (2009) Force probing surfaces of living cells to molecular resolution. Nat Chem Biol 5: 383-390.
39. Gaur NK, Klotz SA, (1997) Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect Immun 65: 5289-5294.
40. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, et al. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274: 99-102.
41. Ram AF, Klis FM, (2006) Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protocol 1: 2253-6.
42. Reynolds TB, Fink GR, (2001) Bakers' yeast, a model for fungal biofilm formation. Science 291: 878-881.
43. Alsteens D, Garcia MC, Lipke PN, Dufrene YF, (2010) Force-induced formation and propagation of adhesion nanodomains in living fungal cells. Proc Natl Acad Sci U S A in press.
44. Alsteens D, Dupres V, Klotz SA, Gaur NK, Lipke PN, et al. (2009) Unfolding Individual Als5p Adhesion Proteins on Live Cells. ACS Nano 3: 3063-3068.
45. Fernandez-Escamilla A-M, Rousseau F, Schymkowitz J, Serrano L, (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotech 22: 1302-1306.
46. Eisert R, Felau L, Brown LR, (2006) Methods for enhancing the accuracy and reproducibility of Congo red and thioflavin T assays. Anal Biochem 353: 144-146.
47. Lockhart A, Ye L, Judd DB, Merritt AT, Lowe PN, et al. (2005) Evidence for the presence of three distinct binding sites for the thioflavin T class of Alzheimer's disease PET imaging agents on beta-amyloid peptide fibrils. J Biol Chem 280: 7677-7684.
48. Granic I, Masman MF, Kees Mulder C, Nijholt IM, Naude PJ, et al. (2010) LPYFDa neutralizes amyloid-beta-induced memory impairment and toxicity. J Alzheimers Dis 19: 991-1005.
49. Citron M, (2010) Alzheimer's disease: strategies for disease modification. Nat Rev Drug Discov 9: 387-398.
50. Loza L, Fu Y, Ibrahim AS, Sheppard DC, Filler SG, et al. (2004) Functional analysis of the Candida albicans ALS1 gene product. Yeast 21: 473-482.
51. Cantor CR, Schimmel PR, (1980) The behavior of biological macromolecules. San Francisco W. H. Freeman pp. 878-893.
52. Gaur NK, Smith RL, Klotz SA, (2002) Candida albicans and Saccharomyces cerevisiae expressing ALA1/ALS5 adhere to accessible threonine, serine, or alanine patches. Cell Commun Adhes 9: 45-57.
53. Kapteyn JC, Hoyer LL, Hecht JE, Muller WH, Andel A, et al. (2000) The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol 35: 601-611.
54. Gonzalez M, Goddard N, Hicks C, Ovalle R, Rauceo JM, et al. (2010) A screen for deficiencies in GPI-anchorage of wall glycoproteins in yeast. Yeast 27: 583-596.