The E. coli CsgB nucleator of curli assembles to β-sheet oligomers that alter the CsgA fibrillization mechanism

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 17, 2012, Pages 6502-6507

  Shu, Qin ^a   Crick, Scott L ^a   Pinkner, Jerome S ^a   Ford, Bradley ^a   Hultgren, Scott J ^a   Frieden, Carl ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atomic force microscopy; Biofilm formation; Circular dichroism; Thioflavin T

Indexed keywords

AMYLOID PROTEIN; BACTERIAL PROTEIN; CURLI; OLIGOMER; PROTEIN CSGA; PROTEIN CSGB; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; CIRCULAR DICHROISM; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN STRUCTURE;

BIOPOLYMERS; CIRCULAR DICHROISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE; KINETICS; MICROSCOPY, ATOMIC FORCE; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84860171314     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1204161109     Document Type: Article

References (35)

1. Olsén A, Jonsson A, Normark S (1989) Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338:652-655. (Pubitemid 19104644)
2. Collinson SK, Emödy L, Müller KH, Trust TJ, Kay WW (1991) Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol 173:4773-4781.
3. Collinson SK, Emödy L, Trust TJ, Kay WW (1992) Thin aggregative fimbriae from diarrheagenic Escherichia coli. J Bacteriol 174:4490-4495.
4. Hammar M, Bian Z, Normark S (1996) Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci USA 93:6562-6566. (Pubitemid 26230347)
5. Bian Z, Normark S (1997) Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli. EMBO J 16:5827-5836. (Pubitemid 27427279)
6. Chapman MR, et al. (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851-855. (Pubitemid 34118365)
7. Barnhart MM, Chapman MR (2006) Curli biogenesis and function. Annu Rev Microbiol 60:131-147. (Pubitemid 44627943)
8. Kikuchi T, Mizunoe Y, Takade A, Naito S, Yoshida S (2005) Curli fibers are required for development of biofilm architecture in Escherichia coli K-12 and enhance bacterial adherence to human uroepithelial cells. Microbiol Immunol 49:875-884. (Pubitemid 41373940)
9. Vidal O, et al. (1998) Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: Involvement of a new ompR allele that increases curli expression. J Bacteriol 180:2442-2449. (Pubitemid 28217359)
10. Austin JW, Sanders G, Kay WW, Collinson SK (1998) Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol Lett 162:295-301. (Pubitemid 28225095)
11. Saldaña Z, et al. (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.
12. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: A common cause of persistent infections. Science 284:1318-1322. (Pubitemid 29289651)
13. Habash M, Reid G (1999) Microbial biofilms: Their development and significance for medical device-related infections. J Clin Pharmacol 39:887-898. (Pubitemid 30644024)
14. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2:95-108. (Pubitemid 39490064)
15. Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34-40. (Pubitemid 40082395)
16. Hatt JK, Rather PN (2008) Role of bacterial biofilms in urinary tract infections. Curr Top Microbiol Immunol 322:163-192.
17. Hammar M, Arnqvist A, Bian Z, Olsén A, Normark S (1995) Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18:661-670. (Pubitemid 26007676)
18. Olsén A, Arnqvist A, Hammar M, Sukupolvi S, Normark S (1993) The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin- binding curli in Escherichia coli. Mol Microbiol 7:523-536. (Pubitemid 23062579)
19. Arnqvist A, Olsén A, Normark S (1994) Sigma S-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by sigma 70 in the absence of the nucleoid-associated protein H-NS. Mol Microbiol 13:1021-1032.
20. Collinson SK, Parker JM, Hodges RS, Kay WW (1999) Structural predictions of AgfA, the insoluble fimbrial subunit of Salmonella thin aggregative fimbriae. J Mol Biol 290:741-756. (Pubitemid 29355705)
21. White AP, et al. (2001) Structure and characterization of AgfB from Salmonella enteritidis thin aggregative fimbriae. J Mol Biol 311:735-749. (Pubitemid 32803732)
22. Wang X, Smith DR, Jones JW, Chapman MR (2007) In vitro polymerization of a functional Escherichia coli amyloid protein. J Biol Chem 282:3713-3719. (Pubitemid 47084435)
23. Hammer ND, Schmidt JC, Chapman MR (2007) The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci USA 104:12494-12499. (Pubitemid 47206166)
24. Shewmaker F, et al. (2009) The functional curli amyloid is not based on in-register parallel beta-sheet structure. J Biol Chem 284:25065-25076.
25. DueholmMS, et al. (2011) Fibrillation of themajor curli subunit CsgA under a wide range of conditions implies a robust design of aggregation. Biochemistry 50:8281-8290.
26. Fowler DM, Koulov AV, Balch WE, Kelly JW (2007) Functional amyloid - from bacteria to humans. Trends Biochem Sci 32:217-224. (Pubitemid 46694328)
27. Groenning M (2009) Binding mode of Thioflavin T and other molecular probes in the context of amyloid fibrils-current status. J Chem Biol 3:1-18.
28. Carrotta R, Bauer R, Waninge R, Rischel C (2001) Conformational characterization of oligomeric intermediates and aggregates in β-lactoglobulin heat aggregation. Protein Sci 10:1312-1318. (Pubitemid 32568098)
29. Liang Y, Lynn DG, Berland KM (2010) Direct observation of nucleation and growth in amyloid self-assembly. J Am Chem Soc 132:6306-6308.
30. Eichner T, Radford SE (2011) A diversity of assembly mechanisms of a generic amyloid fold. Mol Cell 43:8-18.
31. Kreplak L, Aebi U (2006) From the polymorphism of amyloid fibrils to their assembly mechanism and cytotoxicity. Adv Protein Chem 73:217-233. (Pubitemid 44960405)
32. Kayed R, et al. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489. (Pubitemid 36444329)
33. Shorter J, Lindquist S (2004) Hsp104 catalyzes formation and elimination of selfreplicating Sup35 prion conformers. Science 304:1793-1797. (Pubitemid 38787894)
34. Lesné S, et al. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440:352-357.
35. Vassar PS, Culling CF (1959) Fluorescent stains, with special reference to amyloid and connective tissues. Arch Pathol 68:487-498.