The C-terminal repeating units of CsgB direct bacterial functional amyloid nucleation

Journal of Molecular Biology

Volumn 422, Issue 3, 2012, Pages 376-389

  Hammer, Neal D ^a   McGuffie, Bryan A ^b   Zhou, Yizhou ^b   Badtke, Matthew P ^b   Reinke, Ashley A ^b   Brännström, Kristoffer ^c   Gestwicki, Jason E ^b   Olofsson, Anders ^c   Almqvist, Fredrik ^c   Chapman, Matthew R ^b,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UMEÅ UNIVERSITY   (Sweden)

Author keywords

functional amyloid; nucleator; polymerization

Indexed keywords

AMYLOID; CURLI FIBER SUBUNIT PROTEIN A; CURLI FIBER SUBUNIT PROTEIN B; SELF ASSEMBLED MONOLAYER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; CONTROLLED STUDY; DELETION MUTANT; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OUTER MEMBRANE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN PURIFICATION; WILD TYPE;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE;

EID: 84865098035     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.05.043     Document Type: Article

References (62)

1. F.E. Cohen, and J.W. Kelly Therapeutic approaches to protein-misfolding diseases Nature 426 2003 905 909
2. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366
3. J.T. Jarrett, and P.T. Lansbury Jr Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73 1993 1055 1058
4. A. Lomakin, D.S. Chung, G.B. Benedek, D.A. Kirschner, and D.B. Teplow On the nucleation and growth of amyloid beta-protein fibrils: detection of nuclei and quantitation of rate constants Proc. Natl Acad. Sci. USA 93 1996 1125 1129
5. J.S. Pedersen, G. Christensen, and D.E. Otzen Modulation of S6 fibrillation by unfolding rates and gatekeeper residues J. Mol. Biol. 341 2004 575 588
6. T.R. Serio, A.G. Cashikar, A.S. Kowal, G.J. Sawicki, J.J. Moslehi, and L. Serpell Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 289 2000 1317 1321
7. V.N. Uversky, J. Li, P. Souillac, I.S. Millett, S. Doniach, and R. Jakes Biophysical properties of the synucleins and their propensities to fibrillate: inhibition of alpha-synuclein assembly by beta- and gamma-synucleins J. Biol. Chem. 277 2002 11970 11978
8. X. Wang, D.R. Smith, J.W. Jones, and M.R. Chapman In vitro polymerization of a functional Escherichia coli amyloid protein J. Biol. Chem. 282 2007 3713 3719
9. J.C. Rochet, and P.T. Lansbury Jr Amyloid fibrillogenesis: themes and variations Curr. Opin. Struct. Biol. 10 2000 60 68
10. M.R. Chapman, L.S. Robinson, J.S. Pinkner, R. Roth, J. Heuser, and M. Hammar Role of Escherichia coli curli operons in directing amyloid fiber formation Science 295 2002 851 855
11. D.M. Fowler, A.V. Koulov, C. Alory-Jost, M.S. Marks, W.E. Balch, and J.W. Kelly Functional amyloid formation within mammalian tissue PLoS Biol. 4 2006 e6
12. T.R. Serio, and S.L. Lindquist The yeast prion [PSI +]: molecular insights and functional consequences Adv. Protein Chem. 59 2001 391 412
13. X. Wang, M. Rochon, A. Lamprokostopoulou, H. Lunsdorf, M. Nimtz, and U. Romling Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29 Cell. Mol. Life Sci. 63 2006 2352 2363
14. M.M. Barnhart, and M.R. Chapman Curli biogenesis and function Annu. Rev. Microbiol. 60 2006 131 147
15. U. Gerstel, and U. Romling The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium Res. Microbiol. 154 2003 659 667
16. A. Olsen, A. Jonsson, and S. Normark Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli Nature 338 1989 652 655
17. G.A. Uhlich, P.H. Cooke, and E.B. Solomon Analyses of the red-dry-rough phenotype of an Escherichia coli O157:H7 strain and its role in biofilm formation and resistance to antibacterial agents Appl. Environ. Microbiol. 72 2006 2564 2572
18. O. Vidal, R. Longin, C. Prigent-Combaret, C. Dorel, M. Hooreman, and P. Lejeune 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 1998 2442 2449
19. L. Cegelski, G.R. Marshall, G.R. Eldridge, and S.J. Hultgren The biology and future prospects of antivirulence therapies Nat. Rev. Microbiol. 6 2008 17 27
20. A.E. Clatworthy, E. Pierson, and D.T. Hung Targeting virulence: a new paradigm for antimicrobial therapy Nat. Chem. Biol. 3 2007 541 548
21. Y.M. Lee, F. Almqvist, and S.J. Hultgren Targeting virulence for antimicrobial chemotherapy Curr. Opin. Pharmacol. 3 2003 513 519
22. L. Cegelski, J.S. Pinkner, N.D. Hammer, C.K. Cusumano, C.S. Hung, and E. Chorell Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation Nat. Chem. Biol. 5 2009 913 919
23. E. Chorell, C. Bengtsson, T.S. Banchelin, P. Das, H. Uvell, and A.K. Sinha Synthesis and application of a bromomethyl substituted scaffold to be used for efficient optimization of anti-virulence activity Eur. J. Med. Chem. 46 2011 1103 1116
24. I. Horvath, C.F. Weise, E.K. Andersson, E. Chorell, M. Sellstedt, and C. Bengtsson Mechanisms of protein oligomerization: inhibitor of functional amyloids templates alpha-synuclein fibrillation J. Am. Chem. Soc. 2012
25. Z. Bian, and S. Normark Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli EMBO J. 16 1997 5827 5836
26. M. Hammar, Z. Bian, and S. Normark Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli Proc. Natl Acad. Sci. USA 93 1996 6562 6566
27. A.P. White, S.K. Collinson, P.A. Banser, D.L. Gibson, M. Paetzel, N.C. Strynadka, and W.W. Kay Structure and characterization of AgfB from Salmonella enteritidis thin aggregative fimbriae J. Mol. Biol. 311 2001 735 749
28. M. Hammar, A. Arnqvist, Z. Bian, A. Olsen, and S. Normark 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 1995 661 670
29. H. Loferer, M. Hammar, and S. Normark Availability of the fibre subunit CsgA and the nucleator protein CsgB during assembly of fibronectin-binding curli is limited by the intracellular concentration of the novel lipoprotein CsgG Mol. Microbiol. 26 1997 11 23
30. X. Wang, and M.R. Chapman Sequence determinants of bacterial amyloid formation J. Mol. Biol. 380 2008 570 580
31. X. Wang, N.D. Hammer, and M.R. Chapman The molecular basis of functional bacterial amyloid polymerization and nucleation J. Biol. Chem. 283 2008 21530 21539
32. S.K. Collinson, J.M. Parker, R.S. Hodges, and W.W. Kay Structural predictions of AgfA, the insoluble fimbrial subunit of Salmonella thin aggregative fimbriae J. Mol. Biol. 290 1999 741 756
33. F. Shewmaker, R.P. McGlinchey, K.R. Thurber, P. McPhie, F. Dyda, R. Tycko, and R.B. Wickner The functional curli amyloid is not based on in-register parallel beta-sheet structure J. Biol. Chem. 284 2009 25065 25076
34. N.D. Hammer, J.C. Schmidt, and M.R. Chapman The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization Proc. Natl Acad. Sci. USA 104 2007 12494 12499
35. A.A. Nenninger, L.S. Robinson, N.D. Hammer, E.A. Epstein, M.P. Badtke, S.J. Hultgren, and M.R. Chapman CsgE is a curli secretion specificity factor that prevents amyloid fibre aggregation Mol. Microbiol. 81 2011 486 499
36. L.S. Robinson, E.M. Ashman, S.J. Hultgren, and M.R. Chapman Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein Mol. Microbiol. 59 2006 870 881
37. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, and J. Zurdo Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 2002 507 511
38. J. Larson, G. Lynch, D. Games, and P. Seubert Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice Brain Res. 840 1999 23 35
39. L.F. Lue, Y.M. Kuo, A.E. Roher, L. Brachova, Y. Shen, and L. Sue Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease Am. J. Pathol. 155 1999 853 862
40. M. Malisauskas, J. Ostman, A. Darinskas, V. Zamotin, E. Liutkevicius, E. Lundgren, and L.A. Morozova-Roche Does the cytotoxic effect of transient amyloid oligomers from common equine lysozyme in vitro imply innate amyloid toxicity? J. Biol. Chem. 280 2005 6269 6275
41. C.A. McLean, R.A. Cherny, F.W. Fraser, S.J. Fuller, M.J. Smith, and K. Beyreuther Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease Ann. Neurol. 46 1999 860 866
42. D. Moechars, I. Dewachter, K. Lorent, D. Reverse, V. Baekelandt, and A. Naidu Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain J. Biol. Chem. 274 1999 6483 6492
43. I. Sirangelo, C. Malmo, C. Iannuzzi, A. Mezzogiorno, M.R. Bianco, M. Papa, and G. Irace Fibrillogenesis and cytotoxic activity of the amyloid-forming apomyoglobin mutant W7FW14F J. Biol. Chem. 279 2004 13183 13189
44. M.M. Sousa, I. Cardoso, R. Fernandes, A. Guimaraes, and M.J. Saraiva Deposition of transthyretin in early stages of familial amyloidotic polyneuropathy: evidence for toxicity of nonfibrillar aggregates Am. J. Pathol. 159 2001 1993 2000
45. J. Wang, D.W. Dickson, J.Q. Trojanowski, and V.M. Lee The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging Exp. Neurol. 158 1999 328 337
46. M. Bokvist, F. Lindstrom, A. Watts, and G. Grobner Two types of Alzheimer's beta-amyloid (1-40) peptide membrane interactions: aggregation preventing transmembrane anchoring versus accelerated surface fibril formation J. Mol. Biol. 335 2004 1039 1049
47. C. Cecchi, S. Baglioni, C. Fiorillo, A. Pensalfini, G. Liguri, and D. Nosi Insights into the molecular basis of the differing susceptibility of varying cell types to the toxicity of amyloid aggregates J. Cell Sci. 118 2005 3459 3470
48. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489
49. M. Stefani, and C.M. Dobson Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81 2003 678 699
50. J. Bieschke, M. Herbst, T. Wiglenda, R.P. Friedrich, A. Boeddrich, and F. Schiele Small-molecule conversion of toxic oligomers to nontoxic beta-sheet-rich amyloid fibrils Nat. Chem. Biol. 8 2011 93 101
51. J. Shorter, and S. Lindquist Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers Science 304 2004 1793 1797
52. X. Wang, Y. Zhou, J.J. Ren, N.D. Hammer, and M.R. Chapman Gatekeeper residues in the major curlin subunit modulate bacterial amyloid fiber biogenesis Proc. Natl Acad. Sci. USA 107 2009 163 168
53. A.A. Nenninger, L.S. Robinson, and S.J. Hultgren Localized and efficient curli nucleation requires the chaperone-like amyloid assembly protein CsgF Proc. Natl Acad. Sci. USA 106 2009 900 905
54. C.B. Ramsook, C. Tan, M.C. Garcia, R. Fung, G. Soybelman, and R. Henry Yeast cell adhesion molecules have functional amyloid-forming sequences Eukaryot. Cell 9 2010 393 404
55. H.N. Otoo, K.G. Lee, W. Qiu, and P.N. Lipke Candida albicans Als adhesins have conserved amyloid-forming sequences Eukaryot. Cell 7 2008 776 782
56. D. Romero, H. Vlamakis, R. Losick, and R. Kolter An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms Mol. Microbiol. 80 2011 1155 1168
57. D. Romero, C. Aguilar, R. Losick, and R. Kolter Amyloid fibers provide structural integrity to Bacillus subtilis biofilms Proc. Natl Acad. Sci. USA 107 2010 2230 2234
58. R. Kayed, Y. Sokolov, B. Edmonds, T.M. McIntire, S.C. Milton, J.E. Hall, and C.G. Glabe Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 279 2004 46363 46366
59. W. de Jong, H.A. Wosten, L. Dijkhuizen, and D. Claessen Attachment of Streptomyces coelicolor is mediated by amyloidal fimbriae that are anchored to the cell surface via cellulose Mol. Microbiol. 73 2009 1128 1140
60. M.J. Casadaban Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu J. Mol. Biol. 104 1976 541 555
61. T. Baba, T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, and M. Baba Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection Mol. Syst. Biol. 2 2006 2006 0008
62. R.B. Goldberg, R.A. Bender, and S.L. Streicher Direct selection for P1-sensitive mutants of enteric bacteria J. Bacteriol. 118 1974 810 814