Isolation, characterization, and aggregation of a structured bacterial matrix precursor

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17559-17568

  Chai, Liraz ^a   Romero, Diego ^a,d   Kayatekin, Can ^b   Akabayov, Barak ^a   Vlamakis, Hera ^a   Losick, Richard ^c   Kolter, Roberto ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c HARVARD UNIVERSITY   (United States)

^d UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS SUBTILIS; BACTERIAL BIOFILM; EXTERNAL CONDITIONS; EXTRACELLULAR MATRICES; HELICAL STRUCTURES; HYDROPHOBIC SURFACES; MATRIX PRECURSORS; PURIFICATION METHOD;

ATOMIC FORCE MICROSCOPY; BIOFILMS; FIBERS; GLYCOPROTEINS; INFRARED SPECTROSCOPY; NUCLEIC ACIDS; OLIGOMERS; SURFACE CHEMISTRY;

PROTEINS;

BACTERIAL PROTEIN; OLIGOMER; TASA PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; ATOMIC FORCE MICROSCOPY; BACILLUS SUBTILIS; BETA SHEET; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HYDROPHOBICITY; IN VITRO STUDY; INFRARED SPECTROSCOPY; LIGHT SCATTERING; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN STABILITY; STRUCTURE ANALYSIS; SURFACE PROPERTY;

AMYLOID PRECURSOR PROTEIN; BACILLUS; BIOFILM; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; MICROBIOLOGY; PROTEIN AGGREGATION;

ADSORPTION; ALUMINUM SILICATES; AMYLOID; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOFILMS; EXTRACELLULAR MATRIX PROTEINS; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIGHT; MICROSCOPY, ATOMIC FORCE; PARTICLE SIZE; PROTEIN MULTIMERIZATION; SCATTERING, RADIATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SURFACE PROPERTIES;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 84879043414     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.453605     Document Type: Article

References (47)

1. Flemming, H. C., and Wingender, J. (2010) The biofilm matrix. Nat. Rev. Microbiol. 8, 623-633
2. Mulcahy, H., Charron-Mazenod, L., and Lewenza, S. (2008) Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4, e1000213
3. Wilking, J. N., Angelini, T. E., Seminara, A., Brenner, M. P., and Weitz, D. A. (2011) Biofilms as complex fluids. MRS Bull. 36, 385-391
4. Rubinstein, S. M., Kolodkin-Gal, I., McLoon, A., Chai, L., Kolter, R., Losick, R., and Weitz, D. A. (2012) Osmotic pressure can regulate matrix gene expression in Bacillus subtilis. Mol. Microbiol. 86, 426-436
5. Epstein, A. K., Pokroy, B., Seminara, A., and Aizenberg, J. (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc. Natl. Acad. Sci. U.S.A. 108, 995-1000
6. Kobayashi, K., and Iwano, M. (2012) BslA(YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol. Microbiol. 85, 51-66
7. Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., Normark, S., and Hultgren, S. J. (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295, 851-855 (Pubitemid 34118365)
8. Schwartz, K., Syed, A. K., Stephenson, R. E., Rickard, A. H., and Boles, B. R. (2012) Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms. PLoS Pathog. 8, e1002744
9. Dueholm, M. S., Petersen, S. V., Sønderkær, M., Larsen, P., Christiansen, G., Hein, K. L., Enghild, J. J., Nielsen, J. L., Nielsen, K. L., Nielsen, P. H., and Otzen, D. E. (2010) Functional amyloid in Pseudomonas. Mol. Microbiol. 77, 1009-1020
10. Stöver, A. G., and Driks, A. (1999) Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. J. Bacteriol. 181, 1664-1672 (Pubitemid 29110829)
11. Branda, S. S., Chu, F., Kearns, D. B., Losick, R., and Kolter, R. (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol. Microbiol. 59, 1229-1238
12. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U.S.A. 107, 2230-2234
13. Karatan, E., and Watnick, P. (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol. Mol. Biol. Rev. 73, 310-347
14. Epstein, E. A., and Chapman, M. R. (2008) Polymerizing the fibre between bacteria and host cells: the biogenesis of functional amyloid fibres. Cell. Microbiol. 10, 1413-1420 (Pubitemid 351837262)
15. Barnhart, M. M., and Chapman, M. R. (2006) Curli biogenesis and function. Annu. Rev. Microbiol. 60, 131-147 (Pubitemid 44627943)
16. Shu, Q., Crick, S. L., Pinkner, J. S., Ford, B., Hultgren, S. J., and Frieden, C. (2012) The E. coli CsgB nucleator of curli assembles to β-sheet oligomers that alter the CsgA fibrillization mechanism. Proc. Natl. Acad. Sci. U.S.A. 109, 6502-6507
17. Blanco, L. P., Evans, M. L., Smith, D. R., Badtke, M. P., and Chapman, M. R. (2012) Diversity, biogenesis and function of microbial amyloids. Trends Microbiol. 20, 66-73
18. Romero, D., Vlamakis, H., Losick, R., and Kolter, R. (2011) An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol. Microbiol. 80, 1155-1168
19. Kearns, D. B., Chu, F., Branda, S. S., Kolter, R., and Losick, R. (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol. Microbiol. 55, 739-749 (Pubitemid 40203690)
20. Berne, B. J., and Pecora, R. (1976) Dynamic Light Scattering: With Applications to Chemistry, Biology, and Physics, John Wiley & Sons, New York
21. Branda, S. S., Vik, S., Friedman, L., and Kolter, R. (2005) Biofilms: the matrix revisited. Trends Microbiol. 13, 20-26 (Pubitemid 40082393)
22. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry 38, 16424-16431
23. Flory, P. J. (1953) Principles of Polymer Chemistry, Cornell University Press, Ithaca, NY
24. Sutherland, I. (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147, 3-9
25. Maoz, R., Netzer, L., Gun, J., and Sagiv, J. (1988) Self-assembling monolayers in the construction of planned supramolecular structures and as modifiers of surface properties. J. Chim. Phys. Chim. Biol. 85, 1059-1065
26. Wasserman, S. R., Tao, Y. T., and Whitesides, G. M. (1989) Structure and reactivity of alkylsiloxane monolayers formed by reaction of alkyltrichlorosilanes on silicon substrates. Langmuir 5, 1074-1087
27. Serio, T. R., Cashikar, A. G., Kowal, A. S., Sawicki, G. J., Moslehi, J. J., Serpell, L., Arnsdorf, M. F., and Lindquist, S. L. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289, 1317-1321 (Pubitemid 30656041)
28. Magdassi, S. (1996) Surface Activities of Proteins: Chemical and Physical Modifications, Marcel Dekker, New York, NY
29. Zurdo, J., Guijarro, J. I., Jiménez, J. L., Saibil, H. R., and Dobson, C. M. (2001) Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain. J. Mol. Biol. 311, 325-340 (Pubitemid 32744545)
30. 2-microglobulin and amyloid formation in vitro. Biochemistry 39, 8735-8746
31. Pfefferkorn, C. M., McGlinchey, R. P., and Lee, J. C. (2010) Effects of pH on aggregation kinetics of the repeat domain of a functional amyloid, Pmel17. Proc. Natl. Acad. Sci. U.S.A. 107, 21447-21452
32. McGlinchey, R. P., Shewmaker, F., Hu, K. N., McPhie, P., Tycko, R., and Wickner, R. B. (2011) Repeat domains of melanosome matrix protein Pmel17 orthologs form amyloid fibrils at the acidic melanosomal pH. J. Biol. Chem. 286, 8385-8393
33. Orte, A., Birkett, N. R., Clarke, R. W., Devlin, G. L., Dobson, C. M., and Klenerman, D. (2008) Direct characterization of amyloidogenic oligomers by single-molecule fluorescence. Proc. Natl. Acad. Sci. U.S.A. 105, 14424-14429
34. Dueholm, M. S., Nielsen, S. B., Hein, K. L., Nissen, P., Chapman, M., Christiansen, G., Nielsen, P. H., and Otzen, D. E. (2011) Fibrillation of the major curli subunit CsgA under a wide range of conditions implies a robust design of aggregation. Biochemistry 50, 8281-8290
35. Shahnawaz, M., and Soto, C. (2012) Microcin amyloid fibrils A are reservoir of toxic oligomeric species. J. Biol. Chem. 287, 11665-11676
36. Eichner, T., and Radford, S. E. (2011) A diversity of assembly mechanisms of a generic amyloid fold. Mol. Cell 43, 8-18
37. Barth, A., and Zscherp, C. (2002) What vibrations tell us about proteins. Q. Rev. Biophys. 35, 369-430 (Pubitemid 36207229)
38. Barth, A. (2007) Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767, 1073-1101
39. Singh, B. R. (2000) Infrared Analysis of Peptides and Proteins: Principles and Applications, ACS Symposium Series, Vol. 750, American Chemical Society, Washington, D. C.
40. Fraser, P. E., Nguyen, J. T., Surewicz, W. K., and Kirschner, D. A. (1991) pH-dependent structural transitions of Alzheimer amyloid peptides. Biophys. J. 60, 1190-1201
41. Chang, W. S., van de Mortel, M., Nielsen, L., Nino de Guzman, G., Li, X., and Halverson, L. J. (2007) Alginate production by Pseudomonas putida creates a hydrated microenvironment and contributes to biofilm architecture and stress tolerance under water-limiting conditions. J. Bacteriol. 189, 8290-8299 (Pubitemid 350178941)
42. Sokolowski, F., Modler, A. J., Masuch, R., Zirwer, D., Baier, M., Lutsch, G., Moss, D. A., Gast, K., and Naumann, D. (2003) Formation of critical oligomers is a key event during conformational transition of recombinant Syrian hamster prion protein. J. Biol. Chem. 278, 40481-40492 (Pubitemid 37280858)
43. Parrish, J. R., Jr., and Blout, E. R. (1972) The conformation of poly-L-alanine in hexafluoroisopropanol. Biopolymers 11, 1001-1020
44. Bartels, T., Choi, J. G., and Selkoe, D. J. (2011) [agr]-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477, 107-110
45. Wang, X., Smith, D. R., Jones, J. W., and Chapman, M. R. (2007) In vitro polymerization of a functional Escherichia coli amyloid protein. J. Biol. Chem. 282, 3713-3719 (Pubitemid 47084435)
46. Keller, A., Fritzsche, M., Yu, Y. P., Liu, Q., Li, Y. M., Dong, M., and Besenbacher, F. (2011) Influence of hydrophobicity on the surface-catalyzed assembly of the islet amyloid polypeptide. ACS Nano 5, 2770-2778
47. Yamada, M., Tsukagoshi, H., Otomo, E., and Hayakawa, M. (1987) Cerebral amyloid angiopathy in the aged. J. Neurol. 234, 371-376