New insight into the molecular control of bacterial functional amyloids

Frontiers in Cellular and Infection Microbiology

Volumn 5, Issue APR, 2015, Pages

  Taylor, Jonathan D ^a   Matthews, Steve J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Alzheimer's; Amyloid; Biofilm; Chaperone; Curli; Parkinson's; Secretion

Indexed keywords

AMYLOID; BACTERIAL PROTEIN;

BACTERIAL OUTER MEMBRANE; BACTERIUM; CRYSTAL STRUCTURE; CRYSTALLIZATION; ELECTRON MICROSCOPY; NONHUMAN; PROTEIN STRUCTURE; SHORT SURVEY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN TRANSPORT;

AMYLOID; BACTERIA; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; PROTEIN TRANSPORT;

EID: 84989778442     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2015.00033     Document Type: Short Survey

References (46)

1. 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. doi: 10.1016/j.tim.2011.11.005
2. Cao, B., Zhao, Y., Kou, Y., Ni, D., Zhang, X. C., and Huang, Y. (2014). Structure of the nonameric bacterial amyloid secretion channel. Proc. Natl. Acad. Sci. U.S.A. 111, E5439-E5444. doi: 10.1073/pnas.1411942111
3. Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., et al. (2002). Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295, 851-855. doi: 10.1126/science.1067484
4. Chen, A. Y., Deng, Z., Billings, A. N., Seker, U. O., Lu, M. Y., Citorik, R. J., et al. (2014). Synthesis and patterning of tunable multiscale materials with engineered cells. Nat. Mater. 13, 515-523. doi: 10.1038/nmat3912
5. Cheng, B., Gong, H., Xiao, H., Petersen, R. B., Zheng, L., and Huang, K. (2013). Inhibiting toxic aggregation of amyloidogenic proteins: a therapeutic strategy for protein misfolding diseases. Biochim. Biophys. Acta 1830, 4860-4871. doi: 10.1016/j.bbagen.2013.06.029
6. Cohen, S. I., Arosio, P., Presto, J., Kurudenkandy, F. R., Biverstal, H., Dolfe, L., et al. (2015). A molecular chaperone breaks the catalytic cycle that generates toxic Abeta oligomers. Nat. Struct. Mol. Biol. 22, 207-213. doi: 10.1038/nsmb.2971
7. Dueholm, M. S., Albertsen, M., Otzen, D., and Nielsen, P. H. (2012). Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS ONE 7:e51274. doi: 10.1371/journal.pone.0051274
8. Dueholm, M. S., Petersen, S. V., Sonderkaer, M., Larsen, P., Christiansen, G., Hein, K. L., et al. (2010). Functional amyloid in Pseudomonas. Mol. Microbiol. 77, 1009-1020. doi: 10.1111/j.1365-2958.2010.07269.x
9. Epstein, E. A., Reizian, M. A., and Chapman, M. R. (2009). Spatial clustering of the curlin secretion lipoprotein requires curli fiber assembly. J. Bacteriol. 191, 608-615. doi: 10.1128/JB.01244-08
10. Evans, M. L., Chorell, E., Taylor, J. D., Aden, J., Gotheson, A., Li, F., et al. (2015). The Bacterial Curli system possesses a potent and selective inhibitor of amyloid formation. Mol. Cell 57, 445-455. doi: 10.1016/j.molcel.2014.12.025
11. Evans, M. L., Schmidt, J. C., Ilbert, M., Doyle, S. M., Quan, S., Bardwell, J. C., et al. (2011). E. coli chaperones DnaK, Hsp33 and Spy inhibit bacterial functional amyloid assembly. Prion 5, 323-334. doi: 10.4161/pri.18555
12. Ferguson, A. D., Hofmann, E., Coulton, J. W., Diederichs, K., and Welte, W. (1998). Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282, 2215-2220.
13. Galvagnion, C., Buell, A. K., Meisl, G., Michaels, T. C., Vendruscolo, M., Knowles, T. P., et al. (2015). Lipid vesicles trigger alpha-synuclein aggregation by stimulating primary nucleation. Nat. Chem. Biol. 11, 229-234. doi: 10.1038/nchembio.1750
14. Gandhi, C. S., Walton, T. A., and Rees, D. C. (2011). OCAM: a new tool for studying the oligomeric diversity of MscL channels. Protein Sci. 20, 313-326. doi: 10.1002/pro.562
15. Garcia, M., Lipke, P., and Klotz, S. (2013). Pathogenic microbial amyloids: their function and the host response. OA Microbiol. 1:2.
16. Gibson, D. L., White, A. P., Rajotte, C. M., and Kay, W. W. (2007). AgfC and AgfE facilitate extracellular thin aggregative fimbriae synthesis in Salmonella enteritidis. Microbiology 153, 1131-1140. doi: 10.1099/mic.0.2006/000935-0
17. Goyal, P., Krasteva, P. V., Van Gerven, N., Gubellini, F., Van Den Broeck, I., Troupiotis-Tsailaki, A., et al. (2014). Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature 516, 250-253. doi: 10.1038/nature13768
18. Goyal, P., Van Gerven, N., Jonckheere, W., and Remaut, H. (2013). Crystallization and preliminary X-ray crystallographic analysis of the curli transporter CsgG. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 69, 1349-1353. doi: 10.1107/S1744309113028054
19. Iacovache, I., Bischofberger, M., and Van Der Goot, F. G. (2010). Structure and assembly of pore-forming proteins. Curr. Opin. Struct. Biol. 20, 241-246. doi: 10.1016/j.sbi.2010.01.013
20. Jordal, P. B., Dueholm, M. S., Larsen, P., Petersen, S. V., Enghild, J. J., Christiansen, G., et al. (2009). Widespread abundance of functional bacterial amyloid in mycolata and other gram-positive bacteria. Appl. Environ. Microbiol. 75, 4101-4110. doi: 10.1128/AEM.02107-08
21. Krantz, B. A., Melnyk, R. A., Zhang, S., Juris, S. J., Lacy, D. B., Wu, Z., et al. (2005). A phenylalanine clamp catalyzes protein translocation through the anthrax toxin pore. Science 309, 777-781. doi: 10.1126/science.1113380
22. Larsen, P., Nielsen, J. L., Dueholm, M. S., Wetzel, R., Otzen, D., and Nielsen, P. H. (2007). Amyloid adhesins are abundant in natural biofilms. Environ. Microbiol. 9, 3077-3090. doi: 10.1111/j.1462-2920.2007.01418.x
23. Loferer, H., Hammar, M., and Normark, S. (1997). 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, 11-23.
24. Mika, F., and Hengge, R. (2013). Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella. Int. J. Mol. Sci. 14, 4560-4579. doi: 10.3390/ijms14034560
25. Nenninger, A. A., Robinson, L. S., Hammer, N. D., Epstein, E. A., Badtke, M. P., Hultgren, S. J., et al. (2011). CsgE is a curli secretion specificity factor that prevents amyloid fibre aggregation. Mol. Microbiol. 81, 486-499. doi: 10.1111/j.1365-2958.2011.07706.x
26. Nenninger, A. A., Robinson, L. S., and Hultgren, S. J. (2009). Localized and efficient curli nucleation requires the chaperone-like amyloid assembly protein CsgF. Proc. Natl. Acad. Sci. U.S.A. 106, 900-905. doi: 10.1073/pnas.0812143106
27. Nguyen, P. Q., Botyanszki, Z., Tay, P. K., and Joshi, N. S. (2014). Programmable biofilm-based materials from engineered curli nanofibres. Nat. Commun. 5, 4945. doi: 10.1038/ncomms5945
28. Nivala, J., Marks, D. B., and Akeson, M. (2013). Unfoldase-mediated protein translocation through an alpha-hemolysin nanopore. Nat. Biotechnol. 31, 247-250. doi: 10.1038/nbt.2503
29. Olsen, A., Jonsson, A., and Normark, S. (1989). Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338, 652-655. doi: 10.1038/338652a0
30. Otzen, D., and Nielsen, P. H. (2008). We find them here, we find them there: functional bacterial amyloid. Cell. Mol. Life Sci. 65, 910-927. doi: 10.1007/s00018-007-7404-4
31. Rapsinski, G. J., Wynosky-Dolfi, M. A., Oppong, G. O., Tursi, S. A., Wilson, R. P., Brodsky, I. E., et al. (2015). Toll-Like receptor 2 and NLRP3 cooperate to recognize a Functional Bacterial Amyloid, Curli. Infect. Immun. 83, 693-701. doi: 10.1128/IAI.02370-14
32. Remaut, H., Tang, C., Henderson, N. S., Pinkner, J. S., Wang, T., Hultgren, S. J., et al. (2008). Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133, 640-652. doi: 10.1016/j.cell.2008.03.033
33. Robinson, L. S., Ashman, E. M., Hultgren, S. J., and Chapman, M. R. (2006). Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol. Microbiol. 59, 870-881. doi: 10.1111/j.1365-2958.2005.04997.x
34. 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. doi: 10.1073/pnas.0910560107
35. Shewmaker, F., Mcglinchey, R. P., Thurber, K. R., Mcphie, P., Dyda, F., Tycko, R., et al. (2009). The functional curli amyloid is not based on in-register parallel beta-sheet structure. J. Biol. Chem. 284, 25065-25076. doi: 10.1074/jbc.M109.007054
36. Sivanathan, V., and Hochschild, A. (2013). A bacterial export system for generating extracellular amyloid aggregates. Nat. Protoc. 8, 1381-1390. doi: 10.1038/nprot.2013.081
37. Soo, V. W., and Wood, T. K. (2013). Antitoxin MqsA represses curli formation through the master biofilm regulator CsgD. Sci. Rep. 3:3186. doi: 10.1038/srep03186
38. Taylor, J. D., Zhou, Y., Salgado, P. S., Patwardhan, A., Mcguffie, M., Pape, T., et al. (2011). Atomic resolution insights into curli fiber biogenesis. Structure 19, 1307-1316. doi: 10.1016/j.str.2011.05.015
39. Tukel, C., Wilson, R. P., Nishimori, J. H., Pezeshki, M., Chromy, B. A., and Baumler, A. J. (2009). Responses to amyloids of microbial and host origin are mediated through toll-like receptor 2. Cell Host Microbe. 6, 45-53. doi: 10.1016/j.chom.2009.05.020
40. Van Den Berg, B., Clemons, W. M. Jr., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., et al. (2004). X-ray structure of a protein-conducting channel. Nature 427, 36-44. doi: 10.1038/nature02218
41. Van Gerven, N., Goyal, P., Vandenbussche, G., De Kerpel, M., Jonckheere, W., De Greve, H., et al. (2014). Secretion and functional display of fusion proteins through the curli biogenesis pathway. Mol. Microbiol. 91, 1022-1035. doi: 10.1111/mmi.12515
42. White, A. P., Collinson, S. K., Burian, J., Clouthier, S. C., Banser, P. A., and Kay, W. W. (1999). High efficiency gene replacement in Salmonella enteritidis: chimeric fimbrins containing a T-cell epitope from Leishmania major. Vaccine 17, 2150-2161. doi: 10.1016/S0264-410X(98)00491-5
43. Yamashita, K., Kawai, Y., Tanaka, Y., Hirano, N., Kaneko, J., Tomita, N., et al. (2011). Crystal structure of the octameric pore of staphylococcal gamma-hemolysin reveals the beta-barrel pore formation mechanism by two components. Proc. Natl. Acad. Sci. U.S.A. 108, 17314-17319. doi: 10.1073/pnas.1110402108
44. Zakikhany, K., Harrington, C. R., Nimtz, M., Hinton, J. C., and Romling, U. (2010). Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 77, 771-786. doi: 10.1111/j.1365-2958.2010.07247.x
45. Zhong, C., Gurry, T., Cheng, A. A., Downey, J., Deng, Z., Stultz, C. M., et al. (2014). Strong underwater adhesives made by self-assembling multi-protein nanofibres. Nat. Nanotechnol. 9, 858-866. doi: 10.1038/nnano.2014.199
46. Zhou, Y., Smith, D. R., Hufnagel, D. A., and Chapman, M. R. (2013). Experimental manipulation of the microbial functional amyloid called curli. Methods Mol. Biol. 966, 53-75. doi: 10.1007/978-1-62703-245-2_4