Curli biogenesis: Order out of disorder

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 8, 2014, Pages 1551-1558

  Evans, Margery L ^a   Chapman, Matthew R ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Aggregate; Biofilm; Curli; Functional amyloid; Nucleation precipitation; Type VIII secretion

Indexed keywords

AMYLOID PROTEIN; CURLI PROTEIN; LIPOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL SURFACE; GENE EXPRESSION; GENE EXPRESSION REGULATION; IN VIVO STUDY; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; SECRETION (PROCESS);

BACTERIA (MICROORGANISMS);

AGGREGATE; BIOFILM; CURLI; FUNCTIONAL AMYLOID; NUCLEATION-PRECIPITATION; TYPE VIII SECRETION;

AMYLOID; AMYLOIDOGENIC PROTEINS; BACTERIAL PROTEINS; BIOFILMS; ESCHERICHIA COLI; HUMANS; PROTEIN FOLDING; PROTEIN TRANSPORT;

EID: 84902317524     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.09.010     Document Type: Article

References (108)

1. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
2. Breydo L., Wu J.W., Uversky V.N. Alpha-synuclein misfolding and Parkinson's disease. Biochim. Biophys. Acta 2012, 1822:261-285.
3. Zuccato C., Valenza M., Cattaneo E. Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 2010, 90:905-981.
4. Chapman M.R., Robinson L.S., Pinkner J.S., Roth R., Heuser J., Hammar M., Normark S., Hultgren S.J. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 2002, 295:851-855.
5. Romero D., Aguilar C., Losick R., Kolter R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2230-2234.
6. Scheibel T., Kowal A.S., Bloom J.D., Lindquist S.L. Bidirectional amyloid fiber growth for a yeast prion determinant. Curr. Biol. 2001, 11:366-369.
7. Fowler D.M., Koulov A.V., Alory-Jost C., Marks M.S., Balch W.E., Kelly J.W. Functional amyloid formation within mammalian tissue. PLoS Biol. 2006, 4:e6.
8. Larsen P., Nielsen J.L., Dueholm M.S., Wetzel R., Otzen D., Nielsen P.H. Amyloid adhesins are abundant in natural biofilms. Environ. Microbiol. 2007, 9:3077-3090.
9. Blanco L.P., Evans M.L., Smith D.R., Badtke M.P., Chapman M.R. Diversity, biogenesis and function of microbial amyloids. Trends Microbiol. 2012, 20:66-73.
10. Olsen A., Jonsson A., Normark S. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 1989, 338:652-655.
11. Zogaj X., Bokranz W., Nimtz M., Romling U. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 2003, 71:4151-4158.
12. Zogaj X., Nimtz M., Rohde M., Bokranz W., Romling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 2001, 39:1452-1463.
13. Dueholm M.S., Albertsen M., Otzen D., Nielsen P.H. Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS One 2012, 7:e51274.
14. McCrate O.A., Zhou X., Reichhardt C., Cegelski L. Sum of the Parts: Composition and Architecture of the Bacterial Extracellular Matrix. J. Mol. Biol. 2013, (in press, PubMed ID: 23827139).
15. Pawar D.M., Rossman M.L., Chen J. Role of curli fimbriae in mediating the cells of enterohaemorrhagic Escherichia coli to attach to abiotic surfaces. J. Appl. Microbiol. 2005, 99:418-425.
16. Boyer R.R., Sumner S.S., Williams R.C., Pierson M.D., Popham D.L., Kniel K.E. Influence of curli expression by Escherichia coli 0157:H7 on the cell's overall hydrophobicity, charge, and ability to attach to lettuce. J. Food Prot. 2007, 70:1339-1345.
17. Hammar M., Arnqvist A., Bian Z., Olsen A., Normark S. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol. Microbiol. 1995, 18:661-670.
18. Collinson S.K., Doig P.C., Doran J.L., Clouthier S., Trust T.J., Kay W.W. Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J. Bacteriol. 1993, 175:12-18.
19. Olsen A., Wick M.J., Morgelin M., Bjorck L. Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect. Immun. 1998, 66:944-949.
20. Kai-Larsen Y., Luthje P., Chromek M., Peters V., Wang X., Holm A., Kadas L., Hedlund K.O., Johansson J., Chapman M.R., Jacobson S.H., Romling U., Agerberth B., Brauner A. Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog. 2010, 6:e1001010.
21. Bian Z., Brauner A., Li Y., Normark S. Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J. Infect. Dis. 2000, 181:602-612.
22. Nilsson M.R. Techniques to study amyloid fibril formation in vitro. Methods 2004, 34:151-160.
23. Wang X., Smith D.R., Jones J.W., Chapman M.R. In vitro polymerization of a functional Escherichia coli amyloid protein. J. Biol. Chem. 2007, 282:3713-3719.
24. Dueholm M.S., Nielsen S.B., Hein K.L., Nissen P., Chapman M., Christiansen G., Nielsen P.H., Otzen D.E. Fibrillation of the major curli subunit CsgA under a wide range of conditions implies a robust design of aggregation. Biochemistry 2011, 50:8281-8290.
25. Collinson S.K., Parker J.M., Hodges R.S., Kay W.W. Structural predictions of AgfA, the insoluble fimbrial subunit of Salmonella thin aggregative fimbriae. J. Mol. Biol. 1999, 290:741-756.
26. Shewmaker F., McGlinchey R.P., Thurber K.R., McPhie P., Dyda F., Tycko R., Wickner R.B. The functional curli amyloid is not based on in-register parallel beta-sheet structure. J. Biol. Chem. 2009, 284:25065-25076.
27. Nelson R., Sawaya M.R., Balbirnie M., Madsen A.O., Riekel C., Grothe R., Eisenberg D. Structure of the cross-beta spine of amyloid-like fibrils. Nature 2005, 435:773-778.
28. Cegelski L., Pinkner J.S., Hammer N.D., Cusumano C.K., Hung C.S., Chorell E., Aberg V., Walker J.N., Seed P.C., Almqvist F., Chapman M.R., Hultgren S.J. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat. Chem. Biol. 2009, 5:913-919.
29. Sivanathan V., Hochschild A. Generating extracellular amyloid aggregates using E. coli cells. Genes Dev. 2012, 26:2659-2667.
30. DePas W.H., Hufnagel D.A., Lee J.S., Blanco L.P., Bernstein H.C., Fisher S.T., James G.A., Stewart P.S., Chapman M.R. Iron induces bimodal population development by Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:2629-2634.
31. Epstein E.A., Reizian M.A., Chapman M.R. Spatial clustering of the curlin secretion lipoprotein requires curli fiber assembly. J. Bacteriol. 2009, 191:608-615.
32. Grantcharova N., Peters V., Monteiro C., Zakikhany K., Romling U. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar typhimurium. J. Bacteriol. 2010, 192:456-466.
33. Serra D.O., Richter A.M., Klauck G., Mika F., Hengge R. Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. MBio 2013, 4:e00103-e00113.
34. Gerstel U., Romling U. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ. Microbiol. 2001, 3:638-648.
35. Olsen A., Arnqvist A., Hammar M., Normark S. Environmental regulation of curli production in Escherichia coli. Infect. Agents Dis. 1993, 2:272-274.
36. Prigent-Combaret C., Vidal O., Dorel C., Lejeune P. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 1999, 181:5993-6002.
37. White A.P., Gibson D.L., Kim W., Kay W.W., Surette M.G. Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J. Bacteriol. 2006, 188:3219-3227.
38. Collinson S.K., Clouthier S.C., Doran J.L., Banser P.A., Kay W.W. Characterization of the agfBA fimbrial operon encoding thin aggregative fimbriae of Salmonella enteritidis. Adv. Exp. Med. Biol. 1997, 412:247-248.
39. Rudd K.E. EcoGene: a genome sequence database for Escherichia coli K-12. Nucleic Acids Res. 2000, 28:60-64.
40. Ishihama A. Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol. Rev. 2010, 34:628-645.
41. Arnqvist A., Olsen A., Pfeifer J., Russell D.G., Normark S. The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101. Mol. Microbiol. 1992, 6:2443-2452.
42. Bougdour A., Lelong C., Geiselmann J. Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J. Biol. Chem. 2004, 279:19540-19550.
43. Brown P.K., Dozois C.M., Nickerson C.A., Zuppardo A., Terlonge J., Curtiss R.r. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol. Microbiol. 2001, 41:349-363.
44. Ogasawara H., Yamamoto K., Ishihama A. Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli. FEMS Microbiol. Lett. 2010, 312:160-168.
45. Romling U., Rohde M., Olsen A., Normark S., Reinkoster J. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 2000, 36:10-23.
46. Brombacher E., Dorel C., Zehnder A.J., Landini P. The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli. Microbiology 2003, 149:2847-2857.
47. Ogasawara H., Yamamoto K., Ishihama A. Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J. Bacteriol. 2011, 193:2587-2597.
48. Zakikhany K., Harrington C.R., Nimtz M., Hinton J.C., Romling U. Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 2010, 77:771-786.
49. Reshamwala S.M., Noronha S.B. Biofilm formation in Escherichia coli cra mutants is impaired due to down-regulation of curli biosynthesis. Arch. Microbiol. 2011, 193:711-722.
50. Shimada T., Katayama Y., Kawakita S., Ogasawara H., Nakano M., Yamamoto K., Ishihama A. A novel regulator RcdA of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli. Microbiologyopen 2012, 1:381-394.
51. Zheng D., Constantinidou C., Hobman J.L., Minchin S.D. Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res. 2004, 32:5874-5893.
52. Dorel C., Vidal O., Prigent-Combaret C., Vallet I., Lejeune P. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 1999, 178:169-175.
53. Jubelin G., Vianney A., Beloin C., Ghigo J.M., Lazzaroni J.C., Lejeune P., Dorel C. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 2005, 187:2038-2049.
54. Ferrieres L., Clarke D.J. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol. Microbiol. 2003, 50:1665-1682.
55. Romling U., Bian Z., Hammar M., Sierralta W.D., Normark S. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 1998, 180:722-731.
56. Prigent-Combaret C., Brombacher E., Vidal O., Ambert A., Lejeune P., Landini P., Dorel C. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 2001, 183:7213-7223.
57. Gerstel U., Kolb A., Romling U. Regulatory components at the csgD promoter-additional roles for OmpR and integration host factor and role of the 5' untranslated region. FEMS Microbiol. Lett. 2006, 261:109-117.
58. Gerstel U., Park C., Romling U. Complex regulation of csgD promoter activity by global regulatory proteins. Mol. Microbiol. 2003, 49:639-654.
59. Ogasawara H., Yamada K., Kori A., Yamamoto K., Ishihama A. Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 2010, 156:2470-2483.
60. Olsen A., Arnqvist A., Hammar M., Sukupolvi S., Normark S. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol. Microbiol. 1993, 7:523-536.
61. Holmqvist E., Reimegard J., Sterk M., Grantcharova N., Romling U., Wagner E.G. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J. 2010, 29:1840-1850.
62. Jorgensen M.G., Thomason M.K., Havelund J., Valentin-Hansen P., Storz G. Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev. 2012, 27:1132-1145.
63. Mika F., Busse S., Possling A., Berkholz J., Tschowri N., Sommerfeldt N., Pruteanu M., Hengge R. Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol. Microbiol. 2012, 84:51-65.
64. Thomason M.K., Fontaine F., De Lay N., Storz G. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol. Microbiol. 2012, 84:17-35.
65. Monteiro C., Papenfort K., Hentrich K., Ahmad I., Le Guyon S., Reimann R., Grantcharova N., Romling U. Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar Typhimurium. RNA Biol. 2012, 9:489-502.
66. Mika F., Hengge R. Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella. Int. J. Mol. Sci. 2013, 14:4560-4579.
67. Collinson S.K., Clouthier S.C., Doran J.L., Banser P.A., Kay W.W. Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J. Bacteriol. 1996, 178:662-667.
68. Gibson D.L., White A.P., Rajotte C.M., Kay W.W. AgfC and AgfE facilitate extracellular thin aggregative fimbriae synthesis in Salmonella enteritidis. Microbiology 2007, 153:1131-1140.
69. Hammar M., Bian Z., Normark S. Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:6562-6566.
70. Hammer N.D., Schmidt J.C., Chapman M.R. The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12494-12499.
71. Desvaux M., Hebraud M., Talon R., Henderson I.R. Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol. 2009, 17:139-145.
72. Taylor J.D., Zhou Y., Salgado P.S., Patwardhan A., McGuffie M., Pape T., Grabe G., Ashman E., Constable S.C., Simpson P.J., Lee W.C., Cota E., Chapman M.R., Matthews S.J. Atomic resolution insights into curli fiber biogenesis. Structure 2011, 19:1307-1316.
73. Nenninger A.A., Robinson L.S., Hammer N.D., Epstein E.A., Badtke M.P., Hultgren S.J., Chapman M.R. CsgE is a curli secretion specificity factor that prevents amyloid fibre aggregation. Mol. Microbiol. 2011, 81:486-499.
74. Nenninger A.A., Robinson L.S., Hultgren S.J. Localized and efficient curli nucleation requires the chaperone-like amyloid assembly protein CsgF. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:900-905.
75. Robinson L.S., Ashman E.M., Hultgren S.J., Chapman M.R. Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol. Microbiol. 2006, 59:870-881.
76. Collinson S.K., Emody L., Muller K.H., Trust T.J., Kay W.W. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J. Bacteriol. 1991, 173:4773-4781.
77. Cherny I., Rockah L., Levy-Nissenbaum O., Gophna U., Ron E.Z., Gazit E. The formation of Escherichia coli curli amyloid fibrils is mediated by prion-like peptide repeats. J. Mol. Biol. 2005, 352:245-252.
78. Wang X., Chapman M.R. Sequence determinants of bacterial amyloid formation. J. Mol. Biol. 2008, 380:570-580.
79. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003, 300:486-489.
80. Zhou Y., Smith D., Leong B.J., Brannstrom K., Almqvist F., Chapman M.R. Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms. J. Biol. Chem. 2012, 287:35092-35103.
81. Wang X., Zhou Y., Ren J.J., Hammer N.D., Chapman M.R. Gatekeeper residues in the major curlin subunit modulate bacterial amyloid fiber biogenesis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:163-168.
82. Wang X., Hammer N.D., Chapman M.R. The molecular basis of functional bacterial amyloid polymerization and nucleation. J. Biol. Chem. 2008, 283:21530-21539.
83. Bian Z., Normark S. Nucleator function of CsgB for the assembly of adhesive surface organelles in Escherichia coli. EMBO J. 1997, 16:5827-5836.
84. Loferer H., Hammar M., Normark S. 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. 1997, 26:11-23.
85. White A.P., Collinson S.K., Banser P.A., Gibson D.L., Paetzel M., Strynadka N.C., Kay W.W. Structure and characterization of AgfB from Salmonella enteritidis thin aggregative fimbriae. J. Mol. Biol. 2001, 311:735-749.
86. Hammer N.D., McGuffie B.A., Zhou Y., Badtke M.P., Reinke A.A., Brannstrom K., Gestwicki J.E., Olofsson A., Almqvist F., Chapman M.R. The C-terminal repeating units of CsgB direct bacterial functional amyloid nucleation. J. Mol. Biol. 2012, 422:376-389.
87. Bardy S.L., Maddock J.R. Polar explorations. Recent insights into the polarity of bacterial proteins. Curr. Opin. Microbiol. 2007, 10:617-623.
88. Ebersbach G., Jacobs-Wagner C. Exploration into the spatial and temporal mechanisms of bacterial polarity. Trends Microbiol. 2007, 15:101-108.
89. Soto G.E., Hultgren S.J. Bacterial adhesins: common themes and variations in architecture and assembly. J. Bacteriol. 1999, 181:1059-1071.
90. Evans M.L., Schmidt J.C., Ilbert M., Doyle S.M., Quan S., Bardwell J.C., Jakob U., Wickner S., Chapman M.R. E. coli chaperones DnaK, Hsp33 and Spy inhibit bacterial functional amyloid assembly. Prion 2011, 5:323-334.
91. Andersson E.K., Bengtsson C., Evans M.L., Chorell E., Sellstedt M., Lindgren A.E.G., Hufnagel D.A., Bhattacharya M., Tessier P.M., Wittung-Stafshede P., Almqvist F., Chapman M.R. Modulation of curli assembly and pellicle biofilm formation by chemical and protein chaperones. Chem. Biol. 2013, (in press, PubMed ID: 24035282).
92. Hardy G.G., Allen R.C., Toh E., Long M., Brown P.J., Cole-Tobian J.L., Brun Y.V. A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol. Microbiol. 2010, 76:409-427.
93. Cole J.L., Hardy G.G., Bodenmiller D., Toh E., Hinz A., Brun Y.V. The HfaB and HfaD adhesion proteins of Caulobacter crescentus are localized in the stalk. Mol. Microbiol. 2003, 49:1671-1683.
94. Sivanathan V., Hochschild A. A bacterial export system for generating extracellular amyloid aggregates. Nat. Protoc. 2013, 8:1381-1390.
95. O'Nuallain B., Wetzel R. Conformational Abs recognizing a generic amyloid fibril epitope. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1485-1490.
96. Kayed R., Head E., Sarsoza F., Saing T., Cotman C.W., Necula M., Margol L., Wu J., Breydo L., Thompson J.L., Rasool S., Gurlo T., Butler P., Glabe C.G. Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol. Neurodegener. 2007, 2:18.
97. Ladiwala A.R., Bhattacharya M., Perchiacca J.M., Cao P., Raleigh D.P., Abedini A., Schmidt A.M., Varkey J., Langen R., Tessier P.M. Rational design of potent domain antibody inhibitors of amyloid fibril assembly. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:19965-19970.
98. Perchiacca J.M., Ladiwala A.R., Bhattacharya M., Tessier P.M. Structure-based design of conformation- and sequence-specific antibodies against amyloid beta. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:84-89.
99. Svensson A., Larsson A., Emtenas H., Hedenstrom M., Fex T., Hultgren S.J., Pinkner J.S., Almqvist F., Kihlberg J. Design and evaluation of pilicides: potential novel antibacterial agents directed against uropathogenic Escherichia coli. Chembiochem 2001, 2:915-918.
100. Aberg V., Norman F., Chorell E., Westermark A., Olofsson A., Sauer-Eriksson A.E., Almqvist F. Microwave-assisted decarboxylation of bicyclic 2-pyridone scaffolds and identification of Abeta-peptide aggregation inhibitors. Org. Biomol. Chem. 2005, 3:2817-2823.
101. Horvath I., Weise C.F., Andersson E.K., Chorell E., Sellstedt M., Bengtsson C., Olofsson A., Hultgren S.J., Chapman M., Wolf-Watz M., Almqvist F., Wittung-Stafshede P. Mechanisms of protein oligomerization: inhibitor of functional amyloids templates alpha-synuclein fibrillation. J. Am. Chem. Soc. 2012, 134:3439-3444.
102. Arnqvist A., Olsen A., Normark S. 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. 1994, 13:1021-1032.
103. Pratt L.A., Silhavy T.J. Crl stimulates RpoS activity during stationary phase. Mol. Microbiol. 1998, 29:1225-1236.
104. Vidal O., Longin R., Prigent-Combaret C., Dorel C., Hooreman M., Lejeune P. 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. 1998, 180:2442-2449.
105. Vianney A., Jubelin G., Renault S., Dorel C., Lejeune P., Lazzaroni J.C. Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 2005, 151:2487-2497.
106. Ogasawara H., Hasegawa A., Kanda E., Miki T., Yamamoto K., Ishihama A. Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. J. Bacteriol. 2007, 189:4791-4799.
107. Liu X., De Wulf P. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 2004, 279:12588-12597.
108. Ogasawara H., Shinohara S., Yamamoto K., Ishihama A. Novel regulation targets of the metal-response BasS-BasR two-component system of Escherichia coli. Microbiology 2012, 158:1482-1492.