Analysis of the σE regulon in Crohn's disease-associated Escherichia coli revealed involvement of the waaWVL operon in biofilm formation

Journal of Bacteriology

Volumn 197, Issue 8, 2015, Pages 1451-1465

  Chassaing, Benoit ^a,b,f   Garénaux, Estelle ^a,b   Carriere, Jessica ^a,b   Rolhion, Nathalie ^a,b,g   Guérardel, Yann ^c,d   Barnich, Nicolas ^a,b   Bonnet, Richard ^a,b,e   Darfeuille Michaud, Arlette ^a,b,e  

^a UNIVERSITÉ CLERMONT AUVERGNE   (France)

^b CEMAGREF   (France)

^c UNIV LILLE   (France)

^d UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^e UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

^f GEORGIA STATE UNIVERSITY   (United States)

^g INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; OUTER MEMBRANE PROTEIN; PERIPLASMIC PROTEIN; TRANSPOSASE; VIRULENCE FACTOR; ESCHERICHIA COLI PROTEIN; SIGMA FACTOR; SPORULATION-SPECIFIC SIGMA FACTORS;

ARTICLE; BIOFILM; CELL ADHESION; COMPUTER MODEL; CROHN DISEASE; ESCHERICHIA COLI; GENOTYPE; HUMAN; HUMAN CELL; IMAGE PROCESSING; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; NONHUMAN; OPERON; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WAAWVL GENE; BACTERIUM ADHERENCE; GENETICS; METABOLISM; MICROBIOLOGY; MULTIGENE FAMILY; PHYSIOLOGY;

ESCHERICHIA COLI;

BACTERIAL ADHESION; BIOFILMS; CROHN DISEASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; MULTIGENE FAMILY; OPERON; REGULON; SIGMA FACTOR;

EID: 84926050756     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02499-14     Document Type: Article

References (68)

1. Kaser A, Zeissig S, Blumberg RS. 2010. Inflammatory bowel disease. Annu Rev Immunol 28:573-621. http://dx.doi.org/10.1146/annurev-immunol-030409-101225.
2. Stappenbeck TS, Rioux JD, Mizoguchi A, Saitoh T, Huett A, Darfeuille-Michaud A, Wileman T, Mizushima N, Carding S, Akira S, Parkes M, Xavier RJ. 2011. Crohn disease: a current perspective on genetics, autophagy and immunity. Autophagy 7:355-374. http://dx.doi.org/10.4161 /auto.7.4.13074.
3. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H. 2005. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 43:3380-3389. http://dx.doi.org/10.1128/JCM.43.7.3380-3389.2005.
4. Sartor RB. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology 134:577-594. http://dx.doi.org/10.1053/j.gastro.2007.11.059.
5. Chassaing B, Darfeuille-Michaud A. 2011. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140:1720-1728. http://dx.doi.org/10.1053 /j.gastro.2011.01.054.
6. Darfeuille-Michaud A, Neut C, Barnich N, Lederman E, Di Martino P, Desreumaux P, Gambiez L, Joly B, Cortot A, Colombel JF. 1998. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn's disease. Gastroenterology 115:1405-1413. http://dx.doi.org /10.1016/S0016-5085(98)70019-8.
7. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF. 2004. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 127:412-421. http://dx.doi.org/10.1053/j.gastro.2004.04.061.
8. Martinez-Medina M, Aldeguer X, Lopez-Siles M, Gonzalez-Huix F, Lopez-Oliu C, Dahbi G, Blanco JE, Blanco J, Garcia-Gil LJ, Darfeuille-Michaud A. 2009. Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn's disease. Inflamm Bowel Dis 15:872-882. http://dx.doi.org/10.1002/ibd.20860.
9. Martin HM, Campbell BJ, Hart CA, Mpofu C, Nayar M, Singh R, Englyst H, Williams HF, Rhodes JM. 2004. Enhanced Escherichia coli adherence and invasion in Crohn's disease and colon cancer. Gastroenterology 127:80-93. http://dx.doi.org/10.1053/j.gastro.2004.03.054.
10. Baumgart M, Dogan B, Rishniw M, Weitzman G, Bosworth B, Yantiss R, Orsi RH, Wiedmann M, McDonough P, Kim SG, Berg D, Schukken Y, Scherl E, Simpson KW. 2007. Culture independent analysis of ileal mucosa reveals a selective increase in invasive Escherichia coli of novel phylogeny relative to depletion of Clostridiales in Crohn's disease involving the ileum. ISME J 1:403-418. http://dx.doi.org /10.1038/ismej.2007.52.
11. Sasaki M, Sitaraman SV, Babbin BA, Gerner-Smidt P, Ribot EM, Garrett N, Alpern JA, Akyildiz A, Theiss AL, Nusrat A, Klapproth JM. 2007. Invasive Escherichia coli are a feature of Crohn's disease. Lab Invest 87:1042-1054. http://dx.doi.org/10.1038/labinvest.3700661.
12. Eaves-Pyles T, Allen CA, Taormina J, Swidsinski A, Tutt CB, Eric Jezek G, Islas-Islas M, Torres AG. 2007. Escherichia coli isolated from a Crohn's disease patient adheres, invades, and induces inflammatory responses in polarized intestinal epithelial cells. Int J Med Microbiol 298:397-409. http://dx.doi.org/10.1016/j.ijmm.2007.05.011.
13. Barnich N, Boudeau J, Claret L, Darfeuille-Michaud A. 2003. Regulatory and functional co-operation of flagella and type 1 pili in adhesive and invasive abilities of AIEC strain LF82 isolated from a patient with Crohn's disease. Mol Microbiol 48:781-794. http://dx.doi.org/10.1046/j.1365-2958.2003.03468.x.
14. Boudeau J, Barnich N, Darfeuille-Michaud A. 2001. Type 1 pilimediated adherence of Escherichia coli strain LF82 isolated from Crohn's disease is involved in bacterial invasion of intestinal epithelial cells. Mol Microbiol 39:1272-1284. http://dx.doi.org/10.1111/j.1365-2958.2001.02315.x.
15. E regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82. Mol Microbiol 63:1684-1700. http://dx.doi.org/10.1111/j.1365-2958.2007.05638.x.
16. Rolhion N, Barnich N, Bringer MA, Glasser AL, Ranc J, Hebuterne X, Hofman P, Darfeuille-Michaud A. 2010. Abnormally expressed ER stress response chaperone Gp96 inCDfavours adherent-invasive Escherichia coli invasion. Gut 59:1355-1362. http://dx.doi.org/10.1136/gut.2010.207456.
17. Chassaing B, Rolhion N, Vallee A, Salim SY, Prorok-Hamon M, Neut C, Campbell BJ, Soderholm JD, Hugot JP, Colombel JF, Darfeuille-Michaud A. 2011. Crohn disease-associated adherent-invasive E. coli bacteria target mouse and human Peyer's patches via long polar fimbriae. J Clin Invest 121:966-975. http://dx.doi.org/10.1172/JCI44632.
18. Miquel S, Peyretaillade E, Claret L, de Vallee A, Dossat C, Vacherie B, Zineb el, Segurens HB, Barbe V, Sauvanet P, Neut C, Colombel JF, Medigue C, Mojica FJ, Peyret P, Bonnet R, Darfeuille-Michaud A. 2010. Complete genome sequence of Crohn's disease-associated adherentinvasive E. coli strain LF82. PLoS One 5:e12714. http://dx.doi.org/10.1371 /journal.pone.0012714.
19. E pathway is involved in biofilm formation by Crohn's disease-associated adherent-invasive Escherichia coli. J Bacteriol 195:76-84. http://dx.doi.org/10.1128/JB.01079-12.
20. Mecsas J, Welch R, Erickson JW, Gross CA. 1995. Identification and characterization of an outer membrane protein, OmpX, in Escherichia coli that is homologous to a family of outer membrane proteins including Ail of Yersinia enterocolitica. J Bacteriol 177:799-804.
21. Missiakas D, Betton JM, Raina S. 1996. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol 21:871-884. http://dx.doi.org/10.1046/j.1365-2958.1996.561412.x.
22. Rouviere PE, De Las Penas A, Mecsas J, Lu CZ, Rudd KE, Gross CA. 1995. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J 14:1032-1042.
23. E stress response in related genomes. PLoS Biol 4:e2. http://dx.doi.org/10.1371/journal.pbio.0040002.
24. Dartigalongue C, Missiakas D, Raina S. 2001. Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276:20866-20875. http://dx.doi.org/10.1074/jbc.M100464200.
25. E regulon identified by a twoplasmid system. FEMS Microbiol Lett 225:1-7. http://dx.doi.org/10.1016 /S0378-1097(03)00480-4.
26. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
27. Chaveroche MK, Ghigo JM, d'Enfert C. 2000. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28:E97. http://dx.doi.org/10.1093/nar/28.22.e97.
28. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130.
29. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res 14:1188-1190. http://dx.doi.org /10.1101/gr.849004.
30. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1462. http://dx.doi.org/10.1126/science.277.5331.1453.
31. Simons RW, Houman F, Kleckner N. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53: 85-96. http://dx.doi.org/10.1016/0378-1119(87)90095-3.
32. Boudeau J, Glasser AL, Masseret E, Joly B, Darfeuille-Michaud A. 1999. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 67:4499-4509.
33. Martinez-Medina M, Naves P, Blanco J, Aldeguer X, Blanco JE, Blanco M, Ponte C, Soriano F, Darfeuille-Michaud A, Garcia-Gil LJ. 2009. Biofilm formation as a novel phenotypic feature of adherent-invasive Escherichia coli (AIEC). BMC Microbiol 9:202. http://dx.doi.org/10.1186 /1471-2180-9-202.
34. Naves P, del Prado G, Huelves L, Gracia M, Ruiz V, Blanco J, Rodriguez-Cerrato V, Ponte MC, Soriano F. 2008. Measurement of biofilm formation by clinical isolates of Escherichia coli is method-dependent. J Appl Microbiol 105:585-590. http://dx.doi.org/10.1111/j.1365-2672.2008.03791.x.
35. Niu C, Gilbert ES. 2004. Colorimetric method for identifying plant essential oil components that affect biofilm formation and structure. Appl Environ Microbiol 70:6951-6956. http://dx.doi.org/10.1128/AEM.70.12.6951-6956.2004.
36. Valdivia RH, Hromockyj AE, Monack D, Ramakrishnan L, Falkow S. 1996. Applications for green fluorescent protein (GFP) in the study of host-pathogen interactions. Gene 173:47-52. http://dx.doi.org/10.1016 /0378-1119(95)00706-7.
37. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395-2407.
38. Hitotsubashi S, Fujii Y, Yamanaka H, Okamoto K. 1992. Some properties of purified Escherichia coli heat-stable enterotoxin II. Infect Immun 60:4468-4474.
39. Beuzon CR, Holden DW. 2001. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect 3:1345-1352. http://dx.doi.org/10.1016/S1286-4579(01)01496-4.
40. Westphal O, Jann K. 1965. Bacterial lipopolysaccharides. Extraction with phenol-water and further applications of the procedure, p 83-91. In Whistler RL, Wolfan ML (ed), Methods in carbohydrate chemistry. Academic Press, New York, NY.
41. Bringer MA, Barnich N, Glasser AL, Bardot O, Darfeuille-Michaud A. 2005. HtrA stress protein is involved in intramacrophagic replication of adherent and invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 73:712-721. http://dx.doi.org/10.1128/IAI.73.2.712-721.2005.
42. E, is required to maintain cell envelope integrity in Escherichia coli. PLoS One 3:e1573. http://dx.doi.org/10.1371/journal.pone.0001573.
43. E. Mol Microbiol 24:373-385. http://dx.doi.org/10.1046/j.1365-2958.1997.3611718.x.
44. E (RpoE) heat-shock transcriptionfactor activity by the RseA, RseB and RseC proteins. Mol Microbiol 24: 355-371. http://dx.doi.org/10.1046/j.1365-2958.1997.3601713.x.
45. Chassaing B, Etienne-Mesmin L, Bonnet R, Darfeuille-Michaud A. 2013. Bile salts induce long polar fimbriae expression favouring Crohn's disease-associated adherent-invasive Escherichia coli interaction with Peyer's patches. Environ Microbiol 15:355-371. http://dx.doi.org/10.1111/j.1462-2920.2012.02824.x.
46. Egler M, Grosse C, Grass G, Nies DH. 2005. Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. J Bacteriol 187:2297-2307. http://dx.doi.org/10.1128/JB.187.7.2297-2307.2005.
47. E downregulates extracytoplasmic stress responses and outer membrane vesicle production in Escherichia coli. J Bacteriol 189:1523-1530. http://dx.doi.org/10.1128/JB.01534-06.
48. Nash JH, Villegas A, Kropinski AM, Aguilar-Valenzuela R, Konczy P, Mascarenhas M, Ziebell K, Torres AG, Karmali MA, Coombes BK. 2010. Genome sequence of adherent-invasive Escherichia coli and comparative genomic analysis with other E. coli pathotypes. BMC Genomics 11:667. http://dx.doi.org/10.1186/1471-2164-11-667.
49. Krause DO, Little AC, Dowd SE, Bernstein CN. 2011. Complete genome sequence of adherent invasive Escherichia coli UM146 isolated from ileal Crohn's disease biopsy tissue. J Bacteriol 193:583. http://dx.doi.org/10.1128/JB.01290-10.
50. Welch RA, Burland V, Plunkett G, III, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, Blattner FR. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 99:17020-17024. http://dx.doi.org/10.1073/pnas.252529799.
51. Chen SL, Hung CS, Xu J, Reigstad CS, Magrini V, Sabo A, Blasiar D, Bieri T, Meyer RR, Ozersky P, Armstrong JR, Fulton RS, Latreille JP, Spieth J, Hooton TM, Mardis ER, Hultgren SJ, Gordon JI. 2006. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad SciUSA103:5977-5982. http://dx.doi.org/10.1073/pnas.0600938103.
52. Hochhut B, Wilde C, Balling G, Middendorf B, Dobrindt U, Brzuszkiewicz E, Gottschalk G, Carniel E, Hacker J. 2006. Role of pathogenicity island-associated integrases in the genome plasticity of uropathogenic Escherichia coli strain 536. Mol Microbiol 61:584-595. http://dx.doi.org /10.1111/j.1365-2958.2006.05255.x.
53. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C, Skyberg JA, Lynne AM, Johnson JR, Nolan LK. 2007. The genome sequence of avian pathogenic Escherichia coli strain O1: K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 189:3228-3236. http://dx.doi.org/10.1128/JB.01726-06.
54. Kaniuk NA, Vinogradov E, Li J, Monteiro MA, Whitfield C. 2004. Chromosomal and plasmid-encoded enzymes are required for assembly of the R3-type core oligosaccharide in the lipopolysaccharide of Escherichia coli O157:H7. J Biol Chem 279:31237-31250. http://dx.doi.org/10.1074/jbc.M401879200.
55. Leipold MD, Vinogradov E, Whitfield C. 2007. Glycosyltransferases involved in biosynthesis of the outer core region of Escherichia coli lipopolysaccharides exhibit broader substrate specificities than is predicted from lipopolysaccharide structures. J Biol Chem 282:26786-26792. http: //dx.doi.org/10.1074/jbc.M704131200.
56. Heinrichs DE, Yethon JA, Amor PA, Whitfield C. 1998. The assembly system for the outer core portion of R1-and R4-type lipopolysaccharides of Escherichia coli. The R1 core-specific beta-glucosyltransferase provides a novel attachment site for O-polysaccharides. J Biol Chem 273:29497-29505.
57. Xu L, Wang Q, Xiao J, Liu Q, Wang X, Chen T, Zhang Y. 2010. Characterization of Edwardsiella tarda waaL: roles in lipopolysaccharide biosynthesis, stress adaptation, and virulence toward fish. Arch Microbiol 192:1039-1047. http://dx.doi.org/10.1007/s00203-010-0635-z.
58. Han Y, Han X, Wang S, Meng Q, Zhang Y, Ding C, Yu S. 2014. The waaL gene is involved in lipopolysaccharide synthesis and plays a role on the bacterial pathogenesis of avian pathogenic Escherichia coli. Vet Microbiol 172:486-491. http://dx.doi.org/10.1016/j.vetmic.2014.05.029.
59. Abeyrathne PD, Daniels C, Poon KK, Matewish MJ, Lam JS. 2005. Functional characterization of WaaL, a ligase associated with linking O-antigen polysaccharide to the core of Pseudomonas aeruginosa lipopolysaccharide. J Bacteriol 187:3002-3012. http://dx.doi.org/10.1128/JB.187.9.3002-3012.2005.
60. Du H, Sheng X, Zhang H, Zou X, Ni B, Xu S, Zhu X, Xu H, Huang X. 2011. RpoE may promote flagellar gene expression in Salmonella enterica serovar Typhi under hyperosmotic stress. Curr Microbiol 62:492-500. http://dx.doi.org/10.1007/s00284-010-9734-y.
61. Auerbuch V, Lenz LL, Portnoy DA. 2001. Development of a competitive index assay to evaluate the virulence of Listeria monocytogenes actA mutants during primary and secondary infection of mice. Infect Immun 69: 5953-5957. http://dx.doi.org/10.1128/IAI.69.9.5953-5957.2001.
62. Sandlin RC, Goldberg MB, Maurelli AT. 1996. Effect of O side-chain length and composition on the virulence of Shigella flexneri 2a. Mol Microbiol 22:63-73. http://dx.doi.org/10.1111/j.1365-2958.1996.tb02656.x.
63. Ciornei CD, Novikov A, Beloin C, Fitting C, Caroff M, Ghigo JM, Cavaillon JM, Adib-Conquy M. 2010. Biofilm-forming Pseudomonas aeruginosa bacteria undergo lipopolysaccharide structural modifications and induce enhanced inflammatory cytokine response in human monocytes. Innate Immun 16:288-301. http://dx.doi.org/10.1177 /1753425909341807.
64. Beloin C, Michaelis K, Lindner K, Landini P, Hacker J, Ghigo JM, Dobrindt U. 2006. The transcriptional antiterminator RfaH represses biofilm formation in Escherichia coli. J Bacteriol 188:1316-1331. http://dx.doi.org/10.1128/JB.188.4.1316-1331.2006.
65. Nakao R, Ramstedt M, Wai SN, Uhlin BE. 2012. Enhanced biofilm formation by Escherichia coli LPS mutants defective in Hep biosynthesis. PLoS One 7:e51241. http://dx.doi.org/10.1371/journal.pone.0051241.
66. Bandara HM, Lam OL, Watt RM, Jin LJ, Samaranayake LP. 2010. Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59:1225-1234. http://dx.doi.org/10.1099/jmm.0.021832-0.
67. Kulesus RR, Diaz-Perez K, Slechta ES, Eto DS, Mulvey MA. 2008. Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76:3019-3026. http://dx.doi.org/10.1128/IAI.00022-08.
68. Raisch J, Sivignon A, Chassaing B, Lapaquette P, Miquel S, Carvalho F, Rolhion N, Bringer MA, Barnich N, Boudeau J, Di Martino P. 2014. In memoriam, Arlette Darfeuille-Michaud, PhD. Gut 63:1681-1682. http: //dx.doi.org/10.1136/gutjnl-2014-308182.