Response of extraintestinal pathogenic Escherichia coli to human serum reveals a protective role for Rcs-regulated exopolysaccharide colanic acid

Infection and Immunity

Volumn 82, Issue 1, 2014, Pages 298-305

  Miajlovic, Helen ^a   Cooke, Niamh M ^a   Moran, Gary P ^b   Rogers, Thomas R F ^a   Smith, Stephen G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CARBENICILLIN; CHLORAMPHENICOL; COLANIC ACID; COMPLEMENT; COMPLEMENTARY DNA; EXOPOLYSACCHARIDE; KANAMYCIN; RNA; UNCLASSIFIED DRUG; VIRULENCE FACTOR; ZYMOSAN;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM CULTURE; BLOODSTREAM INFECTION; COLONY FORMING UNIT; COMPLEMENT SYSTEM; DELETION MUTANT; ESCHERICHIA COLI INFECTION; EXTRAINTESTINAL PATHOGENIC ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GRAM NEGATIVE INFECTION; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERUM; SURVIVAL RATE;

EID: 84890811277     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00800-13     Document Type: Article

References (61)

1. Russo TA, Johnson JR. 2003. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect. 5:449-456. http://dx.doi.org/10.1016/S1286-4579(03)00049-2.
2. Fluit AC, Jones ME, Schmitz FJ, Acar J, Gupta R, Verhoef J. 2000. Antimicrobial susceptibility and frequency of occurrence of clinical blood isolates in Europe from the SENTRY antimicrobial surveillance program, 1997 and 1998. Clin. Infect. Dis. 30:454-460. http://dx.doi.org/10.1086/313710.
3. Stelling JM, Travers K, Jones RN, Turner PJ, O'Brien TF, Levy SB. 2005. Integrating Escherichia coli antimicrobial susceptibility data from multiple surveillance programs. Emerg. Infect. Dis. 11:873-882. http://dx.doi.org/10.3201/eid1106.041160.
4. Buckles EL, Wang X, Lane MC, Lockatell CV, Johnson DE, Rasko DA, Mobley HL, Donnenberg MS. 2009. Role of the K2 capsule in Escherichia coli urinary tract infection and serum resistance. J. Infect. Dis. 199:1689-1697. http://dx.doi.org/10.1086/598524.
5. Wiles TJ, Kulesus RR, Mulvey MA. 2008. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp. Mol. Pathol. 85:11-19. http://dx.doi.org/10.1016/j.yexmp.2008.03.007.
6. Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ. 2000. Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc. Natl. Acad. Sci. U.S.A. 97:8829-8835. http://dx.doi.org/10.1073/pnas.97.16.8829.
7. Taylor RP, Burge J, Horgan CD, Shasby M. 1983. The complementmediated binding of soluble antibody/dsDNA immune complexes to human neutrophils. J. Immunol. 130:2656-2662.
8. Cooper NR. 1999. Biology of the complement system, p 281-315. In Gallin JJ, Snyderman R (ed), Inflammation: basic principles and clinical correlates. Lippincott Williams & Wilkins, Philadelphia, PA.
9. Callewaert L, Michiels CW. 2010. Lysozymes in the animal kingdom. J. Biosci. 35:127-160. http://dx.doi.org/10.1007/s12038-010-0015-5.
10. Whitfield C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75:39-68. http://dx.doi.org/10.1146/annurev.biochem.75.103004.142545.
11. Ferrieres L, Aslam SN, Cooper RM, Clarke DJ. 2007. The yjbEFGH locus in Escherichia coli K-12 is an operon encoding proteins involved in exopolysaccharide production. Microbiology 153:1070-1080. http://dx.doi.org/10.1099/mic.0.2006/002907-0.
12. Stevenson G, Andrianopoulos K, Hobbs M, Reeves PR. 1996. Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J. Bacteriol. 178:4885-4893.
13. Prasadarao NV, Blom AM, Villoutreix BO, Linsangan LC. 2002. A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1. J. Immunol. 169:6352-6360. http://www.jimmunol.org/content/169/11/6352.
14. Mellata M, Dho-Moulin M, Dozois CM, Curtiss R, Lehoux B, Fairbrother JM. 2003. Role of avian pathogenic Escherichia coli virulence factors in bacterial interaction with chicken heterophils and macrophages. Infect. Immun. 71:494-503. http://dx.doi.org/10.1128/IAI.71.1.494-503.2003.
15. Johnson JR. 1991. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 4:80-128.
16. Waters VL, Crosa JH. 1991. Colicin V virulence plasmids. Microbiol. Rev. 55:437-450.
17. Ambrozic J, Ostroversnik A, Starcic M, Kuhar I, Grabnar M, Zgur-Bertok D. 1998. Escherichia coli CoIV plasmid pRK100: genetic organization, stability and conjugal transfer. Microbiology 144(Part 2):343-352. http://dx.doi.org/10.1099/00221287-144-2-343.
18. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, Lockatell CV, Jones BD, Warren JW. 1990. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect. Immun. 58:1281-1289.
19. Ford I, Douglas CW, Heath J, Rees C, Preston FE. 1996. Evidence for the involvement of complement proteins in platelet aggregation by Streptococcus sanguis NCTC 7863. Br. J. Haematol. 94:729-739. http://dx.doi.org/10.1046/j.1365-2141.1996.d01-1857.x.
20. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262.
21. Mangan MW, Lucchini S, Danino V, Croinin TO, Hinton JC, Dorman CJ. 2006. The integration host factor (IHF) integrates stationary-phase and virulence gene expression in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 59:1831-1847. http://dx.doi.org/10.1111/j.1365-2958.2006.05062.x.
22. 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.
23. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291-299. http://dx.doi.org/10.1093/dnares/dsi012.
24. Leying H, Suerbaum S, Kroll HP, Stahl D, Opferkuch W. 1990. The capsular polysaccharide is a major determinant of serum resistance in K-1-positive blood culture isolates of Escherichia coli. Infect. Immun. 58:222-227.
25. Bliska JB, Falkow S. 1992. Bacterial resistance to complement killing mediated by the Ail protein of Yersinia enterocolitica. Proc. Natl. Acad. Sci. U.S.A. 89:3561-3565. http://dx.doi.org/10.1073/pnas.89.8.3561.
26. Ionescu M, Belkin S. 2009. Overproduction of exopolysaccharides by an Escherichia coli K-12 rpoS mutant in response to osmotic stress. Appl. Environ. Microbiol. 75:483-492. http://dx.doi.org/10.1128/AEM.01616-08.
27. Vanderkelen L, Ons E, Van Herreweghe JM, Callewaert L, Goddeeris BM, Michiels CW. 2012. Role of lysozyme inhibitors in the virulence of avian pathogenic Escherichia coli. PLoS One 7:e45954. http://dx.doi.org/10.1371/journal.pone.0045954.
28. Mao Y, Doyle MP, Chen J. 2001. Insertion mutagenesis of wca reduces acid and heat tolerance of enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:3811-3815. http://dx.doi.org/10.1128/JB.183.12.3811-3815.2001.
29. Vogt SL, Raivio TL. 2012. Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol. Lett. 326:2-11. http://dx.doi.org/10.1111/j.1574-6968.2011.02406.x.
30. Quan S, Koldewey P, Tapley T, Kirsch N, Ruane KM, Pfizenmaier J, Shi R, Hofmann S, Foit L, Ren G, Jakob U, Xu Z, Cygler M, Bardwell JC. 2011. Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nat. Struct. Mol. Biol. 18:262-269. http://dx.doi.org/10.1038/nsmb.2016.
31. Bury-Mone S, Nomane Y, Reymond N, Barbet R, Jacquet E, Imbeaud S, Jacq A, Bouloc P. 2009. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet. 5:e1000651. http://dx.doi.org/10.1371/pgen.1000651.
32. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. 2006. Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol. 4:e2. http://dx.doi.org/10.1371/pbio.0040002.
33. Rowley G, Spector M, Kormanec J, Roberts M. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4:383-394. http://dx.doi.org/10.1038/nrmicro1394.
34. Redford P, Roesch PL, Welch RA. 2003. DegS is necessary for virulence and is among extraintestinal Escherichia coli genes induced in murine peritonitis. Infect. Immun. 71:3088-3096. http://dx.doi.org/10.1128/IAI.71.6.3088-3096.2003.
35. Clarke DJ. 2010. The Rcs phosphorelay: more than just a two-component pathway. Future Microbiol. 5:1173-1184. http://dx.doi.org/10.2217/fmb.10.83.
36. Hagiwara D, Sugiura M, Oshima T, Mori H, Aiba H, Yamashino T, Mizuno T. 2003. Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J. Bacteriol. 185:5735-5746. http://dx.doi.org/10.1128/JB.185.19.5735-5746.2003.
37. Garcia-Calderon CB, Garcia-Quintanilla M, Casadesus J, Ramos-Morales F. 2005. Virulence attenuation in Salmonella enterica rcsC mutants with constitutive activation of the Rcs system. Microbiology 151:579-588. http://dx.doi.org/10.1099/mic.0.27520-0.
38. Mouslim C, Delgado M, Groisman EA. 2004. Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Mol. Microbiol. 54:386-395. http://dx.doi.org/10.1111/j.1365-2958.2004.04293.x.
39. Francez-Charlot A, Castanie-Cornet MP, Gutierrez C, Cam K. 2005. Osmotic regulation of the Escherichia coli bdm (biofilm-dependent modulation) gene by the RcsCDB His-Asp phosphorelay. J. Bacteriol. 187: 3873-3877. http://dx.doi.org/10.1128/JB.187.11.3873-3877.2005.
40. Majdalani N, Gottesman S. 2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379-405. http://dx.doi.org/10.1146/annurev.micro.59.050405.101230.
41. Lehti TA, Heikkinen J, Korhonen TK, Westerlund-Wikstrom B. 2012. The response regulator RcsB activates expression of Mat fimbriae in meningitic Escherichia coli. J. Bacteriol. 194:3475-3485. http://dx.doi.org/10.1128/JB.06596-11.
42. Brill JA, Quinlan-Walshe C, Gottesman S. 1988. Fine-structure mapping and identification of two regulators of capsule synthesis in Escherichia coli K-12. J. Bacteriol. 170:2599-2611.
43. Fredericks CE, Shibata S, Aizawa S, Reimann SA, Wolfe AJ. 2006. Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay. Mol. Microbiol. 61:734-747. http://dx.doi.org/10.1111/j.1365-2958.2006.05260.x.
44. Russo TA, Sharma G, Weiss J, Brown C. 1995. The construction and characterization of colanic acid deficient mutants in an extraintestinal isolate of Escherichia coli (O4/K54/H5). Microb. Pathog. 18:269-278.
45. Allen PM, Fisher D, Saunders JR, Hart CA. 1987. The role of capsular polysaccharide K21b of Klebsiella and of the structurally related colanicacid polysaccharide of Escherichia coli in resistance to phagocytosis and serum killing. J. Med. Microbiol. 24:363-370.
46. Li G, Laturnus C, Ewers C, Wieler LH. 2005. Identification of genes required for avian Escherichia coli septicemia by signature-tagged mutagenesis. Infect. Immun. 73:2818-2827. http://dx.doi.org/10.1128/IAI.73.5.2818-2827.2005.
47. Phan MD, Peters KM, Sarkar S, Lukowski SW, Allsopp LP, Moriel DG, Achard ME, Totsika M, Marshall VM, Upton M, Beatson SA, Schembri MA. 2013. The serum resistome of a globally disseminated multidrug resistant uropathogenic Escherichia coli clone. PLoS Genet. 9:e1003834. http://dx.doi.org/10.1371/journal.pgen.1003834.
48. Laubacher ME, Ades SE. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190:2065-2074. http://dx.doi.org/10.1128/JB.01740-07.
49. Kamensek S, Zgur-Bertok D. 2013. Global transcriptional responses to the bacteriocin colicin M in Escherichia coli. BMC Microbiol. 13:42. http://dx.doi.org/10.1186/1471-2180-13-42.
50. Callewaert L, Vanoirbeek KG, Lurquin I, Michiels CW, Aertsen A. 2009. The Rcs two-component system regulates expression of lysozyme inhibitors and is induced by exposure to lysozyme. J. Bacteriol. 191:1979-1981. http://dx.doi.org/10.1128/JB.01549-08.
51. Glover WA, Yang Y, Zhang Y. 2009. Insights into the molecular basis of L-form formation and survival in Escherichia coli. PLoS One 4:e7316. http://dx.doi.org/10.1371/journal.pone.0007316.
52. Ranjit DK, Young KD. 2013. The Rcs stress response and accessory envelope proteins are required for de novo generation of cell shape in Escherichia coli. J. Bacteriol. 195:2452-2462. http://dx.doi.org/10.1128/JB.00160-13.
53. Baquero MR, Bouzon M, Quintela JC, Ayala JA, Moreno F. 1996. dacD, an Escherichia coli gene encoding a novel penicillin-binding protein (PBP6b) with DD-carboxypeptidase activity. J. Bacteriol. 178:7106-7111.
54. Tatar LD, Marolda CL, Polischuk AN, van Leeuwen D, Valvano MA. 2007. An Escherichia coli undecaprenyl-pyrophosphate phosphatase implicated in undecaprenyl phosphate recycling. Microbiology 153:2518-2529. http://dx.doi.org/10.1099/mic.0.2007/006312-0.
55. Liu YF, Yan JJ, Lei HY, Teng MH, Wang C, Tseng CC, Wu JJ. 2012. Loss of outer membrane protein C in Escherichia coli contributes to both antibiotic resistance and escaping antibody-dependent bactericidal activity. Infect. Immun. 80:1815-1822. http://dx.doi.org/10.1128/IAI.06395-11.
56. Bekhit A, Fukamachi T, Saito H, Kobayashi H. 2011. The role of OmpC and OmpF in acidic resistance in Escherichia coli. Biol. Pharm. Bull. 34:330-334. http://dx.doi.org/10.1248/bpb.34.330.
57. Samartzidou H, Delcour AH. 1999. Excretion of endogenous cadaverine leads to a decrease in porin-mediated outer membrane permeability. J. Bacteriol. 181:791-798.
58. Boyer HW, Roulland-Dussoix D. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
59. Achtman M, Mercer A, Kusecek B, Pohl A, Heuzenroeder M, Aaronson W, Sutton A, Silver RP. 1983. Six widespread bacterial clones among Escherichia coli K1 isolates. Infect. Immun. 39:315-335.
60. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
61. Amann E, Ochs B, Abel KJ. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69:301-315.