Mutations that impact the enteropathogenic escherichia coli Cpx envelope stress response attenuate virulence in galleria mellonella

Infection and Immunity

Volumn 80, Issue 9, 2012, Pages 3077-3085

  Leuko, S ^a   Raivio, T L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CECROPIN; ENTEROPATHOGENIC ESCHERICHIA COLI CPX PROTEIN; ENVELOPE PROTEIN; GLOVERIN; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM PILUS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; GALLERIA MELLONELLA; GENE EXPRESSION; IN VIVO STUDY; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL WALL; DISEASE MODELS, ANIMAL; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; LARVA; LEPIDOPTERA; MUTANT PROTEINS; MUTATION, MISSENSE; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; VIRULENCE; VIRULENCE FACTORS;

EID: 84867610333     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00081-12     Document Type: Article

References (77)

1. Andrade A, Pardo JP, Espinosa N, Pérez-Hernández G, González-Pedrajo B. 2007. Enzymatic characterization of the enteropathogenic Escherichia coli type III secretion ATPase EscN. Arch. Biochem. Biophys. 468:121-127.
2. Aperis G, et al. 2007. Galleria mellonella as a model host to study infection by the Francisella tularensis live vaccine strain. Microbes Infect. 9:729-734.
3. Badea L, Beatson SA, Kaparakis M, Ferrero RL, Hartland EL. 2009. Secretion of flagellin by the LEE-encoded type III secretion system of enteropathogenic Escherichia coli. BMC Microbiol. 9:30. doi:10.1186/ 1471-2180-9-30.
4. Barba J, et al. 2005. A positive regulatory loop controls expression of the locus of enterocyte effacement-encoded regulators, Ler and GrlA. J. Bacteriol. 187:7918-7930.
5. Bhatt S, Romeo T, Kalman D. 2011. Honing the message: posttranscriptional and post-translational control in attaching and effacing pathogens. Trends Microbiol. 19:217-224.
6. Bieber D, et al. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 208:2114-2118.
7. Bustamante VH, et al. 2011. PerC and GrlA independently regulate Ler expression in enteropathogenic Escherichia coli. Mol. Microbiol. 82:398-415.
8. Carlsson KE, Liu J, Edqvist PJ, Francis MS. 2007. Influence of the Cpx extracytoplasmic-stress-responsive pathway on Yersinia sp.-eukaryotic cell contact. Infect. Immun. 75:4386-4399.
9. Cevenini R, et al. 1985.Atwo-year longitudinal study on the etiology of acute diarrhea in young children in Northern Italy. Microbiologica 8:51-58.
10. Champion OL, et al. 2009. Galleria mellonella as an alternative infection model for Yersinia pseudotuberculosis. Microbiology 155:1516-1522.
11. Chen HD, Frankel G. 2005. Enteropathogenic Escherichia coli: unravelling pathogenesis. FEMS Microbiol. Rev. 29:83-98.
12. Cornelis GR, Van Gijsegem F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774.
13. Croxen MA, Finlay BB. 2010. Molecular mechanisms of Escherichia coli pathogenicity. Nat. Rev. Microbiol. 8:26-38.
14. Dean P, Kenny B. 2009. The effector repertoire of enteropathogenic E. coli: ganging up on the host cell. Curr. Opin. Microbiol. 12:101-109.
15. De Rycke J, et al. 1997. Enteropathogenic Escherichia coli O103 from rabbit elicits actin stress fibers and focal adhesions in HeLa epithelial cells, cytopathic effects that are linked to an analog of the locus of enterocyte effacement. Infect. Immun. 65:2555-2563.
16. Desbois AP, Coote PJ. 2011. Wax moth larva (Galleria mellonella): an in vivo model for assessing the efficacy of antistaphylococcal agents. J. Antimicrob. Chemother. 66:1785-1790.
17. Dorel C, Lejeune P, Rodrigue A. 2006. The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res. Microbiol. 157:306-314.
18. Duguay AR, Shilhavy TJ. 2004. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694:121-134.
19. Fleischer R, Heermann R, Jung K, Hunke S. 2007. Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J. Biol. Chem. 282:8583-8593.
20. Friedberg D, Umanski T, Fang Y, Rosenshine I. 1999. Hierarchy in the expression of the locus of enterocyte effacement genes of enteropathogenic Escherichia coli. Mol. Microbiol. 34:941-952.
21. Fröhlicher E, Krause G, Zweifel C, Beutin L, Stephan R. 2008. Characterization of attaching and effacing Escherichia coli (AEEC) isolated from pigs and sheep. BMC Microbiol. 8:144. doi:10.1186/1471-2180-8-144.
22. Fuchs BB, O'Brien E, El Khoury JB, Mylonakis E. 2010. Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1:475-482.
23. Gagen SJ, Ratcliffe NA. 1976. Studies on the in vivo cellular reactions and fate of injected bacteria in Galleria mellonella and Pieris brassicae larvae. J. Invert. Pathol. 28:17-24.
24. Held KG, LaRock CN, D'Argenio DA, Berg CA, Collins CM. 2007. A metalloprotease secreted by the insect pathogen Photorhabdus luminescens induces melanization. Appl. Environ. Microbiol. 73:7622-7628.
25. Hill SM, Phillips AD, Walker-Smith JA. 1991. Enteropathogenic Escherichia coli and life threatening chronic diarrhoea. Gut 32:154-158.
26. Hoffmann JA. 1995. Innate immunity of insects. Curr. Opin. Immunol. 7:4-10.
27. Hornsey M, Warenham DW. 2011. In vivo efficacy of glycopeptidecolistin combination therapies in a Galleria mellonella model of Acinetobacter baumannii infection. Antimicrob. Agents Chemother. 55:3534-3537.
28. Hultmark D, Engström Å, Bennich H, Kapur R, Boman HG. 1982. Insect immunity: isolation and structure of cecropin D and four minor antibacterial components from Cecropia pupae. Eur. J. Biochem. 127: 207-217.
29. Humphreys S, et al. 2004. Role of the two-component regulator CpxAR in the virulence of Salmonella enterica serotype Typhimurium. Infect. Immun. 72:4654-4661.
30. Hyland RM, et al. 2008. The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosamine-specific lectin. Cell. Microbiol. 10:177-187.
31. Jander G, Rahme LG, Ausubel FM. 2000. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182:3843-3845.
32. Jerse AE, Yu J, Tall BD, Kaper JB. 1990. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. U. S. A. 87:7839-7843.
33. Jerse AE, Kaper JB. 1991. The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect. Immun. 59:4302-4309.
34. Kitagawa M, et al. 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.
35. Kopácek P, Weise C, Götz P. 1995. The prophenoloxidase from the wax moth Galleria mellonella: purification and characterization of the proenzyme. Insect Biochem. Mol. Biol. 25:1081-1091.
36. Lau-Wong IC, Locke T, Ellison MJ, Raivio TL, Frost LS. 2008. Activation of the Cpx regulon destabilizes the F plasmid transfer activator, TraJ, via the HsIVU protease in Escherichia coli. Mol. Microbiol. 67:516-527.
37. Leblanc, SKD. 2011. Novel inducers and regulon members of the Escherichia coli Bae and Cpx envelope stress response. M.S. thesis. University of Alberta, Edmonton, Canada.
38. Lefoll C, Caubet C, Tasca C, Milon A, Boullier S. 2010. Simultaneous inactivation of espB and tir abrogates the strong, but non-protective, inflammatory response induced by EPEC. Vet. Immunol. Immunopathol. 138:34-44.
39. Levine MM, et al. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet i:1119-1122.
40. ___ΔΔCT method. Methods 25: 402-408.
41. Luperchio SA, Schauer DB. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3:333-340.
42. MacRitchie DM, Ward JD, Nevesinjac AZ, Raivio TL. 2008. Activation of the Cpx envelope stress response down-regulates expression of several locus of enterocyte effacement-encoded genes in enteropathogenic Escherichia coli. Infect. Immun. 76:1465-1475.
43. MacRitchie DM, Buelow DR, Price NL, Raivio TL. 2008. Twocomponent signaling and gram negative envelope stress response systems. Adv. Exp. Med. Biol. 631:80-110.
44. MacRitchie DM, Acosta N, Raivio TL. 2012. DegP is involved in Cpxmediated posttranscriptional regulation of the type III secretion apparatus in enteropathogenic Escherichia coli. Infect. Immun. 80:1766-1772.
45. Maresca M, Miller D, Quitard S, Dean P, Kenny B. 2005. Enteropathogenic Escherichia coli (EPEC) effector-mediated suppression of antimicrobial nitric oxide production in a small intestinal epithelial model system. Cell. Microbiol. 7:1749-1762.
46. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 92:1664-1668.
47. Mellies JL, Elliott SJ, Sperandio V, Donnenberg MS, Kaper JB. 1999. The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33: 296-306.
48. Miyata S, Casey M, Frank DW, Ausubel FM, Drenkard E. 2003. Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect. Immun. 71:2404-2413.
49. Mukherjee K, et al. 2010. Galleria mellonella as a model system for studying Listeria pathogenesis. Appl. Environ. Microbiol. 76:310-317.
50. Mundy R, Girard F, Fitzgerald AJ, Frankel G. 2006. Comparison of colonization dynamics and pathology of mice infected with enteropathogenic Escherichia coli, enterohaemorrhagic E. coli and Citrobacter rodentium. FEMS Microbiol. Lett. 265:126-132.
51. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
52. Nevesinjac AZ, Raivio TL. 2005. The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J. Bacteriol. 187:672-686.
53. Newman JV, Zabel BA, Jha SS, Schauer DB. 1999. Citrobacter rodentium espB is necessary for signal transduction and for infection of laboratory mice. Infect. Immun. 67:6019-6025.
54. Pelayo JS, et al. 1999. Virulence properties of atypical EPEC strains. J. Med. Microbiol. 48:41-49.
55. Peleg AY, et al. 2009. Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob. Agents Chemother. 53:2605-2609.
56. Pukkila-Worley R, Ausubel FM, Mylonakis E. 2011. Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog. 7:e1002074. doi:10.1371/journal.ppat.1002074.
57. Raivio TL, Popkin DL, Silhavy TJ. 1999. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J. Bacteriol. 181:5263-5272.
58. Raivio TL. 2005. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 56:1119-1128.
59. Ratcliffe NA, Gagen SJ. 1976. Cellular defense reactions of insect hemocytes in vivo: nodule formation and development in Galleria mellonella and Pieris brassicae larvae. J. Invert. Pathol. 28:373-382.
60. Robins-Browne RM, et al. 1994. Adherence characteristics of attaching and effacing strains of Escherichia coli from rabbits. Infect. Immun. 62: 1548-1592.
61. Rosenshine I, Ruschkowski S, Finlay BB. 1996. Expression of attaching/ effacing activity by enteropathogenic Escherichia coli depends on growth phase, temperature, and protein synthesis upon contact with epithelial cells. Infect. Immun. 64:966-973.
62. Rowley G, Spector M, Kormanec J, Roberts M. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat. Rev. Microbiol. 4:383-394.
63. Ruchaud-Sparagano MH, Maresca M, Kenny B. 2007. Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell. Microbiol. 9:1909-1921.
64. Savkovic SD, Villanueva J, Turner JR, Matkowskyj KA, Hecht G. 2005. Mouse model of enteropathogenic Escherichia coli infection. Infect. Immun. 73:1161-1170.
65. Schmidt MA. 2010. LEEways: tales of EPEC, ATEC and EHEC. Cell. Microbiol. 12:1544-1552.
66. Seed KD, Dennis JJ. 2008. Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect. Immun. 76:1267-1275.
67. Senior NJ, et al. 2011. Galleria mellonella as an infection model for Campylobacter jejuni virulence. J. Med. Microbiol. 60:661-669.
68. Trabulsi LR, Keller R, Tardelli Gomes TA. 2002. Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 8:508-513.
69. Urban JH, Vogel J. 2007. Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res. 35:1018-1037.
70. Vaara M, Vaara T. 1994. Ability of cecropin B to penetrate the enterobacterial outer membrane. Antimicrob. Agents Chemother. 38:2498-2501.
71. Vogel H, Altincicek B, Glöckner G, Vilcinskas A. 2011. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 12:308. doi:10.1186/1471-2164-12-308.
72. Vogt SL, et al. 2010. The Cpx envelope stress response both facilitates and inhibits elaboration of the enteropathogenic Escherichia coli bundleforming pilus. Mol. Microbiol. 76:1095-1110.
73. Vogt SL, Raivio TL. 2012. Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol. Lett. 326:2-11.
74. Wand ME, Müller CM, Titball RW, Michell SL. 2011. Macrophage and Galleria mellonella infection models reflect the virulence of naturally occurring isolates of B. pseudomallei, B. thailandensis and B. oklahomensis. BMC Microbiol. 11:11. doi:10.1186/1471-2180-11-11.
75. Weatherspoon-Griffin N, et al. 2011. The CpxR/CpxA two-component system up-regulates two Tat-dependent peptidoglycan amidases to confer bacterial resistance to antimicrobial peptides. J. Biol. Chem. 18:5529-5539.
76. Wojda I, Jakubowicz T. 2007. Humoral immune response upon mild heat-shock conditions in Galleria mellonella larvae. J. Insect Physiol. 53: 1134-1144.
77. Zhao C, et al. 2010. Role of methionine sulfoxide reductase A and B of Enterococcus faecalis in oxidative stress and virulence. Infect. Immun. 78: 3889-3897.