Virulence factors of Escherichia coli, with emphasis on avian pathogenic isolates;Virulentiefactoren van Escherichia coli met nadruk op aviair pathogene isolaten

Tijdschrift voor Diergeneeskunde

Volumn 131, Issue 22, 2006, Pages 822-830

  Landman, W J M ^a   Cornelissen, R A ^b  

^a GD ANIMAL HEALTH   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; VIRULENCE FACTOR;

ANIMAL; ANIMAL DISEASE; ARTICLE; BIOSYNTHESIS; BIRD DISEASE; CHICKEN; ENTEROBACTER INFECTION; ESCHERICHIA COLI; METABOLISM; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

ADHESINS, ESCHERICHIA COLI; ANIMALS; CHICKENS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; POULTRY DISEASES; VIRULENCE; VIRULENCE FACTORS;

AVES; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 33845270394     PISSN: 00407453     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (96)

1. Caya F, Fairbrother JM, Lessard L and Quessy S. Characterization of the risk to human health of pathogenic Escherichia coli isolates from chicken carcasses. J Food Prot 1999; 62: 741-746.
2. Lior H. Classification of Escherichia coli. In: Gyles CL, editor. Escherichia coli in domestic animals and humans. Wallingford, United Kingdom: CAB International: 1994: p. 31-72.
3. Nataro JP and Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998; 11: 142-201.
4. Barnes HJ, Vaillancourt J-P and Gross WB. Colibacillosis. In: Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR, Swayne DE, editors. Diseases of poultry. 11 ed. Ames, Iowa, USA: Iowa State Press; 2003: p. 631-656.
5. Cloud SS, Rosenberger JK, Fries PA, Wilson RA and Odor EM. In vitro and in vivo characterization of avian Escherichia coli. 1. Serotypes, metabolic activity, and antibiotic sensitivity. Avian Dis 1985; 29: 1084-1093.
6. Dozois CM, Fairbrother JM, Harel J and Bosse M. pap-and pil-related DNA sequences and other virulence determinants associated with Escherichia coli isolated from septicemic chickens and turkeys. Infect Immun 1992; 60: 2648-2656.
7. Gomis SM, Goodhope R, Kumor L, Caddy N, Riddell C, Potter AA and Allan BJ. Isolation of Escherichia coli from cellulitis and other lesions of the same bird in broilers at slaughter. Can Vet J 1997; 38: 159-162.
8. Vandekerchove D, De Herdt P, Laevens H and Pasmans F. Colibacillosis in caged layer hens: characteristics of the disease and the aetiological agent. Avian Pathol 2004; 33: 117-125.
9. Bisgaard M and Dam A. Salpingitis in poultry. I. Prevalence, bacteriology and possible pathogenesis in broilers. Nord Vet Med 1980; 32: 361-368.
10. Bisgaard M and Dam A. Salpingitis in poultry. II. Prevalence, bacteriology, and possible pathogenesis in egg-laying chickens. Nord Vet Med 1981; 33: 81-89.
11. Blanco JE, Blanco M, Mora A and Blanco J. Production of toxins (enterotoxins, verotoxins, and necrotoxins) and colicins by Escherichia coli strains isolated from septicemic and healthy chickens: relationship with in vivo pathogenicity. J Clin Microbiol 1997; 35: 2953-2957.
12. Carvalho de Moura AC, Irino K and Vidotto MC. Genetic variability of avian Escherichia coli strains evaluated by enterobacterial repetitive intergenic consensus and repetitive extragenic palindromic polymerase chain reaction. Avian Dis 2001; 45: 173-181.
13. Onderka DK, Hanson JA, McMillan KR and Allan B. Escherichia coli-associated cellulitis in broilers: correlation with systemic infection and microscopic visceral lesions, and evaluation for skin trimming. Avian Dis 1997; 41: 935-940.
14. Linnerborg M, Weintraub A and Widmalm G. Structural studies utilizing 13C-enrichment of the O-antigen polysaccharide from the enterotoxigenic Escherichia coli O159 cross-reacting with Shigella dysenteriae type 4. Eur J Biochem 1999; 266: 246-251.
15. Braun V, Bosch V, Klumpp ER, Neff I, Mayer H and Schlecht S. Antigenic determinants of murein lipoprotein and its exposure at the surface of Enterobacteriaceae. Eur J Biochem 1976; 62: 555-566.
16. Ewing WH. Edwards and Ewing's Identification of Enterobacteriaceae. 4th edn. New York: Elsevier Science; 1986.
17. Orskov I, Orskov F, Jann B and Jann K. Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriol Rev 1977; 41: 667-710.
18. Winkle S, Refai M and Rohde R. On the antigenic relationship of 'Vibrio cholerae' to 'Enterobacteriaceae'. Ann Inst Pasteur (Paris). 1972;123:775-781.
19. Gyles CL. Escherichia coli in domestic animals and humans. Wallingford, United Kingdom: CAB International; 1994.
20. Todar K. Pathogenic Escherichia coli. Textbook of Bacteriology 2002 [cited 2006 July, 3rd]; Available from: http://www.textbookofbacteriology.net/e. coli.html
21. Klemm P, Jorgensen BJ, Die I van, Ree H de and Bergmans H. The fim genes responsible for synthesis of type I fimbriae in Escherichia coli, cloning and genetic organization. Mol Gen Genet 1985; 199: 410-414.
22. Sauer FG, Mulvey MA, Schilling JD, Martinez JJ and Hultgren SJ. Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol 2000; 3: 65-72.
23. Dozois CM, Pourbakhsh SA and Fairbrother JM. Expression of P and type 1 (F1) fimbriae in pathogenic Escherichia coli from poultry. Vet Microbiol 1995; 45: 297-309.
24. Pourbakhsh SA, Dho-Moulin M, Bree A, Desautels C, Martineau-Doize B and Fairbrother JM. Localization of the in vivo expression of P and F1 fimbriae in chickens experimentally inoculated with pathogenic Escherichia coli. Microb Pathog 1997; 22: 331-341.
25. Pourbakhsh SA, Boulianne M, Martineau-Doize B and Fairbrother JM. Virulence mechanisms of avian fimbriated Escherichia coli in experimentally inoculated chickens. Vet Microbiol 1997; 58: 195-213.
26. Dho-Moulin M and Fairbrother JM. Avian pathogenic Escherichia coli (APEC). Vet Res 1999; 30: 299-316.
27. Mellata M, Bakour R, Jacquemin E and Mainil JG. Genotypic and phenotypic characterization of potential virulence of intestinal avian Escherichia coli strains isolated in Algeria. Avian Dis 2001; 45: 670-679.
28. Kobayashi H, Pohjanvirta T and Pelkonen S. Prevalence and characteristics of intimin- and Shiga toxin-producing Escherichia coli from gulls, pigeons and broilers in Finland. J Vet Med Sci 2002; 64: 1071-1073.
29. Stordeur P, Marlier D, Blanco J, Oswald E, Biet F, Dho-Moulin M and Mainil J. Examination of Escherichia coli from poultry for selected adhesin genes important in disease caused by mammalian pathogenic E. coli. Vet Microbiol 2002; 84: 231-241.
30. Babai R, Blum-Oehler G, Stern BE, Hacker J and Ron EZ. Virulence patterns from septicemic Escherichia coli O78 strains. FEMS Microbiol Lett 1997; 149: 99-105.
31. Brown PK, Dozois CM, Nickerson CA, Zuppardo A, Terlonge J and Curtiss R, 3rd. 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.
32. Cogan TA, Jorgensen F, Lappin-Scott HM, Benson CE, Woodward MJ and Humphrey TJ. Flagella and curli fimbriae are important for the growth of Salmonella enterica serovars in hen eggs. Microbiology 2004; 150: 1063-1071.
33. Maurer JJ, Brown TP, Steffens WL and Thayer SG. The occurrence of ambient temperature-regulated adhesins, curli, and the temperature-sensitive hemagglutinin tsh among avian Escherichia coli. Avian Dis 1998; 42: 106-118.
34. Mellata M, Dho-Moulin M, Dozois CM, Curtiss R, 3rd, Brown PK, Arne P, Bree A, Desautels C and Fairbrother JM. Role of virulence factors in resistance of avian pathogenic Escherichia coli to serum and in pathogenicity. Infect Immun 2003; 71: 536-540.
35. Mellata M, Dho-Moulin M, Dozois CM, Curtiss R, 3rd, Lehoux B and Fairbrother JM. Role of avian pathogenic Escherichia coli virulence factors in bacterial interaction with chicken heterophils and macrophages. Infect Immun 2003; 71: 494-503.
36. Hammar M, Arnqvist A, Bian Z, Olsen A and 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.
37. Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P and Dorel C. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 2001; 183: 7213-723.
38. Bojesen AM, Torpdahl M, Christensen H, Olsen JE and Bisgaard M. Genetic diversity of Gallibacterium anatis isolates from different chicken flocks. J Clin Microbiol 2003; 41: 2737-2740.
39. Dozois CM, Dho-Moulin M, Bree A, Fairbrother JM, Desautels C and Curtiss R, 3rd. Relationship between the Tsh autotransporter and pathogenicity of avian Escherichia coli and localization and analysis of the tsh genetic region. Infect Immun 2000; 68: 4145-4154.
40. Janssen T, Schwarz C, Preikschat P, Voss M, Philipp HC and Wieler LH. Virulence-associated genes in avian pathogenic Escherichia coli (APEC) isolated from internal organs of poultry having died from colibacillosis. Int J Med Microbiol 2001; 291: 371-378.
41. Parreira VR and Gyles CL. Shiga toxin genes in avian Escherichia coli. Vet Microbiol 2002; 87: 341-352.
42. Lafont JP, Dho M, D'Hauteville HM, Bree A and Sansonetti PJ. Presence and expression of aerobactin genes in virulent avian strains of Escherichia coli. Infect Immun 1987; 55: 193-197.
43. Silveira WD da, Ferreira A, Brocchi M, de Hollanda LM, Pestana Castro AF de, Tatsumi Yamada A and Lancelloti M. Biological characteristics and pathogenicity of avian Escherichia coli strains. Vet Microbiol 2002; 85: 47-53.
44. Wooley RE, Spears KR, Brown J, Nolan LK and Fletcher OJ. Relationship of complement resistance and selected virulence factors in pathogenic avian Escherichia coli. Avian Dis 1992; 36: 679-684.
45. Dozois CM, Daigle F and Curtiss R, 3rd. Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci USA 2003; 100: 247-252.
46. Bhakdi S, Mackman N, Menestrina G, Gray L, Hugo F, Seeger W and Holland IB. The hemolysin of Escherichia coli. Eur J Epidemiol 1988; 4: 135-143.
47. La Ragione RM and Woodward MJ. Virulence factors of Escherichia coli serotypes associated with avian colisepticaemia. Res Vet Sci 2002; 73: 27-35.
48. Martinez JL, Herrero M and Lorenzo V de. The organization of intercistronic regions of the aerobactin operon of pColV-K30 may account for the differential expression of the iucABCD iutA genes. J Mol Biol 1994; 238: 288-293.
49. Lorenzo V de, Wee S, Herrero M and Neilands JB. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol 1987; 169: 2624-2630.
50. Mills SA and Marietta MA. Metal binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli. Biochemistry 2005; 44: 13553-13559.
51. Gophna U, Oelschlaeger TA, Hacker J and Ron EZ. Yersinia HPI in septicemic Escherichia coli strains isolated from diverse hosts. FEMS Microbiol Lett 2001; 196: 57-60.
52. Ewers C, Janssen T, Kiessling S, Philipp HC and Wieler LH. Rapid detection of virulence-associated genes in avian pathogenic Escherichia coli by multiplex polymerase chain reaction. Avian Dis 2005; 49: 269-273.
53. Gilson L, Mahanty HK and Kolter R. Four plasmid genes are required for colicin V synthesis, export, and immunity. J Bacteriol 1987; 169: 2466-2470.
54. Waters VL, and Crosa JH. Colicin V virulence plasmids. Microbiol Rev 1991; 55: 437-450.
55. Path MJ, Mahanty HK and Kolter R. Characterization of a purF operon mutation which affects colicin V production. J Bacteriol 1989; 171: 3158-3161.
56. Slatin SL, Duche D, Kienker PK and Baty D. Gating movements of colicin A and colicin Ia are different. J Membr Biol 2004; 202: 73-83.
57. Zakharov SD and Cramer WA. Colicin crystal structures: pathways and mechanisms for colicin insertion into membranes. Biochim Biophys Acta 2002; 1565: 333-346.
58. McPeake SJ, Smyth JA and Ball HJ. Characterisation of avian pathogenic Excherichia coli (APEC) associated with colisepticaemia compared to faecal isolates from healthy birds. Vet Microbiol 2005; 110: 245-253.
59. Beutin L, Geier D, Steinruck H, Zimmermann S and Scheutz F. Prevalence and some properties of verotoxin (Shiga-like toxin)-producing Escherichia coli in seven different species of healthy domestic animals. J Clin Microbiol 1993; 31: 2483-2488.
60. Cherifi A, Contrepois M, Picard B, Goullet Ph, de Rycke J, Fairbrother J and Barnouin. Factors and markers of virulence in Escherichia coli from human septicemia. FEMS Microbiol Lett 1990; 70: 279-283.
61. Vidotto MC, Muller EE, Freitas JC de, Alfieri AA, Guimaraes IG and Santos DS. Virulence factors of avian Escherichia coli. Avian Dis 1990; 34: 531-538.
62. McNab RM, Flagella, in Escherichia coli and Salmonella thyphimurium. In: Neidhardt FC, Aarestrup FM, Babai R, Camp M. D'Hauteville HM, editors. Cellular and Molecular Biology. Washington, D.C.: American Society for Microbiology; 1987: p. 70-83.
63. McNab RM. Motility and chemotaxis, in Escherichia coli and Salmonella thyphimurium. In: Neidhardt FC, Aarestrup FM, Babai R, Camp M. D'Hauteville HM, editors. Cellular and Molecular Biology. Washington, D.C.: American Society for Microbiology; 1987: p. 732-59.
64. Wyborn NR, Clark A, Roberts RE, Jamieson SJ, Tzokov S, Bullough PA, Stillman TJ, Artymiuk PJ, Galen JE, Zhao L, Levine MM and Green. J. Properties of haemolysin E (HlyE) from a pathogenic Escherichia coli avian isolate and studies of HlyE export. Microbiology 2004; 150: 1495-1505.
65. Reingold J, Starr N, Maurer J and Lee MD. Identification of a new Escherichia coli She haemolysin homolog in avian E. coli. Vet Microbiol 1999; 66: 125-134.
66. Parreira VR and Yano T. Cytotoxin produced by Escherichia coli isolated from chickens with swollen head syndrome (SHS). Vet Microbiol 1998; 62: 111-119.
67. Delicato ER, Brito BG de, Gaziri LC and Vidotto MC. Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis. Vet Microbiol 2003; 94: 97-103.
68. Stathopoulos C, Provence DL and Curtiss R, 3rd. Characterization of the avian pathogenic Escherichia coli hemagglutinin Tsh, a member of the immunoglobulin A protease-type family of autotransporters. Infect Immun 1999; 67: 772-781.
69. Altekruse S. Characterization of Clinical and Commensal Escherichia coli. Isolates from an Integrated Turkey Operation [PhD Thesis, Virginia Polytechnic Institute and State University]; 2001.
70. Beutler B and Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 2003; 3: 169-176.
71. Rocha AC da, Silva AB da, Brito AB de, Moraes HL, Pontes AP, Ce MC, Nascimento VP do and Salle CT. Virulence factors of avian pathogenic Escherichia coli isolated from broilers from the south of Brazil. Avian Dis 2002; 46: 749-753.
72. Nolan LK, Horne SM, Giddings CW, Foley SL, Johnson TJ, Lynne AM and Skyberg J. Resistance to serum complement, iss, and virulence of avian Escherichia coli. Vet Res Commun 2003; 27: 101-110.
73. Jeffrey JS, Nolan LK, Tonooka KH, Wolfe S, Giddings CW, Home SM. Foley SL, Lynne AM, Ebert JO, Elijah LM, Bjorklund G, Pfaff-McDonough SJ, Singer RS and Doetkott C. Virulence factors of Escherichia coli from cellulitis or colisepticemia lesions in chickens. Avian Dis 2002;46:48-52.
74. Vandemaele F, Assadzadeh A, Derijcke J, Vereecken M and Goddeeris BM. Avian pathogenic Escherichia coli (APEC). Tijdschr Diergeneeskd 2002; 127: 582-588.
75. Bree A, Dho M and Lafont JP. Comparative infectivity for axenic and specific-pathogen-free chickens of O2 Escherichia coli strains with or without virulence factors. Avian Dis 1989; 33: 134-139.
76. Van Dijk WC, Verbrugh HA, Tol ME van der, Peters R and Verhoef J. Role of Escherichia coli K capsular antigens during complement activation, C3 fixation, and opsonization. Infect Immun 1979; 25: 603-609.
77. Feria C, Machado J, Correia JD, Goncalves J and Gaastra W. Virulence genes and P fimbriae PapA subunit diversity in canine and feline uropathogenic Escherichia coli. Vet Microbiol 2001; 82: 81-89.
78. Johnson JR, Stell AL, Scheutz F, O'Bryan TT, Russo TA, Carlino UB, Fasching C, Kavle J, van Dijk L and Gaastra W. Analysis of the F antigen-specific papA alleles of extraintestinal pathogenic Escherichia coli using a novel multiplex PCR-based assay. Infect Immun 2000; 68: 1587-1599.
79. Skyberg JA, Horne SM, Giddings CW, Wooley RE, Gibbs PS and Nolan LK. Characterizing avian Escherichia coli isolates with multiplex polymerase chain reaction. Avian Dis 2003; 47: 1441-1447.
80. Dozois CM, Harel J and Fairbrother JM. P-fimbriae-producing septicaemic Escherichia coli from poultry possess fel-related gene clusters whereas pap-hybridizing P-fimbriae-negative strains have partial or divergent P fimbrial gene clusters. Microbiology 1996; 142: 2759-2766.
81. Dho M and Lafont JP. Escherichia coli colonization of the trachea in poultry: comparison of virulent and avirulent strains in gnotoxenic chickens. Avian Dis 1982; 26: 787-797.
82. Dho M and Lafont JP. Adhesive properties and iron uptake ability in Escherichia coli lethal and nonlethal for chicks. Avian Dis 1984; 28: 1016-1025.
83. Vidotto MC, Gaziri LC and Delicato ER. Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis: correction. Vet Microbiol 2004; 102: 95-96.
84. Vandekerchove D, Vandemaele F, Adriaensen C, Zaleska M, Hernalsteens JP, De Baets L, Butaye P, Immerseel F van, Wattiau P, Laevens H, Mast J, Goddeeris B and Pasmans F. Virulence-associated traits in avian Escherichia coli: comparison between isolates from colibacillosis-affected and clinically healthy layer flocks. Vet Microbiol 2005; 108:75-87.
85. Nolan LK, Giddings CW, Horne SM, Doetkott C, Gibbs PS, Wooley RE and Foley SL. Complement resistance, as determined by viable count and flow cytometric methods, and its association with the presence of iss and the virulence of avian Escherichia coli. Avian Dis 2002; 46: 386-392.
86. Gibbs PS, Maurer JJ, Nolan LK and Wooley RE. Prediction of chicken embryo lethality with the avian Escherichia coli traits complement resistance, colicin V production, and presence of the increased serum survival gene cluster (iss). Avian Dis 2003; 47: 370-379.
87. Gibbs PS and Wooley RE. Comparison of the intravenous chicken challenge method with the embryo lethality assay for studies in avian colibacillosis. Avian Dis 2003; 47: 672-680.
88. Abe A, Heczko U, Regele RG and Finlay BB. Two enteropathogenic Escherichia coli type III secreted proteins, EspA and EspB, are virulence factors. J Exp Med 1998; 188: 1907-1916.
89. Johnson JR, Jelacic S, Schoening LM, Clabots C, Shaikh N, Mobley HL and Tarr PI. The IrgA homologue adhesin Iha is an Escherichia coli virulence factor in murine urinary tract infection. Infect Immun 2005; 73: 965-971.
90. Arne P, Mare D, Bree A, Schouler C and Dho-Moulin M. Increased tracheal colonization in chickens without impairing pathogenic properties of avian pathogenic Escherichia coli MT78 with a fimH deletion. Avian Dis 2000; 44: 343-355.
91. Hacker J, Hof H, Emödy L and Goebel W. Influence of cloned Escherichia coli hemolysin genes, S-fimbriae and serum resistance on pathogenicity in different animal models. Microb Pathog 1986; 1: 533-547.
92. Powell CJ, Jr and Finkelstein RA. Virulence of Escherichia coli strains for chick embryos. J Bact 1966; 91: 1410-1417.
93. Wooley RE, Gibbs PS, Dickerson HW, Brown J and Nolan LK. Analysis of plasmids cloned from a virulent avian Escherichia coli and transformed into E. coli DH5 alpha. Avian Dis 1996; 40: 533-539.
94. Brombacher E. Function and regulatory mechanisms of genes involved in microbial adhesion and biofilm formation [PhD Thesis, Diss ETH No 15755]; 2004.
95. Euo Y, Frey EA, Pfuetzner RA, Creagh AL, Knoechel DG, Haynes CA, Finlay BB and Strynadka NC. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature. 2000; 405: 1073-1077.
96. Wallace AJ, Stillman TJ, Atkins A, Jamieson SJ, Bullough PA, Green J and Artymiuk PJ. E. coli hemolysin E (HlyE, ClyA, SheA): X-ray crystal structure of the toxin and observation of membrane pores by electron microscopy. Cell 2000; 100: 265-276.