Skip to main content
Canadian Journal of Veterinary Research logoLink to Canadian Journal of Veterinary Research
. 1997 Jul;61(3):193–199.

Presence of pap-, sfa-, and afa-related sequences in necrotoxigenic Escherichia coli isolates from cattle: evidence for new variants of the AFA family.

J G Mainil 1, E Jacquemin 1, F Hérault 1, E Oswald 1
PMCID: PMC1189403  PMID: 9242999

Abstract

Necrotoxigenic Escherichia coli (NTEC) are associated with intestinal and extraintestinal diseases in animals and human beings and produce Cytotoxic Necrotizing Factor 1 (CNF1) or 2 (CNF2). Fourty-three NTEC1, 42 NTEC2, and 32 CNF-negative isolates from cattle were tested by colony DNA hybridization, by plasmid DNA hybridization and by PCR assays for the presence of DNA sequences homologous to the operons coding for fimbrial (PAP/PRS, SFA/FIC, and F17) and afimbrial (AFA/Dr) adhesins of extraintestinal E. coli. Most NTEC1 isolates hybridized with the PAP probes and either the SFA probe (37%) or the AFA probes (49%). Most NTEC2 isolates, in contrast, hybridized with the F17 probe (45%), the AFA probes (19%), or the F17 and AFA probes (22%). A probe-positive plasmid was identified in each of the 19 NTEC2 isolates studied. They all hybridized with the CNF2 toxin probe (Vir plasmids) and most of them with the F17 (6 plasmids) or AFA (7 plasmids) probes. PCR amplification was obtained with 6 of the 11 NTEC isolates tested for the papGII/prsG genes; with all 5 NTEC isolates tested for the sfa and related operons; but with none of the 18 NTEC isolates tested for the afa and related operons. pap-, sfa-, and afa-related sequences are thus present in NTEC isolates from cattle in addition to f17-related operons and may code for adhesins corresponding to specific colonization factors. f17- and afa-related sequences can be located on the Vir plasmids along with the cnf2 gene. Existence of new variants of the AFA/Dr family is evident from the negative results of this family-specific PCR assay.

Full text

PDF
194

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ansuini A., Candotti P., Vecchi G., Falbo V., Minelli F., Caprioli A. Necrotoxigenic E coli in rabbits and horses. Vet Rec. 1994 Jun 4;134(23):608–608. doi: 10.1136/vr.134.23.608-a. [DOI] [PubMed] [Google Scholar]
  2. Archambaud M., Courcoux P., Labigne-Roussel A. Detection by molecular hybridization of pap, afa, and sfa adherence systems in Escherichia coli strains associated with urinary and enteral infections. Ann Inst Pasteur Microbiol. 1988 Sep-Oct;139(5):575–588. doi: 10.1016/0769-2609(88)90156-1. [DOI] [PubMed] [Google Scholar]
  3. Bertin Y., Girardeau J. P., Darfeuille-Michaud A., Contrepois M. Characterization of 20K fimbria, a new adhesin of septicemic and diarrhea-associated Escherichia coli strains, that belongs to a family of adhesins with N-acetyl-D-glucosamine recognition. Infect Immun. 1996 Jan;64(1):332–342. doi: 10.1128/iai.64.1.332-342.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bilge S. S., Clausen C. R., Lau W., Moseley S. L. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J Bacteriol. 1989 Aug;171(8):4281–4289. doi: 10.1128/jb.171.8.4281-4289.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blanco J., Alonso M. P., González E. A., Blanco M., Garabal J. I. Virulence factors of bacteraemic Escherichia coli with particular reference to production of cytotoxic necrotising factor (CNF) by P-fimbriate strains. J Med Microbiol. 1990 Mar;31(3):175–183. doi: 10.1099/00222615-31-3-175. [DOI] [PubMed] [Google Scholar]
  6. Blanco J., González E. A., García S., Blanco M., Regueiro B., Bernárdez I. Production of toxins by Escherichia coli strains isolated from calves with diarrhoea in galicia (north-western Spain). Vet Microbiol. 1988 Dec;18(3-4):297–311. doi: 10.1016/0378-1135(88)90095-8. [DOI] [PubMed] [Google Scholar]
  7. Blanco M., Blanco J., Blanco J. E., Ramos J. Enterotoxigenic, verotoxigenic, and necrotoxigenic Escherichia coli isolated from cattle in Spain. Am J Vet Res. 1993 Sep;54(9):1446–1451. [PubMed] [Google Scholar]
  8. Blum G., Falbo V., Caprioli A., Hacker J. Gene clusters encoding the cytotoxic necrotizing factor type 1, Prs-fimbriae and alpha-hemolysin form the pathogenicity island II of the uropathogenic Escherichia coli strain J96. FEMS Microbiol Lett. 1995 Feb 15;126(2):189–195. doi: 10.1111/j.1574-6968.1995.tb07415.x. [DOI] [PubMed] [Google Scholar]
  9. Broes A., Fairbrother J. M., Mainil J., Harel J., Lariviere S. Phenotypic and genotypic characterization of enterotoxigenic Escherichia coli serotype O8:KX105 and O8:K"2829" strains isolated from piglets with diarrhea. J Clin Microbiol. 1988 Nov;26(11):2402–2409. doi: 10.1128/jcm.26.11.2402-2409.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Caprioli A., Falbo V., Roda L. G., Ruggeri F. M., Zona C. Partial purification and characterization of an escherichia coli toxic factor that induces morphological cell alterations. Infect Immun. 1983 Mar;39(3):1300–1306. doi: 10.1128/iai.39.3.1300-1306.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cherifi A., Contrepois M., Picard B., Goullet P., de Rycke J., Fairbrother J., Barnouin J. Factors and markers of virulence in Escherichia coli from human septicemia. FEMS Microbiol Lett. 1990 Aug;58(3):279–283. doi: 10.1111/j.1574-6968.1990.tb13989.x. [DOI] [PubMed] [Google Scholar]
  12. De Rycke J., González E. A., Blanco J., Oswald E., Blanco M., Boivin R. Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates of Escherichia coli. J Clin Microbiol. 1990 Apr;28(4):694–699. doi: 10.1128/jcm.28.4.694-699.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. De Rycke J., Guillot J. F., Boivin R. Cytotoxins in non-enterotoxigenic strains of Escherichia coli isolated from feces of diarrheic calves. Vet Microbiol. 1987 Oct;15(1-2):137–150. doi: 10.1016/0378-1135(87)90139-8. [DOI] [PubMed] [Google Scholar]
  14. De Rycke J., Plassiart G. Toxic effects for lambs of cytotoxic necrotising factor from Escherichia coli. Res Vet Sci. 1990 Nov;49(3):349–354. [PubMed] [Google Scholar]
  15. Denich K., Blyn L. B., Craiu A., Braaten B. A., Hardy J., Low D. A., O'Hanley P. D. DNA sequences of three papA genes from uropathogenic Escherichia coli strains: evidence of structural and serological conservation. Infect Immun. 1991 Nov;59(11):3849–3858. doi: 10.1128/iai.59.11.3849-3858.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Falbo V., Famiglietti M., Caprioli A. Gene block encoding production of cytotoxic necrotizing factor 1 and hemolysin in Escherichia coli isolates from extraintestinal infections. Infect Immun. 1992 Jun;60(6):2182–2187. doi: 10.1128/iai.60.6.2182-2187.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Harel J., Daigle F., Maiti S., Désautels C., Labigne A., Fairbrother J. M. Occurrence of pap-, sfa-, and afa-related sequences among F165-positive Escherichia coli from diseased animals. FEMS Microbiol Lett. 1991 Aug 1;66(2):177–182. doi: 10.1016/0378-1097(91)90329-9. [DOI] [PubMed] [Google Scholar]
  18. Harel J., Forget C., Saint-Amand J., Daigle F., Dubreuil D., Jacques M., Fairbrother J. Molecular cloning of a determinant coding for fimbrial antigen F165(1), a Prs-like fimbrial antigen from porcine septicaemic Escherichia coli. J Gen Microbiol. 1992 Jul;138(7):1495–1502. doi: 10.1099/00221287-138-7-1495. [DOI] [PubMed] [Google Scholar]
  19. Harel J., Jacques M., Fairbrother J. M., Bossé M., Forget C. Cloning of determinants encoding F165(2) fimbriae from porcine septicaemic Escherichia coli confirms their identity as F1C fimbriae. Microbiology. 1995 Jan;141(Pt 1):221–228. doi: 10.1099/00221287-141-1-221. [DOI] [PubMed] [Google Scholar]
  20. Johnson J. R. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev. 1991 Jan;4(1):80–128. doi: 10.1128/cmr.4.1.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kado C. I., Liu S. T. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol. 1981 Mar;145(3):1365–1373. doi: 10.1128/jb.145.3.1365-1373.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Labigne-Roussel A. F., Lark D., Schoolnik G., Falkow S. Cloning and expression of an afimbrial adhesin (AFA-I) responsible for P blood group-independent, mannose-resistant hemagglutination from a pyelonephritic Escherichia coli strain. Infect Immun. 1984 Oct;46(1):251–259. doi: 10.1128/iai.46.1.251-259.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Labigne-Roussel A., Falkow S. Distribution and degree of heterogeneity of the afimbrial-adhesin-encoding operon (afa) among uropathogenic Escherichia coli isolates. Infect Immun. 1988 Mar;56(3):640–648. doi: 10.1128/iai.56.3.640-648.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Le Bouguenec C., Archambaud M., Labigne A. Rapid and specific detection of the pap, afa, and sfa adhesin-encoding operons in uropathogenic Escherichia coli strains by polymerase chain reaction. J Clin Microbiol. 1992 May;30(5):1189–1193. doi: 10.1128/jcm.30.5.1189-1193.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Le Bouguenec C., Garcia M. I., Ouin V., Desperrier J. M., Gounon P., Labigne A. Characterization of plasmid-borne afa-3 gene clusters encoding afimbrial adhesins expressed by Escherichia coli strains associated with intestinal or urinary tract infections. Infect Immun. 1993 Dec;61(12):5106–5114. doi: 10.1128/iai.61.12.5106-5114.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lintermans P., Pohl P., Deboeck F., Bertels A., Schlicker C., Vandekerckhove J., Van Damme J., Van Montagu M., De Greve H. Isolation and nucleotide sequence of the F17-A gene encoding the structural protein of the F17 fimbriae in bovine enterotoxigenic Escherichia coli. Infect Immun. 1988 Jun;56(6):1475–1484. doi: 10.1128/iai.56.6.1475-1484.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Low D. A., Braaten B. A., Ling G. V., Johnson D. L., Ruby A. L. Isolation and comparison of Escherichia coli strains from canine and human patients with urinary tract infections. Infect Immun. 1988 Oct;56(10):2601–2609. doi: 10.1128/iai.56.10.2601-2609.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mainil J. G., Bex F., Dreze P., Kaeckenbeeck A., Couturier M. Replicon typing of virulence plasmids of enterotoxigenic Escherichia coli isolates from cattle. Infect Immun. 1992 Aug;60(8):3376–3380. doi: 10.1128/iai.60.8.3376-3380.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mainil J. G., Jacquemin E. R., Kaeckenbeeck A. E., Pohl P. H. Association between the effacing (eae) gene and the Shiga-like toxin-encoding genes in Escherichia coli isolates from cattle. Am J Vet Res. 1993 Jul;54(7):1064–1068. [PubMed] [Google Scholar]
  30. Maiti S. N., Harel J., Fairbrother J. M. Structure and copy number analyses of pap-, sfa-, and afa-related gene clusters in F165-positive bovine and porcine Escherichia coli isolates. Infect Immun. 1993 Jun;61(6):2453–2461. doi: 10.1128/iai.61.6.2453-2461.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Marklund B. I., Tennent J. M., Garcia E., Hamers A., Båga M., Lindberg F., Gaastra W., Normark S. Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol. 1992 Aug;6(16):2225–2242. doi: 10.1111/j.1365-2958.1992.tb01399.x. [DOI] [PubMed] [Google Scholar]
  32. Morschhäuser J., Vetter V., Emödy L., Hacker J. Adhesin regulatory genes within large, unstable DNA regions of pathogenic Escherichia coli: cross-talk between different adhesin gene clusters. Mol Microbiol. 1994 Feb;11(3):555–566. doi: 10.1111/j.1365-2958.1994.tb00336.x. [DOI] [PubMed] [Google Scholar]
  33. Nowicki B., Labigne A., Moseley S., Hull R., Hull S., Moulds J. The Dr hemagglutinin, afimbrial adhesins AFA-I and AFA-III, and F1845 fimbriae of uropathogenic and diarrhea-associated Escherichia coli belong to a family of hemagglutinins with Dr receptor recognition. Infect Immun. 1990 Jan;58(1):279–281. doi: 10.1128/iai.58.1.279-281.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Oswald E., De Rycke J., Guillot J. F., Boivin R. Cytotoxic effect of multinucleation in HeLa cell cultures associated with the presence of Vir plasmid in Escherichia coli strains. FEMS Microbiol Lett. 1989 Mar;49(1):95–99. doi: 10.1016/0378-1097(89)90349-2. [DOI] [PubMed] [Google Scholar]
  35. Oswald E., Pohl P., Jacquemin E., Lintermans P., Van Muylem K., O'Brien A. D., Mainil J. Specific DNA probes to detect Escherichia coli strains producing cytotoxic necrotising factor type 1 or type 2. J Med Microbiol. 1994 Jun;40(6):428–434. doi: 10.1099/00222615-40-6-428. [DOI] [PubMed] [Google Scholar]
  36. Oswald E., de Rycke J., Lintermans P., van Muylem K., Mainil J., Daube G., Pohl P. Virulence factors associated with cytotoxic necrotizing factor type two in bovine diarrheic and septicemic strains of Escherichia coli. J Clin Microbiol. 1991 Nov;29(11):2522–2527. doi: 10.1128/jcm.29.11.2522-2527.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ott M., Hoschützky H., Jann K., Van Die I., Hacker J. Gene clusters for S fimbrial adhesin (sfa) and F1C fimbriae (foc) of Escherichia coli: comparative aspects of structure and function. J Bacteriol. 1988 Sep;170(9):3983–3990. doi: 10.1128/jb.170.9.3983-3990.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Pawelzik M., Heesemann J., Hacker J., Opferkuch W. Cloning and characterization of a new type of fimbria (S/F1C-related fimbria) expressed by an Escherichia coli O75:K1:H7 blood culture isolate. Infect Immun. 1988 Nov;56(11):2918–2924. doi: 10.1128/iai.56.11.2918-2924.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Pohl P., Oswald E., Van Muylem K., Jacquemin E., Lintermans P., Mainil J. Escherichia coli producing CNF1 and CNF2 cytotoxins in animals with different disorders. Vet Res. 1993;24(4):311–315. [PubMed] [Google Scholar]
  40. Schmoll T., Morschhäuser J., Ott M., Ludwig B., van Die I., Hacker J. Complete genetic organization and functional aspects of the Escherichia coli S fimbrial adhesion determinant: nucleotide sequence of the genes sfa B, C, D, E, F. Microb Pathog. 1990 Nov;9(5):331–343. doi: 10.1016/0882-4010(90)90067-z. [DOI] [PubMed] [Google Scholar]
  41. Senior D. F., deMan P., Svanborg C. Serotype, hemolysin production, and adherence characteristics of strains of Escherichia coli causing urinary tract infection in dogs. Am J Vet Res. 1992 Apr;53(4):494–498. [PubMed] [Google Scholar]
  42. Smith H. W. Transmissible pathogenic characteristics of invasive strains of Escherichia coli. J Am Vet Med Assoc. 1978 Sep 1;173(5 Pt 2):601–607. [PubMed] [Google Scholar]
  43. Wray C., Piercy D. W., Carroll P. J., Cooley W. A. Experimental infection of neonatal pigs with CNF toxin-producing strains of Escherichia coli. Res Vet Sci. 1993 May;54(3):290–298. doi: 10.1016/0034-5288(93)90125-y. [DOI] [PubMed] [Google Scholar]
  44. el Mazouari K., Oswald E., Hernalsteens J. P., Lintermans P., De Greve H. F17-like fimbriae from an invasive Escherichia coli strain producing cytotoxic necrotizing factor type 2 toxin. Infect Immun. 1994 Jun;62(6):2633–2638. doi: 10.1128/iai.62.6.2633-2638.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Canadian Journal of Veterinary Research are provided here courtesy of Canadian Veterinary Medical Association

RESOURCES