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Infect Immun. May 1995; 63(5): 1663–1668.
PMCID: PMC173207

dra-related X adhesins of gestational pyelonephritis-associated Escherichia coli recognize SCR-3 and SCR-4 domains of recombinant decay-accelerating factor.


Bacterial adhesins are important virulence factors that allow colonization of the human urogenital tract by Escherichia coli. Adhesins of the Dr family have been found to be more frequently expressed in strains associated with symptomatic urinary tract infections. Because of the high frequency of symptomatic urinary tract infections during pregnancy, we screened E. coli isolates from 64 gestational pyelonephritis patients for the expression of Dr and X adhesins to address their potential virulence roles in this population. Using PCR and primers for the afaB gene, we detected dra-related operons in 17 isolates (27%). On the basis of the lack of hemagglutination of Dr(a-) erythrocytes containing a point mutation in the decay-accelerating factor (DAF) short consensus repeat-3 (SCR-3) domain, 12 of these strains were categorized as classical Dr adhesins. The hemagglutination of O erythrocytes by Dr+ strains was blocked or reduced by a monoclonal antibody to the DAF SCR-3 domain. The remaining five dra-positive strains agglutinated Dr(a-) erythrocytes. Monoclonal antibody to the DAF SCR-3 domain failed to block O-erythrocyte hemagglutination. Adhesins in these strains did not fulfill criteria for Dr hemagglutinins because of the undefined receptor specificities and were categorized as X. E. coli strains bearing dra-related X adhesins bound to DAF cDNA-transfected Chinese hamster ovary cells. Three of these dra-related X-adhesin-bearing E. coli strains failed to attach to the SCR-3 delta deletion transfectant, which suggested that binding sites were located in the SCR-3 domain but outside the region blocked by the monoclonal anti-SCR-3 immunoglobulin G. The binding sites of the remaining two dra-related X adhesin strains were localized to the SCR-4 domain, as the attachment was shown to be abolished on an SCR-4 delta mutant but unaffected by an SCR-3 delta deletion. The heterogeneity in the binding sites of E. coli DAF (Dr) family adhesins from gestational pyelonephritis isolates may reflect the ability of the adhesins to evolve to recognize alternate peptide epitopes for efficient colonization.

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Selected References

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  • Agace WW, Hedges SR, Ceska M, Svanborg C. Interleukin-8 and the neutrophil response to mucosal gram-negative infection. J Clin Invest. 1993 Aug;92(2):780–785. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Archambaud M, Courcoux P, Ouin V, Chabanon G, Labigne-Roussel A. Phenotypic and genotypic assays for the detection and identification of adhesins from pyelonephritic Escherichia coli. Ann Inst Pasteur Microbiol. 1988 Sep-Oct;139(5):557–573. [PubMed]
  • Arthur M, Johnson CE, Rubin RH, Arbeit RD, Campanelli C, Kim C, Steinbach S, Agarwal M, Wilkinson R, Goldstein R. Molecular epidemiology of adhesin and hemolysin virulence factors among uropathogenic Escherichia coli. Infect Immun. 1989 Feb;57(2):303–313. [PMC free article] [PubMed]
  • Coyne KE, Hall SE, Thompson S, Arce MA, Kinoshita T, Fujita T, Anstee DJ, Rosse W, Lublin DM. Mapping of epitopes, glycosylation sites, and complement regulatory domains in human decay accelerating factor. J Immunol. 1992 Nov 1;149(9):2906–2913. [PubMed]
  • Girón JA, Jones T, Millán-Velasco F, Castro-Muñoz E, Zárate L, Fry J, Frankel G, Moseley SL, Baudry B, Kaper JB, et al. Diffuse-adhering Escherichia coli (DAEC) as a putative cause of diarrhea in Mayan children in Mexico. J Infect Dis. 1991 Mar;163(3):507–513. [PubMed]
  • Green CP, Thomas VL. Hemagglutination of human type O erythrocytes, hemolysin production, and serogrouping of Escherichia coli isolates from patients with acute pyelonephritis, cystitis, and asymptomatic bacteriuria. Infect Immun. 1981 Jan;31(1):309–315. [PMC free article] [PubMed]
  • Hagberg L, Engberg I, Freter R, Lam J, Olling S, Svanborg Edén C. Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect Immun. 1983 Apr;40(1):273–283. [PMC free article] [PubMed]
  • Johnson JR. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev. 1991 Jan;4(1):80–128. [PMC free article] [PubMed]
  • Johnson JR, Stamm WE. Urinary tract infections in women: diagnosis and treatment. Ann Intern Med. 1989 Dec 1;111(11):906–917. [PubMed]
  • Källenius G, Möllby R, Svenson SB, Helin I, Hultberg H, Cedergren B, Winberg J. Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet. 1981 Dec 19;2(8260-61):1369–1372. [PubMed]
  • Kaul A, Nowicki BJ, Martens MG, Goluszko P, Hart A, Nagamani M, Kumar D, Pham TQ, Nowicki S. Decay-accelerating factor is expressed in the human endometrium and may serve as the attachment ligand for Dr pili of Escherichia coli. Am J Reprod Immunol. 1994 Oct;32(3):194–199. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Labigne-Roussel A, Schmidt MA, Walz W, Falkow S. Genetic organization of the afimbrial adhesin operon and nucleotide sequence from a uropathogenic Escherichia coli gene encoding an afimbrial adhesin. J Bacteriol. 1985 Jun;162(3):1285–1292. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Le Bouguenec C, Garcia MI, Ouin V, Desperrier JM, 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. [PMC free article] [PubMed]
  • Lipsky BA. Urinary tract infections in men. Epidemiology, pathophysiology, diagnosis, and treatment. Ann Intern Med. 1989 Jan 15;110(2):138–150. [PubMed]
  • Lublin DM, Atkinson JP. Decay-accelerating factor and membrane cofactor protein. Curr Top Microbiol Immunol. 1990;153:123–145. [PubMed]
  • Lublin DM, Coyne KE. Phospholipid-anchored and transmembrane versions of either decay-accelerating factor or membrane cofactor protein show equal efficiency in protection from complement-mediated cell damage. J Exp Med. 1991 Jul 1;174(1):35–44. [PMC free article] [PubMed]
  • Lublin DM, Thompson ES, Green AM, Levene C, Telen MJ. Dr(a-) polymorphism of decay accelerating factor. Biochemical, functional, and molecular characterization and production of allele-specific transfectants. J Clin Invest. 1991 Jun;87(6):1945–1952. [PMC free article] [PubMed]
  • Martens MG. Pyelonephritis. Obstet Gynecol Clin North Am. 1989 Jun;16(2):305–315. [PubMed]
  • Naeye RL. Causes of the excessive rates of perinatal mortality and prematurity in pregnancies complicated by maternal urinary-tract infections. N Engl J Med. 1979 Apr 12;300(15):819–823. [PubMed]
  • Nowicki B, Hart A, Coyne KE, Lublin DM, Nowicki S. Short consensus repeat-3 domain of recombinant decay-accelerating factor is recognized by Escherichia coli recombinant Dr adhesin in a model of a cell-cell interaction. J Exp Med. 1993 Dec 1;178(6):2115–2121. [PMC free article] [PubMed]
  • Nowicki B, Hull R, Moulds J. Use of the Dr hemagglutinin of uropathogenic Escherichia coli to differentiate normal from abnormal red cells in paroxysmal nocturnal hemoglobinuria. N Engl J Med. 1988 Nov 10;319(19):1289–1290. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Nowicki B, Martens M, Hart A, Nowicki S. Gestational age-dependent distribution of Escherichia coli fimbriae in pregnant patients with pyelonephritis. Ann N Y Acad Sci. 1994 Aug 15;730:290–291. [PubMed]
  • Nowicki B, Moulds J, Hull R, Hull S. A hemagglutinin of uropathogenic Escherichia coli recognizes the Dr blood group antigen. Infect Immun. 1988 May;56(5):1057–1060. [PMC free article] [PubMed]
  • Nowicki B, Svanborg-Edén C, Hull R, Hull S. Molecular analysis and epidemiology of the Dr hemagglutinin of uropathogenic Escherichia coli. Infect Immun. 1989 Feb;57(2):446–451. [PMC free article] [PubMed]
  • Nowicki B, Truong L, Moulds J, Hull R. Presence of the Dr receptor in normal human tissues and its possible role in the pathogenesis of ascending urinary tract infection. Am J Pathol. 1988 Oct;133(1):1–4. [PMC free article] [PubMed]
  • Pere A, Nowicki B, Saxén H, Siitonen A, Korhonen TK. Expression of P, type-1, and type-1C fimbriae of Escherichia coli in the urine of patients with acute urinary tract infection. J Infect Dis. 1987 Oct;156(4):567–574. [PubMed]
  • Stenqvist K, Sandberg T, Lidin-Janson G, Orskov F, Orskov I, Svanborg-Edén C. Virulence factors of Escherichia coli in urinary isolates from pregnant women. J Infect Dis. 1987 Dec;156(6):870–877. [PubMed]
  • Edén CS, Hanson LA, Jodal U, Lindberg U, Akerlund AS. Variable adherence to normal human urinary-tract epithelial cells of Escherichia coli strains associated with various forms of urinary-tract infection. Lancet. 1976 Sep 4;1(7984):490–492. [PubMed]
  • Swanson TN, Bilge SS, Nowicki B, Moseley SL. Molecular structure of the Dr adhesin: nucleotide sequence and mapping of receptor-binding domain by use of fusion constructs. Infect Immun. 1991 Jan;59(1):261–268. [PMC free article] [PubMed]
  • Väisänen-Rhen V, Elo J, Väisänen E, Siitonen A, Orskov I, Orskov F, Svenson SB, Mäkelä PH, Korhonen TK. P-fimbriated clones among uropathogenic Escherichia coli strains. Infect Immun. 1984 Jan;43(1):149–155. [PMC free article] [PubMed]
  • Väisänen V, Elo J, Tallgren LG, Siitonen A, Mäkelä PH, Svanborg-Edén C, Källenius G, Svenson SB, Hultberg H, Korhonen T. Mannose-resistant haemagglutination and P antigen recognition are characteristic of Escherichia coli causing primary pyelonephritis. Lancet. 1981 Dec 19;2(8260-61):1366–1369. [PubMed]

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