Characterization of urinary tract infection-associated Shiga toxin-producing Escherichia coli

Infection and Immunity

Volumn 82, Issue 11, 2014, Pages 4631-4642

  Toval, Francisco ^a   Schiller, Roswitha ^a,b   Meisen, Iris ^a   Putze, Johannes ^a   Kouzel, Ivan U ^a   Zhang, Wenlan ^a   Karch, Helge ^a   Bielaszewska, Martina ^a   Mormann, Michael ^a   Müthing, Johannes ^a   Dobrindt, Ulrich ^a,b  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GLOBOTETRAOSYLCERAMIDE; GLOBOTRIAOSYLCERAMIDE; GLYCOSPHINGOLIPID; SHIGA TOXIN; UNCLASSIFIED DRUG;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM ISOLATION; BLADDER EPITHELIUM; CONTROLLED STUDY; DISEASE ASSOCIATION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; FEMALE; FIMBRIA; GENE EXPRESSION; GENOTYPE; HEMOLYTIC UREMIC SYNDROME ASSOCIATED ESCHERICHIA COLI; HOSPITAL PATIENT; HUMAN; HUMAN CELL; IN VITRO STUDY; MASS SPECTROMETRY; MOLECULAR CLONING; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; THIN LAYER CHROMATOGRAPHY; URINALYSIS; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI; ADULT; ANIMAL; CASE REPORT; CELL LINE; CYSTITIS; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; YOUNG ADULT;

ADULT; AGED; ANIMALS; CELL LINE; CYSTITIS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMANS; MICE; URINARY TRACT INFECTIONS; YOUNG ADULT;

EID: 84907960444     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01701-14     Document Type: Article

References (70)

1. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2:123-140. http://dx.doi.org/10.1038/nrmicro818.
2. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. 2013. Recent advances in understanding enteric pathogenic Escherichia coli. Clin. Microbiol. Rev. 26:822-880. http://dx.doi.org/10.1128/CMR.00022-13.
3. Russo TA, Johnson JR. 2000. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J. Infect. Dis. 181:1753-1754. http://dx.doi.org/10.1086/315418.
4. Karch H, Tarr PI, Bielaszewska M. 2005. Enterohaemorrhagic Escherichia coli in human medicine. Int. J. Med. Microbiol. 295:405-418. http://dx.doi.org/10.1016/j.ijmm.2005.06.009.
5. Melton-Celsa A, Mohawk K, Teel L, O'Brien A. 2012. Pathogenesis of Shiga-toxin producing Escherichia coli. Curr. Top. Microbiol. Immunol. 357:67-103. http://dx.doi.org/10.1007/82_2011_176.
6. Johnson JR, Russo TA. 2002. Extraintestinal pathogenic Escherichia coli: "the other bad E. coli." J. Lab. Clin. Med. 139:155-162. http://dx.doi.org/10.1067/mlc.2002.121550.
7. Johnson JR, Russo TA. 2005. Molecular epidemiology of extraintestinal pathogenic (uropathogenic) Escherichia coli. Int. J. Med. Microbiol. 295:383-404. http://dx.doi.org/10.1016/j.ijmm.2005.07.005.
8. Köhler CD, Dobrindt U. 2011. What defines extraintestinal pathogenic Escherichia coli? Int. J. Med. Microbiol. 301:642-647. http://dx.doi.org/10.1016/j.ijmm.2011.09.006.
9. Beutin L, Karch H, Aleksic S, Spencker FB, Rosenbaum U. 1994. Occurrence of verotoxin (Shiga-like toxin) producing Escherichia coli in human urinary tract infection. Infection 22:425. http://dx.doi.org/10.1007/BF01715504.
10. Johnson JR, Jerome C, Boster DR, Stapleton AE, Tarr PI. 2002. Analysis of urinary Escherichia coli isolates for ability to produce Shiga toxin. J. Clin. Microbiol. 40:2247-2248. http://dx.doi.org/10.1128/JCM.40.6.2247-2248.2002.
11. Toval F, Köhler CD, Vogel U, Wagenlehner F, Mellmann A, Fruth A, Schmidt MA, Karch H, Bielaszewska M, Dobrindt U. 2014. Characterization of Escherichia coli isolates from hospital inpatients or outpatients with urinary tract infection. J. Clin. Microbiol. 52:407-418. http://dx.doi.org/10.1128/JCM.02069-13.
12. Betz J, Bielaszewska M, Thies A, Humpf HU, Dreisewerd K, Karch H, Kim KS, Friedrich AW, Müthing J. 2011. Shiga toxin glycosphingolipid receptors in microvascular and macrovascular endothelial cells: differential association with membrane lipid raft microdomains. J. Lipid Res. 52:618-634. http://dx.doi.org/10.1194/jlr.M010819.
13. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
14. Bielaszewska M, Mellmann A, Zhang W, Köck R, Fruth A, Bauwens A, Peters G, Karch H. 2011. Characterisation of the Escherichia coli strain associated with an outbreak of haemolytic uraemic syndrome in Germany, 2011: a microbiological study. Lancet Infect. Dis. 11:671-676. http://dx.doi.org/10.1016/S1473-3099(11)70165-7.
15. Johnson JR, Stell AL. 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis. 181:261-272. http://dx.doi.org/10.1086/315217.
16. Müller D, Greune L, Heusipp G, Karch H, Fruth A, Tschäpe H, Schmidt MA. 2007. Identification of unconventional intestinal pathogenic Escherichia coli isolates expressing intermediate virulence factor profiles by using a novel single-step multiplex PCR. Appl. Environ. Microbiol. 73:3380-3390. http://dx.doi.org/10.1128/AEM.02855-06.
17. Scheutz F, Teel LD, Beutin L, Piérard D, Buvens G, Karch H, Mellmann A, Caprioli A, Tozzoli R, Morabito S, Strockbine NA, Melton-Celsa AR, Sanchez M, Persson S, O'Brien AD. 2012. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J. Clin. Microbiol. 50:2951-2963. http://dx.doi.org/10.1128/JCM.00860-12.
18. Oswald E, Schmidt H, Morabito S, Karch H, Marches O, Caprioli A. 2000. Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect. Immun. 68:64-71. http://dx.doi.org/10.1128/IAI.68.1.64-71.2000.
19. Zhang WL, Köhler B, Oswald E, Beutin L, Karch H, Morabito S, Caprioli A, Suerbaum S, Schmidt H. 2002. Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J. Clin. Microbiol. 40:4486-4492. http://dx.doi.org/10.1128/JCM.40.12.4486-4492.2002.
20. Bielaszewska M, Stoewe F, Fruth A, Zhang W, Prager R, Brockmeyer J, Mellmann A, Karch H, Friedrich AW. 2009. Shiga toxin, cytolethal distending toxin, and hemolysin repertoires in clinical Escherichia coli O91 isolates. J. Clin. Microbiol. 47:2061-2066. http://dx.doi.org/10.1128/JCM.00201-09.
21. Brockmeyer J, Bielaszewska M, Fruth A, Bonn ML, Mellmann A, Humpf HU, Karch H. 2007. Subtypes of the plasmid-encoded serine protease EspP in Shiga toxin-producing Escherichia coli: distribution, secretion, and proteolytic activity. Appl. Environ. Microbiol. 73:6351-6359. http://dx.doi.org/10.1128/AEM.00920-07.
22. Polzin S, Huber C, Eylert E, Elsenhans I, Eisenreich W, Schmidt H. 2013. Growth media simulating ileal and colonic environments affect the intracellular proteome and carbon fluxes of enterohemorrhagic Escherichia coli O157:H7 strain EDL933. Appl. Environ. Microbiol. 79:3703-3715. http://dx.doi.org/10.1128/AEM.00062-13.
23. Brockmeyer J, Aldick T, Soltwisch J, Zhang W, Tarr PI, Weiss A, Dreisewerd K, Müthing J, Bielaszewska M, Karch H. 2011. Enterohaemorrhagic Escherichia coli haemolysin is cleaved and inactivated by serine protease EspPα. Environ. Microbiol. 13:1327-1341. http://dx.doi.org/10.1111/j.1462-2920.2011.02431.x.
24. Zhang W, Bielaszewska M, Bauwens A, Fruth A, Mellmann A, Karch H. 2012. Real-time multiplex PCR for detecting Shiga toxin 2-producing Escherichia coli O104:H4 in human stools. J. Clin. Microbiol. 50:1752-1754. http://dx.doi.org/10.1128/JCM.06817-11.
25. Appleyard RK. 1954. Segregation of new lysogenic types during growth of a doubly lysogenic strain derived from Escherichia coli K12. Genetics 39:440-452.
26. Chaudhuri RR, Sebaihia M, Hobman JL, Webber MA, Leyton DL, Goldberg MD, Cunningham AF, Scott-Tucker A, Ferguson PR, Thomas CM, Frankel G, Tang CM, Dudley EG, Roberts IS, Rasko DA, Pallen MJ, Parkhill J, Nataro JP, Thomson NR, Henderson IR. 2010. Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One 5:e8801. http://dx.doi.org/10.1371/journal.pone.0008801.
27. Schmidt H, Rüssmann H, Karch H. 1993. Virulence determinants in nontoxinogenic Escherichia coli O157 strains that cause infantile diarrhea. Infect. Immun. 61:4894-4898.
28. Storck W, Meisen I, Gianmoena K, Pläger I, Kouzel IU, Bielaszewska M, Haier J, Mormann M, Humpf HU, Karch H, Müthing J. 2012. Shiga toxin glycosphingolipid receptor expression and toxin susceptibility of human pancreatic ductal adenocarcinomas of differing origin and differentiation. Biol. Chem. 393:785-799. http://dx.doi.org/10.1515/hsz-2012-0165.
29. Kouzel IU, Pohlentz G, Storck W, Radamm L, Hoffmann P, Bie-laszewska M, Bauwens A, Cichon C, Schmidt MA, Mormann M, Karch H, Müthing J. 2013. Association of Shiga toxin glycosphingolipid receptors with membrane microdomains of toxin-sensitive lymphoid and myeloid cells. J. Lipid Res. 54:692-710. http://dx.doi.org/10.1194/jlr.M031781.
30. Müthing J, Maurer U, Šoštarić K, Neumann U, Brandt H, Duvar S, Peter-Katalinić J, Weber-Schürholz S. 1994. Different distributions of glycosphingolipids in mouse and rabbit skeletal muscle demonstrated by biochemical and immunohistological analyses. J. Biochem. 115:248-256.
31. Souady J, Soltwisch J, Dreisewerd K, Haier J, Peter-Katalinić J, Müthing J. 2009. Structural profiling of individual glycosphingolipids in a single thin-layer chromatogram by multiple sequential immunodetection matched with direct IR-MALDI-o-TOF mass spectrometry. Anal. Chem. 81:9481-9492. http://dx.doi.org/10.1021/ac901948h.
32. Chester MA. 1998. IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Nomenclature of glyolipids-recommendations 1997. Eur. J. Biochem. 257:293-298.
33. Meisen I, Rosenbrück R, Galla HJ, Hüwel S, Kouzel IU, Mormann M, Karch H, Müthing J. 2013. Expression of Shiga toxin 2e glycosphingolipid receptors of primary porcine brain endothelial cells and toxinmediated breakdown of the blood-brain barrier. Glycobiology 23:745-759. http://dx.doi.org/10.1093/glycob/cwt013.
34. Domon B, Costello CE. 1988. Structure elucidation of glycosphingolipids and gangliosides using high-performance tandem mass spectrometry. Biochemistry 27:1534-1543. http://dx.doi.org/10.1021/bi00405a021.
35. Brzuszkiewicz E, Brüggemann H, Liesegang H, Emmerth M, Ölschläger T, Nagy G, Albermann K, Wagner C, Buchrieser C, Emödy L, Gottschalk G, Hacker J, Dobrindt U. 2006. How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc. Natl. Acad. Sci. U. S. A. 103:12879-12884. http://dx.doi.org/10.1073/pnas.0603038103.
36. Hagberg L, Engberg I, Freter R, Lam J, Olling S, Svanborg Eden C. 1983. Ascending, unobstructed urinary tract infection in mice caused by pyelonephritogenic Escherichia coli of human origin. Infect. Immun. 40:273-283.
37. Bielaszewska M, Schiller R, Lammers L, Bauwens A, Fruth A, Middendorf B, Schmidt MA, Tarr PI, Dobrindt U, Karch H, Mellmann A. 2014. Heteropathogenic virulence and phylogeny reveal phased pathogenic metamorphosis in Escherichia coli O2:H6. EMBO Mol. Med. 6:347-357. http://dx.doi.org/10.1002/emmm.201303133.
38. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
39. Mellmann A, Bielaszewska M, Köck R, Friedrich AW, Fruth A, Middendorf B, Harmsen D, Schmidt MA, Karch H. 2008. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 14:1287-1290. http://dx.doi.org/10.3201/eid1408.071082.
40. Jenkins C, Perry NT, Cheasty T, Shaw DJ, Frankel G, Dougan G, Gunn GJ, Smith HR, Paton AW, Paton JC. 2003. Distribution of the saa gene in strains of Shiga toxin-producing Escherichia coli of human and bovine origins. J. Clin. Microbiol. 41:1775-1778. http://dx.doi.org/10.1128/JCM.41.4.1775-1778.2003.
41. Klemm P, Hancock V, Schembri MA. 2010. Fimbrial adhesins from extraintestinal Escherichia coli. Environ. Microbiol. Rep. 2:628-640. http://dx.doi.org/10.1111/j.1758-2229.2010.00166.x.
42. Oelschlaeger TA, Dobrindt U, Hacker J. 2002. Virulence factors of uropathogens. Curr. Opin. Urol. 12:33-38. http://dx.doi.org/10.1097/00042307-200201000-00007.
43. Connell I, Agace W, Klemm P, Schembri M, Marild S, Svanborg C. 1996. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl. Acad. Sci. U. S. A. 93:9827-9832. http://dx.doi.org/10.1073/pnas.93.18.9827.
44. Gunther NW, IV, Snyder JA, Lockatell V, Blomfield I, Johnson DE, Mobley HL. 2002. Assessment of virulence of uropathogenic Escherichia coli type 1 fimbrial mutants in which the invertible element is phaselocked on or off. Infect. Immun. 70:3344-3354. http://dx.doi.org/10.1128/IAI.70.7.3344-3354.2002.
45. Bielaszewska M, Middendorf B, Köck R, Friedrich AW, Fruth A, Karch H, Schmidt MA, Mellmann A. 2008. Shiga toxin-negative attaching and effacing Escherichia coli: distinct clinical associations with bacterial phylogeny and virulence traits and inferred in-host pathogen evolution. Clin. Infect. Dis. 47:208-217. http://dx.doi.org/10.1086/589245.
46. Liebchen A, Benz I, Mellmann A, Karch H, Gomes TA, Yamamoto D, Hernandes RT, Sampaio J, Sampaio SC, Fruth A, Schmidt MA. 2011. Characterization of Escherichia coli strains isolated from patients with diarrhea in Sao Paulo, Brazil: identification of intermediate virulence factor profiles by multiplex PCR. J. Clin. Microbiol. 49:2274-2278. http://dx.doi.org/10.1128/JCM.00386-11.
47. Bielaszewska M, Köck R, Friedrich AW, von Eiff C, Zimmerhackl LB, Karch H, Mellmann A. 2007. Shiga toxin-mediated hemolytic uremic syndrome: time to change the diagnostic paradigm? PLoS One 2:e1024. http://dx.doi.org/10.1371/journal.pone.0001024.
48. Lindberg AA, Brown JE, Stromberg N, Westling-Ryd M, Schultz JE, Karlsson KA. 1987. Identification of the carbohydrate receptor for Shiga toxin produced by Shigella dysenteriae type 1. J. Biol. Chem. 262:1779-1785.
49. Müsken A, Souady J, Dreisewerd K, Zhang W, Distler U, Peter-Katalinić J, Miller-Podraza H, Karch H, Müthing J. 2010. Application of thin-layer chromatography/infrared matrix-assisted laser desorption/ionization orthogonal time-of-flight mass spectrometry to structural analysis of bacteria-binding glycosphingolipids selected by affinity detection. Rapid Commun. Mass Spectrom. 24:1032-1038. http://dx.doi.org/10.1002/rcm.4480.
50. Chiurchiu C, Firrincieli A, Santostefano M, Fusaroli M, Remuzzi G, Ruggenenti P. 2003. Adult nondiarrhea hemolytic uremic syndrome associated with Shiga toxin Escherichia coli O157:H7 bacteremia and urinary tract infection. Am. J. Kidney Dis. 41:E4. http://dx.doi.org/10.1053/ajkd.2003.50022.
51. Gadea Mdel P, Deza N, Mota MI, Carbonari C, Robatto M, D'Astek B, Balseiro V, Bazet C, Rugnitz E, Livrelli V, Schelotto F, Rivas M, Varela G. 2012. Two cases of urinary tract infection caused by Shiga toxinproducing Escherichia coli O157:H7 strains. Rev. Argent. Microbiol. 44:94-96.
52. Hogan MC, Gloor JM, Uhl JR, Cockerill FR, Milliner DS. 2001. Two cases of non-O157:H7 Escherichia coli hemolytic uremic syndrome caused by urinary tract infection. Am. J. Kidney Dis. 38:E22.
53. Nguyen QV, Hochstrasser L, Chuard C, Hachler H, Regamey C, Descombes E. 2007. Adult hemolytic-uremic syndrome associated with urosepsis due to Shigatoxin-producing Escherichia coli O138:H. Ren. Fail. 29:747-750. http://dx.doi.org/10.1080/08860220701460418.
54. Starr M, Bennett-Wood V, Bigham AK, de Koning-Ward TF, Bordun AM, Lightfoot D, Bettelheim KA, Jones CL, Robins-Browne RM. 1998. Hemolytic-uremic syndrome following urinary tract infection with enterohemorrhagic Escherichia coli: case report and review. Clin. Infect. Dis. 27:310-315. http://dx.doi.org/10.1086/514656.
55. Tarr PI, Fouser LS, Stapleton AE, Wilson RA, Kim HH, Vary JC, Jr, Clausen CR. 1996. Hemolytic-uremic syndrome in a six-year-old girl after a urinary tract infection with Shiga-toxin-producing Escherichia coli O103:H2. N. Engl. J. Med. 335:635-638. http://dx.doi.org/10.1056/NEJM199608293350905.
56. Beutin L, Zimmermann S, Gleier K. 1998. Human infections with Shiga toxin-producing Escherichia coli other than serogroup O157 in Germany. Emerg. Infect. Dis. 4:635-639. http://dx.doi.org/10.3201/eid0404.980415.
57. Elliott EJ, Robins-Browne RM, O'Loughlin EV, Bennett-Wood V, Bourke J, Henning P, Hogg GG, Knight J, Powell H, Redmond D. 2001. Nationwide study of haemolytic uraemic syndrome: clinical, microbiological, and epidemiological features. Arch. Dis. Child. 85:125-131. http://dx.doi.org/10.1136/adc.85.2.125.
58. Sánchez S, Cenoz MG, Martin C, Beristain X, Llorente MT, Herrera-Leon S. 2014. Cluster investigation of mixed O76:H19 Shiga toxinproducing Escherichia coli and atypical enteropathogenic E. coli infection in a Spanish household. Epidemiol. Infect. 142:1029-1033. http://dx.doi.org/10.1017/S0950268813001842.
59. Gordon DM, Riley MA. 1992. A theoretical and experimental analysis of bacterial growth in the bladder. Mol. Microbiol. 6:555-562. http://dx.doi.org/10.1111/j.1365-2958.1992.tb01500.x.
60. Alteri CJ, Mobley HL. 2007. Quantitative profile of the uropathogenic Escherichia coli outer membrane proteome during growth in human urine. Infect. Immun. 75:2679-2688. http://dx.doi.org/10.1128/IAI.00076-06.
61. Roos V, Nielsen EM, Klemm P. 2006. Asymptomatic bacteriuria Escherichia coli strains: adhesins, growth and competition. FEMS Microbiol. Lett. 262:22-30. http://dx.doi.org/10.1111/j.1574-6968.2006.00355.x.
62. Friedrich AW, Borell J, Bielaszewska M, Fruth A, Tschäpe H, Karch H. 2003. Shiga toxin 1c-producing Escherichia coli strains: phenotypic and genetic characterization and association with human disease. J. Clin. Microbiol. 41:2448-2453. http://dx.doi.org/10.1128/JCM.41.6.2448-2453.2003.
63. Paton AW, Srimanote P, Woodrow MC, Paton JC. 2001. Characterization of Saa, a novel autoagglutinating adhesin produced by locus of enterocyte effacement-negative Shiga-toxigenic Escherichia coli strains that are virulent for humans. Infect. Immun. 69:6999-7009. http://dx.doi.org/10.1128/IAI.69.11.6999-7009.2001.
64. Dodson KW, Pinkner JS, Rose T, Magnusson G, Hultgren SJ, Waksman G. 2001. Structural basis of the interaction of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell 105:733-743. http://dx.doi.org/10.1016/S0092-8674(01)00388-9.
65. Stapleton AE, Stroud MR, Hakomori SI, Stamm WE. 1998. The globoseries glycosphingolipid sialosyl galactosyl globoside is found in urinary tract tissues and is a preferred binding receptor in vitro for uropathogenic Escherichia coli expressing pap-encoded adhesins. Infect. Immun. 66:3856-3861.
66. Striker R, Nilsson U, Stonecipher A, Magnusson G, Hultgren SJ. 1995. Structural requirements for the glycolipid receptor of human uropathogenic Escherichia coli. Mol. Microbiol. 16:1021-1029. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02327.x.
67. Lanne B, Olsson BM, Jovall PA, Angström J, Linder H, Marklund BI, Bergström J, Karlsson KA. 1995. Glycoconjugate receptors for P-fimbriated Escherichia coli in the mouse. An animal model of urinary tract infection. J. Biol. Chem. 270:9017-9025.
68. Olsson BM, Karlsson H, Larsson T, Lanne B. 1999. Mass spectrometric analysis of ceramide composition in mono-, di-, tri-, and tetraglycosylceramides from mouse kidney: an experimental model for uropathogenic Escherichia coli. J. Mass Spectrom. 34:942-951. http://dx.doi.org/10.1002/(SICI)1096-9888(199909)34:9<942::AID-JMS855>3.0.CO;2-1.
69. Hung CS, Bouckaert J, Hung D, Pinkner J, Widberg C, DeFusco A, Auguste CG, Strouse R, Langermann S, Waksman G, Hultgren SJ. 2002. Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol. Microbiol. 44:903-915.
70. Moreno E, Andreu A, Pigrau C, Kuskowski MA, Johnson JR, Prats G. 2008. Relationship between Escherichia coli strains causing acute cystitis in women and the fecal E. coli population of the host. J. Clin. Microbiol. 46:2529-2534. http://dx.doi.org/10.1128/JCM.00813-08.