Virulence of the shiga toxin type 2-expressing escherichia coli O104: H4 german outbreak isolate in two animal models

Infection and Immunity

Volumn 81, Issue 5, 2013, Pages 1562-1574

  Zangari, Tonia ^a   Melton Celsa, Angela R ^a   Panda, Aruna ^b   Boisen, Nadia ^c   Smith, Mark A ^a   Tatarov, Ivan ^b   De Tolla, Louis J ^b   Nataro, James P ^c   O'Brien, Alison D ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; TOXIN ANTIBODY; VEROTOXIN 2; VIRULENCE FACTOR;

ACUTE KIDNEY TUBULE NECROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; CYTOTOXICITY; DIARRHEA; ENTEROAGGREGATIVE ESCHERICHIA COLI; EPIDEMIC; ESCHERICHIA COLI INFECTION; EXPERIMENTAL RABBIT; KIDNEY FUNCTION; KIDNEY INJURY; LETHARGY; LOOSE FECES; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SHIGA TOXIN PRODUCING ESCHERICHIA COLI; VERO CELL; WEIGHT GAIN; WEIGHT REDUCTION;

AMPICILLIN; ANALYSIS OF VARIANCE; ANIMALS; ANTI-BACTERIAL AGENTS; DISEASE MODELS, ANIMAL; DISEASE OUTBREAKS; ESCHERICHIA COLI INFECTIONS; FEMALE; GERMANY; MICE; MICE, INBRED C57BL; RABBITS; SHIGA TOXIN 2; SHIGA-TOXIGENIC ESCHERICHIA COLI; VIRULENCE;

EID: 84877819058     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01310-12     Document Type: Article

References (78)

1. Gault G, Weill FX, Mariani-Kurkdjian P, Jourdan-da Silva N, King L, Aldabe B, Charron M, Ong N, Castor C, Mace M, Bingen E, Noel H, Vaillant V, Bone A, Vendrely B, Delmas Y, Combe C, Bercion R, d'Andigne E, Desjardin M, de Valk H, Rolland P. 2011. Outbreak of haemolytic uraemic syndrome and bloody diarrhoea due to Escherichia coli O104:H4, south-west France, June 2011. Euro Surveill. 16(26): pii-19905. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId 19905.
2. Mariani-Kurkdjian P, Bingen E, Gault G, Jourdan-Da Silva N, Weill FX. 2011. Escherichia coli O104:H4 south-west France, June 2011. Lancet Infect. Dis. 11:732-733.
3. King LA, Nogareda F, Weill FX, Mariani-Kurkdjian P, Loukiadis E, Gault G, Jourdan-DaSilva N, Bingen E, Mace M, Thevenot D, Ong N, Castor C, Noel H, Van Cauteren D, Charron M, Vaillant V, Aldabe B, Goulet V, Delmas G, Couturier E, Le Strat Y, Combe C, Delmas Y, Terrier F, Vendrely B, Rolland P, de Valk H. 2012. Outbreak of Shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin. Infect. Dis. 54:1588-1594.
4. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Muller L, King LA, Rosner B, Buchholz U, Stark K, Krause G, HUS Investigation Team. 2011. Epidemic profile of Shigatoxin- producing Escherichia coli O104:H4 outbreak in Germany. N. Engl. J. Med. 365:1771-1780.
5. Robert Koch Institute. September 2011. Final presentation and evaluation of epidemiological findings in the EHEC O104:H4 outbreak, Germany 2011. Robert Koch Institute, Berlin, Germany.
6. World Health Organization. 2011. Outbreaks of E. coli O104:H4 infection: update 30. World Health Organization, Geneva, Switzerland.
7. Frank C, Faber MS, Askar M, Bernard H, Fruth A, Gilsdorf A, Hohle M, Karch H, Krause G, Prager R, Spode A, Stark K, Werber D, HUS Investigation Team. 2011. Large and ongoing outbreak of haemolytic uraemic syndrome, Germany, May 2011. Euro Surveill. 16(21): pii=19878. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId =19878.
8. European Food Safety Authority. 2011. Tracing seeds, in particular fenugreek (Trigonella foenum-graecum) seeds, in relation to the Shiga toxinproducing E. coli (STEC) O104:H4 2011 outbreaks in Germany and France. European Food Safety Authority, Parma, Italy.
9. Buchholz U, Bernard H, Werber D, Bohmer MM, Remschmidt C, Wilking H, Delere Y, an der Heiden M, Adlhoch C, Dreesman J, Ehlers J, Ethelberg S, Faber M, Frank C, Fricke G, Greiner M, Hohle M, Ivarsson S, Jark U, Kirchner M, Koch J, Krause G, Luber P, Rosner B, Stark K, Kuhne M. 2011. German outbreak of Escherichia coli O104:H4 associated with sprouts. N. Engl. J. Med. 365:1763-1770.
10. Scheutz F, Nielsen EM, Frimodt-Moller J, Boisen N, Morabito S, Tozzoli R, Nataro JP, Caprioli A. 2011. Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104:H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Euro Surveill. 16(24):pii=19889. http://www .eurosurveillance.org/ViewArticle.aspx?ArticleId=19889.
11. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, Klammer A, Peluso P, Lee L, Kislyuk AO, Bullard J, Kasarskis A, Wang S, Eid J, Rank D, Redman JC, Steyert SR, Frimodt-Moller J, Struve C, Petersen AM, Krogfelt KA, Nataro JP, Schadt EE, Waldor MK. 2011. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N. Engl. J. Med. 365:709-717.
12. Bielaszewska M, Mellmann A, Zhang W, Kock 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.
13. Cheung MK, Li L, Nong W, Kwan HS. 2011. 2011 German Escherichia coli O104:H4 outbreak: whole-genome phylogeny without alignment. BMC Res. Notes 4:533. doi:10.1186/1756-0500-4-533.
14. Rohde H, Qin J, Cui Y, Li D, Loman NJ, Hentschke M, Chen W, Pu F, Peng Y, Li J, Xi F, Li S, Li Y, Zhang Z, Yang X, Zhao M, Wang P, Guan Y, Cen Z, Zhao X, Christner M, Kobbe R, Loos S, Oh J, Yang L, Danchin A, Gao GF, Song Y, Yang H, Wang J, Xu J, Pallen MJ, Aepfelbacher M, Yang R. 2011. Open-source genomic analysis of Shigatoxin-producing E. coli O104:H4. N. Engl. J. Med. 365:718-724.
15. Bockemuhl J, Aleksic S, Karch H. 1992. Serological and biochemical properties of Shiga-like toxin (verocytotoxin)-producing strains of Escherichia coli, other than O-group 157, from patients in Germany. Zentralbl. Bakteriol. 276:189-195.
16. Mellmann A, Bielaszewska M, Kock 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.
17. Boudailliez B, Berquin P, Mariani-Kurkdjian P, Ilef D, Cuvelier B, Capek I, Tribout B, Bingen E, Piussan C. 1997. Possible person-toperson transmission of Escherichia coli O111-associated hemolytic uremic syndrome. Pediatr. Nephrol. 11:36-39.
18. Morabito S, Karch H, Mariani-Kurkdjian P, Schmidt H, Minelli F,Bingen E, Caprioli A. 1998. Enteroaggregative, Shiga toxin-producing Escherichia coli O111:H2 associated with an outbreak of hemolytic-uremic syndrome. J. Clin. Microbiol. 36:840-842.
19. Willshaw GA, Scotland SM, Smith HR, Rowe B. 1992. Properties of Vero cytotoxin-producing Escherichia coli of human origin of O serogroups other than O157. J. Infect. Dis. 166:797-802.
20. Centers for Disease Control and Prevention. 2011. Investigation update: outbreak of Shiga toxin-producing E. coli O104 (STEC O104:H4) infections associated with travel to Germany. Centers for Disease Control and Prevention, Atlanta, GA.
21. Iyoda S, Tamura K, Itoh K, Izumiya H, Ueno N, Nagata K, Togo M, Terajima J, Watanabe H. 2000. Inducible stx2 phages are lysogenized in the enteroaggregative and other phenotypic Escherichia coli O86:HNM isolated from patients. FEMS Microbiol. Lett. 191:7-10.
22. Smith HR, Cheasty T, Rowe B. 1997. Enteroaggregative Escherichia coli and outbreaks of gastroenteritis in UK. Lancet 350:814-815.
23. Tompkins DS, Hudson MJ, Smith HR, Eglin RP, Wheeler JG, Brett MM, Owen RJ, Brazier JS, Cumberland P, King V, Cook PE. 1999. A study of infectious intestinal disease in England: microbiological findings in cases and controls. Commun. Dis. Public Health 2:108-113.
24. Pabst WL, Altwegg M, Kind C, Mirjanic S, Hardegger D, Nadal D. 2003. Prevalence of enteroaggregative Escherichia coli among children with and without diarrhea in Switzerland. J. Clin. Microbiol. 41:2289-2293.
25. Itoh Y, Nagano I, Kunishima M, Ezaki T. 1997. Laboratory investigation of enteroaggregative Escherichia coli O untypeable:H10 associated with a massive outbreak of gastrointestinal illness. J. Clin. Microbiol. 35:2546-2550.
26. Huang DB, Dupont HL. 2004. Enteroaggregative Escherichia coli: an emerging pathogen in children. Semin. Pediatr. Infect. Dis. 15:266-271.
27. Bhan MK, Bhandari N, Sazawal S, Clemens J, Raj P, Levine MM, Kaper JB. 1989. Descriptive epidemiology of persistent diarrhoea among young children in rural northern India. Bull. World Health Organ. 67:281-288.
28. Okeke IN, Lamikanra A, Steinruck H, Kaper JB. 2000. Characterization of Escherichia coli strains from cases of childhood diarrhea in provincial southwestern Nigeria. J. Clin. Microbiol. 38:7-12.
29. Ruttler ME, Renna NF, Balbi L, Garcia B, Guidone L, Fernandez R, Puig O, Ortiz A. 2002. Characterization of enteroaggregative Escherichia coli strains isolated from children with acute diarrhea, in Mendoza, Argentina. Rev. Argent. Microbiol. 34:167-170.
30. Cobeljic M, Miljkovic-Selimovic B, Paunovic-Todosijevic D, Velickovic Z, Lepsanovic Z, Zec N, Savic D, Ilic R, Konstantinovic S, Jovanovic B, Kostic V. 1996. Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol. Infect. 117:11-16.
31. Huppertz HI, Rutkowski S, Aleksic S, Karch H. 1997. Acute and chronic diarrhoea and abdominal colic associated with enteroaggregative Escherichia coli in young children living in western Europe. Lancet 349:1660-1662.
32. Mossoro C, Glaziou P, Yassibanda S, Lan NT, Bekondi C, Minssart P, Bernier C, Le Bouguenec C, Germani Y. 2002. Chronic diarrhea, hemorrhagic colitis, and hemolytic-uremic syndrome associated with HEp-2 adherent Escherichia coli in adults infected with human immunodeficiency virus in Bangui, Central African Republic. J. Clin. Microbiol. 40: 3086-3088.
33. Mayer HB, Wanke CA. 1995. Enteroaggregative Escherichia coli as a possible cause of diarrhea in an HIV-infected patient. N. Engl. J. Med. 332:273-274.
34. Mathewson JJ, Jiang ZD, Zumla A, Chintu C, Luo N, Calamari SR, Genta RM, Steephen A, Schwartz P, DuPont HL. 1995. HEp-2 celladherent Escherichia coli in patients with human immunodeficiency virusassociated diarrhea. J. Infect. Dis. 171:1636-1639.
35. Jiang ZD, Greenberg D, Nataro JP, Steffen R, DuPont HL. 2002. Rate of occurrence and pathogenic effect of enteroaggregative Escherichia coli virulence factors in international travelers. J. Clin. Microbiol. 40:4185-4190.
36. Mathewson JJ, Johnson PC, DuPont HL, Morgan DR, Thornton SA, Wood LV, Ericsson CD. 1985. A newly recognized cause of travelers' diarrhea: enteroadherent Escherichia coli. J. Infect. Dis. 151:471-475.
37. Adachi JA, Ericsson CD, Jiang ZD, DuPont MW, Pallegar SR, DuPont HL. 2002. Natural history of enteroaggregative and enterotoxigenic Escherichia coli infection among US travelers to Guadalajara, Mexico. J. Infect. Dis. 185:1681-1683.
38. Adachi JA, Jiang ZD, Mathewson JJ, Verenkar MP, Thompson S, Martinez-Sandoval F, Steffen R, Ericsson CD, DuPont HL. 2001. Enteroaggregative Escherichia coli as a major etiologic agent in traveler's diarrhea in 3 regions of the world. Clin. Infect. Dis. 32:1706-1709.
39. Gascon J, Vargas M, Quinto L, Corachan M, Jimenez de Anta MT, Vila J. 1998. Enteroaggregative Escherichia coli strains as a cause of traveler's diarrhea: a case-control study. J. Infect. Dis. 177:1409-1412.
40. Boisen N, Scheutz F, Rasko DA, Redman JC, Persson S, Simon J, Kotloff KL, Levine MM, Sow S, Tamboura B, Toure A, Malle D, Panchalingam S, Krogfelt KA, Nataro JP. 2012. Genomic characterization of enteroaggregative Escherichia coli from children in Mali. J. Infect. Dis. 205:431-444.
41. Czeczulin JR, Whittam TS, Henderson IR, Navarro-Garcia F, Nataro JP. 1999. Phylogenetic analysis of enteroaggregative and diffusely adherent Escherichia coli. Infect. Immun. 67:2692-2699.
42. Kang G, Pulimood AB, Mathan MM, Mathan VI. 2001. Enteroaggregative Escherichia coli infection in a rabbit model. Pathology 33:341-346.
43. Sainz T, Perez J, Fresan MC, Flores V, Jimenez L, Hernandez IHU, Eslava C. 2002. Histological alterations and immune response induced by Pet toxin during colonization with enteroaggregative Escherichia coli (EAEC) in a mouse model infection. J. Microbiol. 40:91-97.
44. Harrington SM, Sheikh J, Henderson IR, Ruiz-Perez F, Cohen PS, Nataro JP. 2009. The Pic protease of enteroaggregative Escherichia coli promotes intestinal colonization and growth in the presence of mucin. Infect. Immun. 77:2465-2473.
45. Morin N, Tirling C, Ivison SM, Kaur AP, Nataro JP, Steiner TS. 2010. Autoactivation of the AggR regulator of enteroaggregative Escherichia coli in vitro and in vivo. FEMS Immunol. Med. Microbiol. 58:344-355.
46. Martinez-Jehanne V, du Merle L, Bernier-Febreau C, Usein C, Gassama-Sow A, Wane AA, Gouali M, Damian M, Aidara-Kane A, Germani Y, Fontanet A, Coddeville B, Guerardel Y, Le Bouguenec C. 2009. Role of deoxyribose catabolism in colonization of the murine intestine by pathogenic Escherichia coli strains. Infect. Immun. 77:1442-1450.
47. Torres AG, Cieza RJ, Rojas-Lopez M, Blumentritt CA, Souza CS, Johnston RK, Strockbine N, Kaper JB, Sbrana E, Popov VL. 2012. In vivo bioluminescence imaging of Escherichia coli O104:H4 and role of aerobactin during colonization of a mouse model of infection. BMC Microbiol. 12:112. doi:10.1186/1471-2180-12-112.
48. Roche JK, Cabel A, Sevilleja J, Nataro J, Guerrant RL. 2010. Enteroaggregative Escherichia coli (EAEC) impairs growth while malnutrition worsens EAEC infection: a novel murine model of the infection malnutrition cycle. J. Infect. Dis. 202:506-514.
49. Al Safadi R, Abu-Ali GS, Sloup RE, Rudrik JT, Waters CM, Eaton KA, Manning SD. 2012. Correlation between in vivo biofilm formation and virulence gene expression in Escherichia coli O104:H4. PLoS One 7:e41628. doi:10.1371/journal.pone.0041628.
50. Garcia A, Fox JG. 2003. The rabbit as a new reservoir host of enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 9:1592-1597.
51. Panda A, Tatarov I, Melton-Celsa AR, Kolappaswamy K, Kriel EH, Petkov D, Coksaygan T, Livio S, McLeod CG, Nataro JP, O'Brien AD, DeTolla LJ. 2010. Escherichia coli O157:H7 infection in Dutch belted and New Zealand white rabbits. Comp. Med. 60:31-37.
52. Garcia A, Bosques CJ, Wishnok JS, Feng Y, Karalius BJ, Butterton JR, Schauer DB, Rogers AB, Fox JG. 2006. Renal injury is a consistent finding in Dutch belted rabbits experimentally infected with enterohemorrhagic Escherichia coli. J. Infect. Dis. 193:1125-1134.
53. Melton-Celsa AR, Zangari T, Panda A, Smith MA, Boisen N, Taratov I, Lipsky MM, DeTolla LJ, Kaper JP, O'Brien AD. 2012. Abstr. 8th Int. Symp. Shiga Toxin (Verocytotoxin) Producing Escherichia coli Infect., Amsterdam, The Netherlands, abstr. D2-7.
54. National Research Council, Committee for the Update of the Guide for the Care and Use of Laboratory Animals. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
55. Centers for Disease Control and Prevention and National Institutes of Health. 2007. Biosafety in microbiological and biomedical laboratories (BMBL), 5th ed. U.S. Government Printing Office, Washington, DC.
56. Shaikh N, Tarr PI. 2003. Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J. Bacteriol. 185:3596-3605.
57. Scheutz F, Teel LD, Beutin L, Pierard 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.
58. Roche Applied Sciences. 2009. DIG application manual for filter hybridization. Roche Applied Sciences, Mannheim, Germany.
59. Lindgren SW, Melton AR, O'Brien AD. 1993. Virulence of enterohemorrhagic Escherichia coli O91:H21 clinical isolates in an orally infected mouse model. Infect. Immun. 61:3832-3842.
60. Gentry MK, Dalrymple JM. 1980. Quantitative microtiter cytotoxicity assay for Shigella toxin. J. Clin. Microbiol. 12:361-366.
61. Schmitt CK, McKee ML, O'Brien AD. 1991. Two copies of Shiga-like toxin II-related genes common in enterohemorrhagic Escherichia coli strains are responsible for the antigenic heterogeneity of the O157:H strain E32511. Infect. Immun. 59:1065-1073.
62. Wadolkowski EA, Burris JA, O'Brien AD. 1990. Mouse model for colonization and disease caused by enterohemorrhagic Escherichia coli O157: H7. Infect. Immun. 58:2438-2445.
63. Mohawk KL, Melton-Celsa AR, Zangari T, Carroll EE, O'Brien AD. 2010. Pathogenesis of Escherichia coli O157:H7 strain 86-24 following oral infection of BALB/c mice with an intact commensal flora. Microb. Pathog. 48:131-142.
64. Tzipori S, Montanaro J, Robins-Browne RM, Vial P, Gibson R, Levine MM. 1992. Studies with enteroaggregative Escherichia coli in the gnotobiotic piglet gastroenteritis model. Infect. Immun. 60:5302-5306.
65. Hicks S, Candy DC, Phillips AD. 1996. Adhesion of enteroaggregative Escherichia coli to pediatric intestinal mucosa in vitro. Infect. Immun. 64:4751-4760.
66. Wadolkowski EA, Sung LM, Burris JA, Samuel JE, O'Brien AD. 1990. Acute renal tubular necrosis and death of mice orally infected with Escherichia coli strains that produce Shiga-like toxin type II. Infect. Immun. 58:3959-3965.
67. Maura D, Morello E, du Merle L, Bomme P, Le Bouguenec C, Debarbieux L. 2012. Intestinal colonization by enteroaggregative Escherichia coli supports long-term bacteriophage replication in mice. Environ. Microbiol. 14:1844-1854.
68. Maura D, Galtier M, Le Bouguenec C, Debarbieux L. 2012. Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob. Agents Chemother. 56:6235-6242.
69. Wells CL, Maddaus MA, Jechorek RP, Simmons RL. 1988. Role of intestinal anaerobic bacteria in colonization resistance. Eur. J. Clin. Microbiol. Infect. Dis. 7:107-113.
70. Schlessinger D. 1988. Failure of aminoglycoside antibiotics to kill anaerobic, low-pH, and resistant cultures. Clin. Microbiol. Rev. 1:54-59.
71. van der Waaij D, Berghuis-de Vries JM, Lekkerkerk-van der Wees JEC. 1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (Lond.) 69:405-411.
72. van der Waaij D, Vossen JM, Altes CK, Hartgrink C. 1977. Reconventionalization following antibiotic decontamination in man and animals. Am. J. Clin. Nutr. 30:1887-1895.
73. Ake JA, Jelacic S, Ciol MA, Watkins SL, Murray KF, Christie DL, Klein EJ, Tarr PI. 2005. Relative nephroprotection during Escherichia coli O157:H7 infections: association with intravenous volume expansion. Pediatrics 115:e673-e680. doi:10.1542/peds.2004-2236.
74. Karpman D, Hakansson A, Perez MT, Isaksson C, Carlemalm E, Caprioli A, Svanborg C. 1998. Apoptosis of renal cortical cells in the hemolytic-uremic syndrome: in vivo and in vitro studies. Infect. Immun. 66: 636-644.
75. Kaneko K, Kiyokawa N, Ohtomo Y, Nagaoka R, Yamashiro Y, Taguchi T, Mori T, Fujimoto J, Takeda T. 2001. Apoptosis of renal tubular cells in Shiga-toxin-mediated hemolytic uremic syndrome. Nephron 87:182-185.
76. Meyers KE, Kaplan BS. 2000. Many cell types are Shiga toxin targets. Kidney Int. 57:2650-2651.
77. Robinson CM, Sinclair JF, Smith MJ, O'Brien AD. 2006. Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc. Natl. Acad. Sci. U. S. A. 103:9667-9672.
78. Sinclair JF, O'Brien AD. 2002. Cell surface-localized nucleolin is a eukaryotic receptor for the adhesin intimin-gamma of enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem. 277:2876-2885.