Mechanisms and consequences of bladder cell invasion by uropathogenic Escherichia coli

European Journal of Clinical Investigation

Volumn 38, Issue SUPPL.2, 2008, Pages 2-11

  Dhakal, B K ^a,b   Kulesus, R R ^a,b   Mulvey, M A ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Fimbriae; Integrin; Invasion; UPEC; Uroplakin; UTI

Indexed keywords

BACTERIUM PILUS; CYSTITIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; UROPATHOGENIC ESCHERICHIA COLI;

ANIMALS; BACTERIAL ADHESION; CYSTITIS; DISEASE PROGRESSION; DISEASE RESERVOIRS; EPITHELIAL CELLS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; HUMANS; OPPORTUNISTIC INFECTIONS; URINARY BLADDER; VIRULENCE;

EID: 52649173133     PISSN: 00142972     EISSN: 13652362     Source Type: Journal    
DOI: 10.1111/j.1365-2362.2008.01986.x     Document Type: Review

References (110)

1. Muhldorfer I, Ziebuhr W, Hacker J. Escherichia coli in Urinary Tract Infections. In : Sussman M, editor. Molecular Med Microbiology. London : Academic Press 2001 pp. 1739 48.
2. Scholes D, Hooton TM, Roberts PL, Gupta K, Stapleton AE, Stamm WE. Risk factors associated with acute pyelonephritis in healthy women. Ann Intern Med 2005 142 : 20 7.
3. Foxman B, Brown P. Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 2003 17 : 227 41.
4. Mehnert-Kay SA. Diagnosis and management of uncomplicated urinary tract infections. Am Fam Physician 2005 72 : 451 6.
5. Ronald A. The etiology of urinary tract infection: traditional and emerging pathogens. Am J Med 2002 113 (Suppl. 1A 14S 9S.
6. Kucheria R, Dasgupta P, Sacks SH, Khan MS, Sheerin NS. Urinary tract infections: new insights into a common problem. Postgrad Med J 2005 81 : 83 6.
7. Jacobsen SM, Stickler DJ, Mobley HL, Shirtliff ME. Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin Microbiol Rev 2008 21 : 26 59.
8. Russo TA, Johnson JR. Medical and economic impact of extraintestinal infections due to Escherichia coli: focus on an increasingly important endemic problem. Microbes Infect 2003 5 : 449 56.
9. Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C et al. The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 2007 189 : 3228 36.
10. Moulin-Schouleur M, Reperant M, Laurent S, Bree A, Mignon-Grasteau S, Germon P et al. Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 2007 45 : 3366 76.
11. Rodriguez-Siek KE, Giddings CW, Doetkott C, Johnson TJ, Fakhr MK, Nolan LK. Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 2005 151 : 2097 110.
12. Ron EZ. Host specificity of septicemic Escherichia coli: human and avian pathogens. Curr Opin Microbiol 2006 9 : 28 32.
13. Foxman B, Manning SD, Tallman P, Bauer R, Zhang L, Koopman JS et al. Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. Am J Epidemiol 2002 156 : 1133 40.
14. Servin AL. Pathogenesis of Afa/Dr diffusely adhering Escherichia coli. Clin Microbiol Rev 2005 18 : 264 92.
15. Bower JM, Eto DS, Mulvey MA. Covert operations of uropathogenic Escherichia coli within the urinary tract. Traffic 2005 6 : 18 31.
16. Johnson JR. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev 1991 4 : 80 128.
17. McTaggart LA, Rigby RC, Elliott TS. The pathogenesis of urinary tract infections associated with Escherichia coli, Staphylococcus saprophyticus and S. epidermidis. J Med Microbiol 1990 32 : 135 41.
18. Fukushi Y, Orikasa S, Kagayama M. An electron microscopic study of the interaction between vesical epithelium and E. coli. Invest Urol 1979 17 : 61 8.
19. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Koopman JS et al. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 1998 282 : 1494 7.
20. Mulvey MA, Schilling JD, Hultgren SJ. Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 2001 69 : 4572 9.
21. Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ. Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci USA 2000 97 : 8829 35.
22. Eto DS, Sundsbak JL, Mulvey MA. Actin-gated intracellular growth and resurgence of uropathogenic Escherichia coli. Cell Microbiol 2006 8 : 704 17.
23. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ. Intracellular bacterial biofilm-like pods in urinary tract infections. Science 2003 301 : 105 7.
24. Justice SS, Hung C, Theriot JA. Fletcher DA, Anderson GG, Footer MJ et al. Differentiation and developmental pathways of uropathogenic Escherichia coli in urinary tract pathogenesis. Proc Natl Acad Sci USA 2004 101 : 1333 8.
25. Schilling JD, Lorenz RG, Hultgren SJ. Effect of trimethoprim- sulfamethoxazole on recurrent bacteriuria and bacterial persistence in mice infected with uropathogenic Escherichia coli. Infect Immun 2002 70 : 7042 9.
26. Kerrn MB, Struve C, Blom J, Frimodt-Moller N, Krogfelt KA. Intracellular persistence of Escherichia coli in urinary bladders from mecillinam-treated mice. J Antimicrob Chemother 2005 55 : 383 6.
27. Hvidberg H, Struve C, Krogfelt KA, Christensen N, Rasmussen SN, Frimodt-Moller N. Development of a long-term ascending urinary tract infection mouse model for antibiotic treatment studies. Antimicrob Agents Chemother 2000 44 : 156 63.
28. Eto DS, Jones TA, Sundsbak JL, Mulvey MA. Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 2007 3 : e100.
29. Garofalo CK, Hooton TM, Martin SM, Stamm WE, Palermo JJ, Gordon JI et al. Escherichia coli from urine of female patients with urinary tract infections is competent for intracellular bacterial community formation. Infect Immun 2007 75 : 52 60.
30. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ. Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 2007 4 : e329.
31. Hicks RM. The mammalian bladder: an accommodating organ. Biol Rev Camb Philos Soc 1975 50 : 1123.
32. Apodaca G. The uroepithelium: not just a passive barrier. Traffic 2004 5 : 117 28.
33. Mysorekar IU, Mulvey MA, Hultgren SJ, Gordon JI. Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli. J Biol Chem 2002 277 : 7412 9.
34. Schilling JD, Mulvey MA, Vincent CD, Lorenz RG, Hultgren SJ. Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism. J Immunol 2001 166 : 1148 55.
35. Bishop BL, Duncan MJ, Song J, Li G, Zaas D, Abraham SN. Cyclic AMP-regulated exocytosis of Escherichia coli from infected bladder epithelial cells. Nat Med 2007 13 : 625 30.
36. Justice SS. Hunstad DA, Seed PC, Hultgren SJ. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. Proc Natl Acad Sci USA 2006 103 : 19 884 9.
37. Smith YC, Grande KK, Rasmussen SB, O'Brien AD. Novel three-dimensional organoid model for evaluation of the interaction of uropathogenic Escherichia coli with terminally differentiated human urothelial cells. Infect Immun 2006 74 : 750 7.
38. Wiles TJ, Dhakal BK, Eto DS, Mulvey MA. Inactivation of host AKT/PKB signaling by bacterial pore-forming toxins. Mol Biol Cell 2008 19 : 1427 38.
39. Klumpp DJ, Rycyk MT, Chen MC, Thumbikat P, Sengupta S, Schaeffer AJ. Uropathogenic Escherichia coli induces extrinsic and intrinsic cascades to initiate urothelial apoptosis. Infect Immun 2006 74 : 5106 13.
40. Klumpp DJ, Weiser AC, Sengupta S, Forrestal SG, Batler RA, Schaeffer AJ. Uropathogenic Escherichia coli potentiates type 1 pilus-induced apoptosis by suppressing NF-kappaB. Infect Immun 2001 69 : 6689 95.
41. Jezernik K, Medalia O, Aronson M. A comparative study of the desquamation of urothelial cells during gestation and in adult mice following moderate stress or endotoxin treatment. Cell Biol Int 1995 19 : 887 93.
42. Martinez JJ, Mulvey MA, Schilling JD, Pinkner JS, Hultgren SJ. Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. Embo J 2000 19 : 2803 12.
43. Schlager TA, Whittam TS, Hendley JO, Bhang JL, Wobbe CL, Stapleton A. Variation in frequency of the virulence-factor gene in Escherichia coli clones colonizing the stools and urinary tracts of healthy prepubertal girls. J Infect Dis 2003 188 : 1059 64.
44. Thankavel K, Madison B, Ikeda T, Malaviya R, Shah AH, Arumugam PM et al. Localization of a domain in the FimH adhesin of Escherichia coli type 1 fimbriae capable of receptor recognition and use of a domain-specific antibody to confer protection against experimental urinary tract infection. J Clin Invest 1997 100 : 1123 36.
45. Connell H, Agace W, Klemm P, Schembri M, Marild S, Svanborg C. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci USA 1996 93 : 9827 32.
46. Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS, Burlein J et al. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science 1997 276 : 607 11.
47. Brinton CC. Non-flagellar appendages of bacteria. Nature 1959 183 : 782 6.
48. Buchanan K, Falkow S, Hull RA, Hull SI. Frequency among Enterobacteriaceae of the DNA sequences encoding type 1 pili. J Bacteriol 1985 162 : 799 803.
49. Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, Abraham SN et al. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc Natl Acad Sci USA 1995 92 : 2081 5.
50. Sauer FG, Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ. Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin Microbiol 2000 3 : 65 72.
51. Brinton CC Jr. The structure, function, synthesis and genetic control of bacterial pili and a molecular model for DNA and RNA transport in gram negative bacteria. Trans N Y Acad Sci 1965 27 : 1003 54.
52. Russell PW, Orndorff PE. Lesions in two Escherichia coli type 1 pilus genes alter pilus number and length without affecting receptor binding. J Bacteriol 1992 174 : 5923 35.
53. Wold AE, Mestecky J, Tomana M, Kobata A, Ohbayashi H, Endo T et al. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect Immun 1990 58 : 3073 7.
54. Baorto DM, Gao Z, Malaviya R, Dustin ML, van der Merwe A, Lublin DM et al. Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature 1997 389 : 636 9.
55. Leusch HG, Drzeniek Z, Markos-Pusztai Z, Wagener C. Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose. Infect Immun 1991 59 : 2051 7.
56. Sauter SL, Rutherfurd SM, Wagener C, Shively JE, Hefta SA. Binding of nonspecific cross-reacting antigen, a granulocyte membrane glycoprotein, to Escherichia coli expressing type 1 fimbriae. Infect Immun 1991 59 : 2485 93.
57. Pak J, Pu Y, Zhang ZT, Hasty DL, Wu XR. Tamm-Horsfall protein binds to type 1 fimbriated Escherichia coli and prevents E. coli from binding to uroplakin Ia and Ib receptors. J Biol Chem 2001 276 : 9924 30.
58. Gbarah A, Gahmberg CG, Ofek I, Jacobi U, Sharon N. Identification of the leukocyte adhesion molecules CD11 and CD18 as receptors for type 1-fimbriated (mannose-specific) Escherichia coli. Infect Immun 1991 59 : 4524 30.
59. Zhou G, Mo WJ, Sebbel P, Min G, Neubert TA, Glockshuber R et al. Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci 2001 114 : 4095 103.
60. Pouttu R, Puustinen T, Virkola R, Hacker J, Klemm P, Korhonen TK. Amino acid residue Ala-62 in the FimH fimbrial adhesin is critical for the adhesiveness of meningitis-associated Escherichia coli to collagens. Mol Microbiol 1999 31 : 1747 57.
61. Kukkonen M, Raunio T, Virkola R, Lahteenmaki K, Makela PH, Klemm P et al. Basement membrane carbohydrate as a target for bacterial adhesion: binding of type I fimbriae of Salmonella enterica and Escherichia coli to laminin. Mol Microbiol 1993 7 : 229 37.
62. Sokurenko EV, Courtney HS, Abraham SN, Klemm P, Hasty DL. Functional heterogeneity of type 1 fimbriae of Escherichia coli. Infect Immun 1992 60 : 4709 19.
63. Wright KJ, Seed PC, Hultgren SJ. Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 2007 9 : 2230 41.
64. Ulett GC, Valle J, Beloin C, Sherlock O, Ghigo JM, Schembri MA. Functional analysis of antigen 43 in uropathogenic Escherichia coli reveals a role in long-term persistence in the urinary tract. Infect Immun 2007 75 : 3233 44.
65. Arnaout MA, Mahalingam B, Xiong JP. Integrin structure, allostery, and bidirectional signaling. Annu Rev Cell Dev Biol 2005 21 : 381 410.
66. Martinez JJ, Hultgren SJ. Requirement of Rho-family GTPases in the invasion of Type 1-piliated uropathogenic Escherichia coli. Cell Microbiol 2002 4 : 19 28.
67. Song J, Bishop BL, Li G, Duncan MJ, Abraham SN. TLR4-initiated and cAMP-mediated abrogation of bacterial invasion of the bladder. Cell Host Microbe 2007 1 : 287 98.
68. Shoelson SE, Sivaraja M, Williams KP, Hu P, Schlessinger J, Weiss MA. Specific phosphopeptide binding regulates a conformational change in the PI 3-kinase SH2 domain associated with enzyme activation. Embo J 1993 12 : 795 802.
69. Yin HL, Janmey PA. Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 2003 65 : 761 89.
70. Hartwig JH, Bokoch GM, Carpenter CL, Janmey PA, Taylor LA, Toker A et al. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 1995 82 : 643 53.
71. Southgate J, Kennedy W, Hutton KA, Trejdosiewicz LK. Expression and in vitro regulation of integrins by normal human urothelial cells. Cell Adhes Commun 1995 3 : 231 42.
72. Wang H, Liang FX, Kong XP. Characteristics of the phagocytic cup induced by uropathogenic E. coli. J Histochem Cytochem 2008 56 : 597 604.
73. Duncan MJ, Li G, Shin JS, Carson JL, Abraham SN. Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem 2004 279 : 18944 51.
74. Blott EJ, Griffiths GM. Secretory lysosomes. Nat Rev Mol Cell Biol 2002 3 : 122 31.
75. Reddy A, Caler EV, Andrews NW. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 2001 106 : 157 69.
76. Rodriguez A, Samoff E, Rioult MG, Chung A, Andrews NW. Host cell invasion by trypanosomes requires lysosomes and microtubule/kinesin-mediated transport. J Cell Biol 1996 134 : 349 62.
77. Gruenberg J, van der Goot FG. Mechanisms of pathogen entry through the endosomal compartments. Nat Rev Mol Cell Biol 2006 7 : 495 504.
78. Chen Y, Guo X, Deng FM, Liang FX, Sun W, Ren M et al. Rab27b is associated with fusiform vesicles and may be involved in targeting uroplakins to urothelial apical membranes. Proc Natl Acad Sci U S A 2003 100 : 14012 7.
79. Eto DS, Mulvey MA. Flushing bacteria out of the bladder. Nat Med 2007 13 : 531 2.
80. Parkkinen J, Korhonen TK, Pere A, Hacker J, Soinila S. Binding sites in the rat brain for Escherichia coli S fimbriae associated with neonatal meningitis. J Clin Invest 1988 81 : 860 5.
81. Lane MC, Mobley HL. Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 2007 72 : 19 25.
82. Parkkinen J, Hacker J, Korhonen TK. Enhancement of tissue plasminogen activator-catalyzed plasminogen activation by Escherichia coli S fimbriae associated with neonatal septicaemia and meningitis. Thromb Haemost 1991 65 : 483 6.
83. Marre R, Hacker J, Henkel W, Goebel W. Contribution of cloned virulence factors from uropathogenic Escherichia coli strains to nephropathogenicity in an experimental rat pyelonephritis model. Infect Immun 1986 54 : 761 7.
84. Goluszko P, Moseley SL, Truong LD, Kaul A, Williford JR, Selvarangan R et al. Development of experimental model of chronic pyelonephritis with Escherichia coli O75:K5:H-bearing Dr fimbriae: mutation in the dra region prevented tubulointerstitial nephritis. J Clin Invest 1997 99 : 1662 72.
85. Mulvey MA. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 2002 4 : 257 71.
86. Khan AS, Kniep B, Oelschlaeger TA, Van Die I, Korhonen T, Hacker J. Receptor structure for F1C fimbriae of uropathogenic Escherichia coli. Infect Immun 2000 68 : 3541 7.
87. Cota E, Jones C, Simpson P, Altroff H, Anderson KL, du Merle L et al. The solution structure of the invasive tip complex from Afa/Dr fibrils. Mol Microbiol 2006 62 : 356 66.
88. Plancon L, Du Merle L, Le Friec S, Gounon P, Jouve M, Guignot J et al. Recognition of the cellular beta1-chain integrin by the bacterial AfaD invasin is implicated in the internalization of afa-expressing pathogenic Escherichia coli strains. Cell Microbiol 2003 5 : 681 93.
89. Goluszko P, Popov V, Selvarangan R, Nowicki S, Pham T, Nowicki BJ. Dr fimbriae operon of uropathogenic Escherichia coli mediate microtubule-dependent invasion to the HeLa epithelial cell line. J Infect Dis 1997 176 : 158 67.
90. Nowicki B, Selvarangan R, Nowicki S. Family of Escherichia coli Dr adhesins: decay-accelerating factor receptor recognition and invasiveness. J Infect Dis 2001 183 (Suppl. 1 S24 7.
91. Foxman B, Zhang L, Tallman P, Palin K, Rode C, Bloch C et al. Virulence characteristics of Escherichia coli causing first urinary tract infection predict risk of second infection. J Infect Dis 1995 172 : 1536 41.
92. Zhang L, Foxman B, Tallman P, Cladera E, Le Bouguenec C, Marrs CF. Distribution of drb genes coding for Dr binding adhesins among uropathogenic and fecal Escherichia coli isolates and identification of new subtypes. Infect Immun 1997 65 : 2011 8.
93. 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 56 : 640 8.
94. Pham T, Kaul A, Hart A, Goluszko P, Moulds J, Nowicki S et al. Dra-related X adhesins of gestational pyelonephritis-associated Escherichia coli recognize SCR-3 and SCR-4 domains of recombinant decay-accelerating factor. Infect Immun 1995 63 : 1663 8.
95. 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 58 : 279 81.
96. Hasan RJ, Pawelczyk E, Urvil PT, Venkatarajan MS, Goluszko P, Kur J et al. Structure-function analysis of decay-accelerating factor: identification of residues important for binding of the Escherichia coli Dr adhesin and complement regulation. Infect Immun 2002 70 : 4485 93.
97. 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 178 : 2115 21.
98. Medof ME, Walter EI, Rutgers JL, Knowles DM, Nussenzweig V. Identification of the complement decay-accelerating factor (DAF) on epithelium and glandular cells and in body fluids. J Exp Med 1987 165 : 848 64.
99. Lublin DM, Review. Cromer and DAF: role in health and disease. Immunohematol 2005 21 : 39 47.
100. Le Bouguenec C, Servin AL. Diffusely adherent Escherichia coli strains expressing Afa/Dr adhesins (Afa/Dr DAEC): hitherto unrecognized pathogens. FEMS Microbiol Lett 2006 256 : 185 94.
101. Guignot J, Peiffer I, Bernet-Camard MF, Lublin DM, Carnoy C, Moseley SL et al. Recruitment of CD55 and CD66e brush border-associated glycosylphosphatidylinositol-anchored proteins by members of the Afa/Dr diffusely adhering family of Escherichia coli that infect the human polarized intestinal Caco-2/TC7 cells. Infect Immun 2000 68 : 3554 63.
102. Berger CN, Billker O, Meyer TF, Servin AL, Kansau I. Differential recognition of members of the carcinoembryonic antigen family by Afa/Dr adhesins of diffusely adhering Escherichia coli (Afa/Dr DAEC). Mol Microbiol 2004 52 : 963 83.
103. Guignot J, Bernet-Camard MF, Pous C, Plancon L, Le Bouguenec C, Servin AL. Polarized entry of uropathogenic Afa/Dr diffusely adhering Escherichia coli strain IH11128 into human epithelial cells: evidence for alpha5beta1 integrin recognition and subsequent internalization through a pathway involving caveolae and dynamic unstable microtubules. Infect Immun 2001 69 : 1856 68.
104. Selvarangan R, Goluszko P, Popov V, Singhal J, Pham T, Lublin DM et al. Role of decay-accelerating factor domains and anchorage in internalization of Dr-fimbriated Escherichia coli. Infect Immun 2000 68 : 1391 9.
105. Kansau I, Berger C, Hospital M, Amsellem R, Nicolas V, Servin AL et al. Zipper-like internalization of Dr-positive Escherichia coli by epithelial cells is preceded by an adhesin-induced mobilization of raft-associated molecules in the initial step of adhesion. Infect Immun 2004 72 : 3733 42.
106. Chen M, Tofighi R, Bao W, Aspevall O, Jahnukainen T, Gustafsson LE et al. Carbon monoxide prevents apoptosis induced by uropathogenic Escherichia coli toxins. Pediatric Nephrol (Berlin, Germany) 2006 21 : 382 9.
107. Russo TA, Davidson BA, Genagon SA, Warholic NM, Macdonald U, Pawlicki PD et al. E. coli virulence factor hemolysin induces neutrophil apoptosis and necrosis/lysis in vitro and necrosis/lysis and lung injury in a rat pneumonia model. Am J Physiol Lung Cell Mol Physiol 2005 289 : L207 16.
108. Mills M, Meysick KC, O'Brien AD. Cytotoxic necrotizing factor type 1 of uropathogenic Escherichia coli kills cultured human uroepithelial 5637 cells by an apoptotic mechanism. Infect Immun 2000 68 : 5869 80.
109. Lerm M, Pop M, Fritz G, Aktories K, Schmidt G. Proteasomal degradation of cytotoxic necrotizing factor 1-activated rac. Infect Immun 2002 70 : 4053 8.
110. Doye A, Mettouchi A, Bossis G, Clement R, Buisson-Touati C, Flatau G et al. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 2002 111 : 553 64.