Production of the Escherichia coli common pilus by uropathogenic E. coli is associated with adherence to HeLa and HTB-4 cells and invasion of mouse bladder urothelium

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Saldaña, Zeus ^a   De La Cruz, Miguel A ^a,e   Carrillo Casas, Erika Margarita ^c   Durán, Laura ^a   Zhang, Yushan ^b   Hernández Castro, Rigoberto ^c   Puente, José L ^d   Daaka, Yehia ^b   Girón, Jorge A ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c HOSPITAL GENERAL DR MANUEL GEA GONZÁLEZ   (Mexico)

^d INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^e INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM PILUS; BIOFILM; BLADDER CANCER CELL LINE; CHILD; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ECPA GENE; ESCHERICHIA COLI COMMON PILUS; FEMALE; GENE FUNCTION; HELA CELL LINE; HOST PATHOGEN INTERACTION; HTB 4 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; SCHOOL CHILD; URINARY TRACT INFECTION; UROPATHOGENIC ESCHERICHIA COLI; ANIMAL; BLADDER; CYTOLOGY; EPITHELIUM CELL; FIMBRIA; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MUTATION; PHYSIOLOGY; UROTHELIUM;

ECPA PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; FIMBRIA PROTEIN;

ANIMALS; BACTERIAL ADHESION; BIOFILMS; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HELA CELLS; HUMANS; MICE; MUTATION; URINARY BLADDER; UROPATHOGENIC ESCHERICHIA COLI; UROTHELIUM;

EID: 84904490597     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101200     Document Type: Article

References (37)

1. Nougayrede JP, Fernandes PJ, Donnenberg MS (2003) Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 5: 359-372. (Pubitemid 36748487)
2. Foxman B (2003) Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Dis Mon 49: 53-70.
3. Schilling JD, Martin SM, Hunstad DA, Patel KP, Mulvey MA, et al. (2003) CD14- and Toll-like receptor-dependent activation of bladder epithelial cells by lipopolysaccharide and type 1 piliated Escherichia coli. Infect Immun 71: 1470-1480. (Pubitemid 36254334)
4. Mulvey MA (2002) Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4: 257-271. (Pubitemid 34567594)
5. Eto DS, Jones TA, Sundsbak JL, Mulvey MA (2007) Integrin-mediated host cell invasion by type 1-piliated uropathogenic Escherichia coli. PLoS Pathog 3: e100.
6. Bishop BL, Duncan MJ, Song J, Li G, Zaas D, et al. (2007) Cyclic AMP-regulated exocytosis of Escherichia coli from infected bladder epithelial cells. Nat Med 13: 625-630. (Pubitemid 46828483)
7. Song J, Bishop BL, Li G, Duncan MJ, Abraham SN (2007) TLR4-initiated and cAMP-mediated abrogation of bacterial invasion of the bladder. Cell Host Microbe 1: 287-298. (Pubitemid 46865609)
8. Wang Z, Humphrey C, Frilot N, Wang G, Nie Z, et al. (2011) Dynamin2- and endothelial nitric oxide synthase-regulated invasion of bladder epithelial cells by uropathogenic Escherichia coli. J Cell Biol 192: 101-110.
9. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, et al. (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301: 105-107. (Pubitemid 36801572)
10. Mysorekar IU, Hultgren SJ (2006) Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc Natl Acad Sci U S A 103: 14170-14175. (Pubitemid 44452998)
11. Schilling JD, Hultgren SJ, Lorenz RG (2002) Recent advances in the molecular basis of pathogen recognition and host responses in the urinary tract. Int Rev Immunol 21: 291-304.
12. Rosen DA, Hooton TM, Stamm WE, Humphrey PA, Hultgren SJ (2007) Detection of intracellular bacterial communities in human urinary tract infection. PLoS Med 4: e329.
13. Blattner FR, Plunkett G, 3rd, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
14. Pouttu R, Westerlund-Wikstrom B, Lang H, Alsti K, Virkola R, et al. (2001) matB, a common fimbrillin gene of Escherichia coli, expressed in a genetically conserved, virulent clonal group. J Bacteriol 183: 4727-4736. (Pubitemid 32708957)
15. Rendon MA, Saldana Z, Erdem AL, Monteiro-Neto V, Vazquez A, et al. (2007) Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci U S A 104: 10637-10642. (Pubitemid 47185717)
16. Avelino F, Saldana Z, Islam S, Monteiro-Neto V, Dall'Agnol M, et al. (2010) The majority of enteroaggregative Escherichia coli strains produce the E. coli common pilus when adhering to cultured epithelial cells. Int J Med Microbiol 300: 440-448.
17. Blackburn D, Husband A, Saldana Z, Nada RA, Klena J, et al. (2009) Distribution of the Escherichia coli common pilus among diverse strains of human enterotoxigenic E. coli. J Clin Microbiol 47: 1781-1784.
18. Saldana Z, Erdem AL, Schuller S, Okeke IN, Lucas M, et al. (2009) The Escherichia coli common pilus and the bundle-forming pilus act in concert during the formation of localized adherence by enteropathogenic E. coli. J Bacteriol 191: 3451-3461.
19. Martinez-Santos VI, Medrano-Lopez A, Saldana Z, Giron JA, Puente JL (2012) Transcriptional regulation of the ecp operon by EcpR, IHF, and H-NS in attaching and effacing Escherichia coli. J Bacteriol 194: 5020-5033.
20. Lehti TA, Bauchart P, Dobrindt U, Korhonen TK, Westerlund-Wikstrom B (2012) The fimbriae activator MatA switches off motility in Escherichia coli by repression of the flagellar master operon flhDC. Microbiology 158: 1444-1455.
21. Lehti TA, Bauchart P, Heikkinen J, Hacker J, Korhonen TK, et al. (2010) Mat fimbriae promote biofilm formation by meningitis-associated Escherichia coli. Microbiology 156: 2408-2417.
22. Alcantar-Curiel MD, Blackburn D, Saldana Z, Gayosso-Vazquez C, Iovine NM, et al. (2013) Multi-functional analysis of Klebsiella pneumoniae fimbrial types in adherence and biofilm formation. Virulence 4: 129-138.
23. Lehti TA, Bauchart P, Kukkonen M, Dobrindt U, Korhonen TK, et al. (2013) Phylogenetic group-associated differences in regulation of the common colonization factor Mat fimbria in Escherichia coli. Mol Microbiol. 87: 1200-1222.
24. Girón JA, Ho AS, Schoolnik GK (1991) An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710-713. (Pubitemid 21917393)
25. Girón JA, Torres AG, Freer E, Kaper JB (2002) The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 44: 361-379. (Pubitemid 34429742)
26. Berry RE, Klumpp DJ, Schaeffer AJ (2009) Urothelial cultures support intracellular bacterial community formation by uropathogenic Escherichia coli. Infect Immun 77: 2762-2772.
27. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645. (Pubitemid 30412767)
28. McMichael JC, Ou JT (1979) Structure of common pili from Escherichia coli. J Bacteriol 138: 969-975. (Pubitemid 9208092)
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
30. Brinton CC, Jr. (1959) Non-flagellar appendages of bacteria. Nature 183: 782-786.
31. Davey ME, O'Toole G A (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64: 847-867. (Pubitemid 32475933)
32. de Oliveira-Garcia D, Dall'Agnol M, Rosales M, Azzuz AC, Alcantara N, et al. (2003) Fimbriae and adherence of Stenotrophomonas maltophilia to epithelial cells and to abiotic surfaces. Cell Microbiol 5: 625-636. (Pubitemid 37080673)
33. Xicohtencatl-Cortes J, Monteiro-Neto V, Saldana Z, Ledesma MA, Puente JL, et al. (2009) The type 4 pili of enterohemorrhagic Escherichia coli O157:H7 are multipurpose structures with pathogenic attributes. J Bacteriol 191: 411-421.
34. Garnett JA, Martinez-Santos VI, Saldana Z, Pape T, Hawthorne W, et al. (2012) Structural insights into the biogenesis and biofilm formation by the Escherichia coli common pilus. Proc Natl Acad Sci U S A 109: 3950-3955.
35. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, et al. (1990) Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58: 1281-1289. (Pubitemid 20151789)
36. Stapleton A, Moseley S, Stamm WE (1991) Urovirulence determinants in Escherichia coli isolates causing first-episode and recurrent cystitis in women. J Infect Dis 163: 773-779.
37. Mulvey MA, Schilling JD, Hultgren SJ (2001) Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 69: 4572-4579. (Pubitemid 32574459)