Retraction of entero pathogenic E. coli type IV pili promotes efficient host cell colonization, effector translocation and tight junction disruption

Gut Microbes

Volumn 3, Issue 3, 2012, Pages 267-271

  Aroeti, Benjamin ^a   Friedman, Gil ^a   Zlotkin Rivkin, Efrat ^a   Donnenberg, Michael S ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

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

Author keywords

Bundle forming pili; Enteropathogenic E. coli; Polarized epithelial cells; Tight junctions; Type IV pili

Indexed keywords

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; BACTERIUM PILUS; CELL ADHESION; EFFECTOR CELL; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIUM CELL; HOST CELL; HUMAN; NONHUMAN; PATHOGENESIS; TIGHT JUNCTION; ANIMAL; BACTERIUM ADHERENCE; CELL LINE; FIMBRIA; METABOLISM; MICROBIOLOGY; MICROSCOPY; PATHOGENICITY; PROTEIN TRANSPORT; REVIEW; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ESCHERICHIA COLI PROTEIN; VIRULENCE FACTOR;

ANIMALS; BACTERIAL ADHESION; CELL LINE; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; FIMBRIAE, BACTERIAL; HUMANS; MICROSCOPY; PROTEIN TRANSPORT; TIGHT JUNCTIONS; VIRULENCE; VIRULENCE FACTORS;

EID: 84872009116     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.19814     Document Type: Article

References (48)

1. Zahavi EE, Lieberman JA, Donnenberg MS, Nitzan M, Baruch K, Rosenshine I, et al. Bundleforming pilus retraction enhances entero pathogenic Escherichia coli infectivity. Mol Biol Cell 2011; 22:2436-447;PMID:21613538; http://dx.doi.org/10.1091/mbc.E11-01-0001.
2. Proft T, Baker EN. Pili in Gram-negative and Gram-positive bacteria-structure, assembly and their role in disease. Cell Mol Life Sci 2009; 66:613-635; PMID:18953686; http://dx.doi.org/10.1007/s00018-008-8477-4.
3. Craig L, Pique ME, Tainer JA. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2004; 2:363-378; PMID:15100690; http://dx.doi.org/10.1038/nrmicro885.7864134.
4. Bieber D, Ramer SW, Wu CY, Murray WJ, Tobe T, Fernandez R, et al. Type IV pili, transient bacterial aggregates and virulence of enteropathogenic Escherichia coli. Science 1998; 280:2114-2118; PMID:9641917; http://dx.doi.org/10.1126/science.280.5372.2114.
5. Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, Gault J, et al. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 2011; 331:778-782; PMID:21311024; http://dx.doi.org/10.1126/science.1200729.
6. Jin F, Conrad JC, Gibiansky ML, Wong GC. Bacteria use type-IV pili to slingshot on surfaces. Proc Natl Acad Sci USA 2011; 108:12617-22; PMID:21768344;http://dx.doi.org/10.1073/pnas.1105073108.
7. Gibiansky ML, Conrad JC, Jin F, Gordon VD, Motto DA, Mathewson MA, et al. Bacteria use type IV pili to walk upright and detach from surfaces. Science 2010; 330:197; PMID:20929769; http://dx.doi.org/10.1126/science.1194238.
8. Merz AJ, So M, Sheetz MP. Pilus retraction powers bacterial twitching motility. Nature 2000; 407:98-102; PMID:10993081; http://dx.doi.org/10.1038/35024105.
9. Skerker JM, Berg HC. Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA 2001; 98:6901-6904; PMID:11381130; http://dx.doi.org/10.1073/pnas.121171698.
10. Pelicic V. Type IV pili: e pluribus unum? Mol Microbiol 2008; 68:827-837; PMID:18399938;http://dx.doi.org/10.1111/j.1365-2958.2008.06197.x.
11. Craig L, Li J. Type IV pili: paradoxes in form and function. Curr Opin Struct Biol 2008; 18:267-277; PMID:18249533; http://dx.doi.or/10.1016/j.sbi.2007.12.009.
12. namegr typeauthornamesnameMaier/sname/namex/xnamex /xfnameB/fname/name/namegr. Using laser tweezers to measure twitching motility in Neisseria. Curr Opin Microbiol 2005; 8:344-349; PMID:15939360; http://dx.doiorg/10.1016/j.mib.2005.04.002.
13. Maier B, Potter L, So M, Long CD, Seifert HS, Sheetz MP. Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci USA 2002; 99:16012-16017; PMID:12446837; http://dx.doi.org/10.1073/pnas.242523299.
14. Biais N, Higashi DL, Brujic J, So M, Sheetz MP. Force-dependent polymorphism in type IV pili reveals hidden epitopes. Proc Natl Acad Sci USA2010; 107:11358-1363; PMID:20534431; http://dx.doi.org/10.1073/pnas.0911328107.
15. Ochoa TJ, Contreras CA. Enteropatho genic Escherichia coli infection in children. Curr Opin Infect Dis 2011; 24:478-483; PMID:21857511; http://dx.doi.org/10.1097/QCO.0b013e32834a8b8b.
16. Girn JA, Ho AS, Schoolnk S. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 1991; 254:710-713; PMID:1683004;http://dx.doi.org/10.1126/science.1683004.
17. Scaletsky IC, Silva ML, Trabulsi LR. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 1984; 45:534-536;PMID:6146569.
18. Frankel G, Phillips AD. Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell Microbiol 2008; 10:549-556; PMID:18053003; http://dx.doi.org/10.1111/j.1462-5822.2007.01103.x.
19. Guttman JA, Finlay BB. Subcellular alterations that lead to diarrhea during bacterial pathogenesis. Trends Microbiol 2008; 16:535-542; PMID:18819802;http://dx.doi.org/10.1016/j.tim.2008.08.004.
20. Phillips N, Hayward RD, Koronakis V. Phosphorylation of the enteropathogenic E. coli receptor by the Src-family kinase c-Fyn triggers actin pedestal formation. Nat Cell Biol 2004; 6:618-625; PMID:15220932; http://dx.doi.org/10.1038/ncb1148.
21. Schmidt MA. LEEways: tales of EPEC, ATEC and EHEC. Cell Microbiol 2010; 12:1544-1552; PMID:20716205; http://dx.doi.org/10.1111/j.1462-5822.2010.01518.x.
22. Dean P, Kenny B. The effect or repertoire of entero pathogenic E. coli: ganging up on the host cell. Curr Opin Microbiol 2009; 12:101-109; PMID:19144561;http://dx.doi.org/10.1016/j.mib.2008.11.006.
23. Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, et al. Enteropathogenic and entero haemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 2011; 80:1420-1438;PMID:21488979; http://dx.doi.org/10.1111/j.1365-2958.2011.07661.x.
24. Guttman JA, Finlay BB. Tight junctions as targets of infectious agents. Biochim Biophys Acta 2009; 1788:832-841; PMID:19059200; http://dx.doi.org/10.1016/j.bbamem.2008.10.028.
25. Hodges K, Gill R. Infectious diarrhea: Cellular and molecular mechanisms. Gut Microbes 2010; 1:4-21; PMID:21327112; http://dx.doi.org/10.4161/gmic.1.1.11036.
26. Viswanathan VK, Hodges K, Hecht G. Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nat Rev Micro biol 2009; 7:110-119; PMID:19116615.
27. Donnenberg MS, Kaper JB. Enteropathogenic Escherichia coli. Infect Immun 1992; 60:3953-3961; PMID:1398907.
28. Milgotina EDM. The bundlin-forming pilus and other Type IV pili. Chapter 3 In: Jarrell KF, Ed. Pili and Flagella: Current Research and Future Trends Norfolk (UK): Caister Academic Press 2009.
29. Blank TE, Lacher DW, Scaletsky IC, Zhong H, Whittam TS, Donnenberg MS. Enteropathogenic Escherichia coli O157 strains from Brazil. Emerg Infect Dis 2003; 9:113-115; PMID:12533292.
30. Blank TE, Zhong H, Bell AL, Whittam TS, Donnenberg MS. Molecular variation among type IV pilin (bfpA) genes from diverse enteropathogenic Escherichia coli strains. Infect Immun 2000; 68:7028-7038; PMID:11083828; http://dx.doi.org/10.1128/IAI.68.12.7028-38.2000.
31. Fernandes PJ, Guo Q, Donnenberg MS. Functional consequences of sequence variation in bundlin, the enteropathogenic Escherichia coli type IV pilin protein. Infect Immun 2007; 75:4687-4696; PMID:17635860;http://dx.doi.org/10.1128/IAI.00009-07.
32. Hyland RM, Sun J, Griener TP, Mulvey GL, Klassen JS, Donnenberg MS, et al. The bundlin pilin protein of enteropathogenic Escherichia coli is an N-acetyllactosamine-specific lectin. Cell Microbiol 2008; 10:177-187; PMID:17697132.
33. Hyland RM, Beck P, Mulvey GL, Kitov PI, Armstrong GD. N-acetyllactosamine conjugated to gold nanoparticles inhibits enteropathogenic Escherichia coli colonization of the epithelium in human intestinal biopsy specimens. Infect Immun 2006; 74:5419-5421; PMID:16926439; http://dx.doi.org/10.1128/IAI.00739-06.
34. Humphries RM, Griener TP, Vogt SL, Mulvey GL, Raivio T, Donnenberg MS, et al. N-acetyllactosamineinduced retraction of bundle-forming pili regulates virulence-associated gene expression in enteropathogenic Escherichia coli. Mol Microbiol 2010; 76:1111-1126; PMID:20487271; http://dx.doi.org/10.1111/j.1365-2958.2010.07192.x.
35. Mills E, Baruch K, Charpentier X, Kobi S, Rosenshine I. Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 2008; 3:104-113; PMID:18312845; http://dx.doi.org/10.1016/j.chom.2007.11.007.
36. McNamara BP, Koutsouris A, O'Connell CB, Nougayréde JP, Donnenberg MS, Hecht G. Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J Clin Invest 2001; 107:621-629; PMID:11238563;http://dx.doi.org/10.1172/JCI11138.
37. Howitt MR, Lee JY, Lertsethtakarn P, Vogelmann R, Joubert LM, Ottemann KM, et al. ChePep controls Helicobacter pylori Infection of the gastric glands and chemotaxis in the Epsilonproteobacteria. MBio 2011; 2:98-111; PMID:21791582; http://dx.doi.org/10.1128/mBio.00098-11.
38. Lafont F, van der Goot FG. Bacterial invasion via lipid rafts. Cell Microbiol 2005; 7:613-620;PMID:15839890; http://dx.doi.org/10.1111/j.1462-5822.2005.00515.x.
39. Boettcher JP, Kirchner M, Churin Y, Kaushansky A, Pompaiah M, Thorn H, et al. Tyrosine-phosphorylated caveolin-1 blocks bacterial uptake by inducing Vav2- RhoA-mediated cytoskeletal rearrangements. PLoS Biol 2010; 8:1000457; PMID:20808760; http://dx.doi.org/10.1371/journal.pbio.1000457.
40. Sason H, Milgrom M, Weiss AM, Melamed-Book N, Balla T, Grinstein S, et al. Enteropathogenic Escherichia coli subverts phosphatidylinositol- 4,5-bisphosphate and phosphatidylinositol-3,4,5- trisphosphate upon epithelial cell infection. Mol Biol Cell 2009; 20:544-555; PMID:18987340; http://dx.doi.org/10.1091/mbc.E08-05-0516.
41. Hanajima-Ozawa M, Matsuzawa T, Fukui A, Kamitani S, Ohnishi H, Abe A, et al. Enteropathogenic Escherichia coli, Shigella flexneri and Listeria monocytogenes recruit a junctional protein, zonula occludens-1, to actin tails and pedestals. Infect Immun 2007; 75:565-573; PMID:17118974;http://dx.doi.org/10.1128/IAI.01479-06.
42. Simonovic I, Rosenberg J, Koutsouris A, Hecht G. Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol 2000; 2:305-315;PMID:11207587; http://dx.doi.org/10.1046/j.1462-5822.2000.00055.x.
43. Zolotarevsky Y, Hecht G, Koutsouris A, Gonzalez DE, Quan C, Tom J, et al. A membrane-permeant peptide that inhibits MLC kinase restores barrier function inin vitro models of intestinal disease. Gastroenterology 2002; 123:163-172; PMID:12105845; http://dx.doi.org/10.1053/gast.2002.34235.
44. Coureuil M, Mikaty G, Miller F, Lécuyer H, Bernard C, Bourdoulous S, et al. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 2009; 325:83-87; PMID:19520910;http://dx.doi.org/10.1126/science.1173196.
45. McKee ML, O'Brien AD. Investigation of enterohemorrhagic Escherichia coli O157:H7 adherence characteristics and invasion potential reveals a new attachment pattern shared by intestinal E. coli. Infect Immun 1995; 63:2070-2074; PMID:7537254.
46. Canil C, Rosenshine I, Ruschkowski S, Donnenberg MS, Kaper JB, Finlay BB. Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infect Immun 1993; 61:2755-2762; PMID:8514377.
47. Philpott DJ, McKay DM, Sherman PM, Perdue MH. Infection of T84 cells with enteropathogenic Escherichia coli alters barrier and transport functions. Am J Physiol 1996; 270:634-645; PMID:8928793.
48. Spitz J, Yuhan R, Koutsouris A, Blatt C, Alverdy J, Hecht G. Enteropathogenic Escherichia coli adherence to intestinal epithelial monolayers diminishes barrier function. Am J Physiol 1995; 268:374-379;PMID:7864134.