Bacterial-enterocyte crosstalk: Cellular mechanisms in health and disease

Journal of Pediatric Gastroenterology and Nutrition

Volumn 36, Issue 2, 2003, Pages 175-185

  Köhler, Henrik ^a,b   McCormick, Beth A ^a   Walker, W Allan ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESALAZINE; PROBIOTIC AGENT;

ACUTE DIARRHEA; ANTIINFLAMMATORY ACTIVITY; BACTERIAL FLORA; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; COMMENSALISM; ESCHERICHIA COLI; HUMAN; INFLAMMATION; INTESTINE CELL; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; LACTOBACILLUS; LACTOBACILLUS JOHNSONII; MOLECULAR MECHANICS; NEUTROPHIL CHEMOTAXIS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SALMONELLA; SHIGELLA; SHIGELLOSIS; SYMBIOSIS; TYPHOID FEVER; ULCERATIVE COLITIS; BACTERIAL PHENOMENA AND FUNCTIONS; CHILD; CYTOLOGY; DIGESTIVE SYSTEM; GASTROINTESTINAL DISEASE; MICROBIOLOGY; PATHOGENICITY; PHAGOCYTOSIS; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LACTOBACILLUS; LACTOBACILLUS JOHNSONII; SALMONELLA; SHIGELLA;

BACTERIAL ADHESION; BACTERIAL PHYSIOLOGY; CHILD; DIGESTIVE SYSTEM; ENTEROCYTES; ESCHERICHIA COLI; GASTROINTESTINAL DISEASES; HUMANS; PHAGOCYTOSIS; PROBIOTICS; SALMONELLA; SHIGELLA; SYMBIOSIS;

EID: 0037867722     PISSN: 02772116     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005176-200302000-00005     Document Type: Review

References (105)

1. Hooper LV, Gordon JI. Commensal Host-Bacterial relationship in the gut. Science 2001;292:1115-18.
2. Fuller R. Probiotics in human medicine. Gut 1991:32:439-42.
3. Duggan C, Gannon J, Walker WA. Protective nutrients and functional foods for the gastrointestinal tract. Am J Clin Nutr 2002;75:789-808.
4. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607-25.
5. Brocks JJ, Logan GA, Buick R, Summons RE. Archean molecular fossils and the early rise of eukaryotes. Science. 1999:285:1033-36.
6. Ben C, Martins J, Zoya I, Glass RI. The magnitude of the global problem of diarrhoeal disease: a ten year update. Bull WHO 1992;70:705-14.
7. Donnerberg MS. Pathogenic strategies of enteric bacteria. Nature 2000;406:768-74.
8. Hueck CJ. Type III protein secretion systems in bacterial pathogens in animals and plants. Microbiol Mol Biol Rev 1998;62:379-433.
9. Blocker A, Gounon P, Larquet E, et al. The tripartite type III secretion of Shigelle flexneri inserts IpaB and IpaC into host membranes. J Cell Biol 1999;147:683-93.
10. Kubori T. Matsushima Y, Nakamura D, et al. Supramolecular structure of the Salmonella typhimurium type III secretion system. Science 1998;280:602-05.
11. Knutton S, Rosenshine I, Pallen MJ, et al. A novel EspA-associated surface organelle of enteropathogenic Escherichia involved in protein translocation into epithelial cells. EMBO J 1998;17:2166-76
12. Bäumler A, Tsolis RM, Heffron F. Contribution of fimbrial operons to attachment to and invasion of epithelial cell lines by Salmonella typhimurium. Infect Immun 1996;64:1862-65.
13. Ohl ME, Miller SI. Salmonella: A model for bacterial pathogenesis. Annu Rev Med 2001.52:259-74.
14. Collazo CM, Galan JE. The invasion associated type III protein secretion system in Salmonella - a review. Gene 1997;192:51-9.
15. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998;279:509-14.
16. Chen LM, Hobbie S, Galan JE. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear response. Science 1996;274:2115-18.
17. Criss AK, Ahlgreen DM, Jou TS, McCormick BA, Casanova JE. The GTPas Rac1 selectively regulates Salmonella invasion at the apical side of polarized epithelial cells. J Cell Sci 2001;114:1331-41.
18. Wood MW, Rosqvist R, Mullan PB, Edwards MH, Galyov EE. SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via sip-dependent mechanism and promotes bacterial entry. Mol Microbiol 1996;22:327-38.
19. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998;93:815-26.
20. Rudolph MG, Weise C, Mirold S, et al. Biochemical analysis of SopE from Salmonella typhimurium, a highly efficent guanosine nucleotide exchange factor for RhoGTPases. J Biol Chem 1999;274:30501-509.
21. Bakshi CS, Singh VP, Wood MW, Jones PW, Wallis TS, Galyov EE. Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE2 and involved in bacterial invasion of epithelial cells. J Bacteriol 2000;182:2341-44.
22. Stender S, Friebel A, Lindner S, Rhode M, Mirold S, Hardt WD. Identification of SopE2 from Salmonella typhimurium a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol 2000;36:1206-21.
23. Zhou D, Mooseker MS, Galan JE. Role of the S. typhimurium acting-binding protein SipA in bacterial internalization. Science 1999;283:2092-95.
24. Hayward RD, Koronakis V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. EMBO 1999;18:4926-34.
25. Bennish, ML 1991. Potentially lethal complications of Shigellosis. Rev Infect Dis 13:319-24.
26. Sansonetti PJ. Microbes and microbial toxins: Paradigms for microbial-mucosal interactions. III. Shigellosis: from symptoms to molecular basis. Am J Physiol Gastrointes Liver Physiol 2001;280:G319-G323.
27. Maurelli AT, Baudry B, D'Hautville H, Hale TL, Sansonetti PJ. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella felxneri. Infect Immun 1985;49:164-71.
28. Mounier, J, Vasselon R, Hellio M, Lesourd N, Sansonetti PJ. Shigella enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect Immun 1992;60:237-48.
29. Sansonetti PJ, Phalipon A. M cells as ports of entry for entero-invasive pathogens: mechanisms of interaction, consequences for the disease process. Semin Immunol 1999;11:193-203.
30. Sakaguchi T, Köhler H, Gu X, McCormick BA, Reinecker HC. Shigella flexneri Regulates Tight Junction associated Proteins in Human Intestinal Epithelial Cells. Cell Microbiol 2002;4:367-81.
31. Watari M, Funato S, Sasakawa C. Interaction of Ipa proteins of Shigella flexneri with alpha5beta1 integrin promotes entry of the bacteria into mammalian cells. J Exp Med 1996;183:991-99.
32. Skoudy A. J. Mounier A. Aruffo H, et al. CD44 binds to the Shigella IpaB protein and participates in bacterial invasion of epithelial cells. Cell Micobiol 2000;2:19-33.
33. Parsot C, Sansonetti PJ. Invasion and pathogenesis of Shigella infections. Curr Top Microbiol Immunol 1996;209:25-42.
34. Köhler H, Rodrigues SP, McCormick BA. Shigella flexneri interactions with the basolateral membrane domain of polarized model intestinal epithelium: Role of lipopolysaccharide in cell invasion and in activation of the mitogen-activated protein kinase ERK. Infect Immun 2002;70:1150-58.
35. Tran Van Nhieu G, Caron E, Hall A, Sansonetti PJ. IpaC determines filopodia formation during Shigella entry into epithelial cells. EMBO J 1999;18:3249-62.
36. Adam T, Arpin M, Prévost MC, Gounon P, Sansonetti PJ. Cytoskeletal rearrangements and the functional role of T-plastin during entry of Shigelle flexneri into HeLa cells. J Cell Biol 1995;129:367-81.
37. c-srcmediated signaling pathway. EMBO J 1995;14:2471-482.
38. Tran van Nhieu G, Ben Ze'ev A, Sansonetti PJ. Modulation of bacterial in epithelial cells by association between vinculin and the Shigella IpaA invasin. EMBO J 1997;16:2717-729.
39. Bourdet-Sicard R, Rudiger M, Sansonettei PJ, Tran Van Nhieu G. Vinculin is unfolded by the Shigella protein IpaA, and the complex promotes F-actin depolymerization. EMBO J 1999;18:5853-862.
40. Fagundes-Neto U, Scaletsky IC. The gut at war: the consequences of enteropathogenic Escherichia coli infection as a factor of diarrhea and malnutrition. Sao Paulo Med J 2000;118:21-9.
41. Donnerberg MS, Kaper JB. Enteropathogenic Escherichia coli. Infect Immun 1992;60:3953-61.
42. Celli J, Deng W, Finlay BB. Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cytoskeleton from the outside. Cell Microbiol 2000;2;1-9.
43. Hecht G. Microbes and Microbial Toxins: Paradigms for Microbial-Mucosal Interaction VII. Enteropathogenic Escheria coli: physiological alterations from an extracellular position. Am J Physiol Gastrointest Liver Physiol 2001;281:G1-G7.
44. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB. Enteropthogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 1997;91:511-20.
45. Deibel C, Kramer S, Chakraborty T, Ebel F. EspE, a novel secreted protein of attaching and effacing bacterial, is directly translocated into effected host cells, where it appears as a tyrosine-phosphorylated 90kDa protein. Mol Microbiol 1998;28:463-74.
46. Frankel G, Lider O, Hershkoviz R, et al. The cell-binding domain of intimin from enteropathogenic Escherichia coli binds to β1 integrins. J Biol Chem 1996;271:20359-364.
47. Todiriki K, Mukai T, Sato S, Toba T. Inhibition of adhesion of food-borne pathogens to Caco-2 cells by Lactobacillus strains. J Appl Microbiol 2001;91:154-59.
48. Bernet MF, Brassart D, Neeser JR, Servin AL. Lactobacillus acidophilus LA1 binds to cultured human intestinla cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 1994;35:483-89.
49. Ouwehand A, Conway P. Specificity of spent culture fluids of Lactobacillus spp. to inhibit adhesion of enteropathogenic fimbriated Escherichia coli cells. Microbiol Ecol Health Dis 1996;9:239-46.
50. Köhler H, Rodrigues SP, Maurelli AT, McCormick BA. Piperidine, a metabolite of the intestinal microflora, inhibits Salmonella typhimurium enteropathogenicity. J Infec Dis 2002;186:1122-30.
51. Mack DR, Michail S, Wei S, McDougall L, Hollingsworth MA. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. Am J Physiol Gastrointest Liver Physiol 1999;276:G941-G950.
52. Nanthakumar NN, Dai D, Newburg DS, Walker WA. The role of indigenous microflora on the development of the murine gut. FASEB 2002. (In press)
53. Madara JL. Regulation of the movements of solutes across tight junctions. Annu Rev Physiol 1998;60:143-59.
54. Mitic, LL, Anderson JM. Molecular architecture of tight junctions. Annu Rev Physiol 1998;60:121-42.
55. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 1998;141:1539-50.
56. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 1993;123:1777-88.
57. Anderson JM. Cell signalling: MAGUK magic. Curr Biol 1996;6:382-84.
58. Jesaitis LA, Goodenough DA. Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs-large tumor suppressor protein. J Cell Biol 1994:124:949-61.
59. Gumbiner B. Generation and maintenance of epithelial cell polarity. Curr Opin Cell Biol 1990;2881-57.
60. Gumbiner BM. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 1996;84:345-57.
61. Sears LC. Molecular physiology and pathophysiology of tight junctions. V. Assault of the tight junctions by enteric pathogens. Am J Pysiol Gastrointest Liver Physiol 2000;279:G1129-G1134.
62. Sears CL, Kaper JB. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol Rev 1996;60:167-15.
63. Gerhardt R, Schmidt G, Hofman F, Aktories K. Activation of Rho GTPases by Escherichia coli cytotoxic necrotizing factor 1 increases intestinal permeability in Caco-2 cells. Infect Immun 1998;66:5125-31.
64. Sonoda N, Furuse M, Sasaki H, et al. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: Evidence for direct involvement of claudins in tight junction barrier. Cell Biol 1999;147:195-204.
65. Simonovic I, Rosenberg J, Koutsouris A, Hecht G. Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol. 2000;2:305-15.
66. McNamara BP, Koutsouris A, O'Connell CB, Nougayrede JP, Donnenberg MS, Hecht G Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J Clin Invest 2001;107:621-9.
67. Tafazoli F, Holmstrom A, Forsberg A, Magnusson KE. Apically exposed, tight junction-associated beta1-integrins allow binding and YopE-mediated perturbation of epithelial barriers by wild-type Yersinia bacteria. Infect Immun 2000 Sep;68:5335-43.
68. Yuhan R, Koutsouris A, Savkovic SD, Hecht G. Enteropathogenic Escherichia coli-induced myosin light chain phosphorylation alters intestinal epithelial permeability. Gastroenterology 1997;113:1873-82.
69. Chen ML, Pothoulakis C, LaMont JT. Protein kinase C signaling regulates ZO-1 translocation and increased paracellular flux of T84 colonocytes exposed to clostridium difficile Toxin A. J Biol Chem 2002;277:4247-54.
70. Jepson MA, Collares-Buzato CB, Clark MA, Hirst BH, Simmons NL. Rapid disruption of epithelial barrier function by Salmonella typhimurium is associated with structural modification of intercellular junctions. Infect Immun 1995 Jan;63:356-59.
71. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001:291:881-84.
72. Mangell P, Nejdfors P, Wang M, Ahrne S, Weström B, Thorlacius H, Jeppson B. Lactobacillus plantarum 299v inhibits Escherichia coli-induced intestinal permaebility. Dig Dis Sci 2002;47:511-16.
73. Madsen K, Cornish A, Soper P, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology 2001;121:580-91.
74. McCormick BA, Hofman PM, Kim J, Carnes DK, Miller SI, Madara JL. Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J Cell Biol 1995;131:1599-1608.
75. McCormick BA, Parkos CA, Colgan SP, Carnes DK, Madara JL. Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J Immunol 1998;160:455-66.
76. McCormick BA, Colgan SP, Archer CD, Miller SI, Madara JL. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 1993;123:895-907.
77. Hayashi F, Smith KD, Ozinsky O, Hawn TR, Yi, EC, Goodlet DR, Eng JK, Akira S, Underhill DA, Aderem A. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001;410:1099-1103.
78. Gewirtz AT, Novas T A, Lyons S, Godowski PJ, Madara JL. Cutting Edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory genes expression. J Immunol 2001;167:1882-85.
79. Criss, AK, Silva M, Casanova JE, McCormick BA. Regulation of Salmonella-induced neutrophil migration by epithelial ADP-ribosylation factor 6. J Biol Chem 2001;276:48431-439.
80. Gewirtz AT, Siber AM, Madara JL, McCormick BA. Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect Immun 1999;67:608-17.
81. Lee CA, Silva M, Siber AM, Kelly AJ, Galyov E, McCormick BA. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci USA 2000;97:12283-288.
82. Savcovic S, Koutsouris A, Hecht G. Attachement of a non-invasive enteric pathogen enteropthogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration f neutrophils. Infect Immun 1996;64:4480-87.
83. Steiner TS, Nataro JP, Poteet-Smith CE, Smith JA, Guerrant RL. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J Clin Invest;105:1769-77.
84. Aderem A, Ulevitch RJ. Toll-like receptors in the induction of innate immune response. Nature 2000;406:782-87.
85. Cario E, Rosenberg IM, Brandwein SL, Bech PL, Reinecker HC, Podolsky DK. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol 2000;164:966-72.
86. Philpott DJ, Yamaokao S, Israël A, Sansonetti PJ. Invasive Shigella flexneri activates NF-κB through a lipopolysaccharide-dependent innate intracellular response and leads to IL-8 expression in epithelial cells. J Immunol 2000;165:903-14.
87. Hornef MW, Frisan T, Vandewalle A, Normark S, Richter-Dahlfors A. Toll-like receptor 4 resides in the Golgi apparatus and colocalizes with internalized lipopolysaccharide in intestinal epithelial cells. J Exp Med 2002;195:559-70.
88. Girardin SE, Toumebize R, Mavris M, et al. CARD4/NOD1 mediates NF-κB and JNK activation by invasive Shigella flexneri. EMBO Rep 2001:2:736-42.
89. Sandlin RC, Goldberg MB, Maurelli AT. Effect of O-side chain length and composition on the virulence of Shigella flexneri 2a. Mol Microbiol 1996;22:63-73.
90. Sandlin RC, Lampel KA, Keasler SP, Goldberg MB, Stolzer L, Maurelli AT. Avirulence of rough mutants of Shigella flexneri: Requirement of O Antigen for correct unipolar localization of icsA in the bacterial outer membrane. Infect Immun 1995;63:229-37.
91. Bernardini ML, Mounier J, d'Hauteville H, Coquis-Rondon M, Sansonetti PJ. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction of F-actin. Proc Natl Acad Sci USA 1989;86:3867-871.
92. Vasselon T, Mounier J, Hellio R, Sansonetti PJ. Movement along actin filaments of the perijunctional area and de novo polymerization of cellular actin are required for Shigella flexneri colonization of epithelial Caco-2 cell monolayers. Infect Immunol 1992;60:1031-40.
93. Sansonetti, PJ, Arondel J, Fontaine A, d'Hauteville, H, Bernardini ML. OmpB (osmo-regulation) and icsA (cell to cell spread) mutants of Shigella flexneri: Vaccine candidates and probes to study the pathogenesis of shigellosis. Vaccine 1991;9:416-22.
94. Vasselon T, Mounier J, Prevost MC, Hellio R, Sansonetti PJ. Stress fiber-based movement of Shigella flexneri within cells. Infect Immunol 1991;59:1723-732
95. Fernandez IM, Silva M, Schuch R, Walker WA, Siber AM, Maurelli AT, McCormick BA. Cadaverine prevents the escape of Shigella flexneri from the phagolysosome: A connection between bacterial dissemination and neutrophil transepithelial signaling. J Infect Dis 2001;184:743-53.
96. Perdomo, JJ, Gounon P, Sansonetti PJ. Polymorphonuclear leukocyte transmigration promotes invasion of colonic epithelial monolayer by Shigella flexneri. J Clin Invest 1994;93:633-43.
97. Hurley BP, Thorpe CM, Acheson DW. Shiga toxin across intestinal epithelial cells in enhanced by neutrophil transmigration. Infect Immun 2001;69:6148-155.
98. Rembacken BJ, Snelling AM, Hawkey PM, Chalmers DM, Axon AT. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 1999;354:635-39.
99. Campieri M, Gionechetti P. Probiotics in inflammatory bowel disease; new insight to pathogenesis or a possible therapeutic alternative. Gastroenterology 1998;116;1246-60.
100. Neish AS, Gewirtz AT, Zeng H et al. Prokaryotic regulation of epithelial responses by inhibition of IκB-α ubiquination. Science 2000;289:1560-63.
101. Xavier RJ, Podolsky DK. How to get along-Friendly microbes in a hostile world. Science 2000;289:1483-84.
102. Maurelli AT, Fernandez RE, Bloch CA, Rode CK, Fasano A. 'Black holes' and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci USA 1998;95:3943-8.
103. Vidal K, Donnet-Hughes A, Granato D. Lipoteichoic acids from Lactobacillus strain La1 and Lactobacillus acidophillus strain La10 antagonize responsiveness of human intestinal epithelial HT29 cells to lipopolysaccharide. Infect Immun 2002:70:2065-3002.
104. Elliot SJ, O'Connel CB, Kotsouris A, et al. A gene from the locus enterocyte effacement that is required for enteropathenic Escherichia coli to increase tight-junction permeability encodes a chaperone for EspF. Infect Immun 2002;70:2271-77.
105. Fagarasan S, Muramatsu M, Suzuki K, Nagaoka, Hiai H, Honjo T. Critical roles of activation-induced cytidine deaminase in the hemostasis of gut flora. Science 2002;298:1424-27.