Detergent-resistant microdomains mediate activation of host cell signaling in response to attaching-effacing bacteria

Laboratory Investigation

Volumn 90, Issue 2, 2010, Pages 266-281

  Shen Tu, Grace ^a,b   Schauer, David B ^c   Jones, Nicola L ^a,b,d   Sherman, Philip M ^a,b,d  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Citrobacter rodentium; Colonic epithelial cell hyperplasia; Enterohemorrhagic Escherichia coli O157:H7; Lipid rafts; Microbial host interaction; Phosphoinositide 3 kinase

Indexed keywords

CAVEOLIN; CHOLESTEROL; INTIMIN; PHOSPHATIDYLINOSITOL 3 KINASE; VEROTOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTACHING EFFACING BACTERIA; BACTERIAL COLONIZATION; BACTERIUM; CITROBACTER RODENTIUM; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; EPITHELIUM CELL; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID RAFT; MOUSE; NIEMANN PICK DISEASE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ULTRACENTRIFUGATION;

EID: 75949124397     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.131     Document Type: Article

References (78)

1. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004;2:123-140.
2. Jandu N, Shen S, Wickham ME, et al. Multiple seropathotypes of verotoxin-producing Escherichia coli (VTEC) disrupt interferon-gamma-induced tyrosine phosphorylation of signal transducer and activator of transcription (Stat)-1. Microb Pathog 2007;42:62-71.
3. Cooley M, Carychao D, Crawford-Miksza L, et al. Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California. PLoS ONE 2007;2:e1159.
4. Rendon MA, Saldana Z, Erdem AL, et al. Commensal and pathogenic Escherichia coli use a common pilus adherence factor for epithelial cell colonization. Proc Natl Acad Sci USA 2007;104:10637-10642.
5. Nutikka A, Lingwood C. Generation of receptor-active, globotriaosyl ceramide/cholesterol lipid 'rafts' in vitro: a new assay to define factors affecting glycosphingolipid receptor activity. Glycoconj J 2004;20:33-38.
6. Gobert AP, Vareille M, Glasser AL, et al. Shiga toxin produced by enterohemorrhagic Escherichia coli inhibits PI3K/NF-kappaB signaling pathway in globotriaosylceramide-3-negative human intestinal epithelial cells. J Immunol 2007;178:8168-8174.
7. Gyles CL. Shiga toxin-producing Escherichia coli: an overview. J Anim Sci 2007;85(13 Suppl):E45-E62.
8. Welinder-Olsson C, Kaijser B. Enterohemorrhagic Escherichia coli (EHEC). Scand J Infect Dis 2005;37:405-416.
9. Campellone KG, Robbins D, Leong JM. EspFU is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell 2004;7:217-228.
10. Mundy R, MacDonald TT, Dougan G, et al. Citrobacter rodentium of mice and man. Cell Microbiol 2005;7:1697-1706.
11. Allen-Vercoe E, Waddell B, Livingstone S, et al. Enteropathogenic Escherichia coli Tir translocation and pedestal formation requires membrane cholesterol in the absence of bundle-forming pili. Cell Microbiol 2006;8:613-624.
12. Zobiack N, Rescher U, Laarmann S, et al. Cell-surface attachment of pedestal-forming enteropathogenic E. coli induces a clustering of raft components and a recruitment of annexin 2. J Cell Sci 2002;115 (Part 1):91-98.
13. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000;1:31-39.
14. Brown DA, London E. Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 1998;14:111-136.
15. Fielding CJ, Fielding PE. Membrane cholesterol and the regulation of signal transduction. Biochem Soc Trans 2004;32(Part 1):65-69.
16. Laude AJ, Prior IA. Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol 2004;21:193-205.
17. Ceponis PJ, McKay DM, Ching JC, et al. Enterohemorrhagic Escherichia coli O157:H7 disrupts Stat1-mediated gamma interferon signal transduction in epithelial cells. Infect Immun 2003;71:1396-1404.
18. Jandu N, Ceponis PJ, Kato S, et al. Conditioned medium from enterohemorrhagic Escherichia coli-infected T84 cells inhibits signal transducer and activator of transcription 1 activation by gamma interferon. Infect Immun 2006;74:1809-1818.
19. Kilsdonk EP, Yancey PG, Stoudt GW, et al. Cellular cholesterol efflux mediated by cyclodextrins. J Biol Chem 1995;270:17250-17256.
20. Riff JD, Callahan JW, Sherman PM. Cholesterol-enriched membrane microdomains are required for inducing host cell cytoskeleton rearrangements in response to attaching-effacing Escherichia coli. Infect Immun 2005;73:7113-7125.
21. Johnson-Henry K, Wallace JL, Basappa NS, et al. Inhibition of attaching and effacing lesion formation following enteropathogenic Escherichia coli and Shiga toxin-producing E. coli infection. Infect Immun 2001;69:7152-7158.
22. Schraw W, Li Y, McClain MS, et al. Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J Biol Chem 2002;277: 34642-34650.
23. Song KS, Li S, Okamoto T, et al. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 1996;271:9690-9697.
24. Macdonald JL, Pike LJ. A simplified method for the preparation of detergent-free lipid rafts. J Lipid Res 2005;46:1061-1067.
25. Hatano T, Kubo S, Imai S, et al. Leucine-rich repeat kinase 2 associates with lipid rafts. Hum Mol Genet 2007;16:678-690.
26. Dennis A, Kudo T, Kruidenier L, et al. The p50 subunit of NF-kappaB is critical for in vivo clearance of the noninvasive enteric pathogen Citrobacter rodentium. Infect Immun 2008;76:4978-4988.
27. Johnson-Henry KC, Nadjafi M, Avitzur Y, et al. Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J Infect Dis 2005;191:2106-2117.
28. Mogilner JG, Srugo I, Lurie M, et al. Effect of probiotics on intestinal regrowth and bacterial translocation after massive small bowel resection in a rat. J Pediatr Surg 2007;42:1365-1371.
29. Kubo M, Li TS, Suzuki R, et al. Hypoxic preconditioning increases survival and angiogenic potency of peripheral blood mononuclear cells via oxidative stress resistance. Am J Physiol Heart Circ Physiol 2008;294:H590-H595.
30. Jones NL, Day AS, Jennings H, et al. Enhanced disease severity in Helicobacter pylori-infected mice deficient in Fas signaling. Infect Immun 2002;70:2591-2597.
31. Bewick V, Cheek L, Ball J. Statistics review 9: one-way analysis of variance. Crit Care 2004;8:130-136. (Pubitemid 38436421)
32. Cole LE, Shirey KA, Barry E, et al. Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect Immun 2007;75:4127-4137.
33. Shen S, Mascarenhas M, Rahn K, et al. Evidence for a hybrid genomic island in verocytotoxin-producing Escherichia coli CL3 (serotype O113:H21) containing segments of EDL933 (serotype O157:H7) O islands 122 and 48. Infect Immun 2004;72:1496-1503.
34. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002;296:1655-1657.
35. Borenshtein D, McBee ME, Schauer DB. Utility of the Citrobacter rodentium infection model in laboratory mice. Curr Opin Gastroenterol 2008;24:32-37.
36. Higgins LM, Frankel G, Douce G, et al. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect Immun 1999;67:3031-3039.
37. Chen CC, Louie S, McCormick B, et al. Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice. Infect Immun 2005;73:5468-5481.
38. Ismaili A, Philpott DJ, Dytoc MT, et al. Signal transduction responses following adhesion of verocytotoxin-producing Escherichia coli. Infect Immun 1995;63:3316-3326.
39. Shaner NC, Sanger JW, Sanger JM. Actin and alpha-actinin dynamics in the adhesion and motility of EPEC and EHEC on host cells. Cell Motil Cytoskeleton 2005;60:104-120.
40. Philpott DJ, McKay DM, Mak W, et al. Signal transduction pathways involved in enterohemorrhagic Escherichia coli-induced alterations in T84 epithelial permeability. Infect Immun 1998;66:1680-1687.
41. Pizarro-Cerda J, Cossart P. Bacterial adhesion and entry into host cells. Cell 2006;124:715-727.
42. Kierbel A, Gassama-Diagne A, Rocha C, et al. Pseudomonas aeruginosa exploits a PIP3-dependent pathway to transform apical into basolateral membrane. J Cell Biol 2007;177:21-27.
43. Kierbel A, Gassama-Diagne A, Mostov K, et al. The phosphoinositol-3- kinase-protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol Biol Cell 2005;16:2577-2585.
44. Wiles TJ, Dhakal BK, Eto DS, et al. Inactivation of host Akt/protein kinase B signaling by bacterial pore-forming toxins. Mol Biol Cell 2008;19:1427-1438.
45. Edwards JL, Apicella MA. Neisseria gonorrhoeae PLD directly interacts with Akt kinase upon infection of primary, human, cervical epithelial cells. Cell Microbiol 2006;8:1253-1271.
46. Bosse T, Ehinger J, Czuchra A, et al. Cdc42 and phosphoinositide 3-kinase drive Rac-mediated actin polymerization downstream of c-Met in distinct and common pathways. Mol Cell Biol 2007;27: 6615-6628.
47. Takenouchi H, Kiyokawa N, Taguchi T, et al. Shiga toxin binding to globotriaosyl ceramide induces intracellular signals that mediate cytoskeleton remodeling in human renal carcinoma-derived cells. J Cell Sci 2004;117(Part 17):3911-3922.
48. Tang CH, Lu DY, Yang RS, et al. Leptin-induced IL-6 production is mediated by leptin receptor, insulin receptor substrate-1, phosphatidylinositol 3-kinase, Akt, NF-kappaB, and p300 pathway in microglia. J Immunol 2007;179:1292-1302.
49. Guttman JA, Li Y, Wickham ME, et al. Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell Microbiol 2006;8:634-645.
50. Sason H, Milgrom M, Weiss AM, 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.
51. Robinson CM, Sinclair JF, Smith MJ, et al. Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc Natl Acad Sci USA 2006;103:9667-9672.
52. Proulx F, Seidman EG, Karpman D. Pathogenesis of Shiga toxin-associated hemolytic uremic syndrome. Pediatr Res 2001;50:163-171.
53. Absi M, Burnham MP, Weston AH, et al. Effects of methyl beta-cyclodextrin on EDHF responses in pig and rat arteries; association between SK(Ca) channels and caveolin-rich domains. Br J Pharmacol 2007;151:332-340.
54. Marbeuf-Gueye C, Stierle V, Sudwan P, et al. Perturbation of membrane microdomains in GLC4 multidrug-resistant lung cancer cells-modification of ABCC1 (MRP1) localization and functionality. FEBS J 2007;274:1470-1480.
55. Goluszko P, Nowicki B. Membrane cholesterol: a crucial molecule affecting interactions of microbial pathogens with mammalian cells. Infect Immun 2005;73:7791-7796.
56. Lafont F, van der Goot FG. Bacterial invasion via lipid rafts. Cell Microbiol 2005;7:613-620.
57. Catron DM, Sylvester MD, Lange Y, et al. The salmonella-containing vacuole is a major site of intracellular cholesterol accumulation and recruits the GPI-anchored protein CD55. Cell Microbiol 2002;4:315-328.
58. Lafont F, Tran Van Nhieu G, Hanada K, et al. Initial steps of Shigella infection depend on the cholesterol/sphingolipid raft-mediated CD44-IpaB interaction. EMBO J 2002;21:4449-4457.
59. Watarai M, Makino S, Michikawa M, et al. Macrophage plasma membrane cholesterol contributes to Brucella abortus infection of mice. Infect Immun 2002;70:4818-4825.
60. Kansau I, Berger C, Hospital M, 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;72:3733-3742.
61. Knodler LA, Vallance BA, Hensel M, et al. Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol Microbiol 2003;49:685-704.
62. Hayward RD, Cain RJ, McGhie EJ, et al. Cholesterol binding by the bacterial type III translocon is essential for virulence effector delivery into mammalian cells. Mol Microbiol 2005;56:590-603.
63. Chang TY, Reid PC, Sugii S, et al. Niemann-Pick type C disease and intracellular cholesterol trafficking. J Biol Chem 2005;280:20917-20920.
64. Liscum L, Sturley SL. Intracellular trafficking of Niemann-Pick C proteins 1 and 2: obligate components of subcellular lipid transport. Biochim Biophys Acta 2004;1685:22-27.
65. Mukherjee S, Maxfield FR. Lipid and cholesterol trafficking in NPC. Biochim Biophys Acta 2004;1685:28-37.
66. Garver WS, Krishnan K, Gallagos JR, et al. Niemann-Pick C1 protein regulates cholesterol transport to the trans-Golgi network and plasma membrane caveolae. J Lipid Res 2002;43:579-589.
67. Mundy R, Pickard D, Wilson RK, et al. Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol Microbiol 2003;48:795-809.
68. Schauer DB, Falkow S. The eae gene of Citrobacter freundii biotype 4280 is necessary for colonization in transmissible murine colonic hyperplasia. Infect Immun 1993;61:4654-4661. (Pubitemid 23320518)
69. van der Goot FG, Tran van Nhieu G, Allaoui A, et al. Rafts can trigger contact-mediated secretion of bacterial effectors via a lipid-based mechanism. J Biol Chem 2004;279:47792-47798.
70. Wiles S, Clare S, Harker J, et al. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen Citrobacter rodentium. Cell Microbiol 2004;6:963-972.
71. Gruenheid S, Sekirov I, Thomas NA, et al. Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 2004;51:1233-1249.
72. Mundy R, Petrovska L, Smollett K, et al. Identification of a novel Citrobacter rodentium type III secreted protein, EspI, and roles of this and other secreted proteins in infection. Infect Immun 2004;72:2288-2302.
73. Hansen KK, Sherman PM, Cellars L, et al. A major role for proteolytic activity and proteinase-activated receptor-2 in the pathogenesis of infectious colitis. Proc Natl Acad Sci USA 2005;102:8363-8368.
74. Artis D, Potten CS, Else KJ, et al. Trichuris muris: host intestinal epithelial cell hyperproliferation during chronic infection is regulated by interferon-gamma. Exp Parasitol 1999;92:144-153.
75. O'Garra A, Vieira PL, Vieira P, et al. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J Clin Invest 2004;114:1372-1378.
76. Powrie F. Immune regulation in the intestine: a balancing act between effector and regulatory T cell responses. Ann N Y Acad Sci 2004;1029:132-141.
77. McKay DM. The beneficial helminth parasite? Parasitology 2006;132(Part 1):1-12.
78. Reardon C, Sanchez A, Hogaboam CM, et al. Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect Immun 2001;69:4417-4423.