Citrobacter rodentium infection induces MyD88-dependent formation of ubiquitinated protein aggregates in the intestinal epithelium

Journal of Innate Immunity

Volumn 3, Issue 1, 2011, Pages 83-98

  Kaniuk, Natalia A ^a   Lam, Grace Y ^a,c   Ma, Caixia ^d   Galindo Mata, Esther ^a   Jones, Nicola ^a,b,c   Vallance, Bruce A ^d,e   Brumell, John H ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d BC CHILDREN S HOSPITAL   (Canada)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Bacterial infection; Innate immunity; MyD88; NADPH oxidase; Protein ubiquitination

Indexed keywords

INTIMIN RECEPTOR; MYELOID DIFFERENTIATION FACTOR 88; REACTIVE OXYGEN METABOLITE; RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; CITROBACTER RODENTIUM; CONTROLLED STUDY; ENTEROBACTERIACEAE INFECTION; HELICOBACTER INFECTION; HOST CELL; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; STOMACH; TYPE III SECRETION SYSTEM; UBIQUITINATION;

ANIMALS; BACTERIAL LOAD; CELL LINE; CITROBACTER RODENTIUM; COLON; ENTEROBACTERIACEAE INFECTIONS; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; NADH, NADPH OXIDOREDUCTASES; UBIQUITINATED PROTEINS;

EID: 78650516522     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000320644     Document Type: Article

References (64)

1. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S: Citrobacter rodentium of mice and man. Cell Microbiol 2005;7:1697-1706.
2. Vallance BA, Finlay BB: Exploitation of host cells by enteropathogenic Escherichia coli. Proc Natl Acad Sci USA 2000;97:8799-8806.
3. Deng W, Li Y, Vallance BA, Finlay BB: Locus of enterocyte effacement from citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect Immun 2001;69:6323-6335.
4. Donnenberg MS, Whittam TS: Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J Clin Invest 2001;107:539-548.
5. Dean P, Kenny B: Intestinal barrier dysfunction by enteropathogenic Escherichia coli is mediated by two effector molecules and a bacterial surface protein. Mol Microbiol 2004;54:665-675.
6. Gruenheid S, Finlay BB: Microbial pathogenesis and cytoskeletal function. Nature 2003;422:775-781.
7. Rosenshine I, Ruschkowski S, Stein M, Reinscheid DJ, Mills SD, Finlay BB: A pathogenic bacterium triggers epithelial signals to form a functional bacterial receptor that mediates actin pseudopod formation. EMBO J 1996;15:2613-2624.
8. Ma C, Wickham ME, Guttman JA, Deng W, Walker J, Madsen KL, Jacobson K, Vogl WA, Finlay BB, Vallance BA: Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cell Microbiol 2006;8:1669-1686.
9. Mundy R, Pickard D, Wilson RK, Simmons CP, Dougan G, Frankel G: Identification of a novel type IV pilus gene cluster required for gastrointestinal colonization of Citrobacter rodentium. Mol Microbiol 2003;48:795-809.
10. Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, Vazquez A, Barba J, Ibarra JA, O'Donnell P, Metalnikov P, Ashman K, Lee S, Goode D, Pawson T, Finlay BB: Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 2004;101:3597-3602.
11. Crane JK, McNamara BP, Donnenberg MS: Role of ESPF in host cell death induced by enteropathogenic Escherichia coli. Cell Microbiol 2001;3:197-211.
12. Higgins LM, Frankel G, Douce G, Dougan G, MacDonald TT: 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.
13. Luperchio SA, Schauer DB: Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect 2001;3:333-340.
14. Guttman JA, Samji FN, Li Y, Deng W, Lin A, Finlay BB: Aquaporins contribute to diarrhoea caused by attaching and effacing bacterial pathogens. Cell Microbiol 2007;9:131-141.
15. Deng W, Vallance BA, Li Y, Puente JL, Finlay BB: Citrobacter rodentium translocated intimin receptor (Tir) is an essential virulence factor needed for actin condensation, intestinal colonization and colonic hyperplasia in mice. Mol Microbiol 2003;48:95-115.
16. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB: Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of enterobacteriaceae. Cell Host Microbe 2007;2:119-129.
17. Wiles S, Clare S, Harker J, Huett A, Young D, Dougan G, Frankel G: Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen citrobacter rodentium. Cell Microbiol 2004;6:963-972.
18. Abreu MT: Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol;10:131-144.
19. Eckmann L: Innate immunity and mucosal bacterial interactions in the intestine. Curr Opin Gastroenterol 2004;20:82-88.
20. Diacovich L, Gorvel JP: Bacterial manipulation of innate immunity to promote infection. Nat Rev Microbiol;8:117-128.
21. Rumbo M, Nempont C, Kraehenbuhl JP, Sirard JC: Mucosal interplay among commensal and pathogenic bacteria: lessons from flagellin and Toll-like receptor 5. FEBS Lett 2006;580:2976-2984.
22. Gibson DL, Ma C, Rosenberger CM, Bergstrom KS, Valdez Y, Huang JT, Khan MA, Vallance BA: Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell Microbiol 2008;10:388-403.
23. Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, Finlay BB, Vallance BA: Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect Immun 2006;74:2522-2536.
24. Kawai T, Akira S: TLR signaling. Cell Death Differ 2006;13:816-825.
25. Oda K, Kitano H: A comprehensive map of the Toll-like receptor signaling network. Mol Syst Biol 2006;2:2006.0015.
26. Gibson DL, Ma C, Bergstrom KS, Huang JT, Man C, Vallance BA: Myd88 signalling plays a critical role in host defence by controlling pathogen burden and promoting epithelial cell homeostasis during Citrobacter rodentium-induced colitis. Cell Microbiol 2008;10:618-631.
27. Vallance BA, Deng W, De Grado M, Chan C, Jacobson K, Finlay BB: Modulation of inducible nitric oxide synthase expression by the attaching and effacing bacterial pathogen Citrobacter rodentium in infected mice. Infect Immun 2002;70:6424-6435.
28. Szanto I, Rubbia-Brandt L, Kiss P, Steger K, Banfi B, Kovari E, Herrmann F, Hadengue A, Krause KH: Expression of NOX1, a superoxidegenerating NADPH oxidase, in colon cancer and inflammatory bowel disease. J Pathol 2005;207:164-176.
29. Geiszt M, Lekstrom K, Brenner S, Hewitt SM, Dana R, Malech HL, Leto TL: NAD (P) H oxidase 1, a product of differentiated colon epithelial cells, can partially replace glycoprotein 91phox in the regulated production of superoxide by phagocytes. J Immunol 2003;171:299-306.
30. Kawahara T, Kuwano Y, Teshima-Kondo S, Takeya R, Sumimoto H, Kishi K, Tsunawaki S, Hirayama T, Rokutan K: Role of nicotinamide adenine dinucleotide phosphate oxidase1 in oxidative burst response to Toll-like receptor 5 signaling in large intestinal epithelial cells. J Immunol 2004;172:3051-3058.
31. Ha EM, Oh CT, Bae YS, Lee WJ: A direct role for dual oxidase in drosophila gut immunity. Science 2005;310:847-850.
32. Canadien V, Tan T, Zilber R, Szeto J, Perrin AJ, Brumell JH: Cutting edge: microbial products elicit formation of dendritic cell aggresomelike induced structures in macrophages. J Immunol 2005;174:2471-2475.
33. Herter S, Osterloh P, Hilf N, Rechtsteiner G, Hohfeld J, Rammensee HG, Schild H: Dendritic cell aggresome-like-induced structure formation and delayed antigen presentation coincide in influenza virus-infected dendritic cells. J Immunol 2005;175:891-898.
34. Lelouard H, Gatti E, Cappello F, Gresser O, Camosseto V, Pierre P: Transient aggregation of ubiquitinated proteins during dendritic cell maturation. Nature 2002;417:177-182.
35. Yewdell JW, Anton LC, Bennink JR: Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules? J Immunol 1996;157:1823-1826.
36. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, Buttgereit F, Bennink JR, Yewdell JW: Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 2003;18:343-354.
37. Kaniuk NA, Kiraly M, Bates H, Vranic M, Volchuk A, Brumell JH: Ubiquitinated-protein aggregates form in pancreatic β-cells during diabetes-induced oxidative stress and are regulated by autophagy. Diabetes 2007;56:930-939.
38. Szeto J, Kaniuk NA, Canadien V, Nisman R, Mizushima N, Yoshimori T, Bazett-Jones DP, Brumell JH: ALIS are stress-induced protein storage compartments for substrates of the proteasome and autophagy. Autophagy 2006;2:189-199.
39. Lelouard H, Ferrand V, Marguet D, Bania J, Camosseto V, David A, Gatti E, Pierre P: Dendritic cell aggresome-like induced structures are dedicated areas for ubiquitination and storage of newly synthesized defective proteins. J Cell Biol 2004;164:667-675.
40. Viala JP, Mochegova SN, Meyer-Morse N, Portnoy DA: A bacterial pore-forming toxin forms aggregates in cells that resemble those associated with neurodegenerative diseases. Cell Microbiol 2008;10:985-993.
41. Ivanov SS, Roy CR: Modulation of ubiquitin dynamics and suppression of DALIS formation by the Legionella pneumophila Dot/Icm system. Cell Microbiol 2009;11:261-278.
42. Raju D, Jones NL: Methods to monitor autophagy in H. pylori vacuolating cytotoxin A (VacA)-treated cells. Autophagy 2010;6:138-143.
43. Fujimuro M, Yokosawa H: Production of antipolyubiquitin monoclonal antibodies and their use for characterization and isolation of polyubiquitinated proteins. Methods Enzymol 2005;399:75-86.
44. Mundy R, Petrovska L, Smollett K, Simpson N, Wilson RK, Yu J, Tu X, Rosenshine I, Clare S, Dougan G, Frankel G: 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.
45. Hardwidge PR, Deng W, Vallance BA, Rodriguez-Escudero I, Cid VJ, Molina M, Finlay BB: Modulation of host cytoskeleton function by the enteropathogenic Escherichia coli and Citrobacter rodentium effector protein EspG. Infect Immun 2005;73:2586-2594.
46. Guttman JA, Samji FN, Li Y, Vogl AW, Finlay BB: Evidence that tight junctions are disrupted due to intimate bacterial contact and not inflammation during attaching and effacing pathogen infection in vivo. Infect Immun 2006;74:6075-6084.
47. Guttman JA, Li Y, Wickham ME, Deng W, Vogl AW, Finlay BB: Attaching and effacing pathogen-induced tight junction disruption in vivo. Cell Microbiol 2006;8:634-645.
48. Mancuso G, Midiri A, Beninati C, Biondo C, Galbo R, Akira S, Henneke P, Golenbock D, Teti G: Dual role of TLR2 and myeloid differentiation factor 88 in a mouse model of invasive group B streptococcal disease. J Immunol 2004;172:6324-6329.
49. Skerrett SJ, Liggitt HD, Hajjar AM, Wilson CB: Cutting edge: Myeloid differentiation factor 88 is essential for pulmonary host defense against Pseudomonas aeruginosa but not Staphylococcus aureus. J Immunol 2004;172:3377-3381.
50. Albiger B, Sandgren A, Katsuragi H, Meyer-Hoffert U, Beiter K, Wartha F, Hornef M, Normark S, Normark BH: Myeloid differentiation factor 88-dependent signalling controls bacterial growth during colonization and systemic pneumococcal disease in mice. Cell Microbiol 2005;7:1603-1615.
51. Nathan C, Shiloh MU: Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci USA 2000;97:8841-8848.
52. Kubes P: Inducible nitric oxide synthase: a little bit of good in all of us. Gut 2000;47:6-9.
53. Ljung T, Herulf M, Beijer E, Jacobsson H, Lundberg J, Finkel Y, Hellstrom PM: Rectal nitric oxide assessment in children with Crohn disease and ulcerative colitis. Indicator of ileocaecal and colorectal affection. Scand J Gastroenterol 2001;36:1073-1076.
54. Perner A, Andresen L, Normark M, Rask-Madsen J: Constitutive expression of inducible nitric oxide synthase in the normal human colonic epithelium. Scand J Gastroenterol 2002;37:944-948.
55. Banfi B, Maturana A, Jaconi S, Arnaudeau S, Laforge T, Sinha B, Ligeti E, Demaurex N, Krause KH: A mammalian H+ channel generated through alternative splicing of the NADPH oxidase homolog NOH-1. Science 2000;287:138-142.
56. Kikuchi H, Hikage M, Miyashita H, Fukumoto M: NADPH oxidase subunit, GP91 (PHOX) homologue, preferentially expressed in human colon epithelial cells. Gene 2000;254:237-243.
57. Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD: Cell transformation by the superoxidegenerating oxidase MOX1. Nature 1999;401:79-82.
58. Kawahara T, Kohjima M, Kuwano Y, Mino H, Teshima-Kondo S, Takeya R, Tsunawaki S, Wada A, Sumimoto H, Rokutan K: Helicobacter pylori lipopolysaccharide activates Rac1 and transcription of NADPH oxidase NOX1 and its organizer NOXO1 in guinea pig gastric mucosal cells. Am J Physiol Cell Physiol 2005;288: C450-C457.
59. Kuwano Y, Kawahara T, Yamamoto H, Teshima-Kondo S, Tominaga K, Masuda K, Kishi K, Morita K, Rokutan K: Interferon-gamma activates transcription of NADPH oxidase 1gene and upregulates production of superoxide anion by human large intestinal epithelial cells. Am J Physiol Cell Physiol 2006;290: C433-C443.
60. Necchi V, Sommi P, Ricci V, Solcia E: In vivo accumulation of helicobacter pylori products, NOD1, ubiquitinated proteins and proteasome in a novel cytoplasmic structure. PLoS One 2010;5: e9716.
61. DeFillipo AM, Dai J, Li Z: Heat shock-induced dendritic cell maturation is coupled by transient aggregation of ubiquitinated proteins independently of heat shock factor 1 or inducible heat shock protein 70. Mol Immunol 2004;41:785-792.
62. Pierre P: Dendritic cells, DRiPs, and DALIS in the control of antigen processing. Immunol Rev 2005;207:184-190.
63. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, Boone D, Eves EM, Rosner MR, Gibbs JS, Embry A, Dolan B, Das S, Hickman HD, Berglund P, Bennink JR, Yewdell JW, Pan T: Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 2009;462:522-526.
64. Fassbender M, Herter S, Holtappels R, Schild H: Correlation of dendritic cell maturation and the formation of aggregates of polyubiquitinated proteins in the cytosol. Med Microbiol Immunol 2008;197:185-189.