Bringing down the host: Enteropathogenic and enterohaemorrhagic Escherichia coli effector-mediated subversion of host innate immune pathways

Cellular Microbiology

Volumn 17, Issue 3, 2015, Pages 318-332

  Santos, Andrew S ^a,b   Finlay, B Brett ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CELL PROTEIN; CYTOKINE; FAS ASSOCIATED DEATH DOMAIN PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE; PATTERN RECOGNITION RECEPTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN; ESCHERICHIA COLI PROTEIN; VIRULENCE FACTOR;

APOPTOSIS; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL DEATH; CELL MEMBRANE; CELL SURVIVAL; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI INFECTION; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; INFLAMMATION; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; TYPE III SECRETION SYSTEM; BACTERIAL SECRETION SYSTEM; IMMUNE EVASION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; MICROBIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL SECRETION SYSTEMS; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNE TOLERANCE; VIRULENCE FACTORS;

EID: 84925248876     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12412     Document Type: Review

References (116)

1. Allen, L.A., and Aderem, A. (1996) Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages. J Exp Med 184: 627-637.
2. Alto, N.M., Weflen, A.W., Rardin, M.J., Yarar, D., Lazar, C.S., Tonikian, R., etal. (2007) The type III effector EspF coordinates membrane trafficking by the spatiotemporal activation of two eukaryotic signaling pathways. J Cell Biol 178: 1265-1278.
3. Anderson, C.L., Shen, L., Eicher, D.M., Wewers, M.D., and Gill, J.K. (1990) Phagocytosis mediated by three distinct Fc gamma receptor classes on human leukocytes. J Exp Med 171: 1333-1345.
4. Arbeloa, A., Blanco, M., Moreira, F.C., Bulgin, R., López, C., Dahbi, G., etal. (2009) Distribution of espM and espT among enteropathogenic and enterohaemorrhagic Escherichia coli. J Med Microbiol 58: 988-995.
5. Arbibe, L., Mira, J.P., Teusch, N., Kline, L., Guha, M., Mackman, N., etal. (2000) Toll-like receptor 2-mediated NF-kappa B activation requires a Rac1-dependent pathway. Nat Immunol 1: 533-540.
6. Baruch, K., Gur-Arie, L., Nadler, C., Koby, S., Yerushalmi, G., Ben-Neriah, Y., etal. (2011) Metalloprotease type III effectors that specifically cleave JNK and NF-κB. EMBO J 30: 221-231.
7. Battle, S.E., Brady, M.J., Vanaja, S.K., Leong, J.M., and Hecht, G.A. (2014) Actin pedestal formation by enterohemorrhagic Escherichia coli enhances bacterial host cell attachment and concomitant type III translocation. Infect Immun 82: 3713-3722.
8. Berger, C.N., Crepin, V.F., Baruch, K., Mousnier, A., Rosenshine, I., and Frankel, G. (2012) EspZ of enteropathogenic and enterohemorrhagic Escherichia coli regulates type III secretion system protein translocation. MBio 3: 1-12.
9. Blasche, S., Mörtl, M., Steuber, H., Siszler, G., Nisa, S., Schwarz, F., etal. (2013) The E. coli effector protein NleF is a caspase inhibitor. PLoS ONE 8: e58937.
10. Bömer, U., Rassow, J., Zufall, N., Pfanner, N., Meijer, M., and Maarse, A.C. (1996) The preprotein translocase of the inner mitochondrial membrane: evolutionary conservation of targeting and assembly of Tim17. J Mol Biol 262: 389-395.
11. Bulgin, R., Raymond, B., Garnett, J.A., Frankel, G., Crepin, V.F., Berger, C.N., and Arbeloa, A. (2010) Bacterial guanine nucleotide exchange factors SopE-like and WxxxE effectors. Infect Immun 78: 1417-1425.
12. Caron, E., and Hall, A. (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282: 1717-1721.
13. Celli, J., Olivier, M., and Finlay, B.B. (2001) Enteropathogenic Escherichia coli mediates antiphagocytosis through the inhibition of PI 3-kinase-dependent pathways. EMBO J 20: 1245-1258.
14. Chacinska, A., Koehler, C.M., Milenkovic, D., Lithgow, T., and Pfanner, N. (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644.
15. Chang, C., Xu, X., Cui, H., Savchenko, A., Adkins, J., and Joachimiak, A. (2014) The crystal structure of non-LEE encoded type III effector C from Citrobacter rodentium. PDB ID: 4O2I. URL http://www.rcsb.org/pdb/explore/explore.do?structureId=4O2I.
16. Chen, L.F., Fischle, W., Verdin, E., and Greene, W.C. (2001) Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293: 1653-1657.
17. Crane, J.K., McNamara, B.P., and Donnenberg, M.S. (2001) Role of EspF in host cell death induced by enteropathogenic Escherichia coli. Cell Microbiol 3: 197-211.
18. Creasey, E.A., Delahay, R.M., Daniell, S.J., and Frankel, G. (2003) Yeast two-hybrid system survey of interactions between LEE-encoded proteins of enteropathogenic Escherichia coli. Microbiology 149: 2093-2106.
19. Creuzburg, K., Middendorf, B., Mellmann, A., Martaler, T., Holz, C., Fruth, A., etal. (2011) Evolutionary analysis and distribution of type III effector genes in pathogenic Escherichia coli from human, animal and food sources. Environ Microbiol 13: 439-452.
20. Croxen, M.A., Law, R.J., Scholz, R., Keeney, K.M., Wlodarska, M., and Finlay, B.B. (2013) Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 26: 822-880.
21. Cui, J., Yao, Q., Li, S., Ding, X., Lu, Q., Mao, H., etal. (2010) Glutamine deamidation and dysfunction of ubiquitin/NEDD8 induced by a bacterial effector family. Science 329: 1215-1218.
22. Dahan, S., Wiles, S., La Ragione, R.M., Best, A., Woodward, M.J., Stevens, M.P., etal. (2005) EspJ is a prophage-carried type III effector protein of attaching and effacing pathogens that modulates infection dynamics. Infect Immun 73: 679-686.
23. Dann, S.M., Spehlmann, M.E., Hammond, D.C., Iimura, M., Hase, K., Choi, L.J., etal. (2008) IL-6-dependent mucosal protection prevents establishment of a microbial niche for attaching/effacing lesion-forming enteric bacterial pathogens. J Immunol 180: 6816-6826.
24. Deng, W., Puente, J.L., Gruenheid, S., Li, Y., Vallance, B.A., Vázquez, A., etal. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci USA 101: 3597-3602.
25. Dong, N., Liu, L., and Shao, F. (2010) A bacterial effector targets host DH-PH domain RhoGEFs and antagonizes macrophage phagocytosis. EMBO J 29: 1363-1376.
26. Dong, N., Zhu, Y., Lu, Q., Hu, L., Zheng, Y., and Shao, F. (2012) Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses. Cell 150: 1029-1041.
27. Echtenkamp, F., Deng, W., Wickham, M.E., Vazquez, A., Puente, J.L., Thanabalasuriar, A., etal. (2008) Characterization of the NleF effector protein from attaching and effacing bacterial pathogens. FEMS Microbiol Lett 281: 98-107.
28. Elmore, S. (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35: 495-516.
29. Feral, C.C., Nishiya, N., Fenczik, C.A., Stuhlmann, H., Slepak, M., and Ginsberg, M.H. (2005) CD98hc (SLC3A2) mediates integrin signaling. Proc Natl Acad Sci USA 102: 355-360.
30. Freeman, S.A., and Grinstein, S. (2014) Phagocytosis: receptors, signal integration, and the cytoskeleton. Immunol Rev 262: 193-215.
31. Gao, X., Wan, F., Mateo, K., Callegari, E., Wang, D., Deng, W., etal. (2009) Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathog 5: e1000708.
32. Gao, X., Wang, X., Pham, T.H., Feuerbacher, L.A., Lubos, M.-L., Huang, M., etal. (2013) NleB, a bacterial effector with glycosyltransferase activity, targets GAPDH function to inhibit NF-κB activation. Cell Host Microbe 13: 87-99.
33. Garabedian, M., Jarnik, M., Kotova, E., and Tulin, A.V. (2011) Generating a knockdown transgene against Drosophila heterochromatic Tim17b gene encoding mitochondrial translocase subunit. PLoS ONE 6: e25945.
34. Golks, A., and Guerini, D. (2008) The O-linked N-acetylglucosamine modification in cellular signalling and the immune system. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep 9: 748-753.
35. Goosney, D.L., Celli, J., Kenny, B., and Finlay, B.B. (1999) Enteropathogenic Escherichia coli inhibits phagocytosis. Infect Immun 67: 490-495.
36. Halavaty, A.S., Anderson, S.M., Wawrzak, Z., Kudritska, M., Skarina, T., Anderson, W.F., and Savchenko, A. (2014) Type III effector NleH2 from Escherichia coli O157:H7 str. Sakai features an atypical protein kinase domain. Biochemistry 53: 2433-2435.
37. Hatada, E.N., Krappmann, D., and Scheidereit, C. (2000) NF-kappaB and the innate immune response. Curr Opin Immunol 12: 52-58.
38. Hemrajani, C., Berger, C.N., Robinson, K.S., Marchès, O., Mousnier, A., and Frankel, G. (2010) NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proc Natl Acad Sci USA 107: 3129-3134.
39. Hsu, Y., Jubelin, G., Taieb, F., Nougayrède, J.-P., Oswald, E., and Stebbins, C.E. (2008) Structure of the cyclomodulin Cif from pathogenic Escherichia coli. J Mol Biol 384: 465-477.
40. Iizumi, Y., Sagara, H., Kabe, Y., Azuma, M., Kume, K., Ogawa, M., etal. (2007) The enteropathogenic E.coli effector EspB facilitates microvillus effacing and antiphagocytosis by inhibiting myosin function. Cell Host Microbe 2: 383-392.
41. Kagnoff, M.F., and Eckmann, L. (1997) Epithelial cells as sensors for microbial infection. J Clin Invest 100: 6-10.
42. Kanack, K.J., Crawford, J.A., Tatsuno, I., Karmali, M.A., and Kaper, J.B. (2005) SepZ/EspZ is secreted and translocated into HeLa cells by the enteropathogenic Escherichia coli type III secretion system. Infect Immun 73: 4327-4337.
43. Kato, L.M., Kawamoto, S., Maruya, M., and Fagarasan, S. (2014) The role of the adaptive immune system in regulation of gut microbiota. Immunol Rev 260: 67-75.
44. Kenny, B., and Jepson, M. (2000) Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2: 579-590.
45. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D.J., Frey, E.A., and Finlay, B.B. (1997) Enteropathogenic E.coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511-520.
46. Kenny, B., Ellis, S., Leard, A.D., Warawa, J., Mellor, H., and Jepson, M.A. (2002) Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol Microbiol 44: 1095-1107.
47. Kurushima, J., Nagai, T., Nagamatsu, K., and Abe, A. (2010) EspJ effector in enterohemorrhagic E.coli translocates into host mitochondria via an atypical mitochondrial targeting signal. Microbiol Immunol 54: 371-379.
48. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S., and Wang, X. (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489.
49. Li, S., Zhang, L., Yao, Q., Li, L., Dong, N., Rong, J., etal. (2013) Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature 501: 242-246.
50. Li, W., Liu, Y., Sheng, X., Yin, P., Hu, F., Liu, Y., etal. (2014) Structure and mechanism of a type III secretion protease, NleC. Acta Crystallogr D Biol Crystallogr 70: 40-47.
51. Ma, C., Wickham, M.E., Guttman, J.A., Deng, W., Walker, J., Madsen, K.L., etal. (2006) Citrobacter rodentium infection causes both mitochondrial dysfunction and intestinal epithelial barrier disruption in vivo: role of mitochondrial associated protein (Map). Cell Microbiol 8: 1669-1686.
52. McNamara, B.P., Koutsouris, A., O'Connell, C.B., Nougayréde, J.P., Donnenberg, M.S., and Hecht, G. (2001) Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J Clin Invest 107: 621-629.
53. Marchés, O., Wiles, S., Dziva, F., La Ragione, R.M., Schüller, S., Best, A., etal. (2005) Characterization of two non-locus of enterocyte effacement-encoded type III-translocated effectors, NleC and NleD, in attaching and effacing pathogens. Infect Immun 73: 8411-8417.
54. Marchès, O., Ledger, T.N., Boury, M., Ohara, M., Tu, X., Goffaux, F., etal. (2003) Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 50: 1553-1567.
55. Marchès, O., Covarelli, V., Dahan, S., Cougoule, C., Bhatta, P., Frankel, G., and Caron, E. (2008) EspJ of enteropathogenic and enterohaemorrhagic Escherichia coli inhibits opsono-phagocytosis. Cell Microbiol 10: 1104-1115.
56. Matarrese, P., Falzano, L., Fabbri, A., Gambardella, L., Frank, C., Geny, B., etal. (2007) Clostridium difficile toxin B causes apoptosis in epithelial cells by thrilling mitochondria. Involvement of ATP-sensitive mitochondrial potassium channels. J Biol Chem 282: 9029-9041.
57. Micheau, O., and Tschopp, J. (2003) Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114: 181-190.
58. Mills, E., Baruch, K., Charpentier, X., Kobi, S., and Rosenshine, I. (2008) Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 3: 104-113.
59. Mills, E., Baruch, K., Aviv, G., Nitzan, M., and Rosenshine, I. (2013) Dynamics of the type III secretion system activity of enteropathogenic Escherichia coli. MBio 4: e00303-00313.
60. Mogensen, T.H. (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22: 240-273.
61. Morikawa, H., Kim, M., Mimuro, H., Punginelli, C., Koyama, T., Nagai, S., etal. (2010) The bacterial effector Cif interferes with SCF ubiquitin ligase function by inhibiting deneddylation of Cullin1. Biochem Biophys Res Commun 401: 268-274.
62. Mühlen, S., Ruchaud-Sparagano, M.H., and Kenny, B. (2011) Proteasome-independent degradation of canonical NFkappaB complex components by the NleC protein of pathogenic Escherichia coli. J Biol Chem 286: 5100-5107.
63. Nadler, C., Baruch, K., Kobi, S., Mills, E., Haviv, G., Farago, M., etal. (2010) The type III secretion effector NleE inhibits NF-kappaB activation. PLoS Pathog 6: e1000743.
64. Nagai, T., Abe, A., and Sasakawa, C. (2005) Targeting of enteropathogenic Escherichia coli EspF to host mitochondria is essential for bacterial pathogenesis: critical role of the 16th leucine residue in EspF. J Biol Chem 280: 2998-3011.
65. Neurath, M.F., Becker, C., and Barbulescu, K. (1998) Role of NF-kappaB in immune and inflammatory responses in the gut. Gut 43: 856-860.
66. Newton, H.J., Pearson, J.S., Badea, L., Kelly, M., Lucas, M., Holloway, G., etal. (2010) The type III effectors NleE and NleB from enteropathogenic E. coli and OspZ from Shigella block nuclear translocation of NF-kappaB p65. PLoS Pathog 6: e1000898.
67. Nougayrède, J.P., and Donnenberg, M.S. (2004) Enteropathogenic Escherichia coli EspF is targeted to mitochondria and is required to initiate the mitochondrial death pathway. Cell Microbiol 6: 1097-1111.
68. Nougayrède, J.P., Foster, G.H., and Donnenberg, M.S. (2007) Enteropathogenic Escherichia coli effector EspF interacts with host protein Abcf2. Cell Microbiol 9: 680-693.
69. Olsen, R.L., Echtenkamp, F., Cheranova, D., Deng, W., Finlay, B.B., and Hardwidge, P.R. (2013) The enterohemorrhagic Escherichia coli effector protein NleF binds mammalian Tmp21. Vet Microbiol 164: 164-170.
70. Pahl, H.L. (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18: 6853-6866.
71. Papatheodorou, P., Domańska, G., Öxle, M., Mathieu, J., Selchow, O., Kenny, B., and Rassow, J. (2006) The enteropathogenic Escherichia coli (EPEC) map effector is imported into the mitochondrial matrix by the TOM/Hsp70 system and alters organelle morphology. Cell Microbiol 8: 677-689.
72. Pearson, J.S., Riedmaier, P., Marchès, O., Frankel, G., and Hartland, E.L. (2011) A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-κB for degradation. Mol Microbiol 80: 219-230.
73. Pearson, J.S., Giogha, C., Ong, S.Y., Kennedy, C.L., Kelly, M., Robinson, K.S., etal. (2013) A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501: 247-251.
74. Peiser, L., Gough, P.J., Kodama, T., and Gordon, S. (2000) Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect Immun 68: 1953-1963.
75. Peralta-Ramírez, J., Hernandez, J.M., Manning-Cela, R., Luna-Muñoz, J., Garcia-Tovar, C., Nougayréde, J.P., etal. (2008) EspF interacts with nucleation-promoting factors to recruit junctional proteins into pedestals for pedestal maturation and disruption of paracellular permeability. Infect Immun 76: 3854-3868.
76. Peterson, L.W., and Artis, D. (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14: 141-153.
77. Pham, T.H., Gao, X., Tsai, K., Olsen, R., Wan, F., and Hardwidge, P.R. (2012) Functional differences and interactions between the Escherichia coli type III secretion system effectors NleH1 and NleH2. Infect Immun 80: 2133-2140.
78. Pham, T.H., Gao, X., Singh, G., and Hardwidge, P.R. (2013) Escherichia coli virulence protein NleH1 interaction with the v-Crk sarcoma virus CT10 oncogene-like protein (CRKL) governs NleH1 inhibition of the ribosomal protein S3 (RPS3)/nuclear factor κB (NF-κB) pathway. J Biol Chem 288: 34567-34574.
79. Quitard, S., Dean, P., Maresca, M., and Kenny, B. (2006) The enteropathogenic Escherichia coli EspF effector molecule inhibits PI-3 kinase-mediated uptake independently of mitochondrial targeting. Cell Microbiol 8: 972-981.
80. Raymond, B., Crepin, V.F., Collins, J.W., and Frankel, G. (2011) The WxxxE effector EspT triggers expression of immune mediators in an Erk/JNK and NF-κB-dependent manner. Cell Microbiol 13: 1881-1893.
81. Robinson, K.S., Mousnier, A., Hemrajani, C., Fairweather, N., Berger, C.N., and Frankel, G. (2010) The enteropathogenic Escherichia coli effector NleH inhibits apoptosis induced by Clostridium difficile toxin B. Microbiology 156: 1815-1823.
82. Ross, G.D., Reed, W., Dalzell, J.G., Becker, S.E., and Hogg, N. (1992) Macrophage cytoskeleton association with CR3 and CR4 regulates receptor mobility and phagocytosis of iC3b-opsonized erythrocytes. J Leukoc Biol 51: 109-117.
83. Roxas, J.L., Koutsouris, A., and Viswanathan, V.K. (2007) Enteropathogenic Escherichia coli-induced epidermal growth factor receptor activation contributes to physiological alterations in intestinal epithelial cells. Infect Immun 75: 2316-2324.
84. Roxas, J.L., Wilbur, J.S., Zhang, X., Martinez, G., Vedantam, G., and Viswanathan, V.K. (2012) The enteropathogenic Escherichia coli-secreted protein EspZ inhibits host cell apoptosis. Infect Immun 80: 3850-3857.
85. Roxas, J.L., Ryan, K., Vedantam, G., and Viswanathan, V.K. (2014) Enteropathogenic Escherichia coli dynamically regulates EGFR signaling in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 307: G374-G380.
86. Royan, S.V, Jones, R.M., Koutsouris, A., Roxas, J.L., Falzari, K., Weflen, A.W., etal. (2010) Enteropathogenic E.coli non-LEE encoded effectors NleH1 and NleH2 attenuate NF-κB activation. Mol Microbiol 78: 1232-1245.
87. Ruchaud-Sparagano, M.-H., Mühlen, S., Dean, P., and Kenny, B. (2011) The enteropathogenic E. coli (EPEC) Tir effector inhibits NF-κB activity by targeting TNFα receptor-associated factors. PLoS Pathog 7: e1002414.
88. Rudel, T., Kepp, O., and Kozjak-Pavlovic, V. (2010) Interactions between bacterial pathogens and mitochondrial cell death pathways. Nat Rev Microbiol 8: 693-705.
89. Salvador, F.A., Hernandes, R.T., Vieira, M.A.M., Rockstroh, A.C., and Gomes, T.A.T. (2014) Distribution of non-LEE-encoded type 3 secretion system dependent effectors in enteropathogenic Escherichia coli. Braz J Microbiol 45: 851-855.
90. Samba-Louaka, A., Nougayrède, J.P., Watrin, C., Jubelin, G., Oswald, E., and Taieb, F. (2008) Bacterial cyclomodulin Cif blocks the host cell cycle by stabilizing the cyclin-dependent kinase inhibitors p21 and p27. Cell Microbiol 10: 2496-2508.
91. Samba-Louaka, A., Nougayrède, J.P., Watrin, C., Oswald, E., and Taieb, F. (2009) The enteropathogenic Escherichia coli effector Cif induces delayed apoptosis in epithelial cells. Infect Immun 77: 5471-5477.
92. Selyunin, A.S., Sutton, S.E., Weigele, B.A., Reddick, L.E., Orchard, R.C., Bresson, S.M., etal. (2011) The assembly of a GTPase-kinase signalling complex by a bacterial catalytic scaffold. Nature 469: 107-111.
93. Selyunin, A.S., Reddick, L.E., Weigele, B.A., and Alto, N.M. (2014) Selective protection of an ARF1-GTP signaling axis by a bacterial scaffold induces bidirectional trafficking arrest. Cell Rep 6: 878-891.
94. Sham, H.P., Shames, S.R., Croxen, M.A., Ma, C., Chan, J.M., Khan, M.A., etal. (2011) Attaching and effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-κB and p38 mitogen-activated protein kinase activation. Infect Immun 79: 3552-3562.
95. Shames, S.R., Deng, W., Guttman, J.A., Hoog, C.L., de Li, Y., Hardwidge, P.R., etal. (2010) The pathogenic E. coli type III effector EspZ interacts with host CD98 and facilitates host cell prosurvival signalling. Cell Microbiol 12: 1322-1339.
96. Shames, S.R., Croxen, M.A., Deng, W., and Finlay, B.B. (2011a) The type III system-secreted effector EspZ localizes to host mitochondria and interacts with the translocase of inner mitochondrial membrane 17b. Infect Immun 79: 4784-4790.
97. Shames, S.R., Bhavsar, A.P., Croxen, M.A., Law, R.J., Mak, S.H.C., Deng, W., etal. (2011b) The pathogenic Escherichia coli type III secreted protease NleC degrades the host acetyltransferase p300. Cell Microbiol 13: 1542-1557.
98. Shaulian, E., and Karin, M. (2001) AP-1 in cell proliferation and survival. Oncogene 20: 2390-2400.
99. Sinha, D., Srivastava, S., Krishna, L., and D'Silva, P. (2014) Unraveling the intricate organization of mammalian mitochondrial presequence translocases: existence of multiple translocases for maintenance of mitochondrial function. Mol Cell Biol 34: 1757-1775.
100. Strasser, A., Jost, P.J., and Nagata, S. (2009) The many roles of FAS receptor signaling in the immune system. Immunity 30: 180-192.
101. Swanson, J.A., Johnson, M.T., Beningo, K., Post, P., Mooseker, M., and Araki, N. (1999) A contractile activity that closes phagosomes in macrophages. J Cell Sci 112: 307-316.
102. Tahoun, A., Siszler, G., Spears, K., McAteer, S., Tree, J., Paxton, E., etal. (2011) Comparative analysis of EspF variants in inhibition of Escherichia coli phagocytosis by macrophages and inhibition of E.coli translocation through human- and bovine-derived M cells. Infect Immun 79: 4716-4729.
103. Taieb, F., Nougayrède, J.-P., Watrin, C., Samba-Louaka, A., and Oswald, E. (2006) Escherichia coli cyclomodulin Cif induces G2 arrest of the host cell cycle without activation of the DNA-damage checkpoint-signalling pathway. Cell Microbiol 8: 1910-1921.
104. Takeuchi, O., and Akira, S. (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
105. Thanabalasuriar, A., Bergeron, J., Gillingham, A., Mimee, M., Thomassin, J.-L., Strynadka, N., etal. (2012) Sec24 interaction is essential for localization and virulence-associated function of the bacterial effector protein NleA. Cell Microbiol 14: 1206-1218.
106. Turco, M.M., and Sousa, M.C. (2014) The structure and specificity of the type III secretion system effector NleC suggest a DNA mimicry mechanism of substrate recognition. Biochemistry 53: 5131-5139.
107. Vossenkämper, A., Marchès, O., Fairclough, P.D., Warnes, G., Stagg, A.J., Lindsay, J.O., etal. (2010) Inhibition of NF-κB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. J Immunol 185: 4118-4127.
108. Wan, F., Anderson, D.E., Barnitz, R.A., Snow, A., Bidere, N., Zheng, L., etal. (2007) Ribosomal protein S3: a KH domain subunit in NF-kappaB complexes that mediates selective gene regulation. Cell 131: 927-939.
109. Wan, F., Weaver, A., Gao, X., Bern, M., Hardwidge, P.R., and Lenardo, M.J. (2011) IKKβ phosphorylation regulates RPS3 nuclear translocation and NF-κB function during infection with Escherichia coli strain O157:H7. Nat Immunol 12: 335-343.
110. Weflen, A.W., Alto, N.M., Viswanathan, V.K., and Hecht, G. (2010) E. coli secreted protein F promotes EPEC invasion of intestinal epithelial cells via an SNX9-dependent mechanism. Cell Microbiol 12: 919-929.
111. Wickham, M.E., Brown, N.F., Boyle, E.C., Coombes, B.K., and Finlay, B.B. (2007) Virulence is positively selected by transmission success between mammalian hosts. Curr Biol 17: 783-788.
112. Wong, A.R.C., Clements, A., Raymond, B., Crepin, V.F., and Frankel, G. (2012) The interplay between the Escherichia coli Rho guanine nucleotide exchange factor effectors and the mammalian RhoGEF inhibitor EspH. MBio 3: e00250-11.
113. Yan, D., Wang, X., Luo, L., Cao, X., and Ge, B. (2012) Inhibition of TLR signaling by a bacterial protein containing immunoreceptor tyrosine-based inhibitory motifs. Nat Immunol 13: 1063-1071.
114. Yan, D., Quan, H., Wang, L., Liu, F., Liu, H., Chen, J., etal. (2013) Enteropathogenic Escherichia coli Tir recruits cellular SHP-2 through ITIM motifs to suppress host immune response. Cell Signal 25: 1887-1894.
115. Yen, H., Ooka, T., Iguchi, A., Hayashi, T., Sugimoto, N., and Tobe, T. (2010) NleC, a type III secretion protease, compromises NF-κB activation by targeting p65/RelA. PLoS Pathog 6: e1001231.
116. Zhang, L., Ding, X., Cui, J., Xu, H., Chen, J., Gong, Y.N., etal. (2012) Cysteine methylation disrupts ubiquitin-chain sensing in NF-κB activation. Nature 481: 204-208.