The type III secretion effector NleF of enteropathogenic Escherichia coli activates NF-κB early during infection

Infection and Immunity

Volumn 82, Issue 11, 2014, Pages 4878-4888

  Pallett, Mitchell A ^a   Berger, Cedric N ^a   Pearson, Jaclyn S ^b   Hartland, Elizabeth L ^b   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 4; CASPASE 8; CASPASE 9; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; I KAPPA B ALPHA; INTERLEUKIN 8; MESSENGER RNA; MYC PROTEIN; NLEF PROTEIN; PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RELA; TUBULIN; UNCLASSIFIED DRUG; CASPASE; ESCHERICHIA COLI PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NLEF PROTEIN, E COLI; VIRULENCE FACTOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; ENTEROPATHOGENIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MITOCHONDRION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; IMMUNOLOGY; METABOLISM; UPREGULATION;

CASPASES; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; INTERLEUKIN-8; MITOCHONDRIA; NF-KAPPA B; RNA, MESSENGER; UP-REGULATION; VIRULENCE FACTORS;

EID: 84907960579     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02131-14     Document Type: Article

References (45)

1. Chen DH, Frankel G. 2005. Enteropathogenic Escherichia coli: unravelling pathogenesis. FEMS Microbiol. Rev. 29:83-98. http://dx.doi.org/10.1016/j.femsre.2004.07.002.
2. Pennington H. 2010. Escherichia coli O157. Lancet 376:1428-1435. http://dx.doi.org/10.1016/S0140-6736(10)60963-4.
3. Frankel G, Phillips AD. 2008. Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: getting off the pedestal. Cell. Microbiol. 10:549-556. http://dx.doi.org/10.1111/j.1462-5822.2007.01103.x.
4. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. U. S. A. 92:1664-1668. http://dx.doi.org/10.1073/pnas.92.5.1664.
5. Wong ARC, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL. 2011. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol. Microbiol. 80:1420-1438. http://dx.doi.org/10.1111/j.1365-2958.2011.07661.x.
6. Elliott SJ, Wainwright LA, McDaniel TK, Jarvis KG, Deng Y, Lai L, McNamara BP, Donnenberg MS, Kaper JB. 1998. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol. Microbiol. 28:1-4.
7. Raymond B, Young JC, Pallett M, Endres RG, Clements A, Frankel G. 2013. Subversion of trafficking, apoptosis, and innate immunity by type III secretion system effectors. Trends Microbiol. 21:430-441. http://dx.doi.org/10.1016/j.tim.2013.06.008.
8. Karin M, Lin A. 2002. NF-κB at the crossroads of life and death. Nat. Immunol. 3:221-227. http://dx.doi.org/10.1038/ni0302-221.
9. Li Q, Verma IM. 2002. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2:725-734. http://dx.doi.org/10.1038/nri910.
10. Raymond B, Crepin VF, Collins JW, 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. http://dx.doi.org/10.1111/j.1462-5822.2011.01666.x.
11. Yen H, Ooka T, Iguchi A, Hayashi T, Sugimoto N, Tobe T. 2010. NleC, a type III secretion protease, compromises NF-κB activation by targeting p65/RelA. PLoS Pathog. 6:e1001231. http://dx.doi.org/10.1371/journal.ppat.1001231.
12. Pearson JS, Riedmaier P, Marchès O, Frankel G, Hartland EL. 2011. A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-κB for degradation. Mol. Microbiol. 80:219-230. http://dx.doi.org/10.1111/j.1365-2958.2011.07568.x.
13. Zhang L, Ding X, Cui J, Xu H, Chen J, Gong Y, Hu L, Zhou Y, Ge J, Lu Q, Chen S, Shao F. 2011. Cysteine methylation disrupts ubiquitin-chain sensing in NF-κB activation. Nature 481:204-208. http://dx.doi.org/10.1038/nature10690.
14. Nadler C, Baruch K, Kobi S, Mills E, Haviv G, Farago M, Alkalay I, Bartfeld S, Meyer TF, Ben-Neriah Y, Rosenshine I. 2010. The type III secretion effector NleE inhibits NF-κB activation. PLoS Pathog. 6:e1000743. http://dx.doi.org/10.1371/journal.ppat.1000743.
15. Newton HJ, Pearson JS, Badea L, Kelly M, Lucas M, Holloway G, Wagstaff KM, Dunstone MA, Sloan J, Whisstock JC, Kaper JB, Robins-Browne RM, Jans DA, Frankel G, Phillips AD, Coulson BS, Hartland EL. 2010. The type III effectors NleE and NleB from enteropathogenic E. coli and OspZ from Shigella block nuclear translocation of NF-κB p65. PLoS Pathog. 6:e1000898. http://dx.doi.org/10.1371/journal.ppat.1000898.
16. Vossenkämper A, Marchès O, Fairclough PD, Warnes G, Stagg AJ, Lindsay JO, Evans PC, Luong LA, Croft NM, Naik S, Frankel G, MacDonald TT. 2010. Inhibition of NF-κB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE. J. Immunol. 185:4118-4127. http://dx.doi.org/10.4049/jimmunol.1000500.
17. Gao X, Wan F, Mateo K, Callegari E, Wang D, Deng W, Puente J, Li F, Chaussee MS, Finlay BB, Lenardo MJ, Hardwidge PR. 2009. Bacterial effector binding to ribosomal protein S3 subverts NF-κB function. PLoS Pathog. 5:e1000708. http://dx.doi.org/10.1371/journal.ppat.1000708.
18. Tobe T, Beatson SA, Taniguchi H, Abe H, Bailey CM, Fivian A, Younis R, Matthews S, Marches O, Frankel G, Hayashi T, Pallen MJ. 2006. An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc. Natl. Acad. Sci. U. S. A. 103:14941-14946. http://dx.doi.org/10.1073/pnas.0604891103.
19. Echtenkamp F, Deng W, Wickham ME, Vazquez A, Puente JL, Thanabalasuriar A, Gruenheid S, Finlay BB, Hardwidge PR. 2008. Characterization of the NleF effector protein from attaching and effacing bacterial pathogens. FEMS Microbiol. Lett. 281:98-107. http://dx.doi.org/10.1111/j.1574-6968.2008.01088.x.
20. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, Henderson IR, Harris D, Asadulghani M, Kurokawa K, Dean P, Kenny B, Quail MA, Thurston S, Dougan G, Hayashi T, Parkhill J, Frankel G. 2009. Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J. Bacteriol. 191:347-354. http://dx.doi.org/10.1128/JB.01238-08.
21. Blasche S, Mortl M, Steuber H, Siszler G, Nisa S, Schwarz F, Lavrik I, Gronewold TMA, Maskos K, Donnenberg MS, Ullmann D, Uetz P, Kögl M. 2013. The E. coli effector protein NleF is a caspase inhibitor. PLoS One 8:e58937. http://dx.doi.org/10.1371/journal.pone.0058937.
22. Olsen RL, Echtenkamp F, Cheranova D, Deng W, Finlay BB, Hardwidge PR. 2013. The enterohemorrhagic Escherichia coli effector protein NleF binds mammalian Tmp21. Vet. Microbiol. 164:164-170. http://dx.doi.org/10.1016/j.vetmic.2013.01.028.
23. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
24. Lakshmanan U, Porter AG. 2007. Caspase-4 interacts with TNF receptorassociated factor 6 and mediates lipopolysaccharide-induced NF-κB dependent production of IL-8 and CC chemokine ligand 4 (macrophageinflammatory protein-1ß). J. Immunol. 179:8480-8490. http://dx.doi.org/10.4049/jimmunol.179.12.8480.
25. Chaudhary P, Eby M, Jasmin A, Kumar A, Liu L, Hood L. 2000. Activation of the NF-κB pathway by caspase 8 and its homologs. Oncogene 19:4451-4460. http://dx.doi.org/10.1038/sj.onc.1203812.
26. Baruch K, Gur-Arie L, Nadler C, Koby S, Yerushalmi G, Ben-Neriah Y, Yogev O, Shaulian E, Guttman C, Zarivach R, Rosenshine I. 2011. Metalloprotease type III effectors that specifically cleave JNK and NF-κB. EMBO J. 30:221-231. http://dx.doi.org/10.1038/emboj.2010.297.
27. Czerucka D, Dahan S, Mograbi B, Rossi B, Rampal P. 2001. Implication of mitogen-activated protein kinases in T84 cell responses to enteropathogenic Escherichia coli infection. Infect. Immun. 69:1298-1305. http://dx.doi.org/10.1128/IAI.69.3.1298-1305.2001.
28. Savkovic SD, Ramaswamy A, Koutsouris A, Hecht G. 2001. EPECactivated ERK1/2 participate in inflammatory response but not tight junction barrier disruption. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G890-G898.
29. de Grado M, Rosenberger CM, Gauthier A, Vallance BA, Finlay BB. 2001. Enteropathogenic Escherichia coli infection induces expression of the early growth response factor by activating mitogen-activated protein kinase cascades in epithelial cells. Infect. Immun. 69:6217-6224. http://dx.doi.org/10.1128/IAI.69.10.6217-6224.2001.
30. Savkovic SD, Koutsouris A, Hecht G. 1997. Activation of NF-κB in intestinal epithelial cells by enteropathogenic Escherichia coli. Am. J. Physiol. 273:C1160-C1167.
31. Higgins LM, Frankel G, Douce G, Dougan G, MacDonald TT. 1999. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 67:3031-3039.
32. Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, Finlay BB, Vallance BA. 2006. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect. Immun. 74:2522-2536. http://dx.doi.org/10.1128/IAI.74.5.2522-2536.2006.
33. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB. 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2:119-129. http://dx.doi.org/10.1016/j.chom.2007.06.010.
34. Blasche S. 2012. Escherichia coli as host and pathogen. Ph.D. thesis. University of Heidelberg, Heidelberg, Germany.
35. Wang H, Kazanietz MG. 2010. p23/Tmp21 differentially targets the Rac-GAP ß2-chimaerin and protein kinase C via their C1 domains. Mol. Biol. Cell 21:1398-1408. http://dx.doi.org/10.1091/mbc.E09-08-0735.
36. Wang H, Xiao L, Kazanietz MG. 2011. p23/Tmp21 associates with protein kinase Cδ (PKCδ) and modulates its apoptotic function. J. Biol. Chem. 286:15821-15831. http://dx.doi.org/10.1074/jbc.M111.227991.
37. Loegering DJ, Lennartz MR. 2011. Protein kinase C and Toll-like receptor signaling. Enzyme Res. 2011:537821. http://dx.doi.org/10.4061/2011/537821.
38. Savkovic S, Koutsouris A, Hecht G. 2003. PKCζ participates in activation of inflammatory response induced by enteropathogenic E. coli. Am. J. Physiol. Cell Physiol. 285:C512-C521. http://dx.doi.org/10.1152/ajpcell.00444.2002.
39. Ren J, Wang Q, Morgan S, Si Y, Ravichander A, Dou C, Kent KC, Liu B. 2014. Protein kinase C-δ (PKCδ) regulates proinflammatory chemokine expression through cytosolic interaction with the NF-κB subunit p65 in vascular smooth muscle cells. J. Biol. Chem. 289:9013-9026. http://dx.doi.org/10.1074/jbc.M113.515957.
40. Li RC, Ping P, Zhang J, Wead WB, Cao X, Gao J, Zheng Y, Huang S, Han J, Bolli R. 2000. PKCe modulates NF-κB and AP-1 via mitogenactivated protein kinases in adult rabbit cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 279:H1679-H1689.
41. Levine MM, Nalin DR, Hornick RB, Bergquist EJ, Waterman DH, Young CR, Sotman S, Rowe B. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet i:1119-1122.
42. Garmendia J, Phillips AD, Carlier M, Chong Y, Schüller S, Marches O, Dahan S, Oswald E, Shaw RK, Knutton S, Frankel G. 2004. TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell. Microbiol. 6:1167-1183. http://dx.doi.org/10.1111/j.1462-5822.2004.00459.x.
43. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
44. Schlosser-Silverman E, Elgrably-Weiss M, Rosenshine I, Kohen R, Altuvia S. 2000. Characterization of Escherichia coli DNA lesions generated within J774 macrophages. J. Bacteriol. 182:5225-5230.
45. Kenny B, Ellis S, Leard AD, Warawa J, Mellor H, Jepson MA. 2002. Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol. Microbiol. 44:1095-1107. http://dx.doi.org/10.1046/j.1365-2958.2002.02952.x.