Nlec, a type III secretion protease, compromises NF-kB activation by targeting p65/rela

PLoS Pathogens

Volumn 6, Issue 12, 2010, Pages

  Yen, Hilo ^a   Ooka, Tadasuke ^b   Iguchi, Atsushi ^c   Hayashi, Tetsuya ^b,c   Sugimoto, Nakaba ^a   Tobe, Toru ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF MIYAZAKI   (Japan)

^c UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN NIEC; PROTEIN NIEE; PROTEINASE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; NLEE PROTEIN, E COLI; PEPTIDE HYDROLASE; VIRULENCE FACTOR; Z0986 PROTEIN, E COLI;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL VIRULENCE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYME ANALYSIS; INFLAMMATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN TARGETING; DRUG ANTAGONISM; IMMUNE EVASION; METABOLISM; PATHOGENICITY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; IMMUNE EVASION; NF-KAPPA B; PEPTIDE HYDROLASES; TRANSCRIPTION FACTOR RELA; VIRULENCE FACTORS;

EID: 78651257387     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001231     Document Type: Article

References (42)

1. Clarke SC (2001) Diarrhoeagenic Escherichia coli-an emerging problem? Diagn Microbiol Infect Dis 41: 93-98.
2. Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2: 123-140.
3. Moon HW, Whipp SC, Argenzio RA, Levine MM, Giannella RA (1983) Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun 41: 1340-1351.
4. Jerse AE, Yu J, Tall BD, Kaper JB (1990) A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci USA 87: 7839-7843.
5. Knutton S, Baldwin T, Williams PH, McNeish AS (1989) Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 57:1290-1298.
6. Garmendia J, Frankel G, Crepin VF (2005) Enteropathogenic and enterohe-morrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 73: 2573-2585.
7. McDaniel TK, Kaper JB (1997) A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol 23: 399-407.
8. Jarvis KG, Giron JA, Jerse AE, McDaniel TK, Donnenberg MS, et al. (1995) Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci U S A 92: 7996-8000.
9. Tobe T, Beatson SA, Taniguchi H, Abe H, Bailey CM, et al. (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.
10. Ogura Y, Abe H, Katsura K, Kurokawa K, Asadulghani M, et al. (2008) Systematic Identification and Sequence Analysis of the Genomic Islands of the Enteropathogenic Escherichia coli Strain B171-8 by the Combined Use of Whole-Genome PCR Scanning and Fosmid Mapping. J Bacteriol 190:6948-6960.
11. Iguchi A, Thomson NR, Ogura Y, Saunders D, Ooka T, et al. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 191: 347-354.
12. Dean P, Kenny B (2009) The effector repertoire of enteropathogenic E. coli: ganging up on the host cell. Curr Opin Microbiol 12: 101-109.
13. Fiocchi C (1997) Intestinal inflammation: a complex interplay of immune and nonimmune cell interactions. Am J Physiol 273: G769-775.
14. Sansonetti PJ (2004) War and peace at mucosal surfaces. Nat Rev Immunol 4:953-964.
15. Rothwarf DM (1999) The NF-kappaB Activation Pathway: A Paradigm in Information Transfer from Membrane to Nucleus. Science's STKE 1999: 1re-1.
16. Sen R, Baltimore D (1986) Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 47: 921-928.
17. O'Neill LAJ, Bowie AG (2007) The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat Rev Immunol 7: 353-364.
18. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499-511.
19. Häcker H, Karin M (2006) Regulation and function of IKK and IKK-related kinases. Sci STKE 2006: re13.
20. Bonizzi G, Karin M (2004) The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25: 280-288.
21. Savkovic SD, Koutsouris A, Hecht G (1996) Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration of neutrophils. Infect Immun 64:4480-4487.
22. Hauf N, Chakraborty T (2003) Suppression of NF-kappa B activation and proinflammatory cytokine expression by Shiga toxin-producing Escherichia coli. J Immunol 170: 2074-2082.
23. Ruchaud-Sparagano M-H, Maresca M, Kenny B (2007) Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell Microbiol 9: 1909-1921.
24. Gao X, Wan F, Mateo K, Callegari E, Wang D, et al. (2009) Bacterial effector binding to ribosomal protein s3 subverts NF-kappaB function. PLoS Pathog 5:e1000708.
25. Nadler C, Baruch K, Kobi S, Mills E, Haviv G, et al. (2010) The Type III Secretion Effector NleE Inhibits NF-kappaB Activation. PLoS Pathog 6:e1000743.
26. Newton HJ, Pearson JS, Badea L, Kelly M, Lucas M, et al. (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.
27. Hayashi T, Makino K, Ohnishi M, Kurokawa K, Ishii K, et al. (2001) Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res 8: 11-22.
28. Ogura Y, Ooka T, Iguchi A, Toh H, Asadulghani M, et al. (2009) Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proceedings of the National Academy of Sciences 106: 17939-17944.
29. Nakagawa R, Naka T, Tsutsui H, Fujimoto M, Kimura A, et al. (2002) SOCS-1 participates in negative regulation of LPS responses. Immunity 17: 677-687.
30. Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, et al. (2006) Suppressor of cytokine signaling 1negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7: 148-155.
31. Ryo A, Suizu F, Yoshida Y, Perrem K, Liou Y-C, et al. (2003) Regulation of NF-kappaB signaling by Pin1-dependent prolyl isomerization and ubiquitin-mediated proteolysis of p65/RelA. Mol Cell 12: 1413-1426.
32. Geng H, Wittwer T, Dittrich-Breiholz O, Kracht M, Schmitz ML (2009) Phosphorylation of NF-kappaB p65 at Ser468 controls its COMMD1-dependent ubiquitination and target gene-specific proteasomal elimination. EMBO Rep 10:381-386.
33. Coiras M, Lo ́pez-Huertas MR, Mateos E, Alcamí J (2008) Caspase-3-mediated cleavage of p65/RelA results in a carboxy-terminal fragment that inhibits IkappaBalpha and enhances HIV-1 replication in human T lymphocytes. Retrovirology 5: 109.
34. Hooper NM (1994) Families of zinc metalloproteases. FEBS J 354: 1-6.
35. Arbibe L, Kim DW, Batsche E, Pedron T, Mateescu B, et al. (2007) An injected bacterial effector targets chromatin access for transcription factor NF-kappaB to alter transcription of host genes involved in immune responses. Nat Immunol 8: 47-56.
36. Kim DW, Lenzen G, Page AL, Legrain P, Sansonetti PJ, et al. (2005) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci U S A 102:14046-14051.
37. Lad SP, Yang G, Scott DA, Wang G, Nair P, et al. (2007) Chlamydial CT441 is a PDZ domain-containing tail-specific protease that interferes with the NF-kappaB pathway of immune response. J Bacteriol 189: 6619-6625.
38. Marches O, Wiles S, Dziva F, La Ragione RM, Schuller S, et al. (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.
39. Kelly M, Hart E, Mundy R, Marches O, Wiles S, et al. (2006) Essential role of the type III secretion system effector NleB in colonization of mice by Citrobacter rodentium. Infect Immun 74: 2328-2337.
40. Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C, et al. (2001) Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci U S A 98: 11638-11643.
41. Yu J-H, Hamari Z, Han K-H, Seo J-A, Reyes-DomÌnguez Y, et al. (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genetics and Biology 41: 973-981.
42. Wang RF, Kushner SR (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.