Escherichia coli cytotoxic necrotizing factor 1 inhibits intestinal epithelial wound healing in vitro after mechanical injury

Infection and Immunity

Volumn 72, Issue 10, 2004, Pages 5733-5740

  Brest, Patrick ^a   Turchi, Laurent ^a   Le'Negrate, Gaelic ^a   Berto, Frédérick ^a   Moreilhon, Chimène ^c   Mari, Bernard ^a   Ponzio, Gilles ^a   Hofman, Paul ^a,b  

^a INSERM   (France)

^b Lab de Pathol Clin et Exp   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BACTERIAL PROTEIN; CYTOTOXIC NECROTIZING FACTOR 1; FOCAL ADHESION KINASE; GELATINASE B; GLUTAMINE; GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN CDC42; RAC PROTEIN; RHO FACTOR; RHO KINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; CATALYSIS; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DEAMINATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ESCHERICHIA COLI; FILOPODIUM; GENE ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; INTESTINE EPITHELIUM; INTESTINE INJURY; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; UPREGULATION; WOUND HEALING;

AMIDES; BACTERIAL TOXINS; CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CYTOTOXINS; ENZYME ACTIVATION; EPITHELIAL CELLS; EPITHELIUM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FOCAL ADHESION KINASE 1; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; INTESTINES; MATRIX METALLOPROTEINASE 9; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PYRIDINES; RAC GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; WOUND HEALING;

EID: 4644266757     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.10.5733-5740.2004     Document Type: Article

References (52)

1. Birkedal-Hansen, H. 1995. Proteolytic remodeling of extracellular matrix. Curr. Opin. Cell Biol. 7:728-735.
2. Bond, M., R. P. Fabunmi, A. H. Baker, and A. C. Newby. 1998. Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kappa B. FEES Lett. 435:29-34.
3. Boquet, P. 1998. Cytotoxic necrotizing factor 1 from Escherichia coli: a toxin with a new intracellular activity for eukaryotic cells. Folia Microbiol. 43:285-289.
4. Brest, P., B. Mograbi, V. Hofman, A. Loubat, B. Rossi, P. Auberger, and P. Hofman. 2003. Rho GTPase is activated by cytotoxic necrotizing factor 1 in peripheral blood T lymphocytes: potential cytotoxicity for intestinal epithelial cells. Infect. Immun. 71:1161-1169.
5. Buetow, L., G. Flatau, K. Chiu, P. Boquet, and P. Ghosh. 2002. Strategies for the structural determination of the catalytic domain of Escherichia coli cytotoxic necrotizing factor 1. Acta Crystallogr. Sect. D Biol. Crystallogr. 58:366-369.
6. Caprioli, A., V. Falbo, L. G. Roda, F. M. Ruggeri, and C. Zona. 1983. Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect. Immun. 39:1300-1306.
7. Chardin, P., P. Boquet, P. Madaule, M. R. Popoff, E. J. Rubin, and D. M. Gill. 1989. The mammalian G protein RhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J. 8:1087-1092.
8. Chen, B. H., J. T. Tzen, A. R. Bresnick, and H. C. Chen. 2002. Roles of Rho-associated kinase and myosin light chain kinase in morphological and migratory defects of focal adhesion kinase-null cells. J. Biol. Chem. 277:33857-33863.
9. Doye, A., A. Mettouchi, G. Bossis, R. Clement, C. Buisson-Touati, G. Flatau, L. Gagnoux, M. Piechaczyk, P. Boquet, and E. Lemichez. 2002. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 111:553-564.
10. Eberhardt, W., A. Huwiler, K. F. Beck, S. Walpen, and J. Pfeilschifter. 2000. Amplification of IL-1 beta-induced matrix metalloproteinase-9 expression by superoxide in rat glomerular mesangial cells is mediated by increased activities of NF-kappa B and activating protein-1 and involves activation of the mitogen-activated protein-kinase pathways. J. Immunol. 165:5788-5797.
11. Falzano, L., C. Fiorentini, G. Donelli, E. Michel, C. Kocks, P. Cossart, L. Cabanie, E. Oswald, and P. Boquet. 1993. Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type 1. Mol. Microbiol. 9:1247-1254.
12. Falzano, L., M. G. Quaranta, S. Travaglione, P. Filippini, A. Fabbri, M. Viora, G. Donelli, and C. Fiorentini. 2003. Cytotoxic necrotizing factor 1 enhances reactive oxygen species-dependent transcription and secretion of proinflammatory cytokines in human uroepithelial cells. Infect. Immun. 71:4178-4181.
13. Fenteany, G., P. A. Janmey, and T. P. Stossel. 2000. Signaling pathways and cell mechanics involved in wound closure by epithelial cell sheets. Curr. Biol. 10:831-838.
14. Fiorentini, C., P. Matarrese, E. Straface, L. Falzano, G. Donelli, P. Boquet, and W. Malorni. 1998. Rho-dependent cell spreading activated by E. coli cytotoxic necrotizing factor 1 hinders apoptosis in epithelial cells. Cell Death Differ. 5:921-929.
15. Flatau, G., L. Landraud, P. Boquet, M. Bruzzone, and P. Munro. 2000. Deamidation of RhoA glutamine 63 by the Escherichia coli CNF1 toxin requires a short sequence of the GTPase switch 2 domain. Biochem. Biophys. Res. Commun. 267:-592.
16. Flatau, G., E. Lemichez, M. Gauthier, P. Chardin, S. Paris, C. Fiorentini, and P. Boquet. 1997. Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387:729-733.
17. Goke, M., M. Kanai, K. Lynch-Devaney, and D. K. Podolsky. 1998. Rapid mitogen-activated protein kinase activation by transforming growth factor alpha in wounded rat intestinal epithelial cells. Gastroenterology 114:697-705.
18. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
19. Hauck, C. R., D. A. Hsia, X. S. Puente, D. A. Cheresh, and D. D. Schlaepfer. 2002. FRNK blocks v-Src-stimulated invasion and experimental metastases without effects on cell motility or growth. EMBO J. 21:6289-6302.
20. Hauck, C. R., D. J. Sieg, D. A. Hsia, J. C. Loftus, W. A. Gaarde, B. P. Monia, and D. D. Schlaepfer. 2001. Inhibition of focal adhesion kinase expression or activity disrupts epidermal growth factor-stimulated signaling promoting the migration of invasive human carcinoma cells. Cancer Res. 61:7079-7090.
21. Hofman, P., G. Flatau, E. Selva, M. Gauthier, G. Le Negrate, C. Fiorentini, B. Rossi, and P. Boquet. 1998. Escherichia coli cytotoxic necrotizing factor 1 effaces microvilli and decreases transmigration of polymorphonuclear leukocytes in intestinal T84 epithelial cell monolayers. Infect. Immun. 66:2494-2500.
22. Hofman, P., G. Le Negrate, B. Mograbi, V. Hofman, P. Brest, A. Alliana-Schmid, G. Flatau, P. Boquet, and B. Rossi. 2000. Escherichia coli cytotoxic necrotizing factor-1 (CNF-1) increases the adherence to epithelia and the oxidative burst of human polymorphonuclear leukocytes but decreases bacteria phagocytosis. J. Leukoc. Biol. 68:522-528.
23. Hopkins, A. M., S. V. Walsh, P. Verkade, P. Boquet, and A. Nusrat. 2003. Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function. J. Cell Sci. 116:725-742.
24. Hsia, D. A., S. K. Mitra, C. R. Hauck, D. N. Streblow, J. A. Nelson, D. Ilic, S. Huang, E. Li, G. R. Nemerow, J. Leng, K. S. Spencer, D. A. Cheresh, and D. D. Schlaepfer. 2003. Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 160:753-767.
25. Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, and T. Yamamoto. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377:539-544.
26. Kaibuchi, K., S. Kuroda, and M. Amano. 1999. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68:459-486.
27. Keely, P. J., J. K. Westwick, I. P. Whitehead, C. J. Der, and L. V. Parise. 1997. Cdc42 and Rac1 induce integrin-mediated cell motility and invasiveness through PI(3)K. Nature 390:632-636.
28. Lacerda, H. M., G. D. Pullinger, A. J. Lax, and E. Rozengurt. 1997. Cytotoxic necrotizing factor 1 from Escherichia coli and dermonecrotic toxin from Bordetella bronchiseptica induce p21(rho)-dependent tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 cells. J. Biol. Chem. 272:9587-9596.
29. Lerm, M., J. Selzer, A. Hoffmeyer, U. R. Rapp, K. Aktories, and G. Schmidt. 1999. Deamidation of Cdc42 and Rac by Escherichia coli cytotoxic necrotizing factor 1: activation of c-Jun N-terminal kinase in HeLa cells. Infect. Immun. 67:496-503.
30. Madara, J. L., S. Colgan, A. Nusrat, C. Delp, and C. Parkos. 1992. A simple approach to measurement of electrical parameters of cultured epithelial monolayers: use in assessing neutrophil epithelial monolayers transmigration. J. Tissue Cult. Methods 14:209-216.
31. Maekawa, M., T. Ishizaki, S. Boku, N. Watanabe, A. Fujita, A. Iwamatsu, T. Obinata, K. Ohashi, K. Mizuno, and S. Narumiya. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285:895-898.
32. Mills, M., K. C. Meysick, and A. D. O'Brien. 2000. Cytotoxic necrotizing factor type 1 of uropathogenic Escherichia coli kills cultured human uroepithelial 5637 cells by an apoptotic mechanism. Infect. Immun. 68:5869-5880.
33. Munaut, C., T. Salonurmi, S. Kontusaari, P. Reponen, T. Morita, J. M. Foidart, and K. Tryggvason. 1999. Murine matrix metalloproteinase 9 gene 5′-upstream region contains cis-acting elements for expression in osteoclasts and migrating keratinocytes in transgenic mice. J. Biol. Chem. 274:5588-5596.
34. Nobes, C. D., and A. Hall. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144:1235-1244.
35. Nobes, C. D., and A. Hall. 1995. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
36. Parks, W. C. 1999. Matrix metalloproteinases in repair. Wound Repair Regen. 7:423-432.
37. Parsons, J. T., K. H. Martin, J. K. Slack, J. M. Taylor, and S. A. Weed. 2000. Focal adhesion kinase: a regulator of focal adhesion dynamics and cell movement. Oncogene 19:5606-5613.
38. Ridley, A. J., and A. Hall. 1992, The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389-399.
39. Ridley, A. J., H. F. Paterson, C. L. Johnston, D. Diekmann, and A. Hall. 1992. The small GTP-binding protein Rac regulates growth factor-induced membrane ruffling. Cell 70:401-410.
40. Salo, T., M. Makela, M. Kylmaniemi, H. Autio-Harmainen, and H. Larjava. 1994. Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab. Investig. 70:176-182.
41. Santos, M. F., S. A. McCormack, Z. Guo, J. Okolicany, Y. Zheng, L. R. Johnson, and G. Tigyi. 1997. Rho proteins play a critical role in cell migration during the early phase of mucosal restitution. J. Clin. Investig. 100:216-225.
42. Schmidt, G., P. Sehr, M. Wilm, J. Selzer, M. Mann, and K. Aktories. 1997. Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387:725-729.
43. Schmitz, A. A., E. E. Govek, B. Bottner, and L. Van Aelst. 2000. Rho GTPases: signaling, migration, and invasion. Exp. Cell Res. 261:1-12.
44. Shibata, K., F. Kikkawa, A. Nawa, A. A. Thant, K. Naruse, S. Mizutani, and M. Hamaguchi. 1998. Both focal adhesion kinase and c-Ras are required for the enhanced matrix metalloproteinase 9 secretion by fibronectin in ovarian cancer cells. Cancer Res. 58:900-903.
45. Singer, A. J., and R. A. Clark. 1999. Cutaneous wound healing. N. Engl. J. Med. 341:738-746.
46. Sternlicht, M. D., and Z. Werb. 2001. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17:463-516.
47. Thomas, W., G. D. Pullinger, A. J. Lax, and E. Rozengurt. 2001. Escherichia coli cytotoxic necrotizing factor and Pasteurella multotida toxin induce focal adhesion kinase autophosphorylation and Src association. Infect. Immun. 69:1-5935.
48. Turchi, L., A. A. Chassot, I. Bourget, C. Baldescchi, J. P. Ortonne, G. Meneguzzi, E. Lemichez, and G. Ponzio. 2003. Cross-talk between Rho GTPases and stress activated kinases for matrix metalloproteinase-9 induction in response to keratinocytes injury. J. Investig. Dermatol. 121:1291-1300.
49. Turchi, L., A. A. Chassot, R. Rezzonico, K. Yeow, A. Loubat, B. Ferrua, G. Lenegrate, J. P. Ortonne, and G. Ponzio. 2002. Dynamic characterization of the molecular events during in vitro epidermal wound healing. J. Investig. Dermatol. 119:56-63.
50. Underwood, D. C., R. R. Osborn, S. Bochnowicz, E. F. Webb, D. J. Rieman, J. C. Lee, A. M. Romanic, J. L. Adams, D. W. Hay, and D. E. Griswold. 2000. SB 239063, a p38 MAPK inhibitor, reduces neutrophilia, inflammatory cytokines, MMP-9, and fibrosis in lung. Am. J. Physiol. Lung Cell Mol. Physiol. 279:L895-L902.
51. Yao, J., S. Xiong, K. Klos, N. Nguyen, R. Grijalva, P. Li, and D. Yu. 2001. Multiple signaling pathways involved in activation of matrix metalloproteinase-9 (MMP-9) by heregulin-beta1 in human breast cancer cells. Oncogene 20:8066-8074.
52. Zhuge, Y., and J. Xu. 2001. Rac1 mediates type I collagen-dependent MMP-2 activation. Role in cell invasion across collagen barrier. J. Biol. Chem. 276:16248-16256.