Constitutive activation of Rho proteins by CNF-1 influences tight junction structure and epithelial barrier function

Journal of Cell Science

Volumn 116, Issue 4, 2003, Pages 725-742

  Hopkins, Ann M ^a   Walsh, Shaun V ^a   Verkade, Paul ^b   Boquet, Patrice ^c   Nusrat, Asma ^a  

^a EMORY UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c INSERM   (France)

Author keywords

Epithelium; F actin; Paracellular permeability; Rho GTPases; Tight junction

Indexed keywords

BINDING PROTEIN; CALCIUM; CAVEOLIN 1; CELL ADHESION MOLECULE; CONTRACTILE PROTEIN; CYTOTOXIC NECROTIZING FACTOR 1; ESCHERICHIA COLI ENDOTOXIN; F ACTIN; MYOSIN LIGHT CHAIN; OCCLUDIN; PAXILLIN; PROTEIN CDC42; RAC PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TYROSINE; UNCLASSIFIED DRUG; VILLIN;

BASOLATERAL MEMBRANE; CELL FUNCTION; CELL JUNCTION; CELL POLARITY; CELL STRUCTURE; CELL TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; CYTOTOXICITY; ENDOSOME; ENZYME ACTIVITY; EPITHELIUM CELL; FOCAL ADHESION; HUMAN; HUMAN CELL; IMMUNOGOLD ELECTRON MICROSCOPY; INTESTINE EPITHELIUM; MICROVILLUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION;

ACTINS; ADHERENS JUNCTIONS; BACTERIAL TOXINS; CADHERINS; CARRIER PROTEINS; CAVEOLIN 1; CAVEOLINS; CDC42 GTP-BINDING PROTEIN; CELL ADHESION MOLECULES; CELL MEMBRANE PERMEABILITY; CYTOSKELETAL PROTEINS; CYTOTOXINS; ENDOSOMES; EPITHELIAL CELLS; EPITHELIUM; ESCHERICHIA COLI PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE PROTEINS; MICROFILAMENT PROTEINS; MICROSCOPY, ELECTRON; PAXILLIN; PHOSPHOPROTEINS; RAC GTP-BINDING PROTEINS; RECEPTORS, CELL SURFACE; RHO GTP-BINDING PROTEINS; TIGHT JUNCTIONS; TUMOR CELLS, CULTURED;

ESCHERICHIA COLI;

EID: 0037442918     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00300     Document Type: Review

References (84)

1. Aktories, K. (1997). Bacterial toxins that target Rho proteins. J. Clin. Invest. 99, 827-829.
2. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y. and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
3. Anderson, R. G. (1998). The caveolae membrane system. Annu Rev. Biochem. 67, 199-225.
4. Andreu, A., Stapleton, A. E., Fennell, C., Lockman, H. A., Xercavins, M., Fernandez, F. and Stamm, W. E. (1997). Urovirulence determinants in Escherichia coli strains causing prostatitis [published erratum appears in J. Infect Dis. 1997 Nov; 176(5):1416]. J. Infect. Dise. 176, 464-469.
5. Aspenstrom, P. (1999). Effectors for the Rho GTPases. Curr. Opin. Cell Biol. 11, 95-102.
6. Barth, H., Olenik, C., Sehr, P., Schmidt, G., Aktories, K. and Meyer, D. K. (1999). Neosynthesis and activation of Rho by Escherichia coli cytotoxic necrotizing factor (CNF1) reverse cytopathic effects of ADP-ribosylated Rho. J. Biol. Chem. 274, 27407-27414.
7. Ben-Ami, G., Ozeri, V., Hanski, E., Hofmann, F., Aktories, K., Hahn, K. M., Bokoch, G. M. and Rosenshine, I. (1998). Agents that inhibit Rho, Rac, and Cdc42 do not block formation of actin pedestals in HeLa cells infected with enteropathogenic Escherichia coli. Infect. Immun. 66, 1755-1758.
8. Blanco, M., Blanco, J., Blanco, J. E., Alonso, M. P., Abalia, I., Rodriguez, E., Bilbao, J. R. and Umaran, A. (1995). [Virulence factors and 0 serogroups of Escherichia coli as a cause of community-acquired urinary infections]. Enferm. Infecc. Microbiol. Clin. 13, 236-241 [Spanish].
9. Boquet, P. (1999). Bacterial toxins inhibiting or activating small GTP-binding proteins. Ann. N. Y. Acad. Sci. 886, 83-90.
10. Boquet, P., Sansonetti, P. J. and Tran Van Nhieu, G. (1999). Rho GTP-binding proteins as targets for microbial pathogens. Prog. Mol. Subcell. Biol. 22, 183-199,
11. Caprioli, A., Falbo, V., Roda, L. G., Ruggeri, F. M. and Zona, C. (1983). Partial purification and characterization of an Escherichia coli toxic factor that induces morphological cell alterations. Infect. Immun. 39, 1300-1306.
12. Caprioli, A., Donelli, G., Falbo, V., Possenti, R., Roda, L. G., Roscetti, G. and Ruggeri, F. M. (1984). A cell division-active protein from E. coli. Biochem. Biophys. Res. Commun. 118, 587-593.
13. Caprioli, A., Falbo, V., Ruggeri, F. M., Baldassarri, L., Bisicchia, R., Ippolito, G., Romoli, E. and Donelli, G. (1987). Cytotoxic necrotizing factor production by hemolytic strains of Escherichia coli causing extraintestinal infections. J. Clin. Microbiol. 25, 146-149.
14. Casanova, J. E., Wang, X., Kumar, R., Bhartur, S. G., Navarre, J., Woodrum, J. E., Altschuler, Y., Ray, G. S. and Goldenring, J. R. (1999). Association of Rab25 and Rab1la with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 10, 47-61.
15. Contamin, S., Galmiche, A., Doye, A., Flatau, G., Benmerah, A. and Boquet, P. (2000). The p21 Rho-activating toxin cytotoxic necrotizing factor 1 is endocytosed by a clathrin-independent mechanism and enters the cytosol by an acidic-dependent membrane translocation step. Mol. Biol. Cell 11, 1775-1787.
16. De Rycke, J., Nougayrede, J. P., Oswald, E. and Mazars, P. (1997). Interaction of Escherichia coli producing cytotoxic necrotizing factor with HeLa epithelial cells. Adv. Exp. Med. Biol. 412, 363-366.
17. Denker, B. M. and Nigam, S. K. (1998). Molecular structure and assembly of the tight junction. Am. J. Physiol. 274, F1-9.
18. Dharmsathaphorn, K. and Madara, J. L. (1990). Established intestinal cell lines as model systems for electrolyte transport studies. Methods Enzymol. 192, 354-389.
19. Dharmsathaphorn, K., McRoberts, J. A., Mandel, K. G., Tisdale, L. D. and Masui, H. (1984). A human colonic tumor cell line that maintains vectorial electrolyte transport. Am. J. Physiol. 246, G204-208.
20. Elliott, S. J., Srinivas, S., Albert, M. J., Alam, K., Robins-Browne, R. M., Gunzburg, S. T., Mee, B. J. and Chang, B. J. (1998). Characterization of the roles of hemolysin and other toxins in enteropathy caused by alpha-hemolytic Escherichia coli linked to human diarrhea. Infect. Immun. 66, 2040-2051.
21. Falzano, L., Fiorentini, C., Donelli, G., Michel, E., Kocks, C., Cossart, P., Cabanie, L., Oswald, E. and Boquet, P. (1993). Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type 1. Mol. Microbiol. 9, 1247-1254.
22. Fiorentini, C., Arancia, G., Caprioli, A., Falbo, V., Ruggeri, F. M. and Donelli, G. (1988). Cytoskeletal changes induced in HEp-2 cells by the cytotoxic necrotizing factor of Escherichia coli. Toxicon 26, 1047-1056.
23. Fiorentini, C., Fabbri, A., Matarrese, P., Falzano, L., Boquet, P. and Malorni, W. (1997). Hinderance of apoptosis and phagocytic behaviour induced by Escherichia coli cytotoxic necrotizing factor 1: two related activities in epithelial cells. Biochem. Biophys. Res. Commun. 241, 341-346.
24. Fiorentini, C., Gauthier, M., Donelli, G. and Boquet, P. (1998a). Bacterial toxins and the Rho GTP-binding protein: what microbes teach us about cell regulation. Cell Death Differ. 5, 720-728.
25. Fiorentini, C., Matarrese, P., Straface, E., Falzano, L., Donelli, G., Boquet, P. and Malorni, W. (1998b). Rho-dependent cell spreading activated by E. coli cytotoxic necrotizing factor 1 hinders apoptosis in epithelial cells. Cell Death Differ. 5, 921-929.
26. Fiorentini, C., Matarrese, P., Straface, E., Falzano, L., Fabbri, A., Donelli, G., Cossarizza, A., Boquet, P. and Malorni, W. (1998c). Toxin-induced activation of Rho GTP-binding protein increases Bcl-2 expression and influences mitochondrial homeostasis. Exp. Cell Res. 242, 341-350.
27. Flatau, G., Lemichez, E., Gauthier, M., Chardin, P., Paris, S., Fiorentini, C. and Boquet, P, (1997). Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387, 729-733.
28. Fukata, Y., Kimura, K., Oshiro, N., Saya, H., Matsuura, Y. and Kaibuchi, K. (1998). Association of the myosin-binding subunit of myosin phosphatase and moesin: dual regulation of moesin phosphorylation by Rho-associated kinase and myosin phosphatase. J. Cell Biol. 141, 409-418.
29. Gerhard, R., Schmidt, G., Hofmann, E and Aktories, K. (1998). Activation of Rho GTPases by Escherichia coli cytotoxic necrotizing factor 1 increases intestinal permeability in Caco-2 cells. Infect. Immun. 66, 5125-5131.
30. Gopalakrishnan, S., Raman, N., Atkinson, S. J. and Marrs, J. A. (1998). Rho GTPase signaling regulates tight junction assembly and protects tight junctions during ATP depletion. Am. J. Physiol. 275, C798-809.
31. Gyles, C. L. (1992). Escherichia coli cytotoxins and enterotoxins. Can. J. Microbiol. 38, 734-746.
32. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
33. Hall, A. (1990). The cellular functions of small GTP-binding proteins. Science 249, 635-640.
34. Hasegawa, H., Fujita, H., Katoh, H., Aoki, J., Nakamura, K., Ichikawa, A. and Negishi, M. (1999). Opposite regulation of transepithelial electrical resistance and paracellular permeability by Rho in Madin-Darby canine kidney cells. J. Biol. Chem. 274, 20982-20988.
35. Hirase, T., Kawashima, S., Wong, E. Y., Ueyama, T., Rikitake, Y., Tsukita, S., Yokoyama, M. and Staddon, J. M. (2001). Regulation of tight junction permeability and occludin phosphorylation by RhoA-p160ROCK-dependent and -independent mechanisms. J. Biol. Chem. 276, 10423-10431.
36. Hofman, P., Flatau, G., Selva, E., Gauthier, M., le Negrate, G., Fiorentini, C., Rossi, B. and Boquet, P. (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.
37. Hopkins, A. M., Li, D., Mrsny, R. J., Walsh, S. V. and Nusrat, A. (2000). Modulation of tight junction function by G protein-coupled events. Adv. Drug Deliv. Rev. 41, 329-340.
38. Imamura, F., Mukai, M., Ayaki, M. and Akedo, H. (2000). Y-27632, an inhibitor of rho-associated protein kinase, suppresses tumor cell invasion via regulation of focal adhesion and focal adhesion kinase. Jpn J. Cancer Res. 91, 811-816.
39. Island, M. D., Cui, X., Foxman, B., Marrs, C. F., Stamm, W. E., Stapleton, A. E. and Warren, J. W. (1998). Cytotoxicity of hemolytic, cytotoxic necrotizing factor 1-positive and -negative Escherichia coli to human T24 bladder cells. Infect. Immun. 66, 3384-3389.
40. Island, M. D., Cui, X. and Warren, J. W. (1999). Effect of Escherichia coli cytotoxic necrotizing factor 1 on repair of human bladder cell monolayers in vitro. Infect. Immun. 67, 3657-3661.
41. Jou, T. S. and Nelson, W. J. (1998). Effects of regulated expression of mutant RhoA and Rac1 small GTPases on the development of epithelial (MDCK) cell polarity. J. Cell Biol. 142, 85-100.
42. Jou, T. S., Schneeberger, E. E. and Nelson, W. J. (1998). Structural and functional regulation of tight junctions by RhoA and Rac1 small GTPases. J. Cell Biol. 142, 101-115.
43. Jou, T. S., Leung, S. M., Fung, L. M., Ruiz, W. G., Nelson, W. J. and Apodaca, G. (2000). Selective alterations in biosynthetic and endocytic protein traffic in Madin-Darby canine kidney epithelial cells expressing mutants of the small GTPase Rac1. Mol. Biol. Cell 11, 287-304.
44. Kazmierczak, B. I., Jou, T. S., Mostov, K. and Engel, J. N. (2001). Rho GTPase activity modulates Pseudomonas aeruginosa internalization by epithelial cells. Cell. Microbiol. 3, 85-98.
45. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K. et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
46. Kranenburg, O., Poland, M., van Horck, F. P., Drechsel, D., Hall, A. and Moolenaar, W. H. (1999). Activation of RhoA by lysophosphatidic acid and Galpha 12/13 subunits in neuronal cells: induction of neurite retraction. Mol. Biol. Cell 10, 1851-1857.
47. Lemichez, E., Flatau, G., Bruzzone, M., Boquet, P. and Gauthier, M. (1997). Molecular localization of the Escherichia coli cytotoxic necrotizing factor CNF1 cell-binding and catalytic domains. Mol. Microbiol. 24, 1061-1070.
48. Lerm, M., Schmidt, G., Goehring, U. M., Schirmer, J. and Aktories, K. (1999a). Identification of the region of rho involved in substrate recognition by Escherichia coli cytotoxic necrotizing factor 1 (CNF1). J. Biol. Chem. 274, 28999-29004.
49. Lerm, M., Selzer, J., Hoffmeyer, A., Rapp, U. R., Aktories, K. and Schmidt, G. (1999b). 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.
50. Lerm, M., Schmidt, G. and Aktories, K. (2000). Bacterial protein toxins targeting Rho GTPases. FEMS Microbiol. Lett. 188, 1-6.
51. Lesser, C. F., Scherer, C. A. and Miller, S. I. (2000). Rac, ruffle and rho: orchestration of Salmonella invasion. Trends Microbiol. 8, 151-152.
52. Liu, Y., Nusrat, A., Schnell, F. J., Reaves, T. A., Walsh, S. V., Pochet, M. P, and Parkos, C. A. (2000). Human junction adhesion molecule regulates tight junction resealing in epithelia. J. Cell Sci. 113, 2363-2374.
53. Mackay, D. J., Esch, F., Furthmayr, H. and Hall, A. (1997). Rho- and rac-dependent assembly of focal adhesion complexes and actin filaments in permeabilized fibroblasts: an essential role for ezrin/radixin/moesin proteins. J. Cell Biol, 138, 927-938.
54. Madara, J. L. (1987). Intestinal absorptive cell tight junctions are linked to cytoskeleton. Am. J. Physiol. 253, C171-175.
55. Madara, J. L. (1998). Regulation of the movement of solutes across tight junctions. Ann. Rev. Physiol. 60, 143-159.
56. Madara, J. L. and Dharmsathaphorn, K. (1985). Occluding junction structure-function relationships in a cultured epithelial monolayer. J. Cell Biol. 101, 2124-2133.
57. Madara, J. L., Moore, R. and Carlson, S. (1987). Alteration of intestinal tight junction structure and permeability by cytoskeletal contraction. Am. J. Physiol. 253, C854-861.
58. Madara, J. L., Stafford, J., Barenberg, D. and Carlson, S. (1988). Functional coupling of tight junctions and microfilaments in T84 monolayers. Am. J. Physiol, 254, G416-423.
59. Michaely, P. A., Mineo, C., Ying, Y. S. and Anderson, R. G. (1999). Polarized distribution of endogenous Rac1 and RhoA at the cell surface. J Biol. Chem. 274, 21430-21436.
60. Mineo, C. and Anderson, R. G. (2001). Potocytosis. Robert Feulgen Lecture. Histochem. Cell Biol. 116, 109-118.
61. Nobes, C. D. and Hall, A. (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.
62. Nusrat, A., Giry, M., Turner, J. R., Colgan, S. P., Parkos, C. A., Carnes, D., Lemichez, E., Boquet, P. and Madara, J. L. (1995). Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc. Natl. Acad. Sci. USA 92, 10629-10633.
63. Nusrat, A., Parkos, C. A., Verkade, P., Foley, C. S., Liang, T. W., Innis-Whitehouse, W., Eastburn, K. K. and Madara, J. L. (2000). Tight junctions are membrane microdomains. J. Cell Sci. 113, 1771-1781.
64. Nusrat, A., von Eichel-Streiber, C., Turner, J. R., Verkade, P., Madara, J. L. and Parkos, C. A. (2001). Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect. Immun. 69, 1329-1336.
65. Parkos, C. A., Colgan, S. P., Bacarra, A. E., Nusrat, A., Delp-Archer, C., Carlson, S., Su, D. H. and Madara, J. L. (1995). Intestinal epithelia (T84) possess basolateral ligands for CD11b/CD18-mediated neutrophil adherence. Am. J. Physiol. 268, C472-479.
66. Ridley, A. J. and Hall, A. (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.
67. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
68. Rojas, R., Ruiz, W. G., Leung, S. M., Jou, T. S. and Apodaca, G. (2001). Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell. 12, 2257-2274.
69. Sagi, S. A., Seasholtz, T. M., Kobiashvili M., Wilson, B. A., Toksoz, D. and Brown, J. H. (2001). Physical and functional interactions of Galphaq with Rho and its exchange factors. J. Biol. Chem. 276, 15445-15452.
70. Sanders, S. E., Madara, J. L., McGuirk, D. K., Gelman, D. S. and Colgan, S. P. (1995). Assessment of inflammatory events in epithelial permeability: a rapid screening method using fluorescein dextrans. Epithelial Cell Biol. 4, 25-34.
71. Schmidt, G., Sehr, P., Wilm, M., Selzer, J., Mann, M. and Aktories, K. (1997). Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387, 725-729.
72. Schmidt, G. and Aktories, K. (1998). Bacterial cytotoxins target Rho GTPases. Naturwissenschaften 85, 253-261.
73. Sears, C. L. and Kaper, J. B. (1996). Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60, 167-215.
74. Seasholtz, T. M., Zhang, T., Morissette, M. R., Howes, A. L., Yang, A. H. and Brown, J. H. (2001). Increased expression and activity of RhoA are associated with increased DNA synthesis and reduced p27(Kip1) expression in the vasculature of hypertensive rats. Circ. Res. 89, 488-495.
75. Sinnett-Smith, J., Lunn, J. A., Leopoldt, D. and Rozengurt, E. (2001). Y-27632, an inhibitor of Rho-associated kinases, prevents tyrosine phosphorylation of focal adhesion kinase and paxillin induced by bombesin: dissociation from tyrosine phosphorylation of p130(CAS). Exp. Cell Res. 266, 292-302.
76. Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H. and Takai, Y. (1997). Regulation of cell-cell adhesion by Rac and Rho small G proteins in MDCK cells. J. Cell Biol. 139, 1047-1059.
77. Troyanovsky, S. M. (1999). Mechanism of cell-cell adhesion complex assembly. Curr. Opin. Cell Biol. 5, 561-566.
78. Turner, C. E. (2000). Paxillin interactions. J. Cell Sci. 113, 4139-4140.
79. Turner, J. R. and Madara, J. L. (1995). Physiological regulation of intestinal epithelial tight junctions as a consequence of Na(+)-coupled nutrient transport. Gastroenterology 109, 1391-1396.
80. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. and Parton, R. G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
81. von Eichel-Streiber, C., Boquet, P., Sauerborn, M. and Thelestam, M. (1996). Large clostridial cytotoxins - a family of glycosyltransferases modifying small GTP-binding proteins. Trends Microbiol. 4, 375-382.
82. Vouret-Craviari, V., Grall, D., Flatau, G., Pouyssegur, J., Boquet, P. and Van Obberghen-Schilling, E. (1999). Effects of cytotoxic necrotizing factor 1 and lethal toxin on actin cytoskeleton and VE-cadherin localization in human endothelial cell monolayers. Infect. Immun. 67, 3002-3008.
83. Walsh, S. V., Hopkins, A. M., Chen, J., Narumiya, S., Parkos, C. A. and Nusrat, A. (2001). Rho-kinase regulates tight junction function and is necessary for tight junction assembly in polarized intestinal epithelia. Gastroenterology 121, 566-579.
84. Yuri K., Nakata, K., Katae, H., Yamamoto, S. and Hasegawa, A. (1998). Distribution of uropathogenic virulence factors among Escherichia coli strains isolated from dogs and cats. J. Vet. Med. Sci. 60, 287-290.