Activation of Rho through a cross-link with polyamines catalyzed by Bordetella dermonecrotizing toxin

EMBO Journal

Volumn 19, Issue 4, 2000, Pages 521-530

  Masuda, Minako ^a   Betancourt, Lazaro ^b   Matsuzawa, Takeshi ^a   Kashimoto, Takashige ^a   Takao, Toshifumi ^b   Shimonishi, Yasutsugu ^b   Horiguchi, Yasuhiko ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Bordetella dermonecrotizing toxin; Polyamine; Rho; Transglutaminase

Indexed keywords

BACTERIAL TOXIN; GUANOSINE TRIPHOSPHATASE; POLYAMINE; PUTRESCINE; RHO FACTOR; SPERMIDINE; SPERMINE;

ARTICLE; BORDETELLA; CATALYSIS; CROSS LINKING; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); BORDETELLA;

EID: 0034651790     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.4.521     Document Type: Article

References (50)

1. Aeschilimann, D. and Paulsson, M. (1994) Transglutaminases: protein cross-linking enzymes in tissues and body fluids. Thromb. Haemost., 71, 402-415.
2. Aktories, K. (1997) Rho proteins: targets for bacterial toxins. Trends Microbiol., 5, 282-288.
3. Amano, M., Mukai, H., Ono, Y., Chihara, K., Matsui, T., Hamajima, Y., Okawa, K., Iwamatsu, A. and Kaibuchi, K. (1996) Identification of a putative target for Rho as the serine-threonine kinase protein kinase N. Science, 271, 648-650.
4. Amano, M., Chihara, K., Kimura, K., Fukata, Y., Nakamura, N., Matsuura, Y. and Kaibuchi, K. (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science, 275, 1308-1311.
5. Beninati, S. and Folk, J.E. (1988) Covalent polyamine-protein conjugates: analysis and distribution. Adv. Exp. Med. Biol. 250, 411-422.
6. Beppu, T., Shirahata, A., Takahashi, N., Hosoda, H. and Samejima, K. (1995) Specific depletion of spermidine and spermine in HTC cells treated with inhibitors of aminopropyltransferases. J. Biochem., 117, 339-345.
7. Chen, K.Y. (1984) Transglutaminase catalyzed incorporation of putrescine into surface proteins of mouse neuroblastoma cells. Mol. Cell. Biochem., 58, 91-97.
8. Coburn, J. (1992) Pseudomonas aeruginosa exoenzyme S. Curr. Top. Microbiol. Immunol., 175, 133-143.
9. 2. J. Biochem., 113, 164-173.
10. Flatau, G., Lemichez, E., Gauthler, 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.
11. Folk, J.E. (1980) Transglutaminase. Annu. Rev. Biochem., 49, 517-531.
12. Folk, J.E., Park, M.H., Chung, S.I., Schrode, J., Lester, E.P. and Cooper, H.L. (1980) Polyamines as physiological substrates for transglutaminases. J. Biol. Chem., 255, 3695-3700.
13. ROCK, a Rho-associated coiled-coil containing protein kinase. J. Biol. Chem., 271, 23022-23028.
14. Fujisawa, K., Madaule, P., Ishizaki, T., Watanabe, G., Bito, H., Saito, Y., Hall, A. and Narumiya, S. (1998) Different regions of Rho determine Rho-selective binding of different classes of Rho target molecules. J. Biol. Chem., 273, 18943-18949.
15. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science, 279, 509-515.
16. Hill, C.S., Wynne, J. and Treisman, R. (1995) The rho family GTPases rhoA, racl and cdc42Hs regulate transcriptional activation by SRF. Cell, 81, 1159-1170.
17. Horiguchi, Y., Nakai, T. and Kume, K. (1990) Simplified procedure for purification of Bordetella bronchiseptica dermonecrotic toxin. FEMS Microbiol. Lett., 66, 39-43.
18. Horiguchi, Y., Nakai, T. and Kume, K. (1991) Effects of Bordetella bronchiseptica dermonecrotic toxin on the structure and function of osteoblastic clone MC3T3-E1 cells. Infect. Immun., 59, 1112-1116.
19. Horiguchi, Y., Sugimoto, N. and Matsuda, M. (1993) Stimulation of DNA synthesis in osteoblast-like MC3T3-E1 cells by Bordetella bronchiseptica dermonecrotic toxin. Infect. Immun., 61, 3611-3615.
20. Horiguchi, Y., Senda, T., Sugimoto, N., Katahira, J. and Matsuda, M. (1995) Bordetella bronchiseptica dermonecrotizing toxin stimulates assembly of actin fibers and focal adhesions by modifying the small GTP-binding protein rho. J. Cell Sci., 108, 3243-3251.
21. Horiguchi, Y., Inoue, N., Masuda, M., Kashimoto, T., Katahira, J., Sugimoto, N. and Matsuda, M. (1997) Bordetella bronchiseptica dermonecrotizing toxin induces reorganization of actin stress fibers through deamidation of Gin-63 of the GTP-binding protein Rho. Proc. Natl Acad. Sci. USA, 94, 11623-11626.
22. Ishizaki, T. et al. (1996) The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J., 15, 1885-1893.
23. Ishizaki, T., Naito, M., Fujiwara, K., Maekawa, M., Watanabe, N., Saito, Y. and Narumiya, S. (1997) p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett., 404, 118-124.
24. Janne, J., Poso, H. and Raina, A. (1978) Polyamines in rapid growth and cancer. Biochim. Biophys. Acta, 473, 241-293.
25. Johnson, R.S., Martin, S.A., Biemann, K., Stults, J.T. and Watson, J.T. (1987) Novel fragmentation process of peptides by collision-induced decomposition in a tandem mass spectrometer: differentiation of leucine and isoleucine. Anal. Chem., 59, 2621-2625.
26. Kanaji, T., Ozaki, H., Takao, T., Kawajiri, H., Ide, H., Motoki, M. and Shimonishi, Y. (1993) Primary structure of microbial transglutaminase from Streptoverticillium sp. strain s-8112. J. Biol. Chem., 268, 11565-11572.
27. Kashimoto, T., Katahira, J., Cornejo, W.R., Masuda, M., Fukuoh, A., Matsuzawa, T., Ohnishi, T. and Horiguchi, Y. (1999) Identification of functional domains of Bordetella dermonecrotizing toxin. Infect. Immun., 67, 3727-3732.
28. Kashiwagi, K. and Igarashi, K. (1988) Adjustment of polyamine contents in Escherichia coli. J. Bacteriol., 170, 3131-3135.
29. Kikuchi, A., Sasaki, T., Araki, S., Hata, Y. and Takai, Y. (1989) Purification and characterization from bovine brain cytosol of two GTPase-activating proteins specific for smg p21, a GTP-binding protein having the same effector domain as c-ras p2ls. J. Biol. Chem., 264, 9133-9136.
30. Kimura, K. et al. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science, 273, 245-248.
31. Kureishi, Y., Kobayashi, S., Amano, M., Kimura, K., Kanaide, H., Nakano, T., Kaibuchi, K. and Ito, M. (1997) Rho-associated kinase directly induces smooth muscle contraction through myosin light chain phosphorylation. J. Biol. Chem., 272, 12257-12260.
32. Leung, T., Manser, E., Tan, L. and Lim, L. (1995) A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem., 270, 29051-29054.
33. Leung, T., Chen, X., Manser, E. and Lim, L. (1996) The p160 RhoA-binding kinase ROKa is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol., 16, 5313-5327.
34. Madaule, P., Eda, M., Watanabe, N., Fujisawa, K., Matsuoka, T., Bito, H., Ishizaki, T. and Narumiya, S. (1998) Role of citron kinase as a target of the small GTPase Rho in cytokinesis. Nature, 394, 491-494.
35. Matsui, T. et al. (1996) Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP binding protein Rho. EMBO J., 15, 2208-2216.
36. Miki, H., Sasaki, T., Takai, Y. and Takenawa, T. (1998) Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature, 391, 93-96.
37. 1. Science, 269, 1270-1272.
38. rho induces rapid changes in cell morphology. J. Cell Biol., 111, 1001-1007.
39. Piacentini, M., Martinet, N., Beninati, S. and Folk, J.E. (1988) Free and protein-conjugated polyamines in mouse epidermal cells. Effect of high calcium and retinoic acid. J. Biol. Chem., 263, 3790-3794.
40. Reid, T., Furuyashiki, T., Ishizaki, T., Watanabe, G., Watanabe, N., Fujisawa, K., Morii, N., Madaule, P. and Narumiya, S. (1996) Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN and rhophilin in the Rho-binding domain. J. Biol. Chem., 271, 13556-13560.
41. Schmidt, G., Sehr, P. Wilm, M., Selzer, J., Mann, M. and Aktories, K. (1997) GIn 63 of Rho is deamidated by Excherichia coli cytotoxic necrotizing factor-1. Nature, 387, 725-729.
42. Schmidt, G., Selzer, J., Lerm, M. and Aktories, K. (1998) The Rho-deamidating cytotoxic necrotizing factor I from Escherichia coli possesses transglutaminase activity. J. Biol Chem., 273, 13669-13674.
43. Sin, W., Chen, X., Leung, T. and Lim, L. (1998) RhoA-binding kinase a translocation is facilitated by the collapse of the vimentin intermediate filament network. Mol. Cell. Biol., 18, 6325-6339.
44. Takaishi, K., Sasaki, T., Kato, M., Yamochi, W., Kuroda, S., Nakamura, T., Takeichi, M. and Takai, Y. (1994) Involvement of Rho p21 small GTP-binding protein and its regulator in the HGF-induced cell motility. Oncagene, 9, 273-279.
45. Uehata, M. et al. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature, 389, 990-994.
46. 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.
47. Watanabe, G. et al. (1996) Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small GTPase Rho. Science, 271, 645-648.
48. Watanabe, N., Kato, T. Fujita, A., Ishizaki, T. and Narumiya, S. (1999) Cooperation between mDial and ROCK in Rho-induced actin reorganization. Nature Cell Biol., 1, 136-143.
49. 1 phase of the cell cycle. Oncogene, 8, 1449-1455.
50. Zong, H., Raman, N., Mickelson-Young, L.A., Atkinson, S.J. and Quilliam, L.A. (1999) Loop 6 of RhoA confers specificity for effector binding, stress fiber formation and cellular transformation. J. Biol. Chem., 274, 4551-4560.