Cytoprotective effect of the small GTPase RhoB expressed upon treatment of fibroblasts with the Ras-glucosylating Clostridium sordellii lethal toxin

FEBS Letters

Volumn 586, Issue 20, 2012, Pages 3665-3673

  Huelsenbeck, Johannes ^a   May, Martin ^a   Schulz, Florian ^a   Schelle, Ilona ^a   Ronkina, Natalia ^a   Hohenegger, Martin ^b   Fritz, Gerhard ^c   Just, Ingo ^a   Gerhard, Ralf ^a   Genth, Harald ^a  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Apoptosis; Caspase; Glucosyltransferase; P38 Map kinase; Proteasome

Indexed keywords

CASPASE 3; CLOSTRIDIUM TOXIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; APOPTOSIS; BACTERIAL TOXINS; CASPASES; CLOSTRIDIUM SORDELLII; ENZYME ACTIVATION; FIBROBLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLYCOSYLATION; MICE; NIH 3T3 CELLS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEOLYSIS; RAS PROTEINS; RHOB GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

CLOSTRIDIUM SORDELLII;

EID: 84867571726     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.08.024     Document Type: Article

References (60)

1. A.B. Jaffe, and A. Hall Rho GTPases: biochemistry and biology Annu. Rev. Cell Dev. Biol. 21 2005 247 269
2. R. Karlsson, E.D. Pedersen, Z. Wang, and C. Brakebusch Rho GTPase function in tumorigenesis Biochim. Biophys. Acta 1796 2009 91 98
3. G. Fritz, I. Just, and B. Kaina Rho GTPases are over-expressed in human tumors Int. J. Cancer 81 1999 682 687
4. J. Zhou, Y. Zhu, G. Zhang, N. Liu, L. Sun, M. Liu, M. Qiu, D. Luo, Q. Tang, Z. Liao, Y. Zheng, and F. Bi A distinct role of RhoB in gastric cancer suppression Int. J. Cancer 128 2011 1057 1068
5. M. Huang, and G.C. Prendergast RhoB in cancer suppression Histol. Histopathol. 21 2006 213 218
6. G. Fritz, and B. Kaina Ras-related GTPase RhoB forces alkylation-induced apoptotic cell death Biochem. Biophys. Res. Commun. 268 2000 784 789
7. Ax. Liu, G.J. Cerniglia, E.J. Bernhard, and G.C. Prendergast RhoB is required to mediate apoptosis in neoplastically transformed cells after DNA damage Proc. Natl. Acad. Sci. USA 98 2001 6192 6197
8. K. Jiang, F.L. Delarue, and S.M. Sebti EGFR, ErbB2 and Ras but not Src suppress RhoB expression while ectopic expression of RhoB antagonizes oncogene-mediated transformation Oncogene 23 2004 1136 1145
9. K. Jiang, J. Sun, J. Cheng, J.Y. Djeu, S. Wei, and S. Sebti Akt mediates Ras downregulation of RhoB, a suppressor of transformation, invasion, and metastasis Mol. Cell. Biol. 24 2004 5565 5576
10. G. Fritz, and B. Kaina RhoB encoding a UV-inducible ras-related small GTP-binding prottein is regulated by GTPases of the Rho family and independent of JNK, ERK, and p38 MAP kinase J. Biol. Chem. 272 1997 30637 30644
11. K. Wennerberg, and C.J. Der Rho-family GTPases: it's not only Rac and Rho (and I like it) J. Cell Sci. 117 2004 1301 1312
12. T. Malcolm, E. Ettehadieh, and I. Sadowski Mitogen-responsive expression of RhoB is reulated by RNA stability Oncogene 22 2003 6142 6150
13. F.L. Delarue, J. Adnane, B. Joshi, M.A. Blaskovich, D.A. Wang, J. Hawker, F. Bizouarn, J. Ohkanda, K. Zhu, A.D. Hamilton, S. Chellappan, and S.M. Sebti Farnesyltransferase and geranylgeranyltransferase I inhibitors upregulate RhoB expression by HDAC1 dissociation, HAT association and histone acetylation of the RhoB promoter Oncogene 26 2007 633 640
14. G. Fritz, and B. Kaina Rho GTPases: promising cellular targets for novel anticancer drugs Curr. Cancer Drug Targets 6 2006 1 14
15. H. Genth, and I. Just Functional implications of lethal toxin-catalysed glucosylation of (H/K/N)Ras and Rac1 in Clostridium sordellii-associated disease Eur. J. Cell Biol. 90 2011 959 965
16. M.J. Aldape, A.E. Bryant, and D.L. Stevens Clostridium sordellii infection: epidemiology, clinical findings, and current perspectives on diagnosis and treatment Clin. Infect. Dis. 43 2006 1436 1446
17. S.C. Huelsenbeck, I. Klose, M. Reichenbach, J. Huelsenbeck, and H. Genth Distinct kinetics of (H/K/N)Ras glucosylation and Rac1 glucosylation catalysed by Clostridium sordellii lethal toxin FEBS Lett. 583 2009 3133 3139
18. M.R. Popoff, and B. Geny Rho/Ras-GTPase-dependent and -independent activity of clostridial glucosylating toxins J. Med. Microbiol. 60 2011 1057 1069
19. H. Genth, F. Schulz, and I. Just Glucosylation of Rho/Ras proteins by lethal toxin - implications of actin re-organization and apoptosis in C. sordellii-associated disease Open Toxinol. J. 3 2010 13 18
20. S.C. Dreger, F. Schulz, J. Huelsenbeck, R. Gerhard, F. Hofmann, I. Just, and H. Genth Killing of rat basophilic leukemia cells by lethal toxin from Clostridium sordellii: critical role of phosphatidylinositide 3′-OH kinase/Akt signaling Biochemistry 48 2009 1785 1792
21. F. Schulz, I. Just, and H. Genth Prevention of Clostridium sordellii lethal toxin-induced apoptotic cell death by tauroursodeoxycholic acid Biochemistry 48 2009 9002 9010
22. D.E. Voth, and J.D. Ballard Critical intermediate steps in Clostridium sordellii lethal toxin-induced apoptosis Biochem. Biophys. Res. Commun. 363 2007 959 964
23. B. Geny, and M.R. Popoff Activation of a c-Jun-NH2-terminal kinase pathway by the lethal toxin from Clostridium sordellii, TcsL-82, occurs independently of the toxin intrinsic enzymatic activity and facilitates small GTPase glucosylation Cell Microbiol. 11 2009 1102 1113
24. H. Genth, J. Selzer, C. Busch, J. Dumbach, F. Hofmann, K. Aktories, and I. Just New method to generate enzymatically deficient Clostridium difficile toxin B as an antigen for immunization Infect. Immun. 68 2000 1094 1101
25. M. Huang, U. Kamasani, and G.C. Prendergast RhoB facilitates c-Myc turnover by supporting efficient nuclear accumulation of GSK-3 Oncogene 25 2006 1281 1289
26. R.H. Adams, A. Porras, G. Alonso, M. Jones, K. Vintersten, S. Panelli, A. Valladares, L. Perez, R. Klein, and A.R. Nebreda Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development Mol. Cell 6 2000 109 116
27. H. Genth, J. Huelsenbeck, B. Hartmann, F. Hofmann, I. Just, and R. Gerhard Cellular stability of Rho-GTPases glucosylated by Clostridium difficile toxin B FEBS Lett. 580 2006 3565 3569
28. J. Huelsenbeck, S. Dreger, R. Gerhard, H. Barth, I. Just, and H. Genth Difference in the cytotoxic effects of toxin B from Clostridium difficile strain VPI 10463 and toxin B from variant Clostridium difficile strain 1470 Infect. Immun. 75 2007 801 809
29. S. Sola, M.M. Aranha, C.J. Steer, and C.M. Rodrigues Game and players: mitochondrial apoptosis and the therapeutic potential of ursodeoxycholic acid Curr. Issues Mol. Biol. 9 2007 123 138
30. R. Gerhard, H. Tatge, H. Genth, T. Thum, J. Borlak, G. Fritz, and I. Just Clostridium difficile toxin A induces expression of the stress-induced early gene product RhoB J. Biol. Chem. 280 2005 1499 1505
31. J. Ahn, J.H. Choi, M. Won, C.M. Kang, M.R. Gyun, H.M. Park, C.H. Kim, and K.S. Chung The activation of p38 MAPK primarily contributes to UV-induced RhoB expression by recruiting the c-Jun and p300 to the distal CCAAT box of the RhoB promoter Biochem. Biophys. Res. Commun. 409 2011 211 216
32. D. Faust, I. Dolado, A. Cuadrado, F. Oesch, C. Weiss, A.R. Nebreda, and C. Dietrich P38alpha MAPK is required for contact inhibition Oncogene 24 2005 7941 7945
33. P.R. Young, M.M. McLaughlin, S. Kumar, S. Kassis, M.L. Doyle, D. McNulty, T.F. Gallagher, S. Fisher, P.C. McDonnell, S.A. Carr, M.J. Huddleston, G. Seibel, T.G. Porter, G.P. Livi, J.L. Adams, and J.C. Lee Pyridinyl imidazole inhibitors of p38 mitogen-activated protein kinase bind in the ATP site J. Biol. Chem. 272 1997 12116 12121
34. C.C. Lanning, J.L. Daddona, R. Ruiz-Velasco, S.H. Shafer, and C.L. Williams The Rac1 C-terminal polybasic region regulates the nuclear localization and protein degradation of Rac1 J. Biol. Chem. 279 2004 44197 44210
35. P. Petit, J. Bréard, V. Montalescot, N.B. El Hadj, T. Levade, M. Popoff, and B. Geny Lethal toxin from Clostridium sordellii induces apoptotic cell death by disruption of mitochondrial homeostasis in HL-60 cells Cell. Microbiol. 5 2003 761 771
36. T.T. Ho, S.D. Merajver, C.M. Lapiere, B.V. Nusgens, and C.F. Deroanne RhoA-GDP regulates RhoB protein stability. Potential involvement of RhoGDIalpha J. Biol. Chem. 283 2008 21588 21598
37. J. Milia, F. Teyssier, F. Dalenc, I. Ader, C. Delmas, A. Pradines, I. Lajoie-Mazenc, R. Baron, J. Bonnet, E. Cohen-Jonathan, G. Favre, and C. Toulas Farnesylated RhoB inhibits radiation-induced mitotic cell death and controls radiation-induced centrosome overduplication Cell Death Differ. 12 2005 492 501
38. B. Canguilhem, A. Pradines, C. Baudouin, C. Boby, I. Lajoie-Mazenc, M. Charveron, and G. Favre RhoB protects human keratinocytes from UVB-induced apoptosis through epidermal growth factor receptor signaling J. Biol. Chem. 280 2005 43257 43263
39. J. Huelsenbeck, S.C. Dreger, R. Gerhard, G. Fritz, I. Just, and H. Genth Upregulation of the immediate early gene product RhoB by exoenzyme C3 from Clostridium limosum and Toxin B from Clostridium difficile Biochemistry 46 2007 4923 4931
40. K. Koera, K. Nakamura, K. Nakao, J. Miyoshi, K. Toyoshima, T. Hatta, H. Otani, A. Aiba, and M. Katsuki K-ras is essential for the development of the mouse embryo Oncogene 15 1997 1151 1159
41. L. Johnson, D. Greenbaum, K. Cichowski, K. Mercer, E. Murphy, E. Schmitt, R.T. Bronson, H. Umanoff, W. Edelmann, R. Kucherlapati, and T. Jacks K-ras is an essential gene in the mouse with partial functional overlap with N-ras Genes Dev. 11 1997 2468 2481
42. J. Zhang, and H.F. Lodish Identification of K-ras as the major regulator for cytokine-dependent Akt activation in erythroid progenitors in vivo Proc. Natl. Acad. Sci. USA 102 2005 14605 14610
43. L. Liu, S. Zhu, Z. Gong, and B.C. Low K-ras/PI3K-Akt signaling is essential for zebrafish hematopoiesis and angiogenesis PLoS ONE 3 2008 e2850
44. J.A. Choi, M.T. Park, C.M. Kang, H.D. Um, S. Bae, K.H. Lee, T.H. Kim, J.H. Kim, C.K. Cho, Y.S. Lee, H.Y. Chung, and S.J. Lee Opposite effects of Ha-Ras and Ki-Ras on radiation-induced apoptosis via differential activation of PI3K/Akt and Rac/p38 mitogen-activated protein kinase signaling pathways Oncogene 23 2004 9 20
45. K. Otkjaer, H. Holtmann, T.W. Kragstrup, S.R. Paludan, C. Johansen, M. Gaestel, K. Kragballe, and L. Iversen The p38 MAPK regulates IL-24 expression by stabilization of the 3′ UTR of IL-24 mRNA PLoS ONE 5 2010 e8671
46. V. Lafarga, A. Cuadrado, I. Lopez de Silanes, R. Bengoechea, O. Fernandez-Capetillo, and A.R. Nebreda P38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint Mol. Cell. Biol. 29 2009 4341 4351
47. A. Dasari, J.N. Bartholomew, D. Volonte, and F. Galbiati Oxidative stress induces premature senescence by stimulating caveolin-1 gene transcription through p38 mitogen-activated protein kinase/Sp1-mediated activation of two GC-rich promoter elements Cancer Res. 66 2006 10805 10814
48. G. Fritz, and B. Kaina RhoB encoding a UV-inducible Ras-related small GTP-binding protein is regulated by GTPases of the Rho family and independent of JNK, ERK, and p38 MAP kinase J. Biol. Chem. 272 1997 30637 30644
49. G. Fritz, and B. Kaina Transcriptional activation of the small GTPase gene rhoB by genotoxic stress is regulated via a CCAAT element Nucleic Acids Res. 29 2001 792 798
50. S. Wang, Y. Yan-Neale, D. Fischer, M. Zeremski, R. Cai, J. Zhu, F. Asselbergs, G. Hampton, and D. Cohen Histone deacetylase 1 represses the small GTPase RhoB expression in human nonsmall lung carcinoma cell line Oncogene 22 2003 6204 6213
51. K.L. Rossman, C.J. Der, and J. Sondek GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors Nat. Rev. Mol. Cell Biol. 6 2005 167 180
52. E. Chaves-Olarte, E. Freer, A. Parra, C. Guzmán-Verri, E. Moreno, and M. Thelestam R-Ras glucosylation and transient RhoA activation determine the cytopathic effect produced by toxin B variants from toxin A-negative strains of Clostridium difficile J. Biol. Chem. 278 2003 7956 7963
53. P.F. Lebowitz, J.P. Davide, and G.C. Prendergast Evidence that farnesyltransferase inhibitors supress ras transformation by interfering with rho activity Mol. Cell. Biol. 15 1995 6613 6622
54. M.E. Engel, P.K. Datta, and H.L. Moses RhoB is stabilized by transforming growth factor β and antagonizes transcriptional activation J. Biol. Chem. 273 1998 9921 9926
55. E. Gasteiger, A. Gattiker, C. Hoogland, I. Ivanyi, R.D. Appel, and A. Bairoch ExPASy: The proteomics server for in-depth protein knowledge and analysis Nucleic Acids Res. 31 2003 3784 3788
56. J.Y. Kong, and S.W. Rabkin The association between RhoB and caspase-2: changes with lovastatin-induced apoptosis Biochem. Cell Biol. 83 2005 608 619
57. M. Hebert, S. Potin, M. Sebbagh, J. Bertoglio, J. Breard, and J. Hamelin Rho-ROCK-dependent ezrin-radixin-moesin phosphorylation regulates Fas-mediated apoptosis in Jurkat cells J. Immunol. 181 2008 5963 5973
58. A.D. Deward, K. Leali, R.A. West, G.C. Prendergast, and A.S. Alberts Loss of RhoB expression enhances the myelodysplastic phenotype of mammalian diaphanous-related formin mDia1 knockout mice PLoS ONE 4 9 2009 e7102
59. S. Barberan, K. McNair, K. Iqbal, N.C. Smith, G.C. Prendergast, T.W. Stone, S.R. Cobb, and B.J. Morris Altered apoptotic responses in neurons lacking RhoB GTPase Eur. J. Neurosci. 34 2011 1737 1746
60. J. Downward Targeting RAS signalling pathways in cancer therapy Nat. Rev. Cancer 3 2003 11 22