Ubiquitination in rho signaling

Current Topics in Medicinal Chemistry

Volumn 11, Issue 23, 2011, Pages 2879-2887

  Ding, Feng ^a   Yin, Zhenyu ^a   Wang, Hong Rui ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

E3 ubiquitin ligase; Rho GTPase; Ubiquitination

Indexed keywords

CUL3 PROTEIN; CYTOTOXIC NECROTIZING FACTOR 1; PROTEASOME; RAC1 PROTEIN; REGULATOR PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMURF1 PROTEIN; SYNAPTOPODIN; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL FATE; CELL FUNCTION; CELL MOTILITY; CELL POLARITY; DROSOPHILA; HUMAN; MAMMAL CELL; METASTASIS; NERVE CELL; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 83455178869     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/156802611798281357     Document Type: Article

References (74)

1. Takai, Y.; Sasaki, T.; Matozaki, T. Small GTP-binding proteins. Physiol. Rev., 2001, 81,153-208.
2. Aspenstrom, P.; Ruusala, A.; Pacholsky, D. Taking Rho GTPases to the next level: the cellular functions of atypical Rho GTPases. Exp. Cell Res., 2007, 313, 3673-3679.
3. Etienne-Manneville, S.; Hall, A. Rho GTPases in cell biology. Nature, 2002, 420, 629-635.
4. Boettner, B.; Van Aelst, L. The role of Rho GTPases in disease development. Gene, 2002, 286, 155-174.
5. Bustelo, X.R.; Sauzeau, V.; Berenjeno, I.M. GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bioessays, 2007, 29, 356-370.
6. Jaffe, A.B.; Hall, A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol., 2005, 21, 247-269.
7. Kaibuchi, K.; Kuroda, S.; Amano, M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem., 1999, 68, 459-486.
8. Olofsson, B. Rho guanine dissociation inhibitors: pivotal molecules in cellular signalling. Cell Signal, 1999, 11, 545-554.
9. Welchman, R.L.; Gordon, C.; Mayer, R.J. Ubiquitin and ubiquitinlike proteins as multifunctional signals. Nat. Rev. Mol. Cell Biol., 2005, 6, 599-609.
10. Ikeda, F.; Dikic, I. Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep., 2008, 9, 536-542.
11. Pickart, C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem., 2001, 70, 503-533.
12. Schrader, E.K.; Harstad, K.G.; Matouschek, A. Targeting proteins for degradation. Nat. Chem. Biol., 2009, 5, 815-822.
13. Haglund, K.; Dikic, I. Ubiquitylation and cell signaling. EMBO J., 2005, 24, 3353-3359.
14. Hershko, A.; Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem., 1998, 67, 425-479.
15. Hoeller, D.; Hecker, C.M.; Dikic, I. Ubiquitin and ubiquitin-like proteins in cancer pathogenesis. Nat. Rev. Cancer, 2006, 6, 776-788.
16. Zhou, H.; Wertz, I.; O'Rourke, K.; Ultsch, M.; Seshagiri, S.; Eby, M.; Xiao, W.; Dixit, V.M. Bcl10 activates the NF-kappaB pathway through ubiquitination of NEMO. Nature, 2004, 427, 167-171.
17. Deshaies, R.J.; Joazeiro, C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem., 2009, 78, 399-434.
18. Doye, A.; Mettouchi, A.; Bossis, G.; Clement, R.; Buisson-Touati, C.; Flatau, G.; Gagnoux, L.; Piechaczyk, M.; Boquet, P.; Lemichez, E. CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell, 2002, 111, 553-564.
19. Wang, H.R.; Zhang, Y.; Ozdamar, B.; Ogunjimi, A.A.; Alexandrova, E.; Thomsen, G.H.; Wrana, J.L. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science, 2003, 302, 1775-1779.
20. Boquet, P. The cytotoxic necrotizing factor 1 (CNF1) from Escherichia coli. Toxicon, 2001, 39, 1673-1680.
21. Munro, P.; Flatau, G.; Doye, A.; Boyer, L.; Oregioni, O.; Mege, J.L.; Landraud, L.; Lemichez, E. Activation and proteasomal degradation of rho GTPases by cytotoxic necrotizing factor-1 elicit a controlled inflammatory response. J. Biol. Chem., 2004, 279, 35849-35857.
22. Doye, A.; Boyer, L.; Mettouchi, A.; Lemichez, E. Ubiquitinmediated proteasomal degradation of Rho proteins by the CNF1 toxin. Methods Enzymol., 2006, 406, 447-456.
23. Visvikis, O.; Lores, P.; Boyer, L.; Chardin, P.; Lemichez, E.; Gacon, G. Activated Rac1, but not the tumorigenic variant Rac1b, is ubiquitinated on Lys 147 through a JNK-regulated process. FEBS J., 2008, 275, 386-396.
24. Schwamborn, J.C.; Muller, M.; Becker, A.H.; Puschel, A.W. Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J., 2007, 26, 1410-1422.
25. Massague, J. TGF-beta signal transduction. Annu. Rev. Biochem., 1998, 67, 753-791.
26. Attisano, L.; Wrana, J.L. Signal transduction by the TGF-beta superfamily. Science, 2002, 296, 1646-1647.
27. Shi, Y.; Massague, J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 2003, 113, 685-700.
28. Zhu, H.; Kavsak, P.; Abdollah, S.; Wrana, J.L.; Thomsen, G.H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature, 1999, 400, 687-693.
29. Izzi, L.; Attisano, L. Regulation of the TGFbeta signalling pathway by ubiquitin-mediated degradation. Oncogene, 2004, 23, 2071-2078.
30. Kavsak, P.; Rasmussen, R.K.; Causing, C.G.; Bonni, S.; Zhu, H.; Thomsen, G.H.; Wrana, J.L. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol. Cell, 2000, 6, 1365-1375.
31. Lin, X.; Liang, M.; Feng, X.H. Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem., 2000, 275, 36818-36822.
32. Zhang, Y.; Chang, C.; Gehling, D.J.; Hemmati-Brivanlou, A.; Derynck, R. Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl. Acad. Sci. USA, 2001, 98, 974-979.
33. Inoue, Y.; Imamura, T. Regulation of TGF-beta family signaling by E3 ubiquitin ligases. Cancer Sci., 2008, 99, 2107-2112.
34. Etienne-Manneville, S.; Hall, A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell, 2001, 106, 489-498.
35. Joberty, G.; Petersen, C.; Gao, L.; Macara, I.G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol., 2000, 2, 531-539.
36. Lin, D.; Edwards, A.S.; Fawcett, J.P.; Mbamalu, G.; Scott, J.D.; Pawson, T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat. Cell Biol., 2000, 2, 540-547.
37. Qiu, R.G.; Abo, A.; Steven Martin, G. A human homolog of the C. elegans polarity determinant Par-6 links Rac and Cdc42 to PKCzeta signaling and cell transformation. Curr. Biol., 2000, 10, 697-707.
38. Jaffe, A.B.; Hall, A. Cell biology. Smurfing at the leading edge. Science, 2003, 302, 1690-1691.
39. Boyer, L.; Turchi, L.; Desnues, B.; Doye, A.; Ponzio, G.; Mege, J.L.; Yamashita, M.; Zhang, Y.E.; Bertoglio, J.; Flatau, G. et al. CNF1-induced ubiquitylation and proteasome destruction of activated RhoA is impaired in Smurf1-/- cells. Mol. Biol. Cell, 2006, 17, 2489-2497.
40. Ozdamar, B.; Bose, R.; Barrios-Rodiles, M.; Wang, H.R.; Zhang, Y.; Wrana, J.L. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science, 2005, 307, 1603-1609.
41. Grunert, S.; Jechlinger, M.; Beug, H. Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat. Rev. Mol. Cell Biol., 2003, 4, 657-665.
42. Miyoshi, J.; Takai, Y. Molecular perspective on tight-junction assembly and epithelial polarity. Adv. Drug Deliv. Rev., 2005, 57, 815-855.
43. Shook, D.; Keller, R. Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech. Dev., 2003, 120, 1351-1383.
44. Wodarz, A.; Nathke, I. Cell polarity in development and cancer. Nat. Cell Biol., 2007, 9, 1016-1024.
45. Chiang, A.C.; Massague, J. Molecular basis of metastasis. N. Engl. J. Med., 2008, 359, 2814-2823.
46. Kang, Y.; Massague, J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell, 2004, 118, 277-279.
47. Nguyen, D.X.; Bos, P.D.; Massague, J. Metastasis: from dissemination to organ-specific colonization. Nat. Rev. Cancer, 2009, 9, 274-284.
48. Massague, J. TGFbeta in cancer. Cell, 2008, 134, 215-230.
49. Padua, D.; Massague, J. Roles of TGFbeta in metastasis. Cell Res., 2009, 19, 89-102.
50. Sahai, E.; Garcia-Medina, R.; Pouyssegur, J.; Vial, E. Smurf1 regulates tumor cell plasticity and motility through degradation of RhoA leading to localized inhibition of contractility. J. Cell Biol., 2007, 176, 35-42.
51. Sahai, E.; Marshall, C.J. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol., 2003, 5, 711-719.
52. Mundel, P.; Heid, H.W.; Mundel, T.M.; Kruger, M.; Reiser, J.; Kriz, W. Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes. J. Cell Biol., 1997, 139, 193-204.
53. Asanuma, K.; Yanagida-Asanuma, E.; Faul, C.; Tomino, Y.; Kim, K.; Mundel, P. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat. Cell Biol., 2006, 8, 485-491.
54. Schwamborn, J.C.; Puschel, A.W. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci., 2004, 7, 923-929.
55. Schwamborn, J.C.; Khazaei, M.R.; Puschel, A.W. The interaction of mPar3 with the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. J. Biol. Chem., 2007, 282, 35259-35268.
56. Deshaies, R.J. SCF and Cullin/Ring H2-based ubiquitin ligases. Annu. Rev. Cell Dev. Biol., 1999, 15, 435-467.
57. Geyer, R.; Wee, S.; Anderson, S.; Yates, J.; Wolf, D.A. BTB/POZ domain proteins are putative substrate adaptors for cullin 3 ubiquitin ligases. Mol. Cell, 2003, 12, 783-790.
58. Pintard, L.; Willis, J.H.; Willems, A.; Johnson, J.L.; Srayko, M.; Kurz, T.; Glaser, S.; Mains, P.E.; Tyers, M.; Bowerman, B.; Peter, M. The BTB protein MEL-26 is a substrate-specific adaptor of the CUL-3 ubiquitin-ligase. Nature, 2003, 425, 311-316.
59. Wilkins, A.; Ping, Q.; Carpenter, C.L. RhoBTB2 is a substrate of the mammalian Cul3 ubiquitin ligase complex. Genes Dev., 2004, 18, 856-861.
60. Hamaguchi, M.; Meth, J.L.; von Klitzing, C.; Wei, W.; Esposito, D.; Rodgers, L.; Walsh, T.; Welcsh, P.; King, M.C.; Wigler, M.H. DBC2, a candidate for a tumor suppressor gene involved in breast cancer. Proc. Natl. Acad. Sci. USA, 2002, 99, 13647-13652.
61. Cho, Y.G.; Choi, B.J.; Kim, C.J.; Song, J.H.; Zhang, C.; Nam, S.W.; Lee, J.Y.; Park, W.S. Genetic analysis of the DBC2 gene in gastric cancer. Acta Oncol., 2008, 47, 366-371.
62. Knowles, M.A.; Aveyard, J.S.; Taylor, C.F.; Harnden, P.; Bass, S. Mutation analysis of the 8p candidate tumour suppressor genes DBC2 (RHOBTB2) and LZTS1 in bladder cancer. Cancer Lett., 2005, 225, 121-130.
63. Berthold, J.; Schenkova, K.; Ramos, S.; Miura, Y.; Furukawa, M.; Aspenstrom, P.; Rivero, F. Characterization of RhoBTB-dependent Cul3 ubiquitin ligase complexes--evidence for an autoregulatory mechanism. Exp. Cell Res., 2008, 314, 3453-3465.
64. Chang, F.K.; Sato, N.; Kobayashi-Simorowski, N.; Yoshihara, T.; Meth, J.L.; Hamaguchi, M. DBC2 is essential for transporting vesicular stomatitis virus glycoprotein. J. Mol. Biol., 2006, 364, 302-308.
65. Chen, Y.; Yang, Z.; Meng, M.; Zhao, Y.; Dong, N.; Yan, H.; Liu, L.; Ding, M.; Peng, H.B.; Shao, F. Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell, 2009, 35, 841-855.
66. Stogios, P.J.; Downs, G.S.; Jauhal, J.J.; Nandra, S.K.; Prive, G.G. Sequence and structural analysis of BTB domain proteins. Genome Biol., 2005, 6, R82.
67. Su, L.; Lineberry, N.; Huh, Y.; Soares, L.; Fathman, C.G. A novel E3 ubiquitin ligase substrate screen identifies Rho guanine dissociation inhibitor as a substrate of gene related to anergy in lymphocytes. J. Immunol., 2006, 177, 7559-7566.
68. Huibregtse, J.M.; Scheffner, M.; Howley, P.M. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell Biol., 1993, 13, 775-784.
69. Jiang, Y.; Lev-Lehman, E.; Bressler, J.; Tsai, T.F.; Beaudet, A.L. Genetics of Angelman syndrome. Am. J. Hum. Genet., 1999, 65, 1-6.
70. Prokopenko, S.N.; Brumby, A.; O'Keefe, L.; Prior, L.; He, Y.; Saint, R.; Bellen, H.J. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev., 1999, 13, 2301-2314.
71. Reiter, L.T.; Seagroves, T.N.; Bowers, M.; Bier, E. Expression of the Rho-GEF Pbl/ECT2 is regulated by the UBE3A E3 ubiquitin ligase. Hum. Mol. Genet., 2006, 15, 2825-2835.
72. Tatsumoto, T.; Xie, X.; Blumenthal, R.; Okamoto, I.; Miki, T. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J. Cell Biol., 1999, 147, 921-928.
73. Yamaguchi, K.; Ohara, O.; Ando, A.; Nagase, T. Smurf1 directly targets hPEM-2, a GEF for Cdc42, via a novel combination of protein interaction modules in the ubiquitin-proteasome pathway. Biol. Chem., 2008, 389, 405-413.
74. Carr, H.S.; Cai, C.; Keinanen, K.; Frost, J.A. Interaction of the RhoA exchange factor Net1 with discs large homolog 1 protects it from proteasome-mediated degradation and potentiates Net1 activity. J. Biol. Chem., 2009, 284, 24269-24280.