Direct modifications of Rho proteins: Deconstructing GTPase regulation

Biology of the Cell

Volumn 102, Issue 7, 2010, Pages 377-389

  Visvikis, Orane ^a,b   Maddugoda, Madhavi P ^a,b   Lemichez, Emmanuel ^a,b,c  

^a CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

Author keywords

Actin cytoskeleton; Pathogenic bacterium; Post translational modification; Rho protein; Toxin; Virulence factor

Indexed keywords

RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; VIRULENCE FACTOR;

ADENOSINE DIPHOSPHATE RIBOSYLATION; AMPYLATION; BACTERIUM; COVALENT BOND; DEAMINATION; GLUCOSAMINYLATION; GLYCOSYLATION; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HYDROLYSIS; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SECRETION; REGULATORY MECHANISM; REVIEW; TRANSGLUTAMINATION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; ENZYME ACTIVATION; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN PROCESSING, POST-TRANSLATIONAL; RHO GTP-BINDING PROTEINS; UBIQUITINATION; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS);

EID: 77954858290     PISSN: 02484900     EISSN: 1768322X     Source Type: Journal    
DOI: 10.1042/BC20090151     Document Type: Review

References (98)

1. Aktories, K. and Barbieri, J.T. (2005) Bacterial cytotoxins: targeting eukaryotic switches. Nat. Rev. Microbiol. 3, 397-410
2. *Ambruso, D.R., Knall, C., Abell, A.N., Panepinto, J., Kurkchubasche, A., Thurman, G., Gonzalez-Aller, C., Hiester, A., deBoer, M., Harbeck, R.J., Oyer, R., Johnson, G.L. and Roos, D. (2000) Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc. Natl. Acad. Sci. U.S.A. 97, 4654-4659
3. Arbibe, L., Mira, J.P., Teusch, N., Kline, L., Guha, M., Mackman, N., Godowski, P.J., Ulevitch, R.J. and Knaus, U.G. (2000) Toll-like receptor 2-mediated NF-κB activation requires a Rac1-dependent pathway. Nat. Immunol. 1, 533-540
4. Aspenstrom, P., Ruusala, A. and Pacholsky, D. (2007) Taking Rho GTPases to the next level: the cellular functions of atypical Rho GTPases. Exp. Cell Res. 313, 3673-3679
5. Bokoch, G.M. (2005) Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 15, 163-171 (Pubitemid 40332539)
6. Boquet, P. and Lemichez, E. (2003) Bacterial virulence factors targeting Rho GTPases: parasitism or symbiosis? Trends Cell Biol. 13, 238-246
7. -/- cells. Mol. Biol. Cell 17, 2489-2497
8. *Boyer, L., Doye, A., Rolando, M., Flatau, G., Munro, P., Gounon, P., Clement, R., Pulcini, C., Popoff, M.R., Mettouchi, A., Landraud, L., Dussurget, O. and Lemichez, E. (2006b) Induction of transient macroapertures in endothelial cells through RhoA inhibition by Staphylococcus aureus factors. J. Cell Biol. 173, 809-819
9. Carman, C.V. and Springer, T.A. (2008) Trans-cellular migration: cell - cell contacts get intimate. Curr. Opin. Cell Biol. 20, 533-540
10. Chardin, P. (2006) Function and regulation of Rnd proteins. Nat. Rev. Mol. Cell Biol. 7, 54-62
11. *Chardin, P., Boquet, P., Madaule, P., Popoff, M.R., Rubin, E.J. and Gill, D.M. (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
12. Chaves-Olarte, E., Low, P., Freer, E., Norlin, T., Weidmann, M., von Eichel-Streiber, C. and Thelestam, M. (1999) A novel cytotoxin from Clostridium difficile serogroup F is a functional hybrid between two other large clostridial cytotoxins. J. Biol. Chem. 274, 11046-11052
13. Chen, C. and Matesic, L.E. (2007) The Nedd4-like family of E3 ubiquitin ligases and cancer. Cancer Metastasis Rev. 26, 587-604 (Pubitemid 350119775)
14. Chen, Y., Yang, Z., Meng, M., Zhao, Y., Dong, N., Yan, H., Liu, L., Ding, M., Peng, H.B. and Shao, F. (2009) Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell 35, 841-855
15. Dai, Y., Dudek, N.L., Patel, T.B. and Muma, N.A. (2008) Transglutaminase-catalyzed transamidation: a novel mechanism for Rac1 activation by 5-hydroxytryptamine2A receptor stimulation. J. Pharmacol. Exp. Ther. 326, 153-162
16. DerMardirossian, C. and Bokoch, G.M. (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15, 356-363 (Pubitemid 40943524)
17. Diebold, B.A. and Bokoch, G.M. (2005) Rho GTPases and the control of the oxidative burst in polymorphonuclear leukocytes. Curr. Top. Microbiol. Immunol. 291, 91-111
18. *Doye, A., Mettouchi, A., Bossis, G., Clement, R., Buisson-Touati, C., Flatau, G., Gagnoux, L., Piechaczyk, M., Boquet, P. and Lemichez, E. (2002) CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 111, 553-564
19. Doye, A., Boyer, L., Mettouchi, A. and Lemichez, E. (2006) Ubiquitin-mediated proteasomal degradation of Rho proteins by the CNF1 toxin. Methods Enzymol. 406, 447-456 (Pubitemid 43207458)
20. Ellerbroek, S.M., Wennerberg, K. and Burridge, K. (2003) Serine phosphorylation negatively regulates RhoA in vivo. J. Biol. Chem. 278, 19023-19031
21. Engel, M.E., Datta, P.K. and Moses, H.L. (1998) RhoB is stabilized by transforming growth factor β and antagonizes transcriptional activation. J. Biol. Chem. 273, 9921-9926
22. Etienne-Manneville, S. and Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635
23. Faber, P.W., Barnes, G.T., Srinidhi, J., Chen, J., Gusella, J.F. and MacDonald, M.E. (1998) Huntingtin interacts with a family of WW domain proteins. Hum. Mol. Genet. 7, 1463-1474
24. *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
25. Fueller, F. and Schmidt, G. (2008) The polybasic region of Rho GTPases defines the cleavage by Yersinia enterocolitica outer protein T (YopT). Protein Sci. 17, 1456-1462
26. Fujihara, H., Walker, L.A., Gong, M.C., Lemichez, E., Boquet, P., Somlyo, A.V. and Somlyo, A.P. (1997) Inhibition of RhoA translocation and calcium sensitization by in vivo ADP-ribosylation with the chimeric toxin DC3B. Mol. Biol. Cell. 8, 2437-2447
27. Galan, J.E. and Cossart, P. (2005) Host - pathogen interactions: a diversity of themes, a variety of molecular machines. Curr. Opin. Microbiol. 8, 1-3
28. Genth, H., Hofmann, F., Selzer, J., Rex, G., Aktories, K. and Just, I. (1996) Difference in protein substrate specificity between hemorrhagic toxin and lethal toxin from Clostridium sordellii. Biochem. Biophys. Res. Commun. 229, 370-374
29. Genth, H., Schmidt, M., Gerhard, R., Aktories, K. and Just, I. (2003) Activation of phospholipase D1 by ADP-ribosylated RhoA. Biochem. Biophys. Res. Commun. 302, 127-132
30. Gu, Y., Chae, H.D., Siefring, J.E., Jasti, A.C., Hildeman, D.A. and Williams, D.A. (2006) RhoH GTPase recruits and activates Zap70 required for T cell receptor signaling and thymocyte development. Nat. Immunol. 7, 1182-1190
31. Guilluy, C., Rolli-Derkinderen, M., Tharaux, P.L., Melino, G., Pacaud, P. and Loirand, G. (2007) Transglutaminase-dependent RhoA activation and depletion by serotonin in vascular smooth muscle cells. J. Biol. Chem. 282, 2918-2928
32. 188 of RhoA to induce vasodilation in response to angiotensin II Type2 receptor activation. Circ. Res. 102, 1265-1274
33. Heasman, S.J. and Ridley, A.J. (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701
34. Hoffmann, C., Pop, M., Leemhuis, J., Schirmer, J., Aktories, K. and Schmidt, G. (2004) The Yersinia pseudotuberculosis cytotoxic necrotizing factor (CNFY) selectively activates RhoA. J. Biol. Chem. 279, 16026-16032
35. 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 Gln-63 of the GTP-binding protein Rho. Proc. Natl. Acad. Sci. U.S.A. 94, 11623-11626
36. Jaffe, A.B. and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269
37. Jank, T., Pack, U., Giesemann, T., Schmidt, G. and Aktories, K. (2006) Exchange of a single amino acid switches the substrate properties of RhoA and RhoD toward glucosylating and transglutaminating toxins. J. Biol. Chem. 281, 19527-19535
38. Just, I., Schallehn, G. and Aktories, K. (1992a) ADP-ribosylation of small GTP-binding proteins by Bacillus cereus. Biochem. Biophys. Res. Commun. 183, 931-936
39. Just, I., Mohr, C., Schallehn, G., Menard, L., Didsbury, J.R., Vandekerckhove, J., van Damme, J. and Aktories, K. (1992b) Purification and characterization of an ADP-ribosyltransferase produced by Clostridium limosum. J. Biol. Chem. 267, 10274-10280
40. *Just, I., Selzer, J., Wilm, M., von Eichel-Streiber, C., Mann, M. and Aktories, K. (1995) Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature 375, 500-503
41. Kerscher, O., Felberbaum, R. and Hochstrasser, M. (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu. Rev. Cell Dev. Biol. 22, 159-180
42. Kinch, L.N., Yarbrough, M.L., Orth, K. and Grishin, N.V. (2009) Fido, a novel AMPylation domain common to fic, doc, and AvrB. PLoS One 4, e5818
43. Kwon, T., Kwon, D.Y., Chun, J., Kim, J.H. and Kang, S.S. (2000) Akt protein kinase inhibits Rac1-GTP binding through phosphorylation at serine 71 of Rac1. J. Biol. Chem. 275, 423-428
44. *Lang, P., Gesbert, F., Delespine-Carmagnat, M., Stancou, R., Pouchelet, M. and Bertoglio, J. (1996) Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15, 510-519
45. Le Clainche, C. and Carlier, M.F. (2008) Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol. Rev. 88, 489-513
46. Lemonnier, M., Landraud, L. and Lemichez, E. (2007) Rho GTPase-activating bacterial toxins: from bacterial virulence regulation to eukaryotic cell biology. FEMS Microbiol. Rev. 31, 515-534
47. Lemichez, E., Lecuit, M., Nassif, X. and Bourdoulous, S. (2010) Breaking the wall: targeting of the endothelium by pathogenic bacteria. Nat. Rev. Microbiol. 8, 93-104
48. Lerm, M., Selzer, J., Hoffmeyer, A., Rapp, U.R., Aktories, K. and Schmidt, G. (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
49. Loirand, G., Guilluy, C. and Pacaud, P. (2006) Regulation of Rho proteins by phosphorylation in the cardiovascular system. Trends Cardiovasc. Med. 16, 199-204
50. Lynch, E.A., Stall, J., Schmidt, G., Chavrier, P. and D'Souza-Schorey, C. (2006) Proteasome-mediated degradation of Rac1-GTP during epithelial cell scattering. Mol. Biol. Cell 17, 2236-2242
51. Madaule, P. and Axel, R. (1985) A novel ras-related gene family. Cell 41, 31-40
52. Masuda, M., Betancourt, L., Matsuzawa, T., Kashimoto, T., Takao, T., Shimonishi, Y. and Horiguchi, Y. (2000) Activation of rho through a cross-link with polyamines catalyzed by Bordetella dermonecrotizing toxin. EMBO J. 19, 521-530 (Pubitemid 30093725)
53. Moon, S.Y. and Zheng, Y. (2003) Rho GTPase-activating proteins in cell regulation. Trends Cell Biol. 13, 13-22
54. Munro, P., Flatau, G., Doye, A., Boyer, L., Oregioni, O., Mege, J.L., Landraud, L. and Lemichez, E. (2004) Activation and proteasomal degradation of rho GTPases by cytotoxic necrotizing factor-1 elicit a controlled inflammatory response. J. Biol. Chem. 279, 35849-35857
55. Munro, P., Flatau, G. and Lemichez, E. (2007) Bacteria and the ubiquitin pathway. Curr. Opin. Microbiol. 10, 39-46
56. Nadif Kasri, N. and Van Aelst, L. (2008) Rho-linked genes and neurological disorders. Pflugers Arch. 455, 787-797
57. 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
58. 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. U.S.A. 92, 10629-10633
59. Nusser, N., Gosmanova, E., Makarova, N., Fujiwara, Y., Yang, L., Guo, F., Luo, Y., Zheng, Y. and Tigyi, G. (2006) Serine phosphorylation differentially affects RhoA binding to effectors: implications to NGF-induced neurite outgrowth. Cell Signal. 18, 704-714 (Pubitemid 43113300)
60. Orden, J.A., Dominguez-Bernal, G., Martinez-Pulgarin, S., Blanco, M., Blanco, J.E., Mora, A., Blanco, J., Blanco, J. and de la Fuente, R. (2007) Necrotoxigenic Escherichia coli from sheep and goats produce a new type of cytotoxic necrotizing factor (CNF3) associated with the eae and ehxA genes. Int. Microbiol. 10, 47-55
61. *Ozdamar, B., Bose, R., Barrios-Rodiles, M., Wang, H.R., Zhang, Y. and Wrana, J.L. (2005) Regulation of the polarity protein Par6 by TGF β receptors controls epithelial cell plasticity. Science 307, 1603-1609
62. Pacaud, P., Sauzeau, V. and Loirand, G. (2005) Rho proteins and vascular diseases. Arch. Mal. Coeur Vaiss. 98, 249-254
63. Popoff, M.R., Chaves-Olarte, E., Lemichez, E., von Eichel-Streiber, C., Thelestam, M., Chardin, P., Cussac, D., Antonny, B., Chavrier, P., Flatau, G., Giry, M., de Gunzburg, J. and Boquet, P. (1996) Ras, Rap, and Rac small GTP-binding proteins are targets for Clostridium sordellii lethal toxin glucosylation. J. Biol. Chem. 271, 10217-10224
64. Posern, G. and Treisman, R. (2006) Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16, 588-596 (Pubitemid 44636222)
65. *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
66. *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
67. Riento, K., Totty, N., Villalonga, P., Garg, R., Guasch, R. and Ridley, A.J. (2005) RhoE function is regulated by ROCK I-mediated phosphorylation. EMBO J. 24, 1170-1180 (Pubitemid 40516600)
68. Rolando, M., Munro, P., Stefani, C., Auberger, P., Flatau, G. and Lemichez, E. (2009) Injection of Staphylococcus aureus EDIN by the Bacillus anthracis protective antigen machinery induces vascular permeability. Infect. Immun. 77, 3596-3601
69. Rolli-Derkinderen, M., Sauzeau, V., Boyer, L., Lemichez, E., Baron, C., Henrion, D., Loirand, G. and Pacaud, P. (2005) Phosphorylation of serine 188 protects RhoA from ubiquitin/proteasome-mediated degradation in vascular smooth muscle cells. Circ. Res. 96, 1152-1160
70. Rossman, K.L., Der, C.J. and Sondek, J. (2005) GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180
71. Sahai, E. and Marshall, C.J. (2002) RHO-GTPases and cancer. Nat. Rev. Cancer 2, 133-142
72. 2+ sensitization of contraction in vascular smooth muscle. J. Biol. Chem. 275, 21722-21729
73. Sauzeau, V., Rolli-Derkinderen, M., Marionneau, C., Loirand, G. and Pacaud, P. (2003) RhoA expression is controlled by nitric oxide through cGMP-dependent protein kinase activation. J. Biol. Chem. 278, 9472-9480
74. Savoia, C., Tabet, F., Yao, G., Schiffrin, E.L. and Touyz, R.M. (2005) Negative regulation of RhoA/Rho kinase by angiotensin II type2 receptor in vascular smooth muscle cells: role in angiotensin II-induced vasodilation in stroke-prone spontaneously hypertensive rats. J. Hypertens. 23, 1037-1045 (Pubitemid 40637923)
75. Sawada, N., Itoh, H., Miyashita, K., Tsujimoto, H., Sone, M., Yamahara, K., Arany, Z.P., Hofmann, F. and Nakao, K. (2009) Cyclic GMP kinase and RhoA Ser188 phosphorylation integrate pro- and antifibrotic signals in blood vessels. Mol. Cell. Biol. 29, 6018-6032
76. *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
77. Schmidt, G., Selzer, J., Lerm, M. and Aktories, K. (1998) The Rho-deamidating cytotoxic necrotizing factor 1 from Escherichia coli possesses transglutaminase activity. Cysteine 866 and histidine 881 are essential for enzyme activity. J. Biol. Chem. 273, 13669-13674
78. Schmidt, G., Goehring, U.M., Schirmer, J., Uttenweiler-Joseph, S., Wilm, M., Lohmann, M., Giese, A., Schmalzing, G. and Aktories, K. (2001) Lysine and polyamines are substrates for transglutamination of Rho by the Bordetella dermonecrotic toxin. Infect. Immun. 69, 7663-7670
79. Sekine, A., Fujiwara, M. and Narumiya, S. (1989) Asparagine residue in the rho gene product is the modification site for botulinum ADP- ribosyltransferase. J. Biol. Chem. 264, 8602-8605
80. Selzer, J., Hofmann, F., Rex, G., Wilm, M., Mann, M., Just, I. and Aktories, K. (1996) Clostridium novyi α-toxin-catalyzed incorporation of GlcNAc into Rho subfamily proteins. J. Biol. Chem. 271, 25173-25177
81. Shao, F., Vacratsis, P.O., Bao, Z., Bowers, K.E., Fierke, C.A. and Dixon, J.E. (2003) Biochemical characterization of the Yersinia YopT protease: cleavage site and recognition elements in Rho GTPases. Proc. Natl. Acad. Sci. U.S.A. 100, 904-909
82. Singh, U.S., Kunar, M.T., Kao, Y.L. and Baker, K.M. (2001) Role of transglutaminase II in retinoic acid-induced activation of RhoA-associated kinase-2. EMBO J. 20, 2413-2423
83. Stoll, T., Markwirth, G., Reipschlager, S. and Schmidt, G. (2009) A new member of a growing toxin family-Escherichia coli cytotoxic necrotizing factor 3 (CNF3). Toxicon 54, 745-753
84. Tillement, V., Lajoie-Mazenc, I., Casanova, A., Froment, C., Penary, M., Tovar, D., Marquez, R., Monsarrat, B., Favre, G. and Pradines, A. (2008) Phosphorylation of RhoB by CK1 impedes actin stress fiber organization and epidermal growth factor receptor stabilization. Exp. Cell Res. 314, 2811-2821
85. Tu, S., Wu, W.J., Wang, J. and Cerione, R.A. (2003) Epidermal growth factor-dependent regulation of Cdc42 is mediated by the Src tyrosine kinase. J. Biol. Chem. 278, 49293-49300
86. Vetter, I.R. and Wittinghofer, A. (2001) The guanine nucleotide-binding switch in three dimensions. Science 294, 1299-1304
87. Visvikis, O., Lores, P., Boyer, L., Chardin, P., Lemichez, E. and Gacon, G. (2008) Activated Rac1, but not the tumorigenic variant Rac1b, is ubiquitinated on Lys 147 through a JNK-regulated process. FEBS J. 275, 386-396
88. Walther, D.J., Peter, J.U., Winter, S., Holtje, M., Paulmann, N., Grohmann, M., Vowinckel, J., Alamo-Bethencourt, V., Wilhelm, C.S., Ahnert-Hilger, G. and Bader, M. (2003) Serotonylation of small GTPases is a signal transduction pathway that triggers platelet α-granule release. Cell 115, 851-862
89. Wang, H.R., Zhang, Y., Ozdamar, B., Ogunjimi, A.A., Alexandrova, E., Thomsen, G.H. and Wrana, J.L. (2003) Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302, 1775-1779
90. Wilde, C., Vogelsgesang, M. and Aktories, K. (2003) Rho-specific Bacillus cereus ADP-ribosyltransferase C3cer cloning and characterization. Biochemistry 42, 9694-9702
91. Wojciak-Stothard, B. and Ridley, A.J. (2003) Rho GTPases and the regulation of endothelial permeability. Vascul. Pharmacol. 39, 187-199
92. Wong, K.W. and Isberg, R.R. (2005) Yersinia pseudotuberculosis spatially controls activation and misregulation of host cell Rac1. PLoS Pathog. 1, e16
93. Worby, C.A., Mattoo, S., Kruger, R.P., Corbeil, L.B., Koller, A., Mendez, J.C., Zekarias, B., Lazar, C. and Dixon, J.E. (2009) The fic domain: regulation of cell signaling by adenylylation. Mol. Cell 34, 93-103
94. Yamaguchi, T., Hayashi, T., Takami, H., Ohnishi, M., Murata, T., Nakayama, K., Asakawa, K., Ohara, M., Komatsuzawa, H. and Sugai, M. (2001) Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP-ribosyltransferase, EDIN-C. Infect. Immun. 69, 7760-7771
95. Yamaguchi, T., Nishifuji, K., Sasaki, M., Fudaba, Y., Aepfelbacher, M., Takata, T., Ohara, M., Komatsuzawa, H., Amagai, M. and Sugai, M. (2002) Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect. Immun. 70, 5835-5845
96. Yamashita, M., Ying, S.X., Zhang, G.M., Li, C., Cheng, S.Y., Deng, C.X. and Zhang, Y.E. (2005) Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121, 101-113
97. *Yarbrough, M.L., Li, Y., Kinch, L.N., Grishin, N.V., Ball, H.L. and Orth, K. (2009) AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 323, 269-272
98. Yeung, T., Terebiznik, M., Yu, L., Silvius, J., Abidi, W.M., Philips, M., Levine, T., Kapus, A. and Grinstein, S. (2006) Receptor activation alters inner surface potential during phagocytosis. Science 313, 347-351