Regulation of RhoA signaling by the cAMP-dependent phosphorylation of RhoGDIα

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38705-38715

  Oishi, Atsuro ^a   Makita, Noriko ^a   Sato, Junichiro ^a   Iiri, Taroh ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC FIBROBLASTS; CELL ROUNDING; CELL SHAPES; CYTOSOLS; INTACT CELLS; MOLECULAR MECHANISM; MORPHOLOGICAL CHANGES; PROTEIN KINASE A; RHOA SIGNALING;

CELL CULTURE; MORPHOLOGY; SIGNALING;

PHOSPHORYLATION;

CYCLIC AMP; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN RHOGDI ALPHA; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; FIBROBLAST; GENE SILENCING; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; CATTLE; CELL LINE; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP; GTP-BINDING PROTEINS; HEK293 CELLS; HUMANS; PHOSPHORYLATION; PROTEIN BINDING; RATS; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR ALPHA; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84869015428     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.401547     Document Type: Article

References (53)

1. Narumiya, S. (1996) The small GTPase Rho. Cellular functions and signal transduction. J. Biochem. 120, 215-228
2. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509-514
3. Ridley, A. J. (2001) Rho GTPases and cell migration. J. Cell Sci. 114, 2713-2722
4. Etienne-Manneville, S., and Hall, A. (2002) Rho GTPases in cell biology. Nature 420, 629-635 (Pubitemid 36764489)
5. Miyoshi, J., and Takai, Y. (2009) RhoA. AfCS-Nature Molecule Pages, 10.1038/mp.a0002062.01
6. Garcia-Mata, R., Boulter, E., and Burridge, K. (2011) The "invisible hand." Regulation of RHO GTPases by RHOGDIs. Nat. Rev. Mol. Cell Biol. 12, 493-504
7. 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
8. Vega, F. M., and Ridley, A. J. (2008) Rho GTPases in cancer cell biology. FEBS Lett. 582, 2093-2101
9. Narumiya, S., Tanji, M., and Ishizaki, T. (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis, and invasion. Cancer Metastasis Rev. 28, 65-76
10. Loirand, G., and Pacaud, P. (2010) The role of Rho protein signaling in hypertension. Nat. Rev. Cardiol. 7, 637-647
11. Nunes, K. P., Rigsby, C. S., and Webb, R. C. (2010) RhoA/Rho-kinase and vascular diseases. What is the link? Cell. Mol. Life Sci. 67, 3823-3836
12. 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 (Pubitemid 19151574)
13. 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
14. 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 (Pubitemid 26044564)
15. Dong, J. M., Leung, T., Manser, E., and Lim, L. (1998) cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKα. J. Biol. Chem. 273, 22554-22562 (Pubitemid 28399823)
16. Ellerbroek, S. M., Wennerberg, K., and Burridge, K. (2003) Serine phosphorylation negatively regulates RhoA in vivo. J. Biol. Chem. 278, 19023-19031 (Pubitemid 36799287)
17. Murthy, K. S., Zhou, H., Grider, J. R., and Makhlouf, G. M. (2003) Inhibition of sustained smooth muscle contraction by PKA and PKG preferentially mediated by phosphorylation of RhoA. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G1006-1016 (Pubitemid 36597344)
18. Tamma, G., Klussmann, E., Procino, G., Svelto, M., Rosenthal, W., and Valenti, G. (2003) cAMP-induced AQP2 translocation is associated with RhoA inhibition through RhoA phosphorylation and interaction with RhoGDI. J. Cell Sci. 116, 1519-1525 (Pubitemid 36527498)
19. 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 (Pubitemid 40827690)
20. Essler, M., Staddon, J. M., Weber, P. C., and Aepfelbacher, M. (2000) Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling. J. Immunol. 164, 6543-6549 (Pubitemid 30408840)
21. 2+ sensitization of contraction in vascular smooth muscle. J. Biol. Chem. 275, 21722-21729
22. Bolz, S. S., Vogel, L., Sollinger, D., Derwand, R., de Wit, C., Loirand, G., and Pohl, U. (2003) Nitric oxide-induced decrease in calcium sensitivity of resistance arteries is attributable to activation of the myosin light chain phosphatase and antagonized by the RhoA/Rho kinase pathway. Circulation 107, 3081-3087 (Pubitemid 36758983)
23. Puetz, S., Lubomirov, L. T., and Pfitzer, G. (2009) Regulation of smooth muscle contraction by small GTPases. Physiology 24, 342-356
24. Dovas, A., and Couchman, J. R. (2005) RhoGDI. Multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390, 1-9 (Pubitemid 41192225)
25. Dransart, E., Olofsson, B., and Cherfils, J. (2005) RhoGDIs revisited. Novel roles in Rho regulation. Traffic 6, 957-966 (Pubitemid 41472455)
26. DerMardirossian, C., Schnelzer, A., and Bokoch, G. M. (2004) Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol. Cell 15, 117-127 (Pubitemid 38850224)
27. Qiao, J., Huang, F., and Lum, H. (2003) PKA inhibits RhoA activation. A protection mechanism against endothelial barrier dysfunction. Am. J. Physiol. Lung Cell. Mol. Physiol. 284, L972-980 (Pubitemid 36687132)
28. Qiao, J., Holian, O., Lee, B. S., Huang, F., Zhang, J., and Lum, H. (2008) Phosphorylation of GTP dissociation inhibitor by PKA negatively regulates RhoA. Am. J. Physiol. Cell Physiol. 295, C1161-1168 (Pubitemid 352790336)
29. Zou, Y., Akazawa, H., Qin, Y., Sano, M., Takano, H., Minamino, T., Makita, N., Iwanaga, K., Zhu, W., Kudoh, S., Toko, H., Tamura, K., Kihara, M., Nagai, T., Fukamizu, A., Umemura, S., Iiri, T., Fujita, T., and Komuro, I. (2004) Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat. Cell Biol. 6, 499-506 (Pubitemid 38786592)
30. s mutant. Proc. Natl. Acad. Sci. U. S. A. 94, 5656-5661
31. Makita, N., Sato, J., Manaka, K., Shoji, Y., Oishi, A., Hashimoto, M., Fujita, T., and Iiri, T. (2007) An acquired hypocalciuric hypercalcemia autoantibody induces allosteric transition among active human Ca-sensing receptor conformations. Proc. Natl. Acad. Sci. U. S. A. 104, 5443-5448 (Pubitemid 47175699)
32. s mutant causes pseudohypoparathyroidism type Ia/neonatal diarrhea, a potential cell-specific role of the palmitoylation cycle. Proc. Natl. Acad. Sci. U. S. A. 104, 17424-17429
33. s in patients with gain and loss of endocrine function. Nature 371, 164-168
34. Watanabe, N., Madaule, P., Reid, T., Ishizaki, T., Watanabe, G., Kakizuka, A., Saito, Y., Nakao, K., Jockusch, B. M., and Narumiya, S. (1997) p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 3044-3056 (Pubitemid 27234944)
35. Takahashi, K., Makita, N., Manaka, K., Hisano, M., Akioka, Y., Miura, K., Takubo, N., Iida, A., Ueda, N., Hashimoto, M., Fujita, T., Igarashi, T., Sekine, T., and Iiri, T. (2012) V2 vasopressin receptor (V2R) mutations in partial nephrogenic diabetes insipidus highlight protean agonism of V2R antagonists. J. Biol. Chem. 287, 2099-2106
36. s mutant designed to inhibit receptor signaling through Gs. Proc. Natl. Acad. Sci. U. S. A. 96, 499-504
37. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K., and Koike, T. (2006) Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5, 749-757
38. Shichi, D., Arimura, T., Ishikawa, T., and Kimura, A. (2010) Heart-specific small subunit of myosin light chain phosphatase activates rho-associated kinase and regulates phosphorylation of myosin phosphatase target subunit 1. J. Biol. Chem. 285, 33680-33690
39. Hirose, M., Ishizaki, T., Watanabe, N., Uehata, M., Kranenburg, O., Moolenaar, W. H., Matsumura, F., Maekawa, M., Bito, H., and Narumiya, S. (1998) Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141, 1625-1636 (Pubitemid 28309176)
40. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M., and Narumiya, S. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994 (Pubitemid 27485693)
41. Michaelson, D., Silletti, J., Murphy, G., D'Eustachio, P., Rush, M., and Philips, M. R. (2001) Differential localization of Rho GTPases in live cells. Regulation by hypervariable regions and RhoGDI binding. J. Cell Biol. 152, 111-126 (Pubitemid 32102441)
42. Adamson, P., Paterson, H. F., and Hall, A. (1992) Intracellular localization of the p21 Rho proteins. J. Cell Biol. 119, 617-627
43. Lang, P., Gesbert, F., Thiberge, J. M., Troalen, F., Dutartre, H., Chavrier, P., and Bertoglio, J. (1993) Characterization of a monoclonal antibody specific for the Ras-related GTP-binding protein RhoA. Biochem. Biophys. Res. Commun. 196, 1522-1528 (Pubitemid 23347621)
44. Nemoto, Y., Namba, T., Teru-uchi, T., Ushikubi, F., Morii, N., and Narumiya, S. (1992) A rho gene product in human blood platelets. I. Identification of the platelet substrate for botulinum C3 ADP-ribosyltransferase as rhoA protein. J. Biol. Chem. 267, 20916-20920
45. 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 (Pubitemid 27508574)
46. Tkachenko, E., Sabouri-Ghomi, M., Pertz, O., Kim, C., Gutierrez, E., Machacek, M., Groisman, A., Danuser, G., and Ginsberg, M. H. (2011) Protein kinase A governs a RhoA-RhoGDI protrusion-retraction pacemaker in migrating cells. Nat. Cell Biol. 13, 660-667
47. Sawada, N., Itoh, H., Yamashita, J., Doi, K., Inoue, M., Masatsugu, K., Fukunaga, Y., Sakaguchi, S., Sone, M., Yamahara, K., Yurugi, T., and Nakao, K. (2001) cGMP-dependent protein kinase phosphorylates and inactivates RhoA. Biochem. Biophys. Res. Commun. 280, 798-805 (Pubitemid 32924500)
48. Forget, M. A., Desrosiers, R. R., Gingras, D., and Beliveau, R. (2002) Phosphorylation states of Cdc42 and RhoA regulates their interactions with Rho GDP dissociation inhibitor and their extraction from biological membranes. Biochem. J. 36, 243-254 (Pubitemid 34174491)
49. Hoffman, G. R., Nassar, N., and Cerione, R. A. (2000) Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI. Cell 100, 345-356 (Pubitemid 30353090)
50. DerMardirossian, C., and Bokoch, G. M. (2005) GDIs. Central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15, 356-363 (Pubitemid 40943524)
51. Knezevic, N., Roy, A., Timblin, B., Konstantoulaki, M., Sharma, T., Malik, A. B., and Mehta, D. (2007) GDI-1 phosphorylation switch at serine 96 induces RhoA activation and increased endothelial permeability. Mol. Cell. Biol. 27, 6323-6333 (Pubitemid 47435740)
52. DerMardirossian, C., Rocklin, G., Seo, J. Y., and Bokoch, G. M. (2006) Phosphorylation of RhoGDI by Src regulates Rho GTPase binding and cytosol-membrane cycling. Mol. Biol. Cell 17, 4760-4768 (Pubitemid 44665745)
53. Miura, Y., Kikuchi, A., Musha, T., Kuroda, S., Yaku, H., Sasaki, T., and Takai, Y. (1993) Regulation of morphology by rho p21 and its inhibitory GDP/GTP exchange protein (rho GDI) in Swiss 3T3 cells. J. Biol. Chem. 268, 510-515 (Pubitemid 23021351)