Inhibitory and stimulatory regulation of Rac and cell motility by the G12/13-Rho and Gi pathways integrated downstream of a single G protein-coupled sphingosine-1-phosphate receptor isoform

Molecular and Cellular Biology

Volumn 23, Issue 5, 2003, Pages 1534-1545

  Sugimoto, Naotoshi ^a   Takuwa, Noriko ^a   Okamoto, Hiroyuki ^a   Sakurada, Sotaro ^a   Takuwa, Yoh ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CHEMOATTRACTANT; G PROTEIN COUPLED RECEPTOR; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PERTUSSIS TOXIN; PROTEIN; PROTEIN EDG3; PROTEIN EDG5; PROTEIN S1P2; PROTEIN S1P3; RAC PROTEIN; RHO FACTOR; RHO KINASE; RHO KINASE INHIBITOR; SOMATOMEDIN C; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; UNCLASSIFIED DRUG;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL MOTILITY; CELL SURFACE; CHEMOTAXIS; CHO CELL; CONTROLLED STUDY; DOWN REGULATION; EXPRESSION VECTOR; GENE OVEREXPRESSION; MEMBRANE TRANSPORT; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STRESS FIBER;

3T3 CELLS; ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; BOTULINUM TOXINS; CELL MOVEMENT; CHEMOTAXIS; CHO CELLS; COS CELLS; CRICETINAE; CULTURE MEDIA, SERUM-FREE; DOSE-RESPONSE RELATIONSHIP, DRUG; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HETEROTRIMERIC GTP-BINDING PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; PEPTIDES; PERTUSSIS TOXIN; PLASMIDS; PROTEIN ISOFORMS; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LYSOPHOSPHOLIPID; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

ANIMALIA; VECTORS;

EID: 0037370012     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.5.1534-1545.2003     Document Type: Article

References (50)

1. Akhter, S. A., L. M. Luttrell, H. A. Rockman, G. Iaccarino, R. J. Lefkowitz, and W. J. Koch. 1998. Targeting the receptor-Gq interface to inhibit in vivo pressure overload myocardial hypertrophy. Science 280:574-577.
2. Banyard, J., B. Anand-Apte, M. Symons, and B. R. Zetter. 2000. Motility and invasion are differentially modulated by Rho family GTPases. Oncogene 19:580-591.
3. Bornfeldt, K. E., L. M. Graves, E. W. Raines, Y. Igarashi, G. Wayman, S. Yamamura, Y. Yatomi, J. S. Sidhu, E. G. Krebs, S. Hakomori, and R. Ross. 1995. Sphingosine-1-phosphate inhibits PDGF-induced chemotaxis of human arterial smooth muscle cells: spatial and temporal modulation of PDGF chemotactic signal transduction. J. Cell Biol. 130:193-206.
4. Brinkmann, V., M. D. Davis, C. E. Heise, R. Albert, S. Cottens, R. Hof, C. Bruns, E. Prieschl, T. Baumruker, P. Hiestand, C. A. Foster, M. Zollinger, and K. R. Lynch. 2002. The immune modulator FTY720 targets sphingosine 1-phosphate receptors. J. Biol. Chem. 277:21453-21457.
5. Brzostowski, J. A., and A. R. Kimmel. 2001. Signaling at zero G: G-protein-independent functions for 7-TM receptors. Trends Biochem. Sci. 26:291-297.
6. Chikumi, H., J. Vazquez-Prado, J. M. Servitja, H. Miyazaki, and J. S. Gutkind. 2002. Potent activation of RhoA by Gαq and Gq-coupled receptors. J. Biol. Chem. 277:27130-27134.
7. Chun, J., E. J. Goetzl, T. Hla, Y. Igarashi, K. R. Lynch, W. Moolenaar, S. Pyne, and G. Tigyi. 2002. International Union of Pharmacology. XXXIV. Lysophospholipid receptor nomenclature. Pharmacol. Rev. 54:265-269.
8. Deguchi, J., M. Makuuchi, T. Nakaoka, T. Collins, and Y. Takuwa. 1999. Angiotensin II stimulates platelet-derived growth factor-B chain expression in newborn rat vascular smooth muscle cells and neointimal cells through Ras, ERK, and JNK mechanisms. Circ. Res. 85:565-574.
9. Dickson, B. J. 2001. Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11:103-110.
10. Evers, E. E., G. C. M. Zondag, A. Malliri, L. S. Price, J. P. ten Klooster, R. A. van der Kammen, and J. G. Collard. 2000. Rho family proteins in cell adhesion and cell migration. Eur. J. Cancer 36:1269-1274.
11. Gilchrist, A., M. Bunemann, A. Li, M. M. Hosey, and H. E. Hamm. 1999. A dominant-negative strategy for studying roles of G proteins in vivo. J. Biol. Chem. 274:6610-6616.
12. Gohla, A., S. Offermanns, T. M. Wilkie, and G. Schultz. 1999. Differential involvement of Gα12 and Gα13 in receptor-mediated stress fiber formation. J. Biol. Chem. 274:17901-17907.
13. Gonda, K., H. Okamoto, N. Takuwa, Y. Yatomi, H. Okazaki, T. Sakurai, S. Kimura, R. Sillard, K. Harii, and Y. Takuwa. 1999. The novel sphingosine 1-phosphate receptor AGR16 is coupled via pertussis toxin-sensitive and -insensitive G-proteins to multiple signalling pathways. Biochem. J. 337:67-75.
14. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279:509-514.
15. Hirsch, E., V. L. Katanaev, C. Garlanda, O. Azzolino, L. Pirola, L. Silengo, S. Sozzani, A. Mantovani, F. Altruda, and M. P. Wymann. 2000. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 287:1049-1053.
16. Hla, T., M. J. Lee, N. Ancellin, J. H. Paik, and M. J. Kluk. 2001. Lysophospholipids - receptor revelations. Science 294:1875-1878.
17. Kahn, R. A. 1991. Fluoride is not an activator of the smaller (20-25 kDa) GTP-binding proteins. J. Biol. Chem. 266:15595-15597.
18. Kamath, L., A. Meydani, F. Foss, and A. Kuliopulos. 2001. Signaling from protease-activated receptor-1 inhibits migration and invasion of breast cancer cells. Cancer Res. 61:5933-5940.
19. Katoh, H., J. Aoki, Y. Yamaguchi, Y. Kitano, A. Ichikawa, and M. Negishi. 1998. Constitutively active Gα12, Gα13, and Gαq induce Rho-dependent neurite retraction through different signaling pathways. J. Biol. Chem. 273:28700-28707.
20. Koch, W. J., B. E. Hawes, J. Inglese, L. M. Luttrell, and R. J. Lefkowitz. 1994. Cellular expression of the carboxyl terminus of a G protein-coupled receptor kinase attenuates G β γ-mediated signaling. J. Biol. Chem. 269:6193-6197.
21. Lauffenburger, D. A., and A. F. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell 84:359-369.
22. Lee, M. J., S. Thangada, K. P. Claffey, N. Ancellin, C. H. Liu, M. Kluk, M. Volpi, R. I. Shaafi, and T. Hla. 1999. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99:301-312.
23. Lim, L., E. Manser, T. Leung, and C. Hall. 1996. Regulation of phosphorylation pathways by p21 GTPases. The p21 Ras-related Rho subfamily and its role in phosphorylation signalling pathways. Eur. J. Biochem. 242:171-185.
24. Liu, Y., R. Wada, T. Yamashita, Y. Mi, C. X. Deng, J. P. Hobson, H. M. Rosenfeldt, V. E. Nava, S. S. Chae, M. J. Lee, C. H. Liu, T. Hla, S. Spiegel, and R. L. Proia. 2000. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Investig. 106:951-961.
25. Mandala, S., R. Hajdu, J. Bergstrom, E. Quackenbush, J. Xie, J. Milligan, R. Thornton, G.-J. Shei, D. Card, C. Keohane, M. Rosenbach, J. Hale, C. L. Lynch, K. Rupprecht, W. Parsons, and H. Rosen. 2002. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296:346-349.
26. Nagumo, H., Y. Sasaki, Y. Ono, H. Okamoto, M. Seto, and Y. Takuwa. 2000. Rho kinase inhibitor HA1077 prevents Rho-mediated myosin phosphatase inhibition in smooth muscle cells. Am. J. Physiol. 278:C57-C65.
27. Nobes, C. D., and A. Hall. 1999. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144:1235-1244.
28. Ohtaki, T., Y. Shintani, S. Honda, H. Matsumoto, A. Hori, K. Kanehashi, Y. Terao, S. Kumano, Y. Takatsu, Y. Masuda, Y. Ishibashi, T. Watanabe, M. Asada, T. Yamada, M. Suenaga, C. Kitada, S. Usuki, T. Kurokawa, H. Onda, O. Nishimura, and M. Fujino. 2001. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411:613-617.
29. 2+ mobilization, Ras-mitogen-activated protein kinase activation, and adenylate cyclase inhibition. J. Biol. Chem. 273:27104-27110.
30. Okamoto, H., N. Takuwa, Y. Yatomi, K. Gonda, H. Shigematsu, and Y. Takuwa. 1999. EDG3 is a functional receptor specific for sphingosine 1-phosphate and sphingosylphosphorylcholine with signaling characteristics distinct from EDG1 and AGR16. Biochem. Biophys. Res. Commun. 260:203-208.
31. Okamoto, H., N. Takuwa, T. Yokomizo, N. Sugimoto, S. Sakurada, H. Shigematsu, and Y. Takuwa. 2000. Inhibitory regulation of Rac activation, membrane ruffling, and cell migration by the G protein-coupled sphingosine-1-phosphate receptor EDG5 but not EDG1 or EDG3. Mol. Cell. Biol. 20:9247-9261.
32. 1-containing integrins. J. Biol. Chem. 276:11830-11837.
33. Ryu, Y., N. Takuwa, N. Sugimoto, S. Sakurada, S. Usui, H. Okamoto, O. Matsui, and Y. Takuwa. 2002. Sphingosine-1-phosphate, a platelet-derived lysophospholipid mediator, negatively regulates cellular Rac activity and cell migration in vascular smooth muscle cells. Circ. Res. 90:325-332.
34. Sadahira, Y., F. Ruan, S. Hakomori, and Y. Igarashi. 1992. Sphingosine 1-phosphate, a specific endogenous signaling molecule controlling cell motility and tumor cell invasiveness. Proc. Natl. Acad. Sci. USA 89:9686-9690.
35. Sakurada, S., H. Okamoto, N. Takuwa, N. Sugimoto, and Y. Takuwa. 2001. Rho activation in excitatory agonist-stimulated vascular smooth muscle. Am. J. Physiol. Cell. Physiol. 281:C571-C578.
36. Sanchez-Madrid, F., and M. A. Del Pozo. 1999. Leukocyte polarization in cell migration and immune interactions. EMBO J. 18:501-511.
37. Seifert, R., K. Wenzel-Seifert, and B. K. Kobilka. 1999. GPCR-Gα fusion proteins: molecular analysis of receptor-G-protein coupling. Trends Pharmacol. Sci. 20:383-389.
38. Shamah, S. M., M. Z. Lin, J. L. Goldberg, S. Estrach, M. Sahin, L. Hu, M. Bazalakova, R. L. Neve, G. Corfas, A. Debant, and M. E. Greenberg. 2001. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105:233-244.
39. Spiegel, S., and S. Milstlen. 2000. Functions of a new family of sphingosine-1-phosphate receptors. Biochim. Biophys. Acta 1484:107-116.
40. Stoker, M., and E. Gherardi. 1991. Regulation of cell movement: the motogenic cytokines. Biochim. Biophys. Acta 1072:81-102.
41. Takuwa, N., Y. Fukui, and Y. Takuwa. 1999. Cyclin D1 expression mediated by phosphatidylinositol 3-kinase through mTOR-p70S6K-independent signaling in growth factor-stimulated NIH 3T3 fibroblasts. Mol. Cell. Biol. 19:1346-1358.
42. Takuwa, Y. 2002. Subtype-specific differential regulation of Rho family G proteins and cell migration by the Edg family sphingosine-1-phosphate receptors. Biophys. Biochim. Acta 1582:112-120.
43. Takuwa, Y., N. Takuwa, and N. Sugimoto. 2002. The Edg family G protein-coupled receptors for lysophospholipids: their signaling properties and biological activities. J. Biochem. (Tokyo). 131:767-771.
44. Tessier-Lavigne, M., and C. S. Goodman. 1996. The molecular biology of axon guidance. Science 274:1123-1133.
45. Tsuji, T., T. Ishizaki, M. Okamoto, C. Higashida, K. Kimura, T. Furuyashiki, Y. Arakawa, R. B. Birge, T. Nakamoto, H. Hirai, and S. Narumiya. 2002. ROCK and mDia1 antagonize in Rho-dependent Rac activation in Swiss 3T3 fibroblasts. J. Cell Biol. 157:819-830.
46. Uehata, M., T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya. 1997. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389:990-994.
47. Van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
48. Wahl, S., H. Barth, T. Ciossek, K. Aktories, and B. K. Mueller. 2000. Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J. Cell Biol. 149:263-270.
49. 12 families of heterotrimeric G proteins. J. Biol. Chem. 274:27351-27358.
50. Yamaguchi, Y., H. Katoh, H. Yasui, K. Mori, and M. Negishi. 2001. RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J. Biol. Chem. 276:18977-18983.