Ephexin4 and EphA2 mediate cell migration through a RhoG-dependent mechanism

Journal of Cell Biology

Volumn 190, Issue 3, 2010, Pages 461-477

  Hiramoto Yamaki, Nao ^a   Takeuchi, Shingo ^a   Ueda, Shuhei ^a   Harada, Kohei ^a   Fujimoto, Satoshi ^a   Negishi, Manabu ^a   Katoh, Hironori ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; EPHEXIN 4; EPHRIN RECEPTOR A2; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PROTEIN DOCK4; PROTEIN ELMO2; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER CELL; CELL INVASION; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; GENE ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN INTERACTION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HELA CELLS; HUMANS; RECEPTOR, EPHA2; RHO GTP-BINDING PROTEINS;

EID: 77955444009     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201005141     Document Type: Article

References (67)

1. Benard, V., B.P. Bohl, and G.M. Bokoch. 1999. Characterization of rac and cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274:13198-13204. doi:10.1074/jbc.274. 19.13198 (Pubitemid 129518524)
2. Blangy, A., E. Vignal, S. Schmidt, A. Debant, C. Gauthier- Rouvière, and P. Fort. 2000. TrioGEF1 controls Rac- and Cdc42-dependent cell structures through the direct activation of rhoG. J. Cell Sci. 113:729-739.
3. Brantley-Sieders, D.M., G. Zhuang, D. Hicks, W.B. Fang, Y. Hwang, J.M.M. Cates, K. Coffman, D. Jackson, E. Bruckheimer, R.S. Muraoka-Cook, and J. Chen. 2008. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J. Clin. Invest. 118:64-78. doi:10.1172/JCI33154
4. Brugnera, E., L. Haney, C. Grimsley, M. Lu, S.F. Walk, A.C. Tosello-Trampont, I.G. Macara, H. Madhani, G.R. Fink, and K.S. Ravichandran. 2002. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 4:574-582.
5. Côté, J.F., and K. Vuori. 2002. Identification of an evolutionarily conserved superfamily of DOCK180-related proteins with guanine nucleotide exchange activity. J. Cell Sci. 115:4901-4913. doi:10.1242/jcs.00219
6. Côté, J.F., and K. Vuori. 2007. GEF what? Dock180 and related proteins help Rac to polarize cells in new ways. Trends Cell Biol. 17:383-393. doi:10.1016/j.tcb.2007.05.001
7. Côté, J.F., A.B. Motoyama, J.A. Bush, and K. Vuori. 2005. A novel and evolutionarily conserved PtdIns(3,4,5)P3-binding domain is necessary for DOCK180 signalling. Nat. Cell Biol. 7:797-807. doi:10.1038/ncb1280
8. Cowan, C.W., Y.R. Shao, M. Sahin, S.M. Shamah, M.Z. Lin, P.L. Greer, S. Gao, E.C. Griffith, J.S. Brugge, and M.E. Greenberg. 2005. Vav family GEFs link activated Ephs to endocytosis and axon guidance. Neuron. 46:205-217. doi:10.1016/j.neuron.2005.03.019
9. DesMarais, V., H. Yamaguchi, M. Oser, L. Soon, G. Mouneimne, C. Sarmiento, R. Eddy, and J. Condeelis. 2009. N-WASP and cortactin are involved in invadopodium-dependent chemotaxis to EGF in breast tumor cells. Cell Motil. Cytoskeleton. 66:303-316. doi:10.1002/cm.20361
10. Elfenbein, A., J.M. Rhodes, J. Meller, M.A. Schwartz, M. Matsuda, and M. Simons. 2009. Suppression of RhoG activity is mediated by a syndecan 4-synectin-RhoGDI1 complex and is reversed by PKCα in a Rac1 activation pathway. J. Cell Biol. 186:75-83. doi:10.1083/jcb.200810179
11. Ellerbroek, S.M., K. Wennerberg, W.T. Arthur, J.M. Dunty, D.R. Bowman, K.A. DeMali, C. Der, and K. Burridge. 2004. SGEF, a RhoG guanine nucleotide exchange factor that stimulates macropinocytosis. Mol. Biol. Cell. 15:3309-3319. doi:10.1091/mbc.E04-02-0146
12. Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature. 420:629-635. doi:10.1038/nature01148
13. Fu, W.Y., Y. Chen, M. Sahin, X.S. Zhao, L. Shi, J.B. Bikoff, K.O. Lai, W.H. Yung, A.K.Y. Fu, M.E. Greenberg, and N.Y. Ip. 2007. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 10:67-76. doi:10.1038/nn1811
14. Fujimoto, S., M. Negishi, and H. Katoh. 2009. RhoG promotes neural progenitor cell proliferation in mouse cerebral cortex. Mol. Biol. Cell. 20:4941-4950. doi:10.1091/mbc.E09-03-0200
15. Gadea, G., V. Sanz-Moreno, A. Self, A. Godi, and C.J. Marshall. 2008. DOCK10-mediated Cdc42 activation is necessary for amoeboid invasion of melanoma cells. Curr. Biol. 18:1456-1465. doi:10.1016/j.cub.2008.08.053
16. Gumienny, T.L., E. Brugnera, A.C. Tosello-Trampont, J.M. Kinchen, L.B. Haney, K. Nishiwaki, S.F. Walk, M.E. Nemergut, I.G. Macara, R. Francis, et al. 2001. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell. 107:27-41. doi:10.1016/S0092-8674(01) 00520-7
17. Hiramoto, K., M. Negishi, and H. Katoh. 2006. Dock4 is regulated by RhoG and promotes Rac-dependent cell migration. Exp. Cell Res. 312:4205-4216. doi:10.1016/j.yexcr.2006.09.006
18. Hunter, S.G., G. Zhuang, D. Brantley-Sieders, W. Swat, C.W. Cowan, and J. Chen. 2006. Essential role of Vav family guanine nucleotide exchange factors in EphA receptor-mediated angiogenesis. Mol. Cell. Biol. 26:4830-4842. doi:10.1128/MCB.02215-05
19. Hynes, N.E., and H.A. Lane. 2005. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer. 5:341-354. doi:10.1038/nrc1609
20. Iwasato, T., H. Katoh, H. Nishimaru, Y. Ishikawa, H. Inoue, Y.M. Saito, R. Ando, M. Iwama, R. Takahashi, M. Negishi, and S. Itohara. 2007. Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell. 130:742-753. doi:10.1016/j.cell.2007.07. 022
21. Jarzynka, M.J., B. Hu, K.M. Hui, I. Bar-Joseph, W. Gu, T. Hirose, L.B. Haney, K.S. Ravichandran, R. Nishikawa, and S.Y. Cheng. 2007. ELMO1 and Dock180, a bipartite Rac1 guanine nucleotide exchange factor, promote human glioma cell invasion. Cancer Res. 67:7203-7211. doi:10.1158/0008-5472.CAN-07-0473
22. Katoh, H., and M. Negishi. 2003. RhoG activates Rac1 by direct interaction with the Dock180-binding protein Elmo. Nature. 424:461-464. doi:10.1038/nature01817 (Pubitemid 36917498)
23. Katoh, H., A. Harada, K. Mori, and M. Negishi. 2002. Socius is a novel Rnd GTPase-interacting protein involved in disassembly of actin stress fibers. Mol. Cell. Biol. 22:2952-2964. doi:10.1128/MCB.22.9.2952-2964.2002
24. Katoh, H., K. Hiramoto, and M. Negishi. 2006. Activation of Rac1 by RhoG regulates cell migration. J. Cell Sci. 119:56-65. doi:10.1242/jcs.02720 (Pubitemid 43169298)
25. Kawada, K., G. Upadhyay, S. Ferandon, S. Janarthanan, M. Hall, J.P. Vilardaga, and V. Yajnik. 2009. Cell migration is regulated by platelet-derived growth factor receptor endocytosis. Mol. Cell. Biol. 29:4508-4518. doi:10.1128/MCB.00015-09
26. Kiyokawa, E., Y. Hashimoto, S. Kobayashi, H. Sugimura, T. Kurata, and M. Matsuda. 1998. Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12:3331-3336. doi:10.1101/gad.12.21.3331
27. Kuramoto, K., M. Negishi, and H. Katoh. 2009. Regulation of dendrite growth by the Cdc42 activator Zizimin1/Dock9 in hippocampal neurons. J. Neurosci. Res. 87:1794-1805. doi:10.1002/jnr.21997
28. Kurisu, S., S. Suetsugu, D. Yamazaki, H. Yamaguchi, and T. Takenawa. 2005. Rac-WAVE2 signaling is involved in the invasive and metastatic phenotypes of murine melanoma cells. Oncogene. 24:1309-1319. doi:10.1038/sj.onc.1208177 (Pubitemid 40343111)
29. Larsen, A.B., M.W. Pedersen, M.T. Stockhausen, M.V. Grandal, B. van Deurs, and H.S. Poulsen. 2007. Activation of the EGFR gene target EphA2 inhibits epidermal growth factor-induced cancer cell motility. Mol. Cancer Res. 5:283-293. doi:10.1158/1541-7786.MCR-06-0321
30. Macrae, M., R.M. Neve, P. Rodriguez-Viciana, C. Haqq, J. Yeh, C. Chen, J.W. Gray, and F. McCormick. 2005. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell. 8:111-118. doi:10.1016/j.ccr.2005.07.005
31. Meller, N., M. Irani-Tehrani, W.B. Kiosses, M.A. Del Pozo, and M.A. Schwartz. 2002. Zizimin1, a novel Cdc42 activator, reveals a new GEF domain for Rho proteins. Nat. Cell Biol. 4:639-647. doi:10.1038/ncb835 (Pubitemid 34993699)
32. Meller, N., S. Merlot, and C. Guda. 2005. CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118:4937-4946. doi:10.1242/jcs.02671
33. Meller, N., M.J. Westbrook, J.D. Shannon, C. Guda, and M.A. Schwartz. 2008. Function of the N-terminus of zizimin1: autoinhibition and membrane targeting. Biochem. J. 409:525-533. doi:10.1042/BJ20071263
34. Merlos-Suárez, A., and E. Batlle. 2008. Eph-ephrin signalling in adult tissues and cancer. Curr. Opin. Cell Biol. 20:194-200. doi:10.1016/j.ceb.2008.01.011
35. Miao, H., D.Q. Li, A. Mukherjee, H. Guo, A. Petty, J. Cutter, J.P. Basilion, J. Sedor, J. Wu, D. Danielpour, et al. 2009. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell. 16:9-20. doi:10.1016/j.ccr.2009.04.009
36. Miki, H., S. Suetsugu, and T. Takenawa. 1998. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17:6932-6941. doi:10.1093/emboj/17.23.6932 (Pubitemid 28550287)
37. Miyamoto, Y., and J. Yamauchi. 2010. Cellular signaling of Dock family proteins in neural function. Cell. Signal. 22:175-182. doi:10.1016/j.cellsig. 2009.09.036
38. Miyamoto, Y., J. Yamauchi, A. Sanbe, and A. Tanoue. 2007. Dock6, a Dock-C subfamily guanine nucleotide exchanger, has the dual specificity for Rac1 and Cdc42 and regulates neurite outgrowth. Exp. Cell Res. 313:791-804. doi:10.1016/j.yexcr.2006.11.017
39. Murga, C., M. Zohar, H. Teramoto, and J.S. Gutkind. 2002. Rac1 and RhoG promote cell survival by the activation of PI3K and Akt, independently of their ability to stimulate JNK and NF-kappaB. Oncogene. 21:207-216. doi:10.1038/sj.onc.1205036
40. Namekata, K., Y. Enokido, K. Iwasawa, and H. Kimura. 2004. MOCA induces membrane spreading by activating Rac1. J. Biol. Chem. 279:14331-14337. doi:10.1074/jbc.M311275200 (Pubitemid 38468974)
41. Nishihara, H., S. Kobayashi, Y. Hashimoto, F. Ohba, N. Mochizuki, T. Kurata, K. Nagashima, and M. Matsuda. 1999. Non-adherent cell-specific expression of DOCK2, a member of the human CDM-family proteins. Biochim. Biophys. Acta. 1452:179-187. doi:10.1016/S0167-4889(99)00133-0
42. Ogita, H., S. Kunimoto, Y. Kamioka, H. Sawa, M. Masuda, and N. Mochizuki. 2003. EphA4-mediated Rho activation via Vsm-RhoGEF expressed specifically in vascular smooth muscle cells. Circ. Res. 93:23-31. doi:10.1161/01.RES. 0000079310.81429.C8 (Pubitemid 36859037)
43. Pasquale, E.B. 2008. Eph-ephrin bidirectional signaling in physiology and disease. Cell. 133:38-52. doi:10.1016/j.cell.2008.03.011
44. Pollard, T.D., and G.G. Borisy. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 112:453-465. doi:10.1016/S0092-8674(03)00120-X
45. Ren, X.D., W.B. Kiosses, and M.A. Schwartz. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18:578-585. doi:10.1093/emboj/18.3.578 (Pubitemid 29057242)
46. Rothschild, B.L., A.H. Shim, A.G. Ammer, L.C. Kelley, K.B. Irby, J.A. Head, L. Chen, M. Varella-Garcia, P.G. Sacks, B. Frederick, et al. 2006. Cortactin overexpression regulates actin-related protein 2/3 complex activity, motility, and invasion in carcinomas with chromosome 11q13 amplification. Cancer Res. 66:8017-8025. doi:10.1158/0008-5472.CAN-05-4490
47. Roux, P., C. Gauthier-Rouvière, S. Doucet-Brutin, and P. Fort. 1997. The small GTPases Cdc42Hs, Rac1 and RhoG delineate Raf-independent pathways that cooperate to transform NIH3T3 cells. Curr. Biol. 7:629-637. doi:10.1016/S0960-9822(06)00289-2 (Pubitemid 27408860)
48. Sahai, E., and C.J. Marshall. 2002. RHO-GTPases and cancer. Nat. Rev. Cancer. 2:133-142. doi:10.1038/nrc725
49. Sahin, M., P.L. Greer, M.Z. Lin, H. Poucher, J. Eberhart, S. Schmidt, T.M. Wright, S.M. Shamah, S. O'Connell, C.W. Cowan, et al. 2005. Ephdependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron. 46:191-204. doi:10.1016/j.neuron.2005.01.030
50. Saito, T., and N. Nakatsuji. 2001. Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol. 240:237-246. doi:10.1006/dbio.2001.0439 (Pubitemid 33141120)
51. Sanz-Moreno, V., G. Gadea, J. Ahn, H. Paterson, P. Marra, S. Pinner, E. Sahai, and C.J. Marshall. 2008. Rac activation and inactivation control plasticity of tumor cell movement. Cell. 135:510-523. doi:10.1016/j.cell.2008. 09.043
52. 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. doi:10.1016/S0092-8674(01)00314-2
53. Takeuchi, S., N. Yamaki, T. Iwasato, M. Negishi, and H. Katoh. 2009. β2-chimaerin binds to EphA receptors and regulates cell migration. FEBS Lett. 583:1237-1242. doi:10.1016/j.febslet.2009.03.032
54. Ueda, S., S. Fujimoto, K. Hiramoto, M. Negishi, and H. Katoh. 2008. Dock4 regulates dendritic development in hippocampal neurons. J. Neurosci. Res. 86:3052-3061. doi:10.1002/jnr.21763
55. Upadhyay, G., W. Goessling, T.E. North, R. Xavier, L.I. Zon, and V. Yajnik. 2008. Molecular association between beta-catenin degradation complex and Rac guanine exchange factor DOCK4 is essential for Wnt/beta-catenin signaling. Oncogene. 27:5845-5855. doi:10.1038/onc.2008.202
56. Vega, F.M., and A.J. Ridley. 2008. Rho GTPases in cancer cell biology. FEBS Lett. 582:2093-2101. doi:10.1016/j.febslet.2008.04.039
57. Walker-Daniels, J., D.J. Riese II, and M.S. Kinch. 2002. c-Cbl-dependent EphA2 protein degradation is induced by ligand binding. Mol. Cancer Res. 1:79-87. (Pubitemid 36330213)
58. Wang, Y., H. Suzuki, T. Yokoo, K. Tada-Iida, R. Kihara, M. Miura, K. Watanabe, H. Sone, H. Shimano, H. Toyoshima, and N. Yamada. 2004. WGEF is a novel RhoGEF expressed in intestine, liver, heart, and kidney. Biochem. Biophys. Res. Commun. 324:1053-1058. doi:10.1016/j.bbrc.2004.09.153
59. Weaver, A.M. 2008. Cortactin in tumor invasiveness. Cancer Lett. 265:157-166. doi:10.1016/j.canlet.2008.02.066
60. Weed, S.A., Y. Du, and J.T. Parsons. 1998. Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1. J. Cell Sci. 111:2433-2443.
61. Xie, X., S.W. Chang, T. Tatsumoto, A.M. Chan, and T. Miki. 2005. TIM, a Dbl-related protein, regulates cell shape and cytoskeletal organization in a Rho-dependent manner. Cell. Signal. 17:461-471. doi:10.1016/j.cellsig.2004.09. 012 (Pubitemid 39643064)
62. Yajnik, V., C. Paulding, R. Sordella, A.I. McClatchey, M. Saito, D.C. Wahrer, P. Reynolds, D.W. Bell, R. Lake, S. van den Heuvel, et al. 2003. DOCK4, a GTPase activator, is disrupted during tumorigenesis. Cell. 112:673-684. doi:10.1016/S0092-8674(03)00155-7
63. Yamaki, N., M. Negishi, and H. Katoh. 2007. RhoG regulates anoikis through a phosphatidylinositol 3-kinase-dependent mechanism. Exp. Cell Res. 313:2821-2832. doi:10.1016/j.yexcr.2007.05.010
64. Yamauchi, J., Y. Miyamoto, J.R. Chan, and A. Tanoue. 2008. ErbB2 directly activates the exchange factor Dock7 to promote Schwann cell migration. J. Cell Biol. 181:351-365. doi:10.1083/jcb.200709033 (Pubitemid 351574558)
65. Yamazaki, D., S. Kurisu, and T. Takenawa. 2009. Involvement of Rac and Rho signaling in cancer cell motility in 3D substrates. Oncogene. 28:1570-1583. doi:10.1038/onc.2009.2
66. Zelinski, D.P., N.D. Zantek, J.C. Stewart, A.R. Irizarry, and M.S. Kinch. 2001. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 61:2301-2306.
67. Zhuang, G., S. Hunter, Y. Hwang, and J. Chen. 2007. Regulation of EphA2 receptor endocytosis by SHIP2 lipid phosphatase via phosphatidylinositol 3-Kinase-dependent Rac1 activation. J. Biol. Chem. 282:2683-2694. doi:10.1074/jbc.M608509200 (Pubitemid 47076792)