Ephexin4 and EphA2 mediate resistance to anoikis through RhoG and phosphatidylinositol 3-kinase

Experimental Cell Research

Volumn 317, Issue 12, 2011, Pages 1701-1713

  Harada, Kohei ^a   Hiramoto Yamaki, Nao ^a   Negishi, Manabu ^a   Katoh, Hironori ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Akt; Anoikis; EphA2; Ephexin4; PI3 kinase; RhoG

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; EPHEXIN4; EPHRIN RECEPTOR A2; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANOIKIS; ARTICLE; CELL CULTURE; CELL SUSPENSION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION;

EID: 79958807321     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.05.014     Document Type: Article

References (60)

1. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 1994, 124:619-626.
2. Frisch S.M., Screaton R.A. Anoikis mechanisms. Curr. Opin. Cell Biol. 2001, 13:555-562.
3. Valentijn A.J., Zouq N., Gilmore A.P. Anoikis. Biochem. Sci. 2004, 32:421-425.
4. Reddig P.J., Juliano R.L. Clinging to life: cell to matrix adhesion and cell survival. Cancer Metastasis Rev. 2005, 24:425-439.
5. Geiger T.R., Peeper D.S. The neurotrophic receptor TrkB in anoikis resistance and metastasis: a perspective. Cancer Res. 2005, 65:7033-7036.
6. Rennebeck G., Martelli M., Kyprianou N. Anoikis and survival connections in the tumor microenvironment: is there a role in prostate cancer metastasis?. Cancer Res. 2005, 65:11230-11235.
7. Simpson C.D., Anyiwe K., Schimmer A.D. Anoikis resistance and tumor metastasis. Cancer Lett. 2008, 272:177-185.
8. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: a play in three Akts. Genes Dev. 1999, 13:2905-2927.
9. Zugasti O., Rul W., Roux P., Peyssonnaux C., Eychene A., Franke T.F., Fort P., Hibner U. Raf-MEK-Erk cascade in anoikis is controlled by Rac1 and Cdc42 via Akt. Mol. Cell. Biol. 2001, 19:6706-6717.
10. Grossmann J. Molecular mechanisms of "detachment-induced apoptosis-anoikis". Apoptosis 2002, 7:247-260.
11. Duronio V. The life of cell: apoptosis regulation by the PI3K/PKB pathway. Biochem. J. 2008, 415:333-344.
12. Ridley A.J. Rho family proteins: coordinating cell responses. Trends Cell Biol. 2001, 11:471-477.
13. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
14. Negishi M., Katoh H. Rho family GTPases as key regulators for neuronal network formation. J. Biochem. 2002, 132:157-166.
15. Symons M. Rho family GTPases: the cytoskeleton and beyond. Trends Biochem. Sci. 1996, 21:178-181.
16. Zohn I.M., Campbell S.L., Khosravi-Far R., Rossman K.L., Der C.J. Rho family proteins and Ras transformation: the RHOad less traveled gets congested. Oncogene 1998, 17:1415-1438.
17. Ridley A.J. Rho proteins and cancer. Breast Cancer Res. Treat. 2004, 84:13-19.
18. Rossman K.L., Der C.J., Sondek J. GEF means go: turning on Rho GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 2005, 6:167-180.
19. Bos J.L., Rehmann H., Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007, 129:865-877.
20. Katoh H., Yasui H., Yamaguchi Y., Aoki J., Fujita H., Mori K., Negishi M. Small GTPase RhoG is a key regulator for neurite outgrowth in PC12 cells. Mol. Cell. Biol. 2000, 20:7378-7387.
21. deBakker C.D., Haney L.B., Kinchen J.M., Grimsley C., Lu M., Klingele D., Hsu P.K., Chou B.K., Cheng L.C., Blangy A., Sondek J., Hengartner M.O., Wu Y.C., Ravichandran K.S. Phagocytosis of apoptotic cells is regulated by a UNC-73/TRIO-MIG-2/RhoG signaling module and armadillo repeats of CED-12/ELMO. Curr. Biol. 2004, 14:2208-2216.
22. Katoh H., Hiramoto K., Negishi M. Activation of Rac1 by RhoG regulates cell migration. J. Cell Sci. 2006, 119:56-65.
23. Elfenbein A., Rhodes J.M., Meller J., Schwartz M.A., Matsuda M., Simons M. 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. 2009, 186:75-83.
24. Katoh H., Negishi M. RhoG activates Rac1 by direct interaction with the Dock180-binding protein Elmo. Nature 2003, 424:461-464.
25. Hiramoto K., Negishi M., Katoh H. Dock4 is regulated by RhoG and promotes Rac-dependent cell migration. Exp. Cell Res. 2006, 312:4205-4216.
26. Patel M., Margaron Y., Fradet N., Yang Q., Wilkes B., Bouvier M., Hofmann K., Côté J.F. An evolutionarily conserved autoinhibitory molecular switch in ELMO proteins regulates Rac signaling. Curr. Biol. 2010, 20:2021-2027.
27. Murga C., Zohar M., Teramoto H., Gutkind J.S. Rac1 and RhoG promotes cell survival by the activation of PI3K and Akt, independently of their ability to stimulate JNK and NF-κB. Oncogene 2002, 21:207-216.
28. Yamaki N., Negishi M., Katoh H. RhoG regulates anoikis through a phosphatidylinositol 3-kinase-dependent mechanism. Exp. Cell Res. 2007, 313:2821-2832.
29. Fujimoto S., Negishi M., Katoh H. RhoG promotes neural progenitor cell proliferation in mouse cerebral cortex. Mol. Biol. Cell 2009, 20:4941-4950.
30. Surawska H., Ma P.C., Salgia R. The role of ephrins and Eph receptors in cancer. Cytokine Growth Factor Rev. 2004, 15:419-433.
31. Pasquale E.B. Eph-Ephrin bidirectional signaling in physiology and disease. Cell 2008, 133:38-52.
32. Pasquale E.B. Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat. Rev. Cancer 2010, 10:165-180.
33. Shamah S.M., Lin M.Z., Goldberg J.L., Estrach S., Sahin M., Hu L., Bazalakova M., Neve R.L., Corfas G., Debant A., Greenberg M.E. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 2001, 312:233-244.
34. Sahin M., Greer P.L., Lin M.Z., Poucher H., Eberhart J., Schmidt S., Wright T.M., Shamah S.M., O'Connell S., Cowan C.W., Hu L., Goldberg J.L., Debant A., Corfas G., Krull C.E., Greenberg M.E. Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 2005, 46:191-204.
35. Ogita H., Kunimoto S., Kamioka Y., Sawa H., Matsuda M., Mochizuki N. EphA4-mediated Rho activation via Vsm-RhoGEF expressed specifically in vascular smooth muscle cells. Circ. Res. 2003, 93:23-31.
36. Wang Y., Suzuki H., Yokoo T., Tada-Iida K., Kihara R., Miura M., Watanabe K., Sone H., Shimano H., Toyoshima H., Yamada N. WGEF is a novel RhoGEF expressed in intestine, liver, heart, and kidney. Biochem. Biophys. Res. Commun. 2004, 324:1053-1058.
37. Xie X., Chang S.W., Tatsumoto T., Chan A.M., Miki T. TIM, a Dbl-related protein, regulates cell shape and cytoskeletal organization in a Rho-dependent manner. Cell. Signal. 2005, 17:461-471.
38. Fu W.Y., Chen Y., Sahin M., Zhao X.S., Shi L., Bikoff J.B., Lai K.O., Yung W.H., Fu A.K.Y., Greenberg M.E., Ip N.Y. Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nat. Neurosci. 2007, 10:67-76.
39. Margolis S.S., Salogiannis J., Lipton D.M., Mandel-Brehm C., Wills Z.P., Mardinly A.R., Hu L., Greer P.L., Bikoff J.B., Ho H.Y.H., Soskis M.J., Sahin M., Greenberg M.E. EphB-mediated degradation of the RhoA GEF Ephexin5 relieves a developmental brake on excitatory synapse formation. Cell 2010, 143:442-455.
40. Caddy J., Wilanowski T., Darido C., Dworkin S., Ting S.B., Zhao Q., Rank G., Auden A., Srivastava S., Papenfuss T.A., Murdoch J.N., Humbert P.O., Boulos N., Weber T., Zuo J., Cunningham J.M., Jane S.M. Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev. Cell 2010, 19:138-147.
41. Hiramoto-Yamaki N., Takeuchi S., Ueda S., Harada K., Fujimoto S., Negishi M., Katoh H. Ephexin4 and EphA2 mediate cell migration through a RhoG-dependent mechanism. J. Cell Biol. 2010, 190:461-477.
42. Macrae M., Neve R.M., Rhodriguez-Viciana P., Haqq C., Yeh J., Chen C., Gray J.W., McCormick F. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 2005, 8:111-118.
43. Larsen A.B., Pedersen M.W., Stockhausen M.T., Grandal M.V., van Deurs B., Poulsen H.S. Activation of the EGFR gene target EphA2 inhibits epidermal growth factor-induced cancer cell motility. Mol. Cancer Res. 2007, 5:283-293.
44. Brantley-Sieders D.M., Zhuang G., Hicks D., Fang W.B., Hwang Y., Cates J.M.M., Coffman K., Jackson D., Bruckheimer E., Muraoka-Cook R.S., Chen J. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J. Clin. Invest. 2008, 118:64-78.
45. Wykosky J., Debinski W. The EphA2 receptor and EphrinA1 ligand in solid tumors: function and therapeutic targeting. Mol. Cancer Res. 2008, 6:1795-1806.
46. Miao H., Li D.Q., Mukherjee A., Guo H., Petty H., Cutter J., Basilion J.P., Sedor J., Wu J., Danielpour D., Sloan A.E., Cohen M.L., Wang B. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 2009, 16:9-20.
47. Oinuma I., Katoh H., Negishi M. Semaphorin 4D/Plexin-B1-mediated R-Ras GAP activity inhibits cell migration by regulating β1 integrin activity. J. Cell Biol. 2006, 173:601-613.
48. Takeuchi S., Yamaki N., Negishi M., Katoh H. β2-Chimaerin binds to EphA receptors and regulates cell migration. FEBS Lett. 2007, 583:1237-1242.
49. Ito Y., Oinuma I., Katoh H., Kaibuchi K., Negishi M. Sema4D/plexin-B1 activates GSK-3β through R-Ras GAP activity, inducing growth cone collapse. EMBO Rep. 2006, 7:704-709.
50. Iwasato T., Katoh H., Nishimaru H., Ishikawa Y., Inoue H., Saito Y.M., Ando R., Iwama M., Takahashi R., Negishi M., Itohara S. Rac-GAP alpha-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 signaling. Cell 2007, 130:742-753.
51. Wu Y., Pan S., Luo W., Lin S.H., Kuang J. Hp95 promotes anoikis and inhibits tumorigenicity of HeLa cells. Oncogene 2002, 21:6801-6808.
52. Ke N., Claassen G., Yu D.H., Albers A., Fan W., Tan P., Grifman M., Hu X., DeFife K., Nguy V., Meyhack B., Brachat A., Wong-Staal F., Li Q.X. Nuclear hormone receptor NR4A2 is involved in cell transformation and apoptosis. Cancer Res. 2004, 64:8208-8212.
53. Chiarugi P., Giannoni E. Anoikis: a necessary death program for anchorage-dependent cells. Biochem. Pharmacol. 2008, 76:1352-1364.
54. Duxbury M.S., Ito H., Zinner M.J., Ashley S.W., Whang E.E. EphA2: a determinant of malignant cellular behavior and a potential therapeutic target in pancreatic adenocarcinoma. Oncogene 2004, 23:1448-1456.
55. Vigorito E., Bell S., Hebeis B.J., Reynolds H., McAdam S., Emson P.C., McKenzie A., Turner M. Immunological function in mice lacking the Rac-related GTPase RhoG. Mol. Cell. Biol. 2004, 24:719-729.
56. Estrach S., Schmidt S., Diriong S., Penna A., Blangy A., Fort P., Debant A. The human Rho-GEF trio and its target GTPase RhoG are involved in the NGF pathway, leading to neurite outgrowth. Curr. Biol. 2002, 12:307-312.
57. May V., Schiller M.R., Eipper B.A., Mains R.E. Kalirin Dbl-homology guanine nucleotide exchange factor 1 domain initiates new axon outgrowths via RhoG-mediated mechanisms. J. Neurosci. 2002, 22:6980-6990.
58. D'Angelo R., Aresta S., Blangy A., Maestro L.D., Louvard D., Arpin M. Interaction of Ezrin with the novel guanine nucleotide exchange factor PLEKHG6 promotes RhoG-dependent apical cytoskeleton rearrangements in epithelial cells. Mol. Biol. Cell 2007, 18:4780-4793.
59. Samson T., Welch C., Monaghan-Benson E., Hahn K.M., Burridge K. Endogenous RhoG is rapidly activated after epidermal growth factor stimulation through multiple guanine-nucleotide exchange factors. Mol. Biol. Cell 2010, 21:1629-1642.
60. van Buul J.D., Allingham M.J., Samson T., Meller J., Boulter E., Garcia-Mata R., Burridge K. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J. Cell Biol. 2007, 178:1279-1293.