EphA2 Mediates Ligand-Dependent Inhibition and Ligand-Independent Promotion of Cell Migration and Invasion via a Reciprocal Regulatory Loop with Akt

Cancer Cell

Volumn 16, Issue 1, 2009, Pages 9-20

  Miao, Hui ^a   Li, Da Qiang ^a   Mukherjee, Amitava ^a   Guo, Hong ^a   Petty, Aaron ^a   Cutter, Jennifer ^a   Basilion, James P ^a,b   Sedor, John ^a   Wu, Jiong ^d   Danielpour, David ^a   Sloan, Andrew E ^c   Cohen, Mark L ^c   Wang, Bingcheng ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Alzheimer Research Laboratory   (United States)

^c UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^d CELL SIGNALING TECHNOLOGY   (United States)

Author keywords

CELLCYCLE

Indexed keywords

ALANINE; EPHRIN A1; EPHRIN RECEPTOR A2; PROTEIN KINASE B; SERINE;

ARTICLE; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MUTATION; GLIOMA; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TUMOR CLASSIFICATION;

EID: 67649361516     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2009.04.009     Document Type: Article

References (56)

1. Alessi D.R., Caudwell F.B., Andjelkovic M., Hemmings B.A., and Cohen P. Molecular basis for the substrate specificity of protein kinase B; comparison with MAPKAP kinase-1 and p70 S6 kinase. FEBS Lett. 399 (1996) 333-338
2. Brat D.J., Castellano-Sanchez A.A., Hunter S.B., Pecot M., Cohen C., Hammond E.H., Devi S.N., Kaur B., and Van Meir E.G. Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res. 64 (2004) 920-927
3. Charest P.G., and Firtel R.A. Feedback signaling controls leading-edge formation during chemotaxis. Curr. Opin. Genet. Dev. 16 (2006) 339-347
4. Charest P.G., and Firtel R.A. Big roles for small GTPases in the control of directed cell movement. Biochem. J. 401 (2007) 377-390
5. Dodelet V.C., and Pasquale E.B. Eph receptors and ephrin ligands: embryogenesis to tumorigenesis. Oncogene 19 (2000) 5614-5619
6. Dohn M., Jiang J., and Chen X. Receptor tyrosine kinase EphA2 is regulated by p53-family proteins and induces apoptosis. Oncogene 20 (2001) 6503-6515
7. Engelman J.A., Luo J., and Cantley L.C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7 (2006) 606-619
8. Enomoto A., Murakami H., Asai N., Morone N., Watanabe T., Kawai K., Murakumo Y., Usukura J., Kaibuchi K., and Takahashi M. Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 9 (2005) 389-402
9. Fang W.B., Brantley-Sieders D.M., Parker M.A., Reith A.D., and Chen J. A kinase-dependent role for EphA2 receptor in promoting tumor growth and metastasis. Oncogene 24 (2005) 7859-7868
10. Friedl P., and Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3 (2003) 362-374
11. Furnari F.B., Fenton T., Bachoo R.M., Mukasa A., Stommel J.M., Stegh A., Hahn W.C., Ligon K.L., Louis D.N., Brennan C., et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 21 (2007) 2683-2710
12. Guo H., Miao H., Gerber L., Singh J., Denning M.F., Gilliam A.C., and Wang B. Disruption of EphA2 receptor tyrosine kinase leads to increased susceptibility to carcinogenesis in mouse skin. Cancer Res. 66 (2006) 7050-7058
13. Hafner C., Schmitz G., Meyer S., Bataille F., Hau P., Langmann T., Dietmaier W., Landthaler M., and Vogt T. Differential gene expression of Eph receptors and ephrins in benign human tissues and cancers. Clin. Chem. 50 (2004) 490-499
14. Hall A. Rho GTPases and the actin cytoskeleton. Science 279 (1998) 509-514
15. Higuchi M., Masuyama N., Fukui Y., Suzuki A., and Gotoh Y. Akt mediates Rac/Cdc42-regulated cell motility in growth factor-stimulated cells and in invasive PTEN knockout cells. Curr. Biol. 11 (2001) 1958-1962
16. Hirai H., Maru Y., Hagiwara K., Nishida J., and Takaku F. A novel putative tyrosine kinase receptor encoded by the eph gene. Science 238 (1987) 1717-1720
17. Ireton R.C., and Chen J. EphA2 receptor tyrosine kinase as a promising target for cancer therapeutics. Curr. Cancer Drug Targets 5 (2005) 149-157
18. Jiang P., Enomoto A., Jijiwa M., Kato T., Hasegawa T., Ishida M., Sato T., Asai N., Murakumo Y., and Takahashi M. An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res. 68 (2008) 1310-1318
19. Joy A.M., Beaudry C.E., Tran N.L., Ponce F.A., Holz D.R., Demuth T., and Berens M.E. Migrating glioma cells activate the PI3-K pathway and display decreased susceptibility to apoptosis. J. Cell Sci. 116 (2003) 4409-4417
20. Ju X., Katiyar S., Wang C., Liu M., Jiao X., Li S., Zhou J., Turner J., Lisanti M.P., Russell R.G., et al. Akt1 governs breast cancer progression in vivo. Proc. Natl. Acad. Sci. USA 104 (2007) 7438-7443
21. Kalo M.S., and Pasquale E.B. Multiple in vivo tyrosine phosphorylation sites in EphB receptors. Biochemistry 38 (1999) 14396-14408
22. Kalo M.S., Yu H.H., and Pasquale E.B. In vivo tyrosine phosphorylation sites of activated ephrin-b1 and ephb2 from neural tissue. J. Biol. Chem. 276 (2001) 38940-38948
23. Kim C.S., Vasko V.V., Kato Y., Kruhlak M., Saji M., Cheng S.Y., and Ringel M.D. AKT activation promotes metastasis in a mouse model of follicular thyroid carcinoma. Endocrinology 146 (2005) 4456-4463
24. Kim D., Kim S., Koh H., Yoon S.O., Chung A.S., Cho K.S., and Chung J. Akt/PKB promotes cancer cell invasion via increased motility and metalloproteinase production. FASEB J. 15 (2001) 1953-1962
25. Kullander K., and Klein R. Mechanisms and functions of Eph and ephrin signalling 2. Nat. Rev. Mol. Cell Biol. 3 (2002) 475-486
26. Li J., Yen C., Liaw D., Podsypanina K., Bose S., Wang S.I., Puc J., Miliaresis C., Rodgers L., McCombie R., et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275 (1997) 1943-1947
27. Li J., Ballif B.A., Powelka A.M., Dai J., Gygi S.P., and Hsu V.W. Phosphorylation of ACAP1 by Akt regulates the stimulation-dependent recycling of integrin beta1 to control cell migration. Dev. Cell 9 (2005) 663-673
28. Macrae M., Neve R.M., Rodriguez-Viciana P., Haqq C., Yeh J., Chen C., Gray J.W., and McCormick F. A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 8 (2005) 111-118
29. Manning B.D., and Cantley L.C. AKT/PKB Signaling: Navigating Downstream. Cell 129 (2007) 1261-1274
30. Meng Q., Xia C., Fang J., Rojanasakul Y., and Jiang B.H. Role of PI3K and AKT specific isoforms in ovarian cancer cell migration, invasion and proliferation through the p70S6K1 pathway. Cell. Signal. 18 (2006) 2262-2271
31. Miao H., and Wang B. Eph/ephrin signaling in epithelial development and homeostasis. Int. J. Biochem. Cell Biol. 41 (2008) 762-770
32. Miao H., Burnett E., Kinch M., Simon E., and Wang B. Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol. 2 (2000) 62-69
33. Miao H., Wei B.R., Peehl D.M., Li Q., Alexandrou T., Schelling J.R., Rhim J.S., Sedor J.R., Burnett E., and Wang B. Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat. Cell Biol. 3 (2001) 527-530
34. Miao H., Nickel C.H., Cantley L.G., Bruggeman L.A., Bennardo L.N., and Wang B. EphA kinase activation regulates HGF-induced epithelial branching morphogenesis. J. Cell Biol. 162 (2003) 1281-1292
35. Miao H., Strebhardt K., Pasquale E.B., Shen T.L., Guan J.L., and Wang B. Inhibition of integrin-mediated cell adhesion but not directional cell migration requires catalytic activity of EphB3 receptor tyrosine kinase: role of rho family small GTPases. J. Biol. Chem. 280 (2005) 923-932
36. Miller C.R., and Perry A. Glioblastoma. Arch. Pathol. Lab. Med. 131 (2007) 397-406
37. Nakamoto M., and Bergemann A.D. Diverse roles for the Eph family of receptor tyrosine kinases in carcinogenesis. Microsc. Res. Tech. 59 (2002) 58-67
38. Park B.K., Zeng X., and Glazer R.I. Akt1 induces extracellular matrix invasion and matrix metalloproteinase-2 activity in mouse mammary epithelial cells. Cancer Res. 61 (2001) 7647-7653
39. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 321 (2008) 1807-1812
40. Pasquale E.B. Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6 (2005) 462-475
41. Pasquale E.B. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133 (2008) 38-52
42. Poliakov A., Cotrina M., and Wilkinson D.G. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell 7 (2004) 465-480
43. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., and Horwitz A.R. Cell migration: integrating signals from front to back. Science 302 (2003) 1704-1709
44. Scherer H.J. Structural development in gliomas. Am. J. Cancer 34 (1938) 333-351
45. Shaw R.J., and Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 441 (2006) 424-430
46. Shukla S., MacLennan G.T., Hartman D.J., Fu P., Resnick M.I., and Gupta S. Activation of PI3K-Akt signaling pathway promotes prostate cancer cell invasion. Int. J. Cancer 121 (2007) 1424-1432
47. Somanath P.R., Kandel E.S., Hay N., and Byzova T.V. Akt1 signaling regulates integrin activation, matrix recognition, and fibronectin assembly. J. Biol. Chem. 282 (2007) 22964-22976
48. TCGA Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455 (2008) 1061-1068
49. Tomlins S.A., Rubin M.A., and Chinnaiyan A.M. Integrative biology of prostate cancer progression. Annu. Rev. Pathol. 1 (2006) 243-271
50. Vasko V., Saji M., Hardy E., Kruhlak M., Larin A., Savchenko V., Miyakawa M., Isozaki O., Murakami H., Tsushima T., et al. Akt activation and localisation correlate with tumour invasion and oncogene expression in thyroid cancer. J. Med. Genet. 41 (2004) 161-170
51. Vivanco I., and Sawyers C.L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat. Rev. Cancer 2 (2002) 489-501
52. Wang H., Wang H., Zhang W., Huang H.J., Liao W.S., and Fuller G.N. Analysis of the activation status of Akt, NFkappaB, and Stat3 in human diffuse gliomas. Lab. Invest. 84 (2004) 941-951
53. Wippold F.J., Lammle M., Anatelli F., Lennerz J., and Perry A. Neuropathology for the neuroradiologist: palisades and pseudopalisades. AJNR Am. J. Neuroradiol. 27 (2006) 2037-2041
54. Wykosky J., Gibo D.M., Stanton C., and Debinski W. EphA2 as a novel molecular marker and target in glioblastoma multiforme. Mol. Cancer Res. 3 (2005) 541-551
55. Zelinski D.P., Zantek N.D., Stewart J.C., Irizarry A.R., and Kinch M.S. EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 61 (2001) 2301-2306
56. Zhang G., Njauw C.N., Park J.M., Naruse C., Asano M., and Tsao H. EphA2 is an essential mediator of UV radiation-induced apoptosis. Cancer Res. 68 (2008) 1691-1696