EphA2 engages gitl to suppress arf6 activity modulating epithelial cell-cell contacts

Molecular Biology of the Cell

Volumn 20, Issue 7, 2009, Pages 1949-1959

  Miura, Koichi ^a,c   Nam, Jin Min ^a,b   Kojima, Chie ^a,b   Mochizuki, Naoki ^c   Sabe, Hisataka ^a,b  

^a OSAKA BIOSCIENCE INSTITUTE   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CALCIUM ION; CELL PROTEIN; EPHRIN A1; EPHRIN RECEPTOR A2; G PROTEIN COUPLED RECEPTOR KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NCK PROTEIN; PROTEIN GIT1; PROTEIN SH2; UNCLASSIFIED DRUG; UVOMORULIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADP-RIBOSYLATION FACTOR 6; CALCIUM; CELL CYCLE PROTEIN; GIT1 PROTEIN, MOUSE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; LIGAND; ONCOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL CONTACT; CELL DENSITY; CELL INTERACTION; CELL POLARITY; CONTROLLED STUDY; DOG; DOWN REGULATION; ENZYME ACTIVITY; EPITHELIUM CELL; HUMAN; HUMAN CELL; LIGAND BINDING; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; SYNAPSE; ANIMAL; CELL AGGREGATION; CELL COMMUNICATION; CELL COUNT; CELL FRACTIONATION; CELL LINE; CYTOLOGY; DOMINANT GENE; DRUG EFFECT; METABOLISM; MOUSE; PROTEIN TRANSPORT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADP-RIBOSYLATION FACTORS; ANIMALS; CALCIUM; CELL AGGREGATION; CELL COMMUNICATION; CELL COUNT; CELL CYCLE PROTEINS; CELL LINE; CELL POLARITY; DOGS; EPHRIN-A1; EPITHELIAL CELLS; GENES, DOMINANT; GTPASE-ACTIVATING PROTEINS; HUMANS; LIGANDS; MICE; ONCOGENE PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTOR, EPHA2; SUBCELLULAR FRACTIONS;

EID: 65249147216     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-06-0549     Document Type: Article

References (40)

1. Bagrodia, S., Bailey, D., Lenard, Z., Hart, M., Guan, J. L., Premont, R. T., Taylor, S. J., and Cerione, R. A. (1999). A tyrosine-phosphorylated protein that binds to an important regulatory region on the cool family of p21-activated kinase-binding proteins. J. Biol. Chem. 274, 22393-22400.
2. Bauer, T., Motosugi, N., Miura, K., Sabe, H., and Hiiragi, T. (2008). Dynamic rearrangement of surface proteins is essential for cytokinesis. Genesis 46, 152-162.
3. Becker, E., Huynh-Do, U., Holland, S., Pawson, T., Daniel, T. O., and Skolnik, E. Y. (2000). Nck-interacting Ste20 kinase couples Eph receptors to c-Jun N-terminal kinase and integrin activation. Mol. Cell. Biol. 20, 1537-1545.
4. Cortina, C., et al. (2007). EphB-ephrin-B interactions suppress colorectal cancer progression by compartmentalizing tumor cells. Nat. Genet. 39, 1376-1383.
5. Donaldson, J. G. (2003). Multiple roles for Arf 6, sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278, 41573-41576.
6. Frese, S., Schubert, W. D., Findeis, A. C., Marquardt, T., Roske, Y. S., Stradal, T. E., and Heinz, D. W. (2006). The phosphotyrosine peptide binding specificity of Nck1 and Nck2 Src homology 2 domains. J. Biol. Chem. 281, 18236-18245.
7. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
8. Guo, H., Miao, H., Gerber, L., Singh, J., Denning, M. F., Gilliam, A. C., and Wang, B. (2006). Disruption of EphA2 receptor tyrosine kinase leads to increased susceptibility to carcinogenesis in mouse skin. Cancer Res. 66, 7050-7058.
9. Hiroi, T., Someya, A., Thompson, W., Moss, J., and Vaughan, M. (2006). GEP100/BRAG 2, activator of ADP-ribosylation factor 6 for regulation of cell adhesion and actin cytoskeleton via E-cadherin and a-catenin. Proc. Natl. Acad. Sci. USA 103, 10672-10677.
10. Hoefen, R. J., and Berk, B. C. (2006). The multifunctional GIT family of proteins. J. Cell Sci. 119, 1469-1475.
11. Kullander, K., and Klein, R. (2002). Mechanisms and functions of Eph and ephrin signalling. Nat. Rev. Mol. Cell Biol. 3, 475-486.
12. Laprise, P., Langlois, M. J., Boucher, M. J., Jobin, C., and Rivard, N. (2004). Down-regulation of MEK/ERK signaling by E-cadherin-dependent PI3K/ Akt pathway in differentiating intestinal epithelial cells. J. Cell. Physiol. 199, 32-39.
13. Macrae, M., Neve, R. M., Rodriguez-Viciana, P., Haqq, C., Yeh, J., Chen, C., Gray, J. W., and McCormick, F. (2005). A conditional feedback loop regulates Ras activity through EphA2. Cancer Cell 8, 111-118.
14. Mazaki, Y., et al. (2001). An ADP-ribosylation factor GTPase-activating protein Git2-short/KIAA0148 is involved in subcellular localization of paxillin and actin cytoskeletal organization. Mol. Biol. Cell 12, 645-662.
15. Meyer, M. Z., Deliot, N., Chasserot-Golaz, S., Premont, R. T., Bader, M. F., and Vitale, N. (2006). Regulation of neuroendocrine exocytosis by the ARF6 GT- Pase-activating protein GIT1. J. Biol. Chem. 281, 7919-7926.
16. Miao, H., Burnett, E., Kinch, M., Simon, E., and Wang, B. (2000). Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat. Cell Biol. 2, 62-69.
17. Miao, H., Nickel, C. H., Cantley, L. G., Bruggeman, L. A., Bennardo, L. N., and Wang, B. (2003). EphA kinase activation regulates HGF-induced epithelial branching morphogenesis. J. Cell Biol. 162, 1281-1292.
18. 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. (2001). Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat. Cell Biol. 3, 527-530.
19. Morishige, M., et al. (2008). GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nat. Cell Biol. 10, 85-92.
20. Noblitt, L. W., Bangari, D. S., Shukla, S., Knapp, D. W., Mohammed, S., Kinch, M. S., and Mittal, S. K. (2004). Decreased tumorigenic potential of EphA2- overexpressing breast cancer cells following treatment with adenoviral vectors that express EphrinA1. Cancer Gene Ther. 11, 757-766.
21. Noren, N. K., Foos, G., Hauser, C. A., and Pasquale, E. B. (2006). The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat. Cell Biol. 8, 815-825.
22. Palacios, F., Price, L., Schweitzer, J., Collard, J. G., and D'Souza-Schorey, C. (2001). An essential role for ARF6-regulated membrane traffic in adherens junction turnover and epithelial cell migration. EMBO J. 20, 4973-4986.
23. Palacios, F., Schweitzer, J. K., Boshans, R. L., and D'Souza-Schorey, C. (2002). ARF6-GTP recruits Nm23-H1 to facilitate dynamin-mediated endocytosis during adherens junctions disassembly. Nat. Cell Biol. 4, 929-936.
24. Pasquale, E. B. (2005). Eph receptor signalling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6, 462-475.
25. Pasquale, E. B. (2008). Eph-Ephrin bidirectional signaling in physiology and disease. Cell 133, 38-52.
26. Penela, P., Ribas, C., Aymerich, I., Eijkelkamp, N., Barreiro, O., Heijnen, C. J., Kavelaars, A., Sanchez-Madrid, F., and Mayor, F., Jr. (2008). G protein- coupled receptor kinase 2 positively regulates epithelial cell migration. EMBO J. 27, 1206-1218.
27. Phee, H., Abraham, R. T., and Weiss, A. (2005). Dynamic recruitment of PAK1 to the immunological synapse is mediated by PIX independently of SLP-76 and Vav1. Nat. Immunol. 6, 608-617.
28. Premont, R. T., Claing, A., Vitale, N., Freeman, J. L., Pitcher, J. A., Patton, W. A., Moss, J., Vaughan, M., and Lefkowitz, R. J. (1998). /32-Adrenergic receptor regulation by GIT1, a G protein-coupled receptor kinase-associated ADP ribosylation factor GTPase-activating protein. Proc. Natl. Acad. Sci. USA 95, 14082-14087.
29. Radhakrishna, H., Al Awar, O., Khachikian, Z., and Donaldson, J. G. (1999). ARF6 requirement for Rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J. Cell Sci. 112, 855-866.
30. Ruiz, J. C., and Robertson, E. J. (1994). The expression of the receptor-protein tyrosine kinase gene, eck, is highly restricted during early mouse development. Mech. Dev. 46, 87-100.
31. Santy, L. C., and Casanova, J. E. (2001). Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599-610.
32. Surawska, H., Ma, P. C., and Salgia, R. (2004). The role of ephrins and Eph receptors in cancer. Cytokine Growth Factor Rev. 15, 419-433.
33. Suzuki, T., et al. (2006). Crucial role of the small GTPase ARF6 in hepatic cord formation during liver development. Mol. Cell. Biol. 26, 6149-6156.
34. Tague, S. E., Muralidharan, V., and D'Souza-Schorey, C. (2004). ADP-ribosy- lation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc. Natl. Acad. Sci. USA 101, 9671-9676.
35. Takeichi, M. (1991). Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451-1455.
36. Totaro, A., Paris, S., Asperti, C., and de Curtis, I. (2007). Identification of an intramolecular interaction important for the regulation of GIT1 functions. Mol. Biol. Cell 18, 5124-5138.
37. Vestweber, D., and Kemler, R. (1985). Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 4, 3393-3398.
38. Zantek, N. D., Azimi, M., Fedor-Chaiken, M., Wang, B., Brackenbury, R., and Kinch, M. S. (1999). E-cadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth Differ. 10, 629-638.
39. Zelinski, D. P., Zantek, N. D., Stewart, J. C., Irizarry, A. R., and Kinch, M. S. (2001). EphA2 overexpression causes tumorigenesis of mammary epithelial cells. Cancer Res. 61, 2301-2306.
40. Zhang, H., Webb, D. J., Asmussen, H., and Horwitz, A. F. (2003). Synapse formation is regulated by the signaling adaptor GIT1. J. Cell Biol. 161, 131-142.