Regulation of process retraction and cell migration by EphA3 is mediated by the adaptor protein Nck1

Biochemistry

Volumn 48, Issue 27, 2009, Pages 6369-6378

  Hu, Tianjing ^a   Shi, Guanfang ^a   Larose, Louise ^b   Rivera, Gonzalo M ^c   Mayer, Bruce J ^c   Zhou, Renping ^a,d  

^a RUTGERS UNIVERSITY   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEINS; ANGIOGENESIS; BIOLOGICAL FUNCTIONS; CELL MIGRATION; CO-IMMUNOPRECIPITATION; CYTOPLASMIC DOMAINS; EMBRYONIC DEVELOPMENT; EPHRINS; FUSION PROTEINS; INHIBITING EFFECT; MOLECULAR MECHANISM; NERVOUS SYSTEM; NEURAL ACTIVITY; PATHOLOGICAL CONDITIONS; PHOSPHOTYROSINE; SH2 DOMAIN; STRONG BINDING; TISSUE BOUNDARY; TUMOR PROGRESSIONS; TYROSINE KINASE; WILD TYPES; YEAST TWO HYBRID;

AMINO ACIDS; CYTOLOGY;

LIGANDS;

ADAPTOR PROTEIN; EPHRIN RECEPTOR A3; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; MUTANT PROTEIN; PHOSPHOTYROSINE; PROTEIN NCK1; PROTEIN SH2; PROTEIN SH3; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOPLASM; GENE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MUTATION; NCK1 GENE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TWO HYBRID SYSTEM; WILD TYPE; YEAST;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL MOVEMENT; IMMUNOPRECIPITATION; ONCOGENE PROTEINS; RECEPTOR, EPHA3; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 67650080520     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900831k     Document Type: Article

References (65)

1. Pasquale, E. B. (2005) Eph receptor signaling casts a wide net on cell behaviour. Nat. Rev. Mol. Cell Biol. 6, 462-475.
2. Gale, N. W., Holland, S. J., Valenzuela, D. M., Flenniken, A., Pan, L., Ryan, T. E., Henkemeyer, M., Strebhardt, K., Hirai, H., Wilkinson, D. G., Pawson, T., Davis, S., and Yancopoulos, G. D. (1996) Eph receptors and ligands comprise two major specificity subclasses and are reciprocally compartmentalized during embryogenesis. Neuron 17, 9-19.
3. Zhou, R. (1998) The Eph family receptors and ligands. Pharmacol. Ther. 77, 151-181.
4. Himanen, J. P., Chumley, M. J., Lackmann, M., Li, C., Barton, W. A., Jeffrey, P. D., Vearing, C., Geleick, D., Feldheim, D. A., Boyd, A. W., Henkemeyer, M., and Nikolov, D. B. (2004) Repelling class discrimination: Ephrin-A5 binds to and activates EphB2 receptor signaling. Nat. Neurosci. 7, 501-509.
5. Beckmann, M. P., Cerretti, D. P., Baum, P., Vanden Bos, T., James, L., Farrah, T., Kozlosky, C., Hollingsworth, T., Shilling, H., and Maraskovsky, E..; et al. (1994) Molecular characterization of a family of ligands for eph-related tyrosine kinase receptors. EMBO J. 13, 3757-3762.
6. Pasquale, E. B. (2008) Eph-ephrin bidirectional signaling in physiology and disease. Cell 133, 38-52.
7. Poliakov, A., Cotrina, M., and Wilkinson, D. G. (2004) Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev. Cell 7, 465-480.
8. Gao, P. P., Sun, C. H., Zhou, X. F., DiCicco-Bloom, E., and Zhou, R. (2000) Ephrins stimulate or inhibit neurite outgrowth and survival as a function of neuronal cell type. J. Neurosci. Res. 60, 427-436.
9. Zhou, X., Suh, J., Cerretti, D. P., Zhou, R., and DiCicco-Bloom, E. (2001) Ephrins stimulate neurite outgrowth during early cortical neurogenesis. J. Neurosci. Res. 66, 1054-1063.
10. Hindges, R., McLaughlin, T., Genoud, N., Henkemeyer, M., and O'Leary, D. (2002) EphB Forward Signaling Controls Directional Branch Extension and Arborization Required for Dorsal-Ventral Retinotopic Mapping. Neuron 35, 475-487.
11. Holmberg, J., Clarke, D. L., and Frisen, J. (2000) Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408, 203-206.
12. Eberhart, J., Barr, J., O'Connell, S., Flagg, A., Swartz, M. E., Cramer, K. S., Tosney, K. W., Pasquale, E. B., and Krull, C. E. (2004) Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons. J. Neurosci. 24, 1070-1078.
13. Matsuoka, H., Obama, H., Kelly, M. L., Matsui, T., and Nakamoto, M. (2005) Biphasic functions of the kinase-defective Ephb6 receptor in cell adhesion and migration. J. Biol. Chem. 280, 29355-29363.
14. Miao, H., Strebhardt, K., Pasquale, E. B., Shen, T. L., Guan, J. L., and Wang, B. (2005) 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, 923-932.
15. Davy, A., and Soriano, P. (2005) Ephrin signaling in vivo: Look both ways. Dev. Dyn. 232, 1-10.
16. Grunwald, I. C., Korte, M., Wolfer, D., Wilkinson, G. A., Unsicker, K., Lipp, H. P., Bonhoeffer, T., and Klein, R. (2001) Kinase-Independent Requirement of EphB2 Receptors in Hippocampal Synaptic Plasticity. Neuron 32, 1027-1040.
17. Henderson, J. T., Georgiou, J., Jia, Z., Robertson, J., Elowe, S., Roder, J. C., and Pawson, T. (2001) The Receptor Tyrosine Kinase EphB2 Regulates NMDA-Dependent Synaptic Function. Neuron 32, 1041-1056.
18. 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.
19. Brantley-Sieders, D., Schmidt, S., Parker, M., and Chen, J. (2004) Eph receptor tyrosine kinases in tumor and tumor microenvironment. Curr. Pharm. Des. 10, 3431-3442.
20. Murai, K. K., and Pasquale, E. B. (2005) New exchanges in eph-dependent growth cone dynamics. Neuron 46, 161-163.
21. Iwasato, T., Katoh, H., Nishimaru, H., Ishikawa, Y., Inoue, H., Saito, Y. M., Ando, R., Iwama, M., Takahashi, R., Negishi, M., and Itohara, S. (2007) Rac-GAP α-chimerin regulates motor-circuit formation as a key mediator of EphrinB3/EphA4 forward signaling. Cell 130, 742-753.
22. Wegmeyer, H., Egea, J., Rabe, N., Gezelius, H., Filosa, A., Enjin, A., Varoqueaux, F., Deininger, K., Schnutgen, F., Brose, N., Klein, R., Kullander, K., and Betz, A. (2007) EphA4-dependent axon guidance is mediated by the RacGAP α2-chimaerin. Neuron 55, 756-767.
23. Beg, A. A., Sommer, J. E., Martin, J. H., and Scheiffele, P. (2007) α2-Chimaerin is an essential EphA4 effector in the assembly of neuronal locomotor circuits. Neuron 55, 768-778.
24. Holland, S. J., Gale, N. W., Gish, G. D., Roth, R. A., Songyang, Z., Cantley, L. C., Henkemeyer, M., Yancopoulos, G. D., and Pawson, T. (1997) Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells. EMBO J. 16, 3877-3888.
25. 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.
26. Parri, M., Buricchi, F., Taddei, M. L., Giannoni, E., Raugei, G., Ramponi, G., and Chiarugi, P. (2005) EphrinA1 repulsive response is regulated by an EphA2 tyrosine phosphatase. J. Biol. Chem. 280, 34008-34018.
27. Kikawa, K. D., Vidale, D. R., Van Etten, R. L., and Kinch, M. S. (2002) Regulation of the EphA2 kinase by the low molecular weight tyrosine phosphatase induces transformation. J. Biol. Chem. 277, 39274-39279.
28. Shintani, T., Ihara, M., Sakuta, H., Takahashi, H., Watakabe, I., and Noda, M. (2006) Eph receptors are negatively controlled by protein tyrosine phosphatase receptor type O. Nat. Neurosci. 9, 761-769.
29. Knoll, B., and Drescher, U. (2004) Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J. Neurosci. 24, 6248-6257.
30. Zimmer, G., Kastner, B., Weth, F., and Bolz, J. (2007) Multiple effects of ephrin-A5 on cortical neurons are mediated by SRC family kinases. J. Neurosci. 27, 5643-5653.
31. Parri, M., Buricchi, F., Giannoni, E., Grimaldi, G., Mello, T., Raugei, G., Ramponi, G., and Chiarugi, P. (2007) EphrinA1 activates a Src/focal adhesion kinase-mediated motility response leading to rho-dependent actino/myosin contractility. J. Biol. Chem. 282, 19619-19628.
32. Yue, X., Dreyfus, C., Kong, T. A., and Zhou, R. (2008) A subset of signal transduction pathways is required for hippocampal growth cone collapse induced by ephrin-A5. Dev. Neurobiol. 68, 1269-1286.
33. Dalva, M. B., Takasu, M. A., Lin, M. Z., Shamah, S. M., Hu, L., Gale, N. W., and Greenberg, M. E. (2000) EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945-956.
34. Takasu, M. A., Dalva, M. B., Zigmond, R. E., and Greenberg, M. E. (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295, 491-495.
35. Pawson, T. (2004) Specificity in signal transduction: From phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116, 191-203.
36. Zisch, A. H., Pazzagli, C., Freeman, A. L., Schneller, M., Hadman, M., Smith, J. W., Ruoslahti, E., and Pasquale, E. B. (2000) Replacing two conserved tyrosines of the EphB2 receptor with glutamic acid prevents binding of SH2 domains without abrogating kinase activity and biological responses. Oncogene 19, 177-187.
37. Bladt, F., Aippersbach, E., Gelkop, S., Strasser, G. A., Nash, P., Tafuri, A., Gertler, F. B., and Pawson, T. (2003) The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol. Cell. Biol. 23, 4586-4597.
38. Kudo, C., Ajioka, I., Hirata, Y., and Nakajima, K. (2005) Expression profiles of EphA3 at both the RNA and protein level in the developing mammalian forebrain. J. Comp. Neurol. 487, 255-269.
39. Lawrenson, I. D., Wimmer-Kleikamp, S. H., Lock, P., Schoenwaelder, S. M., Down, M., Boyd, A. W., Alewood, P. F., and Lackmann, M. (2002) Ephrin-A5 induces rounding, blebbing and de-adhesion of EphA3-expressing 293T and melanoma cells by CrkII and Rho-mediated signalling. J. Cell Sci. 115, 1059-1072.
40. Tanaka, M., Gupta, R., and Mayer, B. J. (1995) Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol. Cell. Biol. 15, 6829-6837.
41. Gupta, R. W., and Mayer, B. J. (1998) Dominant-negative mutants of the SH2/SH3 adapters Nck and Grb2 inhibit MAP kinase activation and mesoderm-specific gene induction by eFGF in Xenopus. Oncogene 17, 2155-2165.
42. Stein, E., Lane, A. A., Cerretti, D. P., Schoecklmann, H. O., Schroff, A. D., Van Etten, R. L., and Daniel, T. O. (1998) Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses. Genes Dev. 12, 667-678.
43. Buday, L., Wunderlich, L., and Tamas, P. (2002) The Nck family of adapter proteins. Regulators of actin cytoskeleton. Cell. Signalling 14, 723-731.
44. Roche, S., McGlade, J., Jones, M., Gish, G. D., Pawson, T., and Courtneidge, S. A. (1996) Requirement of phospholipase Cγ, the tyrosine phosphatase Syp and the adaptor proteins Shc and Nck for PDGF-induced DNA synthesis: Evidence for the existence of Ras-dependent and Ras-independent pathways. EMBO J. 15, 4940-4948.
45. Tang, J., Feng, G. S., and Li, W. (1997) Induced direct binding of the adapter protein Nck to the GTPase-activating protein-associated protein p62 by epidermal growth factor. Oncogene 15, 1823-1832.
46. Rivera, G. M., Antoku, S., Gelkop, S., Shin, N. Y., Hanks, S. K., Pawson, T., and Mayer, B. J. (2006) Requirement of Nck adaptors for actin dynamics and cell migration stimulated by platelet-derived growth factor B. Proc. Natl. Acad. Sci. U.S.A. 103, 9536-9541.
47. Li, X., Meriane, M., Triki, I., Shekarabi, M., Kennedy, T. E., Larose, L., and Lamarche-Vane, N. (2002) The adaptor protein Nck-1 couples the netrin-1 receptor DCC (deleted in colorectal cancer) to the activation of the small GTPase Rac1 through an atypical mechanism. J. Biol. Chem. 277, 37788-37797.
48. Songyang, Z., Shoelson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. G., King, F., Roberts, T., Ratnofsky, S., and Lechleider, R. J.; et al. (1993) SH2 domains recognize specific phosphopeptide sequences. Cell 72, 767-778.
49. Stein, E., Huynh-Do, U., Lane, A. A., Cerretti, D. P., and Daniel, T. O. (1998) Nck recruitment to Eph receptor, EphB1/ELK, couples ligand activation to c-Jun kinase. J. Biol. Chem. 273, 1303-1308.
50. Lu, W., Katz, S., Gupta, R., and Mayer, B. J. (1997) Activation of Pak by membrane localization mediated by an SH3 domain from the adaptor protein Nck. Curr. Biol. 7, 85-94.
51. Zhao, Z. S., Manser, E., and Lim, L. (2000) Interaction between PAK and Nck: A template for Nck targets and role of PAK autophosphorylation. Mol. Cell. Biol. 20, 3906-3917.
52. Bokoch, G. M. (2003) Biology of the p21-activated kinases. Annu. Rev. Biochem. 72, 743-781.
53. Edwards, D. C., Sanders, L. C., Bokoch, G. M., and Gill, G. N. (1999) Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1, 253-259.
54. Sanders, L. C., Matsumura, F., Bokoch, G. M., and de Lanerolle, P. (1999) Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
55. Shamah, S. M., Lin, M. Z., Goldberg, J. L., Estrach, S., Sahin, M., Hu, L., Bazalakova, M., Neve, R. L., Corfas, G., Debant, A., and Greenberg, M. E. (2001) EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233-244.
56. Hing, H., Xiao, J., Harden, N., Lim, L., and Zipursky, S. L. (1999) Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97, 853-863.
57. Rohatgi, R., Nollau, P., Ho, H. Y., Kirschner, M. W., and Mayer, B. J. (2001) Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 276, 26448-26452.
58. Rivera, G. M., Briceno, C. A., Takeshima, F., Snapper, S. B., and Mayer, B. J. (2004) Inducible clustering of membrane-targeted SH3 domains of the adaptor protein Nck triggers localized actin polymerization. Curr. Biol. 14, 11-22.
59. Takenawa, T., and Suetsugu, S. (2007) The WASP-WAVE protein network: Connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8, 37-48.
60. Derry, J. M., Ochs, H. D., and Francke, U. (1994) Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 78, 635-644.
61. 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.
62. Su, Y. C., Treisman, J. E., and Skolnik, E. Y. (1998) The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes Dev. 12, 2371-2380.
63. Ruan, W., Pang, P., and Rao, Y. (1999) The SH2/SH3 adaptor protein dock interacts with the Ste20-like kinase misshapen in controlling growth cone motility. Neuron 24, 595-605.
64. Li, W., Fan, J., and Woodley, D. T. (2001) Nck/Dock: An adapter between cell surface receptors and the actin cytoskeleton. Oncogene 20, 6403-6417.
65. Fawcett, J. P., Georgiou, J., Ruston, J., Bladt, F., Sherman, A., Warner, N., Saab, B. J., Scott, R., Roder, J. C., and Pawson, T. (2007) Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc. Natl. Acad. Sci. U.S.A. 104, 20973-20978.