Src family kinases are involved in EphA receptor-mediated retinal axon guidance

Journal of Neuroscience

Volumn 24, Issue 28, 2004, Pages 6248-6257

  Knöll, Bernd ^a   Drescher, Uwe ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Actin cytoskeleton; Axon guidance; Eph family; Intracellular signaling; Retinotectal projection; Src family kinase

Indexed keywords

ACTIN; CORTACTIN; EPHA RECEPTOR TYROSINE KINASE; EPHRIN A1; EPHRIN A2; LIGAND; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CHICKEN; CONTROL SYSTEM; CYTOSKELETON; EMBRYO; ENZYME ACTIVITY; EYE DEVELOPMENT; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOCHEMISTRY; IMMUNOPRECIPITATION; MICROTUBULE; NERVE FIBER; NERVE GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA CONE; RETINA NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CHICK EMBRYO; CORTACTIN; ELECTROPORATION; ENZYME INHIBITORS; EYE PROTEINS; GREEN FLUORESCENT PROTEINS; GROWTH CONES; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; KIDNEY; MICE; MICROFILAMENT PROTEINS; OPTIC NERVE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-TYROSINE KINASES; RECEPTORS, EPH FAMILY; RECOMBINANT FUSION PROTEINS; RETINAL GANGLION CELLS; SRC-FAMILY KINASES;

EID: 17044448886     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0985-04.2004     Document Type: Article

References (62)

1. Abram CL, Courtneidge SA (2000) Src family tyrosine kinases and growth factor signaling. Exp Cell Res 254:1-13.
2. Beggs HE, Soriano P, Maness PF (1994) NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J Cell Biol 127:825-833.
3. 1101 is associated with modulation of receptor function. J Biol Chem 274:8335-8343.
4. Blake RA, Broome MA, Liu X, Wu J, Gishizky M, Sun L, Courtneidge SA (2000) SU6656, a selective Src family kinase inhibitor, used to probe growth factor signaling. Mol Cell Biol 20:9018-9027.
5. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-1026.
6. Cary LA, Cooper JA (2000) Molecular switches in lipid rafts. Nature 404:945-947.
7. Cheng HJ, Nakamoto M, Bergemann AD, Flanagan JG (1995) Complementary gradients in expression and binding of ELF-1 and MEK4 in development of the topographic retinotectal projection map. Cell 82:371-381.
8. Ciossek T, Monschau B, Kremoser C, Löschinger J, Lang S, Müller BK, Bonhoeffer F, Drescher U (1998) Eph receptor-ligand interactions are necessary for guidance of retinal ganglion cell axons in vitro. Eur J Neurosci 10:1574-1580.
9. Connor RJ, Menzel P, Pasquale EB (1998) Expression and tyrosine phosphorylation of Eph receptors suggest multiple mechanisms in patterning of the visual system. Dev Biol 193:21-35.
10. Cox EC, Müller B, Bonhoeffer F (1990) Axonal guidance in the chick visual system: posterior tectal membranes induce collapse of growth cones from the temporal retina. Neuron 2:31-37.
11. Davy A, Gale NW, Murray EW, Klinghoffer RA, Soriano P, Feuerstein C, Robbins SM (1999) Compartmentalized signaling by GPI-anchored ephrin-A5 requires the Fyn tyrosine kinase to regulate cellular adhesion. Genes Dev 13:3125-3135.
12. Drescher U, Bonhoeffer F, Müller BK (1997) The Eph family in retinal axon guidance. Curr Opin Neurobiol 7:75-80.
13. Du Y, Weed SA, Xiong WC, Marshall TD, Parsons JT (1998) Identification of a novel cortactin SH3 domain-binding protein and its localization to growth cones of cultured neurons. Mol Cell Biol 18:5838-5851.
14. fyn. Oncogene 12:1727-1736.
15. Fan L, Di Ciano-Oliveira C, Weed SA, Craig AW, Greer PA, Rotstein OD, Kapus A (2004) Actin depolymerization-induced tyrosine phosphorylation of cortactin: the role of Fer kinase. Biochem J 380[Pt 2]:581-591.
16. Feldheim J, Kim Y-I, Bergemann AD, Frisén J, Barbacid M, Flanagan JG (2000) Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25:563-574.
17. Flanagan JG, Vanderhaeghen P (1998) The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345.
18. Frame MC, Fincham VJ, Carragher NO, Wyke JA (2002) v-Src's hold over actin and cell adhesions. Nat Rev Mol Cell Biol 3:233-245.
19. Guan KL, Rao Y (2003) Signalling mechanisms mediating neuronal responses to guidance cues. Nat Rev Neurosci 4:941-956.
20. Hall A, Nobes CD (2000) Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos Trans R Soc Lond B Biol Sci 355:965-970.
21. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, Connelly PA (1996) Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. J Biol Chem 271:695-701.
22. Harris KF, Shoji I, Cooper EM, Kumar S, Oda H, Howley PM (1999) Ubiquitin-mediated degradation of active Src tyrosine kinase. Proc Natl Acad Sci USA 96:13738-13743.
23. Head JA, Jiang D, Li M, Zorn LJ, Schaefer EM, Parsons JT, Weed SA (2003) Cortactin tyrosine phosphorylation requires Rac1 activity and association with the cortical actin cytoskeleton. Mol Biol Cell 14:3216-3229.
24. Hornberger MR, Dutting D, Ciossek T, Yamada T, Handwerker C, Lang S, Weth F, Huf J, Wessel R, Logan C, Tanaka H, Drescher U (1999) Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 22:731-742.
25. Howell BW, Cooper JA (1994) Csk suppression of Src involves movement of Csk to sites of Src activity. Mol Cell Biol 14:5402-5411.
26. Huai J, Drescher U (2001) An ephrinA-dependent signaling pathway controls integrin function and is linked to the tyrosine phosphorylation of a 120 kDa protein. J Biol Chem 276:6689-6694.
27. Huang C, Ni Y, Wang T, Gao Y, Haudenschild CC, Zhan X (1997a) Downregulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J Biol Chem 272:13911-13915.
28. Huang C, Tandon NN, Greco NJ, Ni Y, Wang T, Zhan X (1997b) Proteolysis of platelet cortactin by calpain. J Biol Chem 272:19248-19252.
29. Huang J, Asawa T, Takato T, Sakai R (2003) Cooperative roles of Fyn and cortactin in cell migration of metastatic murine melanoma. J Biol Chem 278:48367-48376.
30. Ignelzi Jr MA, Miller DR, Soriano P, Maness PF (1994) Impaired neurite outgrowth of Src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12:873-884.
31. Imamoto A, Soriano P (1993) Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 73:1117-1124.
32. Kapus A, Di Ciano C, Sun J, Zhan X, Kim L, Wong TW, Rotstein OD (2000) Cell volume-dependent phosphorylation of proteins of the cortical cytoskeleton and cell-cell contact sites. The role of Fyn and FER kinases. J Biol Chem 275:32289-32298.
33. Kawakatsu H, Sakai T, Takagaki Y, Shinoda Y, Saito M, Owada MK, Yano J (1996) A new monoclonal antibody which selectively recognizes the active form of Src tyrosine kinase. J Biol Chem 271:5680-5685.
34. Klinghoffer RA, Sachsenmaier C, Cooper JA, Soriano P (1999) Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J 18:2459-2471.
35. Knöll B, Drescher U (2002) Ephrin-As as receptors in topographic projections. Trends Neurosci 25:145-149.
36. Knöll B, Zarbalis Z, Wurst W, Drescher U (2001) A role for the EphA family in the topographic targeting of vomeronasal axons. Development 128:895-906.
37. Kullander K, Klein R (2002) Mechanisms and functions of Eph and ephrin signaling. Nat Rev Mol Cell Biol 3:475-486.
38. Lai KO, Ip FC, Cheung J, Fu AK, Ip NY (2001) Expression of Eph receptors in skeletal muscle and their localization at the neuromuscular junction. Mol Cell Neurosci 17:1034-1047.
39. McLaughlin T, Hindges R, O'Leary DD (2003) Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr Opin Neurobiol 13:57-69.
40. Menzel P, Valencia F, Godement P, Dodelet VC, Pasquale EB (2001) Ephrin-A6, a new ligand for EphA receptors in the developing visual system. Dev Biol 230:74-88.
41. Monschau B, Kremoser C, Ohta K, Tanaka H, Kaneko T, Yamada T, Handwerker C, Hornberger MR, Löschinger J, Pasquale EB, Siever DA, Verderame MF, Müller BK, Bonhoeffer F, Drescher U (1997) Shared and distinct functions of RAGS and ELF-1 in guiding retinal axons. EMBO J 16:1258-1267.
42. c-src modulate axonal guidance in the developing mouse olfactory pathway. J Neurobiol 36:53-63.
43. Nada S, Yagi T, Takeda H, Tokunaga T, Nakagawa H, Ikawa Y, Okada M, Aizawa S (1993) Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell 73:1125-1135.
44. Nakagawa T, Tanaka S, Suzuki H, Takayanagi H, Miyazaki T, Nakamura K, Tsuruo T (2000) Overexpression of the csk gene suppresses tumor metastasis in vivo. Int J Cancer 88:384-391.
45. Raper JA, Kapfhammer J (1990) The enrichment of a neuronal growth cone collapsing activity from embryonic chick brain. Neuron 4:21-29.
46. Robles E, Huttenlocher A, Gomez TM (2003) Filopodial calcium transients regulate growth cone motility and guidance through local activation of calpain. Neuron 38:597-609.
47. Shamah SM, Lin MZ, Goldberg JL, Estrach S, Sahin M, Hu L, Bazalakova M, Neve RL, Corfas G, Debant A, Greenberg ME (2001) EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105:233-244.
48. Stein PL, Vogel H, Soriano P (1994) Combined deficiencies of Src, Fyn, and Yes tyrosine kinases in mutant mice. Genes Dev 8:1999-2007.
49. Suetsugu S, Hattori M, Miki H, Tezuka T, Yamamoto T, Mikoshiba K, Takenawa T (2002) Sustained activation of N-WASP through phosphorylation is essential for neurite extension. Dev Cell 3:645-658.
50. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 295:491-495.
51. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609.
52. Shc to activate MAPK/ERK and promote chemotaxis. J Cell Biol 162:661-671.
53. Wahl S, Barth H, Ciossek T, Aktories K, Mueller BK (2000) Ephrin-A5 induces collapse of growth cones by activating Rho and Rho kinase. J Cell Biol 149:263-270.
54. Walter J, Kern-Veits B, Huf J, Stolze B, Bonhoeffer F (1987) Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101:685-696.
55. Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, Cooper JA (2001) Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr Biol 11:370-374.
56. Weed SA, Parsons JT (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20:6418-6434.
57. Weed SA, Du Y, Parsons JT (1998) Translocation of cortactin to the cell periphery is mediated by the small GTPase Rac1. J Cell Sci 111[Pt 16]:2433-2443.
58. Weinl C, Drescher U, Lang S, Bonhoeffer F, Loschinger J (2003) On the turning of Xenopus retinal axons induced by ephrin-A5. Development 130:1635-1643.
59. Wilkinson DG (2000) Topographic mapping: organizing by repulsion and competition? Curr Biol 10:R447-R451.
60. Wong EV, Kerner JA, Jay DG (2004) Convergent and divergent signaling mechanisms of growth cone collapse by ephrinA5 and slit2. J Neurobiol 59:66-81.
61. Worley T, Holt C (1996) Inhibition of protein tyrosine kinases impairs axon extension in the embryonic optic tract. J Neurosci 16:2294-2306.
62. Zisch AH, Kalo MS, Chong LD, Pasquale EB (1998) Complex formation between EphB2 and Src requires phosphorylation of tyrosine 611 in the EphB2 juxtamembrane region. Oncogene 16:2657-2670.