Multiple effects of ephrin-A5 on cortical neurons are mediated by Src family kinases

Journal of Neuroscience

Volumn 27, Issue 21, 2007, Pages 5643-5653

  Zimmer, Geraldine ^a   Kästner, Bettina ^a   Weth, Franco ^a   Bolz, Jürgen ^a  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Adhesion; Ephrin A5; Membrane ripping; Motility; Receptor release; SFKs

Indexed keywords

EPHRIN A5; EPHRIN RECEPTOR; PROTEIN TYROSINE KINASE; EPHRIN RECEPTOR A5;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL ADHESION; CELL AGGREGATION; CELL MOTILITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; ANIMAL; CELL MOTION; CELL STRAIN 3T3; COMPARATIVE STUDY; CYTOLOGY; DRUG ANTAGONISM; ENZYMOLOGY; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CELL AGGREGATION; CELL MOVEMENT; EPHRIN-A5; HUMANS; MICE; NEURONS; NIH 3T3 CELLS; RECEPTOR, EPHA5; SRC-FAMILY KINASES;

EID: 34250656906     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0954-07.2007     Document Type: Article

References (54)

1. Bard JB, Hay ED (1975) The behavior of fibroblasts from the developing avian cornea. Morphology and movement in situ and in vitro. J Cell Biol 67:400-418.
2. Bohme B, VandenBos T, Cerretti DP, Park LS, Holtrich U, Rubsamen-Waigmann H, Strebhardt K (1996) Cell-cell adhesion mediated by binding of membrane-anchored ligand LERK-2 to the EPH-related receptor human embryonal kinase 2 promotes tyrosine kinase activity. J Biol Chem 271:24747-24752.
3. Castellani V, Yue Y, Gao PP, Zhou R, Bolz J (1998) Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits. J Neurosci 18:4663-4672.
4. Chen WT (1981) Mechanism of retraction of the trailing edge during fibroblast movement. J Cell Biol 90:187-200.
5. 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.
6. Dail M, Richter M, Godement P, Pasquale EB (2006) Eph receptors inactivate R-Ras through different mechanisms to achieve cell repulsion. J Cell Sci 119:1244-1254.
7. Depaepe V, Suarez-Gonzalez N, Dufour A, Passante L, Gorski JA, Jones KR, Ledent C, Vanderhaeghen P (2005) Ephrin signalling controls brain size by regulating apoptosis of neural progenitors. Nature 435:1244-1250.
8. Dickson BJ (2002) Molecular mechanisms of axon guidance. Science 298:1959-1964.
9. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F (1995) In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
10. Eberhart J, Barr J, O'Connell S, Flagg A, Swartz ME, Cramer KS, Tosney KW, Pasquale EB, Krull CE (2004) Ephrin-A5 exerts positive or inhibitory effects on distinct subsets of EphA4-positive motor neurons. J Neurosci 24:1070-1078.
11. Ellis C, Kasmi F, Ganju P, Walls E, Panayotou G, Reith AD (1996) A juxtamembrane autophosphorylation site in the Eph family receptor tyrosine kinase, Sek, mediates high affinity interaction with p59fyn. Oncogene 12:1727-1736.
12. Falk J, Bechara A, Fiore R, Nawabi H, Zhou H, Hoyo-Becerra C, Bozon M, Rougon G, Grumet M, Puschel AW, Sanes JR, Castellani V (2005) Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48:63-75.
13. Felsenfeld DP, Schwartzberg PL, Venegas A, Tse R, Sheetz MP (1999) Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src. Nat Cell Biol 1:200-206.
14. Flanagan JG, Vanderhaeghen P (1998) The ephrins and Eph receptors in neural development. Annu Rev Neurosci 21:309-345.
15. 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.
16. 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. Study of Lck- and FynT-dependent T cell activation. J Biol Chem 271:695-701.
17. Hattori M, Osterfield M, Flanagan JG (2000) Regulated cleavage of a contact-mediated axon repellent. Science 289:1360-1365.
18. Heidinger V, Manzerra P, Wang XQ, Strasser U, Yu SP, Choi DW, Behrens MM (2002) Metabotropic glutamate receptor 1-induced upregulation of NMDA receptor current: mediation through the Pyk2/Src-family kinase pathway in cortical neurons. J Neurosci 22:5452-5461.
19. Holmberg J, Clarke DL, Frisen J (2000) Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408: 203-206.
20. Huai J, Drescher U (2001) An ephrin-A-dependent signaling pathway controls integrin function and is linked to the tyrosine phosphorylation of a 120-kDa protein. J Biol Chem 276:6689-6694.
21. Huang C, Ni Y, Wang T, Gao Y, Haudenschild CC, Zhan X (1997) Down-regulation of the filamentous actin cross-linking activity of cortactin by Src-mediated tyrosine phosphorylation. J Biol Chem 272:13911-13915.
22. Huynh-Do U, Vindis C, Liu H, Cerretti DP, McGrew JT, Enriquez M, Chen J, Daniel TO (2002) Ephrin-B1 transduces signals to activate integrin-mediated migration, attachment and angiogenesis. J Cell Sci 115:3073-3081.
23. Janes PW, Saha N, Barton WA, Kolev MV, Wimmer-Kleikamp SH, Nievergall E, Blobel CP, Himanen JP, Lackmann M, Nikolov DB (2005) Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 123:291-304.
24. Klein R (2004) Eph/ephrin signaling in morphogenesis, neural development and plasticity. Curr Opin Cell Biol 16:580-589.
25. Knoll B, Drescher U (2002) Ephrin-As as receptors in topographic projections. Trends Neurosci 25:145-149.
26. Knoll B, Drescher U (2004) Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J Neurosci 24:6248-6257.
27. Kullander K, Klein R (2002) Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3:475-486.
28. 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.
29. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84:359-369.
30. Mann F, Peuckert C, Dehner F, Zhou R, Bolz J (2002) Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections. Development 129:3945-3955.
31. Marston DJ, Dickinson S, Nobes CD (2003) Rac-dependent transendocytosis of ephrinBs regulates Eph-ephrin contact repulsion. Nat Cell Biol 5:879-888.
32. Miao H, Burnett E, Kinch M, Simon E, Wang B (2000) Activation of EphA2 kinase suppresses integrin function and causes focal-adhesion-kinase dephosphorylation. Nat Cell Biol 2:62-69.
33. Nagashima K, Endo A, Ogita H, Kawana A, Yamagishi A, Kitabatake A, Matsuda M, Mochizuki N (2002) Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. Mol Biol Cell 13:4231-4242.
34. Niehage R, Peukert C, Bolz J, Weth F (2005) Developmental expression of Ephrin/Eph wiring molecules in mouse homologs of schizophrenia-related brain regions. Soc Neurosci Abstr 31:485.5.
35. Nomura T, Holmberg J, Frisen J, Osumi N (2006) Pax6-dependent boundary defines alignment of migrating olfactory cortex neurons via the repulsive activity of ephrin A5. Development 133:1335-1345.
36. Noren NK, Pasquale EB (2004) Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell Signal 16:655-666.
37. Palmer A, Zimmer M, Erdmann KS, Eulenburg V, Porthin A, Heumann R, Deutsch U, Klein R (2002) EphrinB phosphorylation and reverse signaling: regulation by Src kinases and PTP-BL phosphatase. Mol Cell 9:725-737.
38. Pasquale EB (2005) Eph receptor signalling casts a wide net on cell behaviour. Nat Rev Mol Cell Biol 6:462-475.
39. Prevost N, Woulfe D, Tanaka T, Brass LF (2002) Interactions between Eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-to-cell contact has occurred. Proc Natl Acad Sci USA 99:9219-9224.
40. Regen CM, Horwitz AF (1992) Dynamics of beta 1 integrin-mediated adhesive contacts in motile fibroblasts. J Cell Biol 119:1347-1359.
41. Santiago A, Erickson CA (2002) Ephrin-B ligands play a dual role in the control of neural crest cell migration. Development 129:3621-3632.
42. Schmidt CE, Horwitz AF, Lauffenburger DA, Sheetz MP (1993) Integrin-cytoskeletal interactions in migrating fibroblasts are dynamic, asymmetric, and regulated. J Cell Biol 123:977-991.
43. Schmidt CE, Dai J, Lauffenburger DA, Sheetz MP, Horwitz AF (1995) Integrin-cytoskeletal interactions in neuronal growth cones. J Neurosci 15:3400-3407.
44. Schwartz MA, Schaller MD, Ginsberg MH (1995) Integrins: emerging paradigms of signal transduction. Annu Rev Cell Dev Biol 11:549-599.
45. Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609.
46. Vielmetter J, Stolze B, Bonhoeffer F, Stuermer CA (1990) In vitro assay to test differential substrate affinities of growing axons and migratory cells. Exp Brain Res 81:283-287.
47. Vindis C, Cerretti DP, Daniel TO, Huynh-Do U (2003) EphB1 recruits c-Src and p52Shc to activate MAPK/ERK and promote chemotaxis. J Cell Biol 162:661-671.
48. 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.
49. Weed SA, Parsons JT (2001) Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene 20:6418-6434.
50. Weth F, Nadler W, Korsching S (1996) Nested expression domains for odorant receptors in zebrafish olfactory epithelium. Proc Natl Acad Sci USA 93:13321-13326.
51. Wilkinson DG (2001) Multiple roles of EPH receptors and ephrins in neural development. Nat Rev Neurosci 2:155-164.
52. Zimmer M, Palmer A, Kohler J, Klein R (2003) EphB-ephrinB bidirectional endocytosis terminates adhesion allowing contact mediated repulsion. Nat Cell Biol 5:869-878.
53. 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.
54. Zou JX, Liu Y, Pasquale EB, Ruoslahti E (2002) Activated SRC oncogene phosphorylates R-ras and suppresses integrin activity. J Biol Chem 277: 1824-1827.