The Eph Receptor Activates NCK and N-WASP, and Inhibits Ena/VASP to Regulate Growth Cone Dynamics during Axon Guidance

1. ChiltonJK 2006 Molecular mechanisms of axon guidance. Dev Biol 292 13 24

2. PasqualeEB 2005 Eph Receptor Signalling Casts a Wide Net on Cell Behaviour. Nat Rev Mol Cell Biol 6 462 475

3. EgeaJKleinR 2007 Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol 17 230 238

4. GeorgeSESimokatKHardinJChisholmAD 1998 The VAB-1 Eph receptor tyrosine kinase functions in neural and epithelial morphogenesis in C. elegans. Cell 92 633 643

5. ZallenJAKirchSABargmannCI 1999 Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 126 3679 3692

6. MohamedAMChin-SangID 2006 Characterization of loss-of-function and gain-of-function Eph receptor tyrosine kinase signaling in C. elegans axon targeting and cell migration. Dev Biol 290 164 176

7. BoulinTPocockRHobertO 2006 A novel Eph receptor-interacting IgSF protein provides C. elegans motoneurons with midline guidepost function. Curr Biol 16 1871 1883

8. BudayLWunderlichLTamasP 2002 The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal 14 723 731

9. LiXMerianeMTrikiIShekarabiMKennedyTE 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

10. FanXLabradorJPHingHBashawGJ 2003 Slit Stimulation Recruits Dock and Pak to the Roundabout Receptor and Increases Rac Activity to Regulate Axon Repulsion at the CNS Midline. Neuron 40 113 127

11. HollandSJGaleNWGishGDRothRASongyangZ 1997 Juxtamembrane tyrosine residues couple the Eph family receptor EphB2/Nuk to specific SH2 domain proteins in neuronal cells. Embo J 16 3877 3888

12. MohamedAMChin-SangID 2011 The C. elegans nck-1 gene encodes two isoforms and is required for neuronal guidance. Dev Biol 354 55 66

13. TakenawaTSuetsuguS 2007 The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8 37 48

14. WitheeJGalliganBHawkinsNGarrigaG 2004 Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 167 1165 1176

15. ShakirMAJiangKStruckhoffECDemarcoRSPatelFB 2008 The Arp2/3 activators WAVE and WASP have distinct genetic interactions with Rac GTPases in Caenorhabditis elegans axon guidance. Genetics 179 1957 1971

16. DreesFGertlerFB 2008 Ena/VASP: proteins at the tip of the nervous system. Curr Opin Neurobiol 18 53 59

17. McIntireSLGarrigaGWhiteJJacobsonDHorvitzHR 1992 Genes Necessary for Directed Axonal Elongation or Fasciculation in C. Elegans. Neuron 8 307 322

18. DesaiCGarrigaGMcIntireSLHorvitzHR 1988 A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336 638 646

19. ChangCAdlerCEKrauseMClarkSGGertlerFB 2006 MIG-10/lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to slit and netrin. Curr Biol 16 854 862

20. NorrisADDyerJOLundquistEA 2009 The Arp2/3 complex, UNC-115/abLIM, and UNC-34/Enabled regulate axon guidance and growth cone filopodia formation in Caenorhabditis elegans. Neural Dev 4 38

21. BashawGJKiddTMurrayDPawsonTGoodmanCS 2000 Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101 703 715

22. YuTWHaoJCLimWTessier_LavigneMBargmannCI 2002 Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/Enabled and a Netrin-independent UNC-40/DCC function. Nat Neurosci 5 1147 1154

23. GitaiZYuTWLundquistEATessier-LavigneMBargmannCI 2003 The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37 53 65

24. EvansIRRenneTGertlerFBNobesCD 2007 Ena/VASP proteins mediate repulsion from ephrin ligands. J Cell Sci 120 289 298

25. ColavitaACulottiJG 1998 Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev Biol 194 72 85

26. MullinsRDHeuserJAPollardTD 1998 The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci U S A 95 6181 6186

27. BlanchoinLAmannKJHiggsHNMarchandJBKaiserDA 2000 Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404 1007 1011

28. GallegosMEBargmannCI 2004 Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. Neuron 44 239 249

29. ChereauDDominguezR 2006 Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly. J Struct Biol 155 195 201

30. Rivero-LezcanoOMMarcillaASameshimaJHRobbinsKC 1995 Wiskott-Aldrich syndrome protein physically associates with Nck through Src homology 3 domains. Mol Cell Biol 15 5725 5731

31. RohatgiRNollauPHoHYKirschnerMWMayerBJ 2001 Nck and phosphatidylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J Biol Chem 276 26448 26452

32. SawaMSuetsuguSSugimotoAMikiHYamamotoM 2003 Essential role of the C. elegans Arp2/3 complex in cell migration during ventral enclosure. J Cell Sci 116 1505 1518

33. YamaguchiHMikiHTakenawaT 2002 Two verprolin homology domains increase the Arp2/3 complex-mediated actin polymerization activities of N-WASP and WAVE1 C-terminal regions. Biochem Biophys Res Commun 297 214 219

34. StrasserGARahimNAVanderWaalKEGertlerFBLanierLM 2004 Arp2/3 is a negative regulator of growth cone translocation. Neuron 43 81 94

35. IdesesYBrill-KarnielyYHavivLBen-ShaulABernheim-GroswasserA 2008 Arp2/3 branched actin network mediates filopodia-like bundles formation in vitro. PLoS One 3 e3297

36. SheffieldMLovelessTHardinJPettittJ 2007 C. elegans Enabled exhibits novel interactions with N-WASP, Abl, and cell-cell junctions. Curr Biol 17 1791 1796

37. FreseSSchubertWDFindeisACMarquardtTRoskeYS 2006 The phosphotyrosine peptide binding specificity of Nck1 and Nck2 Src homology 2 domains. J Biol Chem 281 18236 18245

38. HuTShiGLaroseLRiveraGMMayerBJ 2009 Regulation of process retraction and cell migration by EphA3 is mediated by the adaptor protein Nck1. Biochemistry 48 6369 6378

39. MiuraKNamJMKojimaCMochizukiNSabeH 2009 EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol Biol Cell 20 1949 1959

40. BissonNPoitrasLMikryukovATremblayMMossT 2007 EphA4 signaling regulates blastomere adhesion in the Xenopus embryo by recruiting Pak1 to suppress Cdc42 function. Mol Biol Cell 18 1030 1043

41. FawcettJPGeorgiouJRustonJBladtFShermanA 2007 Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc Natl Acad Sci U S A 104 20973 20978

42. BeckerEHuynh-DoUHollandSPawsonTDanielTO 2000 Nck-interacting Ste20 kinase couples Eph receptors to c-Jun N-terminal kinase and integrin activation. Mol Cell Biol 20 1537 1545

43. HockBBohmeBKarnTFellerSRubsamen-WaigmannH 1998 Tyrosine-614, the major autophosphorylation site of the receptor tyrosine kinase HEK2, functions as multi-docking site for SH2-domain mediated interactions. Oncogene 17 255 260

44. KrauseMDentEWBearJELoureiroJJGertlerFB 2003 Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19 541 564

45. HuttelmaierSHarbeckBSteffensOMesserschmidtTIllenbergerS 1999 Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett 451 68 74

46. LebrandCDentEWStrasserGALanierLMKrauseM 2004 Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42 37 49

47. BearJELoureiroJJLibovaIFasslerRWehlandJ 2000 Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101 717 728

48. KakimotoTKatohHNegishiM 2006 Regulation of neuronal morphology by Toca-1, an F-BAR/EFC protein that induces plasma membrane invagination. J Biol Chem 281 29042 29053

49. PinyolRHaeckelARitterAQualmannBKesselsMM 2007 Regulation of N-WASP and the Arp2/3 complex by Abp1 controls neuronal morphology. PLoS One 2 e400

50. KorobovaFSvitkinaT 2008 Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol Biol Cell 19 1561 1574

51. KrauseMBearJELoureiroJJGertlerFB 2002 The Ena/VASP enigma. Journal of cell science 115 4721 4726

52. IrieFYamaguchiY 2002 EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5 1117 1118

53. RoseSMalabarbaMGKragCSchultzATsushimaH 2007 Caenorhabditis elegans intersectin: a synaptic protein regulating neurotransmission. Molecular biology of the cell 18 5091 5099

54. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

55. BrisbinSLiuJBoudreauJPengJEvangelistaM 2009 A role for C. elegans Eph RTK signaling in PTEN regulation. Dev Cell 17 459 469

56. HobertO 2002 PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32 728 730

57. MelloCCKramerJMStinchcombDAmbrosV 1991 Efficient Gene Transfer in C. elegans: Extrachromosomal Maintenance and Integration of Transforming Sequences. EMBO J 10 3959 3970

58. Chin-SangIDGeorgeSEDingMMoseleySLLynchAS 1999 The ephrin VAB-2/EFN-1 functions in neuronal signaling to regulate epidermal morphogenesis in C. elegans. Cell 99 781 790

59. WhiteJGSouthgateEThomsonJNBrennerS 1986 The structure of the nervous system of the nematode C. elegans. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences 314 1 340

60. ShermanF 1991 Getting Started with Yeast. Methods in Enzymology 194 3 21

61. SchiestlRHGietzRD 1989 High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Current Genetics 16 339 346

62. SerebriiskiiIGGolemisEA 2000 Uses of lacZ to study gene function: evaluation of beta-galactosidase assays employed in the yeast two-hybrid system. Anal Biochem 285 1 15