The caenorhabditis elegans eph receptor activates NCK and N-WASP, and inhibits Ena/VASP to regulate growth cone dynamics during axon guidance

PLoS Genetics

Volumn 8, Issue 2, 2012, Pages

  Mohamed, Ahmed M ^a   Boudreau, Jeffrey R ^a   Yu, Fabian P S ^a   Liu, Jun ^a   Chin Sang, Ian D ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; CAENORHABDITIS ELEGANS PROTEIN; EPHRIN; EPHRIN RECEPTOR; NCK PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN ENA; PROTEIN NCK 1; PROTEIN UNC 34; PROTEIN VAB 1; PROTEIN WSP 1; UNCLASSIFIED DRUG; VASODILATOR STIMULATED PHOSPHOPROTEIN;

ARTICLE; CAENORHABDITIS ELEGANS; COMPLEX FORMATION; FILOPODIUM; GROWTH CONE; GROWTH REGULATION; IN VITRO STUDY; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; REGULATORY MECHANISM;

ACTINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL CYCLE PROTEINS; CYTOSKELETON; GROWTH CONES; MICROFILAMENT PROTEINS; NEURONS; ONCOGENE PROTEINS; PHOSPHOPROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS; ENA;

EID: 84859199020     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002513     Document Type: Article

References (62)

1. Chilton JK, (2006) Molecular mechanisms of axon guidance. Dev Biol 292: 13-24.
2. Pasquale EB, (2005) Eph Receptor Signalling Casts a Wide Net on Cell Behaviour. Nat Rev Mol Cell Biol 6: 462-475.
3. Egea J, Klein R, (2007) Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol 17: 230-238.
4. George SE, Simokat K, Hardin J, Chisholm AD, (1998) The VAB-1 Eph receptor tyrosine kinase functions in neural and epithelial morphogenesis in C. elegans. Cell 92: 633-643.
5. Zallen JA, Kirch SA, Bargmann CI, (1999) Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 126: 3679-3692.
6. Mohamed AM, Chin-Sang ID, (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. Boulin T, Pocock R, Hobert O, (2006) A novel Eph receptor-interacting IgSF protein provides C. elegans motoneurons with midline guidepost function. Curr Biol 16: 1871-1883.
8. Buday L, Wunderlich L, Tamas P, (2002) The Nck family of adapter proteins: regulators of actin cytoskeleton. Cell Signal 14: 723-731.
9. Li X, Meriane M, Triki I, Shekarabi M, Kennedy TE, et al. (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. Fan X, Labrador JP, Hing H, Bashaw GJ, (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. Holland SJ, Gale NW, Gish GD, Roth RA, Songyang Z, et al. (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. Mohamed AM, Chin-Sang ID, (2011) The C. elegans nck-1 gene encodes two isoforms and is required for neuronal guidance. Dev Biol 354: 55-66.
13. Takenawa T, Suetsugu S, (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8: 37-48.
14. Withee J, Galligan B, Hawkins N, Garriga G, (2004) Caenorhabditis elegans WASP and Ena/VASP proteins play compensatory roles in morphogenesis and neuronal cell migration. Genetics 167: 1165-1176.
15. Shakir MA, Jiang K, Struckhoff EC, Demarco RS, Patel FB, et al. (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. Drees F, Gertler FB, (2008) Ena/VASP: proteins at the tip of the nervous system. Curr Opin Neurobiol 18: 53-59.
17. McIntire SL, Garriga G, White J, Jacobson D, Horvitz HR, (1992) Genes Necessary for Directed Axonal Elongation or Fasciculation in C. Elegans. Neuron 8: 307-322.
18. Desai C, Garriga G, McIntire SL, Horvitz HR, (1988) A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336: 638-646.
19. Chang C, Adler CE, Krause M, Clark SG, Gertler FB, et al. (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. Norris AD, Dyer JO, Lundquist EA, (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. Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS, (2000) Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101: 703-715.
22. Yu TW, Hao JC, Lim W, Tessier_Lavigne M, Bargmann CI, (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. Gitai Z, Yu TW, Lundquist EA, Tessier-Lavigne M, Bargmann CI, (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. Evans IR, Renne T, Gertler FB, Nobes CD, (2007) Ena/VASP proteins mediate repulsion from ephrin ligands. J Cell Sci 120: 289-298.
25. Colavita A, Culotti JG, (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. Mullins RD, Heuser JA, Pollard TD, (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. Blanchoin L, Amann KJ, Higgs HN, Marchand JB, Kaiser DA, et al. (2000) Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 404: 1007-1011.
28. Gallegos ME, Bargmann CI, (2004) Mechanosensory neurite termination and tiling depend on SAX-2 and the SAX-1 kinase. Neuron 44: 239-249.
29. Chereau D, Dominguez R, (2006) Understanding the role of the G-actin-binding domain of Ena/VASP in actin assembly. J Struct Biol 155: 195-201.
30. Rivero-Lezcano OM, Marcilla A, Sameshima JH, Robbins KC, (1995) Wiskott-Aldrich syndrome protein physically associates with Nck through Src homology 3 domains. Mol Cell Biol 15: 5725-5731.
31. Rohatgi R, Nollau P, Ho HY, Kirschner MW, Mayer BJ, (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. Sawa M, Suetsugu S, Sugimoto A, Miki H, Yamamoto M, et al. (2003) Essential role of the C. elegans Arp2/3 complex in cell migration during ventral enclosure. J Cell Sci 116: 1505-1518.
33. Yamaguchi H, Miki H, Takenawa T, (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. Strasser GA, Rahim NA, VanderWaal KE, Gertler FB, Lanier LM, (2004) Arp2/3 is a negative regulator of growth cone translocation. Neuron 43: 81-94.
35. Ideses Y, Brill-Karniely Y, Haviv L, Ben-Shaul A, Bernheim-Groswasser A, (2008) Arp2/3 branched actin network mediates filopodia-like bundles formation in vitro. PLoS One 3: e3297.
36. Sheffield M, Loveless T, Hardin J, Pettitt J, (2007) C. elegans Enabled exhibits novel interactions with N-WASP, Abl, and cell-cell junctions. Curr Biol 17: 1791-1796.
37. Frese S, Schubert WD, Findeis AC, Marquardt T, Roske YS, et al. (2006) The phosphotyrosine peptide binding specificity of Nck1 and Nck2 Src homology 2 domains. J Biol Chem 281: 18236-18245.
38. Hu T, Shi G, Larose L, Rivera GM, Mayer BJ, et al. (2009) Regulation of process retraction and cell migration by EphA3 is mediated by the adaptor protein Nck1. Biochemistry 48: 6369-6378.
39. Miura K, Nam JM, Kojima C, Mochizuki N, Sabe H, (2009) EphA2 engages Git1 to suppress Arf6 activity modulating epithelial cell-cell contacts. Mol Biol Cell 20: 1949-1959.
40. Bisson N, Poitras L, Mikryukov A, Tremblay M, Moss T, (2007) EphA4 signaling regulates blastomere adhesion in the Xenopus embryo by recruiting Pak1 to suppress Cdc42 function. Mol Biol Cell 18: 1030-1043.
41. Fawcett JP, Georgiou J, Ruston J, Bladt F, Sherman A, et al. (2007) Nck adaptor proteins control the organization of neuronal circuits important for walking. Proc Natl Acad Sci U S A 104: 20973-20978.
42. Becker E, Huynh-Do U, Holland S, Pawson T, Daniel TO, et al. (2000) Nck-interacting Ste20 kinase couples Eph receptors to c-Jun N-terminal kinase and integrin activation. Mol Cell Biol 20: 1537-1545.
43. Hock B, Bohme B, Karn T, Feller S, Rubsamen-Waigmann H, et al. (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. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB, (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 19: 541-564.
45. Huttelmaier S, Harbeck B, Steffens O, Messerschmidt T, Illenberger S, et al. (1999) Characterization of the actin binding properties of the vasodilator-stimulated phosphoprotein VASP. FEBS Lett 451: 68-74.
46. Lebrand C, Dent EW, Strasser GA, Lanier LM, Krause M, et al. (2004) Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42: 37-49.
47. Bear JE, Loureiro JJ, Libova I, Fassler R, Wehland J, et al. (2000) Negative regulation of fibroblast motility by Ena/VASP proteins. Cell 101: 717-728.
48. Kakimoto T, Katoh H, Negishi M, (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. Pinyol R, Haeckel A, Ritter A, Qualmann B, Kessels MM, (2007) Regulation of N-WASP and the Arp2/3 complex by Abp1 controls neuronal morphology. PLoS One 2: e400.
50. Korobova F, Svitkina T, (2008) Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol Biol Cell 19: 1561-1574.
51. Krause M, Bear JE, Loureiro JJ, Gertler FB, (2002) The Ena/VASP enigma. Journal of cell science 115: 4721-4726.
52. Irie F, Yamaguchi Y, (2002) EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5: 1117-1118.
53. Rose S, Malabarba MG, Krag C, Schultz A, Tsushima H, et al. (2007) Caenorhabditis elegans intersectin: a synaptic protein regulating neurotransmission. Molecular biology of the cell 18: 5091-5099.
54. Brenner S, (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
55. Brisbin S, Liu J, Boudreau J, Peng J, Evangelista M, et al. (2009) A role for C. elegans Eph RTK signaling in PTEN regulation. Dev Cell 17: 459-469.
56. Hobert O, (2002) PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32: 728-730.
57. Mello CC, Kramer JM, Stinchcomb D, Ambros V, (1991) Efficient Gene Transfer in C. elegans: Extrachromosomal Maintenance and Integration of Transforming Sequences. EMBO J 10: 3959-3970.
58. Chin-Sang ID, George SE, Ding M, Moseley SL, Lynch AS, et al. (1999) The ephrin VAB-2/EFN-1 functions in neuronal signaling to regulate epidermal morphogenesis in C. elegans. Cell 99: 781-790.
59. White JG, Southgate E, Thomson JN, Brenner S, (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. Sherman F, (1991) Getting Started with Yeast. Methods in Enzymology 194: 3-21.
61. Schiestl RH, Gietz RD, (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Current Genetics 16: 339-346.
62. Serebriiskii IG, Golemis EA, (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.