UNC-40/DCC, SAX-3/Robo, and VAB-1/Eph Polarize F-Actin during Embryonic Morphogenesis by Regulating the WAVE/SCAR Actin Nucleation Complex

PLoS Genetics

Volumn 8, Issue 8, 2012, Pages

  Bernadskaya, Yelena Y ^a   Wallace, Andre ^a   Nguyen, Jillian ^a   Mohler, William A ^b   Soto, Martha C ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EPHRIN RECEPTOR; F ACTIN; NETRIN; PROTEIN VAB 1; RAC1 PROTEIN; RECEPTOR PROTEIN; ROUNDABOUT RECEPTOR; SLIT PROTEIN; UNC 40 PROTEIN; UNCLASSIFIED DRUG; WAVE SCAR COMPLEX;

ACTIN FILAMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL MIGRATION; CELL POLARITY; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENETIC ANALYSIS; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL CYCLE PROTEINS; CELL MEMBRANE; CELL MOVEMENT; CELL POLARITY; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; NERVE TISSUE PROTEINS; NEURONS; RAC GTP-BINDING PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; VIDEO RECORDING;

CAENORHABDITIS ELEGANS;

EID: 84866233662     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002863     Document Type: Article

References (52)

1. Hedgecock EM, Culotti JG, Hall DH, (1990) The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis of C. elegans. Neuron 4: 61-85.
2. Wadsworth WG, Bhatt H, Hedgecock EM, (1996) Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16: 35-46.
3. Zallen JA, Yi BA, Bargmann CI, (1998) The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell 92: 217-27.
4. Zallen JA, Kirch SA, Bargmann CI, (1999) Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 126: 3679-92.
5. Boulin T, Pocock R, Hobert O, (2006) A novel Eph receptor-interacting IgSF protein provides C. elegans motorneurons with midline guidepost function. Curr Biol 16: 1871-83.
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: 164-76.
7. Chin-Sang ID, George SE, Ding M, Moseley SL, Lynch AS, Chisholm AD, (1999) The ephrin VAB-2/EFN-1 functions in neuronal signaling to regulate epidermal morphogenesis in C. elegans. Cell 99: 781-90.
8. 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: 633-43.
9. Ghenea S, Boudreau JR, Lague NP, Chin-Sang ID, (2005) The VAB-1 Eph receptor tyrosine kinase and SAX-3/Robo neuronal receptors function together during C. elegans embryonic morphogenesis. Development 132: 3679-90.
10. Hao JC, Yu TW, Fujisawa K, Culotti JG, Gengyo-Ando K, et al.(2001) C. elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 32: 25-38.
11. Chan SS, Zheng H, Su MW, Wilk R, Killeen MT, et al.(1996) UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87: 187-95.
12. Patel FP, Bernadskaya YY, Chen E, Jobanputra A, Pooladi A, et al.(2008) The Rac-WAVE/SCAR-Arp2/3 pathway regulates C. elegans morphogenesis by maintaining cytoskeletal and epithelial polarity. Developmental Biology 324: 297-309.
13. Soto MC, Qadota H, Kasuya K, Inoue M, Tsuboi D, et al.(2002) The GEX-2 and GEX-3 proteins are required for tissue morphogenesis and cell migrations in C. elegans. Genes Dev 16: 620-32.
14. 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 C. elegans axon guidance. Genetics 179: 1957-71.
15. Bashaw GJ, Klein R, (2010) Signaling from axon guidance receptors. Cold Spring Harb Perspect Biol 2: a001941.
16. 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.
17. Li X, Saint-Cyr-Proulx E, Aktories K, Lamarche-Vane N, (2002) Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (deleted in colorectal cancer) in N1E-115 neuroblastoma cells. J Biol Chem 277: 15207-15214.
18. Shekarabi M, Kennedy TE, (2002) The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol Cell Neurosci 19: 1-17.
19. Shekarabi M, Moore SW, Tritsch NX, Morris SJ, Bouchard JF, et al.(2005) Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion. J Neurosci 25: 3132-3141.
20. Sahin M, Greer PL, Lin MZ, Poucher H, Eberhart J, et al.(2005) Eph-dependent tyrosine phosphorylation of ephexin1 modulates growth cone collapse. Neuron 46: 191-204.
21. Egea J, Nissen UV, Dufour A, Sahin M, Greer P, et al.(2005) Regulation of EphA 4 kinase activity is required for a subset of axon guidance decisions suggesting a key role for receptor clustering in Eph function. Neuron 47: 515-528.
22. 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.
23. Hakeda-Suzuki S, Ng J, Tzu J, Dietzl G, Sun Y, et al.(2002) Rac function and regulation during Drosophila development. Nature 416: 438-442.
24. Lundstrom A, Gallio M, Englund C, Steneberg P, Hemphala J, et al.(2004) Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev 18: 2161-2171.
25. Totong R, Achilleos A, Nance J, (2007) PAR-6 is required for junction formation but not apicobasal polarization in C. elegans embryonic epithelial cells. Development 134: 1259-68.
26. Chin-Sang ID, Chisholm AD, (2000) Form of the worm: genetics of epidermal morphogenesis in C. elegans. Trends Genet 16: 544-51.
27. Gally C, Wissler F, Zahreddine H, Quintin S, Landmann F, et al.(2009) Myosin II regulation during C. elegans embryonic elongation: LET-502/ROCK, MRCK-1 and PAK-1, three kinases with different roles. Development 136: 3109-19.
28. Williams-Masson EM, Malik AN, Hardin J, (1997) An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 124: 2889-2901.
29. Padrick SB, Rosen MK, (2010) Physical mechanisms of signal integration by WASP family proteins. Annu Rev Biochem 79: 707-35.
30. Kobayashi K, Kuroda S, Fukata M, Nakamura T, Nagase T, et al.(1998) p140Sra-1 (specifically Rac1-associated protein) is a novel specific target for Rac1 small GTPase. J Biol Chem 2;273: 291-5.
31. Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z, et al.(2010) Structure and control of the actin regulatory WAVE complex. Nature 468: 533-8.
32. Reddien PW, Horvitz HR, (2000) CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat Cell Biol 2: 131-6.
33. Moorthy S, Chen L, Bennett V, (2000) Caenorhabditis elegans beta-G spectrin is dispensable for establishment of epithelial polarity, but essential for muscular and neuronal function. J Cell Biol 149: 915-30.
34. Bernadskaya YY, Patel FB, Hsu HT, Soto MC, (2011) Arp2/3 promotes junction formation and maintenance in the C. elegans intestine by regulating membrane association of apical proteins. Molecular Biology of the Cell 22: 2886-99.
35. Lundquist EA, Reddien PW, Hartwieg E, Horvitz HR, Bargmann CI, (2001) Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 128: 4475-88.
36. Boulter E, Garcia-Mata R, Guilluy C, Dubash A, Rossi G, Brennwald PJ, Burridge K, (2010) Regulation of Rho GTPase crosstalk, degradation and activity by RhoGDI1. Nat Cell Biol 12: 477-83.
37. Garcia-Mata R, Boulter E, Burridge K, (2011) The 'invisible hand': regulation of RHO GTPases by RHOGDIs. Nat Rev Mol Cell Biol 12: 493-504.
38. Anderson P, (1995) Mutagenesis. Methods Cell Biol 48: 31-58.
39. 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: 1147-54.
40. Mohamed AM, Bourdreau JR, Yu FP, Chin-Sang ID, (2012) The Caenorhabditis elegans Eph receptor activates NCK and N-WASP, and inhibits Ena/VASP to regulate growth cone dynamics during axon guidance. PLoS Genet 2: e1002513 doi:10.1371/journal.pgen.1002513.
41. Clark SG, Chiu C, (2003) C. elegans ZAG-1, a Zn-finger-homeodomain protein, regulates axonal development and neuronal differentiation. Development 130: 3781-3794.
42. Ydenberg CA, Smith BA, Breitsprecher D, Gelles J, Goode BL, (2011) Cease-fire at the leading edge: new perspectives on actin filament branching, debranching, and cross-linking. Cytoskeleton 68: 596-602.
43. Breitsprecher D, Koestler SA, Chizhov I, Nemethova M, Mueller J, Goode BL, Small JV, Rottner K, Faix J, (2011) Cofilin cooperates with fascin to disassemble filopodial actin filaments. J Cell Sci 124: 3305-18.
44. Parsons JT, Horwitz AR, Schwartz MA, (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11: 633-43.
45. Palamidessi A, Frittoli E, Garré M, Faretta M, Mione M, et al.(2008) Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134: 135-47.
46. Brisbin S, Liu J, Bourdeau J, Peng J, Evangelista M, Chin-Sang I, (2009) A role for C. elegans Eph RTK signaling in PTEN regulation. Dev Cell 17: 459-69.
47. Suzuki Y, Han M, (2006) Genetic redundancy masks diverse functions of the tumor suppressor gene PTEN during C. elegans development. Genes Dev 20: 423-8.
48. Ikegami R, Simokat K, Zheng H, Brown L, Garriga G, et al.(2012) Semaphorin and Eph receptor signaling guide a series of cell movements for ventral enclosure in C. elegans. Curr Biol 22: 1-11.
49. Noegel AA, Blau-Wasser R, Sultana H, Müller R, Israel L, et al.(2004) The cyclase-associated protein CAP as regulator of cell polarity and cAMP signaling in Dictyostelium. Mol Biol Cell 15: 934-45.
50. Ellis RE, Jacobson DM, Horvitz HR, (1991) Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129: 79-94.
51. Francis R, Waterston RH, (1991) Muscle cell attachment in Caenorhabditis elegans. J Cell Biol 114: 465-479.
52. Koppen M, Simske JS, Sims PA, Firestein BL, Hall DH, et al.(2001) Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol 3: 983-991.