UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation

Nature Neuroscience

Volumn 9, Issue 4, 2006, Pages 511-518

  Adler, Carolyn E ^a   Fetter, Richard D ^a   Bargmann, Cornelia I ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; NETRIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLECKSTRIN; PROTEIN; PROTEIN AGE 1; PROTEIN MIG 10; PROTEIN UNC 40; PROTEIN UNC 6; TRANSCRIPTION FACTOR DAF 18; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CELL MATURATION; CONTROLLED STUDY; EMBRYO; NERVE CELL; NERVE CELL GROWTH; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEQUENCE HOMOLOGY;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL POLARITY; LIPIDS; NERVE TISSUE PROTEINS; NEURONS; SIGNAL TRANSDUCTION;

EID: 33645362213     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1666     Document Type: Article

References (47)

1. Dotti, C.G., Sullivan, C.A. & Banker, G.A. The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468 (1988).
2. Inagaki, N. et al. CRMP-2 induces axons in cultured hippocampal neurons. Nat. Neurosci. 4, 781-782 (2001).
3. Shi, S.H., Cheng, T., Jan, L.Y. & Jan, Y.N. APC and GSK-3β are involved in mPar3 targeting to the nascent axon and establishment of neuronal polarity. Curr. Biol. 14, 2025-2032 (2004).
4. Kishi, M., Pan, Y.A., Crump, J.G. & Sanes, J.R. Mammalian SAD kinases are required for neuronal polarization. Science 307, 929-932 (2005).
5. Shi, S.H., Jan, L.Y. & Jan, Y.N. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112, 63-75 (2003).
6. Menager, C., Arimura, N., Fukata, Y. & Kaibuchi, K. PIP3 is involved in neuronal polarization and axon formation. J. Neurochem. 89, 109-118 (2004).
7. da Silva, J.S. & Dotti, C.G. Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3, 694-704 (2002).
8. Goldberg, J.L. et al. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33, 689-702 (2002).
9. Lefcort, F. & Bentley, D. Organization of cytoskeletal elements and organelles preceding growth cone emergence from an identified neuron in situ. J. Cell Biol. 108, 1737-1749 (1989).
10. Halfter, W., Deiss, S. & Schwarz, U. The formation of the axonal pattern in the embryonic avian retina. J. Comp. Neurol. 232, 466-480 (1985).
11. Weiner, O.D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196-202 (2002).
12. Van Haastert, P.J. & Devreotes, P.N. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5, 626-634 (2004).
13. Weiner, O.D. et al. A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat. Cell Biol. 4, 509-513 (2002).
14. Hedgecock, E.M., Culotti, J.G. & Hall, D.H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61-85 (1990).
15. Wadsworth, W.G., Bhatt, H. & Hedgecock, E.M. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35-46 (1996).
16. Serafini, T. et al. The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424 (1994).
17. Hong, K. et al. A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97, 927-941 (1999).
18. Chan, S.S. et al. 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, 187-195 (1996).
19. Keino-Masu, K. et al. Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185 (1996).
20. Hamelin, M., Zhou, Y., Su, M.W., Scott, I.M. & Culotti, J.G. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330 (1993).
21. Desai, C., Garriga, G., McIntire, S.L. & Horvitz, H.R. A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638-646 (1988).
22. Garriga, G., Desai, C. & Horvitz, H.R. Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117, 1071-1087 (1993).
23. Knobel, K.M., Jorgensen, E.M. & Bastiani, M.J. Growth cones stall and collapse during axon outgrowth in Caenorhabditis elegans. Development 126, 4489-4498 (1999).
24. Krause, M., Dent, E.W., Bear, J.E., Loureiro, J.J. & Gertler, F.B. Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu. Rev. Cell Dev. Biol. 19, 541-564 (2003).
25. Gitai, Z., Yu, T.W., Lundquist, E.A., Tessier-Lavigne, M. & Bargmann, C.I. 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 (2003).
26. Lebrand, C. et al. Critical role of Ena/VASP proteins for filopodia formation in neurons and in function downstream of netrin-1. Neuron 42, 37-49 (2004).
27. Manser, J., Roonprapunt, C. & Margolis, B. C. elegans cell migration gene mig-10 shares similarities with a family of SH2 domain proteins and acts cell nonautonomously in excretory canal development. Dev. Biol. 184, 150-164 (1997).
28. Krause, M. et al. Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571-583 (2004).
29. Stringham, E.G., Dixon, D.K., Jones, D. & Candido, E.P. Temporal and spatial expression patterns of the small heat shock (hsp16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3, 221-233 (1992).
30. Gil, E.B., Malone Link, E., Liu, L.X., Johnson, C.D. & Lees, J.A. Regulation of the insulin-like developmental pathway of Caenorhabditis elegans by a homolog of the PTEN tumor suppressor gene. Proc. Natl. Acad. Sci. USA 96, 2925-2930 (1999).
31. Morris, J.Z., Tissenbaum, H.A. & Ruvkun, G. A phosphatidylinositol-3- OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382, 536-539 (1996).
32. Polleux, F., Giger, R.J., Ginty, D.D., Kolodkin, A.L. & Ghosh, A. Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282, 1904-1906 (1998).
33. Lieberam, I., Agalliu, D., Nagasawa, T., Ericson, J. & Jessell, T.M.A. Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47, 667-679 (2005).
34. Gad, J.M., Keeling, S.L., Shu, T., Richards, L.J. & Cooper, H.M. The spatial and temporal expression patterns of netrin receptors, DCC and neogenin, in the developing mouse retina. Exp. Eye Res. 70, 711-722 (2000).
35. Deiner, M.S. et al. Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19, 575-589 (1997).
36. Hiramoto, M., Hiromi, Y., Giniger, E. & Hotta, Y. The Drosophila Netrin receptor Frazzled guides axons by controlling Netrin distribution. Nature 406, 886-889 (2000).
37. Jiang, H., Guo, W., Liang, X. & Rao, Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120, 123-135 (2005).
38. Funamoto, S., Meili, R., Lee, S., Parry, L. & Firtel, R.A. Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell 109, 611-623 (2002).
39. Iijima, M. & Devreotes, P. Tumor suppressor PTEN mediates sensing of chemoattractant gradients. Cell 109, 599-610 (2002).
40. Ming, G. et al. Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23, 139-148 (1999).
41. Campbell, D.S. & Holt, C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026 (2001).
42. Xie, Y. et al. Phosphatidylinositol transfer protein-alpha in netrin-1-induced PLC signalling and neurite outgrowth. Nat. Cell Biol. 7, 1124-1132 (2005).
43. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
44. Mello, C. & Fire, A. DNA transformation. Methods Cell Biol. 48, 451-482 (1995).
45. Baumeister, R., Liu, Y. & Ruvkun, G. Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev. 10, 1395-1410 (1996).
46. Colavita, A., Krishna, S., Zheng, H., Padgett, R.W. & Culotti, J.G. Pioneer axon guidance by UNC-129, a C. elegans TGF-beta. Science 281, 706-709 (1998).
47. Sato, T. A modified method for lead staining of thin sections. J. Electron Microsc. (Tokyo) 17, 158-159 (1968).