E3 Ligase Nedd4 Promotes Axon Branching by Downregulating PTEN

Neuron

Volumn 65, Issue 3, 2010, Pages 341-357

  Drinjakovic, Jovana ^a   Jung, Hosung ^a   Campbell, Douglas S ^a   Strochlic, Laure ^a   Dwivedy, Asha ^a   Holt, Christine E ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

DEVBIO; MOLNEURO; SIGNALING

Indexed keywords

MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; GROWTH REGULATION; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RETINA GANGLION CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ARGININE; AXONS; CELL LINE, TRANSFORMED; DOWN-REGULATION; ELECTROPORATION; EMBRYO, NONMAMMALIAN; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; GROWTH CONES; HUMANS; IMMUNOPRECIPITATION; LYSINE; MICROSCOPY, CONFOCAL; MUTATION; PTEN PHOSPHOHYDROLASE; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; SUPERIOR COLLICULI; TISSUE CULTURE TECHNIQUES; TRANSDUCTION, GENETIC; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; XENOPUS;

EID: 75949103435     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.01.017     Document Type: Article

References (78)

1. Ahn Y., Hwang C.Y., Lee S.R., Kwon K.S., and Lee C. The tumor suppressor PTEN mediates a negative regulation of E3 ubiquitin-protein ligase Nedd4. Biochem. J. 412 (2008) 331-338
2. Alsina B., Vu T., and Cohen-Cory S. Visualizing synapse formation in arborizing optic axons in vivo: dynamics and modulation by BDNF. Nat. Neurosci. 4 (2001) 1093-1101
3. Arévalo J.C., Waite J., Rajagopal R., Beyna M., Chen Z.Y., Lee F.S., and Chao M.V. Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 50 (2006) 549-559
4. Bloom A.J., Miller B.R., Sanes J.R., and DiAntonio A. The requirement for Phr1 in CNS axon tract formation reveals the corticostriatal boundary as a choice point for cortical axons. Genes Dev. 21 (2007) 2593-2606
5. Brose K., and Tessier-Lavigne M. Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr. Opin. Neurobiol. 10 (2000) 95-102
6. Campbell D.S., and Holt C.E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32 (2001) 1013-1026
7. Campbell D.S., and Holt C.E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37 (2003) 939-952
8. Campbell D.S., Regan A.G., Lopez J.S., Tannahill D., Harris W.A., and Holt C.E. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21 (2001) 8538-8547
9. Campbell D.S., Stringham S.A., Timm A., Xiao T., Law M.Y., Baier H., Nonet M.L., and Chien C.B. Slit1a inhibits retinal ganglion cell arborization and synaptogenesis via Robo2-dependent and -independent pathways. Neuron 55 (2007) 231-245
10. Cohen-Cory S., and Fraser S.E. BDNF in the development of the visual system of Xenopus. Neuron 12 (1994) 747-761
11. Cohen-Cory S., and Fraser S.E. Effects of brain-derived neurotrophic factor on optic axon branching and remodelling in vivo. Nature 378 (1995) 192-196
12. Colón-Ramos D.A., Margeta M.A., and Shen K. Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318 (2007) 103-106
13. Cosker K.E., and Eickholt B.J. Phosphoinositide 3-kinase signalling events controlling axonal morphogenesis. Biochem. Soc. Trans. 35 (2007) 207-210
14. Crowder R.J., and Freeman R.S. Glycogen synthase kinase-3 beta activity is critical for neuronal death caused by inhibiting phosphatidylinositol 3-kinase or Akt but not for death caused by nerve growth factor withdrawal. J. Biol. Chem. 275 (2000) 34266-34271
15. Das T., Payer B., Cayouette M., and Harris W.A. In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron 37 (2003) 597-609
16. de la Torre J.R., Höpker V.H., Ming G.L., Poo M.M., Tessier-Lavigne M., Hemmati-Brivanlou A., and Holt C.E. Turning of retinal growth cones in a netrin-1 gradient mediated by the netrin receptor DCC. Neuron 19 (1997) 1211-1224
17. Dent E.W., Barnes A.M., Tang F., and Kalil K. Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J. Neurosci. 24 (2004) 3002-3012
18. DiAntonio A., Haghighi A.P., Portman S.L., Lee J.D., Amaranto A.M., and Goodman C.S. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412 (2001) 449-452
19. Dingwell K.S., Holt C.E., and Harris W.A. The multiple decisions made by growth cones of RGCs as they navigate from the retina to the tectum in Xenopus embryos. J. Neurobiol. 44 (2000) 246-259
20. Dunn R., and Hicke L. Multiple roles for Rsp5p-dependent ubiquitination at the internalization step of endocytosis. J. Biol. Chem. 276 (2001) 25974-25981
21. Falk J., Drinjakovic J., Leung K.M., Dwivedy A., Regan A.G., Piper M., and Holt C.E. Electroporation of cDNA/Morpholinos to targeted areas of embryonic CNS in Xenopus. BMC Dev. Biol. 7 (2007) 107
22. Finley D., Sadis S., Monia B.P., Boucher P., Ecker D.J., Crooke S.T., and Chau V. Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. Mol. Cell. Biol. 14 (1994) 5501-5509
23. Fotia A.B., Cook D.I., and Kumar S. The ubiquitin-protein ligases Nedd4 and Nedd4-2 show similar ubiquitin-conjugating enzyme specificities. Int. J. Biochem. Cell Biol. 38 (2006) 472-479
24. Fouladkou F., Landry T., Kawabe H., Neeb A., Lu C., Brose N., Stambolic V., and Rotin D. The ubiquitin ligase Nedd4-1 is dispensable for the regulation of PTEN stability and localization. Proc. Natl. Acad. Sci. USA 105 (2008) 8585-8590
25. Gitai Z., Yu T.W., Lundquist E.A., Tessier-Lavigne M., and 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 (2003) 53-65
26. Glickman M.H., and Adir N. The proteasome and the delicate balance between destruction and rescue. PLoS Biol. 2 (2004) E13
27. Guan K.L., and Rao Y. Signalling mechanisms mediating neuronal responses to guidance cues. Nat. Rev. Neurosci. 4 (2003) 941-956
28. Guertin D.A., and Sabatini D.M. Defining the role of mTOR in cancer. Cancer Cell 12 (2007) 9-22
29. Harvey K.F., Harvey N.L., Michael J.M., Parasivam G., Waterhouse N., Alnemri E.S., Watters D., and Kumar S. Caspase-mediated cleavage of the ubiquitin-protein ligase Nedd4 during apoptosis. J. Biol. Chem. 273 (1998) 13524-13530
30. Hay N. The Akt-mTOR tango and its relevance to cancer. Cancer Cell 8 (2005) 179-183
31. Holt C.E., Garlick N., and Cornel E. Lipofection of cDNAs in the embryonic vertebrate central nervous system. Neuron 4 (1990) 203-214
32. Ing B., Shteiman-Kotler A., Castelli M., Henry P., Pak Y., Stewart B., Boulianne G.L., and Rotin D. Regulation of Commissureless by the ubiquitin ligase DNedd4 is required for neuromuscular synaptogenesis in Drosophila melanogaster. Mol. Cell. Biol. 27 (2007) 481-496
33. Jaworski J., Spangler S., Seeburg D.P., Hoogenraad C.C., and Sheng M. Control of dendritic arborization by the phosphoinositide-3′-kinase-Akt-mammalian target of rapamycin pathway. J. Neurosci. 25 (2005) 11300-11312
34. Kim D., and Dressler G.R. PTEN modulates GDNF/RET mediated chemotaxis and branching morphogenesis in the developing kidney. Dev. Biol. 307 (2007) 290-299
35. Konishi Y., Stegmüller J., Matsuda T., Bonni S., and Bonni A. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science 303 (2004) 1026-1030
36. Kumar S., Tomooka Y., and Noda M. Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem. Biophys. Res. Commun. 185 (1992) 1155-1161
37. Kumar S., Harvey K.F., Kinoshita M., Copeland N.G., Noda M., and Jenkins N.A. cDNA cloning, expression analysis, and mapping of the mouse Nedd4 gene. Genomics 40 (1997) 435-443
38. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., Li Y., Baker S.J., and Parada L.F. Pten regulates neuronal arborization and social interaction in mice. Neuron 50 (2006) 377-388
39. Lee J.R., Oestreich A.J., Payne J.A., Gunawan M.S., Norgan A.P., and Katzmann D.J. The HECT domain of the ubiquitin ligase Rsp5 contributes to substrate recognition. J. Biol. Chem. 284 (2009) 32126-32137
40. Leung K.M., van Horck F.P., Lin A.C., Allison R., Standart N., and Holt C.E. Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9 (2006) 1247-1256
41. Lewcock J.W., Genoud N., Lettieri K., and Pfaff S.L. The ubiquitin ligase Phr1 regulates axon outgrowth through modulation of microtubule dynamics. Neuron 56 (2007) 604-620
42. Liu Y., Oppenheim R.W., Sugiura Y., and Lin W. Abnormal development of the neuromuscular junction in Nedd4-deficient mice. Dev. Biol. 330 (2009) 153-166
43. Maehama T., and Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273 (1998) 13375-13378
44. Manitt C., Nikolakopoulou A.M., Almario D.R., Nguyen S.A., and Cohen-Cory S. Netrin participates in the development of retinotectal synaptic connectivity by modulating axon arborization and synapse formation in the developing brain. J. Neurosci. 29 (2009) 11065-11077
45. Marler K.J., Becker-Barroso E., Martínez A., Llovera M., Wentzel C., Poopalasundaram S., Hindges R., Soriano E., Comella J., and Drescher U. A TrkB/EphrinA interaction controls retinal axon branching and synaptogenesis. J. Neurosci. 28 (2008) 12700-12712
46. Marshak S., Nikolakopoulou A.M., Dirks R., Martens G.J., and Cohen-Cory S. Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J. Neurosci. 27 (2007) 2444-2456
47. Meyer M.P., and Smith S.J. Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J. Neurosci. 26 (2006) 3604-3614
48. Moody S.A. Cell lineage analysis in Xenopus embryos. Methods Mol. Biol. 135 (2000) 331-347
49. Myat A., Henry P., McCabe V., Flintoft L., Rotin D., and Tear G. Drosophila Nedd4, a ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the roundabout receptor. Neuron 35 (2002) 447-459
50. Narimatsu M., Bose R., Pye M., Zhang L., Miller B., Ching P., Sakuma R., Luga V., Roncari L., Attisano L., and Wrana J.L. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137 (2009) 295-307
51. Nieuwkoop P.D., and Faber J. Normal Table of Xenopus laevis (Daudin) (1967), North-Holland, Amsterdam
52. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., and He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 322 (2008) 963-966
53. Patrick G.N., Bingol B., Weld H.A., and Schuman E.M. Ubiquitin-mediated proteasome activity is required for agonist-induced endocytosis of GluRs. Curr. Biol. 13 (2003) 2073-2081
54. Piper M., Salih S., Weinl C., Holt C.E., and Harris W.A. Endocytosis-dependent desensitization and protein synthesis-dependent resensitization in retinal growth cone adaptation. Nat. Neurosci. 8 (2005) 179-186
55. Piper M., Anderson R., Dwivedy A., Weinl C., van Horck F., Leung K.M., Cogill E., and Holt C. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49 (2006) 215-228
56. Plant P.J., Yeger H., Staub O., Howard P., and Rotin D. The C2 domain of the ubiquitin protein ligase Nedd4 mediates Ca2+-dependent plasma membrane localization. J. Biol. Chem. 272 (1997) 32329-32336
57. Poggi L., Vitorino M., Masai I., and Harris W.A. Influences on neural lineage and mode of division in the zebrafish retina in vivo. J. Cell Biol. 171 (2005) 991-999
58. Roskies A.L., and O'Leary D.D. Control of topographic retinal axon branching by inhibitory membrane-bound molecules. Science 265 (1994) 799-803
59. Ruthazer E.S., Li J., and Cline H.T. Stabilization of axon branch dynamics by synaptic maturation. J. Neurosci. 26 (2006) 3594-3603
60. Schaefer A.M., Hadwiger G.D., and Nonet M.L. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26 (2000) 345-356
61. Schmitz C., Kinge P., and Hutter H. Axon guidance genes identified in a large-scale RNAi screen using the RNAi-hypersensitive Caenorhabditis elegans strain nre-1(hd20) lin-15b(hd126). Proc. Natl. Acad. Sci. USA 104 (2007) 834-839
62. Shewan D., Dwivedy A., Anderson R., and Holt C.E. Age-related changes underlie switch in netrin-1 responsiveness as growth cones advance along visual pathway. Nat. Neurosci. 5 (2002) 955-962
63. Sieburth D., Ch'ng Q., Dybbs M., Tavazoie M., Kennedy S., Wang D., Dupuy D., Rual J.F., Hill D.E., Vidal M., et al. Systematic analysis of genes required for synapse structure and function. Nature 436 (2005) 510-517
64. Smear M.C., Tao H.W., Staub W., Orger M.B., Gosse N.J., Liu Y., Takahashi K., Poo M.M., and Baier H. Vesicular glutamate transport at a central synapse limits the acuity of visual perception in zebrafish. Neuron 53 (2007) 65-77
65. Thomas J.B., and Wyman R.J. Mutations altering synaptic connectivity between identified neurons in Drosophila. J. Neurosci. 4 (1984) 530-538
66. Ueno S., Kono R., and Iwao Y. PTEN is required for the normal progression of gastrulation by repressing cell proliferation after MBT in Xenopus embryos. Dev. Biol. 297 (2006) 274-283
67. van Roessel P., Elliott D.A., Robinson I.M., Prokop A., and Brand A.H. Independent regulation of synaptic size and activity by the anaphase-promoting complex. Cell 119 (2004) 707-718
68. Vignali R., Poggi L., Madeddu F., and Barsacchi G. HNF1(beta) is required for mesoderm induction in the Xenopus embryo. Development 127 (2000) 1455-1465
69. Walz A., McFarlane S., Brickman Y.G., Nurcombe V., Bartlett P.F., and Holt C.E. Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development 124 (1997) 2421-2430
70. Wan H.I., DiAntonio A., Fetter R.D., Bergstrom K., Strauss R., and Goodman C.S. Highwire regulates synaptic growth in Drosophila. Neuron 26 (2000) 313-329
71. Wang G.X., and Poo M.M. Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 434 (2005) 898-904
72. Wang K.H., Brose K., Arnott D., Kidd T., Goodman C.S., Henzel W., and Tessier-Lavigne M. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96 (1999) 771-784
73. Wang X., Trotman L.C., Koppie T., Alimonti A., Chen Z., Gao Z., Wang J., Erdjument-Bromage H., Tempst P., Cordon-Cardo C., et al. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 128 (2007) 129-139
74. Wang X., Shi Y., Wang J., Huang G., and Jiang X. Crucial role of the C-terminus of PTEN in antagonizing NEDD4-1-mediated PTEN ubiquitination and degradation. Biochem. J. 414 (2008) 221-229
75. Yao J., Sasaki Y., Wen Z., Bassell G.J., and Zheng J.Q. An essential role for beta-actin mRNA localization and translation in Ca2+-dependent growth cone guidance. Nat. Neurosci. 9 (2006) 1265-1273
76. Yi J.J., and Ehlers M.D. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol. Rev. 59 (2007) 14-39
77. Yim E.K., Peng G., Dai H., Hu R., Li K., Lu Y., Mills G.B., Meric-Bernstam F., Hennessy B.T., Craven R.J., and Lin S.Y. Rak functions as a tumor suppressor by regulating PTEN protein stability and function. Cancer Cell 15 (2009) 304-314
78. Zhen M., Huang X., Bamber B., and Jin Y. Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26 (2000) 331-343