Disruption of E3 ligase NEDD4 in peripheral neurons interrupts axon outgrowth: Linkage to PTEN

Molecular and Cellular Neuroscience

Volumn 50, Issue 2, 2012, Pages 179-192

  Christie, Kimberly J ^a   Martinez, Jose A ^a   Zochodne, Douglas W ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Axotomy; Dorsal root ganglion DRG ; Injury; Nedd4; Peripheral nerve; Phosphoinositide 3 kinase PI3 K ; PTEN

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE NEDD4;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MALE; NERVE CELL; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SCIATIC NERVE; SENSORY NERVE CELL; SPINAL GANGLION;

ACETYLCYSTEINE; ANIMALS; AXONS; CELLS, CULTURED; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GANGLIA, SPINAL; MALE; NERVE REGENERATION; PTEN PHOSPHOHYDROLASE; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; SCIATIC NERVE; UBIQUITIN-PROTEIN LIGASES;

RATTUS;

EID: 84861426515     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.04.006     Document Type: Article

References (39)

1. Arevalo J.C., Waite J., Rajagopal R., Beyna M., Chen Z.Y., Lee F.S., Chao M.V. Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Neuron 2006, 50:549-559.
2. Casafont I., Berciano M.T., Lafarga M. Bortezomib induces the formation of nuclear poly(A) RNA granules enriched in Sam68 and PABPN1 in sensory ganglia neurons. Neurotox. Res. 2010, 17:167-178.
3. Chen Y.Y., McDonald D., Cheng C., Magnowski B., Durand J., Zochodne D.W. Axon and Schwann cell partnership during nerve regrowth. J. Neuropathol. Exp. Neurol. 2005, 64:613-622.
4. Christie K.J., Webber C.A., Martinez J.A., Singh B., Zochodne D.W. PTEN inhibition to facilitate intrinsic regenerative outgrowth of adult peripheral axons. J. Neurosci. 2010, 30:9306-9315.
5. Cosker K.E., Eickholt B.J. Phosphoinositide 3-kinase signalling events controlling axonal morphogenesis. Biochem. Soc. Trans. 2007, 35:207-210.
6. Crowder R.J., 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. 2000, 275:34266-34271.
7. Drinjakovic J., Jung H., Campbell D.S., Strochlic L., Dwivedy A., Holt C.E. E3 ligase Nedd4 promotes axon branching by downregulating PTEN. Neuron 2010, 65:341-357.
8. Fouladkou F., Landry T., Kawabe H., Neeb A., Lu C., Brose N., Stambolic V., Rotin D. The ubiquitin ligase Nedd4-1 is dispensable for the regulation of PTEN stability and localization. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8585-8590.
9. Fu S.Y., Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J. Neurosci. 1995, 15:3876-3885.
10. Fu S.Y., Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J. Neurosci. 1995, 15:3886-3895.
11. Glickman M.H., Adir N. The proteasome and the delicate balance between destruction and rescue. PLoS Biol. 2004, 2:E13.
12. Jones D.M., Tucker B.A., Rahimtula M., Mearow K.M. The synergistic effects of NGF and IGF-1 on neurite growth in adult sensory neurons: convergence on the PI 3-kinase signaling pathway. J. Neurochem. 2003, 86:1116-1128.
13. Kawabe H., Neeb A., Dimova K., Young S.M., Takeda M., Katsurabayashi S., Mitkovski M., Malakhova O.A., Zhang D.E., Umikawa M., Kariya K., Goebbels S., Nave K.A., Rosenmund C., Jahn O., Rhee J., Brose N. Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 2010, 65:358-372.
14. Kim D., Dressler G.R. PTEN modulates GDNF/RET mediated chemotaxis and branching morphogenesis in the developing kidney. Dev. Biol. 2007, 307:290-299.
15. Kimpinski K., Mearow K. Neurite growth promotion by nerve growth factor and insulin-like growth factor-1 in cultured adult sensory neurons: role of phosphoinositide 3-kinase and mitogen activated protein kinase. J. Neurosci. Res. 2001, 63:486-499.
16. Klimaschewski L., Hausott B., Ingorokva S., Pfaller K. Constitutively expressed catalytic proteasomal subunits are up-regulated during neuronal differentiation and required for axon initiation, elongation and maintenance. J. Neurochem. 2006, 96:1708-1717.
17. Kwak Y.D., Ma T., Diao S., Zhang X., Chen Y., Hsu J., Lipton S.A., Masliah E., Xu H., Liao F.F. NO signaling and S-nitrosylation regulate PTEN inhibition in neurodegeneration. Mol. Neurodegener. 2010, 5:49.
18. Kwak Y.D., Wang B., Pan W., Xu H., Jiang X., Liao F.F. Functional interaction of phosphatase and tensin homologue (PTEN) with the E3 ligase NEDD4-1 during neuronal response to zinc. J. Biol. Chem. 2010, 285:9847-9857.
19. Laser H., Mack T.G., Wagner D., Coleman M.P. Proteasome inhibition arrests neurite outgrowth and causes "dying-back" degeneration in primary culture. J. Neurosci. Res. 2003, 74:906-916.
20. Lee J.R.E., Oestreich A.J., Payne J.A., Gunawan M.S., Norgan A.P., Katzmann D.J. The HECT domain of the ubiquitin ligase Rsp5 contributes to substrate recognition. J. Biol. Chem. 2009, 284:32126-32137.
21. Leslie N.R., Batty I.H., Maccario H., Davidson L., Downes C.P. Understanding PTEN regulation: PIP2, polarity and protein stability. Oncogene 2008, 27:5464-5476.
22. Lin A., Hou Q., Jarzylo L., Amato S., Gilbert J., Shang F., Man H.Y. Nedd4-mediated AMPA receptor ubiquitination regulates receptor turnover and trafficking. J. Neurochem. 2011, 119(1):27-39.
23. Lindsay R.M. Nerve growth factors (NGF, BDNF) enhance axonal regeneration but are not required for survival of adult sensory neurons. J. Neurosci. 1988, 8:2394-2405.
24. Liu K., Lu Y., Lee J.K., Samara R., Willenberg R., Sears-Kraxberger I., Tedeschi A., Park K.K., Jin D., Cai B., Xu B.G., Connolly L., Steward O., Zheng B.H., He Z.G. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat. Neurosci. 2010, 13:1075-1081.
25. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:13375-13378.
26. Narimatsu M., Bose R., Pye M., Zhang L., Miller B., Ching P., Sakuma R., Luga V., Roncari L., Attisano L., Wrana J.L. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 2009, 137:295-307.
27. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B.G., Connolly L., Kramvis I., Sahin M., He Z.G. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
28. Read D.E., Gorman A.M. Involvement of Akt in neurite outgrowth. Cell. Mol. Life Sci. 2009, 66:2975-2984.
29. Soltoff S.P., Rabin S.L., Cantley L.C., Kaplan D.R. Nerve growth factor promotes the activation of phosphatidylinositol 3-kinase and its association with the trk tyrosine kinase. J. Biol. Chem. 1992, 267:17472-17477.
30. Song E.J., Hong H.M., Yoo Y.S. Proteasome inhibition induces neurite outgrowth through posttranslational modification of TrkA receptor. Int. J. Biochem. Cell Biol. 2009, 41:539-545.
31. Tomoda H., Omura S. Lactacystin, a proteasome inhibitor: discovery and its application in cell biology. Yakugaku Zasshi 2000, 120:935-949.
32. van Diepen M.T., Parsons M., Downes C.P., Leslie N.R., Hindges R., Eickholt B.J. MyosinV controls PTEN function and neuronal cell size. Nat. Cell Biol. 2009, 11:1191-1196.
33. Verma P., Chierzi S., Codd A.M., Campbell D.S., Meyer R.L., Holt C.E., Fawcett J.W. Axonal protein synthesis and degradation are necessary for efficient growth cone regeneration. J. Neurosci. 2005, 25:331-342.
34. Wang X., Trotman L.C., Koppie T., Alimonti A., Chen Z., Gao Z., Wang J., Erdjument-Bromage H., Tempst P., Cordon-Cardo C., Pandolfi P.P., Jiang X. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 2007, 128:129-139.
35. Wang X.J., Shi Y.J., Wang J.R., Huang G.C., Jiang X.J. Crucial role of the C-terminus of PTEN in antagonizing NEDD4-1-mediated PTEN ubiquitination and degradation. Biochem. J. 2008, 414:221-229.
36. Whiteman D.C., Zhou X.P., Cummings M.C., Pavey S., Hayward N.K., Eng C. Nuclear PTEN expression and clinicopathologic features in a population-based series of primary cutaneous melanoma. Int. J. Cancer 2002, 99:63-67.
37. Yi J.J., Ehlers M.D. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol. Rev. 2007, 59:14-39.
38. 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., Lin S.Y. Rak functions as a tumor suppressor by regulating PTEN protein stability and function. Cancer Cell 2009, 15:304-314.
39. Yu T., Calvo L., Anta B., Lopez-Benito S., Southon E., Chao M.V., Tessarollo L., Arevalo J.C. Regulation of trafficking of activated TrkA is critical for NGF-mediated functions. Traffic 2011, 12:521-534.