BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Nerve growth factor-induced neurite outgrowth is potentiated by stabilization of TrkA receptors

  • Song, Eun-Joo (Integrated Omics Center, Life Health Division, Korea Institute of Science and Technology) ;
  • Yoo, Young-Sook (Integrated Omics Center, Life Health Division, Korea Institute of Science and Technology)
  • Received : 2010.12.16
  • Accepted : 2011.01.03
  • Published : 2011.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Exogenous stimuli such as nerve growth factor (NGF) exert their effects on neurite outgrowth via Trk neurotrophin receptors. TrkA receptors are known to be ubiquitinated via proteasome inhibition in the presence of NGF. However, the effect of proteasome inhibition on neurite outgrowth has not been studied extensively. To clarify these issues, we investigated signaling events in PC12 cells treated with NGF and the proteasome inhibitor MG132. We found that MG132 facilitated NGF-induced neurite outgrowth and potentiated the phosphorylation of the extracellular signal-regulated kinase/mitogen-activated protein kinase (ERK/MAPK) and phosphatidylinositol-3-kinase (PI3K)/AKT pathways and TrkA receptors. MG132 stimulated internalization of surface TrkA receptor and stabilized intracellular TrkA receptor, and the $Ub^{K63}$ chain was found to be essential for stability. These results indicate that the ubiquitin-proteasome system potentiated neurite formation by regulating the stability of TrkA receptors.

Keywords

References

  1. Alfa, R. W., Tuszynski, M. H. and Blesch, A. (2009) Anovel inducible tyrosine kinase receptor to regulate signaltransduction and neurite outgrowth. J. Neurosci. Res. 87,2624-2631. https://doi.org/10.1002/jnr.22101
  2. Huang, E. and Reichardt, L. (2001) Neurotrophins: roles inneuronal development and function. Annu. Rev. Neurosci.24, 677-736. https://doi.org/10.1146/annurev.neuro.24.1.677
  3. Huang, E. and Reichardt, L. (2003) Trk receptors: roles inneuronal signal transduction. Annu. Rev. Biochem. 72,609-642. https://doi.org/10.1146/annurev.biochem.72.121801.161629
  4. Geetha, T. and Wooten, M. W. (2008) TrkA receptor endolysosomaldegradation is both ubiquitin and proteasomedependent. Traffic 9, 1146-1156. https://doi.org/10.1111/j.1600-0854.2008.00751.x
  5. Moises, T., Wuller, S., Saxena, S., Senderek, J., Weis, J.and Krüttgen, A. (2009) Proteasomal inhibition alters thetrafficking of the neurotrophin receptor TrkA. Biochem.Biophys. Res. Commun. 387, 360-364. https://doi.org/10.1016/j.bbrc.2009.07.032
  6. Chao, M. V. and Hempstead, B. L. (1995) p75 and Trk: atwo-receptor system. Trends Neurosci. 18, 321-326. https://doi.org/10.1016/0166-2236(95)93922-K
  7. Vaudry, D., Stork, P. J., Lazarovici, P. and Eiden, L. E.(2002) Signaling pathways for PC12 cell differentiation:Making the right connections. Science 296, 1648-1649. https://doi.org/10.1126/science.1071552
  8. Hershko, A. and Ciechanover, A. (1998) The ubiquitinsystem. Annu. Rev. Biochem. 67, 425-430. https://doi.org/10.1146/annurev.biochem.67.1.425
  9. Verma, R., Oania, R., Graumann, J. and Deshaies, R. J.(2004) Multiubiquitin chain receptors define a layer ofsubstrate selectivity in the ubiquitin-proteasome system.Cell 118, 99-110. https://doi.org/10.1016/j.cell.2004.06.014
  10. Pickart, C. M. (2001) Ubiquitin enters the new millennium.Mol. Cell 8, 499-504. https://doi.org/10.1016/S1097-2765(01)00347-1
  11. Rubinsztein, D. C. (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature443, 780-786. https://doi.org/10.1038/nature05291
  12. Geetha, T., Jiang, J. and Wooten, M. W. (2005) Lysine 63polyubiquitination of the nerve growth factor receptorTrkA directs internalization and signaling. Mol. Cell 20,301-312. https://doi.org/10.1016/j.molcel.2005.09.014
  13. Geetha, T., Seibenhener, M. L., Chen, L., Madura, K. andWooten, M. W. (2008) p62 serves as a shuttling factor forTrkA interaction with the proteasome. Biochem. Biophys.Res. Commun. 374, 33-37. https://doi.org/10.1016/j.bbrc.2008.06.082
  14. Jadhav, T., Geetha, T., Jiang, J. and Wooten, M. W. (2008)Identification of a consensus site for TRAF6/p62 polyubiquitination.Biochem. Biophys. Res. Commun. 371, 521-524. https://doi.org/10.1016/j.bbrc.2008.04.138
  15. Obin, M., Mesco, E., Gong, X., Haas, A. L., Joseph, J. andTaylor, A. (1999) Neurite outgrowth in PC12 cells. J. Biol.Chem. 274, 11789-11795. https://doi.org/10.1074/jbc.274.17.11789
  16. Inoue, M., Zhai, H., Sahazaki, H., Furuyama, H., Fukuyama,Y. and Hirima, M. (2004). TMC-95A, a reversible proteasomeinhibitor, induces neurite outgrowth in PC12cells. Bioorg. Med. Chem. Lett. 14, 663-665. https://doi.org/10.1016/j.bmcl.2003.11.043
  17. Momose, I., Sekizawa, R., Iinuma, H. and Takeuchi, T.(2002). Inhibition of proteasome activity by tyropeptin Ain PC12 cells. Biosci. Biotechnol. Biochem. 66, 2256-2258. https://doi.org/10.1271/bbb.66.2256
  18. Song, E. J., Hong, H. M. and Yoo, Y. S. (2009) Proteasomeinhibition induces neurite outgrowth through posttranslationalmodification of TrkA receptor. Int. J. Biochem. Cell.Biol. 41, 539-545. https://doi.org/10.1016/j.biocel.2008.04.022
  19. Pasquini, L. A., Paez, P. M., Besio Moreno, M. A., Pasquini,J. M. and Soto, E. F. (2003) Inhibition of the protein bylactacystin enhances oligodendroglial cell differentiation.J. Neurosci. 23, 4635-4644.
  20. Bronfman, F. C., Tcherpakov, M., Jovin, T. M. andFainzilber, M. (2003) Ligand-induced internalization ofthe p75 neurotrophin receptor: a slow route to the signalingendosome. J. Neurosci. 23, 3209-3220.
  21. Kuruvilla, R., Zweifel, L. S., Glebova, N. O., Lonze, B. E., Valdex, G., Ye, H. and Ginty, D. D. (2004) A neurotrophinsignaling cascade coordinates sympathetic neurondevelopment through differential control of TrkA traffickingand retrograde signaling. Cell 118, 243-255. https://doi.org/10.1016/j.cell.2004.06.021
  22. Makkerh, J. P., Ceni, C., Auld, D. S., Vaillancourt, F.,Dorval, G. and Baker, P. A. (2005) p75 neurotrophin receptorreduces ligand-induced Trk receptor ubiquitinationand delays Trk receptor internalization and degradation.EMBO Rep. 6, 936-941. https://doi.org/10.1038/sj.embor.7400503
  23. Alwan, H. A., van Zoelen, E. J. and van Leeuwen, J. E.(2003) Ligand-induced lysosomal epidermal growth factorreceptor (EGFR) degradation is preceded by proteasome-dependentEGFR de-ubiquitination. J. Biol. Chem. 278,35781-35790. https://doi.org/10.1074/jbc.M301326200
  24. Chen, Z. Y., Ieraci, A., Tanowitz, M. and Lee, F. S. (2005)A novel endocytic recycling signal distinguishes biologicalresponses of Trk neurotrophin receptors. Mol. Biol. Cell 6,5761-5772.
  25. Jin, L., Williamson, A., Banerjee, S., Philipp, I. and Rape,M. (2008) Mechanism of ubiquitin-chain formation by thehuman anaphase-promoting complex. Cell 133, 653-665. https://doi.org/10.1016/j.cell.2008.04.012

Cited by

  1. Electroactive Electrospun Polyaniline/Poly[(L-lactide)-co-(ε-caprolactone)] Fibers for Control of Neural Cell Function vol.12, pp.3, 2012, https://doi.org/10.1002/mabi.201100333
  2. The Role of Rab Proteins in Neuronal Cells and in the Trafficking of Neurotrophin Receptors vol.4, pp.4, 2014, https://doi.org/10.3390/membranes4040642
  3. Differentiation of Schwann-like cells from human umbilical cord blood mesenchymal stem cells in vitro vol.11, pp.2, 2015, https://doi.org/10.3892/mmr.2014.2840
  4. Neurotrophic Effects of Mu Bie Zi (Momordica cochinchinensis) Seed Elucidated by High-Throughput Screening of Natural Products for NGF Mimetic Effects in PC-12 Cells vol.40, pp.10, 2015, https://doi.org/10.1007/s11064-015-1560-y
  5. Transcriptional Upregulation of Plasminogen Activator Inhibitor-1 in Rat Primary Astrocytes by a Proteasomal Inhibitor MG132 vol.21, pp.2, 2013, https://doi.org/10.4062/biomolther.2012.102
  6. Neurotrophin production in brain pericytes during hypoxia: A role of pericytes for neuroprotection vol.83, pp.3, 2012, https://doi.org/10.1016/j.mvr.2012.02.009
  7. Neurotrophin receptors in the pathogenesis, diagnosis and therapy of neurodegenerative diseases vol.121, 2017, https://doi.org/10.1016/j.phrs.2017.04.024
  8. Comparative Analysis of Paracrine Factor Expression in Human Adult Mesenchymal Stem Cells Derived from Bone Marrow, Adipose, and Dermal Tissue vol.21, pp.12, 2012, https://doi.org/10.1089/scd.2011.0674
  9. NGF-dependent axon growth and regeneration are altered in sympathetic neurons of dystrophic mdx mice vol.80, 2017, https://doi.org/10.1016/j.mcn.2017.01.006
  10. RANTES has a potential to play a neuroprotective role in an autocrine/paracrine manner after ischemic stroke vol.1517, 2013, https://doi.org/10.1016/j.brainres.2013.04.022
  11. Nuclear Rac1 regulates the bFGF-induced neurite outgrowth in PC12 cells vol.46, pp.12, 2013, https://doi.org/10.5483/BMBRep.2013.46.12.114
  12. The role of Src protein in the process formation of PC12 cells induced by the proteasome inhibitor MG-132 vol.63, pp.5, 2013, https://doi.org/10.1016/j.neuint.2013.07.008
  13. Involvement of P2Y13 receptor in suppression of neuronal differentiation vol.518, pp.1, 2012, https://doi.org/10.1016/j.neulet.2012.04.021
  14. A novel role of suppressor of cytokine signaling-2 in the regulation of TrkA neurotrophin receptor biology vol.129, pp.4, 2014, https://doi.org/10.1111/jnc.12671
  15. Physical exercise, reactive oxygen species and neuroprotection vol.98, 2016, https://doi.org/10.1016/j.freeradbiomed.2016.01.024