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Neural Plasticity
Volume 2016, Article ID 2371893, 11 pages
http://dx.doi.org/10.1155/2016/2371893
Research Article

Selective Requirement for Maintenance of Synaptic Contacts onto Motoneurons by Target-Derived trkB Receptors

Department of Cell Biology, Emory University School of Medicine, Atlanta, GA 30322, USA

Received 4 April 2016; Accepted 7 June 2016

Academic Editor: Michael S. Beattie

Copyright © 2016 Xiya Zhu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. J. Alvarez, H. E. Titus-Mitchell, K. L. Bullinger, M. Kraszpulski, P. Nardelli, and T. C. Cope, “Permanent central synaptic disconnection of proprioceptors after nerve injuryand regeneration. I. Loss of VGLUT1/IA synapses on motoneurons,” Journal of Neurophysiology, vol. 106, no. 5, pp. 2450–2470, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Krakowiak, C. Liu, C. Papudesu, P. J. Ward, J. C. Wilhelm, and A. W. English, “Neuronal BDNF signaling is necessary for the effects of treadmill exercise on synaptic stripping of axotomized motoneurons,” Neural Plasticity, vol. 2015, Article ID 392591, 11 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Blinzinger and G. Kreutzberg, “Displacement of synaptic terminals from regenerating motoneurons by microglial cells,” Zeitschrift für Zellforschung und Mikroskopische Anatomie, vol. 85, no. 2, pp. 145–157, 1968. View at Publisher · View at Google Scholar · View at Scopus
  4. T. M. Rotterman, P. Nardelli, T. C. Cope, and F. J. Alvarez, “Normal distribution of VGLUT1 synapses on spinal motoneuron dendrites and their reorganization after nerve injury,” The Journal of Neuroscience, vol. 34, no. 10, pp. 3475–3492, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. J. C. Wilhelm, D. Cucoranu, M. Xu et al., “Cooperative roles of BDNF expression in neurons and schwann cells are modulated by exercise to facilitate nerve regeneration,” The Journal of Neuroscience, vol. 32, no. 14, pp. 5002–5009, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. A. A. Al-Majed, T. M. Brushart, and T. Gordon, “Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons,” European Journal of Neuroscience, vol. 12, no. 12, pp. 4381–4390, 2000. View at Publisher · View at Google Scholar · View at Scopus
  7. A. A. Al-Majed, L. T. Siu, and T. Gordon, “Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons,” Cellular and Molecular Neurobiology, vol. 24, no. 3, pp. 379–402, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. M. J. Titmus and D. S. Faber, “Axotomy-induced alterations in the electrophysiological characteristics of neurons,” Progress in Neurobiology, vol. 35, no. 1, pp. 1–51, 1990. View at Publisher · View at Google Scholar · View at Scopus
  9. M. A. Davis-López de Carrizosa, C. J. Morado-Díaz, J. J. Tena et al., “Complementary actions of BDNF and neurotrophin-3 on the firing patterns and synaptic composition of motoneurons,” The Journal of Neuroscience, vol. 29, no. 2, pp. 575–587, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. L. M. Mendell, J. B. Munson, and V. L. Arvanian, “Neurotrophins and synaptic plasticity in the mammalian spinal cord,” Journal of Physiology, vol. 533, no. 1, pp. 91–97, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. L. M. Mendell, R. D. Johnson, and J. B. Munson, “Neurotrophin modulation of the monosynaptic reflex after peripheral nerve transection,” Journal of Neuroscience, vol. 19, no. 8, pp. 3162–3170, 1999. View at Google Scholar · View at Scopus
  12. B. Benítez-Temiño, S. Morcuende, G. Z. Mentis, R. R. de la Cruz, and Á. M. Pastor, “Expression of Trk receptors in the oculomotor system of the adult cat,” The Journal of Comparative Neurology, vol. 473, no. 4, pp. 538–552, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Copray and D. Kernell, “Neurotrophins and trk-receptors in adult rat spinal motoneurons: differences related to cell size but not to ‘slow/fast’ specialization,” Neuroscience Letters, vol. 289, no. 3, pp. 217–220, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. M. C. Osborne, T. Verhovshek, and D. R. Sengelaub, “Androgen regulates trkB immunolabeling in spinal motoneurons,” Journal of Neuroscience Research, vol. 85, no. 2, pp. 303–309, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. L. C. Rutherford, A. DeWan, H. M. Lauer, and G. G. Turrigiano, “Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures,” The Journal of Neuroscience, vol. 17, no. 12, pp. 4527–4535, 1997. View at Google Scholar · View at Scopus
  16. S. Marty, R. Wehrle, and C. Sotelo, “Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus,” The Journal of Neuroscience, vol. 20, no. 21, pp. 8087–8095, 2000. View at Google Scholar · View at Scopus
  17. F. J. Seil and R. Drake-Baumann, “TrkB receptor ligands promote activity-dependent inhibitory synaptogenesis,” The Journal of Neuroscience, vol. 20, no. 14, pp. 5367–5373, 2000. View at Google Scholar · View at Scopus
  18. A. I. Chen, C. N. Nguyen, D. R. Copenhagen et al., “TrkB (Tropomyosin-related kinase B) controls the assembly and maintenance of GABAergic synapses in the cerebellar cortex,” The Journal of Neuroscience, vol. 31, no. 8, pp. 2769–2780, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. X.-P. Gao, Q. Liu, B. Nair, and M. T. T. Wong-Riley, “Reduced levels of brain-derived neurotrophic factor contribute to synaptic imbalance during the critical period of respiratory development in rats,” European Journal of Neuroscience, vol. 40, no. 1, pp. 2183–2195, 2014. View at Publisher · View at Google Scholar · View at Scopus
  20. M. A. Davis-López De Carrizosa, C. J. Morado-Díaz, S. Morcuende, R. R. De La Cruz, and Á. M. Pastor, “Nerve growth factor regulates the firing patterns and synaptic composition of motoneurons,” Journal of Neuroscience, vol. 30, no. 24, pp. 8308–8319, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Verhovshek, Y. Cai, M. C. Osborne, and D. R. Sengelaub, “Androgen regulates brain-derived neurotrophic factor in spinal motoneurons and their target musculature,” Endocrinology, vol. 151, no. 1, pp. 253–261, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Liu, P. J. Ward, and A. W. English, “The effects of exercise on synaptic stripping require androgen receptor signaling,” PLoS ONE, vol. 9, no. 6, Article ID e98633, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. D. T. Solum and R. J. Handa, “Estrogen regulates the development of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus,” The Journal of Neuroscience, vol. 22, no. 7, pp. 2650–2659, 2002. View at Google Scholar · View at Scopus
  24. X. Zhu, P. J. Ward, and A. W. English, “Selective withdrawal of synaptic inputs onto motoneurons in trkB knockout mice,” in Neuroscience Meeting Planner, Program No. 467.04/EEE5, Society for Neuroscience, San Diego, Calif, USA, 2013.
  25. R. Klein, R. J. Smeyne, W. Wurst et al., “Targeted disruption of the trkB neurotrophin receptor gene results in nervous system lesions and neonatal death,” Cell, vol. 75, no. 1, pp. 113–122, 1993. View at Publisher · View at Google Scholar · View at Scopus
  26. X.-P. He, R. Kotloski, S. Nef, B. W. Luikart, L. F. Parada, and J. O. McNamara, “Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model,” Neuron, vol. 43, no. 1, pp. 31–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Young, L. Qiu, D. Wang, S. Zhao, J. Gross, and G. Feng, “Single-neuron labeling with inducible Cre-mediated knockout in transgenic mice,” Nature Neuroscience, vol. 11, no. 6, pp. 721–728, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. A. W. English, K. Liu, J. M. Nicolini, A. M. Mulligan, and K. Ye, “Small-molecule trkB agonists promote axon regeneration in cut peripheral nerves,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 40, pp. 16217–16222, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. L. M. Mendell, J. B. Munson, and J. G. Scott, “Alterations of synapses on axotomized motoneurones,” The Journal of Physiology, vol. 255, no. 1, pp. 67–79, 1976. View at Publisher · View at Google Scholar · View at Scopus
  30. I. W. McLean and P. K. Nakane, “Periodate lysine paraformaldehyde fixative. A new fixative for immunoelectron microscopy,” Journal of Histochemistry and Cytochemistry, vol. 22, no. 12, pp. 1077–1083, 1974. View at Publisher · View at Google Scholar · View at Scopus
  31. S. L. McIntire, R. J. Reimer, K. Schuske, R. H. Edwards, and E. M. Jorgensen, “Identification and characterization of the vesicular GABA transporter,” Nature, vol. 389, no. 6653, pp. 870–876, 1997. View at Publisher · View at Google Scholar · View at Scopus
  32. F. A. Chaudhry, R. J. Reimer, E. E. Bellocchio et al., “The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons,” The Journal of Neuroscience, vol. 18, no. 23, pp. 9733–9750, 1998. View at Google Scholar · View at Scopus
  33. D. I. Hughes, E. Polgár, S. A. S. Shehab, and A. J. Todd, “Peripheral axotomy induces depletion of the vesicular glutamate transporter VGLUT1 in central terminals of myelinated afferent fibres in the rat spinal cord,” Brain Research, vol. 1017, no. 1-2, pp. 69–76, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. F. J. Alvarez, R. M. Villalba, R. Zerda, and S. P. Schneider, “Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses,” Journal of Comparative Neurology, vol. 472, no. 3, pp. 257–280, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. A. J. Todd, D. I. Hughes, E. Polgár et al., “The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn,” European Journal of Neuroscience, vol. 17, no. 1, pp. 13–27, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Wang, S. Pillai, J. R. Wolpaw, and X. Y. Chen, “Motor learning changes GABAergic terminals on spinal motoneurons in normal rats,” European Journal of Neuroscience, vol. 23, no. 1, pp. 141–150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. M. A. Bemben, S. L. Shipman, R. A. Nicoll, and K. W. Roche, “The cellular and molecular landscape of neuroligins,” Trends in Neurosciences, vol. 38, no. 8, pp. 496–505, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Tsetsenis, A. A. Boucard, D. Arac, A. T. Brunger, and T. C. Südhof, “Direct visualization of trans-synaptic neurexin-neuroligin interactions during synapse formation,” Journal of Neuroscience, vol. 34, no. 45, pp. 15083–15096, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Berg, J. Zelano, and S. Cullheim, “Netrin G-2 ligand mRNA is downregulated in spinal motoneurons after sciatic nerve lesion,” NeuroReport, vol. 21, no. 11, pp. 782–785, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. P.-L. Cheng, A.-H. Song, Y.-H. Wong, S. Wang, X. Zhang, and M.-M. Poo, “Self-amplifying autocrine actions of BDNF in axon development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 45, pp. 18430–18435, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. V. H. Perry and V. O'Connor, “The role of microglia in synaptic stripping and synaptic degeneration: a revised perspective,” ASN neuro, vol. 2, no. 5, Article ID e00047, 2010. View at Google Scholar · View at Scopus
  42. R. E. Sorge, J. C. S. Mapplebeck, S. Rosen et al., “Different immune cells mediate mechanical pain hypersensitivity in male and female mice,” Nature Neuroscience, vol. 18, no. 8, pp. 1081–1083, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. J. A. M. Coull, S. Beggs, D. Boudreau et al., “BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain,” Nature, vol. 438, no. 7070, pp. 1017–1021, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Kettenmann, F. Kirchhoff, and A. Verkhratsky, “Microglia: new roles for the synaptic stripper,” Neuron, vol. 77, no. 1, pp. 10–18, 2013. View at Publisher · View at Google Scholar · View at Scopus