Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016 (2016), Article ID 3679545, 14 pages
http://dx.doi.org/10.1155/2016/3679545
Review Article

The Chemorepulsive Protein Semaphorin 3A and Perineuronal Net-Mediated Plasticity

1Netherlands Institute for Neuroscience, Royal Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, Netherlands
2John van Geest Centre for Brain Repair, University of Cambridge, Cambridge CB2 OPY, UK
3Department of Neuroscience, Neuroscience Institute of Turin (NIT) and Neuroscience Institute Cavalieri-Ottolenghi (NICO), University of Turin, Orbassano, 10043 Turin, Italy

Received 18 September 2015; Accepted 10 December 2015

Academic Editor: Preston E. Garraghty

Copyright © 2016 F. de Winter 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. C. S. Goodman, “Mechanisms and molecules that control growth cone guidance,” Annual Review of Neuroscience, vol. 19, no. 1, pp. 341–377, 1996. View at Publisher · View at Google Scholar
  2. T. S. Tran, A. L. Kolodkin, and R. Bharadwaj, “Semaphorin regulation of cellular morphology,” Annual Review of Cell and Developmental Biology, vol. 23, no. 1, pp. 263–292, 2007. View at Publisher · View at Google Scholar
  3. Y. Yoshida, “Semaphorin signaling in vertebrate neural circuit assembly,” Frontiers in Molecular Neuroscience, vol. 5, article 71, 2012. View at Publisher · View at Google Scholar
  4. Y. Luo, D. Raible, and J. A. Raper, “Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones,” Cell, vol. 75, no. 2, pp. 217–227, 1993. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Roth, E. Koncina, S. Satkauskas, G. Crémel, D. Aunis, and D. Bagnard, “The many faces of semaphorins: from development to pathology,” Cellular and Molecular Life Sciences, vol. 66, no. 4, pp. 649–666, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Gu and E. Giraudo, “The role of semaphorins and their receptors in vascular development and cancer,” Experimental Cell Research, vol. 319, no. 9, pp. 1306–1316, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. R. J. Pasterkamp, R. J. Giger, M.-J. Ruitenberg et al., “Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS,” Molecular and Cellular Neurosciences, vol. 13, no. 2, pp. 143–166, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. F. De Winter, M. Oudega, A. J. Lankhorst et al., “Injury-induced class 3 semaphorin expression in the rat spinal cord,” Experimental Neurology, vol. 175, no. 1, pp. 61–75, 2002. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Kaneko, A. Iwanami, M. Nakamura et al., “A selective Sema3A inhibitor enhances regenerative responses and functional recovery of the injured spinal cord,” Nature Medicine, vol. 12, no. 12, pp. 1380–1389, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Koropouli and A. L. Kolodkin, “Semaphorins and the dynamic regulation of synapse assembly, refinement, and function,” Current Opinion in Neurobiology, vol. 27, pp. 1–7, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Y. Van Battum, S. Brignani, and R. J. Pasterkamp, “Axon guidance proteins in neurological disorders,” The Lancet Neurology, vol. 14, no. 5, pp. 532–546, 2015. View at Publisher · View at Google Scholar
  12. C. S. Goodman, A. L. Kolodkin, Y. Luo, A. W. Püschel, and J. A. Raper, “Unified nomenclature for the semaphorins/collapsins,” Cell, vol. 97, no. 5, pp. 551–552, 1999. View at Publisher · View at Google Scholar
  13. H. Chen, A. Chédotal, Z. He, C. S. Goodman, and M. Tessier-Lavigne, “Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III,” Neuron, vol. 19, no. 3, pp. 547–559, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. Z. He and M. Tessier-Lavigne, “Neuropilin is a receptor for the axonal chemorepellent Semaphorin III,” Cell, vol. 90, no. 4, pp. 739–751, 1997. View at Publisher · View at Google Scholar · View at Scopus
  15. A. L. Kolodkin, D. V. Levengood, E. G. Rowe, Y.-T. Tai, R. J. Giger, and D. D. Ginty, “Neuropilin is a semaphorin III receptor,” Cell, vol. 90, no. 4, pp. 753–762, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Takahashi, F. Nakamura, and S. M. Strittmatter, “Neuronal and non-neuronal collapsin-1 binding sites in developing chick are distinct from other semaphorin binding sites,” The Journal of Neuroscience, vol. 17, no. 23, pp. 9183–9193, 1997. View at Google Scholar · View at Scopus
  17. T. Takahashi, A. Fournier, F. Nakamura et al., “Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors,” Cell, vol. 99, no. 1, pp. 59–69, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. B. J. Janssen, R. A. Robinson, F. Perez-Branguli et al., “Structural basis of semaphorin-plexin signalling,” Nature, vol. 467, no. 7319, pp. 1118–1122, 2010. View at Publisher · View at Google Scholar
  19. A. Sharma, J. Verhaagen, and A. R. Harvey, “Receptor complexes for each of the class 3 Semaphorins,” Frontiers in Cellular Neuroscience, vol. 6, article 28, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. D. B. Kantor, O. Chivatakarn, K. L. Peer et al., “Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans,” Neuron, vol. 44, no. 6, pp. 961–975, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. R. P. Kruger, J. Aurandt, and K.-L. Guan, “Semaphorins command cells to move,” Nature Reviews Molecular Cell Biology, vol. 6, no. 10, pp. 789–800, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. A. W. Puschel, “GTPases in semaphorin signaling,” in Semaphorins: Receptor and Intracellular Signaling Mechanisms, vol. 600 of Advances in Experimental Medicine and Biology, pp. 12–23, Springer, New York, NY, USA, 2007. View at Publisher · View at Google Scholar
  23. R. J. Pasterkamp and R. J. Giger, “Semaphorin function in neural plasticity and disease,” Current Opinion in Neurobiology, vol. 19, no. 3, pp. 263–274, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. P. K. Hota and M. Buck, “Plexin structures are coming: opportunities for multilevel investigations of semaphorin guidance receptors, their cell signaling mechanisms, and functions,” Cellular and Molecular Life Sciences, vol. 69, no. 22, pp. 3765–3805, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Goshima, F. Nakamura, P. Strittmatter, and S. M. Strittmatter, “Collapsin-induced growth cone collapse mediated by an intracellular protein related to UNC-33,” Nature, vol. 376, no. 6540, pp. 509–514, 1995. View at Publisher · View at Google Scholar · View at Scopus
  26. J. R. Terman, T. Mao, R. J. Pasterkamp, H.-H. Yu, and A. L. Kolodkin, “MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion,” Cell, vol. 109, no. 7, pp. 887–900, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. R. C. Deo, E. F. Schmidt, A. Elhabazi, H. Togashi, S. K. Burley, and S. Strittmatter, “Structural bases for CRMP function in plexin-dependent semaphorin3A signaling,” The EMBO Journal, vol. 23, no. 1, pp. 9–22, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. E. F. Schmidt and S. M. Strittmatter, “The CRMP family of proteins and their role in Sema3A signaling,” in Semaphorins: Receptor and Intracellular Signaling Mechanisms, vol. 600 of Advances in Experimental Medicine and Biology, pp. 1–11, Springer, 2007. View at Google Scholar
  29. E. F. Schmidt, S.-O. Shim, and S. M. Strittmatter, “Release of MICAL autoinhibition by semaphorin-plexin signaling promotes interaction with collapsin response mediator protein,” The Journal of Neuroscience, vol. 28, no. 9, pp. 2287–2297, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. R.-J. Hung, U. Yazdani, J. Yoon et al., “Mical links semaphorins to F-actin disassembly,” Nature, vol. 463, no. 7282, pp. 823–827, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Yamashita and Y. Goshima, “Collapsin response mediator proteins regulate neuronal development and plasticity by switching their phosphorylation status,” Molecular Neurobiology, vol. 45, no. 2, pp. 234–246, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Pecho-Vrieseling, M. Sigrist, Y. Yoshida, T. M. Jessell, and S. Arber, “Specificity of sensory-motor connections encoded by Sema3e-Plxnd1 recognition,” Nature, vol. 459, no. 7248, pp. 842–846, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. B. Ding, W.-J. Oh, B. L. Sabatini, and C. Gu, “Semaphorin 3E-Plexin-D1 signaling controls pathway-specific synapse formation in the striatum,” Nature Neuroscience, vol. 15, no. 2, pp. 215–223, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Morita, N. Yamashita, Y. Sasaki et al., “Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling,” The Journal of Neuroscience, vol. 26, no. 11, pp. 2971–2980, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Yamashita, A. Morita, Y. Uchida et al., “Regulation of spine development by semaphorin3A through cyclin-dependent kinase 5 phosphorylation of collapsin response mediator protein 1,” Journal of Neuroscience, vol. 27, no. 46, pp. 12546–12554, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. T. S. Tran, M. E. Rubio, R. L. Clem et al., “Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS,” Nature, vol. 462, no. 7276, pp. 1065–1069, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. G. P. Demyanenko, V. Mohan, X. Zhang et al., “Neural cell adhesion molecule NrCAM regulates semaphorin 3F-induced dendritic spine remodeling,” Journal of Neuroscience, vol. 34, no. 34, pp. 11274–11287, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Duan, S. Wang, J. Song et al., “Semaphorin 5A inhibits synaptogenesis in early postnatal- and adult-born hippocampal dentate granule cells,” eLife, vol. 3, Article ID e04390, 2014. View at Publisher · View at Google Scholar
  39. S. Paradis, D. B. Harrar, Y. Lin et al., “An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development,” Neuron, vol. 53, no. 2, pp. 217–232, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. M. S. Kuzirian, A. R. Moore, E. K. Staudenmaier, R. H. Friedel, and S. Paradis, “The class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus,” The Journal of Neuroscience, vol. 33, no. 21, pp. 8961–8973, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. A. J. Raissi, E. K. Staudenmaier, S. David, L. Hu, and S. Paradis, “Sema4D localizes to synapses and regulates GABAergic synapse development as a membrane-bound molecule in the mammalian hippocampus,” Molecular and Cellular Neuroscience, vol. 57, pp. 23–32, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Uesaka, M. Uchigashima, T. Mikuni et al., “Retrograde semaphorin signaling regulates synapse elimination in the developing mouse brain,” Science, vol. 344, no. 6187, pp. 1020–1023, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. T. P. O'Connor, K. Cockburn, W. Wang, L. Tapia, E. Currie, and S. X. Bamji, “Semaphorin 5B mediates synapse elimination in hippocampal neurons,” Neural Development, vol. 4, no. 1, article 18, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Sahay, C.-H. Kim, J. P. Sepkuty et al., “Secreted semaphorins modulate synaptic transmission in the adult hippocampus,” The Journal of Neuroscience, vol. 25, no. 14, pp. 3613–3620, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Bouzioukh, G. Daoudal, J. Falk, D. Debanne, G. Rougon, and V. Castellani, “Semaphorin3A regulates synaptic function of differentiated hippocampal neurons,” European Journal of Neuroscience, vol. 23, no. 9, pp. 2247–2254, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. R. J. Giger, R. J. Pasterkamp, S. Heijnen, A. J. G. D. Holtmaat, and J. Verhaagen, “Anatomical distribution of the chemorepellent semaphorin III/collapsin-1 in the adult rat and human brain: predominant expression in structures of the olfactory-hippocampal pathway and the motor system,” Journal of Neuroscience Research, vol. 52, no. 1, pp. 27–42, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Wang and J. Fawcett, “The perineuronal net and the control of CNS plasticity,” Cell and Tissue Research, vol. 349, no. 1, pp. 147–160, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. M. R. Celio and I. Blümcke, “Perineuronal nets—a specialized form of extracellular matrix in the adult nervous system,” Brain Research Reviews, vol. 19, no. 1, pp. 128–145, 1994. View at Publisher · View at Google Scholar · View at Scopus
  49. T. K. Hensch, “Critical period plasticity in local cortical circuits,” Nature Reviews Neuroscience, vol. 6, no. 11, pp. 877–888, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. D. Carulli, S. Foscarin, A. Faralli, E. Pajaj, and F. Rossi, “Modulation of semaphorin3A in perineuronal nets during structural plasticity in the adult cerebellum,” Molecular and Cellular Neuroscience, vol. 57, pp. 10–22, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Vo, D. Carulli, E. M. E. Ehlert et al., “The chemorepulsive axon guidance protein semaphorin3A is a constituent of perineuronal nets in the adult rodent brain,” Molecular and Cellular Neuroscience, vol. 56, pp. 186–200, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Dick, C. Liktan, J. N. Alves et al., “Semaphorin 3A binds to the perineuronal nets via chondroitin sulfate type E motifs in rodent brains,” The Journal of Biological Chemistry, vol. 288, no. 38, pp. 27384–27395, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Sugiyama, A. A. Di Nardo, S. Aizawa et al., “Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity,” Cell, vol. 134, no. 3, pp. 508–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Beurdeley, J. Spatazza, H. H. C. Lee et al., “Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex,” The Journal of Neuroscience, vol. 32, no. 27, pp. 9429–9437, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Carulli, T. Pizzorusso, J. C. F. Kwok et al., “Animals lacking link protein have attenuated perineuronal nets and persistent plasticity,” Brain, vol. 133, no. 8, pp. 2331–2347, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Kosaka and C. W. Heizmann, “Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine,” Brain Research, vol. 483, no. 1, pp. 158–163, 1989. View at Publisher · View at Google Scholar · View at Scopus
  57. J. De Wit, R. F. Toonen, J. Verhaagen, and M. Verhage, “Vesicular trafficking of semaphorin 3A is activity-dependent and differs between axons and dendrites,” Traffic, vol. 7, no. 8, pp. 1060–1077, 2006. View at Publisher · View at Google Scholar · View at Scopus
  58. J. De Wit, R. F. Toonen, and M. Verhage, “Matrix-dependent local retention of secretory vesicle cargo in cortical neurons,” The Journal of Neuroscience, vol. 29, no. 1, pp. 23–37, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Spatazza, H. H. C. Lee, A. A. Di Nardo et al., “Choroid-plexus-derived Otx2 homeoprotein constrains adult cortical plasticity,” Cell Reports, vol. 3, no. 6, pp. 1815–1823, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Alpár, U. Gärtner, W. Härtig, and G. Brückner, “Distribution of pyramidal cells associated with perineuronal nets in the neocortex of rat,” Brain Research, vol. 1120, no. 1, pp. 13–22, 2006. View at Publisher · View at Google Scholar
  61. D. Cabulli, K. E. Rhodes, and J. W. Fawcett, “Upregulation of aggrecan, link protein 1, and hyaluronan synthases during formation of perineuronal nets in the rat cerebellum,” Journal of Comparative Neurology, vol. 501, no. 1, pp. 83–94, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Morawski, G. Brückner, C. Jäger, G. Seeger, H. Künzle, and T. Arendt, “Aggrecan-based extracellular matrix shows unique cortical features and conserved subcortical principles of mammalian brain organization in the Madagascan lesser hedgehog tenrec (Echinops telfairi Martin, 1838),” Neuroscience, vol. 165, no. 3, pp. 831–849, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. E. D. Gundelfinger, R. Frischknecht, D. Choquet, and M. Heine, “Converting juvenile into adult plasticity: a role for the brain's extracellular matrix,” European Journal of Neuroscience, vol. 31, no. 12, pp. 2156–2165, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. J. C. F. Kwok, G. Dick, D. Wang, and J. W. Fawcett, “Extracellular matrix and perineuronal nets in CNS repair,” Developmental Neurobiology, vol. 71, no. 11, pp. 1073–1089, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Sugahara and T. Mikami, “Chondroitin/dermatan sulfate in the central nervous system,” Current Opinion in Structural Biology, vol. 17, no. 5, pp. 536–545, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. K. Kadomatsu and K. Sakamoto, “Mechanisms of axon regeneration and its inhibition: roles of sulfated glycans,” Archives of Biochemistry and Biophysics, vol. 558, pp. 36–41, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. J. De Wit, F. De Winter, J. Klooster, and J. Verhaagen, “Semaphorin 3A displays a punctate distribution on the surface of neuronal cells and interacts with proteoglycans in the extracellular matrix,” Molecular and Cellular Neuroscience, vol. 29, no. 1, pp. 40–55, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. G. Zimmer, S. M. Schanuel, S. Bürger et al., “Chondroitin sulfate acts in concert with semaphorin 3A to guide tangential migration of cortical interneurons in the ventral telencephalon,” Cerebral Cortex, vol. 20, no. 10, pp. 2411–2422, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. L. D. F. Moon, R. A. Asher, K. E. Rhodes, and J. W. Fawcett, “Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC,” Nature Neuroscience, vol. 4, no. 5, pp. 465–466, 2001. View at Google Scholar · View at Scopus
  70. A. W. Barritt, M. Davies, F. Marchand et al., “Chondroitinase ABC promotes sprouting of intact and injured spinal systems after spinal cord injury,” Journal of Neuroscience, vol. 26, no. 42, pp. 10856–10867, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. D. Wang, R. M. Ichiyama, R. Zhao, M. R. Andrews, and J. W. Fawcett, “Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury,” Journal of Neuroscience, vol. 31, no. 25, pp. 9332–9344, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Wang, Y. Katagiri, T. E. McCann et al., “Chondroitin-4-sulfation negatively regulates axonal guidance and growth,” Journal of Cell Science, vol. 121, no. 18, pp. 3083–3091, 2008. View at Publisher · View at Google Scholar · View at Scopus
  73. R. Lin, T. W. Rosahl, P. J. Whiting, J. W. Fawcett, and J. C. F. Kwok, “6-sulphated chondroitins have a positive influence on axonal regeneration,” PLoS ONE, vol. 6, no. 7, Article ID e21499, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Miyata, Y. Komatsu, Y. Yoshimura, C. Taya, and H. Kitagawa, “Persistent cortical plasticity by upregulation of chondroitin 6-sulfation,” Nature Neuroscience, vol. 15, no. 3, pp. 414–422, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Yoo, M. Khaled, K. M. Gibbs et al., “Arylsulfatase B improves locomotor function after mouse spinal cord injury,” PLoS ONE, vol. 8, no. 3, Article ID e57415, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. S. S. Deepa, D. Carulli, C. Galtrey et al., “Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans,” The Journal of Biological Chemistry, vol. 281, no. 26, pp. 17789–17800, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. X. Lin, “Functions of heparan sulfate proteoglycans in cell signaling during development,” Development, vol. 131, no. 24, pp. 6009–6021, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. A. H. Conrad, Y. Zhang, E. S. Tasheva, and G. W. Conrad, “Proteomic analysis of potential keratan sulfate, chondroitin sulfate A, and hyaluronic acid molecular interactions,” Investigative Ophthalmology and Visual Science, vol. 51, no. 9, pp. 4500–4515, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. G. Despras, C. Bernard, A. Perrot et al., “Toward libraries of biotinylated chondroitin sulfate analogues: from synthesis to in vivo studies,” Chemistry—A European Journal, vol. 19, no. 2, pp. 531–540, 2013. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Van Praag, G. Kempermann, and F. H. Gage, “Neural Consequences of environmental enrichment,” Nature Reviews Neuroscience, vol. 1, no. 3, pp. 191–198, 2000. View at Google Scholar · View at Scopus
  81. J. Nithianantharajah and A. J. Hannan, “Enriched environments, experience-dependent plasticity and disorders of the nervous system,” Nature Reviews Neuroscience, vol. 7, no. 9, pp. 697–709, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Foscarin, D. Ponchione, E. Pajaj et al., “Experience-dependent plasticity and modulation of growth regulatory molecules at central synapses,” PLoS ONE, vol. 6, no. 1, Article ID e16666, 2011. View at Publisher · View at Google Scholar · View at Scopus
  83. S. Gianola and F. Rossi, “GAP-43 overexpression in adult mouse Purkinje cells overrides myelin-derived inhibition of neurite growth,” European Journal of Neuroscience, vol. 19, no. 4, pp. 819–830, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Foscarin, S. Gianola, D. Carulli et al., “Overexpression of GAP-43 modifies the distribution of the receptors for myelin-associated growth-inhibitory proteins in injured Purkinje axons,” European Journal of Neuroscience, vol. 30, no. 10, pp. 1837–1848, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. A. J. G. D. Holtmaat, J. A. Gorter, J. De Wit et al., “Transient downregulation of Sema3A mRNA in a rat model for temporal lobe epilepsy: a novel molecular event potentially contributing to mossy fiber sprouting,” Experimental Neurology, vol. 182, no. 1, pp. 142–150, 2003. View at Publisher · View at Google Scholar · View at Scopus
  86. T. Fukuda, S. Takeda, R. Xu et al., “Sema3A regulates bone-mass accrual through sensory innervations,” Nature, vol. 497, pp. 490–493, 2013. View at Publisher · View at Google Scholar
  87. F. Moret, C. Renaudot, M. Bozon, and V. Castellani, “Semaphorin and neuropilin co-expression in motoneurons sets axon sensitivity to environmental semaphorin sources during motor axon pathfinding,” Development, vol. 134, no. 24, pp. 4491–4501, 2007. View at Publisher · View at Google Scholar · View at Scopus
  88. A. A. Cameron, G. M. Smith, D. C. Randall, D. R. Brown, and A. G. Rabchevsky, “Genetic manipulation of intraspinal plasticity after spinal cord injury alters the severity of autonomic dysreflexia,” Journal of Neuroscience, vol. 26, no. 11, pp. 2923–2932, 2006. View at Publisher · View at Google Scholar · View at Scopus
  89. C.-A. Gutekunst, E. N. Stewart, and R. E. Gross, “Immunohistochemical distribution of PlexinA4 in the adult rat central nervous system,” Frontiers in Neuroanatomy, vol. 4, article 25, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. I. Carcea, A. Ma'ayan, R. Mesias, B. Sepulveda, S. R. Salton, and D. L. Benson, “Flotillin-mediated endocytic events dictate cell type-specific responses to Semaphorin 3A,” The Journal of Neuroscience, vol. 30, no. 45, pp. 15317–15329, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. Shen, A. P. Tenney, S. A. Busch et al., “PTPσ Is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration,” Science, vol. 326, no. 5952, pp. 592–596, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Fisher, B. Xing, J. Dill et al., “Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors,” The Journal of Neuroscience, vol. 31, no. 40, pp. 14051–14066, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. T. L. Dickendesher, K. T. Baldwin, Y. A. Mironova et al., “NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans,” Nature Neuroscience, vol. 15, no. 5, pp. 703–712, 2012. View at Publisher · View at Google Scholar · View at Scopus
  94. T. Pizzorusso, P. Medini, N. Berardi, S. Chierzi, J. W. Fawcett, and L. Maffei, “Reactivation of ocular dominance plasticity in the adult visual cortex,” Science, vol. 298, no. 5596, pp. 1248–1251, 2002. View at Publisher · View at Google Scholar · View at Scopus
  95. T. K. Hensch, “Critical period regulation,” Annual Review of Neuroscience, vol. 27, pp. 549–579, 2004. View at Publisher · View at Google Scholar
  96. D. Carulli, K. E. Rhodes, D. J. Brown et al., “Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components,” Journal of Comparative Neurology, vol. 494, no. 4, pp. 559–577, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. C. M. Galtrey, J. C. F. Kwok, D. Carulli, K. E. Rhodes, and J. W. Fawcett, “Distribution and synthesis of extracellular matrix proteoglycans, hyaluronan, link proteins and tenascin-R in the rat spinal cord,” European Journal of Neuroscience, vol. 27, no. 6, pp. 1373–1390, 2008. View at Publisher · View at Google Scholar · View at Scopus
  98. L. Cnops, T.-T. Hu, K. Burnat, E. Van Der Gucht, and L. Arckens, “Age-dependent alterations in CRMP2 and CRMP4 protein expression profiles in cat visual cortex,” Brain Research, vol. 1088, no. 1, pp. 109–119, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. L. Cnops, T.-T. Hu, U. T. Eysel, and L. Arckens, “Effect of binocular retinal lesions on CRMP2 and CRMP4 but not Dyn I and Syt I expression in adult cat area 17,” European Journal of Neuroscience, vol. 25, no. 5, pp. 1395–1401, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. D. Bagnard, M. Lohrum, D. Uziel, A. W. Püschel, and J. Bolz, “Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections,” Development, vol. 125, no. 24, pp. 5043–5053, 1998. View at Google Scholar · View at Scopus
  101. E. W. Dent, A. M. Barnes, F. Tang, and K. Kalil, “Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton,” The Journal of Neuroscience, vol. 24, no. 12, pp. 3002–3012, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. F. Polleux, R. J. Giger, D. D. Ginty, A. L. Kolodkin, and A. Ghosh, “Patterning of cortical efferent projections by semaphorin-neuropilin interactions,” Science, vol. 282, no. 5395, pp. 1904–1906, 1998. View at Publisher · View at Google Scholar · View at Scopus
  103. B. J. C. Janssen, T. Malinauskas, G. A. Weir, M. Z. Cader, C. Siebold, and E. Y. Jones, “Neuropilins lock secreted semaphorins onto plexins in a ternary signaling complex,” Nature Structural and Molecular Biology, vol. 19, no. 12, pp. 1293–1299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  104. K. Shen and C. W. Cowan, “Guidance molecules in synapse formation and plasticity,” Cold Spring Harbor Perspectives in Biology, vol. 2, no. 4, Article ID a001842, 2010. View at Publisher · View at Google Scholar · View at Scopus
  105. G. Barnes, R. S. Puranam, Y. Luo, and J. O. McNamara, “Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus,” Hippocampus, vol. 13, no. 1, pp. 1–20, 2003. View at Publisher · View at Google Scholar · View at Scopus