Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2011, Article ID 859359, 17 pages
http://dx.doi.org/10.1155/2011/859359
Research Article

Deafferentation-Induced Redistribution of MMP-2, but Not of MMP-9, Depends on the Emergence of GAP-43 Positive Axons in the Adult Rat Cochlear Nucleus

Neurobiological Research Laboratory, Department of Otorhinolaryngology, University of Freiburg, Killianst. 5, D-79106 Freiburg, Germany

Received 29 April 2011; Accepted 17 August 2011

Academic Editor: Sarah McFarlane

Copyright © 2011 Michaela Fredrich and Robert-Benjamin Illing. 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. E. C. Kane, “Patterns of degeneration in the caudal cochlear nucleus of the cat after cochlear ablation,” Anatomical Record, vol. 179, no. 1, pp. 67–92, 1974. View at Google Scholar · View at Scopus
  2. D. L. Oliver, S. J. Potashner, D. R. Jones, and D. K. Morest, “Selective labeling of spiral ganglion and granule cells with D-asparatate in the auditory system of cat and guinea pig,” Journal of Neuroscience, vol. 3, no. 3, pp. 455–472, 1983. View at Google Scholar · View at Scopus
  3. R. A. Altschuler, C. E. Sheridan, J. W. Horn, and R. J. Wenthold, “Immunocytochemical localization of glutamate immunoreactivity in the guinea pig cochlea,” Hearing Research, vol. 42, no. 2-3, pp. 167–174, 1989. View at Google Scholar · View at Scopus
  4. R.-B. Illing, M. Horváth, and R. Laszig, “Plasticity of the auditory brainstem: effects of cochlear ablation on GAP-43 immunoreactivity in the rat,” Journal of Comparative Neurology, vol. 382, no. 1, pp. 116–138, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. R.-B. Illing, K. S. Kraus, and M. A. Meidinger, “Reconnecting neuronal networks in the auditory brainstem following unilateral deafening,” Hearing Research, vol. 206, no. 1-2, pp. 185–199, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. L. I. Benowitz and A. Routtenberg, “GAP-43: an intrinsic determinant of neuronal development and plasticity,” Trends in Neurosciences, vol. 20, no. 2, pp. 84–91, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Horváth, C. R. Förster, and R.-B. Illing, “Postnatal development of GAP-43 immunoreactivity in the auditory brainstem of the rat,” Journal of Comparative Neurology, vol. 382, no. 1, pp. 104–115, 1997. View at Publisher · View at Google Scholar · View at Scopus
  8. S. M. de la Monte, H. J. Federoff, S. C. Ng, E. Grabczyk, and M. C. Fishman, “GAP-43 gene expression during development: persistence in a distinctive set of neurons in the mature central nervous system,” Developmental Brain Research, vol. 46, no. 2, pp. 161–168, 1989. View at Google Scholar · View at Scopus
  9. R.-B. Illing and M. Horváth, “Re-emergence of GAP-43 in cochlear nucleus and superior olive following cochlear ablation in the rat,” Neuroscience Letters, vol. 194, no. 1-2, pp. 9–12, 1995. View at Publisher · View at Google Scholar · View at Scopus
  10. M. A. Meidinger, H. Hildebrandt-Schoenfeld, and R.-B. Illing, “Cochlear damage induces GAP-43 expression in cholinergic synapses of the cochlear nucleus in the adult rat: a light and electron microscopic study,” European Journal of Neuroscience, vol. 23, no. 12, pp. 3187–3199, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. R.-B. Illing, N. Rosskothen-Kuhl, M. Fredrich, H. Hildebrandt, and A. C. Zeber, “Imaging the plasticity of the central auditory system on the cellular and molecular level,” Audiological Medicine, vol. 8, no. 2, pp. 63–76, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. K. S. Kraus and R.-B. Illing, “Superior olivary contributions to auditory system plasticity: medial but not lateral olivocochlear neurons are the source of cochleotomy-induced GAP-43 expression in the ventral cochlear nucleus,” Journal of Comparative Neurology, vol. 475, no. 3, pp. 374–390, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. J. S. White and W. B. Warr, “The dual origins of the olivocochlear bundle in the albino rat,” Journal of Comparative Neurology, vol. 219, no. 2, pp. 203–214, 1983. View at Google Scholar · View at Scopus
  14. M. C. Brown, S. Pierce, and A. M. Berglund, “Cochlear-nucleus branches of thick (medial) olivocochlear fibers in the mouse: a cochleotopic projection,” Journal of Comparative Neurology, vol. 303, no. 2, pp. 300–315, 1991. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  15. M. Horváth, K. S. Kraus, and R.-B. Illing, “Olivocochlear neurons sending axon collaterals into the ventral cochlear nucleus of the rat,” Journal of Comparative Neurology, vol. 422, no. 1, pp. 95–105, 2000. View at Google Scholar · View at Scopus
  16. M. C. Brown, M. C. Liberman, T. E. Benson, and D. K. Ryugo, “Brainstem branches from olivocochlear axons in cats and rodents,” Journal of Comparative Neurology, vol. 278, no. 4, pp. 591–603, 1988. View at Google Scholar · View at Scopus
  17. A. F. Ryan, E. M. Keithley, Z. X. Wang, and I. R. Schwartz, “Collaterals from lateral and medial olivocochlear efferent neurons innervate different regions of the cochlear nucleus and adjacent brainstem,” Journal of Comparative Neurology, vol. 300, no. 4, pp. 572–582, 1990. View at Google Scholar · View at Scopus
  18. P. Michaluk and L. Kaczmarek, “Matrix metalloproteinase-9 in glutamate-dependent adult brain function and dysfunction,” Cell Death and Differentiation, vol. 14, no. 7, pp. 1255–1258, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. D. Amantea, M. T. Corasaniti, N. B. Mercuri, G. Bernardi, and G. Bagetta, “Brain regional and cellular localization of gelatinase activity in rat that have undergone transient middle cerebral artery occlusion,” Neuroscience, vol. 152, no. 1, pp. 8–17, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. Y. Yang, E. Candelario-Jalil, J. F. Thompson et al., “Increased intranuclear matrix metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia,” Journal of Neurochemistry, vol. 112, no. 1, pp. 134–149, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. V. W. Yong, “Metalloproteinases: mediators of pathology and regeneration in the CNS,” Nature Reviews Neuroscience, vol. 6, no. 12, pp. 931–944, 2005. View at Publisher · View at Google Scholar · View at PubMed
  22. E. A. Milward, C. Fitzsimmons, A. Szklarczyk, and K. Conant, “The matrix metalloproteinases and CNS plasticity: an overview,” Journal of Neuroimmunology, vol. 187, no. 1-2, pp. 9–19, 2007. View at Publisher · View at Google Scholar · View at PubMed
  23. M. A. Pizzi and M. J. Crowe, “Matrix metalloproteinases and proteoglycans in axonal regeneration,” Experimental Neurology, vol. 204, no. 2, pp. 496–511, 2007. View at Publisher · View at Google Scholar · View at PubMed
  24. M. D. Sternlicht and Z. Werb, “How matrix metalloproteinases regulate cell behavior,” Annual Review of Cell and Developmental Biology, vol. 17, no. 1, pp. 463–516, 2001. View at Publisher · View at Google Scholar · View at PubMed
  25. I. M. Ethell and D. W. Ethell, “Matrix metalloproteinases in brain development and remodeling: synaptic functions and targets,” Journal of Neuroscience Research, vol. 85, no. 13, pp. 2813–2823, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. M. Fredrich and R.-B. Illing, “MMP-2 is involved in synaptic remodeling after cochlear lesion,” NeuroReport, vol. 21, no. 5, pp. 324–327, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. S. Rivera, C. Ogier, J. Jourquin et al., “Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with neuronal death and glial reactivity after global forebrain ischemia,” European Journal of Neuroscience, vol. 15, no. 1, pp. 19–32, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. R. M. Costanzo, L. A. Perrino, and M. Kobayashi, “Response of matrix metalloproteinase-9 to olfactory nerve injury,” NeuroReport, vol. 17, no. 17, pp. 1787–1791, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. H. S. Ranasinghe, C. E. Williams, L. J. Christophidis, M. D. Mitchell, M. Fraser, and A. Scheepens, “Proteolytic activity during cortical development is distinct from that involved in hypoxic ischemic injury,” Neuroscience, vol. 158, no. 2, pp. 732–744, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. J. Y. C. Hsu, L. Y. W. Bourguignon, C. M. Adams et al., “Matrix metalloproteinase-9 facilitates glial scar formation in the injured spinal cord,” Journal of Neuroscience, vol. 28, no. 50, pp. 13467–13477, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, Academic Press, New York, NY, USA, 1986.
  32. T. Gentschev and C. Sotelo, “Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultrastructural study,” Brain Research, vol. 62, no. 1, pp. 37–60, 1973. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Szklarczyk, J. Lapinska, M. Rylski, R. D. G. McKay, and L. Kaczmarek, “Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus,” Journal of Neuroscience, vol. 22, no. 3, pp. 920–930, 2002. View at Google Scholar · View at Scopus
  34. V. Nagy, O. Bozdagi, A. Matynia et al., “Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory,” Journal of Neuroscience, vol. 26, no. 7, pp. 1923–1934, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  35. O. Bozdagi, V. Nagy, K. T. Kwei, and G. W. Huntley, “In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity,” Journal of Neurophysiology, vol. 98, no. 1, pp. 334–344, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. P. Oliveira-Silva, P. B. Jurgilas, P. Trindade et al., “Matrix metalloproteinase-9 is involved in the development and plasticity of retinotectal projections in rats,” NeuroImmunoModulation, vol. 14, no. 3-4, pp. 144–149, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. J. R. Gaddy, M. D. Britt, D. B. Neill, and H. J. Haigler, “Susceptibility of rat neostriatum to damage by kainic acid: age dependence,” Brain Research, vol. 176, no. 1, pp. 192–196, 1979. View at Google Scholar · View at Scopus
  38. K. M. Spangler, N. B. Cant, C. K. Henkel, G. R. Farley, and W. B. Warr, “Descending projections from the superior olivary complex to the cochlear nucleus of the cat,” Journal of Comparative Neurology, vol. 259, no. 3, pp. 452–465, 1987. View at Google Scholar · View at Scopus
  39. T. M. Reeves, M. L. Prins, J. Zhu, J. T. Povlishock, and L. L. Phillips, “Matrix metalloproteinase inhibition alters functional and structural correlates of deafferentation-induced sprouting in the dentate gyrus,” Journal of Neuroscience, vol. 23, no. 32, pp. 10182–10189, 2003. View at Google Scholar · View at Scopus
  40. X. Zhang, M. Cheng, and S. K. Chintala, “Kainic acid-mediated upregulation of matrix metalloproteinase-9 promotes retinal degeneration,” Investigative Ophthalmology and Visual Science, vol. 45, no. 7, pp. 2374–2383, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. C. A. Webber, J. C. Hocking, V. W. Yong, C. L. Stange, and S. McFarlane, “Metalloproteases and guidance of retinal axons in the developing visual system,” Journal of Neuroscience, vol. 22, no. 18, pp. 8091–8100, 2002. View at Google Scholar · View at Scopus
  42. J. Zuo, T. A. Ferguson, Y. J. Hernandez, W. G. Stetler-Stevenson, and D. Muir, “Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite- inhibiting chondroitin sulfate proteoglycan,” Journal of Neuroscience, vol. 18, no. 14, pp. 5203–5211, 1998. View at Google Scholar · View at Scopus
  43. M. J. Galko and M. Tessier-Lavigne, “Function of an axonal chemoattractant modulated by metalloprotease activity,” Science, vol. 289, no. 5483, pp. 1365–1367, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Hattori, M. Osterfield, and J. G. Flanagan, “Regulated cleavage of a contact-mediated axon repellent,” Science, vol. 289, no. 5483, pp. 1360–1365, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. K. M. Thrailkill, L. D. Quarles, H. Nagase, K. Suzuki, D. M. Serra, and J. L. Fowlkes, “Characterization of insulin-like growth factor-binding protein 5-degrading proteases produced throughout murine osteoblast differentiation,” Endocrinology, vol. 136, no. 8, pp. 3527–3533, 1995. View at Google Scholar · View at Scopus
  46. H. Nakamura, Y. Fujii, I. Inoki et al., “Brevican is degraded by matrix metalloproteinases and aggrecanase-1 (ADAMTS4) at different sites,” Journal of Biological Chemistry, vol. 275, no. 49, pp. 38885–38890, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. A. J. H. Gearing, P. Beckett, M. Christodoulou et al., “Processing of tumour necrosis factor-α precursor by metalloproteinases,” Nature, vol. 370, no. 6490, pp. 555–557, 1994. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. J. H. Jung, M. H. Park, S. Y. Choi, and J. Y. Koh, “Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases,” Journal of Biological Chemistry, vol. 280, no. 12, pp. 11995–12001, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. H. Hildebrandt, N. A. Hoffmann, and R.-B. Illing, “Synaptic reorganization in the adult rat's ventral cochlear nucleus following its total sensory deafferentation,” PLoS ONE, vol. 6, no. 8, Article ID e23686, pp. 1–13, 2011. View at Publisher · View at Google Scholar · View at PubMed
  50. 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 PubMed · View at Scopus
  51. 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 PubMed · View at Scopus
  52. N. B. Cant and C. G. Benson, “Wisteria floribunda lectin is associated with specific cell types in the ventral cochlear nucleus of the gerbil, Meriones unguiculatus,” Hearing Research, vol. 216-217, pp. 64–72, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. H. Hilbig, S. Nowack, K. Boeckler, H.-J. Bidmon, and K. Zilles, “Characterization of neuronal subsets surrounded by perineuronal nets in the rhesus auditory brainstem,” Journal of Anatomy, vol. 210, no. 5, pp. 507–517, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. J. L. Wagoner and R. J. Kulesza Jr., “Topographical and cellular distribution of perineuronal nets in the human cochlear nucleus,” Hearing Research, vol. 254, no. 1-2, pp. 42–53, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. 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, pp. 1–14, 2011. View at Publisher · View at Google Scholar · View at PubMed