About this Journal Submit a Manuscript Table of Contents
Biochemistry Research International
Volume 2012 (2012), Article ID 789083, 8 pages
http://dx.doi.org/10.1155/2012/789083
Review Article

Neural Functions of Matrix Metalloproteinases: Plasticity, Neurogenesis, and Disease

1Department of Cell Biology, Osaka Bioscience Institute, 6-2-4 Furuedai, Suita, Osaka 565-0874, Japan
2Graduate School of Biological Science, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma, Nara 630-0192, Japan

Received 5 October 2011; Revised 8 December 2011; Accepted 29 January 2012

Academic Editor: Sanford I. Bernstein

Copyright © 2012 Hiromi Fujioka 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. L. Sorokin, “The impact of the extracellular matrix on inflammation,” Nature Reviews Immunology, vol. 10, no. 10, pp. 712–723, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Faissner, M. Pyka, M. Geissler et al., “Contributions of astrocytes to synapse formation and maturation—potential functions of the perisynaptic extracellular matrix,” Brain Research Reviews, vol. 63, no. 1-2, pp. 26–38, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. 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
  4. J. Dzwonek, M. Rylski, and L. Kaczmarek, “Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain,” FEBS Letters, vol. 567, no. 1, pp. 129–135, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Page-McCaw, A. J. Ewald, and Z. Werb, “Matrix metalloproteinases and the regulation of tissue remodelling,” Nature Reviews Molecular Cell Biology, vol. 8, no. 3, pp. 221–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. 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 Scopus
  7. A. Pagenstecher, A. K. Stalder, C. L. Kincaid, S. D. Shapiro, and I. L. Campbell, “Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states,” American Journal of Pathology, vol. 152, no. 3, pp. 729–741, 1998. View at Scopus
  8. R. Ulrich, I. Gerhauser, F. Seeliger, W. Baumgärtner, and S. Alldinger, “Matrix metalloproteinases and their inhibitors in the developing mouse brain and spinal cord: a reverse transcription quantitative polymerase chain reaction study,” Developmental Neuroscience, vol. 27, no. 6, pp. 408–418, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. V. W. Yong, C. Power, P. Forsyth, and D. R. Edwards, “Metalloproteinases in biology and pathology of the nervous system,” Nature Reviews Neuroscience, vol. 2, no. 7, pp. 502–511, 2001. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Hu, P. E. Van den Steen, Q. X. A. Sang, and G. Opdenakker, “Matrix metalloproteinase inhibitors as therapy for inflammatory and vascular diseases,” Nature Reviews Drug Discovery, vol. 6, no. 6, pp. 480–498, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. 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 Scopus
  12. P. E. Van Den Steen, B. Dubois, I. Nelissen, P. M. Rudd, R. A. Dwek, and G. Opdenakker, “Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9),” Critical Reviews in Biochemistry and Molecular Biology, vol. 37, no. 6, pp. 375–536, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Page-McCaw, J. Serano, J. M. Santë, and G. M. Rubin, “Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development,” Developmental Cell, vol. 4, no. 1, pp. 95–106, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. C. T. Kuo, L. Y. Jan, and Y. N. Jan, “Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 42, pp. 15230–15235, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. K. I. Yasunaga, T. Kanamori, R. Morikawa, E. Suzuki, and K. Emoto, “Dendrite Reshaping of Adult Drosophila Sensory Neurons Requires Matrix Metalloproteinase-Mediated Modification of the Basement Membranes,” Developmental Cell, vol. 18, no. 4, pp. 621–632, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Dityatev, M. Schachner, and P. Sonderegger, “The dual role of the extracellular matrix in synaptic plasticity and homeostasis,” Nature Reviews Neuroscience, vol. 11, no. 11, pp. 735–746, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. 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 Scopus
  18. S. E. Meighan, P. C. Meighan, P. Choudhury et al., “Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity,” Journal of Neurochemistry, vol. 96, no. 5, pp. 1227–1241, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. X. B. Wang, O. Bozdagi, J. S. Nikitczuk, W. Z. Zu, Q. Zhou, and G. W. Huntley, “Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 49, pp. 19520–19525, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Conant, Y. Wang, A. Szklarczyk, A. Dudak, M. P. Mattson, and S. T. Lim, “Matrix metalloproteinase-dependent shedding of intercellular adhesion molecule-5 occurs with long-term potentiation,” Neuroscience, vol. 166, no. 2, pp. 508–521, 2010. View at Scopus
  21. P. Michaluk, M. Wawrzyniak, P. Alot et al., “Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology,” Journal of Cell Science, vol. 124, no. 19, pp. 3369–3380, 2011. View at Publisher · View at Google Scholar
  22. J. Redondo-Muñoz, E. Ugarte-Berzal, M. J. Terol et al., “Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia B cell survival through its hemopexin domain,” Cancer Cell, vol. 17, no. 2, pp. 160–172, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Gawlak, T. Górkiewicz, A. Gorlewicz, F. A. Konopacki, L. Kaczmarek, and G. M. Wilczynski, “High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses,” Neuroscience, vol. 158, no. 1, pp. 167–176, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Michaluk, L. Mikasova, L. Groc, R. Frischknecht, D. Choquet, and L. Kaczmarek, “Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin β1 signaling,” Journal of Neuroscience, vol. 29, no. 18, pp. 6007–6012, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Frischknecht, M. Heine, D. Perrais, C. I. Seidenbecher, D. Choquet, and E. D. Gundelfinger, “Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity,” Nature Neuroscience, vol. 12, no. 7, pp. 897–904, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Duchossoy, J. C. Horvat, and O. Stettler, “MMP-related gelatinase activity is strongly induced in scar tissue of injured adult spinal cord and forms pathways for ingrowing neurites,” Molecular and Cellular Neuroscience, vol. 17, no. 6, pp. 945–956, 2001. View at Publisher · View at Google Scholar · View at Scopus
  27. V. I. Shubayev and R. R. Myers, “Matrix metalloproteinase-9 promotes nerve growth factor-induced neurite elongation but not new sprout formation in vitro,” Journal of Neuroscience Research, vol. 77, no. 2, pp. 229–239, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. Z. Ahmed, R. G. Dent, W. E. Leadbeater, C. Smith, M. Berry, and A. Logan, “Matrix metalloproteases: degradation of the inhibitory environment of the transected optic nerve and the scar by regenerating axons,” Molecular and Cellular Neuroscience, vol. 28, no. 1, pp. 64–78, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Zuo, D. Neubauer, K. Dyess, T. A. Ferguson, and D. Muir, “Degradation of chondroitin sulfate proteoglycan enhances the neurite- promoting potential of spinal cord tissue,” Experimental Neurology, vol. 154, no. 2, pp. 654–662, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. W. Heine, K. Conant, J. W. Griffin, and A. Höke, “Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves,” Experimental Neurology, vol. 189, no. 2, pp. 231–240, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Siebert, N. Dippel, M. Mäder, F. Weber, and W. Brück, “Matrix metalloproteinase expression and inhibition after sciatic nerve axotomy,” Journal of Neuropathology and Experimental Neurology, vol. 60, no. 1, pp. 85–93, 2001.
  32. L. F. Reichardt and K. J. Tomaselli, “Extracellular matrix molecules and their receptors: functions in neural development,” Annual Review of Neuroscience, vol. 14, pp. 531–570, 1991. View at Scopus
  33. G. S. Marrs, T. Honda, L. Fuller et al., “Dendritic arbors of developing retinal ganglion cells are stabilized by β1-integrins,” Molecular and Cellular Neuroscience, vol. 32, no. 3, pp. 230–241, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. E. M. Y. Moresco, S. Donaldson, A. Williamson, and A. J. Koleske, “Integrin-mediated dendrite branch maintenance requires Abelson (Abl) family kinases,” Journal of Neuroscience, vol. 25, no. 26, pp. 6105–6118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Sekine-Aizawa, E. Hama, K. Watanabe et al., “Matrix metalloproteinase (MMP) system in brain: identification and characterization of brain-specific MMP highly expressed in cerebellum,” European Journal of Neuroscience, vol. 13, no. 5, pp. 935–948, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. 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 Scopus
  37. E. Saygili, P. Schauerte, M. Pekassa et al., “Sympathetic neurons express and secrete MMP-2 and MT1-MMP to control nerve sprouting via pro-NGF conversion,” Cellular and Molecular Neurobiology, vol. 31, pp. 17–25, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. C. M. Miller, N. Liu, A. Page-Mccaw, and H. T. Broihier, “Drosophila Mmp2 regulates the matrix molecule faulty attraction (Frac) to promote motor axon targeting in Drosophila,” Journal of Neuroscience, vol. 31, no. 14, pp. 5335–5347, 2011. View at Publisher · View at Google Scholar
  39. C. M. Miller, A. Page-McCaw, and H. T. Broihier, “Matrix metalloproteinases promote motor axon fasciculation in the Drosophila embryo,” Development, vol. 135, no. 1, pp. 95–109, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. B. Gonthier, E. Koncina, S. Satkauskas et al., “A PKC-dependent recruitment of MMP-2 controls semaphorin-3A growth-promoting effect in cortical dendrites,” PLoS One, vol. 4, no. 4, Article ID e5099, 2009. View at Publisher · View at Google Scholar · View at Scopus
  41. G. M. Wilczynski, F. A. Konopacki, E. Wilczek et al., “Important role of matrix metalloproteinase 9 in epileptogenesis,” Journal of Cell Biology, vol. 180, no. 5, pp. 1021–1035, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. P. Frölichsthal-Schoeller, A. L. Vescovi, C. A. Krekoski, G. Murphy, D. R. Edwards, and P. Forsyth, “Expression and modulation of matrix metalloproteinase-2 and tissue inhibitors of metalloproteinases in human embryonic CNS stem cells,” NeuroReport, vol. 10, no. 2, pp. 345–351, 1999. View at Scopus
  43. L. Wójcik-Stanaszek, J. Sypecka, P. Szymczak et al., “The potential role of metalloproteinases in neurogenesis in the gerbil hippocampus following global forebrain ischemia,” PLoS ONE, vol. 6, no. 7, Article ID e22465, 2011. View at Publisher · View at Google Scholar
  44. D. C. Morris, Z. G. Zhang, R. Zhang, Y. LeTourrneau, S. R. Gregg, and M. Chopp, “Stroke increases expression of matrix metalloproteinases and P21-activeted protein kinase in neural progenitor cells,” Academic Emergency Medicine, vol. 13, p. S194, 2006.
  45. L. Lu, A. B. Tonchev, D. B. Kaplamadzhiev et al., “Expression of matrix metalloproteinases in the neurogenic niche of the adult monkey hippocampus after ischemia,” Hippocampus, vol. 18, no. 10, pp. 1074–1084, 2008. View at Publisher · View at Google Scholar
  46. D. W. Williams and J. W. Truman, “Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons,” Development, vol. 132, no. 16, pp. 3631–3642, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. K. Emoto, Y. He, B. Ye et al., “Control of dendritic branching and tiling by the tricornered-kinase/furry signaling pathway in Drosophila sensory neurons,” Cell, vol. 119, no. 2, pp. 245–256, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Emoto, J. Z. Parrish, L. Y. Jan, and Y. N. Jan, “The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance,” Nature, vol. 443, no. 7108, pp. 210–213, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Koike-Kumagai, K. I. Yasunaga, R. Morikawa, T. Kanamori, and K. Emoto, “The target of rapamycin complex 2 controls dendritic tiling of Drosophila sensory neurons through the Tricornered kinase signalling pathway,” EMBO Journal, vol. 28, no. 24, pp. 3879–3892, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Kaneko, K. Yamaguchi, M. Eiraku et al., “Remodeling of monoplanar purkinje cell dendrites during cerebellar circuit formation,” PLoS One, vol. 6, no. 5, Article ID e20108, 2011. View at Publisher · View at Google Scholar
  51. J. E. A. Wells, R. J. Hurlbert, M. G. Fehlings, and V. W. Yong, “Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice,” Brain, vol. 126, no. 7, pp. 1628–1637, 2003. View at Scopus
  52. A. Weaver, A. Goncalves Da Silva, R. K. Nuttall et al., “An elevated matrix metalloproteinase (MMP) in an animal model of multiple sclerosis is protective by affecting Th1/Th2 polarization,” FASEB Journal, vol. 19, no. 12, pp. 1668–1670, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. N. Suenaga, T. Ichiyama, M. Kubota, H. Isumi, J. Tohyama, and S. Furukawa, “Roles of matrix metalloproteinase-9 and tissue inhibitors of metalloproteinases 1 in acute encephalopathy following prolonged febrile seizures,” Journal of the Neurological Sciences, vol. 266, no. 1-2, pp. 126–130, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. F. A. Konopacki, M. Rylski, E. Wilczek et al., “Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA,” Neuroscience, vol. 150, no. 1, pp. 31–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Dubois, S. Masure, U. Hurtenbach et al., “Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions,” Journal of Clinical Investigation, vol. 104, no. 11, pp. 1507–1515, 1999. View at Scopus
  56. L. J. Noble, F. Donovan, T. Igarashi, S. Goussev, and Z. Werb, “Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events,” Journal of Neuroscience, vol. 22, no. 17, pp. 7526–7535, 2002. View at Scopus
  57. J. Esparza, M. Kruse, J. Lee, M. Michaud, and J. A. Madri, “MMP-2 null mice exhibit an early onset and severe experimental autoimmune encephalomyelitis due to an increase in MMP-9 expression and activity,” FASEB Journal, vol. 18, no. 14, pp. 1682–1691, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. A. G. DaSilva and V. W. Yong, “Matrix metalloproteinase-12 deficiency worsens relapsing-remitting experimental autoimmune encephalomyelitis in association with cytokine and chemokine dysregulation,” American Journal of Pathology, vol. 174, no. 3, pp. 898–909, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. S. Agrawal, P. Anderson, M. Durbeej et al., “Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis,” Journal of Experimental Medicine, vol. 203, no. 4, pp. 1007–1019, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. D. C. Mash, J. ffrench-Mullen, N. Adi, Y. Qin, A. Buck, and J. Pablo, “Gene expression in human hippocampus from cocaine abusers identifies genes which regulate extracellular matrix remodeling,” PLoS ONE, vol. 2, no. 11, Article ID e1187, p. e1187, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. T. E. Brown, M. R. Forquer, J. W. Harding, J. W. Wright, and B. A. Sorg, “Increase in matrix metalloproteinase-9 levels in the rat medial prefrontal cortex after cocaine reinstatement of conditioned place preference,” Synapse, vol. 62, no. 12, pp. 886–889, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Mizoguchi, K. Yamada, M. Niwa et al., “Reduction of methamphetamine-induced sensitization and reward in matrix metalloproteinase-2 and -9-deficient mice,” Journal of Neurochemistry, vol. 100, no. 6, pp. 1579–1588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Liu, S. Brown, J. Shaikh, J. A. Fishback, and R. R. Matsumoto, “Relationship between methamphetamine exposure and matrix metalloproteinase 9 expression,” NeuroReport, vol. 19, no. 14, pp. 1407–1409, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. Y. Kawasaki, Z. Z. Xu, X. Wang et al., “Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain,” Nature Medicine, vol. 14, no. 3, pp. 331–336, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. J. P. Miller, J. Holcomb, I. Al-Ramahi et al., “Matrix metalloproteinases are modifiers of huntingtin proteolysis and toxicity in Huntington's disease,” Neuron, vol. 67, no. 2, pp. 199–212, 2010. View at Publisher · View at Google Scholar · View at Scopus