Metalloproteinases: Mediators of pathology and regeneration in the CNS

Nature Reviews Neuroscience

Volumn 6, Issue 12, 2005, Pages 931-944

  Yong, V Wee ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; DISINTEGRIN; EPIDERMAL GROWTH FACTOR; INTERLEUKIN 1BETA; INTERSTITIAL COLLAGENASE; METALLOPROTEINASE; RIBONUCLEASE; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME;

ALLERGIC ENCEPHALOMYELITIS; ANOIKIS; DISEASE SEVERITY; ENZYME ACTIVE SITE; GENETIC LINKAGE; LIPID BILAYER; MYELINATED NERVE; MYELINATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE GROWTH; NERVE INJURY; NERVOUS SYSTEM DEVELOPMENT; NEUROPATHOLOGY; NONHUMAN; OPTIC NERVE LESION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS; UPREGULATION; ZYMOGRAPHY;

ANIMALS; CENTRAL NERVOUS SYSTEM DISEASES; HUMANS; METALLOPROTEASES; MODELS, BIOLOGICAL; MYELIN SHEATH; NERVE REGENERATION;

EID: 28644435880     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1807     Document Type: Review

References (122)

1. Sternlicht, M. D. & Werb, Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516 (2001). A very thorough review on the many roles of metalloproteinases.
2. 1, integrin upon release from keratinocytes migrating on type I collagen. J. Biol. Chem. 276, 29368-29374 (2001).
3. Yu, W. H., Woessner, J. F. Jr, McNeish, J. D. & Stamenkovic, I. CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling. Genes Dev. 16, 307-323 (2002).
4. Mott, J. D. & Werb, Z. Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 16, 558-564 (2004).
5. McCawley, L. J. & Matrisian, L. M. Matrix metalloproteinases: they're not just for matrix anymore! Curr. Opin. Cell Biol. 13, 534-540 (2001).
6. Parks, W. C., Wilson, C. L. & Lopez-Boado, Y. S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nature Rev. Immunol. 4, 617-629 (2004). This review introduces many aspects of MMPs and links the fields of inflammation and metalloproteinase biology in a cohesive manner.
7. Overall, C. M. & Lopez-Otin, C. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nature Rev. Cancer 2, 657-672 (2002).
8. White, J. M. ADAMs: modulators of cell-cell and cell-matrix interactions. Curr. Opin. Cell Biol. 15, 598-606 (2003).
9. Blobel, C. P. ADAMs: key components in EGFR signalling and development. Nature Rev. Mol. Cell Biol. 6, 32-43 (2005). This review considers several aspects of protein ectodomain shedding and discusses several mechanistic aspects of metalloproteinase biology.
10. Murphy, G. et al. Role of TIMPs (tissue inhibitors of metalloproteinases) in pericellular proteolysis: the specificity is in the detail. Biochem. Soc. Symp. 70, 65-80 (2003).
11. Baker, A. H., Edwards, D. R. & Murphy, G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J. Cell Sci. 115, 3719-3727 (2002).
12. Porter, S., Clark, I. M., Kevorkian, L. & Edwards, D. R. The ADAMTS metalloproteinases. Biochem. J. 386, 15-27 (2005).
13. Brundula, V., Rewcastle, N. B., Metz, L. M., Bernard, C. C. & Yong, V. W. Targeting leukocyte MMPs and transmigration: minocycline as a potential therapy for multiple sclerosis. Brain 125, 1297-1308 (2002).
14. Weaver, A. et al. An elevated matrix metalloproteinase in experimental autoimmune encephalomyelitis is protective by affecting Th1/Th2 polarization. FASEB J. 19, 1668-1670 (2005).
15. Karkkainen, I., Rybnikova, E., Pelto-Huikko, M. & Huovila, A. P. Metalloprotease-disintegrin (ADAM) genes are widely and differentially expressed in the adult CNS. Mol. Cell. Neurosci. 15, 547-560 (2000). The first article to emphasize that several metalloproteinases, particularly those of the ADAM family, are found in the CNS.
16. Yong, V. W., Power, C., Forsyth, P. & Edwards, D. R. Metalloproteinases in biology and pathology of the nervous system. Nature Rev. Neurosci. 2, 502-511 (2001). Contains a comprehensive list of the detrimental roles of metalloproteinases in the nervous system, and summarizes the roles of metalloproteinases in several neurological diseases.
17. Lo, E. H., Wang, X. & Cuzner, M. L. Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases. J. Neurosci. Res. 69, 1-9 (2002).
18. Cunningham, L. A., Wetzel, M. & Rosenberg, G. A. Multiple roles for MMPs and TIMPs in cerebral ischemia. Glia 50, 329-339 (2005).
19. Wells, J. E., Hurlbert, R. J., Fehlings, M. G. & Yong, V. W. Neuroprotection by minocycline facilitates significant recovery from spinal cord injury in mice. Brain 126, 1628-1637 (2003).
20. Toft-Hansen, H., Nuttall, R. K., Edwards, D. R. & Owens, T. Key metalloproteinases are expressed by specific cell types in experimental autoimmune encephalomyelitis. J. Immunol. 173, 5209-5218 (2004).
21. Bar-Or, A. et al. Analyses of all matrix metalloproteinase members in leukocytes emphasize monocytes as major inflammatory mediators in multiple sclerosis. Brain 126, 2738-2749 (2003).
22. Power, C. et al. Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann. Neurol. 53, 731-742 (2003).
23. Wells, J. E. et al. An adverse role for matrix metalloproteinase 12 after spinal cord injury in mice. J. Neurosci. 23, 10107-10115 (2003).
24. Opdenakker, G. et al. Gelatinase B functions as regulator and effector in leukocyte biology. J. Leukoc. Biol. 69, 851-859 (2001).
25. Noble, L. J., Donovan, F., Igarashi, T., Goussev, S. & Werb, Z. Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 22, 7526-7535 (2002).
26. Larsen, P. H., Wells, J. E., Stallcup, W. B., Opdenakker, G. & Yong, V. W. Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J. Neurosci. 23, 11127-11135 (2003). The first report to emphasize that some MMPs, which are upregulated after injuries to the adult CNS, can have beneficial functions.
27. Esparza, J., Kruse, M., Lee, J., Michaud, M. & Madri, J. A. MMP-2 null mice exhibit an early onset and severe experimental autoimmune encephalomyelitis due to an increase in MMP-9 expression and activity. FASEB J. 18, 1682-1691 (2004).
28. Waubant, E. et al. Serum MMP-9 and TIMP-1 levels are related to MRI activity in relapsing multiple sclerosis. Neurology 53, 1397-1401 (1999).
29. Correale, J. & de los Milagros Bassani Molinas, M. Temporal variations of adhesion molecules and matrix metalloproteinases in the course of MS. J. Neuroimmunol. 140, 198-209 (2003).
30. Fiotti, N. et al. MMP-9 microsatellite polymorphism and multiple sclerosis. J. Neuroimmunol. 152, 147-153 (2004).
31. Kieseier, B. C., Pischel, H., Neuen-Jacob, E., Tourtellotte, W. W. & Hartung, H. P. ADAM-10 and ADAM-17 in the inflamed human CNS. Glia 42, 398-405 (2003).
32. Goertsches, R., Comabella, M., Navarro, A., Perkal, H. & Montalban, X. Genetic association between polymorphisms in the ADAMTS14 gene and multiple sclerosis. J. Neuroimmunol. 164, 140-147 (2005).
33. Pagenstecher, A., Stalder, A. K., Kincaid, C. L., Shapiro, S. D. & Campbell, I. L. Differential expression of matrix metalloproteinase and tissue inhibitor of matrix metalloproteinase genes in the mouse central nervous system in normal and inflammatory states. Am. J. Pathol. 152, 729-741 (1998).
34. Gottschall, P. E. & Deb, S. Regulation of matrix metalloproteinase expressions in astrocytes, microglia and neurons. Neuroimmunomodulation 3, 69-75 (1996).
35. Vecil, G. G. et al. Interleukin-1 is a key regulator of matrix metalloproteinase-9 expression in human neurons in culture and following mouse brain trauma in vivo. J. Neurosci. Res. 61, 212-224 (2000).
36. Le, D. M. et al. Exploitation of astrocytes by glioma cells to facilitate invasiveness: a mechanism involving matrix metalloproteinase-2 and the urokinase-type plasminogen activator-plasmin cascade. J. Neurosci. 23, 4034-4043 (2003).
37. Rosenberg, G. A. et al. Immunohistochemistry of matrix metalloproteinases in reperfusion injury to rat brain: activation of MMP-9 linked to stromelysin-1 and microglia in cell cultures. Brain Res. 893, 104-112 (2001).
38. Gu, Z. et al. S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190 (2002). Reveals a mechanism by which metalloproteinases regulate cell death.
39. McQuibban, G. A. et al. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 289, 1202-1206 (2000).
40. Van den Steen, P. E., Proost, P., Wuyts, A., Van Damme, J. & Opdenakker, G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by aminoterminal processing, whereas it degrades CTAP-III, PF-4, and GRO-α and leaves RANTES and MCP-2 intact. Blood 96, 2673-2681 (2000).
41. Li, Q., Park, P. W., Wilson, C. L. & Parks, W. C. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111, 635-646 (2002).
42. Zhang, K. et al. HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration. Nature Neurosci. 6, 1064-1071 (2003).
43. Anthony, D. C. et al. Matrix metalloproteinase expression in an experimentally-induced DTH model of multiple sclerosis in the rat CNS. J. Neuroimmunol. 87, 62-72 (1998).
44. Newman, T. A. et al. T-cell- and macrophage-mediated axon damage in the absence of a CNS-specific immune response: involvement of metalloproteinases. Brain 124, 2203-2214 (2001).
45. Proost, P., Van Damme, J. & Opdenakker, G. Leukocyte gelatinase B cleavage releases encephalitogens from human myelin basic protein. Biochem. Biophys. Res. Commun. 192, 1175-1181 (1993).
46. Ito, A. et al. Degradation of interleukin 1β by matrix metalloproteinases. J. Biol. Chem. 271, 14657-14660 (1996).
47. Zalewska, T., Ziemka-Nalecz, M., Sarnowska, A. & Domanska-Janik, K. Involvement of MMPs in delayed neuronal death after global ischemia. Acta Neurobiol. Exp. (Wars.) 62, 53-61 (2002).
48. Bridges, L. C. & Bowditch, R. D. ADAM-integrin interactions: potential integrin regulated ectodomain shedding activity. Curr. Pharm. Des. 11, 837-847 (2005).
49. Chintala, S. K., Zhang, X., Austin, J. S. & Fini, M. E. Deficiency in matrix metalloproteinase gelatinase B (MMP-9) protects against retinal ganglion cell death after optic nerve ligation. J. Biol. Chem. 277, 47461-47468 (2002).
50. Jourquin, J. et al. Neuronal activity-dependent increase of net matrix metalloproteinase activity is associated with MMP-9 neurotoxicity after kainate. Eur. J. Neurosci. 18, 1507-1517 (2003).
51. Zhang, X., Cheng, M. & Chintala, S. K. Kainic acid-mediated upregulation of matrix metalloproteinase-9 promotes retinal degeneration. Invest. Ophthalmol. Vis. Sci. 45, 2374-2383 (2004).
52. Vos, C. M. et al. Cytotoxicity by matrix metalloprotease-1 in organotypic spinal cord and dissociated neuronal cultures. Exp. Neurol. 163, 324-330 (2000).
53. Conant, K. et al. Matrix metalloproteinase 1 interacts with neuronal integrins and stimulates dephosphorylation of Akt. J. Biol. Chem. 279, 8056-8062 (2004).
54. Frolichsthal-Schoeller, P. et al. Expression and modulation of matrix metalloproteinase-2 and tissue inhibitors of metalloproteinases in human embryonic CNS stem cells. Neuroreport 10, 345-351 (1999).
55. Heine, W., Conant, K., Griffin, J. W. & Hoke, A. Transplanted neural stem cells promote axonal regeneration through chronically denervated peripheral nerves. Exp. Neurol. 189, 231-240 (2004).
56. Jaworski, D. M. & Fager, N. Regulation of tissue inhibitor of metalloproteinase-3 (Timp-3) mRNA expression during rat CNS development. J. Neurosci. Res. 61, 396-408 (2000).
57. Perez-Martinez, L. & Jaworski, D. M. Tissue inhibitor of metalloproteinase-2 promotes neuronal differentiation by acting as an anti-mitogenic signal. J. Neurosci. 25, 4917-4929 (2005).
58. Alfandari, D. et al. Xenopus ADAM 13 is a metalloprotease required for cranial neural crest-cell migration. Curr. Biol. 11, 918-930 (2001).
59. Vaillant, C. et al. MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol. Cell. Neurosci. 24, 395-408 (2003).
60. Ayoub, A. E., Cai, T. Q., Kaplan, R. A. & Luo, J. Developmental expression of matrix metalloproteinases 2 and 9 and their potential role in the histogenesis of the cerebellar cortex. J. Comp. Neurol. 481, 403-415 (2005).
61. Schlondorff, J. & Blobel, C. P. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding. J. Cell Sci. 112, 3603-3617 (1999).
62. Baron, W., Colognato, H. & ffrench-Constant, C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia 49, 467-479 (2005).
63. Xian, C. J. & Zhou, X. F. EGF family of growth factors: essential roles and functional redundancy in the nerve system. Front. Biosci. 9, 85-92 (2004).
64. Sheffield, J. B., Krasnopolsky, V. & Dehlinger, E. Inhibition of retinal growth cone activity by specific metalloproteinase inhibitors in vitro. Dev. Dyn. 200, 79-88 (1994).
65. Machida, C. M., Rodland, K. D., Matrisian, L., Magun, B. E. & Ciment, G. NGF induction of the gene encoding the protease transin accompanies neuronal differentiation in PC12 cells. Neuron 2, 1587-1596 (1989).
66. Nordstrom, L. A., Lochner, J., Yeung, W. & Ciment, G. The metalloproteinase stromelysin-1 (transin) mediates PC12 cell growth cone invasiveness through basal laminae. Mol. Cell. Neurosci. 6, 56-68 (1995).
67. Hayashita-Kinoh, H. et al. Membrane-type 5 matrix metalloproteinase is expressed in differentiated neurons and regulates axonal growth. Cell Growth Differ. 12, 573-580 (2001).
68. Sekine-Aizawa, Y. et al. Matrix metalloproteinase (MMP) system in brain: identification and characterization of brain-specific MMP highly expressed in cerebellum. Eur. J. Neurosci. 13, 935-948 (2001).
69. Weeks, B. S., Nomizu, M., Ramchandran, R. S., Yamada, Y. & Kleinman, H. K. Laminin-1 and the RKRLQVQLSIRT laminin-1 α1 globular domain peptide stimulate matrix metalloproteinase secretion by PC12 cells. Exp. Cell Res. 243, 375-382 (1998).
70. Fambrough, D., Pan, D., Rubin, G. M. & Goodman, C. S. The cell surface metalloprotease/disintegrin Kuzbanian is required for axonal extension in Drosophila. Proc. Natl Acad. Sci. USA 93, 13233-13238 (1996).
71. Leighton, P. A. et al. Defining brain wiring patterns and mechanisms through gene trapping in mice. Nature 410, 174-179 (2001).
72. Mitchell, K. J. et al. Functional analysis of secreted and transmembrane proteins critical to mouse development. Nature Genet. 28, 241-249 (2001).
73. Goldsmith, A. P., Gossage, S. J. & ffrench-Constant, C. ADAM23 is a cell-surface glycoprotein expressed by central nervous system neurons. J. Neurosci. Res. 78, 647-658 (2004).
74. Webber, C. A., Hocking, J. C., Yong, V. W., Stange, C. L. & McFarlane, S. Metalloproteases and guidance of retinal axons in the developing visual system. J. Neurosci. 22, 8091-8100 (2002). The first report to demonstrate that the inhibition of metalloproteinases in vivo affects axonal guidance and growth.
75. Hattori, M., Osterfield, M. & Flanagan, J. G. Regulated cleavage of a contact-mediated axon repellent. Science 289, 1360-1365 (2000). Using in vitro systems, the authors showed a role for metalloproteinases in axonal guidance.
76. Galko, M. J. & Tessier-Lavigne, M. Function of an axonal chemoattractant modulated by metalloprotease activity. Science 289, 1365-1367 (2000).
77. Schimmelpfeng, K., Gogel, S. & Klambt, C. The function of leak and kuzbanian during growth cone and cell migration. Mech. Dev. 106, 25-36 (2001).
78. Huang, X., Huang, P., Robinson, M. K., Stern, M. J. & Jin, Y. UNC-71, a disintegrin and metalloprotease (ADAM) protein, regulates motor axon guidance and sex myoblast migration in C. elegans. Development 130, 3147-3161 (2003).
79. Hehr, C. L., Hocking, J. C. & McFarlane, S. Matrix metalloproteinases are required for retinal ganglion cell axon guidance at select decision points. Development 132, 3371-3379 (2005).
80. Shubayev, V. I. & Myers, R. R. Matrix metalloproteinase-9 promotes nerve growth factor-induced neurite elongation but not new sprout formation in vitro. J. Neurosci. Res. 77, 229-239 (2004).
81. Demestre, M. et al. Characterisation of matrix metalloproteinases and the effects of a broad-spectrum inhibitor (BB-1101) in peripheral nerve regeneration. Neuroscience 124, 767-779 (2004).
82. Ahmed, Z. et al. Matrix metalloproteases: degradation of the inhibitory environment of the transected optic nerve and the scar by regenerating axons. Mol. Cell. Neurosci. 28, 64-78 (2005).
83. Zuo, J., Neubauer, D., Dyess, K., Ferguson, T. A. & Muir, D. Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp. Neurol. 154, 654-662 (1998) Introduces the concept that a MMP can be used to remove inhibitory ECM molecules to expose the permissive ones.
84. Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R. D. & Kaczmarek, L. Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J. Neurosci. 22, 920-930 (2002).
85. Kim, H. J., Fillmore, H. L., Reeves, T. M. & Phillips, L. L. Elevation of hippocampal MMP-3 expression and activity during trauma-induced synaptogenesis. Exp. Neurol. 192, 60-72 (2005).
86. Reeves, T. M., Prins, M. L., Zhu, J., Povlishock, J. T. & Phillips, L. L. Matrix metalloproteinase inhibition alters functional and structural correlates of deafferentation-induced sprouting in the dentate gyrus. J. Neurosci. 23, 10182-10189 (2003).
87. Siebert, H., Dippel, N., Mader, M., Weber, F. & Bruck, W. Matrix metalloproteinase expression and inhibition after sciatic nerve axotomy. J. Neuropathol. Exp. Neurol. 60, 85-93 (2001).
88. Bradbury, E. J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (2002).
89. Ughrin, Y. M., Chen, Z. J. & Levine, J. M. Multiple regions of the NG2 proteoglycan inhibit neurite growth and induce growth cone collapse. J. Neurosci. 23, 175-186 (2003).
90. Lee, D. H., Strittmatter, S. M. & Sah, D. W. Targeting the Nogo receptor to treat central nervous system injuries. Nature Rev. Drug Discov. 2, 872-878 (2003).
91. NTR). J. Biol. Chem. 279, 4241-4249 (2004).
92. Domeniconi, M. et al. MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth. Neuron 46, 849-855 (2005).
93. Walmsley, A. R. et al. Zinc metalloproteinase-mediated cleavage of the human Nogo-66 receptor. J. Cell Sci. 117, 4591-4602 (2004). Lays the foundation for considering the involvement of metalloproteinases in overcoming inhibition of axonal regrowth by Nogos.
94. Walmsley, A. R., Mir, A. K. & Frentzel, S. Ectodomain shedding of human Nogo-66 receptor homologue-1 by zinc metalloproteinases. Biochem. Biophys. Res. Commun. 327, 112-116 (2005).
95. Belien, A. T., Paganetti, P. A. & Schwab, M. E. Membrane-type 1 matrix metalloprotease (MT1-MMP) enables invasive migration of glioma cells in central nervous system white matter. J. Cell Biol. 144, 373-384 (1999).
96. Mannello, F., Luchetti, F., Falcieri, E. & Papa, S. Multiple roles of matrix metalloproteinases during apoptosis. Apoptosis 10, 19-24 (2005) A thorough review of metalloproteinases in life and death decisions of a cell.
97. Wetzel, M., Rosenberg, G. A. & Cunningham, L. A. Tissue inhibitor of metalloproteinases-3 and matrix metalloproteinase-3 regulate neuronal sensitivity to doxorubicin-induced apoptosis. Eur. J. Neurosci. 18, 1050-1060 (2003).
98. Naus, S. et al. Ectodomain shedding of the neural recognition molecule CHL1 by the metalloprotease-disintegrin ADAM8 promotes neurite outgrowth and suppresses neuronal cell death. J. Biol. Chem. 279, 16083-16090 (2004).
99. Fowlkes, J. L. & Winkler, M. K. Exploring the interface between metallo-proteinase activity and growth factor and cytokine bioavailability. Cytokine Growth Factor Rev. 13, 277-287 (2002).
100. Lee, R., Kermani, P., Teng, K. K. & Hempstead, B. L. Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948 (2001). Implicates the metalloproteinases in the biology of the neurotrophins.
101. Hwang, J. J., Park, M. H., Choi, S. Y. & Koh, J. Y. Activation of the Trk signaling pathway by extracellular zinc. Role of metalloproteinases. J. Biol. Chem. 280, 11995-12001 (2005).
102. Franklin, R. J. Why does remyelination fail in multiple sclerosis? Nature Rev. Neurosci. 3, 705-714 (2002).
103. Uhm, J. H., Dooley, N. P., Oh, L. Y. & Yong, V. W. Oligodendrocytes utilize a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 22, 53-63 (1998).
104. Oh, L. Y. et al. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 19, 8464-8475 (1999). One of the first papers to suggest beneficial roles of metalloproteinases in the nervous system.
105. Larsen, P. H. & Yong, V. W. The expression of matrix metalloproteinase-12 by oligodendrocytes regulates their maturation and morphological differentiation. J. Neurosci. 24, 7597-7603 (2004).
106. Sagane, K. et al. Ataxia and peripheral nerve hypomyelination in ADAM22-deficient mice. BMC Neurosci. 6, 33 (2005).
107. Bernstein, H. G. et al. ADAM (a disintegrin and metalloprotease) 12 is expressed in rat and human brain and localized to oligodendrocytes. J. Neurosci. Res. 75, 353-360 (2004).
108. John, G. R. et al. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocyte maturation. Nature Med. 8, 1115-1121 (2002).
109. Tsai, H. H. et al. The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell 110, 373-383 (2002).
110. Wang, J. & Tsirka, S. E. Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage. Brain 128, 1622-1633 (2005).
111. Stuve, O. et al. Interferon β-1b decreases the migration of T lymphocytes in vitro: effects on matrix metalloproteinase-9. Ann. Neurol. 40, 853-863 (1996).
112. Leppert, D., Waubant, E., Burk, M. R., Oksenberg, J. R. & Hauser, S. L. Interferon β-1b inhibits gelatinase secretion and in vitro migration of human T cells: a possible mechanism for treatment efficacy in multiple sclerosis. Ann. Neurol. 40, 846-852 (1996).
113. Yong, V. W. Differential mechanisms of action of interferon-β and glatiramer aetate in MS. Neurology 59, 802-808 (2002).
114. Yong, V. W. et al. The promise of minocycline in neurology. Lancet Neurol. 3, 744-751 (2004).
115. Overall, C. M. et al. Protease degradomics: mass spectrometry discovery of protease substrates and the CLIP-CHIP, a dedicated DNA microarray of all human proteases and inhibitors. Biol. Chem. 385, 493-504 (2004). Lays the foundation for a key area of future metalloproteinase research, that of identifying substrates of metalloproteinases in particular contexts.
116. Asahi, M., Sumii, T., Fini, M. E., Itohara, S. & Lo, E. H. Matrix metalloproteinase 2 gene knockout has no effect on acute brain injury after focal ischemia. Neuroreport 12, 3003-3007 (2001).
117. Takahashi, M. et al. In vivo glioma growth requires host-derived matrix metalloproteinase 2 for maintenance of angioarchitecture. Pharmacol. Res. 46, 155-163 (2002).
118. Dubois, B. et al. Resistance of young gelatinase B-deficient mice to experimental autoimmune encephalomyelitis and necrotizing tail lesions. J. Clin. Invest. 104, 1507-1515 (1999).
119. Wang, X. et al. Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J. Neurosci. 20, 7037-7042 (2000).
120. Asahi, M. et al. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J. Neurosci. 21, 7724-7732 (2001).
121. Tang, J. et al. Mmp-9 deficiency enhances collagenase-induced intracerebral hemorrhage and brain injury in mutant mice. J. Cereb. Blood Flow Metab. 24, 1133-1134 (2004).
122. Wells, J. E. A., Biernaskie, J., Szymanska, A., Corbett, D. R. & Yong, V. W. Matrix metalloproteinase (MMP)-12 expression has a negative impact on sensorimotor function following intracerebral haemorrhage in mice. Eur. J. Neurosci. 21, 187-196 (2005).