Pathophysiology of the brain extracellular matrix: A new target for remyelination

Nature Reviews Neuroscience

Volumn 14, Issue 10, 2013, Pages 722-729

  Lau, Lorraine W ^a   Cua, Rowena ^a   Keough, Michael B ^a   Haylock Jacobs, Sarah ^a   Yong, V Wee ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E; CHONDROITIN SULFATE; COLLAGEN TYPE 4; CYTOKINE; ENZYME INHIBITOR; FIBRONECTIN; FREE RADICAL; GELATINASE A; GELATINASE B; GLUCURONIC ACID; GLUTAMIC ACID; GLYCOPROTEIN; GLYCOSAMINOGLYCAN; GROWTH FACTOR; HEPARAN SULFATE; HYALURONIC ACID; LAMININ; MESSENGER RNA; MYELIN; N ACETYLGALACTOSAMINE; N ACETYLGALACTOSAMINE 4 SULFATASE; PROTEINASE; PROTEOGLYCAN; SMALL MOLECULE TRANSPORT AGENT; TENASCIN; TRANSFERASE; UNCLASSIFIED DRUG; XYLOSIDE; XYLOSYLTRANSFERASE 1;

ALZHEIMER DISEASE; ASTROCYTE; BASEMENT MEMBRANE; BIOSYNTHESIS; BLOOD BRAIN BARRIER; BRAIN; CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM DISEASE; DEMYELINATING DISEASE; ENZYME ACTIVITY; EPILEPSY; EXTRACELLULAR MATRIX; HUMAN; IMMUNE SYSTEM; INFLAMMATION; LIPID TRANSPORT; MACROPHAGE ACTIVATION; MICROGLIA; MICROVASCULATURE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INJURY; NEUROLOGIC DISEASE; NONHUMAN; OLIGODENDROGLIA; PATHOPHYSIOLOGY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; REMYELINIZATION; REVIEW; RNA INTERFERENCE; SEIZURE; SPINAL CORD INJURY; SYNAPTOGENESIS;

ANIMALS; BRAIN; CHONDROITIN SULFATE PROTEOGLYCANS; DEMYELINATING DISEASES; EXTRACELLULAR MATRIX; HUMANS; NERVE REGENERATION;

EID: 84884592784     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3550     Document Type: Review

References (80)

1. Bignami, A., Hosley, M. & Dahl, D. Hyaluronic acid and hyaluronic acid-binding proteins in brain extracellular matrix. Anat. Embryol. 188, 419-433 (1993). (Pubitemid 24000108)
2. Cragg, B. Brain extracellular space fixed for electron microscopy. Neurosci. Lett. 15, 301-306 (1979). (Pubitemid 10179224)
3. Bandtlow, C. E. & Zimmermann, D. R. Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol. Rev. 80, 1267-1290 (2000).
4. Dityatev, A. & Schachner, M. Extracellular matrix molecules and synaptic plasticity. Nature Rev. Neurosci. 4, 456-468 (2003). (Pubitemid 37280167)
5. Kwok, J. C. F., Dick, G., Wang, D. & Fawcett, J. W. Extracellular matrix and perineuronal nets in CNS repair. Dev. Neurobiol. 71, 1073-1089 (2011).
6. Rauch, U. Brain matrix: structure, turnover and necessity. Biochem. Soc. Trans. 35, 656-660 (2007). (Pubitemid 47310334)
7. Wang, C. X. & Shuaib, A. Critical role of microvasculature basal lamina in ischemic brain injury. Prog. Neurobiol. 83, 140-148 (2007). (Pubitemid 47484045)
8. McRae, P. A. & Porter, B. E. The perineuronal net component of the extracellular matrix in plasticity and epilepsy. Neurochem. Int. 61, 963-972 (2012).
9. Bellail, A. C., Hunter, S. B., Brat, D. J., Tan, C. & Van Meir, E. G. Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion. Int. J. Biochem. Cell Biol. 36, 1046-1069 (2004). (Pubitemid 38501557)
10. Fukuchi, K., Hart, M. & Li, L. Alzheimer's disease and heparan sulfate proteoglycan. Front. Biosci. 3, d327-d337 (1998).
11. McKeon, R. J., Schreiber, R. C., Rudge, J. S. & Silver, J. Reduction of neurite outgrowth in a model of glial scarring following CNS injury is correlated with the expression of inhibitory molecules on reactive astrocytes. J. Neurosci. 11, 3398-3411 (1991).
12. Jones, L. L., Margolis, R. U. & Tuszynski, M. H. The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp. Neurol. 182, 399-411 (2003). (Pubitemid 36937092)
13. Silver, J. & Miller, J. H. Regeneration beyond the glial scar. Nature Rev. Neurosci. 5, 146-156 (2004). (Pubitemid 38160289)
14. Bradbury, E. J. et al. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416, 636-640 (2002). (Pubitemid 34406764)
15. Grimpe, B. & Silver, J. A novel DNA enzyme reduces glycosaminoglycan chains in the glial scar and allows microtransplanted dorsal root ganglia axons to regenerate beyond lesions in the spinal cord. J. Neurosci. 24, 1393-1397 (2004). (Pubitemid 38222990)
16. Sugahara, K. & Mikami, T. Chondroitin/dermatan sulfate in the central nervous system. Curr. Opin. Struct. Biol. 17, 536-545 (2007). (Pubitemid 350019013)
17. Gilbert, R. J. et al. CS-4,6 is differentially upregulated in glial scar and is a potent inhibitor of neurite extension. Mol. Cell. Neurosci. 29, 545-558 (2005). (Pubitemid 40984696)
18. Karumbaiah, L. et al. Targeted downregulation of N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase significantly mitigates chondroitin sulfate proteoglycan-mediated inhibition. Glia 59, 981-996 (2011).
19. Brown, J. M. et al. A sulfated carbohydrate epitope inhibits axon regeneration after injury. Proc. Natl Acad. Sci. USA 109, 4768-4773 (2012).
20. Shen, Y. et al. PTP? is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326, 592-596 (2009).
21. Lin, R., Rosahl, T. W., Whiting, P. J., Fawcett, J. W. & Kwok, J. C. F. 6-Sulphated chondroitins have a positive influence on axonal regeneration. PloS ONE 6, e21499 (2011).
22. Sherman, L. S. & Back, S. A. A 'GAG' reflex prevents repair of the damaged CNS. Trends Neurosci. 31, 44-52 (2008).
23. Fitch, M. T. & Silver, J. CNS injury, glial scars, and inflammation: inhibitory extracellular matrices and regeneration failure. Exp. Neurol. 209, 294-301 (2008). (Pubitemid 351174127)
24. Seitz, A., Aglow, E. & Heber-Katz, E. Recovery from spinal cord injury: a new transection model in the C57Bl/6 mouse. J. Neurosci. Res. 67, 337-345 (2002). (Pubitemid 34137140)
25. van Horssen, J., B?, L., Dijkstra, C. D. & de Vries, H. E. Extensive extracellular matrix depositions in active multiple sclerosis lesions. Neurobiol. Dis. 24, 484-491 (2006). (Pubitemid 44716678)
26. Sorokin, L. The impact of the extracellular matrix on inflammation. Nature Rev. Immunol. 10, 712-723 (2010).
27. Mohan, H. et al. Extracellular matrix in multiple sclerosis lesions: fibrillar collagens, biglycan and decorin are upregulated and associated with infiltrating immune cells. Brain Pathol. 20, 966-975 (2010).
28. Gray, E., Thomas, T. L., Betmouni, S., Scolding, N. & Love, S. Elevated matrix metalloproteinase-9 and degradation of perineuronal nets in cerebrocortical multiple sclerosis plaques. J. Neuropathol. Exp. Neurol. 67, 888-899 (2008).
29. Galtrey, C. M. & Fawcett, J. W. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res. Rev. 54, 1-18 (2007). (Pubitemid 46498163)
30. Yiu, G. & He, Z. Glial inhibition of CNS axon regeneration. Nature Rev. Neurosci. 7, 617-627 (2006). (Pubitemid 44106744)
31. Back, S. A. et al. Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nature Med. 11, 966-972 (2005). (Pubitemid 41294442)
32. Sobel, R. A. & Ahmed, A. S. White matter extracellular matrix chondroitin sulfate/dermatan sulfate proteoglycans in multiple sclerosis. J. Neuropathol. Exp. Neurol. 60, 1198-1207 (2001). (Pubitemid 33117100)
33. Marret, S. et al. Expression and effects of hyaluronan and of the hyaluronan-binding protein hyaluronectin in newborn rat brain glial cell cultures. J. Neurochem. 62, 1285-1295 (1994). (Pubitemid 24098075)
34. Buttery, P. C. & ffrench-Constant, C. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol. Cell. Neurosci. 14, 199-212 (1999). (Pubitemid 29449223)
35. Chun, S. J., Rasband, M. N., Sidman, R. L., Habib, A. A. & Vartanian, T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J. Cell Biol. 163, 397-408 (2003). (Pubitemid 37363139)
36. Milner, R. et al. Expression of ?v?3 and ?v?8 integrins during oligodendrocyte precursor differentiation in the presence and absence of axons. Glia 21, 350-360 (1997). (Pubitemid 27526672)
37. Colognato, H., Ffrench-Constant, C. & Feltri, M. L. Human diseases reveal novel roles for neural laminins. Trends Neurosci. 28, 480-486 (2005). (Pubitemid 41187797)
38. Relucio, J., Menezes, M. J., Miyagoe-Suzuki, Y., Takeda, S. & Colognato, H. Laminin regulates postnatal oligodendrocyte production by promoting oligodendrocyte progenitor survival in the subventricular zone. Glia 60, 1451-1467 (2012).
39. Siskov?, Z., Baron, W., de Vries, H. & Hoekstra, D. Fibronectin impedes 'myelin' sheet-directed flow in oligodendrocytes: a role for a beta 1 integrin-mediated PKC signaling pathway in vesicular trafficking. Mol. Cell. Neurosci. 33, 150-159 (2006). (Pubitemid 44415490)
40. Stoffels, J. M. J. et al. Fibronectin aggregation in multiple sclerosis lesions impairs remyelination. Brain 136, 116-131 (2013).
41. van Horssen, J., Dijkstra, C. D. & de Vries, H. E. The extracellular matrix in multiple sclerosis pathology. J. Neurochem. 103, 1293-1301 (2007). (Pubitemid 47631831)
42. Kippert, A., Fitzner, D., Helenius, J. & Simons, M. Actomyosin contractility controls cell surface area of oligodendrocytes. BMC Cell Biol. 10, 71 (2009).
43. Lau, L. W. et al. Chondroitin sulfate proteoglycans in demyelinated lesions impair remyelination. Ann. Neurol. 72, 419-432 (2012).
44. Siebert, J. R. & Osterhout, D. J. The inhibitory effects of chondroitin sulfate proteoglycans on oligodendrocytes. J. Neurochem. 119, 176-188 (2011).
45. Siebert, J. R., Stelzner, D. J. & Osterhout, D. J. Chondroitinase treatment following spinal contusion injury increases migration of oligodendrocyte progenitor cells. Exp. Neurol. 231, 19-29 (2011).
46. Karimi-Abdolrezaee, S., Schut, D., Wang, J. & Fehlings, M. G. Chondroitinase and growth factors enhance activation and oligodendrocyte differentiation of endogenous neural precursor cells after spinal cord injury. PloS ONE 7, e37589 (2012).
47. Kuhlmann, T. et al. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131, 1749-1758 (2008). (Pubitemid 351957453)
48. Chang, A. et al. Cortical remyelination: a new target for repair therapies in multiple sclerosis. Ann. Neurol. 72, 918-926 (2012).
49. Watanabe, M., Toyama, Y. & Nishiyama, A. Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J. Neurosci. Res. 69, 826-836 (2002). (Pubitemid 34984700)
50. 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). (Pubitemid 37548948)
51. Kucharova, K., Chang, Y., Boor, A., Yong, V. W. & Stallcup, W. B. Reduced inflammation accompanies diminished myelin damage and repair in the NG2 null mouse spinal cord. J. Neuroinflammation 8, 158 (2011).
52. Yong, V. W., Krekoski, C. A., Forsyth, P. A., Bell, R. & Edwards, D. R. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci. 21, 75-80 (1998).
53. Yong, V. W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nature Rev. Neurosci. 6, 931-944 (2005). (Pubitemid 41753087)
54. Sternlicht, M. D. & Werb, Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516 (2001). (Pubitemid 33096184)
55. Rodríguez, D., Morrison, C. J. & Overall, C. M. Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim. Biophys. Acta 1803, 39-54 (2010).
56. Hsu, J.-Y. C. et al. Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury. J. Neurosci. 26, 9841-9850 (2006). (Pubitemid 44477146)
57. Pizzi, M. A. & Crowe, M. J. Transplantation of fibroblasts that overexpress matrix metalloproteinase-3 into the site of spinal cord injury in rats. J. Neurotrauma 23, 1750-1765 (2006). (Pubitemid 46034449)
58. Zuo, J., Ferguson, T. A., Hernandez, Y. J., Stetler-Stevenson, W. G. & Muir, D. Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J. Neurosci. 18, 5203-5211 (1998). (Pubitemid 28311937)
59. Sisková, Z. et al. Fibronectin attenuates process outgrowth in oligodendrocytes by mislocalizing MMP-9 activity. Mol. Cell. Neurosci. 42, 234-242 (2009).
60. Apte, S. S. A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J. Biol. Chem. 284, 31493-31497 (2009).
61. Tauchi, R. et al. The endogenous proteoglycan-degrading enzyme ADAMTS-4 promotes functional recovery after spinal cord injury. J. Neuroinflammation 9, 53 (2012).
62. Preston, M. et al. Digestion products of the PH20 hyaluronidase inhibit remyelination. Ann. Neurol. 73, 266-280 (2013).
63. Laabs, T. L. et al. Inhibiting glycosaminoglycan chain polymerization decreases the inhibitory activity of astrocyte-derived chondroitin sulfate proteoglycans. J. Neurosci. 27, 14494-14501 (2007).
64. Gloster, T. M. & Vocadlo, D. J. Developing inhibitors of glycan processing enzymes as tools for enabling glycobiology. Nature Chem. Biol. 8, 683-694 (2012).
65. Tan, C. L. et al. Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J. Neurosci. 31, 6289-6295 (2011).
66. Snow, D. M., Brown, E. M. & Letourneau, P. C. Growth cone behavior in the presence of soluble chondroitin sulfate proteoglycan (CSPG), compared to behavior on CSPG bound to laminin or fibronectin. Int. J. Dev. Neurosci. 14, 331-349 (1996). (Pubitemid 26238175)
67. Sharma, K., Selzer, M. E. & Li, S. Scar-mediated inhibition and CSPG receptors in the CNS. Exp. Neurol. 237, 370-378 (2012).
68. Pendleton, J. C. et al. Chondroitin sulfate proteoglycans inhibit oligodendrocyte myelination through PTP?. Exp. Neurol. 247, 113-121 (2013).
69. Condic, M. L., Snow, D. M. & Letourneau, P. C. Embryonic neurons adapt to the inhibitory proteoglycan aggrecan by increasing integrin expression. J. Neurosci. 19, 10036-10043 (1999). (Pubitemid 30226675)
70. Hamby, M. E. & Sofroniew, M. V. Reactive astrocytes as therapeutic targets for CNS disorders. Neurotherapeutics 7, 494-506 (2010).
71. Rolls, A. et al. Two faces of chondroitin sulfate proteoglycan in spinal cord repair: a role in microglia/macrophage activation. PLoS Med. 5, e171 (2008).
72. Engelhardt, B. Development of the blood-brain barrier. Cell Tissue Res. 314, 119-129 (2003). (Pubitemid 37409918)
73. Colognato, H. & Yurchenco, P. D. Form and function: the laminin family of heterotrimers. Dev. Dyn. 218, 213-234 (2000). (Pubitemid 30349637)
74. Engel, M., Maurel, P., Margolis, R. U. & Margolis, R. K. Chondroitin sulfate proteoglycans in the developing central nervous system. I. cellular sites of synthesis of neurocan and phosphacan. J. Comp. Neurol. 366, 34-43 (1996). (Pubitemid 26069848)
75. Ichijo, H. & Kawabata, I. Roles of the telencephalic cells and their chondroitin sulfate proteoglycans in delimiting an anterior border of the retinal pathway. J. Neurosci. 21, 9304-9314 (2001). (Pubitemid 33096874)
76. Bekku, Y. et al. Bral1: its role in diffusion barrier formation and conduction velocity in the CNS. J. Neurosci. 30, 3113-3123 (2010).
77. Fisher, D. et al. Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors. J. Neurosci. 31, 14051-14066 (2011).
78. Koprivica, V. et al. EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 310, 106-110 (2005). (Pubitemid 41434546)
79. Kim, S. et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457, 102-106 (2009).
80. Dickendesher, T. L. et al. NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans. Nature Neurosci. 15, 703-712 (2012).