Regulation of neurogenesis by extracellular matrix and integrins

Acta Neurobiologiae Experimentalis

Volumn 71, Issue 1, 2011, Pages 103-112

  Wojcik Stanaszek, Luiza ^a   Gregor, Anna ^a   Zalewska, Teresa ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

Cell microenvironment; Focal adhesion kinase; Integrin signaling; Metalloproteinases; Neural stem progenitor cells

Indexed keywords

INTEGRIN;

ANIMAL; BIOLOGICAL MODEL; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; EXTRACELLULAR MATRIX; HUMANS; INTEGRINS; MODELS, BIOLOGICAL; NEUROGENESIS; SIGNAL TRANSDUCTION;

EID: 79955370800     PISSN: 00651400     EISSN: 00651400     Source Type: Journal    
DOI: None     Document Type: Review

References (108)

1. Alam N, Goel HL, Zarif MJ, Butterfield JE, Perkins HM, Sansoucy BG, Sawyer TK, Languino LR (2007) The integrin-growth factor receptor duet. J Cell Physiol 213: 649-653.
2. Ali SA, Pappas IS, Parnavelas JG (1998) Collagen type IV promotes the differentiation of neuronal progenitors and inhibits astroglial differentiation in cortical cell cultures. Develop Brain Res 110: 31-38.
3. Andressen C, Adrian S, Fassler R (2005) The contribution of beta1 integrins to neuronal migration and differentiation depends on extracellular matrix molecules. Eur J Cell Biol 84: 973-982.
4. Anton ES, Kreidberg JA, Rakic P (1999) Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22: 277-289.
5. Aoto H, Sasaki H, Ishino M, Sasaki T (2002) Nuclear translocation of cell adhesion kinase beta/proline -rich tyrosine kinase 2. Cell Struct Funct 27: 47-61.
6. Astier A, Avraham H, Manie SN, Groopman J, Canty T, Avraham S, Freedman AS (1997) The related adhesion focal tyrosine kinase is tyrosine-phosphorylated after beta1-integrin stimulation in B cells and binds to p130cas. J Biol Chem 272: 228-232.
7. Avraham S, London R, Fu Y, Ota S, Hiregowdara D, Li J, Jiang S, Pasztor LM, White RA, Groopman JE, et al. (1995) Identification and characterization of a novel related adhesion focal tyrosine kinase (RAFTK)from megakaryocytes and brain. J Biol Chem 270: 27742-27751.
8. Ayoub AE, Cai TQ, Kaplan RA, Luo J (2005) Developmental expression of matrix metalloproteinases 2 and 8 and their potential role in the histogenesis of the cerebellar cortex. J Comp Neurol 481: 413-415.
9. Barkho BZ, Munoz AE, Li X, Li L, Cunningham LA, et al. (2008) Endogenous Matrix Metalloproteinase MMP-3 and MMP-9 Promote Differentiation and Migration of Adult Neural Progenitor Cells in Response to Chemokines. Stem Cells 26: 3139-3149.
10. Bianco P, Riminucci M, Gronthos L, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential application. Stem Cells 19: 180-192.
11. Bovetti S, Bovolin P, Perroteau I, Puche AC (2007) Subventricular zone-derived neuroblast migration to the olfactory bulb is modulated by matrix remodeling. Eur J Neurosci 25: 2021-2033.
12. Bruno MA, Cuello AC (2006) Activity-dependentr release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by protease cascade. Proc Natl Acad Sci USA 103: 6735-6740.
13. Buzanska L, Ruiz A, Zychowicz M, Rauscher H, Ceriotti L, Rossi F, Colpo P, Domanska-Janik K, Coecke S (2009) Patterned growth and differentiation of human cord blood-derived neural stem cells on nano-engineered and bio-functionized surfaces. Acta Neurobiol Exp 69: 24-36.
14. Caloff AL (1995) Intrinsic and extrinsic factors regulating vertebrate neurogenesis. Curr Opin Neurobiol 5: 19-27.
15. Campos LS, Leone DP, Relvas JB, Brakebusch C, Fassler R, Suter U, Ffrench-Constant C (2004) Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131: 3433-3444.
16. Canete Soler R, Gui YH, Linask KK, Muschel RJ (1995) MMP-9 (gelatinase B) mRNA is expressed during mouse neurogenesis and may be associated with vascularization. Brain Res Dev Brain Res 88: 37-52.
17. Chen HC, Appeddu PA, Isoda H, Guan JL (1996) Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase. J Biol Chem 271: 26329-26334.
18. Chen SS, Fitzgerald W, Zimmerberg J, Kleinman HK (2007) Cell-cell and cell-extracellular matrix interaction regulate embryonic stem cell differentiation. Stem Cells 25: 553-561.
19. Deryugina EI, Bourdon MA, Luo GX, Reisfeld RA, Strongin A (1997) Matrix metalloproteinase-2 activation modulates glioma cell migration. J Cell Sci 110: 2473-2482.
20. Dowgiert J, Sosne G, Kurpakus-Wheater m (2004) Laminin-2 stimulates the proliferation of epithelial cells in conjunctival epithelial cell line. Cell Prolif 37: 161-175.
21. Drago J, Nurcombe V, Barlett PF (1991) Laminin through its long arm E8 fragment promotes the proliferation and differentiation of murine neuroepithelial cells in vitro. Exp Cell Res 192: 256-265.
22. Dzwonek J, Rylski M, Kaczmarek L (2004) Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain. FEBS Lett 567: 129-135.
23. Emsley JG, Mitchell BD, Kemperman G, Macklis JD (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75: 321-341.
24. Ethel IM, Ethel DW (2007) Matrix metalloproteinases in brain development and remodeling: Synaptic functions and targets. J Neurosci Res 85: 2813-2823.
25. Ferguson TA, Muir D.(2000) MMP-2 and MMP-9 increase the neurite-promoting potential of schwann cell basal laminae and are upregulated in degenerated nerve. Mol Cell Neurosci16: 157-167.
26. Flaim CJ, Chien S, Bhatia SN (2005) Extracellular matrix promotes the growth and differentiation of murine hematopoietic cells in vitro. Nat Methods 2: 119-125.
27. Flanagan FA, Rebaza LM, Derzic S, Schwartz PH, Monuki ES (2006) Regulation of human precursor cells by laminin and integrins. J Neurosci Res 83: 845-856.
28. Frolichsthal-Schoeller P, vescovi AL, Krekoski CA, et al. (1999) Expression and modulation of matrix metalloproteinase-2 and tissue inhibitors of metalloproteinases in human embryonic CNS stem cells. NeuroReport 10: 345-351.
29. Furuta Y, Illic D, Kanazawa S, Takeda N, Yamamoto T, Aizawa S (1995) Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogen 11: 1989-1995.
30. Gage FH (2000) Mammalian neural stem cells. Science 287: 1433-1438.
31. Gasche Y, Soccal PM, Kanemitsu M, Copin JC (2006) Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front in Biosci 11: 1289-1301
32. Georges-Labouesse E, Mark M, Messaddeq N, Gansmuller A (1998) Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 8: 983-986.
33. Giancotti FG, Ruoslahti (1999) Integrin signaling. Science 285: 1028-1032.
34. Gianelli G, Falk-Marzillier J, Schiraldi O, et al. (1997) Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277: 225-228.
35. Goh KL, Yang JT, Hynes RO (1997) Mesodermal defects and cranial neural crest apoptosis in alpha5 integrin-null embryos. Development. 124: 4309-4319.
36. Goetschy JF, Ulrich D, Aunis D, Ciesielski-Treska J (1987) Fibronectin and collagens modulate the proliferation and morphology of astroglial cells in culture. Int J Dev Neurosci 5: 63-70.
37. Gonthier B, Koncina E, Satkauskas S, Perraut M, Roussel G, et al. (2009) A PKC-dependent recruitment of MMP-2 controls semaphorin-3A growth-promoting effect in cortical dendrites. PLoS One 4: e5099.
38. Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z, Orban P, Klein R, Schittny JC, Mullr U (2001) Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31: 367-379.
39. Gu J, Fujibayashi A, Yamada KM, Sekiguchi K (2002) Laminin 10/11 and fibronectin differentially prevent apoptosis induced by serum removal via phosphatidylinositol 3-kinase Akt- and MEK1/ERK-dependent pathways. J Biol Chem 277: 19922-19928.
40. Hoshina N, Tezuka T, Yokoyama K, Kozuka-Hata H, Oyama M, Yamamoto T (2007) Focal adhesion kinase regulates laminin-induced oligodendroglial process outgrowth. Genes Cells 12: 1245-1254.
41. Hynes R (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
42. Igishi T, Fukuhara S, Patel V, Katz BZ, Yamada KM, Gutkind JS (1999) Divergent signaling pathway link focal adhesion kinase to mitogen-activated protein kinase cascades. J Biol Chem. 274: 30738-30746.
43. Illic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T, Aizawa S (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mouse. Nature 377: 539-544.
44. Illic D, Damsky CH, Yamamoto T (1997) Focal adhesion kinase: at the crossroads of signal transdution. J Cell Sci 110: 401-407.
45. Ishii S, Okada Y, Kadoya T, Matsuzaki Y, Shimazaki T, Okano H (2010) Stromal cell-secreted factors promote the survival of embryonic stem/progenitor cells via the activation of MAPK and PI3K-Akt pathway. J Neurosci Res 88: 722-734.
46. Ishitsuka T, Ikuta T, Ariga H, Matsumoto K (2009) Serum tenascin-X strongly binds to vascular endothelial growth factor. Biol Pharm Bull 32:1004-1011.
47. Iyer AK, Tran KT, Griffith L, Wells A (2008) Cell surface restriction of EGFR by a tenascin cytotactin-encoded EGF-like repeat is preferential for motility-related signaling. J Cell Physiol 214:504-512.
48. Jablonska A, Wojcik L, Zalewska T, Domanska-Janik K, Lukomska B. Neurogenesis in the adult rat brain after human umbilical cord blood stem cells transplantation in an experimental model of cerebral ischemic injury; alterations in the expression of doublecortin and metalloproteinases. (Abstract) 7th International Stem Cell School In Regenerative Medicine 2009; p.70.
49. Jin K, Mao XO, Del Rio Guerra G, Jin L (2005) Heparin-binding epidermal growth factor-like growth factor stimulates cell proliferation in cerebral cortical cultures through phosphatidylinositol 3'-kinase and mitogen-activated protein kinase. J Neurosci Res 81: 497-505.
50. Kearns SM, Laywell ED, Kukekov VK, Steindler DA (2003) Extracellular matrix effects on neurosphere cell motility. Exp Neurol 182: 240-244.
51. Kihara T, Hirose M, Oshima A, Ohgushi H (2006) Exogenous type collagen I facilitates osteogenic differentiation and acts as a substrate for mineralization of rat marrow mesenchymal stem cells in vitro. Biochem Biophys Res Commun 341: 1029-1035.
52. Kuwada SK, Li X (2000) Integrin alpha5/beta1 mediates fibronectin-dependent epithelial cell proliferation through epidermal growth factor receptor activation. Mol Biol Cell 11:2485-2496.
53. Larsen M, Artym VV, Green JA, Yamada KM (2006) The matrix reorganized: extracellular matrix remodeling and integrin sigaling. Curr Op Cell Biol. 18: 463-471.
54. Lee R, Kermani P, Teng KK, et al.(2001) Regulation of cell survival by secreted proneurotrophins. Science 294: 1945-1948.
55. Lee SR, Kim H-J, Rogowska J, Zhao BQ, Bhide P, Parent JM, Lo EH (2006) Involvement of matrix metalloproteinase in neuroblast cell migration from the subventricular zone after stroke. J Neurosci 26: 3491-3495.
56. Li BS, Ma W, Zhang L, Barker JL, Stenger DA, Pant HC (2001) Activation of phosphatidylinositol-3 kinase (PI-3K) and extracellular regulated kinases (Erk1/2) is involved in muscarinic receptor-mediated DNA synthesis in neural progenitor cells. J Neurosci 21: 1569-1579.
57. Lim DA, Alvarez-Buylla A (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci 96: 7526-7531.
58. Lim Y, Han I, Jeon J, Park H, Bahk YY, Oh ES (2004) Phosphorylation of focal adhesion kinase at tyrosine 861 is crucial for Ras transformation of fibroblasts. J Biol Chem. 279: 29060-29065.
59. Lu L, Tonchev AB, Kaplamadzhiev DB, Boneva NB, Mori Y, et al.(2008) Expression of Matrix Metalloproteinases in the Neurogenic Niche of the Adult Monkey Hippocampus After Ischemia. Hippocampus 18: 1074-1084.
60. Luckenbill-Edds L (1997) Laminin and the mechanism of neuronal outgrowth. Brain Res Brain Res Rev 23: 1-27.
61. Mannello F, Tonti GA, Bagnara GP et al. (2006) Role and function of matrix metalloproteinases in the differentiation and biological characterization of mesenchymal stem cells. Stem Cells 24: 475-481.
62. Marchetti G, Escuin S, van der Flier A, De Arcangelis A, Hynes RO (2009) Integrin afa5beta1 is necessary for regulation of cortical neurons during mouse brain development. Europ J Neurosci 31: 399-409.
63. Matsumoto J, Morioka M, Hasegawa Y, Kawano T, Yoshinaga Y, Maeda T, Yano S, Kai Y, Fukunaga K, Kuratsu J (2006) Sodium orthovanadate enhances proliferation of progenitor cells in the adult rat subventricular zone after focal cerebral ischemia. J Pharmacol Exp Ther 318: 982-991.
64. McCawley LJ, Matrisian LM (2001) Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 13: 534-540.
65. Mitra S, Hanson D, Schlaepfer D (2005) Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6: 56-58.
66. Moelling K, Schad K,Bosse M, Zimmerman S, Schweneker M (2002) Regulation of Raf-Akt cross-talk. J Biol Chem 277: 31099.
67. Monson JM, Natzle J, Friedman J, McCarthy BJ (1982) Expression and novel structure of collagen gene in Drosophila. Proc Nat Acad Sci 79: 1761-1765.
68. Morgunova E, Tuuttila A, Bergmann U, Isupov M, Lindquist Y, Schneider G, Tryggvason K (1999) Structure of human promatrix metalloproteinase-2: activation, mechanism revealed. Science 284: 1667-1670.
69. Morris DC, Zhang ZG, Zhang R, LeTourmeau Y, Gregg SR et al. (2006) Stroke increases expression of matrix metalloproteinases and p21-activated protein kinase in neural progenitor cells. ACAD Emerg Med 13: S194.
70. Mott JD, Werb Z (2004) Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 16: 558-564.
71. Mruthyunjaya S, Manchanda R, Godbole R, Pujari R, Shiras A, Shastry P (2010) Laminin-1 induces neurite outgrowth in human mesenchymal stem cells in serum/differentiation factors-free conditions through activation of FAK-MEK/ERK signaling pathways. Biochem Biophys Res Commun 391: 43-48.
72. Murase S, Horwitz AF (2002) Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream.J Neurosci 22: 3568-3579.
73. Nagase H, Woessner JF Jr (1999) Matrix metalloproteinases. J Biol Chem 274: 21491-21494.
74. Oh LY, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, Yong VW (1999) Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocyts. J Neurosci 19: 8464-8475.
75. Ogier C, Bernard A, Chollet AM, Le Diguardher T, Hanessian S, et al. (2006) Matrix metalloproteinase-2 (MMP-2) regulates astrocyte motility in connection with the actin cytoskeleton and integrins. Glia 54: 272-284.
76. Oktay M, Wary KK, Dans M, Birge RB, Giancotti FG (1999) Integrin mediated activation of focal adhesion kinase is required for signaling to jun NH2-terminal kinase and progression through the G1 phase of the cycle. J Cell Biol 145: 1461-1470.
77. Ould-yahoui A, Tremblay E, Sbai O, Ferhat L, Bernard A, et al.(2009) A new role for TIMP-1 in modulating neurite outgrowth and morphology of cortical neurons. PLoS One 4:e8289.
78. Park DH, Eve DJ, Chung YG (2010) Regenerative medicine for neurological disorders. The ScientificWorld J 10: 470-489.
79. Rahman S, Patel Y, Murray J, Patel KV, Sumathipala R, Sobel M, Wijelath ES (2005) Novel hepatocyte growth factor (HGF) binding domains on fibronectin and vitronectin coordinate a distinct and amplified Met-integrin induced signalling pathway in endothelial cells. BMC Cell Biol 6: 8.
80. Sbai O, Ould-Yahoul A, Ferhalt L, et al. (2010) Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 58: 344-366.
81. Schaeffer HJ, Weber MJ (1999) Mitogen-activated protein kinases: specifis messages from ubiquitous messengers. Mol Cell Biol, 19: 2435-2444.
82. Scheffler B, Edenhofer F, Brustle O (2006) Merging fields: stem cells in neurogenesis, transplantation, and disease modeling. Brain Pathol 16: 155-168.
83. Schenk S, Quaranta V (2003) Tales from the crypt[ic] sites of the extracellular matrix. Trends Cell Biol 13:366-375.
84. Schlaepfer DD, Hunter T (1998) Integrin signalling and tyrosine phosphorylation: just the FAKs? Trends Cell Biol 8: 151-157.
85. Seo DW, Li H, Guedez L, Wingfield PT, Diaz T, Salloum R, Wei BY, Stetler-Stevenson WG (2003) TIMP-2 mediated inhibition of angiogenesis an MMP-independent mechanism. Cell 114: 171-180.
86. Shioda N, Han F, Morioka M, Fukunaga K (2008) Bis(1-oxy-2 pyridinethiolato)oxovanadium(IV) enhances neurogenesis via phosphatidylinositol 3-kinase/Akt and extracellular signal regulated kinase activation in the hippocampal subgranular zone after mouse focal cerebral ischemia. Neuroscience 155: 876-887.
87. Song HJ, Stevens CF, Gage FH (2002) Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5: 438-445.
88. Suzuki A, Iwama A, Miyashita H, Nakauchi H, Taniguchi H (2003) Role for growth factors and extracellular matrix components in controlling differentiation of prospectively isolated hepatic stem cells. Development 130: 2513-2524.
89. Sypecka J, Dragun-Szymczak P, Zalewska T, Domanska-Janik K (2009) Laminin promotes oligogliogenesis and increases MMPs activity in human neural stem cells of HUCB-NSC line. Acta Neurobiol Exp 69: 37-45.
90. Szymczak P, Wojcik-Stanaszek L, Sypecka J, Sokolowska A, Zalewska T (2010) Effect of matrix metalloproteinases inhibition on the proliferation and differentiation of HUCB-NSCs cultured in the presence of adhesive substrates. Acta Neurobiol Exp (Wars) 70: 1-11.
91. Tate MC, Garcia AJ, Keselowsky BG, Schumm MA, Archer DR, LaPlaca C (2004) Specific beta1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum. Mol Cell Neurosci 27: 22-31.
92. Tsukatani T, Fillmore HL, Hamilton HR, Holbrook EH, Costanzo RM (2003) Matrix metalloproteinase expression in the olfactory epithelium. NeuroReport 14: 1135-1140.
93. Vaillant C, Didier-Bases M, Hutter A, Belin MF, Thomasset N (1999) Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J Neurosci 19: 4994-5004.
94. Vaillant C, Meissirel C, Mutin M, Beli MF, Lund LR (2003) MMP-9 defficiency affects axonal outgrowth, migration and apoptosis in the developing cerebellum. Mol Cell Neurosci 24: 395-408.
95. Von der Mark K, Ocalan M (1989) Antagonistic effects of laminin and fibronectin on the expression of the myogenic phenotype. Differentiation 40: 150-157.
96. Weston CR, Lambright DG, Davis RJ (2002) Signal transduction. MAP kinase signaling specificity. Science 296: 2345-2347.
97. Wijelath ES, Rahman S, Namekata M, Murray J, Nishimura T, Mostafavi-Pour Z, Patel Y, Suda Y, Humphries MJ, Sobel M (2006) Heparin-II domain of fibronectin is a vascular endothelial growth factor-binding domain: enhancement of VEGF biological activity by a singular growth factor/matrix protein synergism. Circ Res 99: 853-860
98. Wojcik L, Sawicka A, Rivera S, Zalewska T (2009) Neurogenesis in gerbil hippocampus following brain ischemia: focus on the involvement of metalloproteinases. Acta Neurobiol Exp (Wars) 69: 52-61.
99. Xu J, Rodriguez D, Petitclerc E, et al.(2001) Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo. J Cell Biol 154: 1069-1080.
100. Yamada KM, Even-Ram S (2002) Integrin regulation of growth receptors. Nat Cell Biol 4: E75-76.
101. Yang Y, Candelario-Jalil E, Thompson JF (2010) Increased intranuclear metalloproteinase activity in neurons interferes with oxidative DNA repair in focal cerebral ischemia. J Neurochem; 112: 134-149.
102. Yarwood SJ, Woodgett JR (2001) Extracellular matrix composition determines the transcriptional response to epidermal growth factor receptor activation. PNAS 98: 4472-4477.
103. Yong VW (2005) Metalloproteinases mediators of pathology and regeneration in the CNS. Nat Rev Neurosci 6: 931-944.
104. Zhao J, Heinz R, Guan JL (1998) Regulation of the cell cycle by focal adhesion kinase. J Cell Biol 143: 1997-2008.
105. Zhao J, Zheng C, Guan J (2000) Pyk2 and FAK differentially regulate progression of the cell cycle. J Cell Sci.113: 3063-3072.
106. Ziemka-Nalecz M, Wojcik-Stanaszek L, Zajac H, Zalewska T. FAK- and Pyk2-coupled pathway may contribute to the neurogenesis in gerbil hippocampus after ischemia. (Abstract) 10th International Symposium "Molecular Basis of Pathology and Therapy in Neurological Disorders" 2010, p.89.
107. Zipori D (2004) Mesenchymal stem cells: Harnessing cell plasticity to tissue and organ repair. Blood Cells Mol Dis 33: 211-215.
108. Zuo J, Ferguson TA, Hernandez YJ, Stetler-Stevenson WG, Muir D (1998) Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J. Neurosci 18: 5203-5211.