Fibronectin attenuates process outgrowth in oligodendrocytes by mislocalizing MMP-9 activity

Molecular and Cellular Neuroscience

Volumn 42, Issue 3, 2009, Pages 234-242

  Šišková, Zuzana ^a   Yong, V Wee ^b   Nomden, Anita ^a   van Strien, Miriam ^c   Hoekstra, Dick ^a   Baron, Wia ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b UNIVERSITY OF CALGARY   (Canada)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

ECM; MMP 9; Myelin biogenesis; Oligodendrocytes; Process budding

Indexed keywords

FIBRONECTIN; GELATINASE B; MEROSIN; PROTEIN KINASE C;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; GROWTH INHIBITION; MYELIN SHEATH; MYELINATION; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; OLIGODENDROGLIA; PERIKARYON; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; CELL DIFFERENTIATION; CELL SURFACE EXTENSIONS; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; EXTRACELLULAR MATRIX; FIBRONECTINS; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; OLIGODENDROGLIA; PROTEIN KINASE C; RATS; RATS, WISTAR;

EID: 69249234725     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.07.005     Document Type: Article

References (56)

1. Ahmed Z., Dent R.G., Leadbeater W.E., Smith C., Berry M., and Logan A. Matrix metalloproteases: degradation of the inhibitory environment of the transected optic nerve and the scar by regenerating axons. Mol. Cell. Neurosci. 28 (2005) 64-78
2. Baker E.A., Stephenson T.J., Reed M.W., and Brown N.J. Expression of proteinases and inhibitors in human breast cancer progression and survival. Mol. Pathol. 55 (2002) 300-304
3. Baron W., De Jonge J.C., de Vries H., and Hoekstra D. Regulation of oligodendrocyte differentiation: protein kinase C activation prevents differentiation of O2A progenitor cells towards oligodendrocytes. Glia 22 (1998) 121-129
4. Baron W., Shattil S.J., and ffrench-Constant C. The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. EMBO J. 21 (2002) 1957-1966
5. Baron W., Decker L., Colognato H., and ffrench-Constant C. Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr. Biol. 13 (2003) 151-155
6. Baron W., Colognato H., and ffrench-Constant C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia 49 (2005) 467-479
7. Bernardo M.M., and Fridman R. TIMP-2 (tissue inhibitor of metalloproteinase-2) regulates MMP-2 (matrix metalloproteinase-2) activity in the extracellular environment after pro-MMP-2 activation by MT1 (membrane type 1)-MMP. Biochem. J. 374 (2003) 739-745
8. Bouvier-Labit C., Liprandi A., Monti G., Pellissier J.F., and Figarella-Branger D. CD44H is expressed by cells of the oligodendrocyte lineage and by oligodendrogliomas in humans. J. Neurooncol. 60 (2002) 127-134
9. Brooks P.C., Stromblad S., Sanders L.C., von Schalscha T.L., Aimes R.T., Stetler-Stevenson W.G., Quigley J.P., and Cheresh D.A. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85 (1996) 683-693
10. Buttery P.C., and ffrench-Constant C. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol. Cell. Neurosci. 3 (1999) 199-212
11. Cauwe B., Van den Steen P.E., and Opdenakker G. The biochemical, biological, and pathological kaleidoscope of cell surface substrates processed by matrix metalloproteinases. Crit. Rev. Biochem. Mol. Biol. 42 (2007) 113-185
12. Chakraborti S., Mandal M., Das S., Mandal A., and Chakraborti T. Regulation of matrix metalloproteinases: an overview. Mol. Cell. Biochem. 253 (2003) 269-285
13. Chun S.J., Rasband M.N., Sidman R.L., Habib A.A., and Vartanian T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J. Cell Biol. 162 (2003) 397-408
14. Colognato H., Baron W., Avellana-Adalid V., Relvas J.B., Baron-Van Evercooren A., Georges-Labouesse E., and ffrench-Constant C. CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 11 (2002) 833-841
15. Colognato H., Ramachandrappa S., Olsen I.M., and ffrench-Constant C. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J. Cell Biol. 167 (2004) 365-375
16. Franklin R.J., and ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9 (2008) 839-855
17. Geurts N., Martens E., Van Aelst I., Proost P., Opdenakker G., and Van den Steen P.E. Beta-hematin interaction with the hemopexin domain of gelatinase B/MMP-9 provokes autocatalytic processing of the propeptide, thereby priming activation by MMP-3. Biochemistry 47 (2008) 2689-2699
18. Hoshina N., Tezuka T., Yokoyama K., Kozuka-Hata H., Oyama M., and Yamamoto T. Focal adhesion kinase regulates laminin-induced oligodendroglial process outgrowth. Genes Cells 12 (2007) 1245-1254
19. Kiaei M., Kipiani K., Calingasan N.Y., Wille E., Chen J., Heissig B., Rafii S., Lorenzl S., and Beal M.F. Matrix metalloproteinase-9 regulates TNF-α and FasL expression in neuronal, glial cells and its absence extends life in a transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 205 (2007) 74-81
20. Hardy R., and Reynolds R. Neuron-oligodendroglial interactions during central nervous system development. J. Neurosci. Res. 36 (1993) 121-126
21. Larsen P.H., and Yong V.W. The expression of matrix metalloproteinase-12 by oligodendrocytes regulates their maturation and morphological differentiation. J. Neurosci. 24 (2004) 7597-7603
22. Larsen P.H., Wells J.E., Stallcup W.B., Opdenakker G., and Yong V.W. Matrix metalloproteinase-9 facilitates remyelination in part by processing the inhibitory NG2 proteoglycan. J. Neurosci. 23 (2003) 11127-11135
23. Larsen P.H., DaSilva A.G., Conant K., and Yong V.W. Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J. Neurosci. 26 (2006) 2207-2214
24. Lemaitre V., and D'Armiento J. Matrix metalloproteinases in development and disease. Birth Defects Res. C. Embryo Today 78 (2006) 1-10
25. Maier O., van der Heide T., van Dam A.M., Baron W., de Vries H., and Hoekstra D. Alteration of the extracellular matrix interferes with raft association of neurofascin in oligodendrocytes. Potential significance for multiple sclerosis. Mol. Cell Neurosci. 28 (2005) 390-401
26. Mira E., Lacalle R.A., Buesa J.M., de Buitrago G.G., Jimenez-Baranda S., Gomez-Mouton C., Martinez-A C., and Manes S. Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J. Cell Sci. 117 (2004) 1847-1857
27. Moretto G., Xu R.Y., and Kim S.U. CD44 expression in human astrocytes and oligodendrocytes in culture. J. Neuropathol. Exp. Neurol. 52 (1993) 419-423
28. Nagase H., and Woessner J.F.J. . Matrix metalloproteinases. J. Biol. Chem. 274 (1999) 21491-21494
29. Oh L.Y., Larsen P.H., Krekoski C.A., Edwards D.R., Donovan F., Werb Z., and Yong V.W. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J. Neurosci. 19 (1999) 8464-8475
30. Olson M.W., Gervasi D.C., Mobashery S., and Fridman R. Kinetic analysis of the binding of human matrix metalloproteinase-2 and -9 to tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2. J. Biol. Chem. 272 (1997) 29975-29983
31. Opdenakker G., Nelissen I., and van Damme J. Functional roles and therapeutic targeting of gelatinase B and chemokines in multiple sclerosis. Lancet Neurol. 2 (2003) 747-756
32. Osterhout D.J., Wolven A., Wolf R.M., Resh M.D., and Chao M.V. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J. Cell Biol. 145 (1999) 1209-1218
33. Pfeiffer S.E., Warrington A.E., and Bansal R. The oligodendrocyte and its many cellular processes. Trends Cell Biol. 3 (1993) 191-197
34. Ranscht B., Clapshaw P.A., Price J., Noble M., and Seifert W. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc. Natl. Acad. Sci. U S A 79 (1982) 2709-2713
35. Relvas J.B., Setzu A., Baron W., Buttery P.C., LaFlamme S.E., Franklin R.J., and ffrench-Constant C. Expression of dominant-negative and chimeric subunits reveals an essential role for beta1 integrin during myelination. Curr. Biol. 11 (2001) 1039-1043
36. Richter-Landsberg C., and Heinrich M. OLN-93: a new permanent oligodendroglia cell line derived from primary rat brain glial cultures. J. Neurosci. Res. 45 (1996) 161-173
37. Sbai O., Ferhat L., Bernard A., Gueye Y., Ould-Yahoui A., Thiolloy S., Charrat E., Charton G., Tremblay E., Risso J.J., Chauvin J.P., Arsanto J.P., Rivera S., and Khrestchatisky M. Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol. Cell Neurosci. 39 (2008) 549-568
38. Shubayev V.I., and Myers R.R. Matrix metalloproteinase-9 promotes nerve growth factor-induced neurite elongation but not new sprout formation in vitro. J. Neurosci. Res. 77 (2004) 229-239
39. Šišková Z., Baron W., de Vries H., and Hoekstra D. Fibronectin impedes "myelin" sheet directed flow in oligodendrocytes: a role for the beta 1 integrin mediated PKC signaling pathway in vesicular trafficking. Mol. Cell Neurosci. 33 (2006) 150-159
40. Sobel R.A., and Mitchell M.E. Fibronectin in multiple sclerosis. Am. J. Pathol. 135 (1989) 161-168
41. Stefanidakis M., and Koivunen E. Cell-surface association between matrix metalloproteinases: role of the complexes in leukocyte migration and cancer progression. Blood 108 (2006) 1441-1450
42. Stefanidakis M., Ruohtula T., Borregaard N., Gahmberg C.G., and Koivunen E. Intracellular and cell surface localization of a complex between alphaMbeta2 integrin and promatrix metalloproteinase-9 progelatinase in neutrophils. J. Immunol. 172 (2004) 7060-7068
43. Tuohy T.M., Wallingford N., Liu Y., Chan F.H., Rizvi T., Xing R., Bebo B., Rao M.S., and Sherman L.S. CD44 overexpression by oligodendrocytes: a novel mouse model of inflammation-independent demyelination and dysmyelination. Glia 47 (2004) 335-345
44. Uhm J.H., Dooley N.P., Oh L.Y., and Yong V.W. Oligodendrocytes utilize a matrix metalloproteinase, MMP-9, to extend processes along an astrocyte extracellular matrix. Glia 22 (1998) 53-63
45. Vaillant C., Meissirel C., Mutin M., Belin M.F., Lund L.R., and Thomasset N. MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol. Cell Neurosci. 24 (2003) 395-408
46. van Horssen J., Bo L., Vos C.M., Virtanen I., and de Vries H.E. Basement membrane proteins in multiple sclerosis-associated inflammatory cuffs: potential role in influx and transport of leukocytes. J. Neuropathol. Exp. Neurol. 64 (2005) 722-729
47. van Horssen J., Dijkstra C., and de Vries H.E. The extracellular matrix in multiple sclerosis pathology. J. Neurochem. 103 (2007) 1293-1301
48. VanSaun M.N., and Matrisian L.M. Matrix metalloproteinases and cellular motility in development and disease. Birth Defects Res. C. Embryo Today 78 (2006) 69-79
49. Vecil G.G., Larsen P.H., Corley S.M., Herx L.M., Besson A., Goodyer C.G., and Yong V.W. 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 (2000) 212-224
50. Visse R., and Nagase H. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92 (2003) 827-839
51. Yong V.W. Metalloproteinases: mediators of pathology and regeneration in the CNS. Nat. Rev. Neurosci. 6 (2005) 931-944
52. Yong V.W., Power C., Forsyth P., and Edwards D.R. Metalloproteinases in biology and pathology of the nervous system. Nat.Rev. Neurosci. 2 (2001) 502-511
53. Yong V.W., Giuliani F., Xue M., Bar-Or A., and Metz L.M. Experimental models of neuroprotection relevant to multiple sclerosis. Neurology 68 (2007) 32-37
54. Yoshizaki T., Maruyama Y., Sato H., and Furukawa M. Expression of tissue inhibitor of matrix metalloproteinase-2 correlates with activation of matrix metalloproteinase-2 and predicts poor prognosis in tongue squamous cell carcinoma. Int. J. Cancer 95 (2001) 44-50
55. Yu W.H., Woessner Jr. J.F., McNeish J.D., and 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 (2002) 307-323
56. Zhang Q., Furukawa K., Chen H.H., Sakakibara T., Urano T., and Furukawa K. Metastatic potential of mouse Lewis lung cancer cells is regulated via ganglioside GM1 by modulating the matrix metalloprotease-9 localization in lipid rafts. J. Biol. Chem. 281 (2006) 18145-18155