Matrix metalloproteinases in the adult brain physiology: A link between c-Fos, AP-1 and remodeling of neuronal connections?

EMBO Journal

Volumn 21, Issue 24, 2002, Pages 6643-6648

  Kaczmarek, Leszek ^a   Lapinska Dzwonek, Joanna ^a   Szymczak, Sylwia ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Dystroglycan; Extracellular matrix; Hippocampus; Neuronal plasticity; TIMP

Indexed keywords

MATRIX METALLOPROTEINASE INHIBITOR; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TISSUE INHIBITOR OF METALLOPROTEINASE 4; TRANSCRIPTION FACTOR AP 1;

BRAIN DISEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; GLIA CELL; LEARNING; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; ONCOGENE C FOS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

ANIMALS; BRAIN; CYTOSKELETAL PROTEINS; DYSTROGLYCANS; HIPPOCAMPUS; HUMANS; MATRIX METALLOPROTEINASES; MEMBRANE GLYCOPROTEINS; MODELS, BIOLOGICAL; NERVOUS SYSTEM DISEASES; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSCRIPTION FACTOR AP-1;

EID: 0037121996     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf676     Document Type: Review

References (71)

1. Alitalo, R., Partanen, J., Pertovaara, L., Holtta, E., Sistonen, L., Andersson, L. and Alitalo, K. (1990) Increased erythroid potentiating activity/tissue inhibitor of metalloproteinases and jun/fos transcription factor complex characterize tumor promoter-induced megakaryoblastic differentiation of K562 leukemia cells. Blood, 75, 1974-1982.
2. Asahi, M., Asahi, K., Jung, J.C., del Zoppo, G.J., Fini, M.E. and Lo, E.H. (2000) Role for matrix metalloproteinase 9 after focal cerebral ischemia: Effects of gene knockout and enzyme inhibition with BB-94. J. Cereb. Blood Flow Metab., 20, 1681-1689.
3. Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J.C., Moskowitz, M.A., Fini, M.E. and Lo, E.H. (2001) 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.
4. Backstrom, J.R., Lim, G.P., Cullen, M.J. and Tokes, Z.A. (1996) Matrix metalloproteinase-9 (MMP-9) is synthesized in neurons of the human hippocampus and is capable of degrading the amyloid-β peptide (1-40). J. Neurosci., 16, 7910-7919.
5. Baranes, D., Lederfein, D., Huang, Y.Y., Chen, M., Bailey, C.H. and Kandel, E.R. (1998) Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron, 21, 813-825.
6. Benbow, U. and Brinckerhoff, C.E. (1997) The AP-1 site and MMP gene regulation: What is all the fuss about? Matrix Biol., 15, 519-526.
7. Botelho, F.M., Edwards, D.R. and Richards, C.D. (1998) Oncostatin M stimulates c-Fos to bind a transcriptionally responsive AP-1 element within the tissue inhibitor of metalloproteinase-1 promoter. J. Biol. Chem., 273, 5211-5218.
8. Bugno, M., Greave, L., Gatsios, P., Koj, A., Heinrich, P.C., Travis, J. and Kordula, T. (1995) Identification of the interleukin-6/oncostation M response element in the rat tissue inhibitor of metalloproteinases-1 promoter. Nucleic Acids Res., 23, 5041-5047.
9. Campbell, C.E., Flenniken, A.M., Skup, D. and Williams, B.R. (1991) Identification of a serum- and phorbol ester-responsive element in the murine tissue inhibitor of metalloproteinase gene. J. Biol. Chem., 266, 7199-7206.
10. Chun, D., Gall, C.M., Bi, X. and Lynch, G. (2001) Evidence that integrins contribute to multiple stages in the consolidation of long term potentiation in rat hippocampus. Neuroscience, 105, 815-829.
11. Clark, A.W., Krekoski, C.A., Bou, S.S., Chapman, K.R. and Edwards, D.R. (1997) Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci. Lett., 238, 53-58.
12. Edwards, D.R., Rocheleau, H., Sharma, R.R., Wills, A.J., Cowie, A., Hassell, J.A. and Heath, J.K. (1992) Involvement of AP1 and PEA3 binding sites in the regulation of murine tissue inhibitor of metalloproteinases-1 (TIMP-1) transcription. Biochim. Biophys. Acta, 1171, 41-55.
13. Fager, N. and Jaworski, D.M. (2000) Differential spatial distribution and temporal regulation of tissue inhibitor of metalloproteinase mRNA expression during rat central nervous system development. Mech. Dev., 98, 105-109.
14. Frey, U. and Morris, R.G. (1998) Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci., 21, 181-188.
15. Gasche, Y., Fujimura, M., Morita-Fujimura, Y., Copin, J.C., Kawase, M., Massengale, J. and Chan, P.H. (1999) Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: A possible role in blood-brain barrier dysfunction. J. Cereb. Blood Flow Metab., 19, 1020-1028.
16. Górecki, D.C., Lukasiuk, K., Szklarczyk, A.W. and Kaczmarek, L. (1998) Kainate-evoked changes in dystrophin mRNA levels in the rat hippocampus. Neuroscience, 84, 467-477.
17. Górecki, D.C., Szklarczyk, A., Lukasiuk, K., Kaczmarek, L. and Simons, J.P. (1999) Differential seizure-induced and developmental changes of neurexin expression. Mol. Cell. Neurosci., 13, 218-227.
18. Hayashita-Kinoh, H., Kinoh, H., Okada, A., Komori, K., Itoh, Y., Chiba, T., Kajita, M., Yana, I. and Seiki, M. (2001) Membrane-type 5 matrix metalloproteinase is expressed in differentiated neurons and regulates axonal growth. Cell Growth Differ., 12, 573-580.
19. Hebb, D.O. (1949) Organization of Behavior. Wiley, New York, NY.
20. Heo, J.H., Lucero, J., Abumiya, T., Koziol, J.A., Copeland, B.R. and del Zoppo, G.J. (1999) Matrix metalloproteinases increase very early during experimental focal cerebral ischemia. J. Cereb. Blood Flow Metab., 19, 624-633.
21. Herdegen, T. and Leah, J.D. (1998) Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev., 28, 370-490.
22. Jaworski, D.M. (2000) Developmental regulation of membrane type-5 matrix metalloproteinase (MT5-MMP) expression in the rat nervous system. Brain Res., 860, 174-177.
23. Jaworski, J. et al. (1999) Neuronal excitation-driven and AP-1-dependent activation of timp-1 gene expression in rodent hippocampus. J. Biol. Chem., 274, 28106-28112.
24. Jiang, X., Namura, S. and Nagata, I. (2001) Matrix metalloproteinase inhibitor KB-R7785 attenuates brain damage resulting from permanent focal cerebral ischemia in mice. Neurosci. Lett., 305, 41-44.
25. Job, C. and Eberwine, J.(2001) Localization and translation of mRNA in dendrites and axons. Nat. Rev. Neurosci., 2, 889-898.
26. Kaczmarek, L. (1993) Molecular biology of vertebrate learning: Is c-fos a new beginning? J. Neurosci. Res., 34, 377-381.
27. Kaczmarek, L. (2002) c-Fos in learning: beyond the mapping of neuronal activity. In Kaczmarek, L. and Robertson, H.A. (eds), Handbook of Chemical Neuroanatomy: Immediate Early Genes and Inducible Transcription Factors in Mapping of the Central Nervous System Function and Dysfunction. Elsevier, Amsterdam, The Netherlands, pp. 189-216.
28. Kaczmarek, L. and Chaudhuri, A. (1997) Sensory regulation of immediate-early gene expression in mammalian visual cortex: Implications for functional mapping and neural plasticity. Brain Res. Rev., 23, 237-256.
29. Kaminska, B., Filipkowski, R.K., Zurkowska, G., Lason, W., Przewlocki, R. and Kaczmarek, L. (1994) Dynamic changes in composition of AP-1 transcription factor DNA binding activity in rat brain following kainate induced seizures and cell death. Eur. J. Neurosci., 6, 1558-1566.
30. Kridel, S.J., Chen, E., Kotra, L.P., Howard, E.W., Mobashery, S. and Smith, J.W. (2001) Substrate hydrolysis by matrix metalloproteinase-9. J. Biol. Chem., 276, 20572-20578.
31. Lee, R., Kermani, P., Teng, K.K. and Hempstead, B.L. (2001) Regulation of cell survival by secreted proneurotrophins. Science, 294, 1945-1948.
32. Leppert, D., Lindberg, R.L.P., Kappos, L. and Leib, S.L. (2001) Matrix metalloproteinases: Multifunctional effectors of inflammation in multiple sclerosis and bacterial meningitis. Brain Res. Rev., 36, 249-257.
33. Liu, Z., Zhou, X., Shapiro, S.D., Shipley, J.M., Twining, S.S., Diaz, L.A., Senior, R.M. and Werb, Z. (2000) The serpin α1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell, 102, 647-655.
34. Logan, S.K., Garabedian, M.J., Campbell, C.E. and Werb, Z. (1996) Synergistic transcriptional activation of the tissue inhibitor of metallproteinases-1 promoter via functional intercation of AP-1 and Ets-1 transcription factors. J. Biol. Chem., 271, 774-782.
35. Lukes, A., Mun-Bryce, S., Lukes, M. and Rosenberg, G.A. (1999) Extracellular matrix degradation by metalloproteinases and central nervous system diseases. Mol. Neurobiol., 19, 267-284.
36. Madani, R., Hulo, S., Toni, N., Madani, H., Steimer, T., Muller, D. and Vassalli, J.D. (1999) Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J., 18, 3007-3012.
37. Martin, K.C., Barad, M. and Kandel, E.R. (2000) Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol., 10, 587-592.
38. Massova, I., Kotra, L.P., Fridman, R. and Mobashery, S. (1998) Matrix metalloproteinases: Structures, evolution, and diversification. FASEB J., 12, 1075-1095.
39. Meiri, N., Masos, T., Rosenblum, K., Miskin, R. and Dudai, Y. (1994) Overexpression of urokinase-type plasminogen activator in transgenic mice is correlated with impaired learning. Proc. Natl. Acad. Sci. USA, 91, 3196-3200.
40. Moore, S.A. et al. (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature, 418, 422-425.
41. Mun-Bryce, S. and Rosenberg, G.A. (1998) Matrix metalloproteinases in cerebrovascular disease. J. Cereb. Blood Flow Metab., 18, 1163-1172.
42. Nedivi, E., Hevroni, D., Naot, D., Israeli, D. and Citri, Y. (1993) Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature, 363, 718-722.
43. Pagenstecher, A., Stalder, A.K. and Campbell, I.L. (1997) RNAse protection assays for the simultaneous and semiquantitative analysis of multiple murine matrix metalloproteinase (MMP) and MMP inhibitor mRNAs. J. Immunol. Methods, 206, 1-9.
44. Qian, Z., Gilbert, M.E., Colicos, M.A., Kandel, E.R. and Kuhl, D. (1993) Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature, 361, 453-457.
45. Rivera, S., Tremblay, E., Timsit, S., Canals, O., Ben-Ari, Y. and Khrestchatisky, M. (1997) Tissue inhibitor of metalloproteinases-1 (TIMP-1) is differentially induced in neurons and astrocytes after seizures: Evidence for developmental, immediate early gene, and lesion response. J. Neurosci., 17, 4223-4235.
46. Rivera, S., Ogier, C., Jourquin, J., Timsit, S., Szklarczyk, A., Miller, K., Gearing, A.J.H., Kaczmarek, L. and Khrestchatisky, M. (2002) Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with cell demise, neuroinflammation and repair processes after global forebrain ischemia. Eur. J. Neurosci., 15, 19-32.
47. Rohrbough, J., Grotewiel, M.S., Davis, R.L. and Broadie, K. (2000) Integrin-mediated regulation of synaptic morphology, transmission, and plasticity. J. Neurosci., 20, 6868-6878.
48. Romanic, A.M., White, R.F., Arleth, A.J., Ohlstein, E.H. and Barone, F.C. (1998). Matrix metalloproteinase expression increases after cerebral focal ischemia in rats. Inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke, 29, 1020-1030.
49. Rooprai, H.K. and McCormick, D. (1997) Proteases and their inhibitors in human brain tumours: A review. Anticancer Res., 17, 4151-4162.
50. Rosa, G., Ceccarini, M., Cavaldesi, M., Zini, M. and Petrucci, T.C. (1996) Localization of the dystrophin binding site at the carboxyl terminus of β-dystroglycan. Biochem. Biophys. Res. Commun., 223, 272-277.
51. Rosenberg, G.A. (1995) Matrix metalloproteinases in brain injury. J. Neurotrauma, 12, 833-842.
52. Rosenberg, G.A., Navratil, M., Barone, F. and Feuerstein, G.Z. (1996) Proteolytic cascade enzymes increase in focal cerebral ischemia in rat. J. Cereb. Blood Flow Metab., 16, 360-366.
53. Rosenberg, G.A., Estrada, E.Y. and Dencoff, J.E. (1998) Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. Stroke, 29, 2189-2195.
54. Sato, H. and Seiki, M. (1993) Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene, 8, 395-405.
55. Seeds, N.W., Williams, B.L. and Bickford, P.C. (1995) Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science, 270, 1992-1994.
56. Sekine-Aizawa, Y. et al. (2001) Matrix metalloproteinase (MMP) system in brain: Identification and characterization of brain-specific MMP highly expressed in cerebellum. Eur. J. Neurosci., 13, 935-948.
57. Sternlicht, M.D. and Werb, Z. (2001) How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol., 17, 463-516.
58. Steward, O. and Schuman, E.M. (2001) Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci., 24, 299-325.
59. Sugita, S., Saito, F., Tang, J., Satz, J., Campbell, K. and Sudhof, T.C. (2001) A stoichiometric complex of neurexins and dystroglycan in brain. J. Cell Biol., 154, 435-445.
60. Szklarczyk, A., Lapinska, J., Rylski, M., McKay, R.D.G. and Kaczmarek, L. (2002) Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J. Neurosci., 22, 920-930.
61. Taishi, P., Sanchez, C., Wang, Y., Fang, J., Harding, J.W. and Krueger, J.M. (2001) Conditions that affect sleep alter the expression of molecules associated with synaptic plasticity. Am. J. Physiol. Regul. Integr. Comp. Physiol., 281, R839-R845.
62. Vaillant, C., Didier-Bazes, M., Hutter, A., Belin, M.F. and Thomasset, N. (1999) Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the postnatal developing rat cerebellum. J. Neurosci., 19, 4994-5004.
63. Vecil, G.G., Larsen, P.H., Corley, S.M., Herx, L.M., Besson, A., Goodyer, C.G. and Yong, V.W. (2000) 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.
64. Vu, T.H. and Werb, Z. (2000) Matrix metalloproteinases: Effectors of development and normal physiology. Genes Dev., 14, 2123-2133.
65. Woessner, J.F. and Nagase, H. (2000) Matrix Metalloproteinases and TIMPs. Oxford University Press, Oxford, UK.
66. Wright, W., Eniko, A., Kramar, E.A., Meighan, S.E. and Harding, J.W. (2002) Extracellular matrix molecules, long-term potentiation, memory consolidation and the brain angiotensin system. Peptides, 23, 221-246.
67. Yamada, H. et al. (2001) Processing of β-dystroglycan by matrix metalloproteinase disrupts the link between the extracellular matrix and cell membrane via the dystroglycan complex. Hum. Mol. Genet. 10, 1563-1569.
68. Yong, V.W., Krekoski, C.A., Forsyth, P.A., Bell, R. and Edwards, D.R. (1998) Matrix metalloproteinases and diseases of the central nervous system. Trends Neurosci., 21, 75-80.
69. Yong, V.W., Power, C., Forsyth, P. and Edwards, D.R. (2001) Metalloproteinases in biology and pathology of the nervous system. Nat. Rev. Neurosci., 2, 502-511.
70. Yoshida, S. and Shiosaka, S. (1999) Plasticity-related serine proteases in the brain. Int. J. Mol. Med., 3, 405-409.
71. Zhang, J.W., Deb, S. and Gottschall, P.E. (1998) Regional and differential expression of gelatinases in rat brain after systemic kainic acid or bicuculline administration. Eur. J. Neurosci., 10, 3358-3368.