Synaptic cell adhesion molecule-2 and collapsin response mediator protein-2 are novel members of the matrix metalloproteinase-9 degradome

Journal of Neurochemistry

Volumn 122, Issue 4, 2012, Pages 775-788

  Bajor, Malgorzata ^a   Michaluk, Piotr ^a   Gulyassy, Peter ^b   Kekesi, Adrienna Katalin ^b   Juhasz, Gabor ^b   Kaczmarek, Leszek ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

Author keywords

CRMP 2; degradome; MMP 9; proteolysis; synaptoneurosomes; SynCAM 2

Indexed keywords

CELL ADHESION MOLECULE; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GELATINASE B; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; SYNAPTIC CELL ADHESION MOLECULE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MALE; MASS SPECTROMETRY; MEMORY; MOUSE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NEUROSYNAPTOSOME; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SYNAPSE; SYNAPTOSOME; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DENSITOMETRY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; EXCITATORY AMINO ACID AGONISTS; GLUTAMIC ACID; HIPPOCAMPUS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; N-METHYLASPARTATE; NERVE TISSUE PROTEINS; NEURAL CELL ADHESION MOLECULES; SYNAPTOSOMES; TANDEM MASS SPECTROMETRY;

MUS;

EID: 84864137954     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2012.07829.x     Document Type: Article

References (79)

1. Agrawal S., Anderson P., Durbeej M., van Rooijen N., Ivars F., Opdenakker G., and, Sorokin L. M., (2006) Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 203, 1007-1019.
2. Arimura N., Menager C., Kawano Y., et al. (2005) Phosphorylation by Rho kinase regulates CRMP-2 activity in growth cones. Mol. Cell. Biol. 25, 9973-9984.
3. 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.
4. 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.
5. 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-beta peptide (1-40). J. Neurosci. 16, 7910-7919.
6. Bayes A., van de Lagemaat L. N., Collins M. O., Croning M. D., Whittle I. R., Choudhary J. S., and, Grant S. G., (2011) Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat. Neurosci. 14, 19-21.
7. Benavides J., Claustre Y., and, Scatton B., (1988) L-glutamate increases internal free calcium levels in synaptoneurosomes from immature rat brain via quisqualate receptors. J. Neurosci. 8, 3607-3615.
8. Biederer T., Sara Y., Mozhayeva M., Atasoy D., Liu X., Kavalali E. T., and, Sudhof T. C., (2002) SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525-1531.
9. Bilousova T. V., Dansie L., Ngo M., Aye J., Charles J. R., Ethell D. W., and, Ethell I. M., (2009) Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J. Med. Gen. 46, 94-102.
10. Bretin S., Rogemond V., Marin P., Maus M., Torrens Y., Honnorat J., Glowinski J., Prémont J., and, Gauchy C., (2006) Calpain product of WT-CRMP2 reduces the amount of surface NR2B NMDA receptor subunit. J. Neurochem. 98, 1252-1265.
11. Brittain J. M., Piekarz A. D., Wang Y., Kondo T., Cummins T. R., and, Khanna R., (2009) An atypical role for collapsin response mediator protein 2 (CRMP-2) in neurotransmitter release via interaction with presynaptic voltage-gated calcium channels. J. Biol. Chem. 284, 31375-31390.
12. Butler G. S., and, Overall C. M., (2009) Updated biological roles for matrix metalloproteinases and new "intracellular" substrates revealed by degradomics. Biochemistry 48, 10830-10845.
13. Cauwe B., and, Opdenakker G., (2010) Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit. Rev. Biochem. Mol. Biol. 45, 351-423.
14. Cauwe B., Martens E., Proost P., and, Opdenakker G., (2009) Multidimensional degradomics identifies systemic autoantigens and intracellular matrix proteins as novel gelatinase B/MMP-9 substrates. Integr. Biol. (Camb) 1, 404-426.
15. Conant K., Wang Y., Szklarczyk A., Dudak A., Mattson M. P., and, Lim S. T., (2010) Matrix metalloproteinase-dependent shedding of intercellular adhesion molecule-5 occurs with long-term potentiation. Neuroscience 166, 508-521.
16. Conant K., Lonskaya I., Szklarczyk A., Krall C., Steiner J., Maguire-Zeiss K., and, Lim S. T., (2011) Methamphetamine-associated cleavage of the synaptic adhesion molecule intercellular adhesion molecule-5. J. Neurochem. 118, 521-532.
17. Czech T., Yang J. W., Csaszar E., Kappler J., Baumgartner C., and, Lubec G., (2004) Reduction of hippocampal collapsin response mediated protein-2 in patients with mesial temporal lobe epilepsy. Neurochem. Res. 29, 2189-2196.
18. De Camilli P., Cameron R., and, Greengard P., (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections. J. Cell Biol. 96, 1337-1354.
19. Dominguez R., Liu R., and, Baudry M., (2007) 17-Beta-estradiol-mediated activation of extracellular-signal regulated kinase, phosphatidylinositol 3-kinase/protein kinase B-Akt and N-methyl-D-aspartate receptor phosphorylation in cortical synaptoneurosomes. J. Neurochem. 101, 232-240.
20. Emes R. D., and, Grant S. G., (2011) The human postsynaptic density shares conserved elements with proteomes of unicellular eukaryotes and prokaryotes. Front. Neurosci. 5, 44-53.
21. Emes R. D., Pocklington A. J., Anderson C. N., et al. (2008) Evolutionary expansion and anatomical specialization of synapse proteome complexity. Nat. Neurosci. 11, 799-806.
22. Fogel A. I., Akins M. R., Krupp A. J., Stagi M., Stein V., and, Biederer T., (2007) SynCAMs organize synapses through heterophilic adhesion. J. Neurosci. 27, 12516-12530.
23. Franken S., Junghans U., Rosslenbroich V., Baader S. L., Hoffmann R., Gieselmann V., Viebahn C., and, Kappler J., (2003) Collapsin response mediator proteins of neonatal rat brain interact with chondroitin sulfate. J. Biol. Chem. 278, 3241-3250.
24. Fukata Y., Itoh T. J., Kimura T., et al. (2002) CRMP-2 binds to tubulin heterodimers to promote microtubule assembly. Nat. Cell Biol. 4, 583-591.
25. Gerrow K., Romorini S., Nabi S. M., Colicos M. A., Sala C., and, El-Husseini A., (2006) A preformed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49, 547-562.
26. Gu Y., and, Ihara Y., (2000) Evidence that collapsin response mediator protein-2 is involved in the dynamics of microtubules. J. Biol. Chem. 275, 17917-17920.
27. Gu Y., Hamajima N., and, Ihara Y., (2000) Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry, 39, 4267-4275.
28. Gu Z., Kaul M., Yan B., Kridel S. J., Cui J., Strongin A., Smith J. W., Liddington R. C., and, Lipton S. A., (2002) S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190.
29. Gu Z., Cui J., Brown S., Fridman R., Mobashery S., Strongin A. Y., and, Lipton S. A., (2005) A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J. Neurosci. 25, 6401-6408.
30. Gursoy-Ozdemir Y., Qiu J., Matsuoka N., Bolay H., Bermpohl D., Jin H., Wang X., Rosenberg G. A., Lo E. H., and, Moskowitz M. A., (2004) Cortical spreading depression activates and upregulates MMP-9. J. Clin. Invest. 113, 1447-1455.
31. Hinkle C. L., Diestel S., Lieberman J., and, Maness P. F., (2006) Metalloprotease-induced ectodomain shedding of neural cell adhesion molecule (NCAM). J. Neurobiol. 66, 1378-1395.
32. Inagaki N., Chihara K., Arimura N., Menager C., Kawano Y., Matsuo N., Nishimura T., Amano M., and, Kaibuchi K., (2001) CRMP-2 induces axons in cultured hippocampal neurons. Nat. Neurosci. 4, 781-782.
33. Jiang S.X., Kappler J., Zurakowski B., Desbois A., Aylsworth A., and, Hou S.T., (2007) Calpain cleavage of collapsin response mediator proteins in ischemic mouse brain. Eur. J. Neurosci. 26, 801-809.
34. Kim J., Lilliehook C., Dudak A., Prox J., Saftig P., Federoff H. J., and, Lim S. T., (2010a) Activity-dependent alpha-cleavage of nectin-1 is mediated by a disintegrin and metalloprotease 10 (ADAM10). J. Biol. Chem. 285, 22919-22926.
35. Kim S. H., Fraser P. E., Westaway D., St George-Hyslop P. H., Ehrlich M. E., and, Gandy S., (2010b) Group II metabotropic glutamate receptor stimulation triggers production and release of Alzheimer's amyloid(beta)42 from isolated intact nerve terminals. J. Neurosci. 30, 3870-3875.
36. Klemmer P., Smit A. B., and, Li K. W., (2009) Proteomics analysis of immuno-precipitated synaptic protein complexes. J. Proteomics 72, 82-90.
37. Kovacs Z., Kekesi K. A., Baracskay P., Juhasz G., and, Czurko A., (2011) Doxycycline could aggravate the absence-like epileptic seizures of WAG/Rij rats via matrix metalloproteinase inhibition. Neurochem. Int. 59, 563-566.
38. 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.
39. Lim S. T., Chang A., Giuliano R. E., and, Federoff H. J., (2012) Ectodomain shedding of nectin-1 regulates the maintenance of dendritic spine density. J. Neurochem. 120, 741-751.
40. Lin K. T., Sloniowski S., Ethell D. W., and, Ethell I. M., (2008) Ephrin-B2-induced cleavage of EphB2 receptor is mediated by matrix metalloproteinases to trigger cell repulsion. J. Biol. Chem. 283, 28969-28979.
41. Lopez-Otin C., and, Overall C. M., (2002) Protease degradomics: a new challenge for proteomics. Nat. Rev. Mol. Cell Biol. 3, 509-519.
42. Marouga R., David S., and, Hawkins E., (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382, 669-678.
43. Meighan S. E., Meighan P. C., Choudhury P., Davis C. J., Olson M. L., Zornes P. A., Wright J. W., and, Harding J. W., (2006) Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J. Neurochem. 96, 1227-1241.
44. Michaluk P., and, Kaczmarek L., (2007) Matrix metalloproteinase-9 in glutamate-dependent adult brain function and dysfunction. Cell Death Differ. 14, 1255-1258.
45. Michaluk P., Kolodziej L., Mioduszewska B., Wilczynski G. M., Dzwonek J., Jaworski J., Gorecki D. C., Ottersen O. P., and, Kaczmarek L., (2007) Beta-dystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J. Biol. Chem. 282, 16036-16041.
46. Michaluk P., Wawrzyniak M., Alot P., et al. (2011) Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J. Cell Sci. 124, 3369-3380.
47. Micheva K. D., Busse B., Weiler N. C., O'Rourke N., and, Smith S. J., (2010) Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68, 639-653.
48. Mizoguchi H., Yamada K., and, Nabeshima T., (2008) Neuropsychotoxicity of abused drugs: involvement of matrix metalloproteinase-2 and -9 and tissue inhibitor of matrix metalloproteinase-2 in methamphetamine-induced behavioral sensitization and reward in rodents. J. Pharmacol. Sci. 106, 9-14.
49. Muddashetty R. S., Kelic S., Gross C., Xu M., and, Bassell G. J., (2007) Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J. Neurosci. 27, 5338-5348.
50. Nagy V., Bozdagi O., Matynia A., Balcerzyk M., Okulski P., Dzwonek J., Costa R. M., Silva A. J., Kaczmarek L., and, Huntley G. W., (2006) Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26, 1923-1934.
51. Nishimura T., Fukata Y., Kato K., Yamaguchi T., Matsuura Y., Kamiguchi H., and, Kaibuchi K., (2003) CRMP-2 regulates polarized Numb-mediated endocytosis for axon growth. Nat. Cell Biol. 5, 819-826.
52. Noble L. J., Donovan F., Igarashi T., Goussev S., and, Werb Z., (2002) Matrix metalloproteinases limit functional recovery after spinal cord injury by modulation of early vascular events. J. Neurosci. 22, 7526-7535.
53. Okulski P., Jay T. M., Jaworski J., Duniec K., Dzwonek J., Konopacki F. A., Wilczynski G. M., Sanchez-Capelo A., Mallet J., and, Kaczmarek L., (2007) TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol. Psychiat. 62, 359-362.
54. Pimenta A. F., Zhukareva V., Barbe M. F., Reinoso B. S., Grimley C., Henzel W., Fischer I., and, Levitt P., (1995) The limbic system-associated membrane protein is an Ig superfamily member that mediates selective neuronal growth and axon targeting. Neuron 15, 287-297.
55. Planas A. M., Sole S., and, Justicia C., (2001) Expression and activation of matrix metalloproteinase-2 and -9 in rat brain after transient focal cerebral ischemia. Neurobiol. Dis. 8, 834-846.
56. Prudova A., auf dem Keller U., Butler G. S., and, Overall C. M., (2010) Multiplex N-terminome analysis of MMP-2 and MMP-9 substrate degradomes by iTRAQ-TAILS quantitative proteomics. Mol. Cell. Proteomics 9, 894-911.
57. Rivera S., Ogier C., Jourquin J., Timsit S., Szklarczyk A. W., Miller K., Gearing A. J., Kaczmarek L., and, Khrestchatisky M., (2002) Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with neuronal death and glial reactivity after global forebrain ischemia. Eur. J. Neurosci. 15, 19-32.
58. Rivera S., Khrestchatisky M., Kaczmarek L., Rosenberg G. A., and, Jaworski D. M., (2010) Metzincin proteases and their inhibitors: foes or friends in nervous system physiology? J. Neurosci. 30, 15337-15357.
59. Rogemond V., Auger C., Giraudon P., Becchi M., Auvergnon N., Belin M. F., Honnorat J., and, Moradi-Ameli M., (2008) Processing and nuclear localization of CRMP2 during brain development induce neurite outgrowth inhibition. J. Biol. Chem. 283, 14751-14761.
60. Rosenberg G. A., Cunningham L. A., Wallace J., Alexander S., Estrada E. Y., Grossetete M., Razhagi A., Miller K., and, Gearing A., (2001) 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.
61. Sara Y., Biederer T., Atasoy D., Chubykin A., Mozhayeva M. G., Sudhof T. C., and, Kavalali E. T., (2005) Selective capability of SynCAM and neuroligin for functional synapse assembly. J. Neurosci. 25, 260-270.
62. Sbai O., Ould-Yahoui A., Ferhat L., et al. (2010) Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 58, 344-366.
63. Shinomura T., Nakao S., Adachi T., and, Shingu K., (1999) Clonidine inhibits and phorbol acetate activates glutamate release from rat spinal synaptoneurosomes. Anesth. Analg. 88, 1401-1405.
64. Takacs E., Nyilas R., Szepesi Z., et al. (2010) Matrix metalloproteinase-9 activity increased by two different types of epileptic seizures that do not induce neuronal death: a possible role in homeostatic synaptic plasticity. Neurochem. Int. 56, 799-809.
65. Thelen K., Kedar V., Panicker A. K., Schmid R. S., Midkiff B. R., and, Maness P. F., (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J. Neurosci. 22, 4918-4931.
66. Tian L., Stefanidakis M., Ning L., Van Lint P., Nyman-Huttunen H., Libert C., Itohara S., Mishina M., Rauvala H., and, Gahmberg C. G., (2007) Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J. Cell Biol. 178, 687-700.
67. Troca-Marin J. A., Alves-Sampaio A., Tejedor F. J., and, Montesinos M. L., (2010) Local translation of dendritic RhoA revealed by an improved synaptoneurosome preparation. Mol. Cell. Neurosci. 43, 308-314.
68. Uchida Y., Ohshima T., Sasaki Y., et al. (2005) Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3beta phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 10, 165-179.
69. Villasana L. E., Klann E., and, Tejada-Simon M. V., (2006) Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J. Neurosci. Met. 158, 30-36.
70. Vu T. H., Shipley J. M., Bergers G., Berger J. E., Helms J. A., Hanahan D., Shapiro S. D., Senior R. M., and, Werb Z., (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422.
71. Wang L. H., and, Strittmatter S. M., (1996) A family of rat CRMP genes is differentially expressed in the nervous system. J. Neurosci. 16, 6197-6207.
72. Wang X., Jung J., Asahi M., Chwang W., Russo L., Moskowitz M. A., Dixon C. E., Fini M. E., and, Lo E. H., (2000) Effects of matrix metalloproteinase-9 gene knock-out on morphological and motor outcomes after traumatic brain injury. J. Neurosci. 20, 7037-7042.
73. Wang X. B., Bozdagi O., Nikitczuk J. S., Zhai Z. W., Zhou Q., and, Huntley G. W., (2008) Extracellular proteolysis by matrix metalloproteinase-9 drives dendritic spine enlargement and long-term potentiation coordinately. Proc. Natl Acad. Sci.USA 105, 19520-19525.
74. Wilczynski G. M., Konopacki F. A., Wilczek E., et al. (2008) Important role of matrix metalloproteinase 9 in epileptogenesis. J. Cell Biol. 180, 1021-1035.
75. Wright J. W., Meighan P. C., Brown T. E., Wiediger R. V., Sorg B. A., and, Harding J. W., (2009) Habituation-induced neural plasticity in the hippocampus and prefrontal cortex mediated by MMP-3. Behav. Brain Res. 203, 27-34.
76. Xia Z., Dudek H., Miranti C. K., and, Greenberg M. E., (1996) Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16, 5425-5436.
77. Yoshimura T., Kawano Y., Arimura N., Kawabata S., Kikuchi A., and, Kaibuchi K., (2005) GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149.
78. Zhang Z., Ottens A. K., Sadasivan S., Kobeissy F. H., Fang T., Hayes R. L., and, Wang K. K., (2007) Calpain-mediated collapsin response mediator protein-1, -2, and -4 proteolysis after neurotoxic and traumatic brain injury. J. Neurotraum. 24, 460-472.
79. Zhou N., Zhao W. D., Liu D. X., Liang Y., Fang W. G., Li B., and, Chen Y. H., (2012) Inactivation of EphA2 promotes tight junction formation and impairs angiogenesis in brain endothelial cells. Microvasc. Res. 82, 113-121.