Activity dependent CAM cleavage and neurotransmission

Frontiers in Cellular Neuroscience

Volumn 9, Issue AUGUST, 2015, Pages

  Conant, Katherine ^a   Allen, Megan ^a   Lim, Seung T ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adhesion; CAM; Dendritic spine; Glutamate; Metalloproteases; MMP

Indexed keywords

ADAM10 ENDOPEPTIDASE; BETA1 INTEGRIN; COLLAGENASE 3; GELATINASE A; GELATINASE B; GLUTAMIC ACID; INTERCELLULAR ADHESION MOLECULE 5; INTERSTITIAL COLLAGENASE; LIMBIC SYSTEM ASSOCIATED MEMBRANE PROTEIN; MACROPHAGE ELASTASE; MATRILYSIN; METHAMPHETAMINE; NERVE CELL ADHESION MOLECULE; NEUREXIN; NEUROLIGIN 1; PROTEINASE ACTIVATED RECEPTOR 1; SNARE PROTEIN; STROMELYSIN; SYNAPSE RECEPTOR; SYNDECAN 2; UNCLASSIFIED DRUG;

ADDICTION; DENDRITIC SPINE; FRAGILE X SYNDROME; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INTRACELLULAR SIGNALING; LEARNING; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84940201895     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00305     Document Type: Review

References (190)

1. Aerts, J., Nys, J., Moons, L., Hu, T. T., and Arckens, L. (2014). Altered neuronal architecture and plasticity in the visual cortex of adult MMP-3-deficient mice. Brain Struct. Funct. doi: 10.1007/s00429-014-0819-4 [Epub ahead of print].
2. Ahmad, M., Takino, T., Miyamori, H., Yoshizaki, T., Furukawa, M., and Sato, H. (2006). Cleavage of amyloid-beta precursor protein (APP) by membrane-type matrix metalloproteinases. J. Biochem. 139, 517-526. doi: 10.1093/jb/mvj054
3. Akiyama, K., Ishihara, T., and Kashihara, K. (1996). Effect of acute and chronic administration of methamphetamine on activator protein-1 binding activities in the rat brain regions. Ann. N. Y. Acad. Sci. 801, 13-28. doi: 10.1111/j.1749-6632.1996.tb17428.x
4. Alvarez, V. A., and Sabatini, B. L. (2007). Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 30, 79-97. doi: 10.1146/annurev.neuro.30.051606.094222
5. Anderson, G. R., Galfin, T., Xu, W., Aoto, J., Malenka, R. C., and Sudhof, T. C. (2012). Candidate autism gene screen identifies critical role for cell-adhesion molecule CASPR2 in dendritic arborization and spine development. Proc. Natl. Acad. Sci. U.S.A.109, 18120-18125. doi: 10.1073/pnas.1216398109
6. Aoto, J., Nam, C. I., Poon, M. M., Ting, P., and Chen, L. (2008). Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 60, 308-320. doi: 10.1016/j.neuron.2008.08.012
7. Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J. C., Moskowitz, M. A., et al. (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.
8. Babayan, A. H., Kramar, E. A., Barrett, R. M., Jafari, M., Haettig, J., Chen, L. Y., et al. (2012). Integrin dynamics produce a delayed stage of long-term potentiation and memory consolidation. J. Neurosci. 32, 12854-12861. doi: 10.1523/JNEUROSCI.2024-12.2012
9. Bajor, M., Michaluk, P., Gulyassy, P., Kekesi, A. K., Juhasz, G., and Kaczmarek, L. (2012). Synaptic cell adhesion molecule-2 and collapsin response mediator protein-2 are novel members of the matrix metalloproteinase-9 degradome. J. Neurochem.122, 775-788. doi: 10.1111/j.1471-4159.2012.07829.x
10. Bechara, E. G., Didiot, M. C., Melko, M., Davidovic, L., Bensaid, M., Martin, P., et al. (2009). A novel function for fragile X mental retardation protein in translational activation. PLoS Biol. 7:e16. doi: 10.1371/journal.pbio.1000016
11. Ben-Hur, T., Ben-Yosef, Y., Mizrachi-Kol, R., Ben-Menachem, O., and Miller, A. (2006). Cytokine-mediated modulation of MMPs and TIMPs in multipotential neural precursor cells. J. Neuroimmunol. 175, 12-18. doi: 10.1016/j.jneuroim.2006.02.002
12. Benson, D. L., and Huntley, G. W. (2012). Synapse adhesion: a dynamic equilibrium conferring stability and flexibility. Curr. Opin. Neurobiol. 22, 397-404. doi: 10.1016/j.conb.2011.09.011
13. Benson, D. L., Yoshihara, Y., and Mori, K. (1998). Polarized distribution and cell type-specific localization of telencephalin, an intercellular adhesion molecule. J. Neurosci. Res. 52, 43-53. doi: 10.1002/(SICI)1097-4547(19980401)52:1<43::AID-JNR5>3.0.CO;2-K
14. Bernard-Trifilo, J. A., Kramar, E. A., Torp, R., Lin, C. Y., Pineda, E. A., Lynch, G., et al. (2005). Integrin signaling cascades are operational in adult hippocampal synapses and modulate NMDA receptor physiology. J. Neurochem. 93, 834-849. doi: 10.1111/j.1471-4159.2005.03062.x
15. Berry, E., Bosonea, A. M., Wang, X., and Fernandez-Patron, C. (2013). Insights into the activity, differential expression, mutual regulation, and functions of matrix metalloproteinases and a disintegrin and metalloproteinases in hypertension and cardiac disease. J. Vasc. Res. 50, 52-68. doi: 10.1159/000345240
16. Biederer, T., Sara, Y., Mozhayeva, M., Atasoy, D., Liu, X., Kavalali, E. T., et al. (2002). SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525-1531. doi: 10.1126/science.1072356
17. Bilousova, T. V., Dansie, L., Ngo, M., Aye, J., Charles, J. R., Ethell, D. W., et al. (2009). Minocycline promotes dendritic spine maturation and improves behavioural performance in the fragile X mouse model. J. Med. Genet. 46, 94-102. doi: 10.1136/jmg.2008.061796
18. Bilousova, T. V., Rusakov, D. A., Ethell, D. W., and Ethell, I. M. (2006). Matrix metalloproteinase-7 disrupts dendritic spines in hippocampal neurons through NMDA receptor activation. J. Neurochem. 97, 44-56. doi: 10.1111/j.1471-4159.2006.03701.x
19. Bourne, J., and Harris, K. M. (2007). Do thin spines learn to be mushroom spines that remember? Curr. Opin. Neurobiol. 17, 381-386. doi: 10.1016/j.conb.2007.04.009
20. Bozdagi, O., Wang, X. B., Nikitczuk, J. S., Anderson, T. R., Bloss, E. B., Radice, G. L., et al. (2010). Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. J. Neurosci. 30, 9984-9989. doi: 10.1523/JNEUROSCI.1223-10.2010
21. Brew, K., and Nagase, H. (2010). The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim. Biophys. Acta 1803, 55-71. doi: 10.1016/j.bbamcr.2010.01.003
22. Brown, T. E., Forquer, M. R., Cocking, D. L., Jansen, H. T., Harding, J. W., and Sorg, B. A. (2007). Role of matrix metalloproteinases in the acquisition and reconsolidation of cocaine-induced conditioned place preference. Learn. Mem. 14, 214-223. doi: 10.1101/lm.476207
23. Brown, T. E., Forquer, M. R., Harding, J. W., Wright, J. W., and Sorg, B. A. (2008). Increase in matrix metalloproteinase-9 levels in the rat medial prefrontal cortex after cocaine reinstatement of conditioned place preference. Synapse 62, 886-889. doi: 10.1002/syn.20562
24. Brown, T. E., Wilson, A. R., Cocking, D. L., and Sorg, B. A. (2009). Inhibition of matrix metalloproteinase activity disrupts reconsolidation but not consolidation of a fear memory. Neurobiol. Learn. Mem. 91, 66-72. doi: 10.1016/j.nlm.2008.09.003
25. Chan, C. S., Weeber, E. J., Zong, L., Fuchs, E., Sweatt, J. D., and Davis, R. L. (2006). Beta 1-integrins are required for hippocampal AMPA receptor-dependent synaptic transmission, synaptic plasticity, and working memory. J. Neurosci. 26, 223-232. doi: 10.1523/JNEUROSCI.4110-05.2006
26. Chang, L., Cloak, C., Jiang, C. S., Farnham, S., Tokeshi, B., Buchthal, S., et al. (2009). Altered neurometabolites and motor integration in children exposed to methamphetamine in utero. Neuroimage 48, 391-397. doi: 10.1016/j.neuroimage.2009.06.062
27. Chen, Q., Zhu, X., Zhang, Y., Wetsel, W. C., Lee, T. H., and Zhang, X. (2010). Integrin-linked kinase is involved in cocaine sensitization by regulating PSD-95 and synapsin I expression and GluR1 Ser845 phosphorylation. J. Mol. Neurosci. 40, 284-294. doi: 10.1007/s12031-009-9218-3
28. Clark, E. A., and Brugge, J. S. (1995). Integrins and signal transduction pathways: the road taken. Science 268, 233-239. doi: 10.1126/science.7716514
29. Conant, K., Lonskaya, I., Szklarczyk, A., Krall, C., Steiner, J., Maguire-Zeiss, K., et al. (2010a). Methamphetamine-associated cleavage of the synaptic adhesion molecule intercellular adhesion molecule-5. J. Neurochem. 118, 521-532. doi: 10.1111/j.1471-4159.2010.07153.x
30. Conant, K., Wang, Y., Szklarczyk, A., Dudak, A., Mattson, M. P., and Lim, S. T. (2010b). Matrix metalloproteinase-dependent shedding of intercellular adhesion molecule-5 occurs with long-term potentiation. Neuroscience 166, 508-521. doi: 10.1016/j.neuroscience.2009.12.061
31. Conant, K., Mcarthur, J. C., Griffin, D. E., Sjulson, L., Wahl, L. M., and Irani, D. N. (1999). Cerebrospinal fluid levels of MMP-2, 7, and 9 are elevated in association with human immunodeficiency virus dementia. Ann. Neurol. 46, 391-398. doi: 10.1002/1531-8249(199909)46:3<391::AID-ANA15>3.0.CO;2-0
32. Conant, K., St Hillaire, C., Anderson, C., Galey, D., Wang, J., and Nath, A. (2004). Human immunodeficiency virus type 1 Tat and methamphetamine affect the release and activation of matrix-degrading proteinases. J. Neurovirol. 10, 21-28. doi: 10.1080/13550280490261699
33. Cremer, H., Chazal, G., Carleton, A., Goridis, C., Vincent, J. D., and Lledo, P. M. (1998). Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 95, 13242-13247. doi: 10.1073/pnas.95.22.13242
34. Darnell, J. C., Van Driesche, S. J., Zhang, C., Hung, K. Y., Mele, A., Fraser, C. E., et al. (2012). FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146, 247-261. doi: 10.1016/j.cell.2011.06.013
35. Dityatev, A., Bukalo, O., and Schachner, M. (2008). Modulation of synaptic transmission and plasticity by cell adhesion and repulsion molecules. Neuron Glia Biol. 4, 197-209. doi: 10.1017/S1740925X09990111
36. Dityatev, A., and Rusakov, D. A. (2011). Molecular signals of plasticity at the tetrapartite synapse. Curr. Opin. Neurobiol. 21, 353-359. doi: 10.1016/j.conb.2010.12.006
37. Dziembowska, M., Milek, J., Janusz, A., Rejmak, E., Romanowska, E., Gorkiewicz, T., et al. (2012). Activity-dependent local translation of matrix metalloproteinase-9. J. Neurosci. 32, 14538-14547. doi: 10.1523/JNEUROSCI.6028-11.2012
38. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., et al. (2000). Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci. 20, 5234-5244.
39. Etherton, M. R., Tabuchi, K., Sharma, M., Ko, J., and Sudhof, T. C. (2011). An autism-associated point mutation in the neuroligin cytoplasmic tail selectively impairs AMPA receptor-mediated synaptic transmission in hippocampus. EMBO J. 30, 2908-2919. doi: 10.1038/emboj.2011.182
40. 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. doi: 10.1523/JNEUROSCI.2739-07.2007
41. Galvez, R., and Greenough, W. T. (2005). Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am. J. Med. Genet. A 135, 155-160. doi: 10.1002/ajmg.a.30709
42. Ganguly, K., Rejmak, E., Mikosz, M., Nikolaev, E., Knapska, E., and Kaczmarek, L. (2013). Matrix metalloproteinase (MMP) 9 transcription in mouse brain induced by fear learning. J. Biol. Chem. 288, 20978-20991. doi: 10.1074/jbc.M113.457903
43. Gardner, J., and Ghorpade, A. (2003). Tissue inhibitor of metalloproteinase (TIMP)-1: the TIMPed balance of matrix metalloproteinases in the central nervous system. J. Neurosci. Res. 74, 801-806. doi: 10.1002/jnr.10835
44. Gerber, S. H., and Sudhof, T. C. (2002). Molecular determinants of regulated exocytosis. Diabetes 51(Suppl. 1), S3-S11. doi: 10.2337/diabetes.51.2007.S3
45. Gingrich, M. B., Junge, C. E., Lyuboslavsky, P., and Traynelis, S. F. (2000). Potentiation of NMDA receptor function by the serine protease thrombin. J. Neurosci. 20, 4582-4595.
46. Gkogkas, C. G., Khoutorsky, A., Cao, R., Jafarnejad, S. M., Prager-Khoutorsky, M., Giannakas, N., et al. (2014). Pharmacogenetic inhibition of eIF4E-dependent Mmp9 mRNA translation reverses fragile X syndrome-like phenotypes. Cell Rep. 9, 1742-1755. doi: 10.1016/j.celrep.2014.10.064
47. Groth, R. D., and Tsien, R. W. (2008). A role for retinoic acid in homeostatic plasticity. Neuron 60, 192-194. doi: 10.1016/j.neuron.2008.10.003
48. Gu, Z., Kaul, M., Yan, B., Kridel, S. J., Cui, J., Strongin, A., et al. (2002). S-nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297, 1186-1190. doi: 10.1126/science.1073634
49. Gutwein, P., Mechtersheimer, S., Riedle, S., Stoeck, A., Gast, D., Joumaa, S., et al. (2003). ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB J. 17, 292-294.
50. Hahn-Dantona, E., Ruiz, J. F., Bornstein, P., and Strickland, D. K. (2001). The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276, 15498-15503. doi: 10.1074/jbc.M100121200
51. Han, K. S., Mannaioni, G., Hamill, C. E., Lee, J., Junge, C. E., Lee, C. J., et al. (2011). Activation of protease activated receptor 1 increases the excitability of the dentate granule neurons of hippocampus. Mol. Brain 4, 32. doi: 10.1186/1756-6606-4-32
52. Hartmann, M., Parra, L. M., Ruschel, A., Lindner, C., Morrison, H., Herrlich, A., et al. (2015). Inside-out regulation of ectodomain cleavage of cluster-of-differentiation-44 [CD44] and of neuregulin-1 requires substrate dimerization. J. Biol. Chem. 290, 17041-17054. doi: 10.1074/jbc.M114.610204
53. Hayashida, K., Bartlett, A. H., Chen, Y., and Park, P. W. (2010). Molecular and cellular mechanisms of ectodomain shedding.Anat. Rec. (Hoboken) 293, 925-937. doi: 10.1002/ar.20757
54. He, B., Peng, H., Zhao, Y., Zhou, H., and Zhao, Z. (2011). Modafinil treatment prevents REM sleep deprivation-induced brain function impairment by increasing MMP-9 expression. Brain Res. 1426, 38-42. doi: 10.1016/j.brainres.2011.09.002
55. Huang, Z., Shimazu, K., Woo, N. H., Zang, K., Muller, U., Lu, B., et al. (2006). Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26, 11208-11219. doi: 10.1523/JNEUROSCI.3526-06.2006
56. Huganir, R. L., and Racker, E. (1980). Endogenous and exogenous proteolysis of the acetylcholine receptor from Torpedo californica. J. Supramol. Struct. 14, 13-19. doi: 10.1002/jss.400140103
57. Huntley, G. W. (2012). Synaptic circuit remodelling by matrix metalloproteinases in health and disease. Nat. Rev. Neurosci.13, 743-757. doi: 10.1038/nrn3320
58. Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P., and Grant, S. G. (2000). Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3, 661-669. doi: 10.1038/76615
59. Iwakura, Y., Wang, R., Abe, Y., Piao, Y. S., Shishido, Y., Higashiyama, S., et al. (2011). Dopamine-dependent ectodomain shedding and release of epidermal growth factor in developing striatum: target-derived neurotrophic signaling (Part 2). J. Neurochem. 118, 57-68. doi: 10.1111/j.1471-4159.2011.07295.x
60. Janusz, A., Milek, J., Perycz, M., Pacini, L., Bagni, C., Kaczmarek, L., et al. (2013). The Fragile X mental retardation protein regulates matrix metalloproteinase 9 mRNA at synapses. J. Neurosci. 33, 18234-18241. doi: 10.1523/JNEUROSCI.2207-13.2013
61. Johnson, C., Drgon, T., Liu, Q. R., Zhang, P. W., Walther, D., Li, C. Y., et al. (2008). Genome wide association for substance dependence: convergent results from epidemiologic and research volunteer samples. BMC Med. Genet. 9:113. doi: 10.1186/1471-2350-9-113
62. Johnston, J. B., Silva, C., and Power, C. (2002). Envelope gene-mediated neurovirulence in feline immunodeficiency virus infection: induction of matrix metalloproteinases and neuronal injury. J. Virol. 76, 2622-2633. doi: 10.1128/JVI.76.6.2622-2633.2002
63. Jordan, B. A., and Kreutz, M. R. (2009). Nucleocytoplasmic protein shuttling: the direct route in synapse-to-nucleus signaling.Trends Neurosci. 32, 392-401. doi: 10.1016/j.tins.2009.04.001
64. Kamiguchi, H., and Lemmon, V. (2000). Recycling of the cell adhesion molecule L1 in axonal growth cones. J. Neurosci. 20, 3676-3686.
65. Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A., and Noguchi, J. (2010). Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci. 33, 121-129. doi: 10.1016/j.tins.2010.01.001
66. Kean, M. J., Williams, K. C., Skalski, M., Myers, D., Burtnik, A., Foster, D., et al. (2009). VAMP3, syntaxin-13 and SNAP23 are involved in secretion of matrix metalloproteinases, degradation of the extracellular matrix and cell invasion. J. Cell Sci. 122, 4089-4098. doi: 10.1242/jcs.052761
67. Kelly, E. A., Tremblay, M. E., Gahmberg, C. G., Tian, L., and Majewska, A. K. (2013). Interactions between intercellular adhesion molecule-5 positive elements and their surroundings in the rodent visual cortex. Commun. Integr. Biol. 6, e27315. doi: 10.4161/cib.27315
68. Khuth, S. T., Akaoka, H., Pagenstecher, A., Verlaeten, O., Belin, M. F., Giraudon, P., et al. (2001). Morbillivirus infection of the mouse central nervous system induces region-specific upregulation of MMPs and TIMPs correlated to inflammatory cytokine expression. J. Virol. 75, 8268-8282. doi: 10.1128/JVI.75.17.8268-8282.2001
69. Kim, H. J., Fillmore, H. L., Reeves, T. M., and Phillips, L. L. (2005). Elevation of hippocampal MMP-3 expression and activity during trauma-induced synaptogenesis. Exp. Neurol. 192, 60-72. doi: 10.1016/j.expneurol.2004.10.014
70. Knapska, E., Lioudyno, V., Kiryk, A., Mikosz, M., Gorkiewicz, T., Michaluk, P., et al. (2013). Reward learning requires activity of matrix metalloproteinase-9 in the central amygdala. J. Neurosci. 33, 14591-14600. doi: 10.1523/JNEUROSCI.5239-12.2013
71. Kochlamazashvili, G., Bukalo, O., Senkov, O., Salmen, B., Gerardy-Schahn, R., Engel, A. K., et al. (2012). Restoration of synaptic plasticity and learning in young and aged NCAM-deficient mice by enhancing neurotransmission mediated by GluN2A-containing NMDA receptors. J. Neurosci. 32, 2263-2275. doi: 10.1523/JNEUROSCI.5103-11.2012
72. Konopacki, F. A., Rylski, M., Wilczek, E., Amborska, R., Detka, D., Kaczmarek, L., et al. (2007). Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA. Neuroscience 150, 31-39. doi: 10.1016/j.neuroscience.2007.08.026
73. Kopec, C. D., Li, B., Wei, W., Boehm, J., and Malinow, R. (2006). Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 26, 2000-2009. doi: 10.1523/JNEUROSCI.3918-05.2006
74. Kuzniewska, B., Rejmak, E., Malik, A. R., Jaworski, J., Kaczmarek, L., and Kalita, K. (2013). Brain-derived neurotrophic factor induces matrix metalloproteinase 9 expression in neurons via the serum response factor/c-Fos pathway. Mol. Cell Biol. 33, 2149-2162. doi: 10.1128/MCB.00008-13
75. Larsen, P. H., Dasilva, A. G., Conant, K., and Yong, V. W. (2006). Myelin formation during development of the CNS is delayed in matrix metalloproteinase-9 and -12 null mice. J. Neurosci. 26, 2207-2214. doi: 10.1523/JNEUROSCI.1880-05.2006
76. Lee, H., Lee, E. J., Song, Y. S., and Kim, E. (2014). Long-term depression-inducing stimuli promote cleavage of the synaptic adhesion molecule NGL-3 through NMDA receptors, matrix metalloproteinases and presenilin/gamma-secretase. Philos. Trans. R. Soc. Lond. B Biol. Sci. 369, 20130158. doi: 10.1098/rstb.2013.0158
77. Lee, R., Kermani, P., Teng, K. K., and Hempstead, B. L. (2001). Regulation of cell survival by secreted proneurotrophins.Science 294, 1945-1948. doi: 10.1126/science.1065057
78. Lee, Y. W., Son, K. W., Flora, G., Hennig, B., Nath, A., and Toborek, M. (2002). Methamphetamine activates DNA binding of specific redox-responsive transcription factors in mouse brain. J. Neurosci. Res. 70, 82-89. doi: 10.1002/jnr.10370
79. Li, W., Chang, L., Rong, Z., and Liu, W. (2011). Retinoic acid diminished the expression of MMP-2 in hyperoxia-exposed premature rat lung fibroblasts through regulating mitogen-activated protein kinases. J. Huazhong. Univ. Sci. Technolog. Med. Sci. 31, 251-257. doi: 10.1007/s11596-011-0262-1
80. Lim, C. J., Kain, K. H., Tkachenko, E., Goldfinger, L. E., Gutierrez, E., Allen, M. D., et al. (2008). Integrin-mediated protein kinase A activation at the leading edge of migrating cells. Mol. Biol. Cell. 19, 4930-4941. doi: 10.1091/mbc.E08-06-0564
81. 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. doi: 10.1111/j.1471-4159.2011.07592.x
82. Lindsberg, P. J., Launes, J., Tian, L., Valimaa, H., Subramanian, V., Siren, J., et al. (2002). Release of soluble ICAM-5, a neuronal adhesion molecule, in acute encephalitis. Neurology 58, 446-451. doi: 10.1212/WNL.58.3.446
83. Liu, Y., Brown, S., Shaikh, J., Fishback, J. A., and Matsumoto, R. R. (2008). Relationship between methamphetamine exposure and matrix metalloproteinase 9 expression. Neuroreport 19, 1407-1409. doi: 10.1097/WNR.0b013e32830dd606
84. Lonskaya, I., Partridge, J., Lalchandani, R. R., Chung, A., Lee, T., Vicini, S., et al. (2013). Soluble ICAM-5, a product of activity dependent proteolysis, increases mEPSC frequency and dendritic expression of GluA1. PLoS ONE 8:e69136. doi: 10.1371/journal.pone.0069136
85. Maggio, N., Cavaliere, C., Papa, M., Blatt, I., Chapman, J., and Segal, M. (2013a). Thrombin regulation of synaptic transmission: implications for seizure onset. Neurobiol. Dis. 50, 171-178. doi: 10.1016/j.nbd.2012.10.017
86. Maggio, N., Itsekson, Z., Dominissini, D., Blatt, I., Amariglio, N., Rechavi, G., et al. (2013b). Thrombin regulation of synaptic plasticity: implications for physiology and pathology. Exp. Neurol. 247, 595-604. doi: 10.1016/j.expneurol.2013.02.011
87. Marambaud, P., Wen, P. H., Dutt, A., Shioi, J., Takashima, A., Siman, R., et al. (2003). A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114, 635-645. doi: 10.1016/j.cell.2003.08.008
88. Marcello, E., Epis, R., Saraceno, C., Gardoni, F., Borroni, B., Cattabeni, F., et al. (2012). SAP97-mediated local trafficking is altered in Alzheimer disease patients' hippocampus. Neurobiol. Aging 33, 422.e1-10. doi: 10.1016/j.neurobiolaging.2010.09.015
89. Marcello, E., Gardoni, F., Di Luca, M., and Perez-Otano, I. (2010). An arginine stretch limits ADAM10 exit from the endoplasmic reticulum. J. Biol. Chem. 285, 10376-10384. doi: 10.1074/jbc.M109.055947
90. Mark, K. A., Soghomonian, J. J., and Yamamoto, B. K. (2004). High-dose methamphetamine acutely activates the striatonigral pathway to increase striatal glutamate and mediate long-term dopamine toxicity. J. Neurosci. 24, 11449-11456. doi: 10.1523/JNEUROSCI.3597-04.2004
91. Matsuno, H., Okabe, S., Mishina, M., Yanagida, T., Mori, K., and Yoshihara, Y. (2006). Telencephalin slows spine maturation.J. Neurosci. 26, 1776-1786. doi: 10.1523/JNEUROSCI.2651-05.2006
92. Matsuzaki, M. (2007). Factors critical for the plasticity of dendritic spines and memory storage. Neurosci. Res. 57, 1-9. doi: 10.1016/j.neures.2006.09.017
93. Matsuzaki, M., Honkura, N., Ellis-Davies, G. C., and Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766. doi: 10.1038/nature02617
94. McKinney, B. C., Grossman, A. W., Elisseou, N. M., and Greenough, W. T. (2005). Dendritic spine abnormalities in the occipital cortex of C57BL/6 Fmr1 knockout mice. Am. J. Med. Genet. B Neuropsychiatr. Genet. 136B, 98-102. doi: 10.1002/ajmg.b.30183
95. Mechtersheimer, S., Gutwein, P., Agmon-Levin, N., Stoeck, A., Oleszewski, M., Riedle, S., et al. (2001). Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J. Cell Biol. 155, 661-673. doi: 10.1083/jcb.200101099
96. Meighan, P. C., Meighan, S. E., Davis, C. J., Wright, J. W., and Harding, J. W. (2007). Effects of matrix metalloproteinase inhibition on short- and long-term plasticity of schaffer collateral/CA1 synapses. J. Neurochem. 102, 2085-2096. doi: 10.1111/j.1471-4159.2007.04682.x
97. Meighan, S. E., Meighan, P. C., Choudhury, P., Davis, C. J., Olson, M. L., Zornes, P. A., et al. (2006). Effects of extracellular matrix-degrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J. Neurochem. 96, 1227-1241. doi: 10.1111/j.1471-4159.2005.03565.x
98. Melis, M., Pace, E., Siena, L., Spatafora, M., Tipa, A., Profita, M., et al. (2003). Biologically active intercellular adhesion molecule-1 is shed as dimers by a regulated mechanism in the inflamed pleural space. Am. J. Respir. Crit. Care Med. 167, 1131-1138. doi: 10.1164/rccm.200207-654OC
99. Michaluk, P., Kolodziej, L., Mioduszewska, B., Wilczynski, G. M., Dzwonek, J., Jaworski, J., et al. (2007). Beta-dystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J. Biol. Chem. 282, 16036-16041. doi: 10.1074/jbc.M700641200
100. Michaluk, P., Wawrzyniak, M., Alot, P., Szczot, M., Wyrembek, P., Mercik, K., et al. (2011). Influence of matrix metalloproteinase MMP-9 on dendritic spine morphology. J. Cell Sci. 124, 3369-3380. doi: 10.1242/jcs.090852
101. Mizoguchi, H., Yamada, K., Mouri, A., Niwa, M., Mizuno, T., Noda, Y., et al. (2007a). Role of matrix metalloproteinase and tissue inhibitor of MMP in methamphetamine-induced behavioral sensitization and reward: implications for dopamine receptor down-regulation and dopamine release. J. Neurochem. 102, 1548-1560. doi: 10.1111/j.1471-4159.2007.04623.x
102. Mizoguchi, H., Yamada, K., Niwa, M., Mouri, A., Mizuno, T., Noda, Y., et al. (2007b). Reduction of methamphetamine-induced sensitization and reward in matrix metalloproteinase-2 and -9-deficient mice. J. Neurochem. 100, 1579-1588.
103. Mortillo, S., Elste, A., Ge, Y., Patil, S. B., Hsiao, K., Huntley, G. W., et al. (2012). Compensatory redistribution of neuroligins and N-cadherin following deletion of synaptic beta1-integrin. J. Comp. Neurol. 520, 2041-2052. doi: 10.1002/cne.23027
104. Moser, M. B., Trommald, M., and Andersen, P. (1994). An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl. Acad. Sci. U.S.A. 91, 12673-12675. doi: 10.1073/pnas.91.26.12673
105. Nagase, H., Enghild, J. J., Suzuki, K., and Salvesen, G. (1990). Stepwise activation mechanisms of the precursor of matrix metalloproteinase 3 (stromelysin) by proteinases and (4-aminophenyl)mercuric acetate. Biochemistry 29, 5783-5789. doi: 10.1021/bi00476a020
106. Nagy, V., Bozdagi, O., and Huntley, G. W. (2007). The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory. Learn. Mem. 14, 655-664. doi: 10.1101/lm.678307
107. Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J., et al. (2006). Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26, 1923-1934. doi: 10.1523/JNEUROSCI.4359-05.2006
108. Nakamura, K., Manabe, T., Watanabe, M., Mamiya, T., Ichikawa, R., Kiyama, Y., et al. (2001). Enhancement of hippocampal LTP, reference memory and sensorimotor gating in mutant mice lacking a telencephalon-specific cell adhesion molecule. Eur. J. Neurosci. 13, 179-189. doi: 10.1046/j.0953-816X.2000.01366.x
109. Natarajan, R., Harding, J. W., and Wright, J. W. (2013). A role for matrix metalloproteinases in nicotine-induced conditioned place preference and relapse in adolescent female rats. J. Exp. Neurosci. 7, 1-14. doi: 10.4137/JEN.S11381
110. Niedringhaus, M., Chen, X., Dzakpasu, R., and Conant, K. (2012). MMPs and soluble ICAM-5 increase neuronal excitability within in vitro networks of hippocampal neurons. PLoS ONE 7:e42631. doi: 10.1371/journal.pone.0042631
111. Nikitczuk, J. S., Patil, S. B., Matikainen-Ankney, B. A., Scarpa, J., Shapiro, M. L., Benson, D. L., et al. (2014). N-cadherin regulates molecular organization of excitatory and inhibitory synaptic circuits in adult hippocampus in vivo. Hippocampus 24, 943-962. doi: 10.1002/hipo.22282
112. Ning, L., Tian, L., Smirnov, S., Vihinen, H., Llano, O., Vick, K., et al. (2013). Interactions between ICAM-5 and beta1 integrins regulate neuronal synapse formation. J. Cell Sci. 126, 77-89. doi: 10.1242/jcs.106674
113. Ogier, C., Creidy, R., Boucraut, J., Soloway, P. D., Khrestchatisky, M., and Rivera, S. (2005). Astrocyte reactivity to Fas activation is attenuated in TIMP-1 deficient mice, an in vitro study. BMC Neurosci. 6:68. doi: 10.1186/1471-2202-6-68
114. Oka, S., Mori, K., and Watanabe, Y. (1990). Mammalian telencephalic neurons express a segment-specific membrane glycoprotein, telencephalin. Neuroscience 35, 93-103. doi: 10.1016/0306-4522(90)90124-M
115. Osteen, K. G., Bruner, K. L., and Sharpe-Timms, K. L. (1996). Steroid and growth factor regulation of matrix metalloproteinase expression and endometriosis. Semin. Reprod. Endocrinol. 14, 247-255. doi: 10.1055/s-2007-1016334
116. Page-McCaw, A., Ewald, A. J., and Werb, Z. (2007). Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233. doi: 10.1038/nrm2125
117. Pan, F., Aldridge, G. M., Greenough, W. T., and Gan, W. B. (2010). Dendritic spine instability and insensitivity to modulation by sensory experience in a mouse model of fragile X syndrome. Proc. Natl. Acad. Sci. U.S.A. 107, 17768-17773. doi: 10.1073/pnas.1012496107
118. Patrick, M. K., Johnston, J. B., and Power, C. (2002). Lentiviral neuropathogenesis: comparative neuroinvasion, neurotropism, neurovirulence, and host neurosusceptibility. J. Virol. 76, 7923-7931. doi: 10.1128/JVI.76.16.7923-7931.2002
119. Paudel, S., Kim, Y. H., Huh, M. I., Kim, S. J., Chang, Y., Park, Y. J., et al. (2013). ADAM10 mediates N-cadherin ectodomain shedding during retinal ganglion cell differentiation in primary cultured retinal cells from the developing chick retina. J. Cell. Biochem. 114, 942-954. doi: 10.1002/jcb.24435
120. Peixoto, R. T., Kunz, P. A., Kwon, H., Mabb, A. M., Sabatini, B. L., Philpot, B. D., et al. (2012). Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 76, 396-409. doi: 10.1016/j.neuron.2012.07.006
121. Phillips, L. L., and Reeves, T. M. (2001). Interactive pathology following traumatic brain injury modifies hippocampal plasticity. Restor. Neurol. Neurosci. 19, 213-235.
122. Pillai-Nair, N., Panicker, A. K., Rodriguiz, R. M., Gilmore, K. L., Demyanenko, G. P., Huang, J. Z., et al. (2005). Neural cell adhesion molecule-secreting transgenic mice display abnormalities in GABAergic interneurons and alterations in behavior. J. Neurosci. 25, 4659-4671. doi: 10.1523/JNEUROSCI.0565-05.2005
123. Pinkstaff, J. K., Lynch, G., and Gall, C. M. (1998). Localization and seizure-regulation of integrin beta 1 mRNA in adult rat brain. Brain Res. Mol. Brain Res. 55, 265-276. doi: 10.1016/S0169-328X(98)00007-2
124. 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. doi: 10.1006/nbdi.2001.0435
125. Porlan, E., Marti-Prado, B., Morante-Redolat, J. M., Consiglio, A., Delgado, A. C., Kypta, R., et al. (2014). MT5-MMP regulates adult neural stem cell functional quiescence through the cleavage of N-cadherin. Nat. Cell Biol. 16, 629-638. doi: 10.1038/ncb2993
126. Prinzen, C., Muller, U., Endres, K., Fahrenholz, F., and Postina, R. (2005). Genomic structure and functional characterization of the human ADAM10 promoter. FASEB J. 19, 1522-1524. doi: 10.1096/fj.04-3619fje
127. Prox, J., Rittger, A., and Saftig, P. (2012). Physiological functions of the amyloid precursor protein secretases ADAM10, BACE1, and presenilin. Exp. Brain Res. 217, 331-341. doi: 10.1007/s00221-011-2952-0
128. Pu, C., Broening, H. W., and Vorhees, C. V. (1996). Effect of methamphetamine on glutamate-positive neurons in the adult and developing rat somatosensory cortex. Synapse 23, 328-334. doi: 10.1002/(SICI)1098-2396(199608)23:4<328::AID-SYN11>3.0.CO;2-T
129. Reiss, K., Maretzky, T., Ludwig, A., Tousseyn, T., De Strooper, B., Hartmann, D., et al. (2005). ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J. 24, 742-752. doi: 10.1038/sj.emboj.7600671
130. Richards, D. A., Mateos, J. M., Hugel, S., De Paola, V., Caroni, P., Gahwiler, B. H., et al. (2005). Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures. Proc. Natl. Acad. Sci. U.S.A. 102, 6166-6171. doi: 10.1073/pnas.0501881102
131. 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. doi: 10.1523/JNEUROSCI.3467-10.2010
132. Rivera, S., Ogier, C., Jourquin, J., Timsit, S., Szklarczyk, A. W., Miller, K., et al. (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. doi: 10.1046/j.0953-816x.2001.01838.x
133. Rossignol, D. A., and Frye, R. E. (2012). A review of research trends in physiological abnormalities in autism spectrum disorders: immune dysregulation, inflammation, oxidative stress, mitochondrial dysfunction and environmental toxicant exposures. Mol. Psychiatry 17, 389-401. doi: 10.1038/mp.2011.165
134. Rylski, M., Amborska, R., Zybura, K., Michaluk, P., Bielinska, B., Konopacki, F. A., et al. (2009). JunB is a repressor of MMP-9 transcription in depolarized rat brain neurons. Mol. Cell. Neurosci. 40, 98-110. doi: 10.1016/j.mcn.2008.09.005
135. Rylski, M., Amborska, R., Zybura, K., Mioduszewska, B., Michaluk, P., Jaworski, J., et al. (2008). Yin Yang 1 is a critical repressor of matrix metalloproteinase-9 expression in brain neurons. J. Biol. Chem. 283, 35140-35153. doi: 10.1074/jbc.M804540200
136. Sakry, D., Neitz, A., Singh, J., Frischknecht, R., Marongiu, D., Biname, F., et al. (2014). Oligodendrocyte precursor cells modulate the neuronal network by activity-dependent ectodomain cleavage of glial NG2. PLoS Biol. 12:e1001993. doi: 10.1371/journal.pbio.1001993
137. Sakurai, E., Hashikawa, T., Yoshihara, Y., Kaneko, S., Satoh, M., and Mori, K. (1998). Involvement of dendritic adhesion molecule telencephalin in hippocampal long-term potentiation. Neuroreport 9, 881-886. doi: 10.1097/00001756-199803300-00022
138. Santoro, M. R., Bray, S. M., and Warren, S. T. (2012). Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol. 7, 219-245. doi: 10.1146/annurev-pathol-011811-132457
139. Sanz, R., Ferraro, G. B., and Fournier, A. E. (2014). IgLON cell adhesion molecules are shed from the cell surface of cortical neurons to promote neuronal growth. J. Biol. Chem. 290, 4330-4342. doi: 10.1074/jbc.M114.628438
140. Saraceno, C., Marcello, E., Di Marino, D., Borroni, B., Claeysen, S., Perroy, J., et al. (2014). SAP97-mediated ADAM10 trafficking from Golgi outposts depends on PKC phosphorylation. Cell Death Dis. 5:e1547. doi: 10.1038/cddis.2014.492
141. Satz, J. S., Ostendorf, A. P., Hou, S., Turner, A., Kusano, H., Lee, J. C., et al. (2010). Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J. Neurosci. 30, 14560-14572. doi: 10.1523/JNEUROSCI.3247-10.2010
142. Sbai, O., Ferhat, L., Bernard, A., Gueye, Y., Ould-Yahoui, A., Thiolloy, S., et al. (2008). Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol. Cell Neurosci. 39, 549-568. doi: 10.1016/j.mcn.2008.08.004
143. Schlondorff, J., Becherer, J. D., and Blobel, C. P. (2000). Intracellular maturation and localization of the tumour necrosis factor alpha convertase (TACE). Biochem. J. 347(Pt 1), 131-138. doi: 10.1042/0264-6021:3470131
144. Senkov, O., Sun, M., Weinhold, B., Gerardy-Schahn, R., Schachner, M., and Dityatev, A. (2006). Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. J. Neurosci. 26, 10888-10898. doi: 10.1523/JNEUROSCI.0878-06.2006
145. Shattil, S. J., Kim, C., and Ginsberg, M. H. (2010). The final steps of integrin activation: the end game. Nat. Rev. Mol. Cell Biol.11, 288-300. doi: 10.1038/nrm2871
146. Sheng, M., and Lee, S. H. (2000). Growth of the NMDA receptor industrial complex. Nat. Neurosci. 3, 633-635. doi: 10.1038/76576
147. 2+/calmodulin-dependent protein kinase II-mediated actin reorganization. J. Neurosci. 26, 1813-1822. doi: 10.1523/JNEUROSCI.4091-05.2006
148. Sidhu, H., Dansie, L. E., Hickmott, P. W., Ethell, D. W., and Ethell, I. M. (2014). Genetic removal of matrix metalloproteinase 9 rescues the symptoms of fragile X syndrome in a mouse model. J. Neurosci. 34, 9867-9879. doi: 10.1523/JNEUROSCI.1162-14.2014
149. Siller, S. S., and Broadie, K. (2011). Neural circuit architecture defects in a Drosophila model of Fragile X syndrome are alleviated by minocycline treatment and genetic removal of matrix metalloproteinase. Dis. Model. Mech. 4, 673-685. doi: 10.1242/dmm.008045
150. Smith, A. C., Kupchik, Y. M., Scofield, M. D., Gipson, C. D., Wiggins, A., Thomas, C. A., et al. (2014). Synaptic plasticity mediating cocaine relapse requires matrix metalloproteinases. Nat. Neurosci. 17, 1655-1657. doi: 10.1038/nn.3846
151. Soh, U. J., Dores, M. R., Chen, B., and Trejo, J. (2010). Signal transduction by protease-activated receptors. Br. J. Pharmacol.160, 191-203. doi: 10.1111/j.1476-5381.2010.00705.x
152. Sonderegger, P., and Matsumoto-Miyai, K. (2014). Activity-controlled proteolytic cleavage at the synapse. Trends Neurosci.37, 413-423. doi: 10.1016/j.tins.2014.05.007
153. Strekalova, H., Buhmann, C., Kleene, R., Eggers, C., Saffell, J., Hemperly, J., et al. (2006). Elevated levels of neural recognition molecule L1 in the cerebrospinal fluid of patients with Alzheimer disease and other dementia syndromes. Neurobiol. Aging 27, 1-9. doi: 10.1016/j.neurobiolaging.2004.11.013
154. Sudhof, T. C. (2013). Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675-690. doi: 10.1016/j.neuron.2013.10.022
155. Sutcliffe, J. S., Nelson, D. L., Zhang, F., Pieretti, M., Caskey, C. T., Saxe, D., et al. (1992). DNA methylation represses FMR-1 transcription in fragile X syndrome. Hum. Mol. Genet. 1, 397-400. doi: 10.1093/hmg/1.6.397
156. Suzuki, K., Hayashi, Y., Nakahara, S., Kumazaki, H., Prox, J., Horiuchi, K., et al. (2012). Activity-dependent proteolytic cleavage of neuroligin-1. Neuron 76, 410-422. doi: 10.1016/j.neuron.2012.10.003
157. Szepesi, Z., Bijata, M., Ruszczycki, B., Kaczmarek, L., and Wlodarczyk, J. (2013). Matrix metalloproteinases regulate the formation of dendritic spine head protrusions during chemically induced long-term potentiation. PLoS ONE 8:e63314. doi: 10.1371/journal.pone.0063314
158. Szklarczyk, A., Lapinska, J., Rylski, M., Mckay, R. D., and Kaczmarek, L. (2002). Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J. Neurosci. 22, 920-930.
159. 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.
160. Tian, L., Lappalainen, J., Autero, M., Hanninen, S., Rauvala, H., and Gahmberg, C. G. (2008). Shedded neuronal ICAM-5 suppresses T-cell activation. Blood 111, 3615-3625. doi: 10.1182/blood-2007-09-111179
161. Tian, L., Stefanidakis, M., Ning, L., Van Lint, P., Nyman-Huttunen, H., Libert, C., et al. (2007). Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. J. Cell Biol. 178, 687-700. doi: 10.1083/jcb.200612097
162. Tippmann, F., Hundt, J., Schneider, A., Endres, K., and Fahrenholz, F. (2009). Up-regulation of the alpha-secretase ADAM10 by retinoic acid receptors and acitretin. FASEB J. 23, 1643-1654. doi: 10.1096/fj.08-121392
163. Uemura, K., Kuzuya, A., Aoyagi, N., Ando, K., Shimozono, Y., Ninomiya, H., et al. (2007). Amyloid beta inhibits ectodomain shedding of N-cadherin via down-regulation of cell-surface NMDA receptor. Neuroscience 145, 5-10. doi: 10.1016/j.neuroscience.2006.12.022
164. Uhl, G. R., Drgonova, J., and Hall, F. S. (2014). Curious cases: altered dose-response relationships in addiction genetics.Pharmacol. Ther. 141, 335-346. doi: 10.1016/j.pharmthera.2013.10.013
165. Vaillant, C., Meissirel, C., Mutin, M., Belin, M. F., Lund, L. R., and Thomasset, N. (2003). MMP-9 deficiency affects axonal outgrowth, migration, and apoptosis in the developing cerebellum. Mol. Cell. Neurosci. 24, 395-408. doi: 10.1016/S1044-7431(03)00196-9
166. van der Kooij, M. A., Fantin, M., Rejmak, E., Grosse, J., Zanoletti, O., Fournier, C., et al. (2014). Role for MMP-9 in stress-induced downregulation of nectin-3 in hippocampal CA1 and associated behavioural alterations. Nat. Commun. 5, 4995. doi: 10.1038/ncomms5995
167. Van Hove, I., Lemmens, K., Van De Velde, S., Verslegers, M., and Moons, L. (2012a). Matrix metalloproteinase-3 in the central nervous system: a look on the bright side. J. Neurochem. 123, 203-216. doi: 10.1111/j.1471-4159.2012.07900.x
168. Van Hove, I., Verslegers, M., Buyens, T., Delorme, N., Lemmens, K., Stroobants, S., et al. (2012b). An aberrant cerebellar development in mice lacking matrix metalloproteinase-3. Mol. Neurobiol. 45, 17-29. doi: 10.1007/s12035-011-8215-z
169. Van Wart, H. E., and Birkedal-Hansen, H. (1990). The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc. Natl. Acad. Sci. U.S.A. 87, 5578-5582. doi: 10.1073/pnas.87.14.5578
170. Vawter, M. P., Usen, N., Thatcher, L., Ladenheim, B., Zhang, P., Vanderputten, D. M., et al. (2001). Characterization of human cleaved N-CAM and association with schizophrenia. Exp. Neurol. 172, 29-46. doi: 10.1006/exnr.2001.7790
171. Vergnolle, N., Wallace, J. L., Bunnett, N. W., and Hollenberg, M. D. (2001). Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol Sci 22, 146-152. doi: 10.1016/S0165-6147(00)01634-5
172. Verkerk, A. J., Pieretti, M., Sutcliffe, J. S., Fu, Y. H., Kuhl, D. P., Pizzuti, A., et al. (1991). Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell 65, 905-914. doi: 10.1016/0092-8674(91)90397-H
173. Visse, R., and Nagase, H. (2003). Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ. Res. 92, 827-839. doi: 10.1161/01.RES.0000070112.80711.3D
174. Volkow, N. D., Chang, L., Wang, G. J., Fowler, J. S., Franceschi, D., Sedler, M., et al. (2001). Loss of dopamine transporters in methamphetamine abusers recovers with protracted abstinence. J. Neurosci. 21, 9414-9418.
175. Von Gertten, C., Holmin, S., Mathiesen, T., and Nordqvist, A. C. (2003). Increases in matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1 mRNA after cerebral contusion and depolarisation. J. Neurosci. Res. 73, 803-810. doi: 10.1002/jnr.10729
176. Wang, W., Schulze, C. J., Suarez-Pinzon, W. L., Dyck, J. R., Sawicki, G., and Schulz, R. (2002). Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 106, 1543-1549. doi: 10.1161/01.CIR.0000028818.33488.7B
177. 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. U.S.A.105, 19520-19525. doi: 10.1073/pnas.0807248105
178. Warren, M. S., Bradley, W. D., Gourley, S. L., Lin, Y. C., Simpson, M. A., Reichardt, L. F., et al. (2012). Integrin beta1 signals through Arg to regulate postnatal dendritic arborization, synapse density, and behavior. J. Neurosci. 32, 2824-2834. doi: 10.1523/JNEUROSCI.3942-11.2012
179. Wilczynski, G. M., Konopacki, F. A., Wilczek, E., Lasiecka, Z., Gorlewicz, A., Michaluk, P., et al. (2008). Important role of matrix metalloproteinase 9 in epileptogenesis. J. Cell Biol. 180, 1021-1035. doi: 10.1083/jcb.200708213
180. Wildering, W. C., Hermann, P. M., and Bulloch, A. G. (2002). Rapid neuromodulatory actions of integrin ligands. J. Neurosci.22, 2419-2426.
181. Williams, H., Johnson, J. L., Jackson, C. L., White, S. J., and George, S. J. (2010). MMP-7 mediates cleavage of N-cadherin and promotes smooth muscle cell apoptosis. Cardiovasc. Res. 87, 137-146. doi: 10.1093/cvr/cvq042
182. Wojtowicz, T., and Mozrzymas, J. W. (2014). Matrix metalloprotease activity shapes the magnitude of EPSPs and spike plasticity within the hippocampal CA3 network. Hippocampus 24, 135-153. doi: 10.1002/hipo.22205
183. Wright, J. W., Masino, A. J., Reichert, J. R., Turner, G. D., Meighan, S. E., Meighan, P. C., et al. (2003). Ethanol-induced impairment of spatial memory and brain matrix metalloproteinases. Brain Res. 963, 252-261. doi: 10.1016/S0006-8993(02)04036-2
184. Xu, D., Sharma, C., and Hemler, M. E. (2009). Tetraspanin12 regulates ADAM10-dependent cleavage of amyloid precursor protein. FASEB J. 23, 3674-3681. doi: 10.1096/fj.09-133462
185. Ye, H., Cai, P. C., Zhou, Q., and Ma, W. L. (2011). Transforming growth factor-beta1 suppresses the up-regulation of matrix metalloproteinase-2 by lung fibroblasts in response to tumor necrosis factor-alpha. Wound Repair Regen. 19, 392-399. doi: 10.1111/j.1524-475X.2011.00680.x
186. 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. doi: 10.1038/35081571
187. 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. doi: 10.1046/j.1460-9568.1998.00347.x
188. Zhang, J., Zhang, X., and Jiang, W. (2013). Propofol impairs spatial memory consolidation and prevents learning-induced increase in hippocampal matrix metalloproteinase-9 levels in rat. Neuroreport 24, 831-836. doi: 10.1097/WNR.0b013e328364fe69
189. Zhang, K., Mcquibban, G. A., Silva, C., Butler, G. S., Johnston, J. B., Holden, J., et al. (2003). HIV-induced metalloproteinase processing of the chemokine stromal cell derived factor-1 causes neurodegeneration. Nat. Neurosci. 6, 1064-1071. doi: 10.1038/nn1127
190. Zhuang, J., Wei, Q., Lin, Z., and Zhou, C. (2015). Effects of ADAM10 deletion on Notch-1 signaling pathway and neuronal maintenance in adult mouse brain. Gene 555, 150-158. doi: 10.1016/j.gene.2014.10.056