Inhibition of matrix metalloproteinases prevents the potentiation of nondeprived-eye responses after monocular deprivation in juvenile rats

Cerebral Cortex

Volumn 22, Issue 3, 2012, Pages 725-734

  Spolidoro, M ^a   Putignano, E ^b   Munaf, C ^a   Maffei, L ^a   Pizzorusso, T ^a,c  

^a CNR   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

metalloproteinases; plasticity; spine density; visual cortex

Indexed keywords

MATRIX METALLOPROTEINASE; PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; ELECTROPHYSIOLOGY; ENZYME INHIBITION; EYE DOMINANCE; LONG TERM POTENTIATION; MONOCULAR DEPRIVATION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; RAT; SYNAPSE; VISUAL CORTEX;

AMAUROSIS FUGAX; ANIMALS; DIPEPTIDES; ENZYME INHIBITORS; EVOKED POTENTIALS, VISUAL; MATRIX METALLOPROTEINASES; NEURAL INHIBITION; NEURONAL PLASTICITY; PHOTIC STIMULATION; RATS; RATS, LONG-EVANS; VISUAL CORTEX;

EID: 84857211294     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhr158     Document Type: Article

References (65)

1. Agrawal SM, Lau L, Yong VW. 2008. MMPs in the central nervous system: where the good guys go bad. Semin Cell Dev Biol. 19:42-51. (Pubitemid 350235982)
2. Berardi N, Pizzorusso T, Maffei L. 2000. Critical periods during sensory development. Curr Opin Neurobiol. 10:138-145. (Pubitemid 30102867)
3. Birkedal-Hansen H. 1995. Proteolytic remodeling of extracellular matrix. Curr Opin Cell Biol. 7:728-735.
4. Coleman JE, Nahmani M, Gavornik JP, Haslinger R, Heynen AJ, Erisir A, Bear MF. 2010. Rapid structural remodeling of thalamocortical synapses parallels experience-dependent functional plasticity in mouse primary visual cortex. J Neurosci. 30:9670-9682.
5. Dang AB, Tay BK, Kim HT, Nauth A, Alfonso-Jaume MA, Lovett DH. 2008. Inhibition of MMP2/MMP9 after spinal cord trauma reduces apoptosis. Spine (Phila Pa 1976). 33:E576-E579.
6. Desai NS, Cudmore RH, Nelson SB, Turrigiano GG. 2002. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci. 5:783-789. (Pubitemid 34827597)
7. Di Cristo G, Berardi N, Cancedda L, Pizzorusso T, Putignano E, Ratto GM, Maffei L. 2001. Requirement of ERK activation for visual cortical plasticity. Science. 292:2337-2340. (Pubitemid 32568057)
8. Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R. 1999. Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci USA. 96:13438-13443.
9. Fischer M, Kaech S, Knutti D, Matus A.1998. Rapid actin-based plasticity in dendritic spines. Neuron. 20: 847-854. (Pubitemid 28247391)
10. Fischer M, Kaech S, Wagner U, Brinkhaus H, Matus A. 2000. Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci. 3:887-894.
11. Frenkel MY, Bear MF. 2004. How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron. 44:917-923. (Pubitemid 39643088)
12. Gan WB, Grutzendler J, Wong WT, Wong RO, Lichtman JW. 2000. Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron. 27:219-225.
13. Gawlak M, Gorkiewicz T, Gorlewicz A, Konopacki FA, Kaczmarek L, Wilczynski GM. 2009. High resolution in situ zymography reveals matrix metalloproteinase activity at glutamatergic synapses. Neuroscience. 158:167-176.
14. Harris KM, Kater SB. 1994. Dendritic spines: cellular specializations imparting both stability and flexibility to synaptic function. Annu Rev Neurosci. 17:341-371. (Pubitemid 24117034)
15. Harris KM, Stevens JK. 1989. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci. 9:2982-2997. (Pubitemid 19214329)
16. Heynen AJ, Yoon BJ, Liu CH, Chung HJ, Huganir RL, Bear MF. 2003. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci. 6:854-862. (Pubitemid 36929707)
17. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M. 2009. Experience leaves a lasting structural trace in cortical circuits. Nature. 457:313-317.
18. Hubel DH, Wiesel TN. 1963. Shape and arrangement of columns in cat's striate cortex. J Physiol. 165:559-568.
19. Hubel DH, Wiesel TN. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol. 206:419-436.
20. Kaneko M, Stellwagen D, Malenka RC, Stryker MP. 2008. Tumor necrosis factor-alpha mediates one component of competitive, experience-dependent plasticity in developing visual cortex. Neuron. 58:673-680. (Pubitemid 351778470)
21. Kiorpes L, Kiper DC, O'Keefe LP, Cavanaugh JR, Movshon JA. 1998. Neuronal correlates of amblyopia in the visual cortex of macaque monkeys with experimental strabismus and anisometropia. J Neurosci. 18:6411-6424. (Pubitemid 28373246)
22. Kirkwood A, Rioult MC, Bear MF. 1996. Experience-dependent modification of synaptic plasticity in visual cortex. Nature. 381:526-528. (Pubitemid 26170931)
23. Konopacki FA, Rylski M, Wilczek E, Amborska R, Detka D, Kaczmarek L, Wilczynski GM. 2007. Synaptic localization of seizure-induced matrix metalloproteinase-9 mRNA. Neuroscience. 150:31-39. (Pubitemid 350198686)
24. Leonardo CC, Hall AA, Collier LA, Gottschall PE, Pennypacker KR. 2009. Inhibition of gelatinase activity reduces neural injury in an ex vivo model of hypoxia-ischemia. Neuroscience. 160:755-766.
25. Leppert D, Lindberg RL, Kappos L, Leib SL. 2001. Matrix metalloproteinases: multifunctional effectors of inflammation in multiple sclerosis and bacterial meningitis. Brain Res Brain Res Rev. 36:249-257. (Pubitemid 33020755)
26. Liu Q, Sun Y, Rihn S, Nolting A, Tsoukas PN, Jost S, Cohen K, Walker B, Alter G. 2009. Matrix metalloprotease inhibitors restore impaired NK cell-mediated antibody-dependent cellular cytotoxicity in human immunodeficiency virus type 1 infection. J Virol. 83:8705-8712.
27. Lodovichi C, Berardi N, Pizzorusso T, Maffei L. 2000. Effects of neurotrophins on cortical plasticity: same or different? J Neurosci. 20:2155-2165. (Pubitemid 30230068)
28. Lynch G, Rex CS, Gall CM. 2007. LTP consolidation: substrates, explanatory power, and functional significance. Neuropharmacology. 52:12-23. (Pubitemid 46026832)
29. Maffei A, Nataraj K, Nelson SB, Turrigiano GG. 2006. Potentiation of cortical inhibition by visual deprivation. Nature. 443:81-84. (Pubitemid 44344051)
30. Maffei A, Nelson SB, Turrigiano GG. 2004. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci. 7:1353-1359. (Pubitemid 41057758)
31. Majewska AK, Newton JR, Sur M. 2006. Remodeling of synaptic structure in sensory cortical areas in vivo. J Neurosci. 26:3021-3029.
32. Mataga N, Mizuguchi Y, Hensch TK. 2004. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron. 44:1031-1041. (Pubitemid 39643098)
33. Mataga N, Nagai N, Hensch TK. 2002. Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci USA. 99:7717-7721. (Pubitemid 34568757)
34. Maurer D, Lewis TL, Brent HP, Levin AV. 1999. Rapid improvement in the acuity of infants after visual input. Science. 286:108-110. (Pubitemid 29484486)
35. Meighan SE, Meighan PC, Choudhury P, Davis CJ, Olson ML, Zornes PA, Wright JW, Harding JW. 2006. Effects of extracellular matrixdegrading proteases matrix metalloproteinases 3 and 9 on spatial learning and synaptic plasticity. J Neurochem. 96:1227-1241.
36. Michaluk P, Kolodziej L, Mioduszewska B, Wilczynski GM, Dzwonek J, Jaworski J, Gorecki DC, Ottersen OP, Kaczmarek L. 2007. Betadystroglycan as a target for MMP-9, in response to enhanced neuronal activity. J Biol Chem. 282:16036-16041. (Pubitemid 47100368)
37. Michaluk P, Mikasova L, Groc L, Frischknecht R, Choquet D, Kaczmarek L. 2009. Matrix metalloproteinase-9 controls NMDA receptor surface diffusion through integrin beta1 signaling. J Neurosci. 29:6007-6012.
38. Mrsic-Flogel TD, Hofer SB, Ohki K, Reid RC, Bonhoeffer T, Hubener M. 2007. Homeostatic regulation of eye-specific responses in visual cortex during ocular dominance plasticity. Neuron. 54:961-972. (Pubitemid 46907503)
39. Nagy V, Bozdagi O, Matynia A, Balcerzyk M, Okulski P, Dzwonek J, Costa RM, Silva AJ, Kaczmarek L, Huntley GW. 2006. Matrix metalloproteinase-9 is required for hippocampal late-phase longterm potentiation and memory. J Neurosci. 26:1923-1934.
40. Okulski P, Jay TM, Jaworski J, Duniec K, Dzwonek J, Konopacki FA, Wilczynski GM, Sanchez-Capelo A, Mallet J, Kaczmarek L. 2007. TIMP-1 abolishes MMP-9-dependent long-lasting long-term potentiation in the prefrontal cortex. Biol Psychiatry. 62:359-362. (Pubitemid 47454516)
41. Oray S, Majewska A, Sur M. 2006. Effects of synaptic activity on dendritic spine motility of developing cortical layer v pyramidal neurons. Cereb Cortex. 16:730-741.
42. Philpot BD, Cho KK, Bear MF. 2007. Obligatory role of NR2A for metaplasticity in visual cortex. Neuron. 53:495-502. (Pubitemid 46216758)
43. Pizzorusso T, Berardi N, Rossi FM, Viegi A, Venstrom K, Reichardt LF, Maffei L. 1999. TrkA activation in the rat visual cortex by antirat trkA IgG prevents the effect of monocular deprivation. Eur J Neurosci. 11:204-212. (Pubitemid 29012324)
44. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. 2002. Reactivation of ocular dominance plasticity in the adult visual cortex. Science. 298:1248-1251. (Pubitemid 35285495)
45. Prusky GT, Douglas RM. 2003. Developmental plasticity of mouse visual acuity. Eur J Neurosci. 17:167-173. (Pubitemid 36098887)
46. Prusky GT, West PW, Douglas RM. 2000. Experience-dependent plasticity of visual acuity in rats. Eur J Neurosci. 12:3781-3786.
47. Rittenhouse CD, Shouval HZ, Paradiso MA, Bear MF. 1999. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature. 397:347-350.
48. Shah RD, Crair MC. 2008. Mechanisms of response homeostasis during retinocollicular map formation. J Physiol. 586:4363-4369.
49. Smith GB, Heynen AJ, Bear MF. 2009. Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex. Philos Trans R Soc Lond B Biol Sci. 364:357-367.
50. Sood RR, Taheri S, Candelario-Jalil E, Estrada EY, Rosenberg GA. 2008. Early beneficial effect of matrix metalloproteinase inhibition on blood-brain barrier permeability as measured by magnetic resonance imaging countered by impaired long-term recovery after stroke in rat brain. J Cereb Blood Flow Metab. 28:431-438. (Pubitemid 351161291)
51. Stellwagen D, Malenka RC. 2006. Synaptic scaling mediated by glial TNF-alpha. Nature. 440:1054-1059.
52. Suzuki Y, Nagai N, Umemura K, Collen D, Lijnen HR. 2007. Stromelysin-1 (MMP-3) is critical for intracranial bleeding after t-PA treatment of stroke in mice. J Thromb Haemost. 5:1732-1739. (Pubitemid 47091418)
53. Szklarczyk A, Lapinska J, Rylski M, McKay RD, Kaczmarek L. 2002. Matrix metalloproteinase-9 undergoes expression and activation during dendritic remodeling in adult hippocampus. J Neurosci. 22:920-930. (Pubitemid 34141772)
54. Takacs E, Nyilas R, Szepesi Z, Baracskay P, Karlsen B, Rosvold T, Bjorkum AA, Czurko A, Kovacs Z, Kekesi AK, 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.
55. Timney B. 1983. The effects of early and late monocular deprivation on binocular depth perception in cats. Brain Res. 283:235-243. (Pubitemid 13082587)
56. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K. 2002. Long-term in vivo imaging of experiencedependent synaptic plasticity in adult cortex. Nature. 420:788-794. (Pubitemid 36019621)
57. Tsuji K, Aoki T, Tejima E, Arai K, Lee SR, Atochin DN, Huang PL, Wang X, Montaner J, Lo EH. 2005. Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke. 36:1954-1959. (Pubitemid 41266533)
58. Wang X, Lee SR, Arai K, Lee SR, Tsuji K, Rebeck GW, Lo EH. 2003. Lipoprotein receptor-mediated induction of matrix metalloproteinase by tissue plasminogen activator. Nat Med. 9:1313-1317. (Pubitemid 37279856)
59. Wilczynski GM, Konopacki FA, Wilczek E, Lasiecka Z, Gorlewicz A, Michaluk P, Wawrzyniak M, Malinowska M, Okulski P, Kolodziej LR, et al. 2008. Important role of matrix metalloproteinase 9 in epileptogenesis. J Cell Biol. 180:1021-1035. (Pubitemid 351398426)
60. Wright JW, Harding JW. 2009. Contributions of matrix metalloproteinases to neural plasticity, habituation, associative learning and drug addiction. Neural Plast. 2009:579382.
61. Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H. 2008. Principles of long-term dynamics of dendritic spines. J Neurosci. 28:13592-13608.
62. Yong VW, Power C, Forsyth P, Edwards DR. 2001. Metalloproteinases in biology and pathology of the nervous system. Nat Rev Neurosci. 2:502-511. (Pubitemid 33676585)
63. Yuste R, Bonhoeffer T. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci. 24:1071-1089. (Pubitemid 32695254)
64. Zhao BQ, Wang S, Kim HY, Storrie H, Rosen BR, Mooney DJ, Wang X, Lo EH. 2006. Role of matrix metalloproteinases in delayed cortical responses after stroke. Nat Med. 12:441-445.
65. Zuo J, Ferguson TA, Hernandez YJ, Stetler-Stevenson WG, Muir D. 1998. Neuronal matrix metalloproteinase-2 degrades and inactivates a neurite-inhibiting chondroitin sulfate proteoglycan. J Neurosci. 18:5203-5211. (Pubitemid 28311937)