TIMP-1 Abolishes MMP-9-Dependent Long-lasting Long-term Potentiation in the Prefrontal Cortex

Okulski, Pawel; Jay, Thérèse M.; Jaworski, Jacek; Duniec, Kamila; Dzwonek, Joanna; Konopacki, Filip A.; Wilczyński, Grzegorz M.; Sánchez-Capelo, Amelia; Mallet, Jacques; Kaczmarek, Leszek

doi:10.1016/j.biopsych.2006.09.012

Cited by 143 publications

(111 citation statements)

References 24 publications

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“…Indeed, evidence suggests that MMP-9 expression is upregulated and the protein becomes proteolytically active during the maintenance phase of LTP at CA3-CA1 synapses in the hippocampus (Nagy et al, 2006;Bozdagi et al, 2007). Similar findings have been recently reported for the rat prefrontal cortex (Okulski et al, 2007). These reports suggest a role for MMP-9 in neuronal plasticity, a concept supported by our findings in PTZ-induced kindled seizure.…”

Section: Discussionsupporting

confidence: 91%

Matrix Metalloproteinase-9 Contributes to Kindled Seizure Development in Pentylenetetrazole-Treated Mice by Converting Pro-BDNF to Mature BDNF in the Hippocampus

Mizoguchi¹,

Nakade²,

Terabe³

et al. 2011

J. Neurosci.

173

142

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(Ϫ/Ϫ) mice compared with wild-type mice, an observation that was accompanied by decreased hippocampal levels of mature brain-derived neurotrophic factor. Microinjecting the BDNF scavenger TrkB-Fc into the right ventricle before each PTZ treatment significantly suppressed the development of kindling in wild-type mice, whereas no effect was observed in MMP-9 (Ϫ/Ϫ) mice. On the other hand, bilateral injections of pro-BDNF into the hippocampal dentate gyrus significantly enhanced kindling in wild-type mice but not MMP-9 (Ϫ/Ϫ) mice. These findings suggest that MMP-9 is involved in the progression of behavioral phenotypes in kindled mice because of conversion of pro-BDNF to mature BDNF in the hippocampus.

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Section: Discussionsupporting

confidence: 91%

Matrix Metalloproteinase-9 Contributes to Kindled Seizure Development in Pentylenetetrazole-Treated Mice by Converting Pro-BDNF to Mature BDNF in the Hippocampus

Mizoguchi¹,

Nakade²,

Terabe³

et al. 2011

J. Neurosci.

173

142

View full text Add to dashboard Cite

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“…When MMP-9 activity is blocked pharmacologically or with specific neutralizing antibodies, the stable maintenance of LTP is significantly impaired, with no effects on LTP induction or early expression. Similar findings have been recently reported in rat prefrontal cortex (Okulski et al 2007). This suggests that MMPs may function in cellular processes that contribute to learning and memory.…”

supporting

confidence: 92%

The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory

Nagy¹,

Bozdagi²,

Huntley³

2007

Learn. Mem.

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Matrix metalloproteinases (MMPs) are a family of extracellularly acting proteolytic enzymes with well-recognized roles in plasticity and remodeling of synaptic circuits during brain development and following brain injury. However, it is now becoming increasingly apparent that MMPs also function in normal, nonpathological synaptic plasticity of the kind that may underlie learning and memory. Here, we extend this idea by investigating the role and regulation of MMP-9 in an inhibitory avoidance (IA) learning and memory task. We demonstrate that following IA training, protein levels and proteolytic activity of MMP-9 become elevated in hippocampus by 6 h, peak at 12-24 h, then decline to baseline values by ∼72 h. When MMP function is abrogated by intrahippocampal infusion of a potent gelatinase (MMP-2 and MMP-9) inhibitor 3.5 h following IA training, a time prior to the onset of training-induced elevation in levels, IA memory retention is significantly diminished when tested 1-3 d later. Animals impaired at 3 d exhibit robust IA memory when retrained, suggesting that such impairment is not likely attributed to toxic or other deleterious effects that permanently disrupt hippocampal function. In anesthetized adult rats, the effective distance over which synaptic plasticity is impaired by a single intrahippocampal infusion of the MMP inhibitor of the kind that blocks IA memory is ∼1200 µm. Taken together, these data suggest that IA training induces a slowly emerging, but subsequently protracted period of MMP-mediated proteolysis critical for enabling long-lasting synaptic modification that underlies long-term memory consolidation.New information is learned and remembered through functional and structural modifications of synaptic connections (Bliss and Collingridge 1993;Rogan et al. 1997;Rioult-Pedotti et al. 1998Jorntell and Hansel 2006;Pastalkova et al. 2006;Whitlock et al. 2006). Several kinds of learning and memory tasks have been shown to drive changes in neurotransmitter receptor function and/or localization (Cammarota et al. 1995;Bevilaqua et al. 2005;Rumpel et al. 2005;Whitlock et al. 2006), as well as induce over time changes in synapse number or morphology (O'Malley et al. 2000;Geinisman et al. 2001;Eyre et al. 2003;Leuner et al. 2003;Maviel et al. 2004;Lamprecht et al. 2006;Rekart et al. 2007). These observations suggest that there must be learninginduced cellular mechanisms for coordinating functional and structural remodeling of synaptic connectivity to enable longterm memory, but there is little known about the molecules that could fulfill such a role.Learning-related, regulated extracellular proteolysis could be one mechanism for coordinating functional and structural synaptic plasticity, thereby enabling memory (Huang et al. 1996;Madani et al. 1999;Calabresi et al. 2000;Pawlak et al. 2002;Tamura et al. 2006). It is well-recognized that extracellular matrix (ECM) proteins as well synaptic cell adhesion molecules contribute to both functional and structural aspects of synaptic plasticity, are modified by l...

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“…Many studies have identified that MMPs are associated with various central nervous system (CNS) pathologies including stroke, traumatic brain injury, cerebral arteriovenous malformation, influenza associated encephalopathy and in bacterial meningitis where it has been identified as a risk factor for developing neurological sequel (8,22,39). Moreover, many studies have reported that MMP-9 has implication in synaptic plasticity, learning and memory (21,25,28,36). Also, MMP-2 has been implicated in dendritic remodeling (36), axonal sprouting (30), synaptic plasticity, and learning in the hippocampus (5, 21).…”

Section: Acar G Et Al: Mmp-9 Expression In Temporal Lobe Epilepsymentioning

confidence: 99%

Increased Expression of Matrix Metalloproteinase-9 in Patients with Temporal Lobe Epilepsy

Acar

Tanrıöver²,

Acar³

et al. 2014

Turkish Neurosurgery

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AIm:The molecular mechanism of epileptogenesis in temporal lobe epilepsy is still unclear. Experimental studies have suggested that matrix metalloproteinases have important roles in this process, but human studies are limited. The aim of this study was to assess the expression of MMP-9, MMP-2 and their tissue inhibitors (TIMP-1 and TIMP-2) in patients with temporal lobe epilepsy with hippocampal sclerosis (TLE-HS). mAterIAl and methOds:The tissue samples from temporal neocortex and hippocampus were obtained from patients with temporal lobe epilepsy with hippocampal sclerosis who had undergone anterior temporal lobectomy for recurrent medically resistant seizures. Immunohistochemical methods were used to determine the expression of MMP-9, MMP-2 and their tissue inhibitors. Tissue samples were also analyzed with transmission electron microscopy. results:The immunoreactivity for MMP-9 both in hippocampal and temporal neocortical neurons was stronger than that of MMP-2. Additionally, there was a mild reaction for its tissue inhibitor TIMP-1 as with TIMP-2. The TEM analysis of the hippocampus revealed that there was apparent ultra-structural damage on the pericarya and neuropil of some neurons. There was obvious damage in the mitochondria and the nuclear membrane. COnClusIOn:The preliminary results of this study revealed that MMP-9 may have a role in patients with drug resistant TLE-HS. KeywOrds:Hippocampal sclerosis, Matrix metalloproteinase-9, Temporal lobe epilepsy ÖZ AmAÇ: Temporal lob epilepsisinde moleküler epileptogenez mekanizmalar halen tam anlaşılamamıştır. Deneysel çalışmalar matriks metaloproteinazların bu süreçte önemli rolü olduğunu ileri sürmektedir, ancak bu konuda insan çalışmaları kısıtlıdır. Çalışmanın amacı, hipokampal sklerozun eşlik ettiği temporal lob epilepsisi (TLE-HS) olan hastalarda MMP-9, MMP-2, TIMP-1 ve TIMP-2 ekspresyonunu değerlendirmektir. yÖntem ve GereÇler: İlaca dirençli epilepsi nedeniyle anterior temporal lobektomi yapılan TLE-HS hastalarından alınan hipokampus ve temporal neokorteks dokuları kullanıldı. MMP-9, MMP-2, TIMP-1 ve TIMP-2 ekspresyonunu incelemek için immünohistokimyasal yöntemler kullanıldı ve dokular transmisyon elektron mikroskopisiyle incelendi.BulGulAr: MMP-9 immünoreaktivitesi hem hipokampal hem de neokortikal nöronlarda MMP-2'ye göre daha güçlü bulundu. Doku inhibitörüü olan TIMP-1'in de ılımlı bir immünoreaktivite gösterdiği tespit edildi. TEM analizinde hipokampal nöronlarda özellikle mitokondriyal ve nükleer membranın belirgin derecede hasara uğradığı tespit edildi.sOnuÇ: Çalışma, MMP-9'un TLE-HS'da rol oynayabileceğini düşündürmektedir.AnAhtAr sÖZCÜKler: Hipokampal skleroz, Matriks metalloproteinaz-9, Temporal lob epilepsi

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TIMP-1 Abolishes MMP-9-Dependent Long-lasting Long-term Potentiation in the Prefrontal Cortex

Cited by 143 publications

References 24 publications

Matrix Metalloproteinase-9 Contributes to Kindled Seizure Development in Pentylenetetrazole-Treated Mice by Converting Pro-BDNF to Mature BDNF in the Hippocampus

Matrix Metalloproteinase-9 Contributes to Kindled Seizure Development in Pentylenetetrazole-Treated Mice by Converting Pro-BDNF to Mature BDNF in the Hippocampus

The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory

Increased Expression of Matrix Metalloproteinase-9 in Patients with Temporal Lobe Epilepsy

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