Hippocampal MMP-3 elevation is associated with passive avoidance conditioning

Olson, Mikel L.; Meighan, Peter C.; Brown, Travis E.; Asay, Aaron L.; Benoist, Caroline C.; Harding, Joseph W.; Wright, John W.

doi:10.1016/j.regpep.2007.07.004

Cited by 31 publications

(26 citation statements)

References 30 publications

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“…Similar results were obtained with the bilateral intra-hippocampal infusion of FN-439 resulting in significant interference with the acquisition of the Morris water maze task [133]. Olson et al [134] have measured elevations in hippocampal MMP-3 beginning 1 hour following passive avoidance training in rats and returning to baselevel by 24 hours post-training. When a specific MMP-3 inhibitor was icv infused 20 minutes prior to, and 50 minutes following training, dose-dependent learning deficits were seen.…”

Section: Categories Of Learningsupporting

confidence: 59%

Contributions of Matrix Metalloproteinases to Neural Plasticity, Habituation, Associative Learning and Drug Addiction

Wright

Harding

2009

Neural Plasticity

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The premise of this paper is that increased expression of matrix metalloproteinases (MMPs) permits the reconfiguration of synaptic connections (i.e., neural plasticity) by degrading cell adhesion molecules (CAMs) designed to provide stability to those extracellular matrix (ECM) proteins that form scaffolding supporting neurons and glia. It is presumed that while these ECM proteins are weakened, and/or detached, synaptic connections can form resulting in new neural pathways. Tissue inhibitors of metalloproteinases (TIMPs) are designed to deactivate MMPs permitting the reestablishment of CAMs, thus returning the system to a reasonably fixed state. This review considers available findings concerning the roles of MMPs and TIMPs in reorganizing ECM proteins thus facilitating the neural plasticity underlying long-term potentiation (LTP), habituation, and associative learning. We conclude with a consideration of the influence of these phenomena on drug addiction, given that these same processes may be instrumental in the formation of addiction and subsequent relapse. However, our knowledge concerning the precise spatial and temporal relationships among the mechanisms of neural plasticity, habituation, associative learning, and memory consolidation is far from complete and the possibility that these phenomena mediate drug addiction is a new direction of research.

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Section: Categories Of Learningsupporting

confidence: 59%

Contributions of Matrix Metalloproteinases to Neural Plasticity, Habituation, Associative Learning and Drug Addiction

Wright

Harding

2009

Neural Plasticity

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“…Matrix metalloproteinases play a key role in normal development as well as pathological conditions (Candelario-Jalil et al, 2009, DeRosa et al, 2008, Bar-Or et al, 2003) Wright and co-workers ((Meighan et al, 2007; Meighan et al, 2006; Olson et al, 2008; Wright and Harding, 2004; Wright and Harding, 2009) have shown that matrix metalloproteinases contribute to synaptic remodeling that could underlie neural plasticity. Our results demonstrate that mere exposure to a novel odor alters gene expression for these enzymes, consistent with those suggestions.…”

Section: Discussionmentioning

confidence: 99%

Novel odors affect gene expression for cytokines and proteinases in the rat amygdala and hippocampus

Irwin

Byers

2012

Brain Research

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Olfaction in rodents provides an excellent modality for the study of cellular mechanisms of information processing and storage, since a single occurrence of precisely timed stimuli has high survival value. We have followed up preliminary evidence of cytokine and proteinase involvement in normal (as opposed to pathologically-induced) brain plasticity by surveying for the presence of these factors in the olfactory circuitry of the rat. Genes for 25–30 common cytokines and their receptors, and over 30 cell matrix and adhesion molecules were found to be expressed across the olfactory bulb, insular cortex, amygdala, and dorsal hippocampus. We then measured by real-time PCR the transcriptional expression of seven of these genes following a one-time exposure to the novel odor of blueberry bars or cornnuts, in contrast to presentation of the familiar odor of lab chow. In the amygdala significant up-regulation of interleukin-1 receptor 1 (IL1r1), interleukin-4 receptor (IL4r), fibroblast growth factor 13 (FGF13), and cathepsin-H (CtsH) was observed in males in response to the odor of cornnuts only. Changes were less consistent and widespread in the hippocampus, but were again sex specific for three genes: cathepsin-L (CtsL), matrix metalloproteinase-14 (MMP-14) and MMP-16. Our results show that transcription for several specific cytokines, growth factors, and proteinases responds to a one-time exposure to a novel odor, in a manner that tends to be region- and sex-specific. This suggests considerable variation in the way that olfactory information is processed at the cellular level in different brain regions and by the two sexes.

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“…Studies in acute slices or in adult rats in vivo have shown that MMP-9 is rapidly activated perisynaptically in area CA1 by LTP-inducing tetanic stimulation of Schaffer collateral-CA1 synapses (Bozdagi et al, 2007; Nagy et al, 2006) (Fig. 3C) or, along with MMP-3, by different types of associative and non-associative learning and memory tasks (Brown et al, 2008; Nagy et al, 2007; Olson et al, 2008; Wright et al, 2007). Loss-of-function approaches, which have included pharmacological blockers, neutralizing antibodies, or genetic deletion, confirm that in the absence of MMP proteolysis, LTP of synapses in hippocampus and other cortical areas is transient (Bozdagi et al, 2007; Meighan et al, 2007; Meighan et al, 2006; Nagy et al, 2006; Okulski et al, 2007; Wang et al, 2008), and behavioral performance in various learning and memory tasks is impaired (Brown et al, 2008; Nagy et al, 2007; Olson et al, 2008; Wright et al, 2007).…”

Section: Proteolytic Cleavage and Synaptic Plasticitymentioning

confidence: 99%

“…3C) or, along with MMP-3, by different types of associative and non-associative learning and memory tasks (Brown et al, 2008; Nagy et al, 2007; Olson et al, 2008; Wright et al, 2007). Loss-of-function approaches, which have included pharmacological blockers, neutralizing antibodies, or genetic deletion, confirm that in the absence of MMP proteolysis, LTP of synapses in hippocampus and other cortical areas is transient (Bozdagi et al, 2007; Meighan et al, 2007; Meighan et al, 2006; Nagy et al, 2006; Okulski et al, 2007; Wang et al, 2008), and behavioral performance in various learning and memory tasks is impaired (Brown et al, 2008; Nagy et al, 2007; Olson et al, 2008; Wright et al, 2007). Additional studies have shown that the stability of spine expansion that typically accompanies LTP (Matsuzaki et al, 2004; Yang et al, 2008) is also dependent on MMP-9 proteolysis (Wang et al, 2008), indicating that the long-term stability of both functional and structural synaptic plasticity depends on MMP-9.…”

Section: Proteolytic Cleavage and Synaptic Plasticitymentioning

confidence: 99%

Building and remodeling synapses

Benson

Huntley

2010

Hippocampus

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Synaptic junctions are generated by adhesion proteins that bridge the synaptic cleft to firmly anchor pre-and postsynaptic membranes. Several cell adhesion molecule (CAM) families localize to synapses, but it is not yet completely understood how each synaptic CAM family contributes to synapse formation and/or structure, and whether or how smaller groups of CAMs serve as minimal, functionally cooperative adhesive units upon which structure is based. Synapse structure and function evolve over the course of development, and in mature animals, synapses are composed of a greater number of proteins, surrounded by a stabilizing extracellular matrix, and often contacted by astrocytic processes. Thus, in mature networks undergoing plasticity, persistent changes in synapse strength, morphology or number must be accompanied by selective and regulated remodeling of the neuropil. Recent work indicates that regulated, extracellular proteolysis may be essential for this, and rather than simply acting permissively to enable synapse plasticity, is more likely playing a proactive role in driving coordinated synaptic structural and functional modifications that underlie persistent changes in network activity. Keywordssynapse; proteinase; cell adhesion molecule; synaptic cleft; extracellular matrix; MMP; CAM Synapse adhesive structureAt CNS synapses, presynaptic terminals are bound to postsynaptic sites by a trans-synaptic adhesive apparatus that spans the intervening cleft. The synaptic cleft is defined by rigidly parallel membranes separated by 15-25 nm, and despite its name, is filled with proteins. High-resolution, ultrastructural techniques have revealed the presence of two sets of filaments within synaptic clefts. The first range between 4 -6 nm and bridge the cleft (Ichimura and Hashimoto, 1988;Landis and Reese, 1983). These filaments are sparsely but evenly distributed and undoubtedly contribute mechanically to junction adhesion. Consistent with this interpretation, recent work employing a cryo-EM technique that circumvents fixation and staining entirely reveals regularly distributed clusters spanning the cleft about 8.5 nm apart (Zuber et al., 2005). The second population of filaments that have been identified runs parallel to the apposing membranes (Ichimura and Hashimoto, 1988;Lucic et al., 2005). Proteins that are enriched in this zone can be stained with EPTA or bismuth iodide (Bloom and Aghajanian, 1968;Pfenninger, 1971a;Pfenninger, 1971b), suggesting that they are rich in basic residues, but the identities of the proteins comprising either bridging or parallel filaments are unknown.

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Hippocampal MMP-3 elevation is associated with passive avoidance conditioning

Cited by 31 publications

References 30 publications

Contributions of Matrix Metalloproteinases to Neural Plasticity, Habituation, Associative Learning and Drug Addiction

Contributions of Matrix Metalloproteinases to Neural Plasticity, Habituation, Associative Learning and Drug Addiction

Novel odors affect gene expression for cytokines and proteinases in the rat amygdala and hippocampus

Building and remodeling synapses

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