Neuronal Excitation-driven and AP-1-dependent Activation of Tissue Inhibitor of Metalloproteinases-1 Gene Expression in Rodent Hippocampus

Jaworski, Jacek; Biedermann, I W; Lapinska, Joanna; Szklarczyk, Arek; Figiel, Izabela; Konopka, D; Nowicka, Dorota; Filipkowski, Robert K.; Hetman, Michał; Kowalczyk, Anna; Kaczmarek, Leszek

doi:10.1074/jbc.274.40.28106

Cited by 67 publications

(49 citation statements)

References 38 publications

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“…Thus, the increased expression of MMP-2 and MMP-9, especially in the hippocampus, can be attributed to upregulation of IL-6 and TNF-␣, which have been described as the main actors in MMP modulation (19,26,54). TIMP-1 upregulation in the cortex, hippocampus, and hypothalamus could be due to synergistic activation of AP-1 (30) and polyoma enhancer activator 3 sites in the TIMP-1 promoter. TIMP-1 upregulation may be mediated by TNF-␣, levels of which were increased in the same structures as TIMP-1, acting by stimulation of early gene production (38), or may reflect activation of the IL-6-oncostatin M-responsive element located in the TIMP-1 promoter (9).…”

Section: Discussionmentioning

confidence: 99%

Morbillivirus Infection of the Mouse Central Nervous System Induces Region-Specific Upregulation of MMPs and TIMPs Correlated to Inflammatory Cytokine Expression

Khuth

Akaoka

Pagenstecher

et al. 2001

J Virol

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Viral infection of the central nervous system (CNS) can result in perturbation of cell-to-cell communication involving the extracellular matrix (ECM). ECM integrity is maintained by a dynamic balance between the synthesis and proteolysis of its components, mainly as a result of the action of matrix metalloproteinases (MMPs) and the tissue inhibitors of metalloproteinases (TIMPs). An MMP/TIMP imbalance may be critical in triggering neurological disorders, in particular in virally induced neural disorders. In the present study, a mouse model of brain infection using a neurotropic strain of canine distemper virus (CDV) was used to study the effect of CNS infection on the MMP/TIMP balance and cytokine expression. CDV replicates almost exclusively in neurons and has a unique pattern of expression (cortex, hypothalamus, monoaminergic nuclei, hippocampus, and spinal cord). Here we show that although several mouse brain structures were infected, they exhibited a differential pattern in terms of MMP, TIMP, and cytokine expression, exemplified by (i) a large increase in pro-MMP9 levels, in particular in the hippocampus, which occurred mainly in neurons and was associated with in situ gelatinolytic activity, (ii) specific and significant upregulation of MT1-MMP mRNA expression in the cortex and hypothalamus, (iii) an MMP/TIMP imbalance, suggested by the upregulation of TIMP-1 mRNA in the cortex, hippocampus, and hypothalamus and of TIMP-3 mRNA in the cortex, and (iv) a concomitant region-specific large increase in expression of Th1-like cytokines, such as gamma interferon, tumor necrosis factor alpha, and interleukin 6 (IL-6), contrasting with weaker induction of Th2-like cytokines, such as IL-4 and IL-10. These data indicate that an MMP/TIMP imbalance in specific brain structures, which is tightly associated with a local inflammatory process as shown by the presence of immune infiltrating cells, differentially impairs CNS integrity and may contribute to the multiplicity of late neurological disorders observed in this viral mouse model.

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Section: Discussionmentioning

confidence: 99%

Morbillivirus Infection of the Mouse Central Nervous System Induces Region-Specific Upregulation of MMPs and TIMPs Correlated to Inflammatory Cytokine Expression

Khuth

Akaoka

Pagenstecher

et al. 2001

J Virol

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“…One possibility is that rapid conversion of pro-to active-MMP-9 is mediated via tissue plasminogen activator (tPA), a serine protease upregulated during, and required for, L-LTP (Qian et al, 1993;Huang et al, 1996;Baranes et al, 1998), because several tPA-dependent pathways have been shown to affect MMP-9 levels and/or activity in non-neuronal cell types (Cuzner and Opdenakker, 1999;Wang et al, 2003b). The mechanism by which L-LTP-induced levels of active MMP-9 are returned to prestimulation levels is unclear, although activity-dependent regulation of endogenous TIMPs is possible (Rivera et al, 1997;Jaworski et al, 1999). more acute role for MMP-9 in LTP.…”

Section: Rapid Upregulation Of Mmp-9 With L-ltpmentioning

confidence: 99%

Matrix Metalloproteinase-9 Is Required for Hippocampal Late-Phase Long-Term Potentiation and Memory

Nagy¹,

Bozdagi²,

Matynia³

et al. 2006

J. Neurosci.

435

551

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Matrix metalloproteinases (MMPs) are extracellular proteases that have well recognized roles in cell signaling and remodeling in many tissues. In the brain, their activation and function are customarily associated with injury or pathology. Here, we demonstrate a novel role for MMP-9 in hippocampal synaptic physiology, plasticity, and memory. MMP-9 protein levels and proteolytic activity are rapidly increased by stimuli that induce late-phase long-term potentiation (L-LTP) in area CA1. Such regulation requires NMDA receptors and protein synthesis. Blockade of MMP-9 pharmacologically prevents induction of L-LTP selectively; MMP-9 plays no role in, nor is regulated during, other forms of short-term synaptic potentiation or long-lasting synaptic depression. Similarly, in slices from MMP-9 null-mutant mice, hippocampal LTP, but not long-term depression, is impaired in magnitude and duration; adding recombinant active MMP-9 to null-mutant slices restores the magnitude and duration of LTP to wild-type levels. Activated MMP-9 localizes in part to synapses and modulates hippocampal synaptic physiology through integrin receptors, because integrin function-blocking reagents prevent an MMP-9-mediated potentiation of synaptic signal strength. The fundamental importance of MMP-9 function in modulating hippocampal synaptic physiology and plasticity is underscored by behavioral impairments in hippocampal-dependent memory displayed by MMP-9 null-mutant mice. Together, these data reveal new functions for MMPs in synaptic and behavioral plasticity.

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“…As a matter of fact, coordination of neuronal plasticity has not only been suggested as IEGs' function, but in a few cases has al-ready been proven (consider, e.g., a pathway of extracellular matrix remodeling driven by AP-1; Refs. 197,209,338). Another important consequence of studies on IEGs/ transcription factors is nuclear localization of the IEGs' protein products that greatly facilitates their immunostaining-based detection, because of excellent spatial resolution and rather simple way of numerical evaluation.…”

Section: Gene Activity As a Mapping Tool: Theoretical And Technicmentioning

confidence: 99%

Functional Internal Complexity of Amygdala: Focus on Gene Activity Mapping After Behavioral Training and Drugs of Abuse

Knapska¹,

Radwańska²,

Werka³

et al. 2007

Physiological Reviews

Self Cite

137

134

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The amygdala is a heterogeneous brain structure implicated in processing of emotions and storing the emotional aspects of memories. Gene activity markers such as c-Fos have been shown to reflect both neuronal activation and neuronal plasticity. Herein, we analyze the expression patterns of gene activity markers in the amygdala in response to either behavioral training or treatment with drugs of abuse and then we confront the results with data on other approaches to internal complexity of the amygdala. c-Fos has been the most often studied in the amygdala, showing specific expression patterns in response to various treatments, most probably reflecting functional specializations among amygdala subdivisions. In the basolateral amygdala, c-Fos expression appears to be consistent with the proposed role of this nucleus in a plasticity of the current stimulus-value associations. Within the medial part of the central amygdala, c-Fos correlates with acquisition of alimentary/gustatory behaviors. On the other hand, in the lateral subdivision of the central amygdala, c-Fos expression relates to attention and vigilance. In the medial amygdala, c-Fos appears to be evoked by emotional novelty of the experimental situation. The data on the other major subdivisions of the amygdala are scarce. In conclusion, the studies on the gene activity markers, confronted with other approaches involving neuroanatomy, physiology, and the lesion method, have revealed novel aspects of the amygdala, especially pointing to functional heterogeneity of this brain region that does not fit very well into contemporarily active debate on serial versus parallel information processing within the amygdala.

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Neuronal Excitation-driven and AP-1-dependent Activation of Tissue Inhibitor of Metalloproteinases-1 Gene Expression in Rodent Hippocampus

Cited by 67 publications

References 38 publications

Morbillivirus Infection of the Mouse Central Nervous System Induces Region-Specific Upregulation of MMPs and TIMPs Correlated to Inflammatory Cytokine Expression

Morbillivirus Infection of the Mouse Central Nervous System Induces Region-Specific Upregulation of MMPs and TIMPs Correlated to Inflammatory Cytokine Expression

Matrix Metalloproteinase-9 Is Required for Hippocampal Late-Phase Long-Term Potentiation and Memory

Functional Internal Complexity of Amygdala: Focus on Gene Activity Mapping After Behavioral Training and Drugs of Abuse

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