"Increased" sensory stimulation leads to changes in energy-related enzymes in the brain

Dietrich, W. Dalton; Durham, Dianne; Lowry, O. H.; Woolsey, TA

doi:10.1523/jneurosci.02-11-01608.1982

Cited by 44 publications

(8 citation statements)

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“…adult (12)(13)(14)(15)(16), the developing, and the aging brain (16 -20). Decreases in CO activity have been described after visual deprivation (24,25), vibrissae removal, or deafferentation (26 -28), whereas increases in CO activity were recorded during recovery from sensory deprivation (29). A close correlation between OD measurements of CO activity by diaminobenzidine histoenzymology, as performed in the present study and the activity of the enzyme measured spectrophotometrically has been established (13).…”

Section: Discussionsupporting

confidence: 64%

Postnatal Maturation of Cytochrome Oxidase and Lactate Dehydrogenase Activity and Age-Dependent Consequences of Lithium-Pilocarpine Status Epilepticus in the Rat: A Regional Histoenzymology Study

2004

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The lithium-pilocarpine (Li-Pilo) model of epilepsy reproduces some pathophysiological, temporal, and developmental features of human temporal lobe epilepsy. In this model, rates of cerebral glucose utilization measured by the [ 14 C]2-deoxyglucose technique increased during the initial status epilepticus (SE) and decreased during the latent or chronic periods. To correlate these metabolic changes with the activities of the enzymes of the glycolytic and tricarboxylic acid cycle pathways, we measured by histoenzymology the regional activity of two key enzymes of glucose metabolism, lactate dehydrogenase (LDH) for the anaerobic pathway and cytochrome oxidase (CO) for the aerobic pathway coupled to oxidative phosphorylation, at various times after SE induced by Li-Pilo in 10-(P10), 21-d-old (P21) and adult rats for CO and in adult rats only for LDH. CO activity was slightly affected in P10 and P21 rats only at 4 and 24 h and normalized by 14 d after SE. In adult rats, CO activity decreased at 4 and 24 h in damaged areas, like entorhinal cortex, hippocampal CA3 area, amygdala, and thalamus. At 14 d after SE, CO activity was decreased only in entorhinal cortex and increased in brainstem regions involved in the remote control of seizures. In adult rats, LDH activity decreased at 24 h and 14 d after SE in sensorimotor and entorhinal cortex. These data show that the enzymatic equipment underlying the metabolism of glucose is not severely affected by Li-Pilo SE and confirm our previous observations concerning the relative metabolic hyperactivity of brain regions involved in the seizure circuit despite marked neuronal loss. Clinical studies suggest that the development of temporal lobe epilepsy is an age-dependent and progressive process (1-3). The nature of the underlying pathophysiological mechanisms and their differences in mature and immature brain remain poorly understood. In this respect, the model of epilepsy induced in rats by Li-Pilo is a useful tool because it reproduces most clinical, developmental, and neuropathological features of human temporal lobe epilepsy (4,5).The consequences of Li-Pilo are age dependent (4 -7). In adult rats, Li-Pilo leads to SE followed by a latent seizure-free phase of a mean duration of 14 -25 d. Thereafter, all animals enter the chronic phase of the disease and exhibit spontaneous recurrent limbic seizures with generalization. Neuronal damage is located mainly in the hippocampus, dentate gyrus, piriform and entorhinal cortices, septum, thalamus, amygdala, and neocortex (4,5,7). In 21-d-old rats (P21), a more moderate pattern of neuronal damage is observed in the hippocampus, amygdala, piriform and entorhinal cortices, and some thalamic nuclei. About 70 -80% of the rats display spontaneous recurrent limbic seizures after a latent phase of a mean duration of 73 d (5,7). In P10 rats, Li-Pilo-induced SE does not lead to neuronal damage or spontaneous recurrent seizures (5,7).In

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Section: Discussionsupporting

confidence: 64%

Postnatal Maturation of Cytochrome Oxidase and Lactate Dehydrogenase Activity and Age-Dependent Consequences of Lithium-Pilocarpine Status Epilepticus in the Rat: A Regional Histoenzymology Study

2004

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“…In the remaining part of the hippocampus, SDH activity was determined by a quantitative histochemical method [6,9]. Enzyme activity was expressed in arbitrary units (arb.…”

Section: Bulletin Of Experfmentalmentioning

confidence: 99%

Effect of sensory input on the levels of enzymes involved in energy metabolism

1994

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Presentation of sensory stimuli of various modalities to rats immediately before their decapitation led to a significant increase in the level of succmate dehydrogenase in the hippocampus, the magnitude of the increase being dependent on the number of stimuli presented. In each individual case, this enzyme's activity was proportional to the amplitude of the population spike recorded in the hippocampus of the same rat. An inverse relationship was noted between the rate of plastic processes in the hippocampus upon rhythmic stimulation and succinate dehydrogenase activity.Key Words: sensory stimulation; hippocampus; succinate dehydrogenase; population spike; frequency facilitationThe regulation of cell-cell interactions is inextricably bound up with assimilation-dissimilation processes. It has been shown that a major part of the glutamate secreted from nerve terminals becomes involved in energy metabolism [10][11][12]14,15]. Most of the glutamate is taken up by astrocytes [13]. The oxidation of exogenous glutamate provides an external energy source for astrocytes during neuronal excitation [5]. The remaining glutamate is taken up by neurons [13].These findings have enabled a hypothesis to be formulated concerning astro-neuronal interactions during functional activity.A convenient structure for verifying the validity of this hypothesis is the hippocampus. The main pathways in the latter are known to be glutamatergic [8]. Presentation of sensory stimuli should be accompartied by an elevation of glutamate secretion in the hippocampus and, according to the above hypothesis, will lead to increased uptake of glutamate by astrocytes followed by its entry into the Krebs cycle. This is bound to activate enzymes for the subsequent reactions, ff so, then glutamate should be expected to influence primarily the level of succihate dehydrogenase (SDH). Indeed, as shown in several studies [1,3,5], glutamate has an activating effect on succinate oxidation, and such activation is usually explained by elimination of oxaloacetic acid, which inhibits SDH [1].The purpose of this study was to elucidate the possible reasons for alterations in the level of SDH in response to sensory stimulation of different types. MATERIALS AND METHODSFour groups of Wistar rats were used for the experiments. Control rats were decapitated without being exposed to any stimulation. The second group were presented 15 light flashes immediately before decapitation, the third group was exposed to 15 electrocutaneous stimuli, and the fourth group,

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“…These questions are important if we are to understand how nerve cell activity and nerve cell energy metabolism are linked, and how defective energy metabolic regulation causes neurological and muscular disease (Morgan-Hughes, 1986). These questions are difficult to address in brain tissue by traditional biochemical methods, since the distribution of energy metabolic enzymes is nonhomogeneous at very local (even subcellular) levels in the brain (Dietrich et al, 1981(Dietrich et al, , 1982Wong-Riley, 1989). …”

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confidence: 99%

“…It is known that the activities of several energy-metabolic enzymes are coupled to the functional activity of nerve cells (Dietrich et al, 1981(Dietrich et al, , 1982Wong-Riley, 1989), but it is not known how neural functional activity signals changes in enzyme activity, or at what levels (transcriptional, translational, distributional, etc. ) expression of enzyme activity is regulated.…”

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confidence: 99%

Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system

1990

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While much progress has been made in studies of brain energy metabolism, relatively little is known about the biochemical regulation of neural energy metabolic capacity. It is known that the activities of several energy-metabolic enzymes are coupled to the functional activity of nerve cells (Dietrich et al., 1981(Dietrich et al., , 1982Wong-Riley, 1989), but it is not known how neural functional activity signals changes in enzyme activity, or at what levels (transcriptional, translational, distributional, etc.) expression of enzyme activity is regulated. These questions are important if we are to understand how nerve cell activity and nerve cell energy metabolism are linked, and how defective energy metabolic regulation causes neurological and muscular disease (Morgan-Hughes, 1986). These questions are difficult to address in brain tissue by traditional biochemical methods, since the distribution of energy metabolic enzymes is nonhomogeneous at very local (even subcellular) levels in the brain (Dietrich et al., 1981(Dietrich et al., , 1982Wong-Riley, 1989).Received Aug. 21, 1989; revised Oct. 23, 1989; accepted Oct. 25, 1989. This work was supported by NIH grants NS18122 and EY05439 to M.W. We have begun investigating these questions using a mitochondrial respiratory complex, cytochrome oxidase (CO; ferrocytochrome c: oxygen oxidoreductase, EC 1.9.3.1; for review, see Kadenbach et al., 1987) as a representative energy metabolic enzyme. While CO is well known among neuroscientists as a marker for neural functional activity (Wong-Riley, 1989) it also serves as an excellent model for studying regulation of enzyme activity. CO is a key enzyme of the oxidative pathway, the major pathway ofbrain energy metabolism (Erecinska and Silver, 1989); the activity of CO is regulated by neural functional activity (Wong-Riley, 1989); histochemical (Wong-Riley, 1979) and immunohistochemical (Hevner and Wong-Riley, 1989a) methods have been developed for studying CO in brain tissue; and genomit and cDNA clones encoding most mammalian CO subunits have been obtained and sequenced (Anderson et al., 198 1,1982; Bibb et al., 198 1;Lomax et al., 1984;Parimoo et al., 1984;Bachman et al., 1987;Suske et al., 1987;Zeviani et al., 1987Zeviani et al., , 1988Rizzuto et al., 1988Rizzuto et al., , 1989 Schlerfet al., 1988;Goto et al., 1989;Taanman et al., 1989). Thus, the role of the enzyme is well known, regulation of its activity has been demonstrated, and tools are available for studying its regulation.We recently found (Hevner and Wong-Riley, 1989a) that local differences in CO activity (shown histochemically) seen in the normal mouse and monkey brain reflect similar local differences in CO protein concentration (shown immunohistochemically), indicating that the local activity of CO is normally determined mainly by enzyme protein levels, and not by modulation of the molecular activity of homogeneously distributed enzyme (see Fig. 1). This finding suggested that changes in CO activity induced by altered neural functional activity might like...

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"Increased" sensory stimulation leads to changes in energy-related enzymes in the brain

Cited by 44 publications

References 5 publications

Postnatal Maturation of Cytochrome Oxidase and Lactate Dehydrogenase Activity and Age-Dependent Consequences of Lithium-Pilocarpine Status Epilepticus in the Rat: A Regional Histoenzymology Study

Postnatal Maturation of Cytochrome Oxidase and Lactate Dehydrogenase Activity and Age-Dependent Consequences of Lithium-Pilocarpine Status Epilepticus in the Rat: A Regional Histoenzymology Study

Effect of sensory input on the levels of enzymes involved in energy metabolism

Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system

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