Effects of discontinuing a high-fat diet on mitochondrial proteins and 6-hydroxydopamine-induced dopamine depletion in rats

Ma, Daifu; Shuler, Jeffrey M.; Raider, Kayla; Rogers, Robert S.; Wheatley, Joshua L.; Geiger, Paige C.; Stanford, John A.

doi:10.1016/j.brainres.2015.03.053

Cited by 16 publications

(13 citation statements)

References 40 publications

(54 reference statements)

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“…The presented results also demonstrate that WD consumption for 12 weeks causes a dysregulation of the dopaminergic system in the striatum and HPC, as reflected by the decrease of DA levels in the striatum by 20% and DA turnover in the HPC by 40% in WD rats compared to controls. Our findings parallel data observed by Ma et al who also showed a decrease of DA levels and no change in DA turnover in the striatum of rats fed a 60 kcal% HFD for 13 weeks (Ma et al, 2015 ). Results by Baladi et al using chronoamperometry also indicated a decrease in DA turnover in the striatum though interestingly this was independent to any observed changes to body weight in high fat diet fed rats (Baladi et al, 2015 ).…”

Section: Discussionsupporting

confidence: 92%

Western Diet Chow Consumption in Rats Induces Striatal Neuronal Activation While Reducing Dopamine Levels without Affecting Spatial Memory in the Radial Arm Maze

Nguyen

Ali

Kosari

et al. 2017

Front. Behav. Neurosci.

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Rats fed high fat diets have been shown to be impaired in hippocampal-dependent behavioral tasks, such as spatial recognition in the Y-maze and reference memory in the Morris water maze (MWM). It is clear from previous studies, however, that motivation and reward factor into the memory deficits associated with obesity and high-fat diet consumption, and that the prefrontal cortex and striatum and neurotransmitter dopamine play important roles in cognitive performance. In this series of studies we extend our research to investigate the effect of a high fat diet on striatal neurochemistry and performance in the delayed spatial win-shift radial arm maze task, a paradigm highly reliant on dopamine-rich brain regions, such as the striatum after high fat diet consumption. Memory performance, neuronal activation and brain dopaminergic levels were compared in rats fed a “Western” (21% fat, 0.15% cholesterol) chow diet compared to normal diet (6% fat, 0.15% cholesterol)-fed controls. Twelve weeks of dietary manipulation produced an increase in weight in western diet-fed rats, but did not affect learning and performance in the delayed spatial win-shift radial arm maze task. Concurrently, there was an observed decrease in dopamine levels in the striatum and a reduction of dopamine turnover in the hippocampus in western diet-fed rats. In a separate cohort of rats Fos levels were measured after rats had been placed in a novel arena and allowed to explore freely. In normal rats, this exposure to a unique environment did not affect neuronal activation. In contrast, rats fed a western diet were found to have significantly increased Fos expression in the striatum, but not prefrontal cortex or hippocampus. Our study demonstrates that while western diet consumption in rats produces weight gain and brain neuronal and neurotransmitter changes, it did not affect performance in the delayed spatial win-shift paradigm in the radial arm maze. We conclude that modeling the cognitive decline-obesity relationship is complex with considerations, of type of memory, behavioral task and dietary intervention (fat, fat and sugar, sugar, and cafeteria diets) all adding to our overall understanding.

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Section: Discussionsupporting

confidence: 92%

Western Diet Chow Consumption in Rats Induces Striatal Neuronal Activation While Reducing Dopamine Levels without Affecting Spatial Memory in the Radial Arm Maze

Nguyen

Ali

Kosari

et al. 2017

Front. Behav. Neurosci.

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“…Increasing evidence indicates that AMPK is a neuroprotective factor [56,57], and a high fat diet likely reduces AMPK activity in brain. Hippocampal levels of both total and phosphorylated AMPK were reduced after high fat consumption [57], and our previous study found that a high fat diet greatly reduced the phosphorylation of AMPK in rat striatum [11]. We also found lower activation of AMPK (measured by pAMPK/total AMPK) in the striatum of high fat rats, suggesting either lower cellular energy demand or suboptimal responses to cellular energy demands.…”

Section: Discussionmentioning

confidence: 60%

“…Conversely, hippocampal cognitive deficits were associated with lower serine racemase (the enzyme that synthesizes D-serine from L-serine) and D-serine concentrations in aged rats [39]. Increased serum insulin levels have been measured in aged rats [40] and in rats fed a high fat diet [10, 11], and likely accounted for the decreased Ser in the current study. The mechanism underlying this effect is unclear, however, because a high fat diet decreases insulin transport across the blood-brain barrier [41].…”

Section: Discussionmentioning

confidence: 78%

“…Hippocampal and striatal sections corresponded with the ROI analyzed with MRS. Brain tissue was frozen until processed as described previously [11,25]. Specifically, frozen samples were diluted in cell extraction buffer and the tissue was homogenized and centrifuged.…”

Section: Methodsmentioning

confidence: 99%

“…In studies examining the effects of a high-fat diet on nigrostriatal function and vulnerability, we found that a high fat diet in young adult rats increases dopamine depletion in the 6-hydroxydopamine (6-OHDA)-lesioned model of PD [10, 11]. We also reported that rats fed a high fat diet exhibit attenuated dopamine release in the striatum and increased iron levels and markers of oxidative stress in the substantia nigra [12].…”

Section: Introductionmentioning

confidence: 99%

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A high fat diet alters metabolic and bioenergetic function in the brain: A magnetic resonance spectroscopy study

Raider

Harris

et al. 2016

Neurochemistry International

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Diet-induced obesity and associated metabolic effects can lead to neurological dysfunction and increase the risk of developing Alzheimer's disease (AD) and Parkinson's disease (PD). Despite these risks, the effects of a high-fat diet on the central nervous system are not well understood. To better understand the mechanisms underlying the effects of high fat consumption on brain regions affected by AD and PD, we used proton magnetic resonance spectroscopy (1H-MRS) to measure neurochemicals in the hippocampus and striatum of rats fed a high fat diet vs. normal low fat chow. We detected lower concentrations of total creatine (tCr) and a lower glutamate-to-glutamine ratio in the hippocampus of high fat rats. Additional effects observed in the hippocampus of high fat rats included higher N-acetylaspartylglutamic acid (NAAG), and lower myo-inositol (mIns) and serine (Ser) concentrations. Post-mortem tissue analyses revealed lower phosphorylated AMP-activated protein kinase (pAMPK) in the striatum but not in the hippocampus of high fat rats. Hippocampal pAMPK levels correlated significantly with tCr, aspartate (Asp), phosphoethanolamine (PE), and taurine (Tau), indicating beneficial effects of AMPK activation on brain metabolic and energetic function, membrane turnover, and edema. A negative correlation between pAMPK and glucose (Glc) indicates a detrimental effect of brain Glc on cellular energy response. Overall, these changes indicate alterations in neurotransmission and in metabolic and bioenergetic function in the hippocampus and in the striatum of rats fed a high fat diet.

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Shared cerebral metabolic pathology in non-transgenic animal models of Alzheimer's and Parkinson's disease

et al. 2020

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Parkinson's disease (PD) and Alzheimer's disease (AD) are the most common chronic neurodegenerative disorders, characterized by motoric dysfunction or cognitive decline in the early stage, respectively, but often by both symptoms in the advanced stage. Among underlying molecular pathologies that PD and AD patients have in common, more attention is recently paid to the central metabolic dysfunction presented as insulin resistant brain state (IRBS) and altered cerebral glucose metabolism, both also explored in animal models of these diseases. This review aims to compare IRBS and alterations in cerebral glucose metabolism in representative non-transgenic animal PD and AD models. The comparison is based on the selectivity of the neurotoxins which cause experimental PD and AD, towards the cellular membrane and intracellular molecular targets as well as towards the selective neurons/non-neuronal cells, and the particular brain regions. Mitochondrial damage and coexpression of insulin receptors, glucose transporter-2 and dopamine transporter on the membrane of particular neurons as well as astrocytes seem to be the key points which are further discussed in a context of alterations in insulin signalling in the brain and its interaction with dopaminergic transmission, particularly regarding the time frame of the experimental AD/ PD pathology appearance and the correlation with cognitive and motor symptoms. Such a perspective provides evidence on IRBS being a common underlying metabolic pathology and a contributor to neurodegenerative processes in representative non-transgenic animal PD and AD models, instead of being a direct cause of a particular neurodegenerative disorder.Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Effects of discontinuing a high-fat diet on mitochondrial proteins and 6-hydroxydopamine-induced dopamine depletion in rats

Cited by 16 publications

References 40 publications

Western Diet Chow Consumption in Rats Induces Striatal Neuronal Activation While Reducing Dopamine Levels without Affecting Spatial Memory in the Radial Arm Maze

Western Diet Chow Consumption in Rats Induces Striatal Neuronal Activation While Reducing Dopamine Levels without Affecting Spatial Memory in the Radial Arm Maze

A high fat diet alters metabolic and bioenergetic function in the brain: A magnetic resonance spectroscopy study

Shared cerebral metabolic pathology in non-transgenic animal models of Alzheimer's and Parkinson's disease

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