The Golgi Apparatus of Neocortical Glial Cells During Hibernation in the Syrian Hamster

León‐Espinosa, Gonzalo; DeFelipe, Javier; Muñoz, Alberto

doi:10.3389/fnana.2019.00092

Cited by 3 publications

(2 citation statements)

References 60 publications

(80 reference statements)

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“…The phenomenon was also observed in several neurodegenerative disorders, including Alzheimer's disease [8], amyotrophic lateral sclerosis [9] or Parkinson's disease [10], where it is believed to be related to neuronal death. On the other hand, GA fragmentation accompanied by changes in expression of structural proteins of the Golgi in hippocampal and neocortical neurons was observed during hibernation in Syrian hamsters, and the recovery of Golgi structure was observed during animal arousal [11]. Hibernating animals have been used as a model to study several aspects of plastic changes that occur in neurons, including the structural plasticity of dendritic spines [12].…”

Section: Introductionmentioning

confidence: 99%

Morphological alterations of the neuronal Golgi apparatus upon seizures

Skupien‐Jaroszek,

Szczepankiewicz,

Rysz

et al. 2023

Neuropathology Appl Neurobio

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AimsEpilepsy is one of the most common chronic neurological disorders, affecting around 50 million people worldwide, but its underlying cellular and molecular events are not fully understood. The Golgi is a highly dynamic cellular organelle and can be fragmented into ministacks under both physiological and pathological conditions. This phenomenon has also been observed in several neurodegenerative disorders, however, the structure of the Golgi apparatus (GA) in human patients suffering from epilepsy has not been described so far. The aim of this study was to assess the changes in GA architecture in epilepsy.MethodsGolgi visualization with immunohistochemical staining in the neocortex of adult patients who underwent epilepsy surgery; 3D reconstruction and quantitative morphometric analysis of GA structure in the rat hippocampi upon kainic acid (KA) induced seizures, as well as in vitro studies with the use of Ca2+ chelator BAPTA‐AM in primary hippocampal neurons upon activation were performed.ResultsWe observed GA dispersion in neurons of the human neocortex of patients with epilepsy, and hippocampal neurons in rats upon KA‐induced seizures. The structural changes of GA were reversible, as GA morphology returned to normal within 24 hours of KA treatment. KA‐induced Golgi fragmentation observed in primary hippocampal neurons cultured in vitro was largely abolished by the addition of BAPTA‐AM.ConclusionsIn our study, we have shown for the first time, that the neuronal Golgi apparatus is fragmented in the human brain of patients with epilepsy and rat brain upon seizures. We have shown that seizure‐induced GA dispersion can be reversible, suggesting that enhanced neuronal activity induces Golgi reorganization that is involved in aberrant neuronal plasticity processes that underlie epilepsy. Moreover, our results revealed that elevated cytosolic Ca2+ is indispensable for these KA‐induced morphological alterations of GA in vitro.

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Section: Introductionmentioning

confidence: 99%

Morphological alterations of the neuronal Golgi apparatus upon seizures

Skupien‐Jaroszek,

Szczepankiewicz,

Rysz

et al. 2023

Neuropathology Appl Neurobio

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“…In addition, we indirectly characterized the changes in activity of orexinergic cells in the different phases of hibernation by analyzing the intensity of immunolabeling of orexin A and the neuronal activity marker C-Fos. Finally, the size of the Golgi apparatus (GA) has been related to the level of cell activity (Lucassen et al, 1993;Salehi et al, 1994) and during hibernation, the GA of different cell types-including hippocampal and neocortical neurons (Popov et al, 1999;Bocharova et al, 2011;Antón-Fernández et al, 2015;León-Espinosa et al, 2019)-undergo a pronounced morphological reorganization including fragmentation and volume decrease during torpor, with a rapid rebuilding during arousals. Therefore, in the present study, we characterized the integrity of the GA of orexinergic neurons throughout hibernation, as revealed by the expression of the GA marker GM-130, a structural GA protein that participates in the protein complex that promotes the stacking and lateral tethering of Golgi cisternae for ribbon formation (Nakamura et al, 1995;Barr et al, 1997Barr et al, , 1998Shorter and Warren, 1999;Linstedt, 2001, 2005;Puthenveedu et al, 2006;Nakamura, 2010).…”

Section: Introductionmentioning

confidence: 99%

Hypothalamic orexinergic neuron changes during the hibernation of the Syrian hamster

et al. 2022

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Hibernation in small mammals is a highly regulated process with periods of torpor involving drops in body temperature and metabolic rate, as well as a general decrease in neural activity, all of which proceed alongside complex brain adaptive changes that appear to protect the brain from extreme hypoxia and low temperatures. All these changes are rapidly reversed, with no apparent brain damage occurring, during the short periods of arousal, interspersed during torpor—characterized by transitory and partial rewarming and activity, including sleep activation, and feeding in some species. The orexins are neuropeptides synthesized in hypothalamic neurons that project to multiple brain regions and are known to participate in the regulation of a variety of processes including feeding behavior, the sleep-wake cycle, and autonomic functions such as brown adipose tissue thermogenesis. Using multiple immunohistochemical techniques and quantitative analysis, we have characterized the orexinergic system in the brain of the Syrian hamster—a facultative hibernator. Our results revealed that orexinergic neurons in this species consisted of a neuronal population restricted to the lateral hypothalamic area, whereas orexinergic fibers distribute throughout the rostrocaudal extent of the brain, particularly innervating catecholaminergic and serotonergic neuronal populations. We characterized the changes of orexinergic cells in the different phases of hibernation based on the intensity of immunostaining for the neuronal activity marker C-Fos and orexin A (OXA). During torpor, we found an increase in C-Fos immunostaining intensity in orexinergic neurons, accompanied by a decrease in OXA immunostaining. These changes were accompanied by a volume reduction and a fragmentation of the Golgi apparatus (GA) as well as a decrease in the colocalization of OXA and the GA marker GM-130. Importantly, during arousal, C-Fos and OXA expression in orexinergic neurons was highest and the structural appearance and the volume of the GA along with the colocalization of OXA/GM-130 reverted to euthermic levels. We discuss the involvement of orexinergic cells in the regulation of mammalian hibernation and, in particular, the possibility that the high activation of orexinergic cells during the arousal stage guides the rewarming as well as the feeding and sleep behaviors characteristic of this phase.

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Effect of Phosphorylated Tau on Cortical Pyramidal Neuron Morphology during Hibernation

Regalado-Reyes

Benavides-Piccione

Fernaud-Espinosa

et al. 2020

Cerebral Cortex Communications

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The dendritic spines of pyramidal cells are the main postsynaptic target of excitatory glutamatergic synapses. Morphological alterations have been described in hippocampal dendritic spines during hibernation—a state of inactivity and metabolic depression that occurs via a transient neuronal tau hyperphosphorylation. Here, we have used the hibernating Syrian hamster to investigate the effect of hyperphosphorylated tau regarding neocortical neuronal structure. In particular, we examined layer Va pyramidal neurons. Our results indicate that hibernation does not promote significant changes in dendritic spine density. However, tau hyperphosphorylated neurons show a decrease in complexity, an increase in the tortuosity of the apical dendrites and an increase in the diameter of the basal dendrites. Tau protein hyperphosphorylation and aggregation have been associated with loss or alterations of dendritic spines in neurodegenerative diseases, such as Alzheimer’s disease (AD). Our results may shed light on the correlation between tau hyperphosphorylation and the neuropathological processes in AD. Moreover, we observed changes in the length and area of the apical and basal dendritic spines during hibernation regardless of tau hyperphosphorylation. The morphological changes observed here also suggest region-specificity, opening up debate about a possible relationship with the differential brain activity registered in these regions in previous studies.

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The Golgi Apparatus of Neocortical Glial Cells During Hibernation in the Syrian Hamster

Cited by 3 publications

References 60 publications

Morphological alterations of the neuronal Golgi apparatus upon seizures

Morphological alterations of the neuronal Golgi apparatus upon seizures

Hypothalamic orexinergic neuron changes during the hibernation of the Syrian hamster

Effect of Phosphorylated Tau on Cortical Pyramidal Neuron Morphology during Hibernation

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