Partial kindling induces neurogenesis, activates astrocytes and alters synaptic morphology in the dentate gyrus of freely moving adult rats

Kraev, Igor; Godukhin, O. V.; Patrushev, Ilya; Davies, Heather A.; Popov, V.I.; Stewart, Michael G.

doi:10.1016/j.neuroscience.2009.05.020

Cited by 21 publications

(18 citation statements)

References 67 publications

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“…When CNS axons are deprived of their target, MVBs appear in large numbers in the target-deprived axon terminals as early as four days later and remain at elevated levels for at least 20 days after target ablation (Marty and Peschanski, 1994). In the CNS of genetically epilepsy-prone rat, neuronal somata, dendrites and axons display an abundance of MVBs (Roberts and Ribak, 1988) consistent with an in vivo study simulating epileptic activity (Kraev et al ., 2009). This is consistent with earlier studies showing increased MVBs after prolonged (1-5 min) electrical stimulation (Kadota and Kadota, 1982; Kadota et al ., 1994) or in Drosophila potassium channel mutants with dramatically increased motoneuron firing and transmitter release (Jia et al ., 1993).…”

Section: Neuronal Mvbs In Development Diseases and Agingsupporting

confidence: 75%

“…In the later two studies MVB frequency per dendrite length was 0.1–0.4 MVB per 10 μm or 5–15 MVBs per 10 μm, respectively. Interestingly, MVB frequency increased in dendritic shafts below spines after tetani or mild focal seizures (Kadota and Kadota, 2002; Kraev et al ., 2009) and after fear conditioning (Ostroff et al ., 2010). Dendritic MVBs can be associated with tubules (Cooney et al ., 2002; Parton et al ., 1992) and smooth endoplasmic reticulum (Chicurel and Harris, 1992), and MVB-tubule complexes at spine origins have been suggested to be storage, sorting, and recycling centers for membrane-associated proteins, while isolated MVBs (MVBs not associated with tubules) may preferentially carry sorted material to the soma (Cooney et al ., 2002).…”

Section: Distribution Of Mvbs In Neuronal Compartmentsmentioning

confidence: 99%

“…MVBs in oligodendrocytes are associated with cholesterol trafficking, and disruptions in this trafficking can lead to neurodegeneration (Liu et al ., 2010). Finally, following a kindling protocol simulating pre-epileptic activity, MVBs are enlarged in dendrites contacting activated astrocytes, and translocate to the neck of the dendritic spine (Kraev et al ., 2009). MVB’s potential association with diverse pathologies, from demyelinating diseases to neurodegeneration, such as Alzheimer’s and Niemann-Pick diseases (see section 11.3.2 – 11.3.3 below), suggests that MVBs are critical for both glial and neuronal cell homeostasis.…”

Section: Mvbs In Glial Cellsmentioning

confidence: 99%

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Multivesicular bodies in neurons: Distribution, protein content, and trafficking functions

Bartheld

Altick

2011

Progress in Neurobiology

176

157

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SummaryMultivesicular bodies (MVBs) are intracellular endosomal organelles characterized by multiple internal vesicles that are enclosed within a single outer membrane. MVBs were initially regarded as purely prelysosomal structures along the degradative endosomal pathway of internalized proteins. MVBs are now known to be involved in numerous endocytic and trafficking functions, including protein sorting, recycling, transport, storage, and release. This review of neuronal MVBs summarizes their research history, morphology, distribution, accumulation of cargo and constitutive proteins, transport, and theories of functions of MVBs in neurons and glia. Due to their complex morphologies, neurons have expanded trafficking and signaling needs, beyond those of "geometrically simpler" cells, but it is not known whether neuronal MVBs perform additional transport and signaling functions. This review examines the concept of compartment-specific MVB functions in endosomal protein trafficking and signaling within synapses, axons, dendrites and cell bodies. We critically evaluate reports of the accumulation of neuronal MVBs based on evidence of stress-induced MVB formation. Furthermore, we discuss potential functions of neuronal and glial MVBs in development, in dystrophic neuritic syndromes, injury, disease, and aging. MVBs may play a role in Alzheimer's, Huntington's, and Niemann-Pick diseases, some types of frontotemporal dementia, prion and virus trafficking, as well as in adaptive responses of neurons to trauma and toxin or drug exposure. Functions of MVBs in neurons have been much neglected, and major gaps in knowledge currently exist. Developing truly MVB-specific markers would help to elucidate the roles of neuronal MVBs in intra-and intercellular signaling of normal and diseased neurons. KeywordsEndosome; Trafficking; Axonal Transport; Sorting; Release; Endocytosis; Degradation Definition of MVBs and scope of this reviewBased on their original discovery and historical tradition, MVBs are defined -as their name implies -by morphological criteria at the ultrastructural level. MVBs appear in ultrathin sections as spherical organelles characterized by a single outer ("limiting") membrane that Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Cooney et al., 2002). The small vesicles as well as the matrix, the lumenal space between the internal vesicles, are typically clear, but they can be of varying electron densities (Roizin et al., 1967). The internal vesicles can have heterogeneous sizes with a diameter of 50-100 nm, although they frequently are uniform in size, about 60-70 nm in...

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Section: Neuronal Mvbs In Development Diseases and Agingsupporting

confidence: 75%

Section: Distribution Of Mvbs In Neuronal Compartmentsmentioning

confidence: 99%

Section: Mvbs In Glial Cellsmentioning

confidence: 99%

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Multivesicular bodies in neurons: Distribution, protein content, and trafficking functions

Bartheld

Altick

2011

Progress in Neurobiology

176

157

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“…This possibility is rather unlikely, however, because neurons can still find space to form proper dendritic spines in the adult brain [26][27][28]. Even newborn astrocytes and neurons can migrate from areas of neurogenesis in adult brain [29][30][31].…”

Section: Discussionmentioning

confidence: 99%

Subcellular location of astrocytic calcium stores favors extrasynaptic neuron–astrocyte communication

Gavrilov²,

et al. 2013

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“…Remodeling of the brain circuitry associated with epilepsy, particularly in excitatory and inhibitory systems, includes alterations in synaptic efficacy as well as the growth of new connections and the loss of existing ones. Neurogenesis, synaptogenesis [10], and neurodegeneration from necrosis and/or apoptosis [11,12] occur during the development of kindling. There is increasing evidence that neurogenesis and synaptogenesis can occur not only in the mossy fiber pathway [13] in the hippocampus but also in other limbic structures.…”

Section: Discussionmentioning

confidence: 99%

Role of Endoplasmic Reticulum Stress in the Amygdaloid Kindling Model of Rats

et al. 2011

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Endoplasmic reticulum (ER) is an organelle responsible for correct folding and sorting of proteins contributing to neurogenesis and neuronal cell death. We used rapid kindling to analyze specific ER stress marker expression underlying focal epileptogenesis. Seven-week-old rats were divided into three groups: sham (n = 6), partially kindled (n = 8), and over-kindled rats (n = 9). Over kindled rats received over100 stimuli. Partially kindled animals had stimuli halted at stage 2. Protein from ipsilateral hippocampus was electrophoresed on SDS-PAGE, followed by hybridization with primary antibodies, anti-KDEL (-Lys-Asp-Glu-coo-), Bcl-2, BDNF (brain-derived neurotrophic factor), CHOP (C/EBP-homolog protein), C/EBP (CCAAT/enhancer-binding protein), NMDA (N-methyl-D-aspartate; -R1 &2A), GluR1 (glutamate receptor), and β-tubulin. Western blotting revealed that the ER stress marker BiP (immunoglobulin heavy chain-binding protein) was markedly increased in both partially- and over-kindled groups. BiP expression was ninefold greater than control in partially kindling while twofold greater than control in over-kindled animals. Although ER stress response was accelerated, CHOP expression, which upregulates when apoptosis signaling is accelerated by ER stress, was suppressed. Bcl-2, which acts as an anti-apoptotic molecule, was upregulated in the over-kindled group. Remarkable elevation of BiP was found in partially kindled animals, but not in over-kindled. Over-kindled rats had spontaneous generalized seizure, while partially kindled ones had only partial seizures. Elevation of markers of ER stress in partial seizures might reflect transfer of discharge to contralateral limbic structures. We observed indications of functional changes and neurogenesis in limbic structure during kindling. Widespread indications of functional changes in several membrane and secreted proteins, including NMDA-R1 & R2A and BDNF, for mossy fiber re-construction on the CA3 area, which are related to protein synthesis in the ER, may be important in epileptogenesis.

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Partial kindling induces neurogenesis, activates astrocytes and alters synaptic morphology in the dentate gyrus of freely moving adult rats

Cited by 21 publications

References 67 publications

Multivesicular bodies in neurons: Distribution, protein content, and trafficking functions

Multivesicular bodies in neurons: Distribution, protein content, and trafficking functions

Subcellular location of astrocytic calcium stores favors extrasynaptic neuron–astrocyte communication

Role of Endoplasmic Reticulum Stress in the Amygdaloid Kindling Model of Rats

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