Aging somatosensory cortex displays increased density of WFA-binding perineuronal nets associated with GAD-negative neurons

Karetko-Sysa, M; Skangiel-Kramska, J; Nowicka, Dorota

doi:10.1016/j.neuroscience.2014.07.049

Cited by 32 publications

(28 citation statements)

References 58 publications

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“…Our data are consistent with other studies showing that approximately 67% of PNs surround GABAergic neurons in mouse somatosensory and rat parietal cortex (Karetko-Sysa et al, 2014, Wegner et al, 2003). In particular, the vast majority (67-90%) of PNs in mouse somatosensory cortex and rat cortex are associated with PV-expressing GABAergic neurons (Hartig et al, 1992, Karetko-Sysa et al, 2014, Kosaka and Heizmann, 1989). We found that approximately 70% of PNs surrounded PV-positive neurons in both the mouse insula and primary motor cortex, also consistent with other reports.…”

Section: Discussionsupporting

confidence: 94%

Repeated Binge Drinking Increases Perineuronal Nets in the Insular Cortex

Lasek

2015

Alcohol Clin Exp Res

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Background Alcohol exposure leads to changes in the extracellular matrix (ECM) in the brain, which profoundly impacts neuronal plasticity. Perineuronal nets (PNs) are specialized ECM structures that enclose subpopulations of neurons in the cortex. Adolescent exposure to alcohol induces long-lasting increases in the expression of PN components in the cortex in adult mice. However, it has not been determined whether binge alcohol exposure in young adults alters PNs. Here, we examined PNs and their core components in the insula and primary motor cortex after repeated binge-like ethanol consumption in adult mice. Methods The 4 day drinking in the dark (DID) procedure was performed in mice for 1 or 6 weeks to model binge alcohol consumption. The impact of ethanol drinking on PNs was examined by fluorescent staining of brain sections using a marker for PNs, Wisteria floribunda agglutinin (WFA). In another set of experiments, cortex was dissected and Western blots and quantitative real-time PCR (qPCR) were performed to evaluate the expression of the PN proteins aggrecan, brevican, and phosphacan. Results Binge-like ethanol drinking for 6 weeks caused a significant increase in PNs in the insula, as measured by WFA binding. Aggrecan, brevican and phosphacan protein expression, and aggrecan mRNA expression, were also elevated in the insula after 6 weeks of ethanol drinking. In contrast, expression of PN components did not change after 1 week of DID. The increase in PNs appears to be specific to the insula, since alterations were not observed in the primary motor cortex. Conclusions Our results provide the first evidence that insular PNs increase after long-term binge drinking. The insula mediates compulsive alcohol use. Since PNs influence neuronal firing and plasticity, increased PNs in the insula after multiple binge cycles may contribute to restricted neuronal plasticity and lead to the development of compulsive alcohol use.

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Section: Discussionsupporting

confidence: 94%

Repeated Binge Drinking Increases Perineuronal Nets in the Insular Cortex

Lasek

2015

Alcohol Clin Exp Res

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“…However, the numbers of PNNs labeled by Cat‐301 monoclonal antibody, which also recognizes the aggrecan glycoform (Matthews et al, ), increased with age in the prefrontal cortex and hippocampus of naïve Fischer 344/N rats (24‐month‐old, male) (Tanaka & Mizoguchi, ). Likewise, the numbers of WFA + PNNs increased with ageing in the somatosensory and visual cortices of C57BL/6J mice (12‐month‐old, female) (Karetko‐Sysa, Skangiel‐Kramska, & Nowicka, ). We have recently reported that the fluorescence intensities of WFA + PNNs increased with age in the dorsal hippocampus of C57BL/6J mice (12‐month‐old, male) (Yamada & Jinno, ).…”

Section: Discussionmentioning

confidence: 99%

Alterations in expression of Cat‐315 epitope of perineuronal nets during normal ageing, and its modulation by an open‐channel NMDA receptor blocker, memantine

Yamada

Ohgomori

Jinno

2017

J of Comparative Neurology

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The perineuronal net (PNN), a specialized aggregate of the extracellular matrix, is involved in neuroprotection against oxidative stress, which is now recognized as a major contributor to age-related decline in brain functions. In this study, we investigated the age-related molecular changes of PNNs using monoclonal antibody Cat-315, which recognizes human natural killer-1 (HNK-1) glycan on aggrecan-based PNNs. Western blot analysis showed that the expression levels of Cat-315 epitope in the hippocampus were higher in middle-aged (MA, 12-month-old) mice than in young adult (YA, 2-month-old) mice. Although there were no differences in the expression levels of Cat-315 epitope between old age (OA, 20-month-old) and MA mice, Cat-315 immunoreactivity was also detected in astrocytes of OA mice. To focus on Cat-315 epitope in PNNs, we used YA and MA mice in the following experiments. Optical disector analysis showed that there were no differences in the numbers of Cat-315-positive (Cat-315 ) PNNs between YA and MA mice. Fluorescence intensity analysis indicated that Cat-315 immunoreactivity in PNNs increased with age in the dorsal hippocampus, which is mainly involved in cognitive functions. Administration of an open-channel blocker of NMDA receptor, memantine, reduced the expression levels of Cat-315 epitope in the hippocampus. Furthermore, the numbers of glutamatergic and GABAergic terminals colocalized with Cat-315 epitope around parvalbumin-positive neurons were decreased by memantine. These findings provide novel insight into the involvement of PNNs in normal brain ageing, and suggest that memantine may counteract the age-related alterations in expression levels of Cat-315 epitope via regulation of its subcellular localization.

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“…We employed WFA as it is largely accepted as a marker for the majority of PNs and has been used in many species (Belichenko et al, 1999;Härtig et al, 1999;Cant and Benson, 2006;Ajmo et al, 2008;Morawski et al, 2012;Foster et al, 2014;Sonntag et al, 2015;. However, the molecular compositions of PNs may vary between brain regions and/or be differentially regulated with aging (Friauf, 2000;Brückner et al, 2003;Ajmo et al, 2008;Giamanco et al, 2010;Wang and Fawcett, 2012;Karetko-Sysa et al, 2014). Methods that use antibodies to CSPG molecules (aggrecan, brevican, phosphacan) can label populations of PNs that WFA does not reveal (Lurie et al, 1997;Ajmo et al, 2008;Karetko-Sysa et al, 2011;Blosa et al, 2013;Sonntag et al, 2015).…”

Section: Technical Considerationsmentioning

confidence: 99%

“…Studies examining the role of PNs in physiological aging are less common and largely address questions in cortex regarding memory and cognition (Foscarin et al, 2017). Furthermore, the role of PNs in aging sensory systems has not been broadly studied and are also commonly restricted to cortex (Karetko-Sysa et al, 2014). Studies that have been conducted in sensory cortices are generally in agreement that PNs increase with age (Tanaka and Mizoguchi, 2009;Yamada and Jinno, 2013;Karetko-Sysa et al, 2014;Ueno et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, the role of PNs in aging sensory systems has not been broadly studied and are also commonly restricted to cortex (Karetko-Sysa et al, 2014). Studies that have been conducted in sensory cortices are generally in agreement that PNs increase with age (Tanaka and Mizoguchi, 2009;Yamada and Jinno, 2013;Karetko-Sysa et al, 2014;Ueno et al, 2018). However, reports in the aging auditory cortex have been inconsistent: Ueno et al (2018) found an overall increase of PNs in the auditory cortex, Brewton et al (2016) found a decrease of PNs, and Cisneros-Franco et al (2018) found an increase of PNs early in life followed by a loss during old age.…”

Section: Introductionmentioning

confidence: 99%

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The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

Mafi

Hofer

Russ

et al. 2020

Front. Aging Neurosci.

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Age-related hearing loss, one of the most frequently diagnosed disabilities in industrialized countries, may result from declining levels of GABA in the aging inferior colliculus (IC). However, the mechanisms of aging and subsequent disruptions of temporal processing in elderly hearing abilities are still being investigated. Perineuronal nets (PNs) are a specialized form of the extracellular matrix and have been linked to GABAergic neurotransmission and to the regulation of structural and synaptic plasticity. We sought to determine whether the density of PNs in the IC changes with age. We combined Wisteria floribunda agglutinin (WFA) staining with immunohistochemistry to glutamic acid decarboxylase in three age groups of Fischer Brown Norway (FBN) rats. The density of PNs on GABAergic and non-GABAergic cells in the three major subdivisions of the IC was quantified. Results first demonstrate that the density of PNs in the FBN IC increase with age. The greatest increases of PN density from young to old age occurred in the central IC (67% increase) and dorsal IC (117% increase). Second, in the young IC, PNs surround non-GABAergic and GABAergic cells with the majority of PNs surrounding the former. The increase of PNs with age in the IC occurred on both non-GABAergic and GABAergic populations. The average density of PN-surrounded non-GABAergic cells increased from 84.9 PNs/mm 2 in the young to 134.2 PNs/mm 2 in the old. While the density of PN-surrounded GABAergic cells increased from 26 PNs/mm 2 in the young to 40.6 PNs/mm 2 in the old. The causality is unclear, but increases in PN density in old age may play a role in altered auditory processing in the elderly, or may lead to further changes in IC plasticity.

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Aging somatosensory cortex displays increased density of WFA-binding perineuronal nets associated with GAD-negative neurons

Cited by 32 publications

References 58 publications

Repeated Binge Drinking Increases Perineuronal Nets in the Insular Cortex

Repeated Binge Drinking Increases Perineuronal Nets in the Insular Cortex

Alterations in expression of Cat‐315 epitope of perineuronal nets during normal ageing, and its modulation by an open‐channel NMDA receptor blocker, memantine

The Density of Perineuronal Nets Increases With Age in the Inferior Colliculus in the Fischer Brown Norway Rat

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