bioRxiv Science⌕ Search

Biology subjects

Maguire-Zeiss, K. A.

Publications and source records attributed to Maguire-Zeiss, K. A..

3 recordsLinked to original sources

Glial cell and perineuronal net interactions in the dorsal striatum of aged mice

CommentaryElucidating how normal aging increases vulnerability to neurodegeneration remains a major gap in our understanding of disease risk and progression. The dorsal striatum serves as the primary input nucleus of the basal ganglia and is a key region implicated in multiple neurodegenerative diseases (NDDs) (1). In Colon et al. 2025 (2), we examined the impact of normal aging on neuroinflammatory signaling and perineuronal net (PNN) homeostasis within the dorsal striatum. We observed age-associated shifts in the inflammatory landscape and evidence of increased microglial activation, yet PNN homeostasis was largely preserved (2). PNNs are highly organized extracellular matrix (ECM) specializations that preferentially enwrap the soma and proximal dendrites of fast-spiking GABAergic parvalbumin (PV) interneurons, where they contribute to the regulation of synaptic plasticity and provide protection against oxidative stress (3,4). Building on these findings, we developed a working hypothesis to explain the apparent preservation of PNN homeostasis despite an aging-associated pro-inflammatory environment. The shift toward a pro-inflammatory milieu, together with increased gliosis and phagocytic activity, would be expected to impact the maintenance and integrity of perineuronal nets. The observed increase in phagocytosis-related markers may reflect microglia-directed activity as well as contributions from additional central nervous system (CNS) cell populations. Microglia are specialized embryonic-derived myeloid cells that serve as the resident immune cells of the brain and contribute to PNN homeostasis under physiological conditions (5). In Colon et al. 2025, we observed evidence of microgliosis (e.g., morphological changes, Iba1, Trem2) along with elevated expression of markers associated with phagocytosis (e.g., Cd68) and extracellular matrix-modifying proteases (e.g., Mmp9, Adam17) capable of cleaving key PNN components (2). Importantly, Cd68 expression is not exclusive to microglia and has been detected in brain infiltrating macrophages, reactive astrocytes, and neutrophils during inflammation (6-8). Thus, increased Cd68 levels may not solely reflect microglial phagocytic activation but may also reflect astrocyte reactivity and phagocytic phenotypes. Furthermore, astrocytes are the most abundant glial cell in the brain, and they play a major role in maintaining CNS homeostasis by regulating extracellular neurotransmitter concentrations, providing metabolic support, contributing to the synthesis and remodeling of PNN components, and modulating neuronal communication through their involvement in the tetrapartite synapse (9-12). Astrocytes can also phagocytosis microglial debris, myelin, and synapses (7). To better define the cellular source of phagocytic activity and its relationship to PNN remodeling in aging, we performed immunostaining for microglia (Iba1+), astrocytes (GFAP+), phagolysosomal activity (CD68+), and PNNs using Wisteria floribunda agglutinin (WFA+), enabling us to assess the spatial relationship between phagocytosis and PNN components.

neuroscience↗

Age-related inflammatory changes and perineuronal net dynamics: implications for neurodegenerative disorders.

BackgroundHealthy aging alone can lead to cognitive decline, decreased brain size, protein aggregation, accumulation of senescent cells and neuroinflammation. Furthermore, age is the primary risk factor for several neurodegenerative disorders such as Parkinsons and Alzheimers disease. Age-related neuroinflammation, as known as inflammaging, is thought to restrict brain plasticity. Perineuronal nets (PNNs), specialized extracellular matrix structures surrounding fast-spiking parvalbumin (PV) interneurons, regulate plasticity and protect neurons from oxidative stress. Given the known impact of inflammaging on neural circuits, this study examines age-associated changes in PNN homeostasis, glial activation, and neuroinflammation in two brain regions relevant to age-related neurodegenerative diseases. MethodsWe analyzed young (4-month-old) and aged (22-month-old) C57BL/6J male mice for several behavioral phenotypes [hippocampal-dependent spatial learning using the Barnes maze; locomotion and anxiety-related behaviors using Open field and T-maze]. Using immunostaining, PNNs (Wisteria floribunda agglutinin and aggrecan), PV interneurons, and microglial activation (Iba1) were quantified in both the hippocampus and dorsal striatum. Glial morphology was examined using a battery of cell body, branching, and endpoint analyses. Quantitative RT-PCR was used to analyze changes in the gene expression of inflammatory and extracellular matrix markers. ResultsAged mice exhibited hippocampal-dependent memory deficits without alterations in locomotion or anxiety-related behavior. PNN counts increased in the aged hippocampus, particularly in CA2, with a higher proportion of WFA+ and aggrecan+ PNNs. In contrast, PNN homeostasis was maintained in the dorsal striatum. In general, Aged mice showed increases in microglial activation and a subset of inflammatory markers. We report brain region- and age-specific gene expression changes in complement, matrix metalloproteinases, and other inflammatory markers. Aged striatal microglia displayed an activated morphology with larger cell bodies and reduced branching, as well as increased expression of markers for microgliosis (Iba1, TREM2, CD68). ConclusionsThese findings suggest that aging differentially affects neuroinflammation and PNN integrity across brain regions. The hippocampus exhibits PNN accumulation, neuroinflammation, and behavioral changes, whereas the striatum maintains PNN homeostasis concurrent with increased microglial activation. This work suggests that neuroinflammation contributes to age-related changes in PNNs and behavior underscoring the importance of region-specific therapeutic strategies targeting PNN regulation.

neuroscience↗

Jedi-1/MEGF12-mediated phagocytosis controls the pro-neurogenic properties of microglia in the ventricular-subventricular zone

Microglia are the primary phagocytes in the central nervous system and are responsible for clearing dead cells generated during development or disease. The phagocytic process shapes the phenotype of the microglia, which affects the local environment. A unique population of microglia reside in the ventricular-subventricular zone (V-SVZ) of neonatal mice, but how they influence this neurogenic niche is not well-understood. Here, we demonstrate that phagocytosis creates a pro-neurogenic microglial phenotype in the V-SVZ and that these microglia phagocytose apoptotic cells via the engulfment receptor Jedi-1. Deletion of Jedi-1 decreases apoptotic cell clearance, triggering the development of a neuroinflammatory phenotype, reminiscent of neurodegenerative and-age-associated microglia, that reduces neural precursor proliferation via elevated interleukin (IL)-1{beta} signaling; inhibition of IL-1 receptor rescues precursor proliferation in vivo. Together, these results reveal a critical role for Jedi-1 in connecting microglial phagocytic activity to a phenotype that promotes neurogenesis in the developing V-SVZ. Graphical Abstract. Jedi-1-dependent phagocytosis supports neurogenesis via suppression of microglial inflammatory pathway activationTop: Wild-type Proliferative-zone-Associated Microglia (PAMs) (cyan) use the engulfment receptor Jedi-1 ( Jedi) to engulf apoptotic cells (yellow) in the neurogenic ventricular-subventricular zone (V-SVZ) of the early postnatal brain. Jedi activation supports neural precursor cell (NPC) proliferation and the generation of new neurons. Bottom: Deletion of Jedi reduces microglial phagocytosis and transforms PAMs into Disease-associated Inflammatory Microglia (DIMs) characterized by the upregulation of canonical inflammatory genes and core DIM markers iden ified in the aging and neurodegenerative brain (Nlrp3, NLR family pyrin domain-containing 3; Tnf, tumor necrosis factor; Ccl4, C-C chemokine ligand 4 (also called macrophage inflammatory protein 1{beta}); Ccr5, C-C chemokine receptor type 5). Increased interleukin-1{beta} (IL-1{beta}) synthesis, release, and signaling in the Jedi-null V-SVZ reduces NPC proliferation and newborn neuron number. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=119 SRC="FIGDIR/small/531012v1_ufig1.gif" ALT="Figure 1"> View larger version (34K): org.highwire.dtl.DTLVardef@16b9785org.highwire.dtl.DTLVardef@a8be50org.highwire.dtl.DTLVardef@66b726org.highwire.dtl.DTLVardef@1825d8b_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIThe engulfment receptor Jedi-1 is expressed by microglia in the neonatal ventricular-subventricular zone (V-SVZ) neurogenic niche. C_LIO_LIJedi-1 knockout microglia have decreased engulfment ability, resulting in accumulation of dead cells in the V-SVZ. C_LIO_LILoss of Jedi-1 leads to a neuroinflammatory phenotype in microglia that is characteristic of neurodegenerative and age-associated microglia. C_LIO_LIMicroglial-specific loss of Jedi-1 reduces neurogenesis, which is rescued in vivo by inhibition of interleukin-1{beta} signaling. C_LI

neuroscience↗