Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model

<b>Background</b>: An acute angle-closure attack (AAC) is an ocular emergency that results from a rapid increase in intraocular pressure (IOP). Sustained IOP elevation induces severe degeneration of retinal ganglion cells (RGCs) without treatment. Overactivated microglia, key participant...

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Main Authors: Taimu Sato, Makoto Ishikawa, Yukitoshi Izumi, Naoya Shibata, Kota Sato, Michiko Ohno-Oishi, Hiroshi Tawarayama, Hiroshi Kunikata, Charles F. Zorumski, Toru Nakazawa
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Language:English
Published: MDPI AG 2025-07-01
Series:Biomedicines
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Online Access:https://www.mdpi.com/2227-9059/13/7/1670
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author Taimu Sato
Makoto Ishikawa
Yukitoshi Izumi
Naoya Shibata
Kota Sato
Michiko Ohno-Oishi
Hiroshi Tawarayama
Hiroshi Kunikata
Charles F. Zorumski
Toru Nakazawa
author_facet Taimu Sato
Makoto Ishikawa
Yukitoshi Izumi
Naoya Shibata
Kota Sato
Michiko Ohno-Oishi
Hiroshi Tawarayama
Hiroshi Kunikata
Charles F. Zorumski
Toru Nakazawa
author_sort Taimu Sato
collection DOAJ
description <b>Background</b>: An acute angle-closure attack (AAC) is an ocular emergency that results from a rapid increase in intraocular pressure (IOP). Sustained IOP elevation induces severe degeneration of retinal ganglion cells (RGCs) without treatment. Overactivated microglia, key participants in innate immune responses, have critical roles in the pathogenesis of IOP-induced RGC death, although precise mechanisms remain unclear. In the present study, we used a rat ex vivo acute glaucoma model to investigate the role of microglial signaling in RGC death and examined whether pharmacological depletion of microglia using a CSF-1R inhibitor, PLX5622, exerts neuroprotection against pressure-induced retinal injury. <b>Methods</b>: Ex vivo rat retinas were exposed to hydrostatic pressure (10 mmHg or 75 mmHg) for 24 h. Pressure-dependent changes in retinal microglia and RGCs were detected by immunofluorescence. Morphological changes in the retina and RGC apoptosis were examined using light microscopy and TUNEL staining, respectively. The expression of NLRP3, active caspase-1, pro IL-1β, and IL-1β were examined using Western blotting. Effects of PLX5622, an agent that depletes microglia, were examined in morphology, apoptosis, and protein expression assays, while TAK-242, a TLR4 inhibitor, was examined against protein expression. <b>Results</b>: Pressure loading at 75 mmHg markedly increased activated microglia and apoptotic RGCs in the isolated retinas. Western blotting revealed increases in expression of NLRP3, active caspase-1, pro IL-1β, and IL-1β at 75 mmHg compared to 10 mmHg. Inhibition of pressure-induced increases in NLRP3 by TAK-242 indicates that pressure elevation induces RGC death via activation of the TLR4–NLRP3 inflammasome cascade. PLX5622 depleted microglia at 75 mmHg and significantly decreased expression of NLRP3, active caspase-1, pro IL-1β, and IL-1β at 75 mmHg, resulting in preservation of RGCs. <b>Conclusions</b>: These results indicate that pressure elevation induces proliferation of inflammatory microglia and promotes IL-1β production via activation of the TLR4–NLRP3 inflammasome cascade, resulting in RGC death. Pharmacological depletion of microglia with PLX5622 could be a potential neuroprotective approach to preserve RGCs from inflammatory cytokines in AAC eyes.
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spelling doaj-art-bc838e613910412abc24e9796bcafa612025-08-20T03:36:35ZengMDPI AGBiomedicines2227-90592025-07-01137167010.3390/biomedicines13071670Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma ModelTaimu Sato0Makoto Ishikawa1Yukitoshi Izumi2Naoya Shibata3Kota Sato4Michiko Ohno-Oishi5Hiroshi Tawarayama6Hiroshi Kunikata7Charles F. Zorumski8Toru Nakazawa9Department of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, JapanDepartment of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, JapanTaylor Family Institute for Innovative Psychiatric Research, Washington University School of Medicine, St. Louis, MO 63110, USAAoba Eye Clinic, Akita 010-1413, JapanDepartment of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, JapanDepartment of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, JapanDepartment of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, JapanDepartment of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, JapanTaylor Family Institute for Innovative Psychiatric Research, Washington University School of Medicine, St. Louis, MO 63110, USADepartment of Ophthalmology, Tohoku University Graduate School of Medicine, Sendai 980-8574, Japan<b>Background</b>: An acute angle-closure attack (AAC) is an ocular emergency that results from a rapid increase in intraocular pressure (IOP). Sustained IOP elevation induces severe degeneration of retinal ganglion cells (RGCs) without treatment. Overactivated microglia, key participants in innate immune responses, have critical roles in the pathogenesis of IOP-induced RGC death, although precise mechanisms remain unclear. In the present study, we used a rat ex vivo acute glaucoma model to investigate the role of microglial signaling in RGC death and examined whether pharmacological depletion of microglia using a CSF-1R inhibitor, PLX5622, exerts neuroprotection against pressure-induced retinal injury. <b>Methods</b>: Ex vivo rat retinas were exposed to hydrostatic pressure (10 mmHg or 75 mmHg) for 24 h. Pressure-dependent changes in retinal microglia and RGCs were detected by immunofluorescence. Morphological changes in the retina and RGC apoptosis were examined using light microscopy and TUNEL staining, respectively. The expression of NLRP3, active caspase-1, pro IL-1β, and IL-1β were examined using Western blotting. Effects of PLX5622, an agent that depletes microglia, were examined in morphology, apoptosis, and protein expression assays, while TAK-242, a TLR4 inhibitor, was examined against protein expression. <b>Results</b>: Pressure loading at 75 mmHg markedly increased activated microglia and apoptotic RGCs in the isolated retinas. Western blotting revealed increases in expression of NLRP3, active caspase-1, pro IL-1β, and IL-1β at 75 mmHg compared to 10 mmHg. Inhibition of pressure-induced increases in NLRP3 by TAK-242 indicates that pressure elevation induces RGC death via activation of the TLR4–NLRP3 inflammasome cascade. PLX5622 depleted microglia at 75 mmHg and significantly decreased expression of NLRP3, active caspase-1, pro IL-1β, and IL-1β at 75 mmHg, resulting in preservation of RGCs. <b>Conclusions</b>: These results indicate that pressure elevation induces proliferation of inflammatory microglia and promotes IL-1β production via activation of the TLR4–NLRP3 inflammasome cascade, resulting in RGC death. Pharmacological depletion of microglia with PLX5622 could be a potential neuroprotective approach to preserve RGCs from inflammatory cytokines in AAC eyes.https://www.mdpi.com/2227-9059/13/7/1670glaucomaintraocular pressureneuroinflammationNLRP3 inflammasomeinterleukin-1βneuroprotection
spellingShingle Taimu Sato
Makoto Ishikawa
Yukitoshi Izumi
Naoya Shibata
Kota Sato
Michiko Ohno-Oishi
Hiroshi Tawarayama
Hiroshi Kunikata
Charles F. Zorumski
Toru Nakazawa
Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model
Biomedicines
glaucoma
intraocular pressure
neuroinflammation
NLRP3 inflammasome
interleukin-1β
neuroprotection
title Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model
title_full Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model
title_fullStr Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model
title_full_unstemmed Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model
title_short Involvement of Microglia in Retinal Ganglion Cell Injury Induced by IOP Elevation in a Rat Ex Vivo Acute Glaucoma Model
title_sort involvement of microglia in retinal ganglion cell injury induced by iop elevation in a rat ex vivo acute glaucoma model
topic glaucoma
intraocular pressure
neuroinflammation
NLRP3 inflammasome
interleukin-1β
neuroprotection
url https://www.mdpi.com/2227-9059/13/7/1670
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