Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization

Functional cell death pathways are essential for normal ocular vascular development and tissue homeostasis. As our understanding of necrosis-based cell death pathways has expanded, the inclusion of regulated forms, including necroptosis, ferroptosis, and oxytosis, has occurred. Although the existenc...

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Main Authors: Yong-Seok Song, Shoujian Wang, SunYoung Park, Barbara Hanna, Kelsey J. Johnson, Soesiawati R. Darjatmoko, Mohammad Ali Saghiri, Ali Mohammad Saghiri, Bo Liu, Christine M. Sorenson, Nader Sheibani
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Language:English
Published: MDPI AG 2024-12-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/13/24/2109
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author Yong-Seok Song
Shoujian Wang
SunYoung Park
Barbara Hanna
Kelsey J. Johnson
Soesiawati R. Darjatmoko
Mohammad Ali Saghiri
Ali Mohammad Saghiri
Bo Liu
Christine M. Sorenson
Nader Sheibani
author_facet Yong-Seok Song
Shoujian Wang
SunYoung Park
Barbara Hanna
Kelsey J. Johnson
Soesiawati R. Darjatmoko
Mohammad Ali Saghiri
Ali Mohammad Saghiri
Bo Liu
Christine M. Sorenson
Nader Sheibani
author_sort Yong-Seok Song
collection DOAJ
description Functional cell death pathways are essential for normal ocular vascular development and tissue homeostasis. As our understanding of necrosis-based cell death pathways has expanded, the inclusion of regulated forms, including necroptosis, ferroptosis, and oxytosis, has occurred. Although the existence of these pathways is well described, our understanding of their role during vascular development and pathological neovascularization is very limited. Here, we examined the role of receptor-interacting protein kinase-3 (Ripk3), a key regulator of necroptosis, in postnatal retinal vascularization and retinal and choroidal neovascularization under pathological conditions. Postnatal vascularization of the retinal superficial layer in the absence of Ripk3 (<i>Ripk3</i><sup>−/−</sup>) was not significantly different from wild-type mice. However, we noted decreased retinal endothelial cells and pericyte numbers at 3 weeks of age when the formation of the retinal primary vascular plexus was complete. In contrast, choroidal and retinal neovascularization following laser treatment and oxygen-induced ischemic retinopathy increased in the absence of Ripk3 expression, respectively. In addition, the inhibition of RIPK1/3 activity suppressed choroidal neovascularization. Thus, Ripk3 expression and/or activity may have unique roles during normal and pathological ocular vascularization through its interactions with Caspase 8 and modulation of cell death processes.
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spelling doaj-art-bbbdfe1808d24ccdac938f37bbd311dc2025-08-20T02:00:43ZengMDPI AGCells2073-44092024-12-011324210910.3390/cells13242109Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological NeovascularizationYong-Seok Song0Shoujian Wang1SunYoung Park2Barbara Hanna3Kelsey J. Johnson4Soesiawati R. Darjatmoko5Mohammad Ali Saghiri6Ali Mohammad Saghiri7Bo Liu8Christine M. Sorenson9Nader Sheibani10Department of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Pediatrics, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Pediatrics, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Restorative Dentistry, Rutgers School of Dental Medicine, Newark, NJ 07103, USADepartment of Computer Science, William Paterson University, Wayne, NJ 07470, USADepartment of Cell and Regenerative Biology, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USAMcPherson Eye Research Institute, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USADepartment of Ophthalmology and Visual Sciences, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USAFunctional cell death pathways are essential for normal ocular vascular development and tissue homeostasis. As our understanding of necrosis-based cell death pathways has expanded, the inclusion of regulated forms, including necroptosis, ferroptosis, and oxytosis, has occurred. Although the existence of these pathways is well described, our understanding of their role during vascular development and pathological neovascularization is very limited. Here, we examined the role of receptor-interacting protein kinase-3 (Ripk3), a key regulator of necroptosis, in postnatal retinal vascularization and retinal and choroidal neovascularization under pathological conditions. Postnatal vascularization of the retinal superficial layer in the absence of Ripk3 (<i>Ripk3</i><sup>−/−</sup>) was not significantly different from wild-type mice. However, we noted decreased retinal endothelial cells and pericyte numbers at 3 weeks of age when the formation of the retinal primary vascular plexus was complete. In contrast, choroidal and retinal neovascularization following laser treatment and oxygen-induced ischemic retinopathy increased in the absence of Ripk3 expression, respectively. In addition, the inhibition of RIPK1/3 activity suppressed choroidal neovascularization. Thus, Ripk3 expression and/or activity may have unique roles during normal and pathological ocular vascularization through its interactions with Caspase 8 and modulation of cell death processes.https://www.mdpi.com/2073-4409/13/24/2109oxygen-induced ischemic retinopathychoroidal neovascularizationnecroptosisRIPK-proteinsretinal vascularization
spellingShingle Yong-Seok Song
Shoujian Wang
SunYoung Park
Barbara Hanna
Kelsey J. Johnson
Soesiawati R. Darjatmoko
Mohammad Ali Saghiri
Ali Mohammad Saghiri
Bo Liu
Christine M. Sorenson
Nader Sheibani
Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization
Cells
oxygen-induced ischemic retinopathy
choroidal neovascularization
necroptosis
RIPK-proteins
retinal vascularization
title Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization
title_full Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization
title_fullStr Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization
title_full_unstemmed Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization
title_short Receptor-Interacting Protein Kinase-3 Expression Impacts Ocular Vascular Development and Pathological Neovascularization
title_sort receptor interacting protein kinase 3 expression impacts ocular vascular development and pathological neovascularization
topic oxygen-induced ischemic retinopathy
choroidal neovascularization
necroptosis
RIPK-proteins
retinal vascularization
url https://www.mdpi.com/2073-4409/13/24/2109
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