Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways

<b>Background:</b> Ouabain is a steroid hormone that binds to the sodium pump (Na<sup>+</sup>, K<sup>+</sup>-ATPase) at physiological (nanomolar) concentrations, activating different signaling pathways. This interaction has been shown to prevent the axotomy-induce...

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Main Authors: Amanda Candida da Rocha Oliveira, Camila Saggioro Figueiredo, Ícaro Raony, Juliana Salles Von-Held-Ventura, Marcelo Gomes Granja, Thalita Mázala-de-Oliveira, Vinícius Henrique Pedrosa-Soares, Aline Araujo dos Santos, Elizabeth Giestal-de-Araujo
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Brain Sciences
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Online Access:https://www.mdpi.com/2076-3425/15/2/123
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author Amanda Candida da Rocha Oliveira
Camila Saggioro Figueiredo
Ícaro Raony
Juliana Salles Von-Held-Ventura
Marcelo Gomes Granja
Thalita Mázala-de-Oliveira
Vinícius Henrique Pedrosa-Soares
Aline Araujo dos Santos
Elizabeth Giestal-de-Araujo
author_facet Amanda Candida da Rocha Oliveira
Camila Saggioro Figueiredo
Ícaro Raony
Juliana Salles Von-Held-Ventura
Marcelo Gomes Granja
Thalita Mázala-de-Oliveira
Vinícius Henrique Pedrosa-Soares
Aline Araujo dos Santos
Elizabeth Giestal-de-Araujo
author_sort Amanda Candida da Rocha Oliveira
collection DOAJ
description <b>Background:</b> Ouabain is a steroid hormone that binds to the sodium pump (Na<sup>+</sup>, K<sup>+</sup>-ATPase) at physiological (nanomolar) concentrations, activating different signaling pathways. This interaction has been shown to prevent the axotomy-induced death of retinal ganglion cells (RGCs), although the underlying mechanisms remain unclear. <b>Objective:</b> In this study, we investigated potential mechanisms by which ouabain promotes RGC survival using primary cultures of rat neural retina. <b>Results:</b> Our findings indicate that ouabain regulates brain-derived neurotrophic factor (BDNF) signaling in retinal cells via matrix metalloproteinase-9-mediated processing of proBDNF to mature BDNF (mBDNF) and by increasing the phosphorylation of the mBDNF receptor, tropomyosin-related receptor kinase B. Ouabain also enhances the maturation of interleukin (IL)-1β through the increased activation of caspase-1, which mediates the processing of proIL-1β into IL-1β, and transiently upregulates both IL-1 receptor and IL-1 receptor antagonist (IL-1Ra). Treatment using either IL-1β or IL-1Ra alone is sufficient to enhance RGC survival similarly to that achieved with ouabain. Finally, we further show that ouabain prevents RGC death through a complex signaling mechanism shared by BDNF and IL-1β, which includes the activation of the Src and protein kinase C pathways. <b>Conclusions:</b> Collectively, these results suggest that ouabain stimulates the maturation and signaling of both BDNF and IL-1β, which act as key mediators of RGC survival.
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spelling doaj-art-4952b4f6e9124cffb6d4f4fc19da0c9d2025-08-20T02:44:55ZengMDPI AGBrain Sciences2076-34252025-01-0115212310.3390/brainsci15020123Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling PathwaysAmanda Candida da Rocha Oliveira0Camila Saggioro Figueiredo1Ícaro Raony2Juliana Salles Von-Held-Ventura3Marcelo Gomes Granja4Thalita Mázala-de-Oliveira5Vinícius Henrique Pedrosa-Soares6Aline Araujo dos Santos7Elizabeth Giestal-de-Araujo8Department of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niteroi 24020-141, BrazilDepartment of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niteroi 24020-141, BrazilInstitute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de Janeiro, Rio de Janeiro 21941-902, BrazilDepartment of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niteroi 24020-141, BrazilResearch, Innovation, and Surveillance Center for COVID-19 and Health Emergencies, Oswaldo Cruz Foundation, Rio de Janeiro 21040-360, BrazilDepartment of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niteroi 24020-141, BrazilDepartment of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niteroi 24020-141, BrazilNational Institute of Science and Technology on Neuroimmunomodulation—INCT-NIM, Oswaldo Cruz Foundation, Rio de Janeiro 21041-250, BrazilDepartment of Neurobiology and Program of Neurosciences, Institute of Biology, Federal Fluminense University, Niteroi 24020-141, Brazil<b>Background:</b> Ouabain is a steroid hormone that binds to the sodium pump (Na<sup>+</sup>, K<sup>+</sup>-ATPase) at physiological (nanomolar) concentrations, activating different signaling pathways. This interaction has been shown to prevent the axotomy-induced death of retinal ganglion cells (RGCs), although the underlying mechanisms remain unclear. <b>Objective:</b> In this study, we investigated potential mechanisms by which ouabain promotes RGC survival using primary cultures of rat neural retina. <b>Results:</b> Our findings indicate that ouabain regulates brain-derived neurotrophic factor (BDNF) signaling in retinal cells via matrix metalloproteinase-9-mediated processing of proBDNF to mature BDNF (mBDNF) and by increasing the phosphorylation of the mBDNF receptor, tropomyosin-related receptor kinase B. Ouabain also enhances the maturation of interleukin (IL)-1β through the increased activation of caspase-1, which mediates the processing of proIL-1β into IL-1β, and transiently upregulates both IL-1 receptor and IL-1 receptor antagonist (IL-1Ra). Treatment using either IL-1β or IL-1Ra alone is sufficient to enhance RGC survival similarly to that achieved with ouabain. Finally, we further show that ouabain prevents RGC death through a complex signaling mechanism shared by BDNF and IL-1β, which includes the activation of the Src and protein kinase C pathways. <b>Conclusions:</b> Collectively, these results suggest that ouabain stimulates the maturation and signaling of both BDNF and IL-1β, which act as key mediators of RGC survival.https://www.mdpi.com/2076-3425/15/2/123brain-derived neurotrophic factorcytokinegrowth factorsteroid hormoneinterleukin-1βmatrix metalloproteinase-9
spellingShingle Amanda Candida da Rocha Oliveira
Camila Saggioro Figueiredo
Ícaro Raony
Juliana Salles Von-Held-Ventura
Marcelo Gomes Granja
Thalita Mázala-de-Oliveira
Vinícius Henrique Pedrosa-Soares
Aline Araujo dos Santos
Elizabeth Giestal-de-Araujo
Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways
Brain Sciences
brain-derived neurotrophic factor
cytokine
growth factor
steroid hormone
interleukin-1β
matrix metalloproteinase-9
title Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways
title_full Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways
title_fullStr Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways
title_full_unstemmed Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways
title_short Ouabain Counteracts Retinal Ganglion Cell Death Through Modulation of BDNF and IL-1 Signaling Pathways
title_sort ouabain counteracts retinal ganglion cell death through modulation of bdnf and il 1 signaling pathways
topic brain-derived neurotrophic factor
cytokine
growth factor
steroid hormone
interleukin-1β
matrix metalloproteinase-9
url https://www.mdpi.com/2076-3425/15/2/123
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