Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets

Background/Objectives: Blast-induced traumatic ocular injuries (bTOI) pose a significant risk to military and civilian populations, often leading to visual impairment or blindness. Retina, the innermost layer of ocular tissue consisting of photoreceptor and glial cells, is highly susceptible to blas...

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Main Authors: Chetan Pundkar, Rex Jeya Rajkumar Samdavid Thanapaul, Manoj Govindarajulu, Gaurav Phuyal, Joseph B. Long, Peethambaran Arun
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Neurology International
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Online Access:https://www.mdpi.com/2035-8377/17/3/42
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author Chetan Pundkar
Rex Jeya Rajkumar Samdavid Thanapaul
Manoj Govindarajulu
Gaurav Phuyal
Joseph B. Long
Peethambaran Arun
author_facet Chetan Pundkar
Rex Jeya Rajkumar Samdavid Thanapaul
Manoj Govindarajulu
Gaurav Phuyal
Joseph B. Long
Peethambaran Arun
author_sort Chetan Pundkar
collection DOAJ
description Background/Objectives: Blast-induced traumatic ocular injuries (bTOI) pose a significant risk to military and civilian populations, often leading to visual impairment or blindness. Retina, the innermost layer of ocular tissue consisting of photoreceptor and glial cells, is highly susceptible to blast injuries. Despite its prevalence, the molecular mechanisms underlying retinal damage following bTOI remain poorly understood, hindering the development of targeted therapies. Melatonin, a neuroprotective indoleamine with antioxidant, anti-inflammatory, and circadian regulatory properties, is synthesized in the retina and plays a crucial role in retinal health. Similarly, retina-specific genes, such as <i>Rhodopsin</i>, <i>Melanopsin</i>, and RPE65, are essential for photoreceptor function, visual signaling, and the visual cycle. However, their responses to blast exposure have not been thoroughly investigated. Methods: In this study, we utilized a ferret model of bTOI to evaluate the temporal expression of melatonin-synthesizing enzymes, such as tryptophan hydroxylase 1 and 2 (<i>TPH</i>1 and <i>TPH</i>2), Aralkylamine N-acetyltransferase (<i>AANAT</i>), and Acetylserotonin-O-methyltransferase (<i>ASMT</i>), and retina-specific genes (<i>Rhodopsin</i>, <i>Melanopsin</i>) and retinal pigment epithelium-specific 65 kDa protein (<i>RPE65</i>) at 4 h, 24 h, 7 days, and 28 days post-blast. Ferrets were exposed to tightly coupled blast overpressure waves using an advanced blast simulator, and retinal tissues were collected for quantitative polymerase chain reaction (qPCR) analysis. Results: The results revealed dynamic and multiphasic transcriptional responses. <i>TPH</i>1 and <i>TPH</i>2 exhibited significant upregulation at 24 h, followed by downregulation at 28 days, indicating blast-induced dysregulation of tryptophan metabolism, including melatonin synthesis. Similarly, <i>AANAT</i> and <i>ASMT</i> showed acute downregulation post-blast, with late-phase disruptions. <i>Rhodopsin</i> expression increased at 24 h but declined at 28 days, while <i>Melanopsin</i> and <i>RPE65</i> demonstrated early upregulation followed by downregulation, reflecting potential disruptions in circadian regulation and the visual cycle. Conclusions: These findings highlight the complex regulatory mechanisms underlying retinal responses to bTOI, involving neuroinflammation, oxidative stress, and disruptions in melatonin synthesis and photoreceptor cell functions. The results emphasize the therapeutic potential of melatonin in mitigating retinal damage and preserving visual function.
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spelling doaj-art-b6d2201a07284a69a9bf4c2e9d7242bc2025-08-20T03:43:29ZengMDPI AGNeurology International2035-83772025-03-011734210.3390/neurolint17030042Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in FerretsChetan Pundkar0Rex Jeya Rajkumar Samdavid Thanapaul1Manoj Govindarajulu2Gaurav Phuyal3Joseph B. Long4Peethambaran Arun5Blast-Induced Neurotrauma Branch, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USABlast-Induced Neurotrauma Branch, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USABlast-Induced Neurotrauma Branch, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USABlast-Induced Neurotrauma Branch, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USABlast-Induced Neurotrauma Branch, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USABlast-Induced Neurotrauma Branch, Center for Military Psychiatry and Neuroscience, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USABackground/Objectives: Blast-induced traumatic ocular injuries (bTOI) pose a significant risk to military and civilian populations, often leading to visual impairment or blindness. Retina, the innermost layer of ocular tissue consisting of photoreceptor and glial cells, is highly susceptible to blast injuries. Despite its prevalence, the molecular mechanisms underlying retinal damage following bTOI remain poorly understood, hindering the development of targeted therapies. Melatonin, a neuroprotective indoleamine with antioxidant, anti-inflammatory, and circadian regulatory properties, is synthesized in the retina and plays a crucial role in retinal health. Similarly, retina-specific genes, such as <i>Rhodopsin</i>, <i>Melanopsin</i>, and RPE65, are essential for photoreceptor function, visual signaling, and the visual cycle. However, their responses to blast exposure have not been thoroughly investigated. Methods: In this study, we utilized a ferret model of bTOI to evaluate the temporal expression of melatonin-synthesizing enzymes, such as tryptophan hydroxylase 1 and 2 (<i>TPH</i>1 and <i>TPH</i>2), Aralkylamine N-acetyltransferase (<i>AANAT</i>), and Acetylserotonin-O-methyltransferase (<i>ASMT</i>), and retina-specific genes (<i>Rhodopsin</i>, <i>Melanopsin</i>) and retinal pigment epithelium-specific 65 kDa protein (<i>RPE65</i>) at 4 h, 24 h, 7 days, and 28 days post-blast. Ferrets were exposed to tightly coupled blast overpressure waves using an advanced blast simulator, and retinal tissues were collected for quantitative polymerase chain reaction (qPCR) analysis. Results: The results revealed dynamic and multiphasic transcriptional responses. <i>TPH</i>1 and <i>TPH</i>2 exhibited significant upregulation at 24 h, followed by downregulation at 28 days, indicating blast-induced dysregulation of tryptophan metabolism, including melatonin synthesis. Similarly, <i>AANAT</i> and <i>ASMT</i> showed acute downregulation post-blast, with late-phase disruptions. <i>Rhodopsin</i> expression increased at 24 h but declined at 28 days, while <i>Melanopsin</i> and <i>RPE65</i> demonstrated early upregulation followed by downregulation, reflecting potential disruptions in circadian regulation and the visual cycle. Conclusions: These findings highlight the complex regulatory mechanisms underlying retinal responses to bTOI, involving neuroinflammation, oxidative stress, and disruptions in melatonin synthesis and photoreceptor cell functions. The results emphasize the therapeutic potential of melatonin in mitigating retinal damage and preserving visual function.https://www.mdpi.com/2035-8377/17/3/42blast-induced traumatic ocular injuryretinamelatonin
spellingShingle Chetan Pundkar
Rex Jeya Rajkumar Samdavid Thanapaul
Manoj Govindarajulu
Gaurav Phuyal
Joseph B. Long
Peethambaran Arun
Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets
Neurology International
blast-induced traumatic ocular injury
retina
melatonin
title Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets
title_full Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets
title_fullStr Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets
title_full_unstemmed Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets
title_short Dysregulation of Retinal Melatonin Biosynthetic Pathway and Differential Expression of Retina-Specific Genes Following Blast-Induced Ocular Injury in Ferrets
title_sort dysregulation of retinal melatonin biosynthetic pathway and differential expression of retina specific genes following blast induced ocular injury in ferrets
topic blast-induced traumatic ocular injury
retina
melatonin
url https://www.mdpi.com/2035-8377/17/3/42
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AT manojgovindarajulu dysregulationofretinalmelatoninbiosyntheticpathwayanddifferentialexpressionofretinaspecificgenesfollowingblastinducedocularinjuryinferrets
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