Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury

<b>Background/Objectives:</b> Traumatic brain injury (TBI) remains a significant and urgent medical concern for the US military. TBI triggers excitotoxic responses immediately, involving mitochondrial dysfunction characterized by loss of calcium (Ca<sup>2+</sup>) cycling, mem...

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Main Authors: Hiren R. Modi, Sudeep Musyaju, Anke H. Scultetus, Jignesh D. Pandya
Format: Article
Language:English
Published: MDPI AG 2025-06-01
Series:Biomedicines
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Online Access:https://www.mdpi.com/2227-9059/13/7/1520
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author Hiren R. Modi
Sudeep Musyaju
Anke H. Scultetus
Jignesh D. Pandya
author_facet Hiren R. Modi
Sudeep Musyaju
Anke H. Scultetus
Jignesh D. Pandya
author_sort Hiren R. Modi
collection DOAJ
description <b>Background/Objectives:</b> Traumatic brain injury (TBI) remains a significant and urgent medical concern for the US military. TBI triggers excitotoxic responses immediately, involving mitochondrial dysfunction characterized by loss of calcium (Ca<sup>2+</sup>) cycling, membrane damage and increased cell death. However, a comprehensive understanding of mitochondria-centric excitotoxic responses over time has yet to be fully demonstrated after severe TBI. The current study evaluated mitochondria-centric time course responses between 30 min and 2 weeks (seven time points) after penetrating TBI (pTBI). <b>Methods</b>: Anesthetized adult male Sprague-Dawley rats were subjected to either 10% unilateral pTBI or Sham craniectomy. Animals were euthanized at various time points, and mitochondria were isolated from the injury core. <b>Results</b>: Post-injury mitochondrial Ca<sup>2+</sup> homeostasis was significantly compromised in pTBI compared to the Sham group. In parallel, mitochondrial membrane integrity markers, including cytochrome c (Cyt C) and voltage-dependent anion channel (VDAC), showed significant reduction over time post-pTBI. Apoptosis-responsive markers, such as glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and B-cell lymphoma 2 (Bcl-2), exhibited elevated responses over time post-pTBI. <b>Conclusions</b>: Our results demonstrate profound insights into elevated excitotoxic mitochondrial damage after severe TBI. This time course study uncovers novel mitochondrial targets involved in TBI excitotoxicity and offers mitigation opportunities to alleviate excitotoxic responses after penetrating TBI.
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spelling doaj-art-e499b8f2a667475994015928151f5e1f2025-08-20T03:36:02ZengMDPI AGBiomedicines2227-90592025-06-01137152010.3390/biomedicines13071520Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain InjuryHiren R. Modi0Sudeep Musyaju1Anke H. Scultetus2Jignesh D. Pandya3Brain Trauma Neuroprotection Branch, Walter Reed Army Institute of Research (WRAIR), Silver Spring, MD 20910, USABrain Trauma Neuroprotection Branch, Walter Reed Army Institute of Research (WRAIR), Silver Spring, MD 20910, USABrain Trauma Neuroprotection Branch, Walter Reed Army Institute of Research (WRAIR), Silver Spring, MD 20910, USABrain Trauma Neuroprotection Branch, Walter Reed Army Institute of Research (WRAIR), Silver Spring, MD 20910, USA<b>Background/Objectives:</b> Traumatic brain injury (TBI) remains a significant and urgent medical concern for the US military. TBI triggers excitotoxic responses immediately, involving mitochondrial dysfunction characterized by loss of calcium (Ca<sup>2+</sup>) cycling, membrane damage and increased cell death. However, a comprehensive understanding of mitochondria-centric excitotoxic responses over time has yet to be fully demonstrated after severe TBI. The current study evaluated mitochondria-centric time course responses between 30 min and 2 weeks (seven time points) after penetrating TBI (pTBI). <b>Methods</b>: Anesthetized adult male Sprague-Dawley rats were subjected to either 10% unilateral pTBI or Sham craniectomy. Animals were euthanized at various time points, and mitochondria were isolated from the injury core. <b>Results</b>: Post-injury mitochondrial Ca<sup>2+</sup> homeostasis was significantly compromised in pTBI compared to the Sham group. In parallel, mitochondrial membrane integrity markers, including cytochrome c (Cyt C) and voltage-dependent anion channel (VDAC), showed significant reduction over time post-pTBI. Apoptosis-responsive markers, such as glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and B-cell lymphoma 2 (Bcl-2), exhibited elevated responses over time post-pTBI. <b>Conclusions</b>: Our results demonstrate profound insights into elevated excitotoxic mitochondrial damage after severe TBI. This time course study uncovers novel mitochondrial targets involved in TBI excitotoxicity and offers mitigation opportunities to alleviate excitotoxic responses after penetrating TBI.https://www.mdpi.com/2227-9059/13/7/1520severe traumatic brain injurytime coursemitochondrial damageexcitotoxicitycalcium homeostasiscell death
spellingShingle Hiren R. Modi
Sudeep Musyaju
Anke H. Scultetus
Jignesh D. Pandya
Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury
Biomedicines
severe traumatic brain injury
time course
mitochondrial damage
excitotoxicity
calcium homeostasis
cell death
title Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury
title_full Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury
title_fullStr Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury
title_full_unstemmed Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury
title_short Temporal Changes in Mitochondria-Centric Excitotoxic Responses Following Severe Penetrating Traumatic Brain Injury
title_sort temporal changes in mitochondria centric excitotoxic responses following severe penetrating traumatic brain injury
topic severe traumatic brain injury
time course
mitochondrial damage
excitotoxicity
calcium homeostasis
cell death
url https://www.mdpi.com/2227-9059/13/7/1520
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