TY - JOUR
T1 - The p53 inactivators pifithrin-μ and pifithrin-α mitigate TBI-induced neuronal damage through regulation of oxidative stress, neuroinflammation, autophagy and mitophagy
AU - Yang, Ling Yu
AU - Greig, Nigel H.
AU - Tweedie, David
AU - Jung, Yoo Jin
AU - Chiang, Yung Hsiao
AU - Hoffer, Barry J.
AU - Miller, Jonathan P.
AU - Chang, Ke Hui
AU - Wang, Jia Yi
N1 - Copyright © 2019. Published by Elsevier Inc.
PY - 2020/2
Y1 - 2020/2
N2 - Traumatic brain injury (TBI) is one of the most common causes of death and disability worldwide. We investigated whether inhibition of p53 using pifithrin (PFT)-α or PFT-μ provides neuroprotective effects via p53 transcriptional dependent or -independent mechanisms, respectively. Sprague Dawley rats were subjected to controlled cortical impact TBI followed by the administration of PFTα or PFT-μ (2 mg/kg, i.v.) at 5 h after TBI. Brain contusion volume, as well as sensory and motor functions were evaluated at 24 h after TBI. TBI-induced impairments were mitigated by both PFT-α and PFT-μ. Fluoro-Jade C staining was used to label degenerating neurons within the TBI-induced cortical contusion region that, together with Annexin V positive neurons, were reduced by PFT-μ. Double immunofluorescence staining similarly demonstrated that PFT-μ significantly increased HO-1 positive neurons and mRNA expression in the cortical contusion region as well as decreased numbers of 4-hydroxynonenal (4HNE)-positive cells. Levels of mRNA encoding for p53, autophagy, mitophagy, anti-oxidant, anti-inflammatory related genes and proteins were measured by RT-qPCR and immunohistochemical staining, respectively. PFT-α, but not PFT-μ, significantly lowered p53 mRNA expression. Both PFT-α and PFT-μ lowered TBI-induced pro-inflammatory cytokines (IL-1β and IL-6) mRNA levels as well as TBI-induced autophagic marker localization (LC3 and p62). Finally, treatment with PFT-μ mitigated TBI-induced declines in mRNA levels of PINK-1 and SOD2. Our data suggest that both PFT-μ and PFT-α provide neuroprotective actions through regulation of oxidative stress, neuroinflammation, autophagy, and mitophagy mechanisms, and that PFT-μ, in particular, holds promise as a TBI treatment strategy.
AB - Traumatic brain injury (TBI) is one of the most common causes of death and disability worldwide. We investigated whether inhibition of p53 using pifithrin (PFT)-α or PFT-μ provides neuroprotective effects via p53 transcriptional dependent or -independent mechanisms, respectively. Sprague Dawley rats were subjected to controlled cortical impact TBI followed by the administration of PFTα or PFT-μ (2 mg/kg, i.v.) at 5 h after TBI. Brain contusion volume, as well as sensory and motor functions were evaluated at 24 h after TBI. TBI-induced impairments were mitigated by both PFT-α and PFT-μ. Fluoro-Jade C staining was used to label degenerating neurons within the TBI-induced cortical contusion region that, together with Annexin V positive neurons, were reduced by PFT-μ. Double immunofluorescence staining similarly demonstrated that PFT-μ significantly increased HO-1 positive neurons and mRNA expression in the cortical contusion region as well as decreased numbers of 4-hydroxynonenal (4HNE)-positive cells. Levels of mRNA encoding for p53, autophagy, mitophagy, anti-oxidant, anti-inflammatory related genes and proteins were measured by RT-qPCR and immunohistochemical staining, respectively. PFT-α, but not PFT-μ, significantly lowered p53 mRNA expression. Both PFT-α and PFT-μ lowered TBI-induced pro-inflammatory cytokines (IL-1β and IL-6) mRNA levels as well as TBI-induced autophagic marker localization (LC3 and p62). Finally, treatment with PFT-μ mitigated TBI-induced declines in mRNA levels of PINK-1 and SOD2. Our data suggest that both PFT-μ and PFT-α provide neuroprotective actions through regulation of oxidative stress, neuroinflammation, autophagy, and mitophagy mechanisms, and that PFT-μ, in particular, holds promise as a TBI treatment strategy.
KW - Autophagy
KW - Mitophagy
KW - Neuroinflammation
KW - p53
KW - PFT-α
KW - PFT-μ
KW - Pifithrin analogs
KW - Traumatic brain injury (TBI)
KW - Neurons/pathology
KW - Autophagy/drug effects
KW - Male
KW - Brain Injuries, Traumatic/drug therapy
KW - Behavior, Animal
KW - Oxidative Stress/drug effects
KW - Sulfonamides/therapeutic use
KW - Cytokines/metabolism
KW - Heme Oxygenase (Decyclizing)/biosynthesis
KW - Benzothiazoles/therapeutic use
KW - Neuroprotective Agents/therapeutic use
KW - Brain Contusion/drug therapy
KW - Toluene/analogs & derivatives
KW - Rats
KW - Rats, Sprague-Dawley
KW - Animals
KW - Antioxidants/metabolism
KW - Encephalitis/drug therapy
KW - Mitophagy/drug effects
KW - Tumor Suppressor Protein p53/antagonists & inhibitors
UR - http://www.scopus.com/inward/record.url?scp=85076186182&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85076186182&partnerID=8YFLogxK
U2 - 10.1016/j.expneurol.2019.113135
DO - 10.1016/j.expneurol.2019.113135
M3 - Article
C2 - 31778663
AN - SCOPUS:85076186182
SN - 0014-4886
VL - 324
JO - Experimental Neurology
JF - Experimental Neurology
M1 - 113135
ER -