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Tannic Acid Provides Neuroprotective Effects Against Traumatic Brain Injury Through the PGC-1α/Nrf2/HO-1 Pathway

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Abstract

The present research was conducted to elucidate a possible molecular mechanism related to neuromodulatory effects of tannic acid (TA) supplementation against traumatic brain injury (TBI) in a rodent model. Oxidative damage and neuroinflammation play a critical role in TBI and lead to behavioral alterations and neuronal dysfunction and death. These changes suggest a potential avenue in neurotherapeutic intervention. The aim of the present study was to investigate the neuroprotective effects of TA and potential mechanism of these effects in a controlled cortical impact injury model of TBI in Wistar rats that were treated with TA (50 mg/kg body weight. i.p.) before 30 min and 6 and 18 h after TBI. TBI-induced rats were examined after 24 h for behavioral dysfunction, Nissl stain, lipid peroxidation rate, glutathione level, activities of antioxidant enzymes (catalase, glutathione S-transferase, glutathione peroxidase, and superoxide dismutase), the expression level of 4-hydroxynonenal, pro-inflammatory cytokines such as tumor necrosis factor alpha and interleukin-1 beta, as well as brain edema and immunoreactivity of glial fibrillary acidic protein. Results indicated that TA supplementation significantly modulated above mentioned alterations. Moreover, TA treatment effectively upregulated the protein expression of peroxisome proliferator–activated receptor gamma co-activator 1 alpha (PGC-1α) and nuclear factor-E2-related factor-2 (Nrf2) as well as mitochondrial transcription factor A and heme oxygenase-1 (HO-1) following TBI. Overall, our results suggest that TA effectively ameliorates the behavioral alterations, oxidative damage, mitochondrial impairment, and inflammation against TBI that may be attributed to activation of PGC-1α/Nrf-2/HO-1 signaling pathway.

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Abbreviations

4-HNE:

4-Hydroxynonenal

CAT:

Catalase

CDNB:

1-Chloro-2,4-dinitrobenzene

DTNB:

5,5′-Dithiobis-2-nitrobenzoic acid

GFAP:

Glial fibrillary acidic protein

GPX:

Glutathione peroxidase

GSH:

Reduced glutathione

GST:

Glutathione S-transferase

HO-1:

Heme oxygenase-1

IL-1β:

Interleukin-1 beta

NADPH:

Nicotinamide adenine dinucleotide phosphate reduced

Nrf2:

Nuclear factor-E-2-regulated factor-2

PARP:

Ploy (ADP-ribose) polymerase

PGC-1α:

Peroxisome proliferator–activated receptor gamma co-activator

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TA:

Tannic acid

TBI:

Traumatic brain injury

Tfam:

Mitochondrial transcription factor A

TNF-α:

Tumor necrosis factor alpha

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Funding

Mr. Mohd Salman is a recipient of Senior Research Fellowship from the Indian Council of Medical Research (File No. 3/1/2/4/Trauma/2019-NCD-1), Government of India. Dr. Heena Tabassum received financial grant from the Department of Biotechnology, Ministry of Science and Technology, Government of India (DBT BioCARe Program, sanction no. BT/Bio-CARe/01/10219/2013-14). The grant nos. [SR/FST/LS-I/2017/05(C)] and [SR/PURSE Phase2/39 (C)], received under DST-FIST and DST-PURSE prorgams from the Department of Science and Technology under Ministry of Science & Technology, Government of India are also acknowledged.

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Authors and Affiliations

  1. Department of Medical Elementology and Toxicology, School of Chemical and Life Sciences, Jamia Hamdard, New Delhi, 110062, India

    Mohd. Salman & Suhel Parvez

  2. Division of Biomedical Sciences, Indian Council of Medical Research, Ministry of Health and Family Welfare, Govt. of India, V. Ramalingaswamy Bhawan, P.O. Box No. 4911, New Delhi, 110029, India

    Heena Tabassum

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Salman, M., Tabassum, H. & Parvez, S. Tannic Acid Provides Neuroprotective Effects Against Traumatic Brain Injury Through the PGC-1α/Nrf2/HO-1 Pathway. Mol Neurobiol 57, 2870–2885 (2020). https://doi.org/10.1007/s12035-020-01924-3

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