Limited Oxidative Stress Favors Resistance to Skeletal Muscle Atrophy in Hibernating Brown Bears (Ursus Arctos)

Chazarin, Blandine; Ziemianin, Anna; Evans, Alina L.; Meugnier, Emmanuelle; Loizon, Emmanuelle; Chery, Isabelle; Arnemo, Jon M.; Swenson, Jon E.; Gauquelin-Koch, Guillemette; Simon, Chantal; Blanc, Stéphane; Lefai, Etienne; Bertile, Fabrice

doi:10.3390/antiox8090334

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Limited Oxidative Stress Favors Resistance to Skeletal Muscle Atrophy in Hibernating Brown Bears (Ursus Arctos)

^1,2,

^1,2,

⁴,

⁴,

¹,

^3,5

^6,7,

Guillemette Gauquelin-Koch

²,

Chantal Simon

⁴

Stéphane Blanc

¹,

Etienne Lefai

^4,8

and

Fabrice Bertile

^1,*

Université de Strasbourg, CNRS, IPHC UMR 7178, F-670000 Strasbourg, France

Centre National d’Etudes Spatiales, CNES, F-75001 Paris, France

Department of Forestry and Wildlife Management, Inland Norway University of Applied Sciences, Campus Evenstad, NO-2480 Koppang, Norway

⁴

CarMen Laboratory, INSERM 1060, INRA 1397, University of Lyon, F-69600 Oullins, France

⁵

Department of Wildlife, Fish, and Environmental Studies, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden

⁶

Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, NO-1432 Ås, Norway

⁷

Norwegian Institute for Nature Research, NO-7485 Trondheim, Norway

⁸

Université d’Auvergne, INRA, UNH UMR1019, F-63122 Saint-Genès Champanelle, France

Author to whom correspondence should be addressed.

Antioxidants 2019, 8(9), 334; https://doi.org/10.3390/antiox8090334

Received: 1 August 2019 / Revised: 18 August 2019 / Accepted: 21 August 2019 / Published: 22 August 2019

(This article belongs to the Section Health Outcomes of Antioxidants and Oxidative Stress)

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Abstract

Oxidative stress, which is believed to promote muscle atrophy, has been reported to occur in a few hibernators. However, hibernating bears exhibit efficient energy savings and muscle protein sparing, despite long-term physical inactivity and fasting. We hypothesized that the regulation of the oxidant/antioxidant balance and oxidative stress could favor skeletal muscle maintenance in hibernating brown bears. We showed that increased expressions of cold-inducible proteins CIRBP and RBM3 could favor muscle mass maintenance and alleviate oxidative stress during hibernation. Downregulation of the subunits of the mitochondrial electron transfer chain complexes I, II, and III, and antioxidant enzymes, possibly due to the reduced mitochondrial content, indicated a possible reduction of the production of reactive oxygen species in the hibernating muscle. Concomitantly, the upregulation of cytosolic antioxidant systems, under the control of the transcription factor NRF2, and the maintenance of the GSH/GSSG ratio suggested that bear skeletal muscle is not under a significant oxidative insult during hibernation. Accordingly, lower levels of oxidative damage were recorded in hibernating bear skeletal muscles. These results identify mechanisms by which limited oxidative stress may underlie the resistance to skeletal muscle atrophy in hibernating brown bears. They may constitute therapeutic targets for the treatment of human muscle atrophy. View Full-Text

Keywords: hibernation; brown bears; skeletal muscle; cold response; oxidative stress; NRF2

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Supplementary Materials

Supplementary File 1:
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Doi: 10.5281/zenodo.3357474
Description: Supplementary Figure S1. Representative blots of bear skeletal muscle proteins. Shown are representative images that have been obtained through western-blot analysis of the levels of catalase (CAT), heat shock protein HSP 90-beta (HSPAB1) mitochondrial stress-70 protein (HSPA9 or GRP75), nuclear factor E2-related factor 2 (NRF2 or NFE2L2), aflatoxin B1 aldehyde reductase member 2 (AKR7A2), carbonyl reductase (CBR1), and endoplasmic reticulum resident protein 29 (ERP29) in bear vastus lateralis muscles (N = 12/ group, except from NRF2: N = 7/ season). Corresponding quantifications can be seen in Figures 3 and 5.

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MDPI and ACS Style

Chazarin, B.; Ziemianin, A.; Evans, A.L.; Meugnier, E.; Loizon, E.; Chery, I.; Arnemo, J.M.; Swenson, J.E.; Gauquelin-Koch, G.; Simon, C.; Blanc, S.; Lefai, E.; Bertile, F. Limited Oxidative Stress Favors Resistance to Skeletal Muscle Atrophy in Hibernating Brown Bears (Ursus Arctos). Antioxidants 2019, 8, 334. https://doi.org/10.3390/antiox8090334

AMA Style

Chazarin B, Ziemianin A, Evans AL, Meugnier E, Loizon E, Chery I, Arnemo JM, Swenson JE, Gauquelin-Koch G, Simon C, Blanc S, Lefai E, Bertile F. Limited Oxidative Stress Favors Resistance to Skeletal Muscle Atrophy in Hibernating Brown Bears (Ursus Arctos). Antioxidants. 2019; 8(9):334. https://doi.org/10.3390/antiox8090334

Chicago/Turabian Style

Chazarin, Blandine, Anna Ziemianin, Alina L. Evans, Emmanuelle Meugnier, Emmanuelle Loizon, Isabelle Chery, Jon M. Arnemo, Jon E. Swenson, Guillemette Gauquelin-Koch, Chantal Simon, Stéphane Blanc, Etienne Lefai, and Fabrice Bertile. 2019. "Limited Oxidative Stress Favors Resistance to Skeletal Muscle Atrophy in Hibernating Brown Bears (Ursus Arctos)" Antioxidants 8, no. 9: 334. https://doi.org/10.3390/antiox8090334

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