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Transformation of Mitochondrial Architecture and Dynamics in the Chinese Soft-Shelled Turtle (Pelodiscus sinensis) During Hibernation

Published online by Cambridge University Press:  23 March 2022

Yufei Huang Open the ORCID record for Yufei Huang [Opens in a new window] ,
Xiaoya Chu ,
Yafei Zhang ,
Sheng Yang ,
Yonghong Shi  and
Qiusheng Chen Open the ORCID record for Qiusheng Chen [Opens in a new window]
Yufei Huang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China Institute of Comparative Medicine, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu Province 225009, P.R. China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, Jiangsu Province 225009, P.R. China
Xiaoya Chu
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China
Yafei Zhang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China
Sheng Yang
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China
Yonghong Shi
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, P.R. China
Qiusheng Chen*
Affiliation:
MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, Jiangsu Province 210095, P.R. China
*
*Corresponding author: Qiusheng Chen, E-mail: [email protected]
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Abstract

Hibernation is a biological status during which hibernating animals acclimatize themselves to reduced energy consumption through extreme but governed decline in self-metabolism. The role of mitochondria (Mt) in metabolic suppression during hibernation has already been elaborated in different organs and species. Nonetheless, the concretely changing process of mitochondrial architecture and the mechanism underlying this transformation during hibernation remains unclear. Herein, the present study was aimed at clarifying the detailed alteration of mitochondrial morphology and its potential role in the Chinese soft-shelled turtle (Pelodiscus sinensis) during different stages of hibernation. Compared with the nonhibernation period, the mitochondrial architecture was changing from round to crescent, and lipid droplet (LD)/Mt interaction was enhanced during hibernation, as observed by transmission electron microscopy (TEM). Further ultrastructural analysis uncovered that mitochondrial fusion was promptly accelerated in the early stage of hibernation, followed by mitochondrial fission in the middle stage, and mitophagy was boosted in the late stage. Moreover, gene and protein expression related to mitochondrial fusion, fission, and mitophagy accorded closely with the mitochondrial ultrastructural changes in different stages of hibernation. Taken together, our results clarified that the transformation of mitochondrial architecture and mitochondrial dynamics are of vital importance in maintaining internal environment homeostasis of Pelodiscus sinensis.

Keywords

chinese soft-shelled turtle (Pelodiscus sinensis)hibernationmitochondriaorganelle interactionultrastructure
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 28 , Issue 3 , June 2022 , pp. 790 - 800
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

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References

Ballinger, MA & Andrews, MT (2018). Nature's fat-burning machine: Brown adipose tissue in a hibernating mammal. J Exp Biol 221(Pt Suppl 1), jeb162586.CrossRefGoogle Scholar
Bose, A & Beal, MF (2016). Mitochondrial dysfunction in Parkinson's disease. J Neurochem 139(Suppl 1), 216–231.CrossRefGoogle ScholarPubMed
Brown, JC, Chung, DJ, Belgrave, KR & Staples, JF (2012). Mitochondrial metabolic suppression and reactive oxygen species production in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. Am J Physiol: Regul, Integr Comp Physiol 302(1), R15–R28.Google ScholarPubMed
Brown, JC & Staples, JF (2014). Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels. J Com Physiol B 184(3), 401–414.CrossRefGoogle ScholarPubMed
Chan, DC (2006). Mitochondria: Dynamic organelles in disease, aging, and development. Cell 125(7), 1241–1252.CrossRefGoogle Scholar
Chazarin, B, Storey, KB, Ziemianin, A, Chanon, S, Plumel, M, Chery, I, Durand, C, Evans, AL, Arnemo, JM, Zedrosser, A, Swenson, JE, Gauquelin-Koch, G, Simon, C, Blanc, S, Lefai, E & Bertile, F (2019). Metabolic reprogramming involving glycolysis in the hibernating brown bear skeletal muscle. Front Zool 16, 12.CrossRefGoogle ScholarPubMed
Chen, B, Niu, C, Yuan, L & Zhang, W (2019). Physiological responses in vitamin C system during hibernation in juvenile Chinese soft-shelled turtle Pelodiscus sinensis. J Oceanol Limnol 37(2), 767–776.CrossRefGoogle Scholar
Cooper, AN, Brown, JC & Staples, JF (2014). Are long chain acyl CoAs responsible for suppression of mitochondrial metabolism in hibernating 13-lined ground squirrels? Com Biochem Physiol Part B, Biochem Mol Biol 170, 50–57.CrossRefGoogle ScholarPubMed
Ferreira-da-Silva, A, Valacca, C, Rios, E, Pópulo, H, Soares, P, Sobrinho-Simões, M, Scorrano, L, Máximo, V & Campello, S (2015). Mitochondrial dynamics protein Drp1 is overexpressed in oncocytic thyroid tumors and regulates cancer cell migration. PLoS One 10(3), e0122308.CrossRefGoogle ScholarPubMed
Gallagher, K & Staples, JF (2013). Metabolism of brain cortex and cardiac muscle mitochondria in hibernating 13-lined ground squirrels ictidomys tridecemlineatus. Physiol Biochem Zool 86(1), 1–8.CrossRefGoogle ScholarPubMed
Garcia, GC, Bartol, TM, Phan, S, Bushong, EA, Perkins, G, Sejnowski, TJ, Ellisman, MH & Skupin, A (2019). Mitochondrial morphology provides a mechanism for energy buffering at synapses. Sci Rep 9(1), 18306.CrossRefGoogle ScholarPubMed
Geiser, F (2013). Hibernation. Curr Biol 23(5), R188–R193.CrossRefGoogle ScholarPubMed
Herinckx, G, Hussain, N, Opperdoes, FR, Storey, KB, Rider, MH & Vertommen, D (2017). Changes in the phosphoproteome of brown adipose tissue during hibernation in the ground squirrel, ictidomys tridecemlineatus. Physiol Genomics 49(9), 462–472.CrossRefGoogle ScholarPubMed
Huang, Y, Chen, H, Yang, P, Bai, X, Shi, Y, Vistro, WA, Tarique, I, Haseeb, A & Chen, Q (2019). Hepatic lipid droplet breakdown through lipolysis during hibernation in Chinese soft-shelled turtle (Pelodiscus sinensis). Aging 11(7), 1990–2002.CrossRefGoogle Scholar
Huang, Y, Yang, S, Bai, X, Shi, Y & Chen, Q (2021). Molecular and cellular mechanisms of lipid droplet breakdown in the liver of Chinese soft-shelled turtle (Pelodiscus sinensis). Front Mar Sci 8, 633425.CrossRefGoogle Scholar
Islam, MS, Hongxin, W, Ali Mahdi, A, Islam, M, Noman, A & an Wei, F (2021). Comparison of nutritional composition, physicochemical and antioxidant properties of muscle, liver, and shell from Grass Turtle (Chinemys reevesii). CyTA - J Food 19(1), 304–315.CrossRefGoogle Scholar
Jensen, BS, Pardue, S, Duffy, B, Kevil, CG, Staples, JF & Fago, A (2021). Suppression of mitochondrial respiration by hydrogen sulfide in hibernating 13-lined ground squirrels. Free Radical Biol Med 169, 181–186.CrossRefGoogle ScholarPubMed
Lahera, V, de Las Heras, N, López-Farré, A, Manucha, W & Ferder, L (2017). Role of mitochondrial dysfunction in hypertension and obesity. Curr Hypertens Rep 19(2), 11.CrossRefGoogle ScholarPubMed
Mishra, P & Chan, DC (2014). Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol 15(10), 634–646.CrossRefGoogle ScholarPubMed
Rambold, AS, Cohen, S & Lippincott-Schwartz, J (2015). Fatty acid trafficking in starved cells: Regulation by lipid droplet lipolysis, autophagy, and mitochondrial fusion dynamics. Dev Cell 32(6), 678–692.CrossRefGoogle ScholarPubMed
Rehman, J, Zhang, HJ, Toth, PT, Zhang, Y, Marsboom, G, Hong, Z, Salgia, R, Husain, AN, Wietholt, C & Archer, SL (2012). Inhibition of mitochondrial fission prevents cell cycle progression in lung cancer. FASEB J 26(5), 2175–2186.CrossRefGoogle ScholarPubMed
Salabei, JK & Hill, BG (2013). Mitochondrial fission induced by platelet-derived growth factor regulates vascular smooth muscle cell bioenergetics and cell proliferation. Redox Biol 1(1), 542–551.CrossRefGoogle ScholarPubMed
Schrepfer, E & Scorrano, L (2016). Mitofusins, from mitochondria to metabolism. Mol Cell 61(5), 683–694.CrossRefGoogle ScholarPubMed
Shirendeb, U, Reddy, AP, Manczak, M, Calkins, MJ, Mao, P, Tagle, DA & Reddy, PH (2011). Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in huntington's disease: Implications for selective neuronal damage. Hum Mol Genet 20(7), 1438–1455.CrossRefGoogle ScholarPubMed
Srivastava, A, Kumar Sarsani, V, Fiddes, I, Sheehan, SM, Seger, RL, Barter, ME, Neptune-Bear, S, Lindqvist, C & Korstanje, R (2019). Genome assembly and gene expression in the American black bear provides new insights into the renal response to hibernation. DNA Res 26(1), 37–44.CrossRefGoogle ScholarPubMed
Suen, DF, Norris, KL & Youle, RJ (2008). Mitochondrial dynamics and apoptosis. Genes Dev 22(12), 1577–1590.CrossRefGoogle ScholarPubMed
Tessier, SN, Wu, CW & Storey, KB (2019). Molecular control of protein synthesis, glucose metabolism, and apoptosis in the brain of hibernating thirteen-lined ground squirrels. Biochem Cell Biol 97(5), 536–544.CrossRefGoogle ScholarPubMed
Varuzhanyan, G, Rojansky, R, Sweredoski, MJ, Graham, RL, Hess, S, Ladinsky, MS & Chan, DC (2019). Mitochondrial fusion is required for spermatogonial differentiation and meiosis. eLife 8, e51601.CrossRefGoogle ScholarPubMed
Wanet, A, Arnould, T, Najimi, M & Renard, P (2015). Connecting mitochondria, metabolism, and stem cell fate. Stem Cells Dev 24(17), 1957–1971.CrossRefGoogle ScholarPubMed
Wu, NN, Zhang, Y & Ren, J (2019). Mitophagy, mitochondrial dynamics, and homeostasis in cardiovascular aging. Oxid Med Cell Longevity 2019, 9825061.CrossRefGoogle ScholarPubMed
Xiao, G, Liu, S, Xiao, Y, Zhu, Y, Zhao, H, Li, A, Li, Z & Feng, J (2019). Seasonal changes in gut microbiota diversity and composition in the greater horseshoe bat. Front Microbiol 10, 2247.CrossRefGoogle ScholarPubMed
Zhang, L, Yang, P, Bian, X, Zhang, Q, Ullah, S, Waqas, Y, Chen, X, Liu, Y, Chen, W, Le, Y, Chen, B, Wang, S & Chen, Q (2015). Modification of sperm morphology during long-term sperm storage in the reproductive tract of the Chinese soft-shelled turtle, Pelodiscus sinensis. Sci Rep 5, 16096.CrossRefGoogle ScholarPubMed
Zhang, WY, Niu, CJ, Chen, BJ & Yuan, L (2017). Antioxidant responses in hibernating Chinese soft-shelled turtle Pelodiscus sinensis hatchlings. Comp Biochem Physiol A Mol Integr Physiol 204, 9–16.CrossRefGoogle ScholarPubMed
Zhou, X, Niu, C, Sun, R & Li, Q (2002). The effect of vitamin C on the non-specific immune response of the juvenile soft-shelled turtle (Trionyx sinensis). Comp Bioche Physiol A, Mol Integr Physiol 131(4), 917–922.CrossRefGoogle Scholar
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