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Article

Thyroid Hormone Induces Ca2+-Mediated Mitochondrial Activation in Brown Adipocytes

by
Minh-Hanh Thi Nguyen
1,2,3,
Dat Da Ly
1,2,
Nhung Thi Nguyen
1,2,
Xu-Feng Qi
4,
Hyon-Seung Yi
5,
Minho Shong
5,
Seung-Kuy Cha
1,2,3,
Sangkyu Park
1,6,* and
Kyu-Sang Park
1,2,3,*
1
Mitohormesis Research Center, Yonsei University Wonju College of Medicine, Wonju 26426, Gangwon-do, Korea
2
Department of Physiology, Yonsei University Wonju College of Medicine, Wonju 26426, Gangwon-do, Korea
3
Department of Global Medical Science, Yonsei University Wonju College of Medicine, Wonju 26426, Gangwon-do, Korea
4
Key Laboratory of Regenerative Medicine, Ministry of Education, Department of Developmental and Regenerative Biology, Jinan University, Guangzhou 510632, China
5
Department of Internal Medicine, Chungnam National University School of Medicine, Daejeon 35015, Korea
6
Department of Precision Medicine, Yonsei University Wonju College of Medicine, Wonju 26426, Gangwon-do, Korea
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2021, 22(16), 8640; https://doi.org/10.3390/ijms22168640
Submission received: 21 June 2021 / Revised: 6 August 2021 / Accepted: 7 August 2021 / Published: 11 August 2021
(This article belongs to the Special Issue Mitochondrial Protein Network: From Biogenesis to Bioenergetics in Health and Disease 2.0)
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Abstract

Thyroid hormones, including 3,5,3′-triiodothyronine (T3), cause a wide spectrum of genomic effects on cellular metabolism and bioenergetic regulation in various tissues. The non-genomic actions of T3 have been reported but are not yet completely understood. Acute T3 treatment significantly enhanced basal, maximal, ATP-linked, and proton-leak oxygen consumption rates (OCRs) of primary differentiated mouse brown adipocytes accompanied with increased protein abundances of uncoupling protein 1 (UCP1) and mitochondrial Ca2+ uniporter (MCU). T3 treatment depolarized the resting mitochondrial membrane potential (Ψm) but augmented oligomycin-induced hyperpolarization in brown adipocytes. Protein kinase B (AKT) and mammalian target of rapamycin (mTOR) were activated by T3, leading to the inhibition of autophagic degradation. Rapamycin, as an mTOR inhibitor, blocked T3-induced autophagic suppression and UCP1 upregulation. T3 increases intracellular Ca2+ concentration ([Ca2+]i) in brown adipocytes. Most of the T3 effects, including mTOR activation, UCP1 upregulation, and OCR increase, were abrogated by intracellular Ca2+ chelation with BAPTA-AM. Calmodulin inhibition with W7 or knockdown of MCU dampened T3-induced mitochondrial activation. Furthermore, edelfosine, a phospholipase C (PLC) inhibitor, prevented T3 from acting on [Ca2+]i, UCP1 abundance, Ψm, and OCR. We suggest that short-term exposure of T3 induces UCP1 upregulation and mitochondrial activation due to PLC-mediated [Ca2+]i elevation in brown adipocytes.
Keywords: brown adipose tissue (BAT); thyroid hormone; mitochondria; uncoupling protein 1 (UCP1); Ca2+ signaling brown adipose tissue (BAT); thyroid hormone; mitochondria; uncoupling protein 1 (UCP1); Ca2+ signaling

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MDPI and ACS Style

Nguyen, M.-H.T.; Ly, D.D.; Nguyen, N.T.; Qi, X.-F.; Yi, H.-S.; Shong, M.; Cha, S.-K.; Park, S.; Park, K.-S. Thyroid Hormone Induces Ca2+-Mediated Mitochondrial Activation in Brown Adipocytes. Int. J. Mol. Sci. 2021, 22, 8640. https://doi.org/10.3390/ijms22168640

AMA Style

Nguyen M-HT, Ly DD, Nguyen NT, Qi X-F, Yi H-S, Shong M, Cha S-K, Park S, Park K-S. Thyroid Hormone Induces Ca2+-Mediated Mitochondrial Activation in Brown Adipocytes. International Journal of Molecular Sciences. 2021; 22(16):8640. https://doi.org/10.3390/ijms22168640

Chicago/Turabian Style

Nguyen, Minh-Hanh Thi, Dat Da Ly, Nhung Thi Nguyen, Xu-Feng Qi, Hyon-Seung Yi, Minho Shong, Seung-Kuy Cha, Sangkyu Park, and Kyu-Sang Park. 2021. "Thyroid Hormone Induces Ca2+-Mediated Mitochondrial Activation in Brown Adipocytes" International Journal of Molecular Sciences 22, no. 16: 8640. https://doi.org/10.3390/ijms22168640

APA Style

Nguyen, M.-H. T., Ly, D. D., Nguyen, N. T., Qi, X.-F., Yi, H.-S., Shong, M., Cha, S.-K., Park, S., & Park, K.-S. (2021). Thyroid Hormone Induces Ca2+-Mediated Mitochondrial Activation in Brown Adipocytes. International Journal of Molecular Sciences, 22(16), 8640. https://doi.org/10.3390/ijms22168640

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