Melatonin Regulates Differentiation of Sheep Brown Adipocyte Precursor Cells AMP-Activated Protein Kinase

Overview

Journal Front Vet Sci

Specialty Veterinary Medicine

Date 2021 Jul 8

PMID 34235199

Citations 4

Authors

Xu-Yang Gao

Bu-Hao Deng

Xin-Rui Li

Yu Wang

Jian-Xin Zhang

Xiao-Yan Hao

Jun-Xing Zhao

Affiliations

Soon will be listed here.

Abstract

In sheep industry, hypothermia caused by insufficient brown adipose tissue (BAT) deposits is one of the major causes of lamb deaths. Enhancing the formation and function of BAT in neonatal lamb increases thermogenesis and hence reduces economic losses. The aim of the present study was to explore the effect and mechanism of melatonin on sheep brown adipocyte formation and function. Sheep brown adipocyte precursor cells (SBACs) isolated from perirenal BAT were treated with melatonin (1 and 10 nM). The SBACs subjected to melatonin exhibited a decreased proliferation ability, accompanied by down-regulated proliferating cell nuclear antigen, cyclin D1, and CDK4 protein contents in a melatonin dose-dependent manner. Melatonin promoted brown adipocyte formation and induced the expression of brown adipogenic markers, including and during differentiation of SBAC. Moreover, the AMP-activated protein kinase α1 (AMPKα1) activity was positively correlated with brown adipocyte formation potential. Importantly, melatonin effectively activated AMPKα1. Furthermore, promotional effects of melatonin were abolished by AMPKα1 knockout, suggesting the involvement of AMPKα1 in this process. Collectively, these results suggested that melatonin enhanced brown adipocyte formation in SBACs through activation of AMPKα1.

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References

Chouchani E, Kazak L, Spiegelman B . New Advances in Adaptive Thermogenesis: UCP1 and Beyond. Cell Metab. 2018; 29(1):27-37. DOI: 10.1016/j.cmet.2018.11.002. View

Yang Q, Liang X, Sun X, Zhang L, Fu X, Rogers C . AMPK/α-Ketoglutarate Axis Dynamically Mediates DNA Demethylation in the Prdm16 Promoter and Brown Adipogenesis. Cell Metab. 2016; 24(4):542-554. PMC: 5061633. DOI: 10.1016/j.cmet.2016.08.010. View

Alexander G, Williams D . Shivering and non-shivering therogenesis during summit metabolism in young lambs. J Physiol. 1968; 198(2):251-76. PMC: 1365322. DOI: 10.1113/jphysiol.1968.sp008605. View

Mendivil-Perez M, Soto-Mercado V, Guerra-Librero A, Fernandez-Gil B, Florido J, Shen Y . Melatonin enhances neural stem cell differentiation and engraftment by increasing mitochondrial function. J Pineal Res. 2017; 63(2). DOI: 10.1111/jpi.12415. View

Tan D, Manchester L, Fuentes-Broto L, Paredes S, Reiter R . Significance and application of melatonin in the regulation of brown adipose tissue metabolism: relation to human obesity. Obes Rev. 2010; 12(3):167-88. DOI: 10.1111/j.1467-789X.2010.00756.x. View

Dasgupta B, Chhipa R . Evolving Lessons on the Complex Role of AMPK in Normal Physiology and Cancer. Trends Pharmacol Sci. 2015; 37(3):192-206. PMC: 4764394. DOI: 10.1016/j.tips.2015.11.007. View

Kajimura S, Seale P, Tomaru T, Erdjument-Bromage H, Cooper M, Ruas J . Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 2008; 22(10):1397-409. PMC: 2377193. DOI: 10.1101/gad.1666108. View

Jiang T, Xia C, Chen X, Hu Y, Wang Y, Wu J . Melatonin promotes the BMP9-induced osteogenic differentiation of mesenchymal stem cells by activating the AMPK/β-catenin signalling pathway. Stem Cell Res Ther. 2019; 10(1):408. PMC: 6925474. DOI: 10.1186/s13287-019-1511-7. View

Desjardins E, Steinberg G . Emerging Role of AMPK in Brown and Beige Adipose Tissue (BAT): Implications for Obesity, Insulin Resistance, and Type 2 Diabetes. Curr Diab Rep. 2018; 18(10):80. DOI: 10.1007/s11892-018-1049-6. View

10.

Mulligan J, Gonzalez A, Stewart A, Carey H, Saupe K . Upregulation of AMPK during cold exposure occurs via distinct mechanisms in brown and white adipose tissue of the mouse. J Physiol. 2007; 580(Pt. 2):677-84. PMC: 2075554. DOI: 10.1113/jphysiol.2007.128652. View

11.

Inagaki T, Sakai J, Kajimura S . Transcriptional and epigenetic control of brown and beige adipose cell fate and function. Nat Rev Mol Cell Biol. 2016; 17(8):480-95. PMC: 4956538. DOI: 10.1038/nrm.2016.62. View

12.

Zaminy A, Kashani I, Barbarestani M, Hedayatpour A, Mahmoudi R, Vardasbi S . Effects of melatonin on the proliferation and differentiation of rat adipose-derived stem cells. Indian J Plast Surg. 2009; 41(1):8-14. PMC: 2739564. DOI: 10.1055/s-0039-1699220. View

13.

Brougham B, Weaver A, Swinbourne A, Lewis Baida B, Kelly J, Walker S . Maternal Supplementation with Dietary Betaine during Gestation to Improve Twin Lamb Survival. Animals (Basel). 2020; 10(10). PMC: 7601746. DOI: 10.3390/ani10101749. View

14.

Cao Y, Liu X, Zhao J, Du M . AMPKα1 regulates Idh2 transcription through H2B O-GlcNAcylation during brown adipogenesis. Acta Biochim Biophys Sin (Shanghai). 2020; 53(1):112-118. DOI: 10.1093/abbs/gmaa136. View

15.

Jung-Hynes B, Schmit T, Reagan-Shaw S, Siddiqui I, Mukhtar H, Ahmad N . Melatonin, a novel Sirt1 inhibitor, imparts antiproliferative effects against prostate cancer in vitro in culture and in vivo in TRAMP model. J Pineal Res. 2010; 50(2):140-9. PMC: 3052633. DOI: 10.1111/j.1600-079X.2010.00823.x. View

16.

Dong P, Zhang C, Parker B, You L, Mathey-Prevot B . Cyclin D/CDK4/6 activity controls G1 length in mammalian cells. PLoS One. 2018; 13(1):e0185637. PMC: 5757913. DOI: 10.1371/journal.pone.0185637. View

17.

Ma X, Hou Y, Dahanayaka S, Satterfield M, Burghardt R, Bazer F . Technical note: Isolation and characterization of ovine brown adipocyte precursor cells. J Anim Sci. 2015; 93(5):2094-9. DOI: 10.2527/jas.2014-8728. View

18.

Torres-Farfan C, Valenzuela F, Mondaca M, Valenzuela G, Krause B, Herrera E . Evidence of a role for melatonin in fetal sheep physiology: direct actions of melatonin on fetal cerebral artery, brown adipose tissue and adrenal gland. J Physiol. 2008; 586(16):4017-27. PMC: 2538916. DOI: 10.1113/jphysiol.2008.154351. View

19.

Saely C, Geiger K, Drexel H . Brown versus white adipose tissue: a mini-review. Gerontology. 2010; 58(1):15-23. DOI: 10.1159/000321319. View

20.

Cardinali D, Vigo D . Melatonin, mitochondria, and the metabolic syndrome. Cell Mol Life Sci. 2017; 74(21):3941-3954. PMC: 11107716. DOI: 10.1007/s00018-017-2611-0. View