Abstract
Adipocyte browning is a potential strategy to treat obesity. Although uncoupling protein 1 (UCP1) plays an important role in browning and thermogenesis in mammals, it is not known for zebrafish. We found that cold stress, as an efficient way of inducing browning in mammals, failed to induce adipocyte browning in zebrafish, evidenced by the cell morphology and expression of browning genes. Other potential approaches including heat stress and treatment with a chemical known to induce adipocyte browning in mammals also failed to induce browning, suggesting that zebrafish may not be a suitable model to study the browning process. Interestingly however, we found that the liver expresses ucp1 much higher than the adipose tissue in zebrafish. Moreover, the expression of ucp1 in the zebrafish liver is positively regulated by the ambient temperature. These findings suggest that the role of ucp1 in zebrafish may be different from its established role in adipocyte browning in mammals but instead be evolved to adapt to environmental temperature.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Blüher M (2019) Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol 15:288–298. https://doi.org/10.1038/s41574-019-0176-8
Busiello RA, Savarese S, Lombardi A (2015) Mitochondrial uncoupling proteins and energy metabolism. Front Physiol 6:36. https://doi.org/10.3389/fphys.2015.00036
Chu D-T, Gawronska-Kozak B (2017) Brown and brite adipocytes: same function, but different origin and response. Biochimie 138:102–105. https://doi.org/10.1016/j.biochi.2017.04.017
Elemans LMH, Cervera IP, Riley SE, Wafer R, Fong R, Tandon P, Minchin JEN (2019) Quantitative analyses of adiposity dynamics in zebrafish. Adipocyte 8:330–338. https://doi.org/10.1080/21623945.2019.1648175
Flynn EJ, Trent CM, Rawls JF (2009) Ontogeny and nutritional control of adipogenesis in zebrafish (Danio rerio). J Lipid Res 50:1641–1652. https://doi.org/10.1194/jlr.M800590-JLR200
Garcia RA, Roemmich JN, Claycombe KJ (2016) Evaluation of markers of beige adipocytes in white adipose tissue of the mouse. Nutr Metab 13:24. https://doi.org/10.1186/s12986-016-0081-2
Gut P, Reischauer S, Stainier DYR, Arnaout R (2017) Little fish, big data: zebrafish as a model for cardiovascular and metabolic disease. Physiol Rev 97:889–938. https://doi.org/10.1152/physrev.00038.2016
Han X, Guo J, You Y, Yin M, Liang J, Ren C, Zhan J, Huang W (2018) Vanillic acid activates thermogenesis in brown and white adipose tissue. Food Funct 9:4366–4375. https://doi.org/10.1039/c8fo00978c
Ikeda K, Yamada T (2020) UCP1 dependent and independent thermogenesis in brown and beige adipocytes. Front Endocrinol 11:498. https://doi.org/10.3389/fendo.2020.00498
Ikeda K, Maretich P, Kajimura S (2018) The common and distinct features of brown and beige adipocytes. Trends Endocrinol Metab 29:191–200. https://doi.org/10.1016/j.tem.2018.01.001
Imrie D, Sadler KC (2010) White adipose tissue development in zebrafish is regulated by both developmental time and fish size. Dev Dyn 239:3013–3023. https://doi.org/10.1002/dvdy.22443
Jastroch M, Wuertz S, Kloas W, Klingenspor M (2005) Uncoupling protein 1 in fish uncovers an ancient evolutionary history of mammalian nonshivering thermogenesis. Physiol Genomics 22:150–156. https://doi.org/10.1152/physiolgenomics.00070.2005
Jung Y, Park J, Kim H-L, Sim J-E, Youn D-H, Kang J, Lim S, Jeong M-Y, Yang WM, Lee S-G, Ahn KS, Um J-Y (2018) Vanillic acid attenuates obesity via activation of the AMPK pathway and thermogenic factors in vivo and in vitro. FASEB J 32:1388–1402. https://doi.org/10.1096/fj.201700231RR
Kajimura S, Seale P, Tomaru T, Erdjument-Bromage H, Cooper MP, Ruas JL, Chin S, Tempst P, Lazar MA, Spiegelman BM (2008) Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev 22:1397–1409. https://doi.org/10.1101/gad.1666108
Kim Y-I, Nam I-K, Lee D-K, Bhandari S, Charton L, Kwak S, Lim J-Y, Hong K, Kim S-J, Lee JN, Kwon SW, So H-S, Linka N, Park R, Choe S-K (2020) Slc25a17 acts as a peroxisomal coenzyme A transporter and regulates multiorgan development in zebrafish. J Cell Physiol 235:151–165. https://doi.org/10.1002/jcp.28954
Kushner RF (2018) Weight loss strategies for treatment of obesity: lifestyle management and pharmacotherapy. Prog Cardiovasc Dis 61:246–252. https://doi.org/10.1016/j.pcad.2018.06.001
Lizcano F (2019) The beige adipocyte as a therapy for metabolic diseases. Int J Mol Sci. https://doi.org/10.3390/ijms20205058
Minchin JEN, Rawls JF (2017) A classification system for zebrafish adipose tissues. Dis Model Mech 10:797–809. https://doi.org/10.1242/dmm.025759
Vargas-Castillo A, Fuentes-Romero R, Rodriguez-Lopez LA, Torres N, Tovar AR (2017) Understanding the biology of thermogenic fat: Is browning a new approach to the treatment of obesity? Arch Med Res 48:401–413. https://doi.org/10.1016/j.arcmed.2017.10.002
Westerfield M (2007) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio), 5th edn. University of Oregon Press, Eugene
Zang L, Maddison LA, Chen W (2018) Zebrafish as a model for obesity and diabetes. Front Cell Dev Biol 6:91. https://doi.org/10.3389/fcell.2018.00091
Acknowledgements
This study was supported by the Grant: NRF-2018R1D1A1B07050552 to S.K.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethical statement
Zebrafish experiment was approved by the committee for ethics in animal experiments of the Wonkwang University (WKU15-151) and carried out according to the guidelines for animal experiments.
Conflict of interest
Yousheng Mao has no conflict of interest. KwangHeum Hong has no conflict of interest. Sushil Bhandari has no conflict of interest. Li Li has no conflict of interest. Weifang Liao has no conflict of interest. SeongJin Kim has no conflict of interest. Yinyi Xiong has no conflict of interest. In‑Koo Nam has no conflict of interest. Seong‑Kyu Choe has no conflict of interest. SeongAe Kwak has no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mao, Y., Hong, K., Bhandari, S. et al. Ambient temperature regulates uncoupling protein 1 expression but fails to induce adipocyte browning in zebrafish. ADV TRADIT MED (ADTM) 21, 379–387 (2021). https://doi.org/10.1007/s13596-021-00580-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13596-021-00580-9