Journal of Nutrition and Health

  • 제57권2호
  • /
  • Pages.171-184
  • /
  • 2024
  • /
  • 2288-3886(pISSN)
  • /
  • 2288-3959(eISSN)
한국영양학회 (The Korean Nutrition Society)
권호 표지
DOI QR코드

DOI QR Code

High-fat diet alters the thermogenic gene expression to β-agonists or 18-carbon fatty acids in adipocytes derived from the white and brown adipose tissue of mice

  • Seonjeong Park (Department of Food and Nutrition, Seoul Women's University) ;
  • Seung A Ock (Department of Food and Nutrition, Seoul Women's University) ;
  • Yun Jeong Park (Department of Food and Nutrition, Seoul Women's University) ;
  • Yoo-Hyun Lee (Department of Food and Nutrition, The University of Suwon) ;
  • Chan Yoon Park (Department of Food and Nutrition, The University of Suwon) ;
  • Sunhye Shin (Department of Food and Nutrition, Seoul Women's University)
  • 투고 : 2023.11.25
  • 심사 : 2024.03.18
  • 발행 : 2024.04.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Purpose: Although activating thermogenic adipocytes is a promising strategy to reduce the risk of obesity and related metabolic disorders, emerging evidence suggests that it is difficult to induce adipocyte thermogenesis in obesity. Therefore, this study aimed to investigate the regulation of adipocyte thermogenesis in diet-induced obesity. Methods: Adipose progenitor cells were isolated from the white and brown adipose tissues of control diet (CD) or high-fat diet (HFD) fed mice, and fully differentiated white and brown adipocytes were treated with β-agonists or 18-carbon fatty acids for β-adrenergic activation or peroxisome proliferator-activated receptor (PPAR) activation. Results: Compared to the CD-fed mice, the expression of uncoupling protein 1 (Ucp1) was lower in the white adipose tissue of the HFD-fed mice; however, this was not observed in the brown adipose tissue. The expression of peroxisome proliferator-activated receptor gamma (Pparg) was lower in the brown adipose progenitor cells isolated from HFD-fed mice than in those isolated from the CD-fed mice. Norepinephrine (NE) treatment exerted lesser effect on peroxisome proliferator-activated receptor-γ coactivator (Pgc1a) upregulation in white adipocytes derived from HFD-fed mice than those derived from CD-fed mice. Regardless which 18-carbon fatty acids were treated, the expression levels of thermogenic genes including Ucp1, Pgc1a, and positive regulatory domain zinc finger region protein 16 (Prdm16) were higher in the white adipocytes derived from HFD-fed mice. Oleic acid (OLA) and γ-linolenic acid (GLA) upregulated Pgc1a expression in white adipocytes derived from HFD-fed mice. Brown adipocytes derived from HFD-fed mice had higher expression levels of Pgc1a and Prdm16 compared to their counterparts. Conclusion: These results indicate that diet-induced obesity may downregulate brown adipogenesis and NE-induced thermogenesis in white adipocytes. Also, HFD feeding may induce thermogenic gene expression in white and brown primary adipocytes, and OLA and GLA could augment the expression levels.

키워드

과제정보

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2021R1G1A1092356).

참고문헌

  1. Harms M, Seale P. Brown and beige fat: development, function and therapeutic potential. Nat Med 2013; 19(10): 1252-1263. https://doi.org/10.1038/nm.3361
  2. Park J, Shin S, Liu L, Jahan I, Ong SG, Xu P, et al. Progenitor-like characteristics in a subgroup of UCP1+ cells within white adipose tissue. Dev Cell 2021; 56(7): 985-999.e4. https://doi.org/10.1016/j.devcel.2021.02.018
  3. Wu R, Park J, Qian Y, Shi Z, Hu R, Yuan Y, et al. Genetically prolonged beige fat in male mice confers long-lasting metabolic health. Nat Commun 2023; 14(1): 2731.
  4. Perez LM, Bernal A, de Lucas B, San Martin N, Mastrangelo A, Garcia A, et al. Altered metabolic and stemness capacity of adipose tissue-derived stem cells from obese mouse and human. PLoS One 2015; 10(4): e0123397.
  5. Shin S, El-Sabbagh AS, Lukas BE, Tanneberger SJ, Jiang Y. Adipose stem cells in obesity: challenges and opportunities. Biosci Rep 2020; 40(6): BSR20194076.
  6. Yuan Y, Shin S, Shi Z, Shu G, Jiang Y. Postnatal tamoxifen exposure induces long-lasting changes to adipose tissue in adult mice. Mol Biotechnol. Forthcoming 2023.
  7. Matsuo T, Takeuchi H, Suzuki H, Suzuki M. Body fat accumulation is greater in rats fed a beef tallow diet than in rats fed a safflower or soybean oil diet. Asia Pac J Clin Nutr 2002; 11(4): 302-308. https://doi.org/10.1046/j.1440-6047.2002.00299.x
  8. Takahashi Y, Ide T, Fujita H. Dietary gamma-linolenic acid in the form of borage oil causes less body fat accumulation accompanying an increase in uncoupling protein 1 mRNA level in brown adipose tissue. Comp Biochem Physiol B Biochem Mol Biol 2000; 127(2): 213-222. https://doi.org/10.1016/S0305-0491(00)00254-6
  9. Shin S, Ajuwon KM. Divergent response of murine and porcine adipocytes to stimulation of browning genes by 18-carbon polyunsaturated fatty acids and beta-receptor agonists. Lipids 2018; 53(1): 65-75.  https://doi.org/10.1002/lipd.12010
  10. Shin S, Ajuwon KM. Effects of diets differing in composition of 18-c fatty acids on adipose tissue thermogenic gene expression in mice fed high-fat diets. Nutrients 2018; 10(2): 256.
  11. Massiera F, Saint-Marc P, Seydoux J, Murata T, Kobayashi T, Narumiya S, et al. Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern? J Lipid Res 2003; 44(2): 271-279. https://doi.org/10.1194/jlr.M200346-JLR200
  12. Shin S. Regulation of adipose tissue biology by long-chain fatty acids: metabolic effects and molecular mechanisms. J Obes Metab Syndr 2022; 31(2): 147-160. https://doi.org/10.7570/jomes22014
  13. Wijers SL, Saris WH, van Marken Lichtenbelt WD. Cold-induced adaptive thermogenesis in lean and obese. Obesity (Silver Spring) 2010; 18(6): 1092-1099. https://doi.org/10.1038/oby.2010.74
  14. Louwen F, Ritter A, Kreis NN, Yuan J. Insight into the development of obesity: functional alterations of adipose-derived mesenchymal stem cells. Obes Rev 2018; 19(7): 888-904. https://doi.org/10.1111/obr.12679
  15. Lumeng CN, Bodzin JL, Saltiel AR. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J Clin Invest 2007; 117(1): 175-184. https://doi.org/10.1172/JCI29881
  16. Lee YH, Petkova AP, Mottillo EP, Granneman JG. In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high-fat feeding. Cell Metab 2012; 15(4): 480-491. https://doi.org/10.1016/j.cmet.2012.03.009
  17. Wu MV, Bikopoulos G, Hung S, Ceddia RB. Thermogenic capacity is antagonistically regulated in classical brown and white subcutaneous fat depots by high fat diet and endurance training in rats: impact on whole-body energy expenditure. J Biol Chem 2014; 289(49): 34129-34140. https://doi.org/10.1074/jbc.M114.591008
  18. Gregoire FM. Adipocyte differentiation: from fibroblast to endocrine cell. Exp Biol Med (Maywood) 2001; 226(11): 997-1002. https://doi.org/10.1177/153537020122601106
  19. Park S, Shin S, Lim Y, Shin JH, Seong JK, Han SN. Korean pine nut oil attenuated hepatic triacylglycerol accumulation in high-fat diet-induced obese mice. Nutrients 2016; 8(1): 59.
  20. Shin S, Ajuwon KM. Lipopolysaccharide alters thermogenic and inflammatory genes in white adipose tissue in mice fed diets with distinct 18-carbon fatty-acid composition. Lipids 2018; 53(9): 885-896. https://doi.org/10.1002/lipd.12101
  21. Xu X, Ying Z, Cai M, Xu Z, Li Y, Jiang SY, et al. Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue. Am J Physiol Regul Integr Comp Physiol 2011; 300(5): R1115-R1125. https://doi.org/10.1152/ajpregu.00806.2010
  22. Carpene C, Galitzky J, Collon P, Esclapez F, Dauzats M, Lafontan M. Desensitization of beta-1 and beta-2, but not beta-3, adrenoceptor-mediated lipolytic responses of adipocytes after long-term norepinephrine infusion. J Pharmacol Exp Ther 1993; 265(1): 237-247.
  23. Rubio A, Raasmaja A, Silva JE. Thyroid hormone and norepinephrine signaling in brown adipose tissue. II: differential effects of thyroid hormone on beta 3-adrenergic receptors in brown and white adipose tissue. Endocrinology 1995; 136(8): 3277-3284. https://doi.org/10.1210/endo.136.8.7628361
  24. Bakopanos E, Silva JE. Thiazolidinediones inhibit the expression of beta3-adrenergic receptors at a transcriptional level. Diabetes 2000; 49(12): 2108-2115. https://doi.org/10.2337/diabetes.49.12.2108
  25. Seale P, Kajimura S, Spiegelman BM. Transcriptional control of brown adipocyte development and physiological function--of mice and men. Genes Dev 2009; 23(7): 788-797. https://doi.org/10.1101/gad.1779209
  26. Kajimura S, Seale P, Spiegelman BM. Transcriptional control of brown fat development. Cell Metab 2010; 11(4): 257-262. https://doi.org/10.1016/j.cmet.2010.03.005
  27. Wang B, Kong Q, Li X, Zhao J, Zhang H, Chen W, et al. A high-fat diet increases gut microbiota biodiversity and energy expenditure due to nutrient difference. Nutrients 2020; 12(10): 3197.
  28. Zhang G, Sun Q, Liu C. Influencing factors of thermogenic adipose tissue activity. Front Physiol 2016; 7: 29.
  29. Laiglesia LM, Lorente-Cebrian S, Prieto-Hontoria PL, Fernandez-Galilea M, Ribeiro SM, Sainz N, et al. Eicosapentaenoic acid promotes mitochondrial biogenesis and beige-like features in subcutaneous adipocytes from overweight subjects. J Nutr Biochem 2016; 37: 76-82. https://doi.org/10.1016/j.jnutbio.2016.07.019
  30. Zhao M, Chen X. Eicosapentaenoic acid promotes thermogenic and fatty acid storage capacity in mouse subcutaneous adipocytes. Biochem Biophys Res Commun 2014; 450(4): 1446-1451. https://doi.org/10.1016/j.bbrc.2014.07.010
  31. Kim J, Okla M, Erickson A, Carr T, Natarajan SK, Chung S. Eicosapentaenoic acid potentiates brown thermogenesis through FFAR4-dependent up-regulation of miR-30b and miR-378. J Biol Chem 2016; 291(39): 20551-20562. https://doi.org/10.1074/jbc.M116.721480
  32. Kim M, Goto T, Yu R, Uchida K, Tominaga M, Kano Y, et al. Fish oil intake induces UCP1 upregulation in brown and white adipose tissue via the sympathetic nervous system. Sci Rep 2015; 5(1): 18013. 
  33. Hwang DH, Kim JA, Lee JY. Mechanisms for the activation of Toll-like receptor 2/4 by saturated fatty acids and inhibition by docosahexaenoic acid. Eur J Pharmacol 2016; 785: 24-35. https://doi.org/10.1016/j.ejphar.2016.04.024
  34. Calder PC. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr 2006; 83(6 Suppl): 1505S-1519S. https://doi.org/10.1093/ajcn/83.6.1505S
  35. Sharma P, Agnihotri N. Fish oil and corn oil induced differential effect on beiging of visceral and subcutaneous white adipose tissue in high-fat-diet-induced obesity. J Nutr Biochem 2020; 84: 108458.
  36. Lim JH, Gerhart-Hines Z, Dominy JE, Lee Y, Kim S, Tabata M, et al. Oleic acid stimulates complete oxidation of fatty acids through protein kinase A-dependent activation of SIRT1-PGC1α complex. J Biol Chem 2013; 288(10): 7117-7126. https://doi.org/10.1074/jbc.M112.415729
  37. Shin S, Ajuwon KM. Effect of lipopolysaccharide on peripheral tissue and hypothalamic expression of metabolic and inflammatory markers in mice fed high-fat diets with distinct 18-carbon fatty acid composition. Lipids 2021; 56(5): 509-519. https://doi.org/10.1002/lipd.12318
  38. Rodriguez VM, Portillo MP, Pico C, Macarulla MT, Palou A. Olive oil feeding up-regulates uncoupling protein genes in rat brown adipose tissue and skeletal muscle. Am J Clin Nutr 2002; 75(2): 213-220. https://doi.org/10.1093/ajcn/75.2.213
  39. Jones PJ, Jew S, AbuMweis S. The effect of dietary oleic, linoleic, and linolenic acids on fat oxidation and energy expenditure in healthy men. Metabolism 2008; 57(9): 1198-1203. https://doi.org/10.1016/j.metabol.2008.04.012
  40. Maurer SF, Dieckmann S, Lund J, Fromme T, Hess AL, Colson C, et al. No effect of dietary fish oil supplementation on the recruitment of brown and brite adipocytes in mice or humans under thermoneutral conditions. Mol Nutr Food Res 2021; 65(2): e2000681.
  41. Keller H, Dreyer C, Medin J, Mahfoudi A, Ozato K, Wahli W. Fatty acids and retinoids control lipid metabolism through activation of peroxisome proliferator-activated receptor-retinoid X receptor heterodimers. Proc Natl Acad Sci U S A 1993; 90(6): 2160-2164. https://doi.org/10.1073/pnas.90.6.2160
  42. Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, et al. Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc Natl Acad Sci U S A 1997; 94(9): 4318-4323. https://doi.org/10.1073/pnas.94.9.4318
  43. Kim KN, Yao Y, Ju SY. Short chain fatty acids and fecal microbiota abundance in humans with obesity: a systematic review and meta-analysis. Nutrients 2019; 11(10): 2512.
  44. Eslick S, Thompson C, Berthon B, Wood L. Short-chain fatty acids as anti-inflammatory agents in overweight and obesity: a systematic review and meta-analysis. Nutr Rev 2022; 80(4): 838-856. https://doi.org/10.1093/nutrit/nuab059