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Amino Acids

, Volume 51, Issue 2, pp 245–254 | Cite as

Anti-obesity effect of taurine through inhibition of adipogenesis in white fat tissue but not in brown fat tissue in a high-fat diet-induced obese mouse model

  • Kyoung Soo KimEmail author
  • Min Ju Jang
  • Sungsoon Fang
  • Seul Gi Yoon
  • Il Yong Kim
  • Je Kyung Seong
  • Hyung-In Yang
  • Dae Hyun HahmEmail author
Original Article

Abstract

This study was conducted to evaluate the anti-obesity effects of long-term taurine supplementation in a mild obese ICR mouse model and to study the mechanism by which taurine induces weight loss. Three groups of male ICR mice were fed a normal chow diet, a high-fat diet (HFD), or an HFD supplemented with 2% taurine in drinking water for 28 weeks. Body weight was measured every week. Metabolic, behavioral, and physiological monitoring were carried out using PhenoMaster at 28 weeks. Interscapular brown fat (BAT), inguinal white fat tissue (WAT), and quadriceps muscle were analyzed and compared to assess the change of gene expression related to adipogenesis. Taurine supplementation showed the trend of anti-obesity effect in ICR mice fed an HFD for 28 weeks. HFD-fed mice did not show significant difference of oxygen consumption (VO2), energy expenditure (EE), respiratory exchange rate (RER), and locomotive activity compared with those of normal chow diet fed mice. The expression of adipogenesis-related genes such as PPAR-α, PPAR-γ, C/EBP-α, C/EBP-β, and AP2 increased in BAT and WAT, but not in muscle tissue. Taurine supplementation showed the downregulation of these genes in WAT but not in BAT or muscle. Consistently, the expression of taurine transporter (TauT) and adipocyte-specific genes such as adiponectin, leptin, and IL-6 was regulated in a similar pattern by taurine supplementation. Long-term taurine supplementation causes weight loss, most likely by inhibiting adipogenesis in WAT. TauT expression may be involved in the expression of various genes regulated by taurine supplementation.

Keywords

Taurine Taurine transporter Adipogenesis White adipose tissue Brown adipose tissue 

Notes

Acknowledgements

The authors thank Dr. Kang Jong-Sun at Sungkyunkwan University School of Medicine for critical reading and comments.

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), which is funded by the Ministry of Education, Science, and Technology (Grant number 2017R1D1AB03031409). This research was partly supported by the Korea Mouse Phenotyping Project (2013M3A9D5072550) of the Ministry of Science, ICT, and Future Planning through the National Research Foundation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts.

Research involving human participants and/or animals

All animal protocols were approved by the Committee on Animals of Kyung Hee University Hospital at GANGDONG (KHNMC AP 2016-009). There are no human participants.

Informed consent

Human tissues and sera were never used in this study. No informed consent is required.

Supplementary material

726_2018_2659_MOESM1_ESM.pptx (61 kb)
Supplementary material 1 Comparison of levels of glucose and lipid of Normal, HFD and HFD (2% taurine drinking water)-fed mice (n = 10). As described in Methods, after sacrifice at 28 weeks, the blood levels of glucose, total triglyceride, total cholesterol, and high-density lipoproteins cholesterol (HDL-C) were measured by automated clinical chemistry analyzer, FUJI DRI-CHEM NX500 (FUJIFILM, Japan). Differences between three groups were analyzed using the nonparametric Kruskal–Wallis test (PPTX 60 kb)

References

  1. Albrecht J, Schousboe A (2005) Taurine interaction with neurotransmitter receptors in the CNS: an update. Neurochem Res 30(12):1615–1621.  https://doi.org/10.1007/s11064-005-8986-6 PubMedCrossRefGoogle Scholar
  2. Batista TM, Ribeiro RA, da Silva PM, Camargo RL, Lollo PC, Boschero AC, Carneiro EM (2013) Taurine supplementation improves liver glucose control in normal protein and malnourished mice fed a high-fat diet. Mol Nutr Food Res 57(3):423–434.  https://doi.org/10.1002/mnfr.201200345 PubMedCrossRefGoogle Scholar
  3. Borck PC, Vettorazzi JF, Branco RCS, Batista TM, Santos-Silva JC, Nakanishi VY, Boschero AC, Ribeiro RA, Carneiro EM (2018) Taurine supplementation induces long-term beneficial effects on glucose homeostasis in ob/ob mice. Amino Acids 50(6):765–774.  https://doi.org/10.1007/s00726-018-2553-3 PubMedCrossRefGoogle Scholar
  4. Cao PJ, Jin YJ, Li ME, Zhou R, Yang MZ (2016) PGC-1alpha may associated with the anti-obesity effect of taurine on rats induced by arcuate nucleus lesion. Nutr Neurosci 19(2):86–93.  https://doi.org/10.1179/1476830514Y.0000000153 PubMedCrossRefGoogle Scholar
  5. Du H, You JS, Zhao X, Park JY, Kim SH, Chang KJ (2010) Antiobesity and hypolipidemic effects of lotus leaf hot water extract with taurine supplementation in rats fed a high fat diet. J Biomed Sci 17(Suppl 1):S42.  https://doi.org/10.1186/1423-0127-17-S1-S42 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:11CrossRefGoogle Scholar
  7. Ide T, Kushiro M, Takahashi Y, Shinohara K, Cha S (2002) mRNA expression of enzymes involved in taurine biosynthesis in rat adipose tissues. Metabolism 51(9):1191–1197PubMedCrossRefGoogle Scholar
  8. Kim KS, Oh DH, Kim JY, Lee BG, You JS, Chang KJ, Chung HJ, Yoo MC, Yang HI, Kang JH, Hwang YC, Ahn KJ, Chung HY, Jeong IK (2012) Taurine ameliorates hyperglycemia and dyslipidemia by reducing insulin resistance and leptin level in Otsuka Long-Evans Tokushima fatty (OLETF) rats with long-term diabetes. Exp Mol Med 44(11):665–673.  https://doi.org/10.3858/emm.2012.44.11.075 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Kim KS, Ji HI, Chung H, Kim C, Lee SH, Lee YA, Yang HI, Yoo MC, Hong SJ (2013) Taurine chloramine modulates the expression of adipokines through inhibition of the STAT-3 signaling pathway in differentiated human adipocytes. Amino Acids 45(6):1415–1422.  https://doi.org/10.1007/s00726-013-1612-z PubMedCrossRefGoogle Scholar
  10. Lambert IH, Kristensen DM, Holm JB, Mortensen OH (2015) Physiological role of taurine–from organism to organelle. Acta Physiol (Oxf) 213(1):191–212.  https://doi.org/10.1111/apha.12365 CrossRefGoogle Scholar
  11. Lifshitz F, Lifshitz JZ (2014) Globesity: the root causes of the obesity epidemic in the USA and now worldwide. Pediatr Endocrinol Rev 12(1):17–34PubMedGoogle Scholar
  12. Lin S, Hirai S, Yamaguchi Y, Goto T, Takahashi N, Tani F, Mutoh C, Sakurai T, Murakami S, Yu R, Kawada T (2013) Taurine improves obesity-induced inflammatory responses and modulates the unbalanced phenotype of adipose tissue macrophages. Mol Nutr Food Res 57(12):2155–2165.  https://doi.org/10.1002/mnfr.201300150 PubMedCrossRefGoogle Scholar
  13. Murakami S (2017) The physiological and pathophysiological roles of taurine in adipose tissue in relation to obesity. Life Sci 186:80–86.  https://doi.org/10.1016/j.lfs.2017.08.008 PubMedCrossRefGoogle Scholar
  14. Murakami S, Kondo Y, Nagate T (2000) Effects of long-term treatment with taurine in mice fed a high-fat diet: improvement in cholesterol metabolism and vascular lipid accumulation by taurine. Adv Exp Med Biol 483:177–186.  https://doi.org/10.1007/0-306-46838-7_19 PubMedCrossRefGoogle Scholar
  15. Murakami S, Fujita M, Nakamura M, Sakono M, Nishizono S, Sato M, Imaizumi K, Mori M, Fukuda N (2016) Taurine ameliorates cholesterol metabolism by stimulating bile acid production in high-cholesterol-fed rats. Clin Exp Pharmacol Physiol 43(3):372–378.  https://doi.org/10.1111/1440-1681.12534 PubMedCrossRefGoogle Scholar
  16. Ribeiro RA, Santos-Silva JC, Vettorazzi JF, Cotrim BB, Mobiolli DD, Boschero AC, Carneiro EM (2012) Taurine supplementation prevents morpho-physiological alterations in high-fat diet mice pancreatic beta-cells. Amino Acids 43(4):1791–1801.  https://doi.org/10.1007/s00726-012-1263-5 PubMedCrossRefGoogle Scholar
  17. Rosa FT, Freitas EC, Deminice R, Jordao AA, Marchini JS (2014) Oxidative stress and inflammation in obesity after taurine supplementation: a double-blind, placebo-controlled study. Eur J Nutr 53(3):823–830.  https://doi.org/10.1007/s00394-013-0586-7 PubMedCrossRefGoogle Scholar
  18. Sagara M, Murakami S, Mizushima S, Liu L, Mori M, Ikeda K, Nara Y, Yamori Y (2015) Taurine in 24-h urine samples is inversely related to cardiovascular risks of middle aged subjects in 50 populations of the world. Adv Exp Med Biol 803:623–636.  https://doi.org/10.1007/978-3-319-15126-7_50 PubMedCrossRefGoogle Scholar
  19. Schuller-Levis GB, Park E (2004) Taurine and its chloramine: modulators of immunity. Neurochem Res 29(1):117–126PubMedCrossRefGoogle Scholar
  20. Speakman J, Hambly C, Mitchell S, Krol E (2007) Animal models of obesity. Obes Rev 8(Suppl 1):55–61.  https://doi.org/10.1111/j.1467-789X.2007.00319.x PubMedCrossRefGoogle Scholar
  21. Tsuboyama-Kasaoka N, Shozawa C, Sano K, Kamei Y, Kasaoka S, Hosokawa Y, Ezaki O (2006) Taurine (2-aminoethanesulfonic acid) deficiency creates a vicious circle promoting obesity. Endocrinology 147(7):3276–3284.  https://doi.org/10.1210/en.2005-1007 PubMedCrossRefGoogle Scholar
  22. Ueki I, Stipanuk MH (2009) 3T3-L1 adipocytes and rat adipose tissue have a high capacity for taurine synthesis by the cysteine dioxygenase/cysteinesulfinate decarboxylase and cysteamine dioxygenase pathways. J Nutr 139(2):207–214.  https://doi.org/10.3945/jn.108.099085 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Yamori Y, Liu L, Ikeda K, Miura A, Mizushima S, Miki T, Nara Y, Disease WH-C, Alimentary Comprarison Study G (2001) Distribution of twenty-four hour urinary taurine excretion and association with ischemic heart disease mortality in 24 populations of 16 countries: results from the WHO-CARDIAC study. Hypertens Res 24(4):453–457PubMedCrossRefGoogle Scholar
  24. Yamori Y, Taguchi T, Mori H, Mori M (2010) Low cardiovascular risks in the middle aged males and females excreting greater 24-hour urinary taurine and magnesium in 41 WHO-CARDIAC study populations in the world. J Biomed Sci 17(Suppl 1):S21.  https://doi.org/10.1186/1423-0127-17-S1-S21 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Zhuhua Z, Zhiquan W, Zhen Y, Yixin N, Weiwei Z, Xiaoyong L, Yueming L, Hongmei Z, Li Q, Qing S (2015) A novel mice model of metabolic syndrome: the high-fat-high-fructose diet-fed ICR mice. Exp Anim 64(4):435–442.  https://doi.org/10.1538/expanim.14-0086 PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Kyoung Soo Kim
    • 1
    • 2
    Email author
  • Min Ju Jang
    • 1
  • Sungsoon Fang
    • 3
  • Seul Gi Yoon
    • 4
  • Il Yong Kim
    • 4
  • Je Kyung Seong
    • 4
    • 5
  • Hyung-In Yang
    • 2
  • Dae Hyun Hahm
    • 6
    Email author
  1. 1.Department of Clinical Pharmacology and TherapeuticsSchool of Medicine, Kyung Hee UniversitySeoulRepublic of Korea
  2. 2.East–West Bone and Joint Disease Research InstituteKyung Hee University Hospital at GangdongSeoulRepublic of Korea
  3. 3.Severance Biomedical Science Institute Gangnam Severance Hospital BK21 PLUS Project for Medical ScienceYonsei University College of MedicineSeoulRepublic of Korea
  4. 4.Laboratory of Developmental Biology and Genomics, Research Institute for Veterinary Science, BK21 PLUS Program for Creative Veterinary Science Research, College of Veterinary Medicine, and Korea Mouse Phenotyping Center (KMPC)Seoul National UniversitySeoulRepublic of Korea
  5. 5.Interdisciplinary Program for Bioinformatics, Program for Cancer Biology and BIO-MAX/N-Bio InstituteSeoul National UniversitySeoulRepublic of Korea
  6. 6.Department of Physiology, School of MedicineKyung Hee UniversitySeoulRepublic of Korea

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