Abstract
Interventions that can modulate subcutaneous white adipose tissue (scWAT) function, such as exercise training and nutritional components, like taurine, modulate the inflammatory process, therefore, may represent strategies for obesity treatment. We investigated the effects of taurine supplementation in conjunction with exercise on inflammatory and oxidative stress markers in plasma and scWAT of obese women. Sixteen obese women were randomized into two groups: Taurine supplementation group (Tau, n = 8) and Taurine supplementation + exercise group (Tau + Exe, n = 8). The intervention was composed of daily taurine supplementation (3 g) and exercise training for 8 weeks. Anthropometry, body fat composition, and markers of inflammatory and oxidative stress were determined in plasma and scWAT biopsy samples before and after the intervention. We found that, although taurine supplementation increased taurine plasma levels, no changes were observed for the anthropometric characteristics. However, Tau alone decreased interleukin-6 (IL-6), and in conjunction with exercise (Tau + Exe), increased anti-inflammatory interleukins (IL-15 and IL10), followed by reduced IL1β gene expression in the scWAT of obese women. Tau and Tau + Exe groups presented reduced adipocyte size and increased connective tissue and multilocular droplets. In conclusion, taurine supplementation in conjunction with exercise modulated levels of inflammatory markers in plasma and scWAT, and improved scWAT plasticity in obese women, promoting protection against obesity-induced inflammation. TRN NCT04279600 retrospectively registered on August 18, 2019.
Similar content being viewed by others
Availability of data
Data may be made available from the corresponding author upon reasonable request.
References
Barbarroja N, López-Pedrera R, Mayas MD et al (2010) The obese healthy paradox: is inflammation the answer? Biochem J 430(1):141–149
Batitucci G, Terrazas SIBM, Nóbrega MP (2018) Effects of taurine supplementation in elite swimmers performance. Motriz e1018137
Batitucci G, Brandao CFC, De Carvalho FG et al (2019) Taurine supplementation increases irisin levels after high intensity physical training in obese women. Cytokine 123:154741. https://doi.org/10.1016/j.cyto.2019.154741
Brandao CFC, De Carvalho FG, Souza AO et al (2019) Physical training, UCP1 expression, mitochondrial density, and coupling in adipose tissue from women with obesity. Scand J Med Sci Sports. https://doi.org/10.1111/sms.13514
Cabral-Santos C, de Lima Junior EA, Fernandes IMDC et al (2019) Interleukin-10 responses from acute exercise in healthy subjects: a systematic review. J Cell Physiol 234(7):9956–9965. https://doi.org/10.1002/jcp.27920
Chupel MU, Minuzzi LG, Furtado G et al (2018) Exercise and taurine in inflammation, cognition, and peripheral markers of blood-brain barrier integrity in older women. Appl Physiol Nutr Metab 43(7):733–741. https://doi.org/10.1139/apnm-2017-0775
Clemente-Postigo M, Tinahones A, El Bekay R et al (2020) The role of autophagy in white adipose tissue function: implications for metabolic health. Metabolites. https://doi.org/10.3390/metabo10050179
De Carvalho FG, Sparks LM (2019) Targeting white adipose tissue with exercise or bariatric surgery as therapeutic strategies in obesity. Biology 8:1. https://doi.org/10.3390/biology8010016
De Carvalho FG, Galan BSM, Santos PC et al (2017) Taurine: a potential ergogenic aid for preventing muscle damage and protein catabolism and decreasing oxidative stress produced by endurance exercise. Front Physiol. https://doi.org/10.3389/fphys.2017.00710
De Carvalho FG, Barbieri RA, Carvalho MB et al (2018) Taurine supplementation can increase lipolysis and affect the contribution of energy systems during front crawl maximal effort. Amino Acids 50(1):189–198. https://doi.org/10.1007/s00726-017-2505-3
De Carvalho FG, Brandao CFC, Batitucci G et al (2021) Taurine supplementation associated with exercise increases mitochondrial activity and fatty acid oxidation gene expression in the subcutaneous white adipose tissue of obese women. Clin Nutr 40:2180–2187. https://doi.org/10.1016/j.clnu.2020.09.044
Deyl Z, Hyanek J, Horakova M (1986) Profiling of amino acids in body fluids and tissues by means of liquid chromatography. J Chromatogr 379:177–250
Divoux A, Moutel S, Poitou C et al (2012) Mast cells in human adipose tissue: link with morbid obesity, inflammatory status, and diabetes. J Clin Endocrinol Metab 97(9):E1677-1685. https://doi.org/10.1210/jc.2012-1532
Fett CA, Fett WC, Marchini JS (2009) Circuit weight training vs jogging in metabolic risk factors of overweight/obese women. Arq Bras Cardiol 93(5):519–525
Gamas L, Matafome P, Seiça R (2015) Irisin and myonectin regulation in the insulin resistant muscle: implications to adipose tissue: muscle crosstalk. J Diabetes Res 2015:359159. https://doi.org/10.1155/2015/359159
Goodpaster BH, Sparks LM (2017) Metabolic flexibility in health and disease. Cell Metab 25(5):1027–1036. https://doi.org/10.1016/j.cmet.2017.04.015
Greenberg AS, Obin MS (2006) Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr 83(2):461S-465S. https://doi.org/10.1093/ajcn/83.2.461S
Guo YY, Li BY, Peng WQ et al (2019) Taurine-mediated browning of white adipose tissue is involved in its anti-obesity effect in mice. J Biol Chem 294(41):15014–15024. https://doi.org/10.1074/jbc.RA119.009936
Gutteridge JM (1976) Superoxide dismutase (erythrocuprein) and free radicals in clinical chemistry. Ann Clin Biochem 13(3):393–398. https://doi.org/10.1177/000456327601300125
Ide T, Kushiro M, Takahashi Y et al (2002) mRNA expression of enzymes involved in taurine biosynthesis in rat adipose tissues. Metabolism 51(9):1191–1197. https://doi.org/10.1053/meta.2002.34036
Jacobsen JG, Smith LH (1968) Biochemistry and physiology of taurine and taurine derivatives. Physiol Rev 48:424–511
Jang SH, Paik IY, Ryu JH et al (2019) Effects of aerobic and resistance exercises on circulating apelin-12 and apelin-36 concentrations in obese middle-aged women: a randomized controlled trial. BMC Womens Health 19(1):23. https://doi.org/10.1186/s12905-019-0722-5
Jeevanandam M, Ramias L, Schiller WR (1991) Altered plasma free amino acid levels in obese traumatized man. Metabolism 40(4):385–390. https://doi.org/10.1016/0026-0495(91)90149-q
Jensen MD (2002) Adipose tissue and fatty acid metabolism in humans. J R Soc Med 95(42):3–7
Jin CH, Rhyu HS, Kim JY (2018) The effects of combined aerobic and resistance training on inflammatory markers in obese men. J Exerc Rehabil 14(4):660–665. https://doi.org/10.12965/jer.1836294.147
Kim SJ, Gupta RC, Lee HW (2007) Taurine-diabetes interaction: from involvement to protection. Curr Diabetes Rev 3(3):165–175
Kim JW, Ko YC, Seo TB et al (2018) Effect of circuit training on body composition, physical fitness, and metabolic syndrome risk factors in obese female college students. J Exerc Rehabil 14(3):460–465. https://doi.org/10.12965/jer.1836194.097
Kim KS, Jang MJ, Fang S et al (2019) 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. Amino Acids 51(2):245–254. https://doi.org/10.1007/s00726-018-2659-7
Kuipers H, Verstappen FT, Keizer HA et al (1985) Variability of aerobic performance in the laboratory and its physiologic correlates. Int J Sports Med 6(4):197–201. https://doi.org/10.1055/s-2008-1025839
Leal LG, Lopes MA, Batista ML (2018) Physical exercise-induced myokines and muscle-adipose tissue crosstalk: a review of current knowledge and the implications for health and metabolic diseases. Front Physiol 9:1307. https://doi.org/10.3389/fphys.2018.01307
Lee MY, Cheong SH, Chang KJ et al (2003) Effect of the obesity index on plasma taurine levels in Korean female adolescents. Adv Exp Med Biol 526:285–290. https://doi.org/10.1007/978-1-4615-0077-3_36
Li S, Li Y, Xiang L et al (2018) Sildenafil induces browning of subcutaneous white adipose tissue in overweight adults. Metabolism 78:106–117. https://doi.org/10.1016/j.metabol.2017.09.008
Lin S, Hirai S, Yamaguchi Y et al (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
Lin CJ, Chiu CC, Chen YC et al (2015) Taurine attenuates hepatic inflammation in chronic alcohol-fed rats through inhibition of TLR4/MyD88 signaling. J Med Food 18(12):1291–1298. https://doi.org/10.1089/jmf.2014.3408
Liu J, Divoux A, Sun J et al (2009) Genetic deficiency and pharmacological stabilization of mast cells reduce diet-induced obesity and diabetes in mice. Nat Med 15(8):940–945. https://doi.org/10.1038/nm.1994
Liu X, Zhang YR, Cai C et al (2019) Taurine alleviates schistosoma-induced liver injury by inhibiting the TXNIP/NLRP3 inflammasome signal pathway and pyroptosis. Infect Immun. https://doi.org/10.1128/IAI.00732-19
Lumeng CN, Saltiel AR (2011) Inflammatory links between obesity and metabolic disease. J Clin Investig 121(6):2111–2117. https://doi.org/10.1172/JCI57132
Maral J, Puget K, Michelson AM (1977) Comparative study of superoxide dismutase, catalase and glutathione peroxidase levels in erythrocytes of different animals. Biochem Biophys Res Commun 77(4):1525–1535. https://doi.org/10.1016/s0006-291x(77)80151-4
Marcinkiewicz J, Grabowska A, Bereta J et al (1995) Taurine chloramine, a product of activated neutrophils, inhibits in vitro the generation of nitric oxide and other macrophage inflammatory mediators. J Leukoc Biol 58(6):667–674. https://doi.org/10.1002/jlb.58.6.667
Murakami S (2015) Role of taurine in the pathogenesis of obesity. Mol Nutr Food Res 59(7):1353–1363. https://doi.org/10.1002/mnfr.201500067
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
Nadeau L, Aguer C (2019) Interleukin-15 as a myokine: mechanistic insight into its effect on skeletal muscle metabolism. Appl Physiol Nutr Metab 44(3):229–238. https://doi.org/10.1139/apnm-2018-0022
Pedersen BK, Febbraio MA (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 8(8):457–465. https://doi.org/10.1038/nrendo.2012.49
Pfrimer K, Moriguti JC, Lima NK (2012) Bioelectrical impedance with different equations versus deuterium oxide dilution method for the inference of body composition in healthy older persons. J Nutr Health Aging 16(2):124–127
Ra SG, Choi Y, Akazawa N et al (2016) Taurine supplementation attenuates delayed increase in exercise-induced arterial stiffness. Appl Physiol Nutr Metab 41(6):618–623. https://doi.org/10.1139/apnm-2015-0560
Rosa FT, Freitas EC, Deminice R et al (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
Schuller-Levis GB, Park E (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226(2):195–202. https://doi.org/10.1016/s0378-1097(03)00611-6
Schulze MB (2019) Metabolic health in normal-weight and obese individuals. Diabetologia 62(4):558–566. https://doi.org/10.1007/s00125-018-4787-8
Shao A, Hathcock JN (2008) Risk assessment for the amino acids taurine, l-glutamine and l-arginine. Regul Toxicol Pharmacol 50(3):376–399. https://doi.org/10.1016/j.yrtph.2008.01.004
Shao M, Wang QA, Song A et al (2019) Cellular origins of beige fat cells revisited. Diabetes 68(10):1874–1885. https://doi.org/10.2337/db19-0308
Sidossis L, Kajimura S (2015) Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Investig 125(2):478–486. https://doi.org/10.1172/JCI78362
Soltani N, Marandi SM, Kazemi M et al (2020) The exercise training modulatory effects on the obesity-induced immunometabolic dysfunctions. Diabetes Metab Syndr Obes 13:785–810. https://doi.org/10.2147/DMSO.S234992
Stanford KI, Goodyear LJ (2018) Muscle-adipose tissue cross talk. Cold Spring Harb Perspect Med. https://doi.org/10.1101/cshperspect.a029801
Tappaz ML (2004) Taurine biosynthetic enzymes and taurine transporter: molecular identification and regulations. Neurochem Res 29(1):83–96
Tsuboyama-Kasaoka N, Shozawa C, Sano K et al (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
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
Walczewska M, Marcinkiewicz J (2011) Taurine chloramine and its potential therapeutical application. Przegl Lek 68(6):334–338
Wang P, Wu P, Siegel MI et al (1994) IL-10 inhibits transcription of cytokine genes in human peripheral blood mononuclear cells. J Immunol 153(2):811–816
You T, Arsenis NC, Disanzo BL et al (2013) Effects of exercise training on chronic inflammation in obesity : current evidence and potential mechanisms. Sports Med 43(4):243–256. https://doi.org/10.1007/s40279-013-0023-3
Żelechowska P, Agier J, Kozłowska E et al (2018) Mast cells participate in chronic low-grade inflammation within adipose tissue. Obes Rev 19(5):686–697. https://doi.org/10.1111/obr.12670
Zhang M, Izumi I, Kagamimori S et al (2004) Role of taurine supplementation to prevent exercise-induced oxidative stress in healthy young men. Amino Acids 26(2):203–207. https://doi.org/10.1007/s00726-003-0002-3
Zhang H, Tong TK, Qiu W et al (2017) Comparable effects of high-intensity interval training and prolonged continuous exercise training on abdominal visceral fat reduction in obese young women. J Diabetes Res 2017:5071740. https://doi.org/10.1155/2017/5071740
Acknowledgements
The authors would like to thank the subjects for participating in this study; Dr. Thays de Vasconcelos Gomes and Dr. Pedro Dal Belo for expert assistance in the biopsy of adipose tissue; Ajinomoto® company (São Paulo, SP) for providing the taurine powder; The São Paulo Research Foundation (Fapesp)-Brazil-grants 2017/10080-2; 2017/08036-5; 2018/19107-3 and Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior (CAPES)-Brazil-Finance Code 001.
Funding
The research was supported by The São Paulo Research Foundation, FAPESP (Grant numbers 2017/10080-2; 2017/08036-5; 2018/19107-3).
Author information
Authors and Affiliations
Contributions
FGDC, CFCB, VRM, JRP, and ECF conceived the design of the study; FGDC, CFCB, GB, and MVMJF performed the data collection; DEC, MEAT, GRT worked in the histological analysis; FGDC, VRM, JRP, LPM, ERR, and ASRS were involved in the data analysis. FGDC, VRM, and ECF drafted the manuscript. JRP, LPM, ERR, DEC, ASRS, and ECF revised it critically for important intellectual content. All authors read and approved the final version.
Corresponding author
Ethics declarations
Conflict of interest
The authors FGDC, CFCB, VRM, GB, JRP, LPM, ERR, DEC, ASRS, MVMJ, MEAT, GRT, JSM, and ECF declare that they have no conflicts of interest.
Ethics approval
The Ethical Committee of the School of Physical Education and Sport of Ribeirão Preto, University of São Paulo approved the study (protocol number: 62643516.7.0000.5659). The study is in accordance with the standards of ethics outlined in the Declaration of Helsinki.
Consent to participate
All subjects gave free written consent for participation.
Additional information
Handling editor: S. W. Schaffer.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
De Carvalho, F.G., Brandao, C.F.C., Muñoz, V.R. et al. Taurine supplementation in conjunction with exercise modulated cytokines and improved subcutaneous white adipose tissue plasticity in obese women. Amino Acids 53, 1391–1403 (2021). https://doi.org/10.1007/s00726-021-03041-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-021-03041-4