Alpha-lipoic acid supplementation increases the efficacy of exercise- and diet-induced obesity treatment and induces immunometabolic changes in female mice and women.


Journal

FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484

Informations de publication

Date de publication:
04 2021
Historique:
revised: 11 12 2020
received: 29 07 2020
accepted: 14 12 2020
entrez: 20 3 2021
pubmed: 21 3 2021
medline: 22 7 2021
Statut: ppublish

Résumé

The decrease in the regulatory T cells (Tregs) population is highly involved in adipose tissue inflammation and insulin resistance in obesity. Tregs depend on fatty acids via β-oxidation for immunosuppressive function adapting their antioxidant systems to allow survival to oxidative stress. In this study, we have hypothesized that a dietary supplementation with alpha-lipoic acid (ALA), a powerful antioxidant, would improve immunometabolism when added to the classical strategy of obesity treatment. First, we showed by in vitro experiments that ALA favors the polarization of mice CD4 + T cells toward Tregs. Next, we have carried out a translational study where female obese mice and women were supplemented with ALA or vehicle/placebo (mice: 2.5 g

Identifiants

pubmed: 33742689
doi: 10.1096/fj.202001817RR
doi:

Substances chimiques

Palmitates 0
Thioctic Acid 73Y7P0K73Y

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e21312

Informations de copyright

© 2021 Federation of American Societies for Experimental Biology.

Références

Longo M, Zatterale F, Naderi J, et al. Adipose tissue dysfunction as determinant of obesity-associated metabolic complications. Int J Mol Sci. 2019;20:2358.
Feuerer M, Herrero L, Cipolletta D, et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med. 2009;15:930-939.
Deng T, Liu J, Deng Y, et al. Adipocyte adaptive immunity mediates diet-induced adipose inflammation and insulin resistance by decreasing adipose Treg cells. Nat Commun. 2017;8:15725.
Pedersen BK, Saltin B. Exercise as medicine-evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports. 2015;25:1-72.
Piening BD, Zhou W, Contrepois K, et al. Integrative personal omics profiles during periods of weight gain and loss. Cell Syst. 2018;6:157-170.e8.
Fothergill E, Guo J, Howard L, et al. Persistent metabolic adaptation 6 years after “The Biggest Loser” competition: persistent metabolic adaptation. Obesity. 2016;24:1612-1619.
Le Garf S, Murdaca J, Mothe-Satney I, et al. Complementary immunometabolic effects of exercise and PPARβ/δ agonist in the context of diet-induced weight loss in obese female mice. Int J Mol Sci. 2019;20:5182.
Gupte AA, Bomhoff GL, Morris JK, Gorres BK, Geiger PC. Lipoic acid increases heat shock protein expression and inhibits stress kinase activation to improve insulin signaling in skeletal muscle from high-fat-fed rats. J Appl Physiol. 2009;106:1425-1434.
Rousseau A-S, Sibille B, Murdaca J, Mothe-Satney I, Grimaldi PA, Neels JG. α-Lipoic acid up-regulates expression of peroxisome proliferator-activated receptor β in skeletal muscle: involvement of the JNK signaling pathway. FASEB J. 2016;30:1287-1299.
Suzuki YJ, Aggarwala BB, Packer L. a-Lipoic acid is a potent inhibitor of NF-KB activation in human T cells. Biochem Biophys Res Commun. 1992;189:1709-1715.
Namazi N, Larijani B, Azadbakht L. Alpha-lipoic acid supplement in obesity treatment: a systematic review and meta-analysis of clinical trials. Clin Nutr. 2018;37:419-428.
Rahimlou M, Asadi M, Banaei Jahromi N, Mansoori A. Alpha-lipoic acid (ALA) supplementation effect on glycemic and inflammatory biomarkers: a systematic review and meta-analysis. Clin Nutr ESPEN. 2019;32:16-28.
Deiuliis JA, Kampfrath T, Ying Z, Maiseyeu A, Rajagopalan S. Lipoic acid attenuates innate immune infiltration and activation in the visceral adipose tissue of obese insulin resistant mice. Lipids. 2011;46:1021-1032.
Wang K-C, Tsai C-P, Lee C-L, et al. α-Lipoic acid enhances endogenous peroxisome-proliferator-activated receptor-γ to ameliorate experimental autoimmune encephalomyelitis in mice. Clin Sci. 2013;125:329-340.
Cui J, Huang D, Zheng Y. Ameliorative effects of α-lipoic acid on high-fat diet-induced oxidative stress and glucose uptake impairment of T cells. Free Radic Res. 2016;50:1106-1115.
Sen CK, Roy S, Han D, Packer L. Regulation of cellular thiols in human lymphocytes by a-lipoic acid: a flow cytometric analysis. Free Radic Biol Med. 1997;22:1241-1257.
Ma Q. Role of Nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol. 2013;53:401-426.
Rochette L, Ghibu S, Richard C, Zeller M, Cottin Y, Vergely C. Direct and indirect antioxidant properties of α-lipoic acid and therapeutic potential. Mol Nutr Food Res. 2013;57:114-125.
Ogborne RM, Rushworth SA, O'Connell MA. α-Lipoic acid-induced heme oxygenase-1 expression is mediated by nuclear factor erythroid 2-related factor 2 and p38 mitogen-activated protein kinase in human monocytic cells. Arterioscler Thromb Vasc Biol. 2005;25:2100-2105.
McCarty MF, Barroso-Aranda J, Contreras F. The, “rejuvenatory” impact of lipoic acid on mitochondrial function in aging rats may reflect induction and activation of PPAR-γ coactivator-1α. Med Hypotheses. 2009;72:29-33.
Buck MD, O'Sullivan D, Pearce EL. T cell metabolism drives immunity. J Exp Med. 2015;212:1345-1360.
Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4:330-336.
Pereira LMS, Gomes STM, Ishak R, Vallinoto ACR. Regulatory T cell and Forkhead box protein 3 as modulators of immune homeostasis. Front Immunol. 2017;8:605.
Shi H, Chi H. Metabolic control of treg cell stability, plasticity, and tissue-specific heterogeneity. Front Immunol. 2019;10:2716.
Berod L, Friedrich C, Nandan A, et al. De novo fatty acid synthesis controls the fate between regulatory T and T helper 17 cells. Nat Med. 2014;20:1327-1333.
Newton R, Priyadharshini B, Turka LA. Immunometabolism of regulatory T cells. Nat Immunol. 2016;17:618-625.
Sena L, Li S, Jairaman A, et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity. 2013;38:225-236.
Chen X, Song M, Zhang B, Zhang Y. Reactive oxygen species regulate T cell immune response in the tumor microenvironment. Oxid Med Cell Longev. 2016;2016:1-10.
Panda S, Ravindran B. Isolation of human PBMCs. BIO-Protoc. 2013;3:e323.
Huang K-C, Kormas N, Steinbeck K, Loughnan G, Caterson ID. Resting metabolic rate in severely obese diabetic and nondiabetic subjects. Obes Res. 2004;12:840-845.
Björkman F, Ekblom-Bak E, Ekblom Ö, Ekblom B. Validity of the revised Ekblom Bak cycle ergometer test in adults. Eur J Appl Physiol. 2016;116:1627-1638.
Maurovich-Horvat P, Massaro J, Fox CS, et al. Comparison of anthropometric, area- and volume-based assessment of abdominal subcutaneous and visceral adipose tissue volumes using multi-detector computed tomography. Int J Obes. 2007;31:500-506.
Patwardhan RS, Singh B, Pal D, et al. Redox regulation of regulatory T cell differentiation and functions. Free Radic Res. 2020:1-14. https://doi.org/10.1080/10715762.2020.1745202
Beier UH, Angelin A, Akimova T, et al. Essential role of mitochondrial energy metabolism in Foxp3 + T-regulatory cell function and allograft survival. FASEB J. 2015;29:2315-2326.
Zeng Q, Sun X, Xiao L, Xie Z, Bettini M, Deng T. A unique population: adipose-resident regulatory T cells. Front Immunol. 2018;9:2075.
Magesh S, Chen Y, Hu L. Small molecule modulators of keap1-Nrf2-ARE pathway as potential preventive and therapeutic agents: small molecule modulators of keap1-NRF2-are pathway. Med Res Rev. 2012;32:687-726.
Blackburn GL. Weight loss and risk factors. In: Fairburn CG, Brownell KD, eds. Eating Disorders and Obesity: A Comprehensive Handbook. 2nd ed. New York: Guilford Press; 2002:484-490.
Anderson EK, Gutierrez DA, Kennedy A, Hasty AH. Weight cycling increases T-cell accumulation in adipose tissue and impairs systemic glucose tolerance. Diabetes. 2013;62:3180-3188.
Vasanthakumar A, Chisanga D, Blume J, et al. Sex-specific adipose tissue imprinting of regulatory T cells. Nature. 2020;579:581-585.
Ishikawa A, Wada T, Nishimura S, et al. Estrogen regulates sex-specific localization of regulatory T cells in adipose tissue of obese female mice. PLoS ONE. 2020;15:e0230885.
Ahnstedt H, Roy-O’Reilly M, Spychala MS, et al. Sex differences in adipose tissue CD8+ T cells and regulatory T cells in middle-aged mice. Front Immunol. 2018;9:659
Wirth A, Steinmetz B. Gender differences in changes in subcutaneous and intra-abdominal fat during weight reduction: an ultrasound study. Obes Res. 1998;6:393-399.
Christensen P, Meinert Larsen T, Westerterp-Plantenga M, et al. Men and women respond differently to rapid weight loss: metabolic outcomes of a multi-centre intervention study after a low-energy diet in 2500 overweight, individuals with pre-diabetes (PREVIEW). Diabetes Obes Metab. 2018;20:2840-2851.
Michalek RD, Gerriets VA, Jacobs SR, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol. 2011;186:3299-3303.
Cluxton D, Petrasca A, Moran B, Fletcher JM. Differential regulation of human Treg and Th17 cells by fatty acid synthesis and glycolysis. Front Immunol. 2019;10:115.
Sena C, Cipriano M, Botelho M, Seiça R. Lipoic acid prevents high-fat diet-induced hepatic steatosis in Goto Kakizaki rats by reducing oxidative stress through Nrf2 activation. Int J Mol Sci. 2018;19:2706.
Maj T, Wang W, Crespo J, et al. Oxidative stress controls regulatory T cell apoptosis and suppressor activity and PD-L1-blockade resistance in tumor. Nat Immunol. 2017;18:1332-1341.
Sireesh D, Dhamodharan U, Ezhilarasi K, Vijay V, Ramkumar KM. Association of NF-E2 related factor 2 (Nrf2) and inflammatory cytokines in recent onset Type 2 Diabetes mellitus. Sci Rep. 2018;8:5126.
Zhang Q, Cui T, Chang Y, et al. HO-1 regulates the function of Treg: association with the immune intolerance in vitiligo. J Cell Mol Med. 2018;22:4335-4343.
Ježek P, Holendová B, Garlid KD, Jabůrek M. Mitochondrial Uncoupling Proteins: Subtle Regulators of Cellular Redox Signaling. Reviewing Editors: Jerzy Beltowski, Joseph Burgoyne, Gabor Csanyi, Sergey Dikalov, Frank Krause, Anibal Vercesi, and Jeremy Ward. Antioxid Redox Signal. 2018;29:667-714.
Klaus S, Keipert S, Rossmeisl M, Kopecky J. Augmenting energy expenditure by mitochondrial uncoupling: a role of AMP-activated protein kinase. Genes Nutr. 2012;7:369-386.
Wagner N-M, Brandhorst G, Czepluch F, et al. Circulating regulatory T cells are reduced in obesity and may identify subjects at increased metabolic and cardiovascular risk: regulatory T cells and obesity. Obesity. 2013;21:461-468.
Tyrrell DJ, Bharadwaj MS, Van Horn CG, et al. Blood-cell bioenergetics are associated with physical function and inflammation in overweight/obese older adults. Exp Gerontol. 2015;70:84-91.
Zou J, Lai B, Zheng M, et al. CD4+ T cells memorize obesity and promote weight regain. Cell Mol Immunol. 2018;15:630-639.
Yadav V, Marracci GH, Munar MY, et al. Pharmacokinetic study of lipoic acid in multiple sclerosis: comparing mice and human pharmacokinetic parameters. Mult Scler J. 2010;16:387-397.

Auteurs

Sébastien Le Garf (S)

INSERM, C3M, Université Côte d'Azur, Nice, France.

Brigitte Sibille (B)

INSERM, C3M, Université Côte d'Azur, Nice, France.

Isabelle Mothe-Satney (I)

INSERM, C3M, Université Côte d'Azur, Nice, France.

Cyril Eininger (C)

Polyclinique Oxford, Cannes, France.

Philippe Fauque (P)

Polyclinique Oxford, Cannes, France.

Joseph Murdaca (J)

INSERM, C3M, Université Côte d'Azur, Nice, France.

Giulia Chinetti (G)

CHU, INSERM, C3M, Université Côte d'Azur, Nice, France.

Jaap G Neels (JG)

INSERM, C3M, Université Côte d'Azur, Nice, France.

Anne-Sophie Rousseau (AS)

INSERM, C3M, Université Côte d'Azur, Nice, France.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH