Sustained caloric restriction potentiates insulin action by activating prostacyclin synthase.
Journal
Obesity (Silver Spring, Md.)
ISSN: 1930-739X
Titre abrégé: Obesity (Silver Spring)
Pays: United States
ID NLM: 101264860
Informations de publication
Date de publication:
17 Oct 2024
17 Oct 2024
Historique:
revised:
08
08
2024
received:
19
04
2024
accepted:
12
08
2024
medline:
18
10
2024
pubmed:
18
10
2024
entrez:
18
10
2024
Statut:
aheadofprint
Résumé
Caloric restriction (CR) is known to enhance insulin sensitivity and reduce the risk of metabolic disorders; however, its molecular mechanisms are not fully understood. This study aims to elucidate specific proteins and pathways responsible for these benefits. We examined adipose tissue from participants in the Comprehensive Assessment of Long-term Effects of Reducing Intake of Energy Phase 2 (CALERIE 2) study, comparing proteomic profiles from individuals after 12 and 24 months of CR with baseline and an ad libitum group. Biochemical and cell-specific physiological approaches complemented these analyses. Our data revealed that CR upregulates prostacyclin synthase (PTGIS) in adipose tissue, an enzyme crucial for producing prostacyclin (PGI2). PGI2 improves the ability of insulin to stimulate the tether-containing UBX domain for GLUT4 (TUG) cleavage pathway, which is essential for glucose uptake regulation. Additionally, iloprost, a PGI2 analog, was shown to increase insulin receptor density on cell membranes, increasing glucose uptake in human adipocytes. CR also reduces carbonylation of GLUT4, a modification that is detrimental to GLUT4 function. CR enhances insulin sensitivity by promoting PTGIS expression and stimulating the TUG cleavage pathway, leading to increased GLUT4 translocation to the cell surface and decreased GLUT4 carbonylation. These findings shed light on the complex molecular mechanisms through which CR favorably impacts insulin sensitivity and metabolic health.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIH HHS
ID : R21 AG06430
Pays : United States
Organisme : NIH HHS
ID : R33-AG070455
Pays : United States
Organisme : NIH HHS
ID : R01DK129466
Pays : United States
Informations de copyright
© 2024 The Obesity Society.
Références
Kraus WE, Bhapkar M, Huffman KM, et al. 2 years of calorie restriction and cardiometabolic risk (CALERIE): exploratory outcomes of a multicentre, phase 2, randomised controlled trial. Lancet Diabetes Endocrinol. 2019;7:673‐683.
Dorling JL, van Vliet S, Huffman KM, et al. Effects of caloric restriction on human physiological, psychological, and behavioral outcomes: highlights from CALERIE phase 2. Nutr Rev. 2021;79:98‐113.
Shen W, Chen J, Zhou J, Martin CK, Ravussin E, Redman LM. Effect of 2‐year caloric restriction on organ and tissue size in nonobese 21‐ to 50‐year‐old adults in a randomized clinical trial: the CALERIE study. Am J Clin Nutr. 2021;114:1295‐1303.
Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001;414:799‐806.
Goodyear LJ, Giorgino F, Sherman LA, Carey J, Smith RJ, Dohm GL. Insulin receptor phosphorylation, insulin receptor substrate‐1 phosphorylation, and phosphatidylinositol 3‐kinase activity are decreased in intact skeletal muscle strips from obese subjects. J Clin Invest. 1995;95:2195‐2204.
Kerouz NJ, Horsch D, Pons S, Kahn CR. Differential regulation of insulin receptor substrates‐1 and ‐2 (IRS‐1 and IRS‐2) and phosphatidylinositol 3‐kinase isoforms in liver and muscle of the obese diabetic (ob/ob) mouse. J Clin Invest. 1997;100:3164‐3172.
Bogan JS. Ubiquitin‐like processing of TUG proteins as a mechanism to regulate glucose uptake and energy metabolism in fat and muscle. Front Endocrinol (Lausanne). 2022;13:1019405.
Habtemichael EN, Li DT, Camporez JP, et al. Insulin‐stimulated endoproteolytic TUG cleavage links energy expenditure with glucose uptake. Nat Metab. 2021;3:378‐393.
Boden G, Homko C, Barrero CA, et al. Excessive caloric intake acutely causes oxidative stress, GLUT4 carbonylation, and insulin resistance in healthy men. Sci Transl Med. 2015;7:304re307.
Curtis JM, Hahn WS, Stone MD, et al. Protein carbonylation and adipocyte mitochondrial function. J Biol Chem. 2012;287:32967‐32980.
Frohnert BI, Bernlohr DA. Protein carbonylation, mitochondrial dysfunction, and insulin resistance. Adv Nutr. 2013;4:157‐163.
Grimsrud PA, Picklo MJ Sr, Griffin TJ, Bernlohr DA. Carbonylation of adipose proteins in obesity and insulin resistance: identification of adipocyte fatty acid‐binding protein as a cellular target of 4‐hydroxynonenal. Mol Cell Proteomics. 2007;6:624‐637.
Ruskovska T, Bernlohr DA. Oxidative stress and protein carbonylation in adipose tissue ‐ implications for insulin resistance and diabetes mellitus. J Proteomics. 2013;92:323‐334.
Xu Q, Hahn WS, Bernlohr DA. Detecting protein carbonylation in adipose tissue and in cultured adipocytes. Methods Enzymol. 2014;538:249‐261.
Frohnert BI, Sinaiko AR, Serrot FJ, et al. Increased adipose protein carbonylation in human obesity. Obesity (Silver Spring). 2011;19:1735‐1741.
Li Y, Zhao T, Li J, et al. Oxidative stress and 4‐hydroxy‐2‐nonenal (4‐HNE): implications in the pathogenesis and treatment of aging‐related diseases. J Immunol Res. 2022;2022:2233906.
Paolisso G, Di Maro G, D'Amore A, et al. Low‐dose iloprost infusion improves insulin action in aged healthy subjects and NIDDM patients. Diabetes Care. 1995;18:200‐205.
Paolisso G, Gambardella A, Saccomanno F, Varricchio G, D'Amore A, Varricchio M. Low‐dose Iloprost infusion improves insulin action and non‐oxidative glucose metabolism in hypertensive patients. Eur J Clin Pharmacol. 1995;48:333‐338.
Shrestha J, Santerre M, Allen CNS, et al. HIV‐1 gp120 impairs spatial memory through cyclic AMP response element‐binding protein. Front Aging Neurosci. 2022;14:811481.
Quinn C, Rico MC, Merali C, Merali S. Dysregulation of S‐adenosylmethionine metabolism in nonalcoholic Steatohepatitis leads to polyamine flux and oxidative stress. Int J Mol Sci. 2022;2:1‐25.
McBrearty N, Arzumanyan A, Bichenkov E, Merali S, Merali C, Feitelson M. Short chain fatty acids delay the development of hepatocellular carcinoma in HBx transgenic mice. Neoplasia. 2021;23:529‐538.
Boden G, Song W, Duan X, et al. Infusion of glucose and lipids at physiological rates causes acute endoplasmic reticulum stress in rat liver. Obesity (Silver Spring). 2011;19:1366‐1373.
Boden G, Merali S. Measurement of the increase in endoplasmic reticulum stress‐related proteins and genes in adipose tissue of obese, insulin‐resistant individuals. Methods Enzymol. 2011;489:67‐82.
Zhang H, Pandey S, Travers M, et al. Targeting CDK9 reactivates epigenetically silenced genes in cancer. Cell. 2018;175:1244‐1258.e1226.
Rossi MT, Langston JC, Singh N, et al. Molecular framework of mouse endothelial cell dysfunction during inflammation: a proteomics approach. Int J Mol Sci. 2022;23:1‐14.
Quinn C, Rico MC, Merali C, et al. Secreted folate receptor gamma drives fibrogenesis in metabolic dysfunction‐associated steatohepatitis by amplifying TGFbeta signaling in hepatic stellate cells. Sci Transl Med. 2023;15:eade2966.
Palomba A, Abbondio M, Fiorito G, Uzzau S, Pagnozzi D, Tanca A. Comparative evaluation of MaxQuant and proteome discoverer MS1‐based protein quantification tools. J Proteome Res. 2021;20:3497‐3507.
Duregon E, Fernandez ME, Martinez Romero J, et al. Prolonged fasting times reap greater geroprotective effects when combined with caloric restriction in adult female mice. Cell Metab. 2023;35(1179–1194):e1175.
Spadaro O, Youm Y, Shchukina I, et al. Caloric restriction in humans reveals immunometabolic regulators of health span. Science. 2022;375:671‐677.
Ray TK, Dutta‐Roy AK, Sinha AK. Regulation of insulin receptor activity of human erythrocyte membrane by prostaglandin E1. Biochim Biophys Acta. 1986;856:421‐427.
Friesen M, Khalil AS, Barrasa MI, Jeppesen JF, Mooney DJ, Jaenisch R. Development of a physiological insulin resistance model in human stem cell‐derived adipocytes. Sci Adv. 2022;8:eabn7298.
Li T, Hentschel A, Ahrends R. Analytical comparison of absolute quantification strategies to investigate the insulin signaling pathway in fat cells. Proteomics. 2022;22:e2100136.
Grimsrud PA, Xie H, Griffin TJ, Bernlohr DA. Oxidative stress and covalent modification of protein with bioactive aldehydes. J Biol Chem. 2008;283:21837‐21841.
Zhang X, Wang Z, Li J, et al. Increased 4‐hydroxynonenal formation contributes to obesity‐related lipolytic activation in adipocytes. PLoS One. 2013;8:e70663.
Ayala A, Munoz MF, Arguelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4‐hydroxy‐2‐nonenal. Oxid Med Cell Longev. 2014;2014:360438.
Datta PK, Deshmane S, Khalili K, et al. Glutamate metabolism in HIV‐1 infected macrophages: role of HIV‐1 Vpr. Cell Cycle. 2016;15:2288‐2298.
Bloch‐Damti A, Bashan N. Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxid Redox Signal. 2005;7:1553‐1567.
Chen ZH, Niki E. 4‐hydroxynonenal (4‐HNE) has been widely accepted as an inducer of oxidative stress. Is this the whole truth about it or can 4‐HNE also exert protective effects? IUBMB Life. 2006;58:372‐373.
Siems W, Grune T. Intracellular metabolism of 4‐hydroxynonenal. Mol Aspects Med. 2003;24:167‐175.
Park S, Park NY, Valacchi G, Lim Y. Calorie restriction with a high‐fat diet effectively attenuated inflammatory response and oxidative stress‐related markers in obese tissues of the high diet fed rats. Mediators Inflamm. 2012;2012:984643.
Zanquetta MM, Seraphim PM, Sumida DH, Cipolla‐Neto J, Machado UF. Calorie restriction reduces pinealectomy‐induced insulin resistance by improving GLUT4 gene expression and its translocation to the plasma membrane. J Pineal Res. 2003;35:141‐148.
Wheatley KE, Nogueira LM, Perkins SN, Hursting SD. Differential effects of calorie restriction and exercise on the adipose transcriptome in diet‐induced obese mice. J Obes. 2011;2011:265417.
Barnes H, Yeoh HL, Fothergill T, Burns A, Humbert M, Williams T. Prostacyclin for pulmonary arterial hypertension. Cochrane Database Syst Rev. 2019;5:CD012785.
Vinals M, Martinez‐Gonzalez J, Badimon JJ, Badimon L. HDL‐induced prostacyclin release in smooth muscle cells is dependent on cyclooxygenase‐2 (Cox‐2). Arterioscler Thromb Vasc Biol. 1997;17:3481‐3488.
Habtemichael EN, Li DT, Alcazar‐Roman A, et al. Usp25m protease regulates ubiquitin‐like processing of TUG proteins to control GLUT4 glucose transporter translocation in adipocytes. J Biol Chem. 2018;293:10466‐10486.
Mattson MP. Roles of the lipid peroxidation product 4‐hydroxynonenal in obesity, the metabolic syndrome, and associated vascular and neurodegenerative disorders. Exp Gerontol. 2009;44:625‐633.