Curcumin Prevents the Glycation of Tricarboxylic Acid Cycle and Cell Respiration Proteins in the Heart of Mice Fed with a High-fructose Diet | Bentham Science
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Research Article

Curcumin Prevents the Glycation of Tricarboxylic Acid Cycle and Cell Respiration Proteins in the Heart of Mice Fed with a High-fructose Diet

Author(s): María Cristina León-García, Oscar Gerardo Silva-Gaona, Magdalena Hernández-Ortiz, Katya Vargas-Ortiz, Joel Ramírez-Emiliano, Ma Eugenia Garay-Sevilla, Sergio Encarnación-Guevara and Victoriano Pérez-Vázquez*

Volume 28, Issue 21, 2022

Published on: 23 May, 2022

Page: [1769 - 1778] Pages: 10

DOI: 10.2174/1381612828666220331160501

Price: $65

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Abstract

Background: A high fructose diet (HFD) induces protein glycation. The latter is related to a higher risk of cardiovascular disease. Curcumin is a natural pleiotropic compound that may possess antiglycant properties.

Objective: The study aims to analyze the effect of curcumin on the content of glycated proteins in the hearts of 6-week-old mice fed with a HFD for 15 weeks.

Methods: Mice were allocated into four groups (n = 6/group): a control group that received a standard diet (CT); a group that received 30% w/v fructose in water (F); a group that received 0.75% w/w curcumin supplemented in food (C); a group that received 30% w/v fructose in water and 0.75% w/w curcumin supplemented in food (F+C). The content of glycated proteins in the heart was determined by Western Blot (whereas the spots were detected by 2D-PAGE) using anti-AGE and anti-CML antibodies. Densitometric analysis was performed using the ImageLab software. Glycated proteins were identified by MALDI-TOF-MS, and an ontological analysis was performed in terms of biological processes and molecular function based on the STRING and DAVID databases.

Results: Fourteen glycated protein spots were detected, two of them with anti-AGE and the other 12 with anti- CML. In total, eleven glycated proteins were identified, out of which three had decreased glycation levels due to curcumin exposure. The identified proteins participate in processes such as cellular respiration, oxidative phosphorylation, lipid metabolism, carbohydrate metabolism, the tricarboxylic acid cycle (TAC), and the organization of intermediate filaments.

Conclusion: Curcumin decreased the fructose-induced glycation level of the ACO2, NDUFS7, and DLAT proteins.

Keywords: ACO2, carboximetil-lysine, curcumin, DLAT, fructose, glycation, NDUFS7.

« Previous
[1]
Basciano H, Federico L, Adeli K. Fructose, insulin resistance, and metabolic dyslipidemia. Nutr Metab (Lond) 2005; 2(1): 5.
[http://dx.doi.org/10.1186/1743-7075-2-5 ] [PMID: 15723702]
[2]
Topsakal S, Ozmen O, Cankara FN, et al. Alpha lipoic acid attenuates high-fructose-induced pancreatic toxicity. Pancreatology 2016; 16(3): 347-52.
[http://dx.doi.org/10.1016/j.pan.2016.03.001 ] [PMID: 27025195]
[3]
Douard V, Ferraris RP. Regulation of the fructose transporter GLUT5 in health and disease. Am J Physiol Endocrinol Metab 2008; 295(2): E227-37.
[http://dx.doi.org/10.1152/ajpendo.90245.2008 ] [PMID: 18398011]
[4]
Jegatheesan P, Beutheu S, Freese K, et al. Preventive effects of citrulline on Western diet-induced non-alcoholic fatty liver disease in rats. Br J Nutr 2016; 116(2): 191-203.
[http://dx.doi.org/10.1017/S0007114516001793 ] [PMID: 27197843]
[5]
Tappy L. Fructose-containing caloric sweeteners as a cause of obesity and metabolic disorders. J Exp Biol 2018; 221(Pt)(Suppl.1): 1-9.
[http://dx.doi.org/10.1242/jeb.164202] [PMID: 29514881]
[6]
Schalkwijk CG, Stehouwer CD, van Hinsbergh VW. Fructose-mediated non-enzymatic glycation: Sweet coupling or bad modification. Diabetes Metab Res Rev 2004; 20(5): 369-82.
[http://dx.doi.org/10.1002/dmrr.488 ] [PMID: 15343583]
[7]
Levi B, Werman MJ. Long-term fructose consumption accelerates glycation and several age-related variables in male rats. J Nutr 1998; 128(9): 1442-9.
[http://dx.doi.org/10.1093/jn/128.9.1442 ] [PMID: 9732303]
[8]
Guilbaud A, Niquet-Leridon C, Boulanger E, Tessier FJ. How can diet affect the accumulation of advanced glycation end-products in the human body? Foods 2016; 5(4): 1-14.
[http://dx.doi.org/10.3390/foods5040084 ] [PMID: 28231179]
[9]
Mastrocola R, Collino M, Rogazzo M, et al. Advanced glycation end products promote hepatosteatosis by interfering with SCAP-SREBP pathway in fructose-drinking mice. Am J Physiol Gastrointest Liver Physiol 2013; 305(6): G398-407.
[http://dx.doi.org/10.1152/ajpgi.00450.2012 ] [PMID: 23868406]
[10]
Mastrocola R, Nigro D, Chiazza F, et al. Fructose-derived advanced glycation end-products drive lipogenesis and skeletal muscle reprogramming via SREBP-1c dysregulation in mice. Free Radic Biol Med 2016; 91: 224-35.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.12.022 ] [PMID: 26721591]
[11]
Ansley DM, Wang B. Oxidative stress and myocardial injury in the diabetic heart. J Pathol 2013; 229(2): 232-41.
[http://dx.doi.org/10.1002/path.4113 ] [PMID: 23011912]
[12]
Han J, Tan C, Wang Y, Yang S, Tan D. Betanin reduces the accumulation and cross-links of collagen in high-fructose-fed rat heart through inhibiting non-enzymatic glycation. Chem Biol Interact 2015; 227: 37-44.
[http://dx.doi.org/10.1016/j.cbi.2014.12.032 ] [PMID: 25559852]
[13]
Stitt AW, Frizzell N, Thorpe SR. Advanced glycation and advanced lipoxidation: Possible role in initiation and progression of diabetic retinopathy. Curr Pharm Des 2004; 10(27): 3349-60.
[http://dx.doi.org/10.2174/1381612043383124 ] [PMID: 15544520]
[14]
Bidasee KR, Zhang Y, Shao CH, et al. Diabetes increases formation of advanced glycation end products on Sarco (endo) plasmic reticulum Ca2+-ATPase. Diabetes 2004; 53(2): 463-73.
[http://dx.doi.org/10.2337/diabetes.53.2.463 ] [PMID: 14747299]
[15]
Bidasee KR, Nallani K, Yu Y, et al. Chronic diabetes increases advanced glycation end products on cardiac ryanodine receptors/calcium-release channels. Diabetes 2003; 52(7): 1825-36.
[http://dx.doi.org/10.2337/diabetes.52.7.1825 ] [PMID: 12829653]
[16]
Ghosh S, Banerjee S, Sil PC. The beneficial role of curcumin on inflammation, diabetes and neurodegenerative disease: A recent update. Food Chem Toxicol 2015; 83: 111-24.
[http://dx.doi.org/10.1016/j.fct.2015.05.022 ] [PMID: 26066364]
[17]
Jiménez-Flores LM, López-Briones S, Macías-Cervantes MH, Ramírez-Emiliano J, Pérez-Vázquez VA. PPARγ, NF-κB and AMPK-dependent mechanism may be involved in the beneficial effects of curcumin in the diabetic db/db mice liver. Molecules 2014; 19(6): 8289-302.
[http://dx.doi.org/10.3390/molecules19068289 ] [PMID: 24945581]
[18]
Liu YH, Lee TL, Han CH, Lee YS, Hou WC. Anti-glycation, anti-hemolysis, and ORAC activities of demethylcurcumin and tetrahydroxycurcumin in vitro and reductions of oxidative stress in ] D-galactose-induced BALB/c mice in vivo. Bot Stud 2019; 60(1): 1-9.
[http://dx.doi.org/10.1186/s40529-019-0258-x ] [PMID: 31250143]
[19]
Sun YP, Gu JF, Tan XB, et al. Curcumin inhibits advanced glycation end product-induced oxidative stress and inflammatory responses in endothelial cell damage via trapping methylglyoxal. Mol Med Rep 2016; 13(2): 1475-86.
[http://dx.doi.org/10.3892/mmr.2015.4725 ] [PMID: 26718010]
[20]
Fleenor BS, Sindler AL, Marvi NK, et al. Curcumin ameliorates arterial dysfunction and oxidative stress with aging. Exp Gerontol 2013; 48(2): 269-76.
[http://dx.doi.org/10.1016/j.exger.2012.10.008 ] [PMID: 23142245]
[21]
Lima TFO, Costa MC, Figueiredo ID, et al. Curcumin, alone or in combination with aminoguanidine, increases antioxidant defenses and glycation product detoxification in streptozotocin-diabetic rats: A therapeutic strategy to mitigate glycoxidative stress. Oxid Med Cell Longev 2020; 2020: 1036360.
[http://dx.doi.org/10.1155/2020/1036360 ] [PMID: 32566072]
[22]
Campos M, Ferreira T, Lima O, et al. Science direct and inflammation and increase glycation product detoxification in the liver and kidney of mice with high-fat diet-induced obesity. J Nutr Biochem 2020; 76: 108303.
[http://dx.doi.org/10.1016/j.jnutbio.2019.108303 ] [PMID: 31812909]
[23]
Xie XW. Liquiritigenin attenuates cardiac injury induced by high fructose-feeding through fibrosis and inflammation suppression. Biomed Pharmacother 2017; 86: 694-704.
[http://dx.doi.org/10.1016/j.biopha.2016.12.066 ] [PMID: 28039849]
[24]
Hurkman WJ, Tanaka CK. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 1986; 81(3): 802-6.
[http://dx.doi.org/10.1104/pp.81.3.802 ] [PMID: 16664906]
[25]
Zor T, Selinger Z. Linearization of the Bradford protein assay increases its sensitivity: Theoretical and experimental studies. Anal Biochem 1996; 236(2): 302-8.
[http://dx.doi.org/10.1006/abio.1996.0171 ] [PMID: 8660509]
[26]
UniProt Consortium. The Universal Protein Resource (UniProt) 2009. Nucleic Acids Res 2009; 37(Database issue): D169-74.
[PMID: 18836194]
[27]
Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999; 20(18): 3551-67.
[http://dx.doi.org/10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2] [PMID: 1061228]
[28]
Szklarczyk D, Franceschini A, Wyder S, et al. STRING v10: Protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 2015; 43(Database issue): D447-52.
[http://dx.doi.org/10.1093/nar/gku1003 ] [PMID: 25352553]
[29]
Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4(1): 44-57.
[http://dx.doi.org/10.1038/nprot.2008.211 ] [PMID: 19131956]
[30]
Liu Z, Sun Y, Qiao Q, et al. Sesamol ameliorates high-fat and high-fructose induced cognitive defects via improving insulin signaling disruption in the central nervous system. Food Funct 2017; 8(2): 710-9.
[http://dx.doi.org/10.1039/C6FO01562J ] [PMID: 28102395]
[31]
Wooten JS, Nick TN, Seija A, Poole KE, Stout KB. High-fructose intake impairs the hepatic hypolipidemic effects of a high-fat fish-oil diet in C57BL/6 mice. J Clin Exp Hepatol 2016; 6(4): 265-74.
[http://dx.doi.org/10.1016/j.jceh.2016.09.001 ] [PMID: 28003715]
[32]
Gulizia MM, Colivicchi F, Ricciardi G, et al. ANMCO/ISS/] AMD/ANCE/ARCA/FADOI/GICR-IACPR/SICI-GISE/SIBioC/] SIC/SICOA/SID/SIF/SIMEU/SIMG/SIMI/SISA Joint Consensus Document on cholesterol and cardiovascular risk: Diagnostic-therapeutic pathway in Italy. Eur Heart J Suppl 2017; 19(Suppl. D): D3-D54.
[http://dx.doi.org/10.1093/eurheartj/sux029 ] [PMID: 28751833]
[33]
Tsai IJ, Chen CW, Tsai SY, Wang PY, Owaga E, Hsieh RH. Curcumin supplementation ameliorated vascular dysfunction and improved antioxidant status in rats fed a high-sucrose, high-fat diet. Appl Physiol Nutr Metab 2018; 43(7): 669-76.
[http://dx.doi.org/10.1139/apnm-2017-0670 ] [PMID: 29378153]
[34]
Bulboacă AD, Bolboacă S, Suci S. Protective effect of curcumin in fructose-induced metabolic syndrome and in streptozotocin-induced diabetes in rats. Iran J Basic Med Sci 2016; 19(6): 585-93.
[PMID: 27482338]
[35]
Yan C, Zhang Y, Zhang X, Aa J, Wang G, Xie Y. Curcumin regulates endogenous and exogenous metabolism via Nrf2-FXR-LXR pathway in NAFLD mice. Biomed Pharmacother 2018; 105: 274-81.
[http://dx.doi.org/10.1016/j.biopha.2018.05.135 ] [PMID: 29860219]
[36]
Yoshida M, McKeown NM, Rogers G, et al. Surrogate markers of insulin resistance are associated with consumption of sugar-sweetened drinks and fruit juice in middle and older-aged adults. J Nutr 2007; 137(9): 2121-7.
[http://dx.doi.org/10.1093/jn/137.9.2121 ] [PMID: 17709452]
[37]
Miller JJ, Shih HA, Andronesi OC, Cahill DP. Isocitrate dehydrogenase-mutant glioma: Evolving clinical and therapeutic implications. Cancer 2017; 123(23): 4535-46.
[http://dx.doi.org/10.1002/cncr.31039 ] [PMID: 28980701]
[38]
Tomilov A, Tomilova N, Shan Y, et al. p46Shc inhibits thiolase and lipid oxidation in mitochondria. J Biol Chem 2016; 291(24): 12575-85.
[http://dx.doi.org/10.1074/jbc.M115.695577 ] [PMID: 27059956]
[39]
Paulsen KE, Orville AM, Frerman FE, Lipscomb JD, Stankovich MT. Redox properties of electron-transfer flavoprotein ubiquinone oxidoreductase as determined by EPR-spectroelectrochemistry. Biochemistry 1992; 31(47): 11755-61.
[http://dx.doi.org/10.1021/bi00162a012 ] [PMID: 1332770]
[40]
Neupane P, Bhuju S, Thapa N, Bhattarai HK. ATP synthase: Structure, function and inhibition. Biomol Concepts 2019; 10(1): 1-10.
[http://dx.doi.org/10.1515/bmc-2019-0001 ] [PMID: 30888962]
[41]
Wu J, Zhou D, Deng C, Wu X, Long L, Xiong Y. Characterization of porcine ENO3: Genomic and cDNA structure, polymorphism and expression. Genet Sel Evol 2008; 40(5): 563-79.
[http://dx.doi.org/10.1186/1297-9686-40-5-563 ] [PMID: 18694551]
[42]
Gugliucci A. Formation of fructose-mediated advanced glycation end products and their roles in metabolic and inflammatory diseases. Adv Nutr 2017; 8(1): 54-62.
[http://dx.doi.org/10.3945/an.116.013912 ] [PMID: 28096127]
[43]
Peppa M, Raptis SA. Advanced glycation end products and cardiovascular disease. Curr Diabetes Rev 2008; 4(2): 92-100.
[http://dx.doi.org/10.2174/157339908784220732 ] [PMID: 18473756]
[44]
Jandeleit-Dahm K, Watson A, Soro-Paavonen A. The AGE/RAGE axis in diabetes-accelerated atherosclerosis. Clin Exp Pharmacol Physiol 2008; 35(3): 329-34.
[http://dx.doi.org/10.1111/j.1440-1681.2007.04875.x ] [PMID: 18290873]
[45]
Mastrocola R, Nigro D, Cento AS, Chiazza F, Collino M, Aragno M. High-fructose intake as risk factor for neurodegeneration: Key role for carboxy methyllysine accumulation in mice hippocampal neurons. Neurobiol Dis 2016; 89: 65-75.
[http://dx.doi.org/10.1016/j.nbd.2016.02.005 ] [PMID: 26851500]
[46]
Diguet N, Mallat Y, Ladouce R, et al. Muscle creatine kinase deficiency triggers both actin depolymerization and desmin disorganization by advanced glycation end products in dilated cardiomyopathy. J Biol Chem 2011; 286(40): 35007-19.
[http://dx.doi.org/10.1074/jbc.M111.252395 ] [PMID: 21768101]
[47]
Ise H, Yamasaki S, Sueyoshi K, Miura Y. Elucidation of GlcNAc-binding properties of type III intermediate filament proteins, using GlcNAc-bearing polymers. Genes Cells 2017; 22(10): 900-17.
[http://dx.doi.org/10.1111/gtc.12535 ] [PMID: 28898551]
[48]
Herrmann H, Aebi U. Intermediate filaments: Structure and assembly. Cold Spring Harb Perspect Biol 2016; 8(11): a018242.
[http://dx.doi.org/10.1101/cshperspect.a018242 ] [PMID: 27803112]
[49]
Zhang SJ, Sandström ME, Lanner JT, Thorell A, Westerblad H, Katz A. Activation of aconitase in mouse fast-twitch skeletal muscle during contraction-mediated oxidative stress. Am J Physiol Cell Physiol 2007; 293(3): C1154-9.
[http://dx.doi.org/10.1152/ajpcell.00110.2007 ] [PMID: 17615160]
[50]
Tretter L, Adam-Vizi V. Inhibition of Krebs cycle enzymes by hydrogen peroxide: A key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J Neurosci 2000; 20(24): 8972-9.
[http://dx.doi.org/10.1523/JNEUROSCI.20-24-08972.2000 ] [PMID: 11124972]
[51]
Wan W, Li H, Xiang J, et al. Aqueous extract of black maca prevents metabolism disorder via regulating the glycolysis/] gluconeogenesis-TCA Cycle and PPARα signaling activation in golden hamsters fed a high-fat, high-fructose diet. Front Pharmacol 2018; 9: 333.
[http://dx.doi.org/10.3389/fphar.2018.00333 ] [PMID: 29681858]
[52]
Chen CM, Wu YR, Chang KH. Altered aconitase 2 activity in Huntington’s disease peripheral blood cells and mouse model striatum. Int J Mol Sci 2017; 18(11): 1-14.
[http://dx.doi.org/10.3390/ijms18112480 ] [PMID: 29160844]
[53]
Piroli GG, Manuel AM, Clapper AC, et al. Succination is increased on select proteins in the brainstem of the NADH dehydrogenase (ubiquinone) Fe-S protein 4 (Ndufs4) knockout mouse, a model of leigh syndrome. Mol Cell Proteomics 2016; 15(2): 445-61.
[http://dx.doi.org/10.1074/mcp.M115.051516 ] [PMID: 26450614]
[54]
Rhein VF, Carroll J, Ding S, Fearnley IM, Walker JE. NDUFAF5 Hydroxylates NDUFS7 at an early stage in the assembly of human complex I. J Biol Chem 2016; 291(28): 14851-60.
[http://dx.doi.org/10.1074/jbc.M116.734970 ] [PMID: 27226634]
[55]
Agip AA, Blaza JN, Bridges HR, et al. Cryo-EM structures of complex I from mouse heart mitochondria in two biochemically defined states. Nat Struct Mol Biol 2018; 25(7): 548-56.
[http://dx.doi.org/10.1038/s41594-018-0073-1 ] [PMID: 29915388]
[56]
Head RA, Brown RM, Zolkipli Z, et al. Clinical and genetic spectrum of pyruvate dehydrogenase deficiency: Dihydrolipoamide acetyltransferase (E2) deficiency. Ann Neurol 2005; 58(2): 234-41.
[http://dx.doi.org/10.1002/ana.20550 ] [PMID: 16049940]
[57]
Chicco A, Soria A, Fainstein-Day P, Gutman R, Lombardo YB. Multiphasic metabolic changes in the heart of rats fed a sucrose-rich diet. Horm Metab Res 1994; 26(9): 397-403.
[http://dx.doi.org/10.1055/s-2007-1001717 ] [PMID: 7835821]
[58]
Wang Z, Xu D, She L, et al. Curcumin restrains hepatic glucose production by blocking cAMP/PKA signaling and reducing acetyl CoA accumulation in High-Fat Diet (HFD)-fed mice. Mol Cell Endocrinol 2018; 474: 127-36.
[http://dx.doi.org/10.1016/j.mce.2018.02.018 ] [PMID: 29499209]

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