Abstract
Zinc is an important micronutrient for mammalians, whereas free/labile zinc ion (Zn2+) level ([Zn2+]i) in cells can be detrimental if it is over the physiological range. The cellular [Zn2+]i is regulated by proteins, responsible for its influx (ZIP family) into cells or efflux (ZnT-family) from cells. In addition, it has been shown that there is a close relationship between cellular [Zn2+]i and increasing oxidative stress, and both are also responsible for the dysregulation of the excitation/contraction coupling in the heart. Although age-dependent changes in the structure and function of the left ventricle are closely related to fibrosis, cellular evidence showed the importance of mitochondria as a potential target for aging medicine. However, several studies have shown that zinc supplementation provides important improvements in the maintenance of cardiovascular disorders, and it is needed to know the exact role of [Zn2+]i and its transporters in aging heart function. Although there is very little information related to the role of Zn2+ transporters in mammalian aging, some studies have shown their importance in cardiovascular disorders including failing human heart. Since few studies examined the role of ZIP14 as an inflammation responsive transporter and amplified with aging, we demonstrated an important data on the ZIP14 status in organelles such as the sarcoplasmic reticulum and mitochondria in aging rat’s ventricular cardiomyocytes. As a summary, we discussed our data in the light of literature data as well.
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References
Anderson R, Lagnado A, Maggiorani D, Walaszczyk A, Dookun E, Chapman J, Birch J, Salmonowicz H, Ogrodnik M, Jurk D, Proctor C, Correia-Melo C, Victorelli S, Fielder E, Berlinguer-Palmini R, Owens A, Greaves LC, Kolsky KL, Parini A, Douin-Echinard V, LeBrasseur NK, Arthur HM, Tual-Chalot S, Schafer MJ, Roos CM, Miller JD, Robertson N, Mann J, Adams PD, Tchkonia T, Kirkland JL, Mialet-Perez J, Richardson GD, Passos JF (2019) Length-independent telomere damage drives post-mitotic cardiomyocyte senescence. The EMBO J 38 (5). https://doi.org/10.15252/embj.2018100492
Aydemir TB, Troche C, Kim MH, Cousins RJ (2016a) Hepatic ZIP14-mediated zinc transport contributes to endosomal insulin receptor trafficking and glucose metabolism. J Biol Chem 291(46):23939–23951. https://doi.org/10.1074/jbc.M116.748632
Aydemir TB, Troche C, Kim J, Kim MH, Teran OY, Leeuwenburgh C, Cousins RJ (2016b) Aging amplifies multiple phenotypic defects in mice with zinc transporter Zip14 (Slc39a14) deletion. Exp Gerontol 85:88–94. https://doi.org/10.1016/j.exger.2016.09.013
Barbieri M, Rizzo MR, Manzella D, Paolisso G (2001) Age-related insulin resistance: is it an obligatory finding? The lesson from healthy centenarians. Diabetes Metab Res Rev 17(1):19–26
Beal MF (2002) Oxidatively modified proteins in aging and disease. Free Radic Biol Med 32(9):797–803
Berg JM, Shi Y (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science (New York, NY) 271(5252):1081–1085
Bhashyam S, Parikh P, Bolukoglu H, Shannon AH, Porter JH, Shen YT, Shannon RP (2007) Aging is associated with myocardial insulin resistance and mitochondrial dysfunction. Am J Physiol Heart Circ Physiol 293(5):H3063–H3071. https://doi.org/10.1152/ajpheart.00163.2007
Billur D, Tuncay E, Okatan EN, Olgar Y, Durak AT, Degirmenci S, Can B, Turan B (2016) Interplay between cytosolic free Zn2+ and mitochondrion morphological changes in rat ventricular cardiomyocytes. Biol Trace Elem Res:1–12
Boengler K, Kosiol M, Mayr M, Schulz R, Rohrbach S (2017) Mitochondria and ageing: role in heart, skeletal muscle and adipose tissue. J Cachexia Sarcopenia Muscle 8(3):349–369. https://doi.org/10.1002/jcsm.12178
Borlaug BA, Kass DA (2006) Mechanisms of diastolic dysfunction in heart failure. Trends Cardiovasc Med 16(8):273–279. https://doi.org/10.1016/j.tcm.2006.05.003
Boudina S (2013) Cardiac aging and insulin resistance: could insulin/insulin-like growth factor (IGF) signaling be used as a therapeutic target? Curr Pharm Des 19(32):5684–5694
Bradford WH, Omens JH, Sheikh F (2017) Vinculin at the heart of aging. Ann Transl Med 5(3):62. https://doi.org/10.21037/atm.2017.01.65
Brown AM, Kristal BS, Effron MS, Shestopalov AI, Ullucci PA, Sheu KF, Blass JP, Cooper AJ (2000) Zn2+ inhibits alpha-ketoglutarate-stimulated mitochondrial respiration and the isolated alpha-ketoglutarate dehydrogenase complex. J Biol Chem 275(18):13441–13447
Cabrera AJ (2015) Zinc, aging, and immunosenescence: an overview. Pathobiol Aging Age Relat Dis 5:25592. https://doi.org/10.3402/pba.v5.25592
Capdor J, Foster M, Petocz P, Samman S (2013) Zinc and glycemic control: a meta-analysis of randomised placebo controlled supplementation trials in humans. J Trace Elem Med Biol 27(2):137–142. https://doi.org/10.1016/j.jtemb.2012.08.001
Carafoli E, Lehninger AL (1971) A survey of the interaction of calcium ions with mitochondria from different tissues and species. Biochem J 122(5):681–690
Chabosseau P, Tuncay E, Meur G, Bellomo EA, Hessels A, Hughes S, Johnson PR, Bugliani M, Marchetti P, Turan B, Lyon AR, Merkx M, Rutter GA (2014) Mitochondrial and ER-targeted eCALWY probes reveal high levels of free Zn2+. ACS Chem Biol 9(9):2111–2120. https://doi.org/10.1021/cb5004064
Chiao YA, Rabinovitch PS (2015) The aging heart. Cold Spring Harb Perspect Med 5(9):a025148. https://doi.org/10.1101/cshperspect.a025148
Chu A, Holdaway C, Varma T, Petocz P, Samman S (2018) Lower serum zinc concentration despite higher dietary zinc intake in athletes: a systematic review and meta-analysis. Sports Med 48(2):327–336. https://doi.org/10.1007/s40279-017-0818-8
Chung KT, Wong TY, Wei CI, Huang YW, Lin Y (1998) Tannins and human health: a review. Crit Rev Food Sci Nutr 38(6):421–464. https://doi.org/10.1080/10408699891274273
Corsetti G, Pasini E, D’Antona G, Nisoli E, Flati V, Assanelli D, Dioguardi FS, Bianchi R (2008) Morphometric changes induced by amino acid supplementation in skeletal and cardiac muscles of old mice. Am J Cardiol 101(11A):26E–34E. https://doi.org/10.1016/j.amjcard.2008.02.078
Cousins RJ, Liuzzi JP, Lichten LA (2006) Mammalian zinc transport, trafficking, and signals. J Biol Chem 281(34):24085–24089. https://doi.org/10.1074/jbc.R600011200
Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, MacCoss MJ, Gollahon K, Martin GM, Loeb LA, Ladiges WC, Rabinovitch PS (2009) Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 119(21):2789–2797. https://doi.org/10.1161/circulationaha.108.822403
Dai DF, Chiao YA, Marcinek DJ, Szeto HH, Rabinovitch PS (2014) Mitochondrial oxidative stress in aging and healthspan. Longev Healthspan 3:6. https://doi.org/10.1186/2046-2395-3-6
Degirmenci S, Olgar Y, Durak A, Tuncay E, Turan B (2018) Cytosolic increased labile Zn(2+) contributes to arrhythmogenic action potentials in left ventricular cardiomyocytes through protein thiol oxidation and cellular ATP depletion. J Trace Elements Med Biol 48:202–212. https://doi.org/10.1016/j.jtemb.2018.04.014
Denton RM, McCormack JG, Edgell NJ (1980) Role of calcium ions in the regulation of intramitochondrial metabolism. Effects of Na+, Mg2+ and ruthenium red on the Ca2+−stimulated oxidation of oxoglutarate and on pyruvate dehydrogenase activity in intact rat heart mitochondria. Biochem J 190(1):107–117
Dey S, DeMazumder D, Sidor A, Foster DB, O’Rourke B (2018) Mitochondrial ROS drive sudden cardiac death and chronic proteome remodeling in heart failure. Circ Res 123(3):356–371. https://doi.org/10.1161/circresaha.118.312708
Dibb KM, Rueckschloss U, Eisner DA, Isenberg G, Trafford AW (2004) Mechanisms underlying enhanced cardiac excitation contraction coupling observed in the senescent sheep myocardium. J Mol Cell Cardiol 37(6):1171–1181. https://doi.org/10.1016/j.yjmcc.2004.09.005
Doets EL, Cavelaars AE, Dhonukshe-Rutten RA, van’t Veer P, de Groot LC (2012) Explaining the variability in recommended intakes of folate, vitamin B12, iron and zinc for adults and elderly people. Public Health Nutr 15(5):906–915. https://doi.org/10.1017/s1368980011002643
Douaud G, Groves AR, Tamnes CK, Westlye LT, Duff EP, Engvig A, Walhovd KB, James A, Gass A, Monsch AU, Matthews PM, Fjell AM, Smith SM, Johansen-Berg H (2014) A common brain network links development, aging, and vulnerability to disease. Proc Natl Acad Sci 111(49):17648. https://doi.org/10.1073/pnas.1410378111
Eby GA, Halcomb WW (2006) High-dose zinc to terminate angina pectoris: a review and hypothesis for action by ICAM inhibition. Med Hypotheses 66(1):169–172. https://doi.org/10.1016/j.mehy.2005.06.013
Efeovbokhan N, Bhattacharya SK, Ahokas RA, Sun Y, Guntaka RV, Gerling IC, Weber KT (2014) Zinc and the prooxidant heart failure phenotype. J Cardiovasc Pharmacol 64(4):393–400. https://doi.org/10.1097/fjc.0000000000000125
Eide DJ (2011) The oxidative stress of zinc deficiency. Metallomics 3(11):1124–1129. https://doi.org/10.1039/c1mt00064k
Eisner V, Cupo RR, Gao E, Csordas G, Slovinsky WS, Paillard M, Cheng L, Ibetti J, Chen SR, Chuprun JK, Hoek JB, Koch WJ, Hajnoczky G (2017) Mitochondrial fusion dynamics is robust in the heart and depends on calcium oscillations and contractile activity. Proc Natl Acad Sci U S A 114(5):E859–e868. https://doi.org/10.1073/pnas.1617288114
Ellis CD, Wang F, MacDiarmid CW, Clark S, Lyons T, Eide DJ (2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 166(3):325–335. https://doi.org/10.1083/jcb.200401157
Elmore SP, Qian T, Grissom SF, Lemasters JJ (2001) The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J 15(12):2286–2287. https://doi.org/10.1096/fj.01-0206fje
Evans GW (1986) Zinc and its deficiency diseases. Clin Physiol Biochem 4(1):94–98
Ferrucci L, Levine ME, Kuo PL, Simonsick EM (2018) Time and the metrics of aging. Circ Res 123(7):740–744. https://doi.org/10.1161/circresaha.118.312816
Fosmire GJ (1990) Zinc toxicity. Am J Clin Nutr 51(2):225–227. https://doi.org/10.1093/ajcn/51.2.225
Foster M, Petocz P, Samman S (2010) Effects of zinc on plasma lipoprotein cholesterol concentrations in humans: a meta-analysis of randomised controlled trials. Atherosclerosis 210(2):344–352. https://doi.org/10.1016/j.atherosclerosis.2009.11.038
Fujishiro H, Doi M, Enomoto S, Himeno S (2011) High sensitivity of RBL-2H3 cells to cadmium and manganese: an implication of the role of ZIP8. Metallomics 3(7):710–718. https://doi.org/10.1039/c1mt00020a
Fujishiro H, Yano Y, Takada Y, Tanihara M, Himeno S (2012) Roles of ZIP8, ZIP14, and DMT1 in transport of cadmium and manganese in mouse kidney proximal tubule cells. Metallomics 4(7):700–708. https://doi.org/10.1039/c2mt20024d
Fukada T, Kambe T (2018) Welcome to the world of zinc signaling. Int J Mol Sci 19(3). https://doi.org/10.3390/ijms19030785
Gartmann L, Wex T, Grungreiff K, Reinhold D, Kalinski T, Malfertheiner P, Schutte K (2018) Expression of zinc transporters ZIP4, ZIP14 and ZnT9 in hepatic carcinogenesis-an immunohistochemical study. J Trace Elements Med Biol 49:35–42. https://doi.org/10.1016/j.jtemb.2018.04.034
Giacconi R, Malavolta M, Costarelli L, Busco F, Galeazzi R, Bernardini G, Gasparini N, Mocchegiani E (2012) Comparison of intracellular zinc signals in nonadherent lymphocytes from young-adult and elderly donors: role of zinc transporters (Zip family) and proinflammatory cytokines. J Nutr Biochem 23(10):1256–1263. https://doi.org/10.1016/j.jnutbio.2011.07.005
Giannoglou GD, Konstantinou DM, Kovatsi L, Chatzizisis YS, Mikhailidis DP (2010) Association of reduced zinc status with angiographically severe coronary atherosclerosis: a pilot study. Angiology 61(5):449–455. https://doi.org/10.1177/0003319710366702
Giorgi C, Baldassari F, Bononi A, Bonora M, De Marchi E, Marchi S, Missiroli S, Patergnani S, Rimessi A, Suski JM, Wieckowski MR, Pinton P (2012) Mitochondrial Ca(2+) and apoptosis. Cell Calcium 52(1):36–43. https://doi.org/10.1016/j.ceca.2012.02.008
Gottdiener JS, McClelland RL, Marshall R, Shemanski L, Furberg CD, Kitzman DW, Cushman M, Polak J, Gardin JM, Gersh BJ, Aurigemma GP, Manolio TA (2002) Outcome of congestive heart failure in elderly persons: influence of left ventricular systolic function. The Cardiovascular Health Study. Ann Intern Med 137(8):631–639
Groth C, Sasamura T, Khanna MR, Whitley M, Fortini ME (2013) Protein trafficking abnormalities in Drosophila tissues with impaired activity of the ZIP7 zinc transporter Catsup. Development 140(14):3018–3027. https://doi.org/10.1242/dev.088336
Grubman A, Lidgerwood GE, Duncan C, Bica L, Tan JL, Parker SJ, Caragounis A, Meyerowitz J, Volitakis I, Moujalled D, Liddell JR, Hickey JL, Horne M, Longmuir S, Koistinaho J, Donnelly PS, Crouch PJ, Tammen I, White AR, Kanninen KM (2014) Deregulation of subcellular biometal homeostasis through loss of the metal transporter, Zip7, in a childhood neurodegenerative disorder. Acta Neuropathol Commun 2:25. https://doi.org/10.1186/2051-5960-2-25
Guthrie GJ, Aydemir TB, Troche C, Martin AB, Chang SM, Cousins RJ (2015) Influence of ZIP14 (slc39A14) on intestinal zinc processing and barrier function. Am J Physiol Gastrointest Liver Physiol 308(3):G171–G178. https://doi.org/10.1152/ajpgi.00021.2014
Haase H, Rink L (2014) Zinc signals and immune function. Biofactors 40(1):27–40. https://doi.org/10.1002/biof.1114
Hamacher-Brady A, Brady NR (2016) Mitophagy programs: mechanisms and physiological implications of mitochondrial targeting by autophagy. Cell Mol Life Sci 73(4):775–795. https://doi.org/10.1007/s00018-015-2087-8
Hammadah M, Al Mheid I, Wilmot K, Ramadan R, Abdelhadi N, Alkhoder A, Obideen M, Pimple PM, Levantsevych O, Kelli HM, Shah A, Sun YV, Pearce B, Kutner M, Long Q, Ward L, Ko YA, Hosny Mohammed K, Lin J, Zhao J, Bremner JD, Kim J, Waller EK, Raggi P, Sheps D, Quyyumi AA, Vaccarino V (2017) Telomere shortening, regenerative capacity, and cardiovascular outcomes. Circ Res 120(7):1130–1138. https://doi.org/10.1161/circresaha.116.309421
Hara T, Takeda TA, Takagishi T, Fukue K, Kambe T, Fukada T (2017) Physiological roles of zinc transporters: molecular and genetic importance in zinc homeostasis. J Physiol Sci 67(2):283–301. https://doi.org/10.1007/s12576-017-0521-4
Heidenreich PA, Albert NM, Allen LA, Bluemke DA, Butler J, Fonarow GC, Ikonomidis JS, Khavjou O, Konstam MA, Maddox TM, Nichol G, Pham M, Pina IL, Trogdon JG (2013) Forecasting the impact of heart failure in the United States: a policy statement from the American Heart Association. Circ Heart Fail 6(3):606–619. https://doi.org/10.1161/HHF.0b013e318291329a
Herraiz-Martinez A, Alvarez-Garcia J, Llach A, Molina CE, Fernandes J, Ferrero-Gregori A, Rodriguez C, Vallmitjana A, Benitez R, Padro JM, Martinez-Gonzalez J, Cinca J, Hove-Madsen L (2015) Ageing is associated with deterioration of calcium homeostasis in isolated human right atrial myocytes. Cardiovasc Res 106(1):76–86. https://doi.org/10.1093/cvr/cvv046
Hershfinkel M, Moran A, Grossman N, Sekler I (2001) A zinc-sensing receptor triggers the release of intracellular Ca2+ and regulates ion transport. Proc Natl Acad Sci U S A 98(20):11749–11754. https://doi.org/10.1073/pnas.201193398
Hogstrand C, Kille P, Nicholson RI, Taylor KM (2009) Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol Med 15(3):101–111. https://doi.org/10.1016/j.molmed.2009.01.004
Hojyo S, Fukada T (2016) Zinc transporters and signaling in physiology and pathogenesis. Arch Biochem Biophys 611:43–50. https://doi.org/10.1016/j.abb.2016.06.020
Hojyo S, Fukada T, Shimoda S, Ohashi W, Bin BH, Koseki H, Hirano T (2011) The zinc transporter SLC39A14/ZIP14 controls G-protein coupled receptor-mediated signaling required for systemic growth. PLoS One 6(3):e18059. https://doi.org/10.1371/journal.pone.0018059
Huang L, Kirschke CP, Zhang Y, Yu YY (2005) The ZIP7 gene (Slc39a7) encodes a zinc transporter involved in zinc homeostasis of the Golgi apparatus. J Biol Chem 280(15):15456–15463. https://doi.org/10.1074/jbc.M412188200
Jackson MJ, Jones DA, Edwards RH (1982) Tissue zinc levels as an index of body zinc status. Clin Physiol 2(4):333–343
Jang Y, Wang H, Xi J, Mueller RA, Norfleet EA, Xu Z (2007) NO mobilizes intracellular Zn2+ via cGMP/PKG signaling pathway and prevents mitochondrial oxidant damage in cardiomyocytes. Cardiovasc Res 75(2):426–433. https://doi.org/10.1016/j.cardiores.2007.05.015
Jenkitkasemwong S, Wang CY, Coffey R, Zhang W, Chan A, Biel T, Kim JS, Hojyo S, Fukada T, Knutson MD (2015) SLC39A14 is required for the development of hepatocellular iron overload in murine models of hereditary hemochromatosis. Cell Metab 22(1):138–150. https://doi.org/10.1016/j.cmet.2015.05.002
Jeong EM, Chung J, Liu H, Go Y, Gladstein S, Farzaneh-Far A, Lewandowski ED, Dudley SC, Jr (2016) Role of mitochondrial oxidative stress in glucose tolerance, insulin resistance, and cardiac diastolic dysfunction. J Am Heart Assoc 5(5). https://doi.org/10.1161/jaha.115.003046
Jiang D, Sullivan PG, Sensi SL, Steward O, Weiss JH (2001) Zn(2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal mitochondria. J Biol Chem 276(50):47524–47529. https://doi.org/10.1074/jbc.M108834200
Jiang S, Yan K, Sun B, Gao S, Yang X, Ni Y, Ma W, Zhao R (2018) Long-term high-fat diet decreases hepatic Iron storage associated with suppressing TFR2 and ZIP14 expression in rats. J Agric Food Chem 66(44):11612–11621. https://doi.org/10.1021/acs.jafc.8b02974
Joseph LC, Barca E, Subramanyam P, Komrowski M, Pajvani U, Colecraft HM, Hirano M, Morrow JP (2017) Correction: inhibition of NAPDH oxidase 2 (NOX2) prevents oxidative stress and mitochondrial abnormalities caused by saturated fat in cardiomyocytes. PLoS One 12(3):e0174525. https://doi.org/10.1371/journal.pone.0174525
Joshi DC, Bakowska JC (2011) Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. J Visual Exp (51). https://doi.org/10.3791/2704
Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C (2005) Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 19(3):419–421. https://doi.org/10.1096/fj.04-2622fje
Jurowski K, Szewczyk B, Nowak G, Piekoszewski W (2014) Biological consequences of zinc deficiency in the pathomechanisms of selected diseases. J Biol Inorg Chem 19(7):1069–1079. https://doi.org/10.1007/s00775-014-1139-0
Kambe T, Geiser J, Lahner B, Salt DE, Andrews GK (2008) Slc39a1 to 3 (subfamily II) Zip genes in mice have unique cell-specific functions during adaptation to zinc deficiency. Am J Physiol Regul Integr Comp Physiol 294(5):R1474–R1481. https://doi.org/10.1152/ajpregu.00130.2008
Kambe T, Fukue K, Ishida R, Miyazaki S (2015) Overview of inherited zinc deficiency in infants and children. J Nutr Sci Vitaminol 61(Suppl):S44–S46. https://doi.org/10.3177/jnsv.61.S44
Kannel WB (1999) Current status of the epidemiology of heart failure. Curr Cardiol Rep 1(1):11–19
Kennedy BK, Steffen KK, Kaeberlein M (2007) Ruminations on dietary restriction and aging. Cell Mol Life Sci 64(11):1323–1328. https://doi.org/10.1007/s00018-007-6470-y
Kimura T, Kambe T (2016) The functions of metallothionein and ZIP and ZnT transporters: an overview and perspective. Int J Mol Sci 17(3):336. https://doi.org/10.3390/ijms17030336
King JC, Shames DM, Woodhouse LR (2000) Zinc homeostasis in humans. J Nutr 130(5S Suppl):1360S–1366S. https://doi.org/10.1093/jn/130.5.1360S
Kirkwood TB (2005) Understanding the odd science of aging. Cell 120(4):437–447. https://doi.org/10.1016/j.cell.2005.01.027
Kumari A, Singh KP, Mandal A, Paswan RK, Sinha P, Das P, Ali V, Bimal S, Lal CS (2017) Intracellular zinc flux causes reactive oxygen species mediated mitochondrial dysfunction leading to cell death in Leishmania donovani. PLoS One 12(6):e0178800. https://doi.org/10.1371/journal.pone.0178800
Lee HY, Oh BH (2010) Aging and arterial stiffness. Circ J 74(11):2257–2262
Lesnefsky EJ, Chen Q, Hoppel CL (2016) Mitochondrial metabolism in aging heart. Circ Res 118(10):1593–1611. https://doi.org/10.1161/circresaha.116.307505
Liuzzi JP, Lichten LA, Rivera S, Blanchard RK, Aydemir TB, Knutson MD, Ganz T, Cousins RJ (2005) Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci U S A 102(19):6843–6848. https://doi.org/10.1073/pnas.0502257102
Mansouri A, Muller FL, Liu Y, Ng R, Faulkner J, Hamilton M, Richardson A, Huang TT, Epstein CJ, Van Remmen H (2006) Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 127(3):298–306. https://doi.org/10.1016/j.mad.2005.11.004
Maret W (2013) Zinc and human disease. Met Ions Life Sci 13:389–414. https://doi.org/10.1007/978-94-007-7500-8_12
McCord MC, Aizenman E (2014) The role of intracellular zinc release in aging, oxidative stress, and Alzheimer’s disease. Front Aging Neurosci 6:77. https://doi.org/10.3389/fnagi.2014.00077
Mirzaei H, Di Biase S, Longo VD (2016) Dietary interventions, cardiovascular aging, and disease: animal models and human studies. Circ Res 118(10):1612–1625. https://doi.org/10.1161/circresaha.116.307473
Mishra P, Chan DC (2016) Metabolic regulation of mitochondrial dynamics. J Cell Biol 212(4):379–387. https://doi.org/10.1083/jcb.201511036
Miyamoto S, Howes AL, Adams JW, Dorn GW 2nd, Brown JH (2005) Ca2+ dysregulation induces mitochondrial depolarization and apoptosis: role of Na+/Ca2+ exchanger and AKT. J Biol Chem 280(46):38505–38512. https://doi.org/10.1074/jbc.M505223200
Mocchegiani E, Malavolta M, Costarelli L, Giacconi R, Cipriano C, Piacenza F, Tesei S, Basso A, Pierpaoli S, Lattanzio F (2010) Zinc, metallothioneins and immunosenescence. Proc Nutr Soc 69(3):290–299. https://doi.org/10.1017/s0029665110001862
Moreira OC, Estebanez B, Martinez-Florez S, de Paz JA, Cuevas MJ, Gonzalez-Gallego J (2017) Mitochondrial function and mitophagy in the elderly: effects of exercise. Oxidative Med Cell Longev 2017:2012798. https://doi.org/10.1155/2017/2012798
Mursu J, Robien K, Harnack LJ, Park K, Jacobs DR Jr (2011) Dietary supplements and mortality rate in older women: the Iowa women’s health study. Arch Intern Med 171(18):1625–1633. https://doi.org/10.1001/archinternmed.2011.445
Nazarewicz RR, Dikalova A, Bikineyeva A, Ivanov S, Kirilyuk IA, Grigor’ev IA, Dikalov SI (2013a) Does scavenging of mitochondrial superoxide attenuate cancer prosurvival signaling pathways? Antioxid Redox Signal 19(4):344–349. https://doi.org/10.1089/ars.2013.5185
Nazarewicz RR, Dikalova AE, Bikineyeva AT, Ivanov SV, Dikalov SI (2013b) Mitochondria-targeted antioxidant mitoTEMPO inhibits glycolysis and induces melanoma cell death by blocking ROSsensitive survival and metabolic pathways. 27 (1_supplement):793.797–793.797. https://doi.org/10.1096/fasebj.27.1_supplement.793.7
Nomura N, Nagase T, Miyajima N, Sazuka T, Tanaka A, Sato S, Seki N, Kawarabayasi Y, Ishikawa K, Tabata S (1994) Prediction of the coding sequences of unidentified human genes. II. The coding sequences of 40 new genes (KIAA0041-KIAA0080) deduced by analysis of cDNA clones from human cell line KG-1 (supplement). DNA Res 1(5):251–262
Ohashi W, Kimura S, Iwanaga T, Furusawa Y, Irie T, Izumi H, Watanabe T, Hijikata A, Hara T, Ohara O, Koseki H, Sato T, Robine S, Mori H, Hattori Y, Watarai H, Mishima K, Ohno H, Hase K, Fukada T (2016) Zinc transporter SLC39A7/ZIP7 promotes intestinal epithelial self-renewal by resolving ER stress. PLoS Genet 12(10):e1006349. https://doi.org/10.1371/journal.pgen.1006349
Olgar Y, Turan B (2018) A SGLT2 inhibitor dapagliflozin comparison with insulin exerts important effects on Zn2+−transporters in cardiomyocytes from insulin-resistant metabolic syndrome rats through inhibition of oxidative stress. Can J Physiol Pharmacol. https://doi.org/10.1139/cjpp-2018-0466
Olgar Y, Degirmenci S, Durak A, Billur D, Can B, Kayki-Mutlu G, Arioglu-Inan E, Turan B (2018a) Aging related functional and structural changes in the heart and aorta: MitoTEMPO improves aged-cardiovascular performance. Exp Gerontol 110:172–181. https://doi.org/10.1016/j.exger.2018.06.012
Olgar Y, Durak A, Tuncay E, Bitirim CV, Ozcinar E, Inan MB, Tokcaer-Keskin Z, Akcali KC, Akar AR, Turan B (2018b) Increased free Zn(2+) correlates induction of sarco(endo)plasmic reticulum stress via altered expression levels of Zn(2+) -transporters in heart failure. J Cell Mol Med 22(3):1944–1956. https://doi.org/10.1111/jcmm.13480
de Oliveira Otto MC, Alonso A, Lee DH, Delclos GL, Jenny NS, Jiang R, Lima JA, Symanski E, Jacobs DR Jr, Nettleton JA (2011) Dietary micronutrient intakes are associated with markers of inflammation but not with markers of subclinical atherosclerosis. J Nutr 141(8):1508–1515. https://doi.org/10.3945/jn.111.138115
Oster O, Dahm M, Oelert H (1993) Element concentrations (selenium, copper, zinc, iron, magnesium, potassium, phosphorous) in heart tissue of patients with coronary heart disease correlated with physiological parameters of the heart. Eur Heart J 14(6):770–774
Owada T, Yamauchi H, Saitoh SI, Miura S, Machii H, Takeishi Y (2017) Resolution of mitochondrial oxidant stress improves aged-cardiovascular performance. Coron Artery Dis 28(1):33–43. https://doi.org/10.1097/mca.0000000000000434
Palmer BM, Vogt S, Chen Z, Lachapelle RR, Lewinter MM (2006) Intracellular distributions of essential elements in cardiomyocytes. J Struct Biol 155(1):12–21. https://doi.org/10.1016/j.jsb.2005.11.017
Pan Z, Choi S, Ouadid-Ahidouch H, Yang JM, Beattie JH, Korichneva I (2017) Zinc transporters and dysregulated channels in cancers. Front Biosci (Landmark edition) 22:623–643
Paolisso G, Tagliamonte MR, Rizzo MR, Scheen A, D’Onofrio F, Lefebvre P (1999) [Is aging associated with a diminution of insulin sensitivity? Roles of IGF1 and dehydroepiandrosterone]. J Ann Diabetol Hotel Dieu :63–74
Payne BA, Chinnery PF (2015) Mitochondrial dysfunction in aging: much progress but many unresolved questions. Biochim Biophys Acta 1847(11):1347–1353. https://doi.org/10.1016/j.bbabio.2015.05.022
Pinilla-Tenas JJ, Sparkman BK, Shawki A, Illing AC, Mitchell CJ, Zhao N, Liuzzi JP, Cousins RJ, Knutson MD, Mackenzie B (2011) Zip14 is a complex broad-scope metal-ion transporter whose functional properties support roles in the cellular uptake of zinc and nontransferrin-bound iron. Am J Physiol Cell Physiol 301(4):C862–C871. https://doi.org/10.1152/ajpcell.00479.2010
Pitt SJ, Stewart AJ (2015) Examining a new role for zinc in regulating calcium release in cardiac muscle. Biochem Soc Trans 43(3):359–363. https://doi.org/10.1042/bst20140285
Pivovarova NB, Stanika RI, Kazanina G, Villanueva I, Andrews SB (2014) The interactive roles of zinc and calcium in mitochondrial dysfunction and neurodegeneration. J Neurochem 128(4):592–602. https://doi.org/10.1111/jnc.12489
Plum LM, Rink L, Haase H (2010) The essential toxin: impact of zinc on human health. Int J Environ Res Public Health 7(4):1342–1365. https://doi.org/10.3390/ijerph7041342
Prasad AS (2008) Clinical, immunological, anti-inflammatory and antioxidant roles of zinc. Exp Gerontol 43(5):370–377. https://doi.org/10.1016/j.exger.2007.10.013
Prasad AS (2013) Discovery of human zinc deficiency: its impact on human health and disease. Adv Nutr (Bethesda, Md) 4(2):176–190. https://doi.org/10.3945/an.112.003210
Prasad AS, Miale A Jr, Farid Z, Sandstead HH, Schulert AR (1990) Clinical and experimental. Zinc metabolism in patients with the syndrome of iron deficiency anemia, hepatosplenomegaly, dwarfism, and hypogonadism. 1963. J Lab Clin Med 116(5):737–749
Prasad AS, Fitzgerald JT, Hess JW, Kaplan J, Pelen F, Dardenne M (1993) Zinc deficiency in elderly patients. Nutrition 9(3):218–224
Puche JE, Garcia-Fernandez M, Muntane J, Rioja J, Gonzalez-Baron S, Castilla Cortazar I (2008) Low doses of insulin-like growth factor-I induce mitochondrial protection in aging rats. Endocrinology 149(5):2620–2627. https://doi.org/10.1210/en.2007-1563
Quarles EK, Dai DF, Tocchi A, Basisty N, Gitari L, Rabinovitch PS (2015) Quality control systems in cardiac aging. Ageing Res Rev 23(Pt A):101–115. https://doi.org/10.1016/j.arr.2015.02.003
van Raaij SEG, Srai SKS, Swinkels DW, van Swelm RPL (2019) Iron uptake by ZIP8 and ZIP14 in human proximal tubular epithelial cells. Biometals 32(2):211–226. https://doi.org/10.1007/s10534-019-00183-7
Rajapakse D, Curtis T, Chen M, Xu H (2017) Zinc protects oxidative stress-induced RPE death by reducing mitochondrial damage and preventing lysosome rupture. Oxidative Med Cell Longev 2017:6926485. https://doi.org/10.1155/2017/6926485
Raza M, Deshpande LS, Blair RE, Carter DS, Sombati S, DeLorenzo RJ (2007) Aging is associated with elevated intracellular calcium levels and altered calcium homeostatic mechanisms in hippocampal neurons. Neurosci Lett 418(1):77–81. https://doi.org/10.1016/j.neulet.2007.03.005
Ristow M (2012) Interview with Michael Ristow. Aging 4(1):2. https://doi.org/10.18632/aging.100430
de Rivera C, Shukitt-Hale B, Joseph JA, Mendelson JR (2006) The effects of antioxidants in the senescent auditory cortex. Neurobiol Aging 27(7):1035–1044. https://doi.org/10.1016/j.neurobiolaging.2005.05.003
Rizzuto R, Simpson AW, Brini M, Pozzan T (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358(6384):325–327. https://doi.org/10.1038/358325a0
Romanjuk A, Lyndin M, Moskalenko R, Gortinskaya O, Lyndina Y (2016) The role of heavy metal salts in pathological biomineralization of breast cancer tissue. Adv Clin Exp Med 25(5):907–910. https://doi.org/10.17219/acem/34472
Santulli G, Xie W, Reiken SR, Marks AR (2015) Mitochondrial calcium overload is a key determinant in heart failure. Proc Natl Acad Sci U S A 112(36):11389–11394. https://doi.org/10.1073/pnas.1513047112
Schmucker DL, Sachs HG (1985) Age-dependent alterations in rat ventricular myocardium: a quantitative analysis. Mech Ageing Dev 31(1):89–101
Schocken DD (2000) Epidemiology and risk factors for heart failure in the elderly. Clin Geriatr Med 16(3):407–418
Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science (New York, NY) 308(5730):1909–1911. https://doi.org/10.1126/science.1106653
Senni M, Tribouilloy CM, Rodeheffer RJ, Jacobsen SJ, Evans JM, Bailey KR, Redfield MM (1999) Congestive heart failure in the community: trends in incidence and survival in a 10-year period. Arch Intern Med 159(1):29–34
Sensi SL, Ton-That D, Sullivan PG, Jonas EA, Gee KR, Kaczmarek LK, Weiss JH (2003) Modulation of mitochondrial function by endogenous Zn2+ pools. Proc Natl Acad Sci U S A 100(10):6157–6162. https://doi.org/10.1073/pnas.1031598100
Sharpley MS, Hirst J (2006) The inhibition of mitochondrial complex I (NADH:ubiquinone oxidoreductase) by Zn2+. J Biol Chem 281(46):34803–34809. https://doi.org/10.1074/jbc.M607389200
Shioi T, Inuzuka Y (2012) Aging as a substrate of heart failure. J Cardiol 60(6):423–428. https://doi.org/10.1016/j.jjcc.2012.07.015
Soinio M, Marniemi J, Laakso M, Pyorala K, Lehto S, Ronnemaa T (2007) Serum zinc level and coronary heart disease events in patients with type 2 diabetes. Diabetes Care 30(3):523–528. https://doi.org/10.2337/dc06-1682
St Croix CM, Wasserloos KJ, Dineley KE, Reynolds IJ, Levitan ES, Pitt BR (2002) Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/thionein. Am J Physiol Lung Cell Mol Physiol 282(2):L185–L192. https://doi.org/10.1152/ajplung.00267.2001
Stanley WC, Recchia FA, Lopaschuk GD (2005) Myocardial substrate metabolism in the normal and failing heart. Physiol Rev 85(3):1093–1129. https://doi.org/10.1152/physrev.00006.2004
Stefanidou M, Maravelias C, Dona A, Spiliopoulou C (2006) Zinc: a multipurpose trace element. Arch Toxicol 80(1):1–9. https://doi.org/10.1007/s00204-005-0009-5
Strait JB, Lakatta EG (2012) Aging-associated cardiovascular changes and their relationship to heart failure. Heart Fail Clin 8(1):143–164. https://doi.org/10.1016/j.hfc.2011.08.011
Tate EL, Herbener GH (1976) A morphometric study of the density of mitochondrial cristae in heart and liver of aging mice. J Gerontol 31(2):129–134
Tatsumi T, Fliss H (1994) Hypochlorous acid mobilizes intracellular zinc in isolated rat heart myocytes. J Mol Cell Cardiol 26(4):471–479. https://doi.org/10.1006/jmcc.1994.1058
Taylor KM, Nicholson RI (2003) The LZT proteins; the LIV-1 subfamily of zinc transporters. Biochim Biophys Acta 1611(1–2):16–30
Taylor KM, Hiscox S, Nicholson RI, Hogstrand C, Kille P (2012) Protein kinase CK2 triggers cytosolic zinc signaling pathways by phosphorylation of zinc channel ZIP7. Sci Signal 5(210):ra11. https://doi.org/10.1126/scisignal.2002585
Thayer SA, Miller RJ (1990) Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro. J Physiol 425:85–115
Tominaga K, Kagata T, Johmura Y, Hishida T, Nishizuka M, Imagawa M (2005) SLC39A14, a LZT protein, is induced in adipogenesis and transports zinc. FEBS J 272(7):1590–1599. https://doi.org/10.1111/j.1742-4658.2005.04580.x
Tuncay E, Bilginoglu A, Sozmen NN, Zeydanli EN, Ugur M, Vassort G, Turan B (2011) Intracellular free zinc during cardiac excitation-contraction cycle: calcium and redox dependencies. Cardiovasc Res 89(3):634–642. https://doi.org/10.1093/cvr/cvq352
Tuncay E, Okatan EN, Vassort G, Turan B (2013) ss-blocker timolol prevents arrhythmogenic Ca(2)(+) release and normalizes Ca(2)(+) and Zn(2)(+) dyshomeostasis in hyperglycemic rat heart. PloS One 8(7):e71014. https://doi.org/10.1371/journal.pone.0071014
Tuncay E, Bitirim V, Durak A, Rutter GA, Turan B (2016) 362 – both reactive ROS and RNS contribute to intracellular free Zn2+ regulation in cardiomyocytes via zinc transporter ZIP7 under hyperglycemia. Free Radic Biol Med 100:S153. https://doi.org/10.1016/j.freeradbiomed.2016.10.403
Tuncay E, Bitirim VC, Durak A, Carrat GRJ, Taylor KM, Rutter GA, Turan B (2017) Hyperglycemia-induced changes in ZIP7 and ZnT7 expression cause Zn(2+) release from the Sarco(endo)plasmic reticulum and mediate ER stress in the heart. Diabetes 66(5):1346–1358. https://doi.org/10.2337/db16-1099
Tuncay E, Bitirim CV, Olgar Y, Durak A, Rutter GA, Turan B (2018) Zn(2+)-transporters ZIP7 and ZnT7 play important role in progression of cardiac dysfunction via affecting sarco(endo)plasmic reticulum-mitochondria coupling in hyperglycemic cardiomyocytes. Mitochondrion. https://doi.org/10.1016/j.mito.2017.12.011
Tuncay E, Olgar Y, Durak A, Degirmenci S, Bitirim CV, Turan B (2019) beta3 -adrenergic receptor activation plays an important role in the depressed myocardial contractility via both elevated levels of cellular free Zn(2+) and reactive nitrogen species. J Cell Physiol. https://doi.org/10.1002/jcp.28015
Turan B, Tuncay E (2017) Impact of labile zinc on heart function: from physiology to pathophysiology. Int J Mol Sci 18(11). https://doi.org/10.3390/ijms18112395
Turan B, Fliss H, Desilets M (1997) Oxidants increase intracellular free Zn2+ concentration in rabbit ventricular myocytes. Am J Phys 272(5 Pt 2):H2095–H2106
Tuschl K, Meyer E, Valdivia LE, Zhao N, Dadswell C, Abdul-Sada A, Hung CY, Simpson MA, Chong WK, Jacques TS, Woltjer RL, Eaton S, Gregory A, Sanford L, Kara E, Houlden H, Cuno SM, Prokisch H, Valletta L, Tiranti V, Younis R, Maher ER, Spencer J, Straatman-Iwanowska A, Gissen P, Selim LA, Pintos-Morell G, Coroleu-Lletget W, Mohammad SS, Yoganathan S, Dale RC, Thomas M, Rihel J, Bodamer OA, Enns CA, Hayflick SJ, Clayton PT, Mills PB, Kurian MA, Wilson SW (2016) Mutations in SLC39A14 disrupt manganese homeostasis and cause childhood-onset parkinsonism-dystonia. Nat Commun 7:11601. https://doi.org/10.1038/ncomms11601
Veronica G, Esther RR (2012) Aging, metabolic syndrome and the heart. Aging Dis 3(3):269–279
Wang G, Biswas AK, Ma W, Kandpal M, Coker C, Grandgenett PM, Hollingsworth MA, Jain R, Tanji K, Lomicronpez-Pintado S, Borczuk A, Hebert D, Jenkitkasemwong S, Hojyo S, Davuluri RV, Knutson MD, Fukada T, Acharyya S (2018) Metastatic cancers promote cachexia through ZIP14 upregulation in skeletal muscle. Nat Med 24(6):770–781. https://doi.org/10.1038/s41591-018-0054-2
Wessells RJ, Fitzgerald E, Cypser JR, Tatar M, Bodmer R (2004) Insulin regulation of heart function in aging fruit flies. Nat Genet 36(12):1275–1281. https://doi.org/10.1038/ng1476
Wilson PW, Kannel WB (2002) Obesity, diabetes, and risk of cardiovascular disease in the elderly. Am J Geriatr Cardiol 11(2):119–123,125
Xi J, Wang H, Mueller RA, Norfleet EA, Xu Z (2009) Mechanism for resveratrol-induced cardioprotection against reperfusion injury involves glycogen synthase kinase 3beta and mitochondrial permeability transition pore. Eur J Pharmacol 604(1–3):111–116. https://doi.org/10.1016/j.ejphar.2008.12.024
Yamasaki S, Sakata-Sogawa K, Hasegawa A, Suzuki T, Kabu K, Sato E, Kurosaki T, Yamashita S, Tokunaga M, Nishida K, Hirano T (2007) Zinc is a novel intracellular second messenger. J Cell Biol 177(4):637–645. https://doi.org/10.1083/jcb.200702081
Yi T, Vick JS, Vecchio MJ, Begin KJ, Bell SP, Delay RJ, Palmer BM (2013) Identifying cellular mechanisms of zinc-induced relaxation in isolated cardiomyocytes. Am J Physiol Heart Circ Physiol 305(5):H706–H715. https://doi.org/10.1152/ajpheart.00025.2013
Zhang W, Song M, Qu J, Liu GH (2018) Epigenetic modifications in cardiovascular aging and diseases. Circ Res 123(7):773–786. https://doi.org/10.1161/circresaha.118.312497
Zhao N, Gao J, Enns CA, Knutson MD (2010) ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J Biol Chem 285(42):32141–32150. https://doi.org/10.1074/jbc.M110.143248
Zhu H, Cong JP, Shenk T (1997) Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc Natl Acad Sci U S A 94(25):13985–13990
Zieman S, Kass D (2004) Advanced glycation end product cross-linking: pathophysiologic role and therapeutic target in cardiovascular disease. Congest Heart Fail 10(3):144–149; quiz 150-141
Acknowledgments
This work has been supported by a grant from TUBITAK (SBAG-216S979) to Belma Turan.
Compliance with Ethical Standards
Animal experimental protocols were performed in accordance with the standards of the European Community guidelines on the care and use of laboratory animals and approved by the Ankara University with a reference number of 2016-18-165.
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No potential conflicts of interest relevant to this article were reported.
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Turan, B., Billur, D., Olgar, Y. (2019). Zinc Signaling in Aging Heart Function. In: Fukada, T., Kambe, T. (eds) Zinc Signaling. Springer, Singapore. https://doi.org/10.1007/978-981-15-0557-7_8
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