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Published in: Cardiovascular Diabetology 1/2015

Open Access 01-12-2015 | Original investigation

The effect of a preparation of minerals, vitamins and trace elements on the cardiac gene expression pattern in male diabetic rats

Authors: Márta Sárközy, Gergő Szűcs, Márton Pipicz, Ágnes Zvara, Katalin Éder, Veronika Fekete, Csilla Szűcs, Judit Bárkányi, Csaba Csonka, László G. Puskás, Csaba Kónya, Péter Ferdinandy, Tamás Csont

Published in: Cardiovascular Diabetology | Issue 1/2015

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Abstract

Background

Diabetic patients have an increased risk of developing cardiovascular diseases, which are the leading cause of death in developed countries. Although multivitamin products are widely used as dietary supplements, the effects of these products have not been investigated in the diabetic heart yet. Therefore, here we investigated if a preparation of different minerals, vitamins, and trace elements (MVT) affects the cardiac gene expression pattern in experimental diabetes.

Methods

Two-day old male Wistar rats were injected with streptozotocin (i.p. 100 mg/kg) or citrate buffer to induce diabetes. From weeks 4 to 12, rats were fed with a vehicle or a MVT preparation. Fasting blood glucose measurement and oral glucose tolerance test were performed at week 12, and then total RNA was isolated from the myocardium and assayed by rat oligonucleotide microarray for 41012 oligonucleotides.

Results

Significantly elevated fasting blood glucose concentration and impaired glucose tolerance were markedly improved by MVT-treatment in diabetic rats at week 12. Genes with significantly altered expression due to diabetes include functional clusters related to cardiac hypertrophy (e.g. caspase recruitment domain family, member 9; cytochrome P450, family 26, subfamily B, polypeptide; FXYD domain containing ion transport regulator 3), stress response (e.g. metallothionein 1a; metallothionein 2a; interleukin-6 receptor; heme oxygenase (decycling) 1; and glutathione S-transferase, theta 3), and hormones associated with insulin resistance (e.g. resistin; FK506 binding protein 5; galanin/GMAP prepropeptide). Moreover the expression of some other genes with no definite cardiac function was also changed such as e.g. similar to apolipoprotein L2; brain expressed X-linked 1; prostaglandin b2 synthase (brain). MVT-treatment in diabetic rats showed opposite gene expression changes in the cases of 19 genes associated with diabetic cardiomyopathy. In healthy hearts, MVT-treatment resulted in cardiac gene expression changes mostly related to immune response (e.g. complement factor B; complement component 4a; interferon regulatory factor 7; hepcidin).

Conclusions

MVT-treatment improved diagnostic markers of diabetes. This is the first demonstration that MVT-treatment significantly alters cardiac gene expression profile in both control and diabetic rats. Our results and further studies exploring the mechanistic role of individual genes may contribute to the prevention or diagnosis of cardiac complications in diabetes.
Appendix
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Literature
2.
go back to reference Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782–7.PubMedCrossRef Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782–7.PubMedCrossRef
3.
go back to reference Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047–53.PubMedCrossRef Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047–53.PubMedCrossRef
4.
go back to reference Astrup A, Finer N. Redefining type 2 diabetes: ‘diabesity’ or ‘obesity dependent DM’? Obes Rev. 2000;1:57–9.PubMedCrossRef Astrup A, Finer N. Redefining type 2 diabetes: ‘diabesity’ or ‘obesity dependent DM’? Obes Rev. 2000;1:57–9.PubMedCrossRef
5.
go back to reference Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94:311–2.PubMedCrossRef Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94:311–2.PubMedCrossRef
6.
go back to reference Li K, Kaaks R, Linseisen J, Rohrmann S. Vitamin/mineral supplementation and cancer, cardiovascular, and all-cause mortality in a German prospective cohort (EPIC-Heidelberg). Eur J Nutr. 2012;51:407–13.PubMedCrossRef Li K, Kaaks R, Linseisen J, Rohrmann S. Vitamin/mineral supplementation and cancer, cardiovascular, and all-cause mortality in a German prospective cohort (EPIC-Heidelberg). Eur J Nutr. 2012;51:407–13.PubMedCrossRef
7.
go back to reference Bailey RL, Fulgoni VL, Keast DR, Dwyer JT. Examination of vitamin intakes among US adults by dietary supplement use. J Acad Nutr Diet. 2012;112:657–63.PubMedCentralPubMedCrossRef Bailey RL, Fulgoni VL, Keast DR, Dwyer JT. Examination of vitamin intakes among US adults by dietary supplement use. J Acad Nutr Diet. 2012;112:657–63.PubMedCentralPubMedCrossRef
8.
go back to reference Song Y, Xu Q, Park Y, Hollenbeck A, Schatzkin A, Chen H. Multivitamins, individual vitamin and mineral supplements, and risk of diabetes among older U.S. adults. Diabetes Care. 2011;34:108–14.PubMedCentralPubMedCrossRef Song Y, Xu Q, Park Y, Hollenbeck A, Schatzkin A, Chen H. Multivitamins, individual vitamin and mineral supplements, and risk of diabetes among older U.S. adults. Diabetes Care. 2011;34:108–14.PubMedCentralPubMedCrossRef
9.
go back to reference Radimer K, Bindewald B, Hughes J, Ervin B, Swanson C, Picciano MF. Dietary supplement use by US adults: data from the National Health and Nutrition Examination Survey, 1999–2000. Am J Epidemiol. 2004;160:339–49.PubMedCrossRef Radimer K, Bindewald B, Hughes J, Ervin B, Swanson C, Picciano MF. Dietary supplement use by US adults: data from the National Health and Nutrition Examination Survey, 1999–2000. Am J Epidemiol. 2004;160:339–49.PubMedCrossRef
10.
go back to reference Rock CL. Multivitamin-multimineral supplements: who uses them? Am J Clin Nutr. 2007;85:277S–9S.PubMed Rock CL. Multivitamin-multimineral supplements: who uses them? Am J Clin Nutr. 2007;85:277S–9S.PubMed
11.
go back to reference Beitz R, Mensink GB, Fischer B, Thamm M. Vitamins–dietary intake and intake from dietary supplements in Germany. Eur J Clin Nutr. 2002;56:539–45.PubMedCrossRef Beitz R, Mensink GB, Fischer B, Thamm M. Vitamins–dietary intake and intake from dietary supplements in Germany. Eur J Clin Nutr. 2002;56:539–45.PubMedCrossRef
12.
go back to reference Csont T, Sárközy M, Szűcs G, Szűcs C, Bárkányi J, Bencsik P, et al. Effect of a multivitamin preparation supplemented with phytosterol on serum lipids and infarct size in rats fed with normal and high cholesterol diet. Lipids Health Dis. 2013;12:138.PubMedCentralPubMedCrossRef Csont T, Sárközy M, Szűcs G, Szűcs C, Bárkányi J, Bencsik P, et al. Effect of a multivitamin preparation supplemented with phytosterol on serum lipids and infarct size in rats fed with normal and high cholesterol diet. Lipids Health Dis. 2013;12:138.PubMedCentralPubMedCrossRef
13.
go back to reference Garaiova I, Muchova J, Nagyova Z, Mislanova C, Oravec S, Dukat A, et al. Effect of a plant sterol, fish oil and B vitamin combination on cardiovascular risk factors in hypercholesterolemic children and adolescents: a pilot study. Nutr J. 2013;12:7.PubMedCentralPubMedCrossRef Garaiova I, Muchova J, Nagyova Z, Mislanova C, Oravec S, Dukat A, et al. Effect of a plant sterol, fish oil and B vitamin combination on cardiovascular risk factors in hypercholesterolemic children and adolescents: a pilot study. Nutr J. 2013;12:7.PubMedCentralPubMedCrossRef
14.
go back to reference Sárközy M, Fekete V, Szűcs G, Török S, Szűcs C, Bárkányi J, et al. Anti-diabetic effect of a preparation of vitamins, minerals and trace elements in diabetic rats: a gender difference. BMC Endocr Disord. 2014;14:72.PubMedCentralPubMedCrossRef Sárközy M, Fekete V, Szűcs G, Török S, Szűcs C, Bárkányi J, et al. Anti-diabetic effect of a preparation of vitamins, minerals and trace elements in diabetic rats: a gender difference. BMC Endocr Disord. 2014;14:72.PubMedCentralPubMedCrossRef
15.
go back to reference Kaur B, Henry J. Micronutrient status in type 2 diabetes: a review. Adv Food Nutr Res. 2014;71:55–100.PubMedCrossRef Kaur B, Henry J. Micronutrient status in type 2 diabetes: a review. Adv Food Nutr Res. 2014;71:55–100.PubMedCrossRef
16.
go back to reference Zabłocka-Słowińska K, Dzielska E, Gryszkin I, Grajeta H. Dietary supplementation during diabetes therapy and the potential risk of interactions. Adv Clin Exp Med. 2014;23:939–46.PubMedCrossRef Zabłocka-Słowińska K, Dzielska E, Gryszkin I, Grajeta H. Dietary supplementation during diabetes therapy and the potential risk of interactions. Adv Clin Exp Med. 2014;23:939–46.PubMedCrossRef
17.
go back to reference McClelland AD, Kantharidis P. MicroRNA in the development of diabetic complications. Clin Sci (Lond). 2014;126:95–110.CrossRef McClelland AD, Kantharidis P. MicroRNA in the development of diabetic complications. Clin Sci (Lond). 2014;126:95–110.CrossRef
18.
go back to reference Asrih M, Steffens S. Emerging role of epigenetics and miRNA in DCM. Cardiovasc Pathol. 2013;22:117–25.PubMedCrossRef Asrih M, Steffens S. Emerging role of epigenetics and miRNA in DCM. Cardiovasc Pathol. 2013;22:117–25.PubMedCrossRef
19.
go back to reference Glyn-Jones S, Song S, Black MA, Phillips AR, Choong SY, Cooper GJ. Transcriptomic analysis of the cardiac left ventricle in a rodent model of diabetic cardiomyopathy: molecular snapshot of a severe myocardial disease. Physiol Genomics. 2007;28:284–93.PubMedCrossRef Glyn-Jones S, Song S, Black MA, Phillips AR, Choong SY, Cooper GJ. Transcriptomic analysis of the cardiac left ventricle in a rodent model of diabetic cardiomyopathy: molecular snapshot of a severe myocardial disease. Physiol Genomics. 2007;28:284–93.PubMedCrossRef
20.
go back to reference Wang N, Yang C, Xie F, Sun L, Su X, Wang Y, et al. Gadd45α: a novel diabetes-associated gene potentially linking diabetic cardiomyopathy and baroreflex dysfunction. PLoS One. 2012;7:e49077.PubMedCentralPubMedCrossRef Wang N, Yang C, Xie F, Sun L, Su X, Wang Y, et al. Gadd45α: a novel diabetes-associated gene potentially linking diabetic cardiomyopathy and baroreflex dysfunction. PLoS One. 2012;7:e49077.PubMedCentralPubMedCrossRef
21.
go back to reference Diao X, Shen E, Wang X, Hu B. Differentially expressed microRNAs and their target genes in the hearts of streptozotocin-induced diabetic mice. Mol Med Rep. 2011;4:633–40.PubMed Diao X, Shen E, Wang X, Hu B. Differentially expressed microRNAs and their target genes in the hearts of streptozotocin-induced diabetic mice. Mol Med Rep. 2011;4:633–40.PubMed
22.
go back to reference D’Souza A, Howarth FC, Yanni J, Dobrzynski H, Boyett MR, Adeghate E, et al. Chronic effects of mild hyperglycaemia on left ventricle transcriptional profile and structural remodelling in the spontaneously type 2 diabetic Goto-Kakizaki rat. Heart Fail Rev. 2014;19:65–74.PubMedCrossRef D’Souza A, Howarth FC, Yanni J, Dobrzynski H, Boyett MR, Adeghate E, et al. Chronic effects of mild hyperglycaemia on left ventricle transcriptional profile and structural remodelling in the spontaneously type 2 diabetic Goto-Kakizaki rat. Heart Fail Rev. 2014;19:65–74.PubMedCrossRef
23.
go back to reference Sárközy M, Zvara A, Gyémánt N, Fekete V, Kocsis GF, Pipis J, et al. Metabolic syndrome influences cardiac gene expression pattern at the transcript level in male ZDF rats. Cardiovasc Diabetol. 2013;12:16.PubMedCentralPubMedCrossRef Sárközy M, Zvara A, Gyémánt N, Fekete V, Kocsis GF, Pipis J, et al. Metabolic syndrome influences cardiac gene expression pattern at the transcript level in male ZDF rats. Cardiovasc Diabetol. 2013;12:16.PubMedCentralPubMedCrossRef
24.
go back to reference Patel SB, Santani D, Patel V, Shah M. Anti-diabetic effects of ethanol extract of Bryonia laciniosa seeds and its saponins rich fraction in neonatally STZ-induced diabetic rats. Pharmacognosy Res. 2015;7:92–9.PubMedCentralPubMedCrossRef Patel SB, Santani D, Patel V, Shah M. Anti-diabetic effects of ethanol extract of Bryonia laciniosa seeds and its saponins rich fraction in neonatally STZ-induced diabetic rats. Pharmacognosy Res. 2015;7:92–9.PubMedCentralPubMedCrossRef
25.
go back to reference Andrade-Cetto A, Revilla-Monsalve C, Wiedenfeld H. Hypoglycemic effect of Tournefortia hirsutissima L. on n-STZ diabetic rats. J Ethnopharmacol. 2007;112:96–100.PubMedCrossRef Andrade-Cetto A, Revilla-Monsalve C, Wiedenfeld H. Hypoglycemic effect of Tournefortia hirsutissima L. on n-STZ diabetic rats. J Ethnopharmacol. 2007;112:96–100.PubMedCrossRef
26.
go back to reference Li L, Yi Z, Seno M, Kojima I. Activin A and betacellulin. Effect on regeneration of pancreatic beta-cells in neonatal STZ-treated rats. Diabetes. 2004;53:608–15.PubMedCrossRef Li L, Yi Z, Seno M, Kojima I. Activin A and betacellulin. Effect on regeneration of pancreatic beta-cells in neonatal STZ-treated rats. Diabetes. 2004;53:608–15.PubMedCrossRef
27.
go back to reference Thyssen S, Arany E, Hill DJ. Ontogeny of regeneration of beta-cells in the neonatal rat after treatment with STZ. Endocrinology. 2006;147:2346–56.PubMedCrossRef Thyssen S, Arany E, Hill DJ. Ontogeny of regeneration of beta-cells in the neonatal rat after treatment with STZ. Endocrinology. 2006;147:2346–56.PubMedCrossRef
28.
go back to reference Patel BM, Raghunathan S, Porwal U. Cardioprotective effects of magnesium valproate in type 2 diabetes mellitus. Eur J Pharmacol. 2014;728:128–34.PubMedCrossRef Patel BM, Raghunathan S, Porwal U. Cardioprotective effects of magnesium valproate in type 2 diabetes mellitus. Eur J Pharmacol. 2014;728:128–34.PubMedCrossRef
29.
go back to reference Patel BM, Bhadada SV. Type 2 diabetes-induced cardiovascular complications: comparative evaluation of spironolactone, atenolol, metoprolol, ramipril and perindopril. Clin Exp Hypertens. 2014;36:340–7.PubMedCrossRef Patel BM, Bhadada SV. Type 2 diabetes-induced cardiovascular complications: comparative evaluation of spironolactone, atenolol, metoprolol, ramipril and perindopril. Clin Exp Hypertens. 2014;36:340–7.PubMedCrossRef
30.
go back to reference Patel BM, Kakadiya J, Goyal RK, Mehta AA. Effect of spironolactone on cardiovascular complications associated with type-2 diabetes in rats. Exp Clin Endocrinol Diabetes. 2013;121:441–7.PubMedCrossRef Patel BM, Kakadiya J, Goyal RK, Mehta AA. Effect of spironolactone on cardiovascular complications associated with type-2 diabetes in rats. Exp Clin Endocrinol Diabetes. 2013;121:441–7.PubMedCrossRef
31.
go back to reference Goyal BR, Parmar K, Goyal RK, Mehta AA. Beneficial role of telmisartan on cardiovascular complications associated with STZ-induced type 2 diabetes in rats. Pharmacol Rep. 2011;63:956–66.PubMedCrossRef Goyal BR, Parmar K, Goyal RK, Mehta AA. Beneficial role of telmisartan on cardiovascular complications associated with STZ-induced type 2 diabetes in rats. Pharmacol Rep. 2011;63:956–66.PubMedCrossRef
32.
go back to reference Abebe W, Mozaffari MS. Vascular reactivity changes in glucose-intolerant rat. J Cardiovasc Pharmacol. 2007;50:590–7.PubMedCrossRef Abebe W, Mozaffari MS. Vascular reactivity changes in glucose-intolerant rat. J Cardiovasc Pharmacol. 2007;50:590–7.PubMedCrossRef
33.
go back to reference Sartoretto JL, Oliveira MA, Nigro D, Carvalho MH, Tostes RC, Fortes ZB. Constrictor responses to noradrenaline, hemodynamic profile, and superoxide levels measured by hydroethidine oxidation in diabetic rats. Biol Pharm Bull. 2007;30:1938–42.PubMedCrossRef Sartoretto JL, Oliveira MA, Nigro D, Carvalho MH, Tostes RC, Fortes ZB. Constrictor responses to noradrenaline, hemodynamic profile, and superoxide levels measured by hydroethidine oxidation in diabetic rats. Biol Pharm Bull. 2007;30:1938–42.PubMedCrossRef
34.
go back to reference Huisamen B, van Zyl M, Keyser A, Lochner A. The effects of insulin and beta-adrenergic stimulation on glucose transport, glut 4 and PKB activation in the myocardium of lean and obese non-insulin dependent diabetes mellitus rats. Mol Cell Biochem. 2001;223:15–25.PubMedCrossRef Huisamen B, van Zyl M, Keyser A, Lochner A. The effects of insulin and beta-adrenergic stimulation on glucose transport, glut 4 and PKB activation in the myocardium of lean and obese non-insulin dependent diabetes mellitus rats. Mol Cell Biochem. 2001;223:15–25.PubMedCrossRef
35.
go back to reference Kocsis GF, Sárközy M, Bencsik P, Pipicz M, Varga ZV, Pálóczi J, et al. Preconditioning protects the heart in a prolonged uremic condition. Am J Physiol Heart Circ Physiol. 2012;303:H1229–36.PubMedCrossRef Kocsis GF, Sárközy M, Bencsik P, Pipicz M, Varga ZV, Pálóczi J, et al. Preconditioning protects the heart in a prolonged uremic condition. Am J Physiol Heart Circ Physiol. 2012;303:H1229–36.PubMedCrossRef
36.
go back to reference Ferdinandy P, Szilvássy Z, Csont T, Csonka C, Nagy E, Koltai M, et al. Nitroglycerin-induced direct protection of the ischaemic myocardium in isolated working hearts of rats with vascular tolerance to nitroglycerin. Br J Pharmacol. 1995;115:1129–31.PubMedCentralPubMedCrossRef Ferdinandy P, Szilvássy Z, Csont T, Csonka C, Nagy E, Koltai M, et al. Nitroglycerin-induced direct protection of the ischaemic myocardium in isolated working hearts of rats with vascular tolerance to nitroglycerin. Br J Pharmacol. 1995;115:1129–31.PubMedCentralPubMedCrossRef
37.
go back to reference Csont T, Páli T, Szilvássy Z, Ferdinandy P. Lack of correlation between myocardial nitric oxide and cyclic guanosine monophosphate content in both nitrate-tolerant and -nontolerant rats. Biochem Pharmacol. 1998;56:1139–44.PubMedCrossRef Csont T, Páli T, Szilvássy Z, Ferdinandy P. Lack of correlation between myocardial nitric oxide and cyclic guanosine monophosphate content in both nitrate-tolerant and -nontolerant rats. Biochem Pharmacol. 1998;56:1139–44.PubMedCrossRef
38.
go back to reference Bell RM, Yellon DM. Conditioning the whole heart–not just the cardiomyocyte. J Mol Cell Cardiol. 2012;53:24–32.PubMedCrossRef Bell RM, Yellon DM. Conditioning the whole heart–not just the cardiomyocyte. J Mol Cell Cardiol. 2012;53:24–32.PubMedCrossRef
39.
go back to reference Cury DP, Dias FJ, Sosthenes MC, Dos Santos Haemmerle CA, Ogawa K, et al. Morphometric, quantitative, and three-dimensional analysis of the heart muscle fibers of old rats: Transmission electron microscopy and high-resolution scanning electron microscopy methods. Microsc Res Tech. 2013;76:184–95.PubMedCrossRef Cury DP, Dias FJ, Sosthenes MC, Dos Santos Haemmerle CA, Ogawa K, et al. Morphometric, quantitative, and three-dimensional analysis of the heart muscle fibers of old rats: Transmission electron microscopy and high-resolution scanning electron microscopy methods. Microsc Res Tech. 2013;76:184–95.PubMedCrossRef
41.
go back to reference Dhalla NS, Takeda N, Rodriguez-Leyva D, Elimban V. Mechanisms of subcellular remodeling in heart failure due to diabetes. Heart Fail Rev. 2014;19:87–99.PubMedCrossRef Dhalla NS, Takeda N, Rodriguez-Leyva D, Elimban V. Mechanisms of subcellular remodeling in heart failure due to diabetes. Heart Fail Rev. 2014;19:87–99.PubMedCrossRef
43.
go back to reference Ren J, Yang M, Qi G, Zheng J, Jia L, Cheng J, et al. Proinflammatory protein CARD9 is essential for infiltration of monocytic fibroblast precursors and cardiac fibrosis caused by Angiotensin II infusion. Am J Hypertens. 2011;24:701–7.PubMedCentralPubMedCrossRef Ren J, Yang M, Qi G, Zheng J, Jia L, Cheng J, et al. Proinflammatory protein CARD9 is essential for infiltration of monocytic fibroblast precursors and cardiac fibrosis caused by Angiotensin II infusion. Am J Hypertens. 2011;24:701–7.PubMedCentralPubMedCrossRef
44.
go back to reference Rokosh DG, Stewart AF, Chang KC, Bailey BA, Karliner JS, Camacho SA, et al. Alpha1-adrenergic receptor subtype mRNAs are differentially regulated by alpha1-adrenergic and other hypertrophic stimuli in cardiac myocytes in culture and in vivo. Repression of alpha1B and alpha1D but induction of alpha1C. J Biol Chem. 1996;271:5839–43.PubMedCrossRef Rokosh DG, Stewart AF, Chang KC, Bailey BA, Karliner JS, Camacho SA, et al. Alpha1-adrenergic receptor subtype mRNAs are differentially regulated by alpha1-adrenergic and other hypertrophic stimuli in cardiac myocytes in culture and in vivo. Repression of alpha1B and alpha1D but induction of alpha1C. J Biol Chem. 1996;271:5839–43.PubMedCrossRef
45.
go back to reference Messner B, Kern J, Wiedemann D, Schwaiger S, Türkcan A, Ploner C, et al. 5-Methoxyleoligin, a lignan from Edelweiss, stimulates CYP26B1-dependent angiogenesis in vitro and induces arteriogenesis in infarcted rat hearts in vivo. PLoS One. 2013;8:e58342.PubMedCentralPubMedCrossRef Messner B, Kern J, Wiedemann D, Schwaiger S, Türkcan A, Ploner C, et al. 5-Methoxyleoligin, a lignan from Edelweiss, stimulates CYP26B1-dependent angiogenesis in vitro and induces arteriogenesis in infarcted rat hearts in vivo. PLoS One. 2013;8:e58342.PubMedCentralPubMedCrossRef
46.
go back to reference Reijntjes S, Blentic A, Gale E, Maden M. The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev Biol. 2005;285:224–37.PubMedCrossRef Reijntjes S, Blentic A, Gale E, Maden M. The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev Biol. 2005;285:224–37.PubMedCrossRef
47.
go back to reference Jia LG, Donnet C, Bogaev RC, Blatt RJ, McKinney CE, Day KH, et al. Hypertrophy, increased ejection fraction, and reduced Na-K-ATPase activity in phospholemman-deficient mice. Am J Physiol Heart Circ Physiol. 2005;288:H1982–8.PubMedCrossRef Jia LG, Donnet C, Bogaev RC, Blatt RJ, McKinney CE, Day KH, et al. Hypertrophy, increased ejection fraction, and reduced Na-K-ATPase activity in phospholemman-deficient mice. Am J Physiol Heart Circ Physiol. 2005;288:H1982–8.PubMedCrossRef
48.
go back to reference Pavlovic D, Fuller W, Shattock MJ. Novel regulation of cardiac Na pump via phospholemman. J Mol Cell Cardiol. 2013;61:83–93.PubMedCrossRef Pavlovic D, Fuller W, Shattock MJ. Novel regulation of cardiac Na pump via phospholemman. J Mol Cell Cardiol. 2013;61:83–93.PubMedCrossRef
49.
go back to reference Boguslavskyi A, Pavlovic D, Aughton K, Clark JE, Howie J, Fuller W, et al. Cardiac hypertrophy in mice expressing unphosphorylatable phospholemman. Cardiovasc Res. 2014;104:72–82.PubMedCentralPubMedCrossRef Boguslavskyi A, Pavlovic D, Aughton K, Clark JE, Howie J, Fuller W, et al. Cardiac hypertrophy in mice expressing unphosphorylatable phospholemman. Cardiovasc Res. 2014;104:72–82.PubMedCentralPubMedCrossRef
50.
go back to reference Shichi D, Kikkawa EF, Ota M, Katsuyama Y, Kimura A, Matsumori A, et al. The haplotype block, NFKBIL1-ATP6V1G2-BAT1-MICB-MICA, within the class III-class I boundary region of the human major histocompatibility complex may control susceptibility to hepatitis C virus-associated dilated cardiomyopathy. Tissue Antigens. 2005;66:200–8.PubMedCrossRef Shichi D, Kikkawa EF, Ota M, Katsuyama Y, Kimura A, Matsumori A, et al. The haplotype block, NFKBIL1-ATP6V1G2-BAT1-MICB-MICA, within the class III-class I boundary region of the human major histocompatibility complex may control susceptibility to hepatitis C virus-associated dilated cardiomyopathy. Tissue Antigens. 2005;66:200–8.PubMedCrossRef
51.
go back to reference Hu X, Sui X, Li L, Huang X, Rong R, Su X, et al. Protocadherin 17 acts as a tumour suppressor inducing tumour cell apoptosis and autophagy, and is frequently methylated in gastric and colorectal cancers. J Pathol. 2013;229:62–73.PubMedCrossRef Hu X, Sui X, Li L, Huang X, Rong R, Su X, et al. Protocadherin 17 acts as a tumour suppressor inducing tumour cell apoptosis and autophagy, and is frequently methylated in gastric and colorectal cancers. J Pathol. 2013;229:62–73.PubMedCrossRef
52.
go back to reference Fritz RD, Varga Z, Radziwill G. CNK1 is a novel Akt interaction partner that promotes cell proliferation through the Akt-FoxO signalling axis. Oncogene. 2010;29:3575–82.PubMedCrossRef Fritz RD, Varga Z, Radziwill G. CNK1 is a novel Akt interaction partner that promotes cell proliferation through the Akt-FoxO signalling axis. Oncogene. 2010;29:3575–82.PubMedCrossRef
53.
54.
go back to reference Lee SH, Demeterco C, Geron I, Abrahamsson A, Levine F, Itkin-Ansari P. Islet specific Wnt activation in human type II diabetes. Exp Diabetes Res. 2008;2008:728763.PubMedCentralPubMedCrossRef Lee SH, Demeterco C, Geron I, Abrahamsson A, Levine F, Itkin-Ansari P. Islet specific Wnt activation in human type II diabetes. Exp Diabetes Res. 2008;2008:728763.PubMedCentralPubMedCrossRef
55.
go back to reference Xue W, Liu Y, Zhao J, Cai L, Li X, Feng W. Activation of HIF-1 by metallothionein contributes to cardiac protection in the diabetic heart. Am J Physiol Heart Circ Physiol. 2012;302:H2528–35.PubMedCrossRef Xue W, Liu Y, Zhao J, Cai L, Li X, Feng W. Activation of HIF-1 by metallothionein contributes to cardiac protection in the diabetic heart. Am J Physiol Heart Circ Physiol. 2012;302:H2528–35.PubMedCrossRef
56.
go back to reference Feng W, Benz FW, Cai J, Pierce WM, Kang YJ. Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress. J Biol Chem. 2006;281:681–7.PubMedCrossRef Feng W, Benz FW, Cai J, Pierce WM, Kang YJ. Metallothionein disulfides are present in metallothionein-overexpressing transgenic mouse heart and increase under conditions of oxidative stress. J Biol Chem. 2006;281:681–7.PubMedCrossRef
57.
go back to reference Interleukin-6 Receptor Mendelian Randomisation Analysis (IL6R MR) Consortium. The interleukin-6 receptor as a target for prevention of coronary heart disease: a mendelian randomisation analysis. Lancet. 2012;379:1214–24.CrossRef Interleukin-6 Receptor Mendelian Randomisation Analysis (IL6R MR) Consortium. The interleukin-6 receptor as a target for prevention of coronary heart disease: a mendelian randomisation analysis. Lancet. 2012;379:1214–24.CrossRef
58.
go back to reference Palomer X, Salvadó L, Barroso E, Vázquez-Carrera M. An overview of the crosstalk between inflammatory processes and metabolic dysregulation during diabetic cardiomyopathy. Int J Cardiol. 2013;68:3160–72.CrossRef Palomer X, Salvadó L, Barroso E, Vázquez-Carrera M. An overview of the crosstalk between inflammatory processes and metabolic dysregulation during diabetic cardiomyopathy. Int J Cardiol. 2013;68:3160–72.CrossRef
59.
go back to reference Wu ML, Ho YC, Yet SF. A central role of heme oxygenase-1 in cardiovascular protection. Antioxid Redox Signal. 2011;15:1835–46.PubMedCrossRef Wu ML, Ho YC, Yet SF. A central role of heme oxygenase-1 in cardiovascular protection. Antioxid Redox Signal. 2011;15:1835–46.PubMedCrossRef
60.
go back to reference Douglas KT. Mechanism of action of glutathione-dependent enzymes. Adv Enzymol Relat Areas Mol Biol. 1987;59:103–67.PubMed Douglas KT. Mechanism of action of glutathione-dependent enzymes. Adv Enzymol Relat Areas Mol Biol. 1987;59:103–67.PubMed
61.
go back to reference L’Ecuyer T, Allebban Z, Thomas R, Vander HR. Glutathione S-transferase overexpression protects against anthracycline-induced H9C2 cell death. Am J Physiol Heart Circ Physiol. 2004;286:H2057–64.PubMedCrossRef L’Ecuyer T, Allebban Z, Thomas R, Vander HR. Glutathione S-transferase overexpression protects against anthracycline-induced H9C2 cell death. Am J Physiol Heart Circ Physiol. 2004;286:H2057–64.PubMedCrossRef
62.
go back to reference Puskas LG, Nagy ZB, Giricz Z, Onody A, Csonka C, Kitajka K, et al. Cholesterol diet-induced hyperlipidemia influences gene expression pattern of rat hearts: a DNA microarray study. FEBS Lett. 2004;562:99–104.PubMedCrossRef Puskas LG, Nagy ZB, Giricz Z, Onody A, Csonka C, Kitajka K, et al. Cholesterol diet-induced hyperlipidemia influences gene expression pattern of rat hearts: a DNA microarray study. FEBS Lett. 2004;562:99–104.PubMedCrossRef
63.
go back to reference Zhang S, Liu H, Amarsingh GV, Cheung CC, Hogl S, Narayanan U, et al. Diabetic cardiomyopathy is associated with defective myocellular copper regulation and both defects are rectified by divalent copper chelation. Cardiovasc Diabetol. 2014;13:100.PubMedCentralPubMedCrossRef Zhang S, Liu H, Amarsingh GV, Cheung CC, Hogl S, Narayanan U, et al. Diabetic cardiomyopathy is associated with defective myocellular copper regulation and both defects are rectified by divalent copper chelation. Cardiovasc Diabetol. 2014;13:100.PubMedCentralPubMedCrossRef
64.
go back to reference Miao X, Wang Y, Sun J, Sun W, Tan Y, Cai L, et al. Zinc protects against diabetes-induced pathogenic changes in the aorta: roles of metallothionein and nuclear factor (erythroid-derived 2)-like 2. Cardiovasc Diabetol. 2013;12:54.PubMedCentralPubMedCrossRef Miao X, Wang Y, Sun J, Sun W, Tan Y, Cai L, et al. Zinc protects against diabetes-induced pathogenic changes in the aorta: roles of metallothionein and nuclear factor (erythroid-derived 2)-like 2. Cardiovasc Diabetol. 2013;12:54.PubMedCentralPubMedCrossRef
65.
go back to reference Li B, Tan Y, Sun W, Fu Y, Miao L, Cai L. The role of zinc in the prevention of diabetic cardiomyopathy and nephropathy. Toxicol Mech Methods. 2013;23:27–33.PubMedCrossRef Li B, Tan Y, Sun W, Fu Y, Miao L, Cai L. The role of zinc in the prevention of diabetic cardiomyopathy and nephropathy. Toxicol Mech Methods. 2013;23:27–33.PubMedCrossRef
66.
go back to reference Csont T, Murlasits Z, Ménesi D, Kelemen JZ, Bencsik P, Pipicz M, et al. Tissue-specific gene expression in rat hearts and aortas in a model of vascular nitrate tolerance. J Cardiovasc Pharmacol. 2015;65:485–93.PubMedCrossRef Csont T, Murlasits Z, Ménesi D, Kelemen JZ, Bencsik P, Pipicz M, et al. Tissue-specific gene expression in rat hearts and aortas in a model of vascular nitrate tolerance. J Cardiovasc Pharmacol. 2015;65:485–93.PubMedCrossRef
68.
go back to reference Gragnoli C. Hypothesis of the neuroendocrine cortisol pathway gene role in the comorbidity of depression, type 2 diabetes, and metabolic syndrome. Appl Clin Genet. 2014;7:43–53.PubMedCentralPubMedCrossRef Gragnoli C. Hypothesis of the neuroendocrine cortisol pathway gene role in the comorbidity of depression, type 2 diabetes, and metabolic syndrome. Appl Clin Genet. 2014;7:43–53.PubMedCentralPubMedCrossRef
69.
go back to reference Fang P, Sun J, Wang X, Zhang Z, Bo P, Shi M. Galanin participates in the functional regulation of the diabetic heart. Life Sci. 2013;92:628–32.PubMedCrossRef Fang P, Sun J, Wang X, Zhang Z, Bo P, Shi M. Galanin participates in the functional regulation of the diabetic heart. Life Sci. 2013;92:628–32.PubMedCrossRef
70.
go back to reference Marino G, Zanghì A. Activins and inhibins: expression and role in normal and pathological canine reproductive organs: a review. Anat Histol Embryol. 2013;42:1–8.PubMedCrossRef Marino G, Zanghì A. Activins and inhibins: expression and role in normal and pathological canine reproductive organs: a review. Anat Histol Embryol. 2013;42:1–8.PubMedCrossRef
72.
go back to reference Cameron FJ, Wherrett DK. Care of diabetes in children and adolescents: controversies, changes, and consensus. Lancet. 2015;385:2096–106.PubMedCrossRef Cameron FJ, Wherrett DK. Care of diabetes in children and adolescents: controversies, changes, and consensus. Lancet. 2015;385:2096–106.PubMedCrossRef
73.
go back to reference Faragó N, Kocsis GF, Fehér LZ, Csont T, Hackler Jr L, Varga-Orvos Z, et al. Gene and protein expression changes in response to normoxic perfusion in mouse hearts. J Pharmacol Toxicol Methods. 2008;57:145–54.PubMedCrossRef Faragó N, Kocsis GF, Fehér LZ, Csont T, Hackler Jr L, Varga-Orvos Z, et al. Gene and protein expression changes in response to normoxic perfusion in mouse hearts. J Pharmacol Toxicol Methods. 2008;57:145–54.PubMedCrossRef
74.
go back to reference Gaziano JM, Sesso HD, Christen WG, Bubes V, Smith JP, MacFadyen J, et al. Multivitamins in the prevention of cancer in men: the Physicians’ Health Study II randomized controlled trial. JAMA. 2012;308:1871–80.PubMedCentralPubMedCrossRef Gaziano JM, Sesso HD, Christen WG, Bubes V, Smith JP, MacFadyen J, et al. Multivitamins in the prevention of cancer in men: the Physicians’ Health Study II randomized controlled trial. JAMA. 2012;308:1871–80.PubMedCentralPubMedCrossRef
Metadata
Title
The effect of a preparation of minerals, vitamins and trace elements on the cardiac gene expression pattern in male diabetic rats
Authors
Márta Sárközy
Gergő Szűcs
Márton Pipicz
Ágnes Zvara
Katalin Éder
Veronika Fekete
Csilla Szűcs
Judit Bárkányi
Csaba Csonka
László G. Puskás
Csaba Kónya
Péter Ferdinandy
Tamás Csont
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2015
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-015-0248-6

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