Zinc rescue of Akt2 gene deletion-linked murine cardiac dysfunction and pathological changes is metallothionein-dependent

Journal of Molecular and Cellular Cardiology

Volumn 74, Issue , 2014, Pages 88-97

  Sun, Weixia ^a,b   Miao, Xiao ^b,c   Zhou, Shanshan ^a,b   Zhang, Li ^a   Epstein, Paul N ^b   Mellen, Nicholas ^b   Zheng, Yang ^a   Fu, Yaowen ^a   Wang, Yuehui ^a   Cai, Lu ^b  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

^c THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

Akt2 knockout; Diabetic heart; GSK 3 ; Insulin resistance; Metallothionein; Zinc

Indexed keywords

GLUCOSE; GLYCOGEN SYNTHASE KINASE 3BETA; HEXOKINASE; HEXOKINASE ISOENZYME; METALLOTHIONEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN TYROSINE PHOSPHATASE 1B; REGULATOR PROTEIN; TRB3 PROTEIN; UNCLASSIFIED DRUG; ZINC; AKT2 PROTEIN, MOUSE; CELL CYCLE PROTEIN; GLUCOSE BLOOD LEVEL; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INSULIN; PPARGC1A PROTEIN, MOUSE; PTEN PROTEIN, MOUSE; PTPN1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRB3 PROTEIN, MOUSE;

AKT2 GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME PHOSPHORYLATION; GENE; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GLUCOSE METABOLISM; HEART DISEASE; HEART PROTECTION; MALE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VITAMIN SUPPLEMENTATION; ANIMAL; CARDIOMYOPATHIES; DEFICIENCY; DIABETES MELLITUS, EXPERIMENTAL; GENE EXPRESSION REGULATION; GENETICS; GLUCOSE BLOOD LEVEL; HEART MUSCLE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; BLOOD GLUCOSE; CARDIOMYOPATHIES; CELL CYCLE PROTEINS; DIABETES MELLITUS, EXPERIMENTAL; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE; GLYCOGEN SYNTHASE KINASE 3; HEXOKINASE; INSULIN; MALE; METALLOTHIONEIN; MICE; MICE, KNOCKOUT; MYOCARDIUM; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; ZINC;

EID: 84904748622     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.04.023     Document Type: Article

References (51)

1. Miao X., Sun W., Fu Y., Miao L., Cai L. Zinc homeostasis in the metabolic syndrome and diabetes. Front Med 2013, 7:31-52.
2. Park J.H., Grandjean C.J., Hart M.H., Erdman S.H., Pour P., Vanderhoof J.A. Effect of pure zinc deficiency on glucose tolerance and insulin and glucagon levels. Am J Physiol 1986, 251:E273-E278.
3. Shen H., Oesterling E., Stromberg A., Toborek M., MacDonald R., Hennig B. Zinc deficiency induces vascular pro-inflammatory parameters associated with NF-kappaB and PPAR signaling. J Am Coll Nutr 2008, 27:577-587.
4. Frustaci A., Sabbioni E., Fortaner S., Farina M., del Torchio R., Tafani M., et al. Selenium- and zinc-deficient cardiomyopathy in human intestinal malabsorption: preliminary results of selenium/zinc infusion. Eur J Heart Fail 2012, 14:202-210.
5. Hashemipour M., Kelishadi R., Shapouri J., Sarrafzadegan N., Amini M., Tavakoli N., et al. Effect of zinc supplementation on insulin resistance and components of the metabolic syndrome in prepubertal obese children. Hormones (Athens) 2009, 8:279-285.
6. Wang J., Song Y., Elsherif L., Song Z., Zhou G., Prabhu S.D., et al. Cardiac metallothionein induction plays the major role in the prevention of diabetic cardiomyopathy by zinc supplementation. Circulation 2006, 113:544-554.
7. Soinio M., Marniemi J., Laakso M., Pyorala K., Lehto S., Ronnemaa T. Serum zinc level and coronary heart disease events in patients with type 2 diabetes. Diabetes Care 2007, 30:523-528.
8. Tang X., Shay N.F. Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytes. J Nutr 2001, 131:1414-1420.
9. Ilouz R., Kaidanovich O., Gurwitz D., Eldar-Finkelman H. Inhibition of glycogen synthase kinase-3beta by bivalent zinc ions: insight into the insulin-mimetic action of zinc. Biochem Biophys Res Commun 2002, 295:102-106.
10. Cho H., Mu J., Kim J.K., Thorvaldsen J.L., Chu Q., Crenshaw E.B., et al. Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 2001, 292:1728-1731.
11. Garofalo R.S., Orena S.J., Rafidi K., Torchia A.J., Stock J.L., Hildebrandt A.L., et al. Severe diabetes, age-dependent loss of adipose tissue, and mild growth deficiency in mice lacking Akt2/PKB beta. J Clin Invest 2003, 112:197-208.
12. Cho H., Thorvaldsen J.L., Chu Q., Feng F., Birnbaum M.J. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem 2001, 276:38349-38352.
13. Dummler B., Tschopp O., Hynx D., Yang Z.Z., Dirnhofer S., Hemmings B.A. Life with a single isoform of Akt: mice lacking Akt2 and Akt3 are viable but display impaired glucose homeostasis and growth deficiencies. Mol Cell Biol 2006, 26:8042-8051.
14. Tschopp O., Yang Z.Z., Brodbeck D., Dummler B.A., Hemmings-Mieszczak M., Watanabe T., et al. Essential role of protein kinase B gamma (PKB gamma/Akt3) in postnatal brain development but not in glucose homeostasis. Development 2005, 132:2943-2954.
15. George S., Rochford J.J., Wolfrum C., Gray S.L., Schinner S., Wilson J.C., et al. A family with severe insulin resistance and diabetes due to a mutation in AKT2. Science 2004, 304:1325-1328.
16. Chanoit G., Lee S., Xi J., Zhu M., McIntosh R.A., Mueller R.A., et al. Exogenous zinc protects cardiac cells from reperfusion injury by targeting mitochondrial permeability transition pore through inactivation of glycogen synthase kinase-3beta. Am J Physiol Heart Circ Physiol 2008, 295:H1227-H1233.
17. Lee S., Chanoit G., McIntosh R., Zvara D.A., Xu Z. Molecular mechanism underlying Akt activation in zinc-induced cardioprotection. Am J Physiol Heart Circ Physiol 2009, 297:H569-H575.
18. Cai L., Satoh M., Tohyama C., Cherian M.G. Metallothionein in radiation exposure: its induction and protective role. Toxicology 1999, 132:85-98.
19. Cai L. Diabetic cardiomyopathy and its prevention by metallothionein: experimental evidence, possible mechanisms and clinical implications. Curr Med Chem 2007, 14:2193-2203.
20. Babula P., Masarik M., Adam V., Eckschlager T., Stiborova M., Trnkova L., et al. Mammalian metallothioneins: properties and functions. Metallomics 2012, 4:739-750.
21. Zhou G., Li X., Hein D.W., Xiang X., Marshall J.P., Prabhu S.D., et al. Metallothionein suppresses angiotensin II-induced nicotinamide adenine dinucleotide phosphate oxidase activation, nitrosative stress, apoptosis, and pathological remodeling in the diabetic heart. J Am Coll Cardiol 2008, 52:655-666.
22. Cai L., Wang J., Li Y., Sun X., Wang L., Zhou Z., et al. Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 2005, 54:1829-1837.
23. Wang Y., Feng W., Xue W., Tan Y., Hein D.W., Li X.K., et al. Inactivation of GSK-3beta by metallothionein prevents diabetes-related changes in cardiac energy metabolism, inflammation, nitrosative damage, and remodeling. Diabetes 2009, 58:1391-1402.
24. Li L., Hua Y., Ren J. Short-chain fatty acid propionate alleviates Akt2 knockout-induced myocardial contractile dysfunction. Exp Diabetes Res 2012, 2012:851717.
25. DeBosch B., Sambandam N., Weinheimer C., Courtois M., Muslin A.J. Akt2 regulates cardiac metabolism and cardiomyocyte survival. J Biol Chem 2006, 281:32841-32851.
26. Etzion S., Etzion Y., DeBosch B., Crawford P.A., Muslin A.J. Akt2 deficiency promotes cardiac induction of Rab4a and myocardial beta-adrenergic hypersensitivity. J Mol Cell Cardiol 2010, 49:931-940.
27. Li X., Mikhalkova D., Gao E., Zhang J., Myers V., Zincarelli C., et al. Myocardial injury after ischemia-reperfusion in mice deficient in Akt2 is associated with increased cardiac macrophage density. Am J Physiol Heart Circ Physiol 2011, 301:H1932-H1940.
28. Hu N., Dong M., Ren J. Hydrogen sulfide alleviates cardiac contractile dysfunction in an Akt2 knockout murine model of insulin resistance: role of mitochondrial injury and apoptosis. Am J Physiol Regul Integr Comp Physiol 2014, [Mar 12 [Epub ahead of print] PubMed PMID: 24622975].
29. Kumar S.D., Vijaya M., Samy R.P., Dheen S.T., Ren M., Watt F., et al. Zinc supplementation prevents cardiomyocyte apoptosis and congenital heart defects in embryos of diabetic mice. Free Radic Biol Med 2012, 53:1595-1606.
30. Chvapil M., Owen J.A. Effect of zinc on acute and chronic isoproterenol induced heart injury. J Mol Cell Cardiol 1977, 9:151-159.
31. Capdor J., Foster M., Petocz P., Samman S. Zinc and glycemic control: a meta-analysis of randomised placebo controlled supplementation trials in humans. J Trace Elem Med Biol 2013, 27:137-142.
32. Jayawardena R., Ranasinghe P., Galappatthy P., Malkanthi R., Constantine G., Katulanda P. Effects of zinc supplementation on diabetes mellitus: a systematic review and meta-analysis. Diabetol Metab Syndr 2012, 4:13.
33. Hussain K., Challis B., Rocha N., Payne F., Minic M., Thompson A., et al. An activating mutation of AKT2 and human hypoglycemia. Science 2011, 334:474.
34. 2-terminal (sites 2+2a) phosphorylation. Am J Physiol Endocrinol Metab 2013, 304:E631-E639.
35. Wan M., Leavens K.F., Hunter R.W., Koren S., von Wilamowitz-Moellendorff A., Lu M., et al. A noncanonical, GSK3-independent pathway controls postprandial hepatic glycogen deposition. Cell Metab 2013, 18:99-105.
36. 2S in cardiovascular physiology. Curr Pharm Biotechnol 2011, 12:1385-1393.
37. Haase H., Maret W. Intracellular zinc fluctuations modulate protein tyrosine phosphatase activity in insulin/insulin-like growth factor-1 signaling. Exp Cell Res 2003, 291:289-298.
38. Wu W., Wang X., Zhang W., Reed W., Samet J.M., Whang Y.E., et al. Zinc-induced PTEN protein degradation through the proteasome pathway in human airway epithelial cells. J Biol Chem 2003, 278:28258-28263.
39. Haase H., Maret W. Fluctuations of cellular, available zinc modulate insulin signaling via inhibition of protein tyrosine phosphatases. J Trace Elem Med Biol 2005, 19:37-42.
40. Mocanu M.M., Yellon D.M. Letter to the editor: "Zinc and cardioprotection: the missing link". Am J Physiol Heart Circ Physiol 2009, 296:H233-H234. [author reply H5].
41. Georgiades S.N., Mak L.H., Angurell I., Rosivatz E., Firouz Mohd Mustapa M., Polychroni C. Identification of a potent activator of Akt phosphorylation from a novel series of phenolic, picolinic, pyridino, and hydroxamic zinc(II) complexes. J Biol Inorg Chem 2011, 16:195-208.
42. Cravero J.D., Carlson C.S., Im H.J., Yammani R.R., Long D., Loeser R.F. Increased expression of the Akt/PKB inhibitor TRB3 in osteoarthritic chondrocytes inhibits insulin-like growth factor 1-mediated cell survival and proteoglycan synthesis. Arthritis Rheum 2009, 60:492-500.
43. Du K., Herzig S., Kulkarni R.N., Montminy M. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 2003, 300:1574-1577.
44. Morse E., Schroth J., You Y.H., Pizzo D.P., Okada S., Ramachandrarao S., et al. TRB3 is stimulated in diabetic kidneys, regulated by the ER stress marker CHOP, and is a suppressor of podocyte MCP-1. Am J Physiol Renal Physiol 2010, 299:F965-F972.
45. Liu J., Wu X., Franklin J.L., Messina J.L., Hill H.S., Moellering D.R., et al. Mammalian Tribbles homolog 3 impairs insulin action in skeletal muscle: role in glucose-induced insulin resistance. Am J Physiol Endocrinol Metab 2010, 298:E565-E576.
46. Bell S.G., Vallee B.L. The metallothionein/thionein system: an oxidoreductive metabolic zinc link. Chembiochem 2009, 10:55-62.
47. Fang C.X., Doser T.A., Yang X., Sreejayan N., Ren J. Metallothionein antagonizes aging-induced cardiac contractile dysfunction: role of PTP1B, insulin receptor tyrosine phosphorylation and Akt. Aging Cell 2006, 5:177-185.
48. Xu X., Hua Y., Sreejayan N., Zhang Y., Ren J. Akt2 knockout preserves cardiac function in high-fat diet-induced obesity by rescuing cardiac autophagosome maturation. J Mol Cell Biol 2013, 5:61-63.
49. Kinlaw W.B., Levine A.S., Morley J.E., Silvis S.E., McClain C.J. Abnormal zinc metabolism in type II diabetes mellitus. Am J Med 1983, 75:273-277.
50. Bideci A., Camurdan M.O., Cinaz P., Dursun H., Demirel F. Serum zinc, insulin-like growth factor-I and insulin-like growth factor binding protein-3 levels in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 2005, 18:1007-1011.
51. Jansen J., Rosenkranz E., Overbeck S., Warmuth S., Mocchegiani E., Giacconi R., et al. Disturbed zinc homeostasis in diabetic patients by in vitro and in vivo analysis of insulinomimetic activity of zinc. J Nutr Biochem 2012, 23:1458-1466.