Zinc protects against diabetes-induced pathogenic changes in the aorta: Roles of metallothionein and nuclear factor (erythroid-derived 2)-like 2

Cardiovascular Diabetology

Volumn 12, Issue 1, 2013, Pages

  Miao, Xiao ^a,c   Wang, Yonggang ^b,c   Sun, Jian ^b   Sun, Weixia ^b,c   Tan, Yi ^c,d   Cai, Lu ^c,d   Zheng, Yang ^b   Su, Guanfang ^a   Liu, Quan ^b   Wang, Yuehui ^a  

^a THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^b THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

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

^d WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Diabetes; Metallothionein; Nrf2; Oxidative stress; Vascular damage; Zinc

Indexed keywords

METALLOTHIONEIN; TRANSCRIPTION FACTOR NRF2; ZINC;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; AORTA; AORTA DISEASE; ARTICLE; BLOOD VESSEL WALL; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC ANGIOPATHY; DIET SUPPLEMENTATION; DRUG MECHANISM; FEMALE; FIBROSIS; HEART PROTECTION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE; UPREGULATION;

ANIMALS; AORTA, THORACIC; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FEMALE; MALE; METALLOTHIONEIN; MICE; MICE, TRANSGENIC; NF-E2-RELATED FACTOR 2; UP-REGULATION; ZINC;

EID: 84875283820     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-12-54     Document Type: Article

References (61)

1. Chen H, Goldberg MS, Burnett RT, Jerrett M, Wheeler AJ, Villeneuve PJ. Long-term exposure to traffic-related air pollution and cardiovascular mortality. Epidemiol 2013, 24(1):35-43.
2. Brunekreef B, Beelen R, Hoek G, Schouten L, Bausch-Goldbohm S, Fischer P, Armstrong B, Hughes E, Jerrett M, Van Den Brandt P. Effects of long-term exposure to traffic-related air pollution on respiratory and cardiovascular mortality in the Netherlands: the NLCS-AIR study. Res Rep Health Eff Inst 2009, (139):5-71. discussion 73-89.
3. James J, Soyibo AK, Hurlock L, Gordon-Strachan G, Barton EN. Cardiovascular risk factors in an eastern Caribbean island: prevalence of non-communicable chronic diseases and associated lifestyle risk factors for cardiovascular morbidity and mortality in the British Virgin Islands. West Indian Med J 2012, 61(4):429-436. 10.7727/wimj.2012.173, 23240481.
4. Bell EJ, Lutsey PL, Windham BG, Folsom AR. Physical Activity and Cardiovascular Disease in African Americans in ARIC. Med Sci Sports Exerc 2012, PMID: 23247714.
5. Wannamethee SG, Papacosta O, Lawlor DA, Whincup PH, Lowe GD, Ebrahim S, Sattar N. Do women exhibit greater differences in established and novel risk factors between diabetes and non-diabetes than men? The British Regional Heart Study and British Women's Heart Health Study. Diabetologia 2012, 55(1):80-87. 10.1007/s00125-011-2284-4, 21861177.
6. Wong NL, Achike FI. Gender discrimination in the influence of hyperglycemia and hyperosmolarity on rat aortic tissue responses to insulin. Regul Pept 2010, 163(1-3):113-119.
7. Donahue RP, Rejman K, Rafalson LB, Dmochowski J, Stranges S, Trevisan M. Sex differences in endothelial function markers before conversion to pre-diabetes: does the clock start ticking earlier among women? The Western New York Study. Diabetes Care 2007, 30(2):354-359. 10.2337/dc06-1772, 17259507.
8. Fukada T, Yamasaki S, Nishida K, Murakami M, Hirano T. Zinc homeostasis and signaling in health and diseases: Zinc signaling. J Biol Inorg Chem 2011, 16(7):1123-1134. 10.1007/s00775-011-0797-4, 3176402, 21660546.
9. McClain C, Morris P, Hennig B. Zinc and endothelial function. Nutrition 1995, 11(1 Suppl):117-120.
10. Hennig B, Meerarani P, Toborek M, McClain CJ. Antioxidant-like properties of zinc in activated endothelial cells. J Am Coll Nutr 1999, 18(2):152-158.
11. Meerarani P, Ramadass P, Toborek M, Bauer HC, Bauer H, Hennig B. Zinc protects against apoptosis of endothelial cells induced by linoleic acid and tumor necrosis factor alpha. Am J Clin Nutr 2000, 71(1):81-87.
12. Jenner A, Ren M, Rajendran R, Ning P, Huat BT, Watt F, Halliwell B. Zinc supplementation inhibits lipid peroxidation and the development of atherosclerosis in rabbits fed a high cholesterol diet. Free Radic Biol Med 2007, 42(4):559-566. 10.1016/j.freeradbiomed.2006.11.024, 17275688.
13. Alissa EM, Bahijri SM, Lamb DJ, Ferns GA. The effects of coadministration of dietary copper and zinc supplements on atherosclerosis, antioxidant enzymes and indices of lipid peroxidation in the cholesterol-fed rabbit. Int J Exp Pathol 2004, 85(5):265-275. 10.1111/j.0959-9673.2004.00392.x, 2517529, 15379959.
14. Cortese MM, Suschek CV, Wetzel W, Kroncke KD, Kolb-Bachofen V. Zinc protects endothelial cells from hydrogen peroxide via Nrf2-dependent stimulation of glutathione biosynthesis. Free Radic Biol Med 2008, 44(12):2002-2012. 10.1016/j.freeradbiomed.2008.02.013, 18355458.
15. Ha KN, Chen Y, Cai J, Sternberg P. Increased glutathione synthesis through an ARE-Nrf2-dependent pathway by zinc in the RPE: implication for protection against oxidative stress. Invest Ophthalmol Vis Sci 2006, 47(6):2709-2715. 10.1167/iovs.05-1322, 16723490.
16. Lee JM, Johnson JA. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 2004, 37(2):139-143. 10.5483/BMBRep.2004.37.2.139, 15469687.
17. Li B, Liu S, Miao L, Cai L. Prevention of diabetic complications by activation of Nrf2: diabetic cardiomyopathy and nephropathy. Exp Diabetes Res 2012, 2012:216512. 3356887, 22645602.
18. Wang J, Song Y, Elsherif L, Song Z, Zhou G, Prabhu SD, Saari JT, Cai L. Cardiac metallothionein induction plays the major role in the prevention of diabetic cardiomyopathy by zinc supplementation. Circulation 2006, 113(4):544-554. 10.1161/CIRCULATIONAHA.105.537894, 16432057.
19. Islam MS, Du Loots T. Diabetes, metallothionein, and zinc interactions: a review. Biofactors 2007, 29(4):203-212. 10.1002/biof.5520290404, 18057551.
20. Yang J, Cherian MG. Protective effects of metallothionein on streptozotocin-induced diabetes in rats. Life Sci 1994, 55(1):43-51. 10.1016/0024-3205(94)90080-9, 8015348.
21. Cai L, Wang Y, Zhou G, Chen T, Song Y, Li X, Kang YJ. Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy. J Am Coll Cardiol 2006, 48(8):1688-1697.
22. Dong F, Li Q, Sreejayan N, Nunn JM, Ren J. Metallothionein prevents high-fat diet induced cardiac contractile dysfunction: role of peroxisome proliferator activated receptor gamma coactivator 1alpha and mitochondrial biogenesis. Diabetes 2007, 56(9):2201-2212. 10.2337/db06-1596, 17575086.
23. Ohly P, Dohle C, Abel J, Seissler J, Gleichmann H. Zinc sulphate induces metallothionein in pancreatic islets of mice and protects against diabetes induced by multiple low doses of streptozotocin. Diabetologia 2000, 43(8):1020-1030. 10.1007/s001250050009, 10990080.
24. Tang Y, Yang Q, Lu J, Zhang X, Suen D, Tan Y, Jin L, Xiao J, Xie R, Rane M. Zinc supplementation partially prevents renal pathological changes in diabetic rats. J Nutr Biochem 2010, 21(3):237-246. 10.1016/j.jnutbio.2008.12.010, 19369054.
25. Yang J, Tan Y, Zhao F, Ma Z, Wang Y, Zheng S, Epstein PN, Yu J, Yin X, Zheng Y. Angiotensin II plays a critical role in diabetic pulmonary fibrosis most likely via activation of NADPH oxidase-mediated nitrosative damage. Am J Physiol Endocrinol Metab 2011, 301(1):E132-E144. 10.1152/ajpendo.00629.2010, 21487074.
26. Cui W, Li B, Bai Y, Miao X, Chen Q, Sun W, Tan Y, Luo P, Zhang C, Zheng S. Potential role for Nrf2 activation in the therapeutic effect of MG132 on diabetic nephropathy in OVE26 diabetic mice. Am J Physiol Endocrinol Metab 2013, 304(1):E87-E99. 10.1152/ajpendo.00430.2012, 23132297.
27. Epstein PN, Overbeek PA, Means AR. Calmodulin-induced early-onset diabetes in transgenic mice. Cell 1989, 58(6):1067-1073. 10.1016/0092-8674(89)90505-9, 2673540.
28. Zheng S, Noonan WT, Metreveli NS, Coventry S, Kralik PM, Carlson EC, Epstein PN. Development of late-stage diabetic nephropathy in OVE26 diabetic mice. Diabetes 2004, 53(12):3248-3257. 10.2337/diabetes.53.12.3248, 15561957.
29. Ozcelik D, Naziroglu M, Tuncdemir M, Celik O, Ozturk M, Flores-Arce MF. Zinc supplementation attenuates metallothionein and oxidative stress changes in kidney of streptozotocin-induced diabetic rats. Biol Trace Elem Res 2012, 150(1-3):342-349.
30. 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(3):523-528. 10.2337/dc06-1682, 17327315.
31. Reiterer G, MacDonald R, Browning JD, Morrow J, Matveev SV, Daugherty A, Smart E, Toborek M, Hennig B. Zinc deficiency increases plasma lipids and atherosclerotic markers in LDL-receptor-deficient mice. J Nutr 2005, 135(9):2114-2118.
32. 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(5):577-587.
33. Tomat AL, Costa Mde L, Arranz CT. Zinc restriction during different periods of life: influence in renal and cardiovascular diseases. Nutrition 2011, 27(4):392-398. 10.1016/j.nut.2010.09.010, 21074972.
34. De Oliveira Otto MC, Alonso A, Lee DH, Delclos GL, Bertoni AG, Jiang R, Lima JA, Symanski E, Jacobs DR, Nettleton JA. Dietary intakes of zinc and heme iron from red meat, but not from other sources, are associated with greater risk of metabolic syndrome and cardiovascular disease. J Nutr 2012, 142(3):526-533. 10.3945/jn.111.149781, 3278268, 22259193.
35. Simon DI. Inflammation and vascular injury: basic discovery to drug development. Circ J 2012, 76(8):1811-1818. 10.1253/circj.CJ-12-0801, 22785436.
36. Ishigami N, Isoda K, Adachi T, Niida T, Kujiraoka T, Hakuno D, Kondo H, Kusuhara M, Ohsuzu F. Deficiency of CuZn superoxide dismutase promotes inflammation and alters medial structure following vascular injury. J Atheroscler Thromb 2011, 18(11):1009-1017. 10.5551/jat.9324, 21946535.
37. Puntmann VO, Taylor PC, Mayr M. Coupling vascular and myocardial inflammatory injury into a common phenotype of cardiovascular dysfunction: systemic inflammation and aging - a mini-review. Gerontology 2011, 57(4):295-303. 10.1159/000316577, 20551624.
38. Davis C, Fischer J, Ley K, Sarembock IJ. The role of inflammation in vascular injury and repair. J Thromb Haemost 2003, 1(8):1699-1709. 10.1046/j.1538-7836.2003.00292.x, 12911580.
39. Zhang D, Li Y, Zhu T, Zhang F, Yang Z, Miao D. Zinc supplementation results in improved therapeutic potential of bone marrow-derived mesenchymal stromal cells in a mouse ischemic limb model. Cytotherapy 2011, 13(2):156-164. 10.3109/14653249.2010.512633, 20839997.
40. Heidarian E, Amini M, Parham M, Aminorroaya A. Effect of zinc supplementation on serum homocysteine in type 2 diabetic patients with microalbuminuria. Rev Diabet Stud 2009, 6(1):64-70. 10.1900/RDS.2009.6.64, 2712914, 19557297.
41. Hashemipour M, Kelishadi R, Shapouri J, Sarrafzadegan N, Amini M, Tavakoli N, Movahedian-Attar A, Mirmoghtadaee P, Poursafa P. Effect of zinc supplementation on insulin resistance and components of the metabolic syndrome in prepubertal obese children. Hormones (Athens) 2009, 8(4):279-285.
42. Parham M, Amini M, Aminorroaya A, Heidarian E. Effect of zinc supplementation on microalbuminuria in patients with type 2 diabetes: a double blind, randomized, placebo-controlled, cross-over trial. Rev Diabet Stud 2008, 5(2):102-109. 10.1900/RDS.2008.5.102, 2556442, 18795212.
43. Bao B, Prasad AS, Beck FW, Snell D, Suneja A, Sarkar FH, Doshi N, Fitzgerald JT, Swerdlow P. Zinc supplementation decreases oxidative stress, incidence of infection, and generation of inflammatory cytokines in sickle cell disease patients. Transl Res 2008, 152(2):67-80. 10.1016/j.trsl.2008.06.001, 18674741.
44. Miao X, Bai Y, Su W, Cui W, Xin Y, Wang Y, Tan Y, Miao L, Fu Y, Su G. Sulforaphane prevention of diabetes-induced aortic damage was associated with the up-regulation of Nrf2 and its down-stream antioxidants. Nutr Metab (Lond) 2012, 9(1):84.
45. Prevost G, Bulckaen H, Gaxatte C, Boulanger E, Beraud G, Creusy C, Puisieux F, Fontaine P. Structural modifications in the arterial wall during physiological aging and as a result of diabetes mellitus in a mouse model: are the changes comparable?. Diabetes Metab 2011, 37(2):106-111. 10.1016/j.diabet.2010.08.005, 21144786.
46. Nuno DW, Lamping KG. The role of rho kinase in sex-dependent vascular dysfunction in type 1 diabetes. Exp Diabetes Res 2010, 2010:176361. 2846338, 20368772.
47. Sasaki N, Yamashita T, Takaya T, Shinohara M, Shiraki R, Takeda M, Emoto N, Fukatsu A, Hayashi T, Ikemoto K. Augmentation of vascular remodeling by uncoupled endothelial nitric oxide synthase in a mouse model of diabetes mellitus. Arterioscler Thromb Vasc Biol 2008, 28(6):1068-1076. 10.1161/ATVBAHA.107.160754, 18403727.
48. Uemura S, Matsushita H, Li W, Glassford AJ, Asagami T, Lee KH, Harrison DG, Tsao PS. Diabetes mellitus enhances vascular matrix metalloproteinase activity: role of oxidative stress. Circ Res 2001, 88(12):1291-1298. 10.1161/hh1201.092042, 11420306.
49. Wold LE, Ren J. Streptozotocin directly impairs cardiac contractile function in isolated ventricular myocytes via a p38 map kinase-dependent oxidative stress mechanism. Biochem Biophys Res Commun 2004, 318(4):1066-1071. 10.1016/j.bbrc.2004.04.138, 15147982.
50. Teiken JM, Audettey JL, Laturnus DI, Zheng S, Epstein PN, Carlson EC. Podocyte loss in aging OVE26 diabetic mice. Anat Rec (Hoboken) 2008, 291(1):114-121.
51. Zheng S, Carlson EC, Yang L, Kralik PM, Huang Y, Epstein PN. Podocyte-specific overexpression of the antioxidant metallothionein reduces diabetic nephropathy. J Am Soc Nephrol 2008, 19(11):2077-2085. 10.1681/ASN.2007080967, 2573005, 18632844.
52. Zhang X, Ye G, Duan J, Chen AF, Ren J. Influence of gender on intrinsic contractile properties of isolated ventricular myocytes from calmodulin-induced diabetic transgenic mice. Endocr Res 2003, 29(2):227-236. 10.1081/ERC-120022318, 12856810.
53. He X, Kan H, Cai L, Ma Q. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol 2009, 46(1):47-58. 10.1016/j.yjmcc.2008.10.007, 19007787.
54. De Haan JB. Nrf2 activators as attractive therapeutics for diabetic nephropathy. Diabetes 2011, 60(11):2683-2684. 10.2337/db11-1072, 3198074, 22025774.
55. Mehta AJ, Joshi PC, Fan X, Brown LA, Ritzenthaler JD, Roman J, Guidot DM. Zinc supplementation restores PU.1 and Nrf2 nuclear binding in alveolar macrophages and improves redox balance and bacterial clearance in the lungs of alcohol-fed rats. Alcohol Clin Exp Res 2011, 35(8):1519-1528. 3128659, 21447000.
56. Liang Q, Carlson EC, Donthi RV, Kralik PM, Shen X, Epstein PN. Overexpression of metallothionein reduces diabetic cardiomyopathy. Diabetes 2002, 51(1):174-181.
57. Song Y, Wang J, Li Y, Du Y, Arteel GE, Saari JT, Kang YJ, Cai L. Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. Am J Pathol 2005, 167(1):17-26. 10.1016/S0002-9440(10)62949-5, 1603431, 15972948.
58. Cai L. Suppression of nitrative damage by metallothionein in diabetic heart contributes to the prevention of cardiomyopathy. Free Radic Biol Med 2006, 41(6):851-861. 10.1016/j.freeradbiomed.2006.06.007, 16934665.
59. Zhou G, Li X, Hein DW, Xiang X, Marshall JP, Prabhu SD, Cai L. 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(8):655-666. 10.1016/j.jacc.2008.05.019, 18702970.
60. Yi T, Cheema Y, Tremble SM, Bell SP, Chen Z, Subramanian M, LeWinter MM, VanBuren P, Palmer BM. Zinc-induced cardiomyocyte relaxation in a rat model of hyperglycemia is independent of myosin isoform. Cardiovasc Diabetol 2012, 11:135. 10.1186/1475-2840-11-135, 3537566, 23116444.
61. Zbinden S, Wang J, Adenika R, Schmidt M, Tilan JU, Najafi AH, Peng X, Lassance-Soares RM, Iantorno M, Morsli H. Metallothionein enhances angiogenesis and arteriogenesis by modulating smooth muscle cell and macrophage function. Arterioscler Thromb Vasc Biol 2010, 30(3):477-482. 10.1161/ATVBAHA.109.200949, 20056912.