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Maternal zinc intake of Wistar rats has a protective effect in the alloxan-induced diabetic offspring

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Abstract

Zinc has a role in the synthesis, storage, and secretion of insulin, and has been suggested to be beneficial when used in the diabetic state. Effect of zinc intake in pregnant rats has been studied here on diabetized offspring. Pregnant rats were divided in two groups; the control group received normal food and water, and the experimental group received zinc sulfate during pregnancy and 3 weeks after offspring birth. Male offspring from the control (C) and experimental (E) groups were divided each in three groups: C1, fed with normal food and water; C2, diabetized with alloxan; C3, received zinc sulfate; E1, fed with normal food and water; E2, diabetized with alloxan; and E3, receiving zinc sulfate. After 30 days, the histological changes of pancreatic tissues were investigated by light microscopy. Body weight, blood glucose, serum insulin levels, food intake, water intake, and urine quantity were also compared between the groups. Water intake and urine quantity were decreased significantly (p < 0.01and p < 0.001) in E2 (experimental diabetic group) in comparison with C2 (control diabetic group), but there was no significant difference in the body weight in C2 in comparison with E2, while blood glucose was decreased significantly (p < 0.001) and blood insulin level was increased significantly (p < 0.01) in E2 in comparison with C2. Microscopic evaluation of pancreas showed that E2 were protected against alloxan-induced beta-cell degeneration. In conclusion, this work showed that maternal zinc intake may influence subsequent deleterious effects of diabetes on alloxan-diabetized offspring.

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References

  1. American Diabetes Association (2008) Standards of medical care in diabetes—2008. Diabetes Care 31(Suppl 1):S12–S54

    Article  Google Scholar 

  2. American Diabetes Association (2011) Diagnosis and classification of diabetes mellitus. Diabetes Care 34(Suppl 1):S62–S69

    Article  Google Scholar 

  3. Astrup AS (2011) Cardiovascular morbidity and mortality in diabetes mellitus: prediction and prognosis. Dan Med Bull 58:B4152

    PubMed  Google Scholar 

  4. Barrio DA, Etcheverry SB (2010) Potential use of vanadium compounds in therapeutics. Curr Med Chem 17:3632–3642

    Article  PubMed  CAS  Google Scholar 

  5. Beletate V, El Dib RP, Atallah ÁN (2007) Zinc supplementation for the prevention of type 2 diabetes mellitus. Cochrane Database of Syst Rev. doi:10.1002/14651858.CD005525.pub2

  6. Bolkent S, Yanardag R, Mutlu O, Yildirim S, Kangawa K, Minegishi Y, Suzuki H (2006) The effect of zinc supplementation on ghrelin-immunoreactive cells and lipid parameters in gastrointestinal tissue of streptozotocin-induced female diabetic rats. Mol Cell Biochem 286:77–85

    Article  PubMed  CAS  Google Scholar 

  7. Brand IA, Kleineke J (1996) Intracellular zinc movement and its effect on the carbohydrate metabolism of isolated rat hepatocytes. J Biol Chem 271:1941–1949

    Article  PubMed  CAS  Google Scholar 

  8. Brown KH, Rivera JA, Bhutta Z, Gibson RS, King JC, Lonnerdal B, Ruel MT, Sandtrom B, Wasantwisut E, Hotz C (2004) International Zinc Nutrition Consultative Group (IZiNCG) technical document #1. Assessment of the risk of zinc deficiency in populations and options for its control. Food Nutr Bull 25:S99–S203

    PubMed  Google Scholar 

  9. Caulfield LE, Zavaleta N, Shankar AH, Merialdi M (1998) Potential contribution of maternal zinc supplementation during pregnancy to maternal and child survival. Am J Clin Nutr 68:499S–508S

    PubMed  CAS  Google Scholar 

  10. Chaves S, Jelic R, Mendonca C, Carrasco M, Yoshikawa Y, Sakurai H, Santos MA (2011) Complexes of hydroxy(thio)pyrone and hydroxy(thio)pyridinone with Zn(II) and Mo(VI). Thermodynamic stability and insulin-mimetic activity. Metallomics 2:220–227

    Article  Google Scholar 

  11. Chen MD, Liou SJ, Lin PY, Yang VC, Alexander PS, Lin WH (1998) Effects of zinc supplementation on the plasma glucose level and insulin activity in genetically obese (ob/ob) mice. Biol Trace Elem Res 61:303–311

    Article  PubMed  CAS  Google Scholar 

  12. Dodson G, Steiner D (1998) The role of assembly in insulin's biosynthesis. Curr Opin Struct Biol 8:189–194

    Article  PubMed  CAS  Google Scholar 

  13. Dunn JS, Mcletchie N (1943) Experimental alloxan diabetes in the rat. Lancet 242:484–487

    Google Scholar 

  14. Elsner M, Gurgul-Convey E, Lenzen S (2006) Relative importance of cellular uptake and reactive oxygen species for the toxicity of alloxan and dialuric acid to insulin-producing cells. Free Radic Biol Med 41:825–834

    Article  PubMed  CAS  Google Scholar 

  15. Emdin SO, Dodson GG, Cutfield JM, Cutfield SM (1980) Role of zinc in insulin biosynthesis. Some possible zinc-insulin interactions in the pancreatic B-cell. Diabetologia 19:174–182

    Article  PubMed  CAS  Google Scholar 

  16. Foster M, Samman S (2010) Zinc and redox signaling: perturbations associated with cardiovascular disease and diabetes mellitus. Antioxid Redox Signal 13:1549–1573

    Article  PubMed  CAS  Google Scholar 

  17. Gandy SE, Buse MG, Crouch RK (1982) Protective role of superoxide dismutase against diabetogenic drugs. J Clin Invest 70:650–658

    Article  PubMed  CAS  Google Scholar 

  18. Gao LH, Liu WP, Wang BL, Li L, Xie MJ, Li YR, Chen ZH, Chen XZ (2006) Effects of bis(alpha-furancarboxylato)oxovanadium(IV) on non-diabetic and streptozotocin-diabetic rats. Clin Chim Acta 368:173–178

    Article  PubMed  CAS  Google Scholar 

  19. Gunasekara P, Hettiarachchi M, Liyanage C, Lekamwasam S (2011) Effects of zinc and multimineral vitamin supplementation on glycemic and lipid control in adult diabetes. Diabetes Metab Syndr Obes 4:53–60

    PubMed  CAS  Google Scholar 

  20. Haase H, Rink L (2009) The immune system and the impact of zinc during aging. Immun Ageing 6:1–17

    Article  Google Scholar 

  21. Harati M, Ani M (2004) Vanadyl sulfate ameliorates insulin resistance and restores plasma dehydroepiandrosterone-sulfate levels in fructose-fed, insulin-resistant rats. Clin Biochem 37:694–697

    Article  PubMed  CAS  Google Scholar 

  22. Heidari Z, Mahmoudzadeh-Sagheb H, Moudi B (2008) A quantitative study of sodium tungstate protective effect on pancreatic beta cells in streptozotocin-induced diabetic rats. Micron 39:1300–1305

    Article  PubMed  CAS  Google Scholar 

  23. Hess SY, King JC (2009) Effects of maternal zinc supplementation on pregnancy and lactation outcomes. Food Nutr Bull 30:S60–S78

    PubMed  Google Scholar 

  24. Ho E, Quan N, Tsai YH, Lai W, Bray TM (2001) Dietary zinc supplementation inhibits NFkappaB activation and protects against chemically induced diabetes in CD1 mice. Exp Biol Med (Maywood) 226:103–111

    CAS  Google Scholar 

  25. Honscheid A, Rink L, Haase H (2009) T-lymphocytes: a target for stimulatory and inhibitory effects of zinc ions. Endocr Metab Immune Disord Drug Targets 9:132–144

    Article  PubMed  Google Scholar 

  26. Hossain MB, Kelleher SL, Lonnerdal B (2011) Maternal iron and zinc supplementation during pregnancy affects body weight and iron status in rat pups at weaning. J Nutr 141:798–804

    Article  PubMed  CAS  Google Scholar 

  27. Huber AM, Gershoff SN (1973) Effect of zinc deficiency in rats on insulin release from the pancreas. J Nutr 103:1739–1744

    PubMed  CAS  Google Scholar 

  28. Ilouz R, Kaidanovich O, Gurwitz D, Eldar-Finkelman H (2002) Inhibition of glycogen synthase kinase-3 [beta] by bivalent zinc ions: insight into the insulin-mimetic action of zinc. Biochem Biophys Res Commun 295:102–106

    Article  PubMed  CAS  Google Scholar 

  29. Jakusch T, Hollender D, Enyedy EA, Gonzalez CS, Montes-Bayon M, Sanz-Medel A, Costa Pessoa J, Tomaz I, Kiss T (2009) Biospeciation of various antidiabetic V(IV)O compounds in serum. Dalton Trans 13:2428–2437

    Article  PubMed  Google Scholar 

  30. Jansen J, Karges W, Rink L (2009) Zinc and diabetes—clinical links and molecular mechanisms. J Nutr Biochem 20:399–417

    Article  PubMed  CAS  Google Scholar 

  31. Kazi TG, Afridi HI, Kazi N, Jamali MK, Arain MB, Jalbani N, Kandhro GA (2008) Copper, chromium, manganese, iron, nickel, and zinc levels in biological samples of diabetes mellitus patients. Biol Trace Elem Res 122:1–18

    Article  PubMed  CAS  Google Scholar 

  32. Kechrid Z, Bouzerna N (2004) Effect of zinc deficiency on zinc and carbohydrate metabolism in genetically diabetic (C57BL/Ksj Db+/Db+) and non-diabetic original strain (C57BL/Ksj) Mice. Turk J Med Sci 34:367–373

    CAS  Google Scholar 

  33. King JC (2000) Determinants of maternal zinc status during pregnancy. Am J Clin Nutr 71:1334S–1343S

    PubMed  CAS  Google Scholar 

  34. Kinlaw WB, Levine AS, Morley JE, Silvis SE, McClain CJ (1983) Abnormal zinc metabolism in type II diabetes mellitus. Am J Med 75:273–277

    Article  PubMed  CAS  Google Scholar 

  35. Laiteerapong N, Karter AJ, Liu JY, Moffet HH, Sudore R, Schillinger D, John PM, Huang ES (2011) Correlates of quality of life in older adults with diabetes: the diabetes & aging study. Diabetes Care 34:1749–1753

    Article  PubMed  Google Scholar 

  36. Lemaire K, Ravier MA, Schraenen A, Creemers JW, Van de Plas R, Granvik M, Van Lommel L, Waelkens E, Chimienti F, Rutter GA, Gilon P, in’t Veld PA, Schuit FC (2009) Insulin crystallization depends on zinc transporter ZnT8 expression, but is not required for normal glucose homeostasis in mice. Proc Natl Acad Sci U S A 106:14872–14877

    Article  PubMed  CAS  Google Scholar 

  37. Lenzen S (2008) The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetologia 51:216–226

    Article  PubMed  CAS  Google Scholar 

  38. Miranda ER, Dey CS (2004) Effect of chromium and zinc on insulin signaling in skeletal muscle cells. Biol Trace Elem Res 101:19–36

    Article  PubMed  CAS  Google Scholar 

  39. Nicolson TJ, Bellomo EA, Wijesekara N, Loder MK, Baldwin JM, Gyulkhandanyan AV, Koshkin V, Tarasov AI, Carzaniga R, Kronenberger K, Taneja TK, da Silva XG, Libert S, Froguel P, Scharfmann R, Stetsyuk V, Ravassard P, Parker H, Gribble FM, Reimann F, Sladek R, Hughes SJ, Johnson PR, Masseboeuf M, Burcelin R, Baldwin SA, Liu M, Lara-Lemus R, Arvan P, Schuit FC, Wheeler MB, Chimienti F, Rutter GA (2009) Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 58:2070–2083

    Article  PubMed  CAS  Google Scholar 

  40. Nomura Y, Okamoto S, Sakamoto M, Feng Z, Nakamura T (2005) Effect of cobalt on the liver glycogen content in the streptozotocin-induced diabetic rats. Mol Cell Biochem 277:127–130

    Article  PubMed  CAS  Google Scholar 

  41. Park JH, Grandjean CJ, Hart MH, Erdman SH, Pour P, Vanderhoof JA (1986) Effect of pure zinc deficiency on glucose tolerance and insulin and glucagon levels. Am J Physiol 251:E273–E278

    PubMed  CAS  Google Scholar 

  42. Rashid K, Bhattacharya S, Sil PC (2012) Protective role of D-saccharic acid-1, 4-lactone in alloxan induced oxidative stress in the spleen tissue of diabetic rats is mediated by suppressing mitochondria dependent apoptotic pathway. Free Radic Res 46:240–252

    Article  PubMed  CAS  Google Scholar 

  43. Reeves PG, O'Dell BL (1983) The effect of zinc deficiency on glucose metabolism in meal-fed rats. Br J Nutr 49:441–452

    Article  PubMed  CAS  Google Scholar 

  44. Robinson LK, Hurley LS (1981) Effect of maternal zinc deficiency of food restriction on rat fetal pancreas. 2. Insulin and glucagon. J Nutr 111:869–877

    PubMed  CAS  Google Scholar 

  45. Rungby J (2010) Zinc, zinc transporters and diabetes. Diabetologia 53:1549–1551

    Article  PubMed  CAS  Google Scholar 

  46. Russell MS, Bailey J, Duffy SJ, Vogels CM, Broderick TL, Westcott SA (2006) Gut transport of a molybdenum/ascorbic acid complex. Drugs R&D 7:111–117

    Article  CAS  Google Scholar 

  47. Saaka M, Oosthuizen J, Beatty S (2009) Effect of prenatal zinc supplementation on birth weight. J Health Popul Nutr 27:619–631

    Article  PubMed  Google Scholar 

  48. Shakher J, Stevens MJ (2011) Update on the management of diabetic polyneuropathies. Diabetes Metab Syndr Obes 4:289–305

    PubMed  Google Scholar 

  49. Sondergaard LG, Stoltenberg M, Doering P, Flyvbjerg A, Rungby J (2006) Zinc ions in the endocrine and exocrine pancreas of zinc deficient rats. Histol Histopathol 21:619–625

    PubMed  CAS  Google Scholar 

  50. Srivastava AK, Mehdi MZ (2005) Insulino-mimetic and anti-diabetic effects of vanadium compounds. Diabet Med 22:2–13

    Article  PubMed  CAS  Google Scholar 

  51. Tang Y, Yang Q, Lu J, Zhang X, Suen D, Tan Y, Jin L, Xiao J, Xie R, Rane M, Li X, Cai L (2010) Zinc supplementation partially prevents renal pathological changes in diabetic rats. J Nutr Biochem 21:237–246

    Article  PubMed  CAS  Google Scholar 

  52. Thaete LG, Crouch RK, Buse MG, Spicer SS (1985) The protective role of copper-zinc superoxide dismutase against alloxan-induced diabetes: morphological aspects. Diabetologia 28:677–682

    Article  PubMed  CAS  Google Scholar 

  53. Tobia MH, Zdanowicz MM, Wingertzahn MA, McHeffey-Atkinson B, Slonim AE, Wapnir RA (1998) The role of dietary zinc in modifying the onset and severity of spontaneous diabetes in the BB Wistar rat. Mol Genet Metab 63:205–213

    Article  PubMed  CAS  Google Scholar 

  54. Trumbo P, Yates AA, Schlicker S, Poos M (2001) Dietary reference intakes vitamin a, vitamin k, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J Am Diet Assoc 101:294–301

    Article  PubMed  CAS  Google Scholar 

  55. Uriu-Adams JY, Keen CL (2010) Zinc and reproduction: effects of zinc deficiency on prenatal and early postnatal development. Birth Defects Res B Dev Reprod Toxicol 89:313–325

    Article  PubMed  CAS  Google Scholar 

  56. Viktorinova A, Toserova E, Krizko M, Durackova Z (2009) Altered metabolism of copper, zinc, and magnesium is associated with increased levels of glycated hemoglobin in patients with diabetes mellitus. Metabolism 58:1477–1482

    Article  PubMed  CAS  Google Scholar 

  57. Wang J, Song Y, Elsherif L, Song Z, Zhou G, Prabhu SD, Saari JT, Cai L (2006) Cardiac metallothionein induction plays the major role in the prevention of diabetic cardiomyopathy by zinc supplementation. Circulation 113:544–554

    Article  PubMed  CAS  Google Scholar 

  58. Wenzlau JM, Juhl K, Yu L, Moua O, Sarkar SA, Gottlieb P, Rewers M, Eisenbarth GS, Jensen J, Davidson HW, Hutton JC (2007) The cation efflux transporter ZnT8 (Slc30A8) is a major autoantigen in human type 1 diabetes. Proc Natl Acad Sci U S A 104:17040–17045

    Article  PubMed  CAS  Google Scholar 

  59. Wiernsperger N, Rapin J (2010) Trace elements in glucometabolic disorders: an update. Diabetol Metab Syndr 19:70

    Article  Google Scholar 

  60. Wijesekara N, Dai FF, Hardy AB, Giglou PR, Bhattacharjee A, Koshkin V, Chimienti F, Gaisano HY, Rutter GA, Wheeler MB (2010) Beta cell-specific Znt8 deletion in mice causes marked defects in insulin processing, crystallisation and secretion. Diabetologia 53:1656–1668

    Article  PubMed  CAS  Google Scholar 

  61. Winterbourn CC, Munday R (1989) Glutathione-mediated redox cycling of alloxan. Mechanisms of superoxide dismutase inhibition and of metal-catalyzed OH formation. Biochem Pharmacol 38:271–277

    Article  PubMed  CAS  Google Scholar 

  62. Zampelas A (2011) Zinc supplementation: another myth or we are heading towards a new era in the treatment of diabetes? Atherosclerosis 219:22–23

    Article  PubMed  CAS  Google Scholar 

  63. Zhang Z, Jiang J, Yu P, Zeng X, Larrick JW, Wang Y (2009) Hypoglycemic and beta cell protective effects of andrographolide analogue for diabetes treatment. J Transl Med 7:62

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, School of Basic Science, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Parichehreh Yaghmaei, Hamideh Esfahani-Nejad & Nasim Hayati-Roodbari

  2. Department of Biology, Islamic Azad University, Qom, Iran

    Ramesh Ahmadi

  3. Endocrinology and Metabolism Research Center, Tehran University of Medical Sciences, Tehran, Iran

    Azadeh Ebrahim-Habibi

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  1. Parichehreh Yaghmaei
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Yaghmaei, P., Esfahani-Nejad, H., Ahmadi, R. et al. Maternal zinc intake of Wistar rats has a protective effect in the alloxan-induced diabetic offspring. J Physiol Biochem 69, 35–43 (2013). https://doi.org/10.1007/s13105-012-0185-8

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