European Journal of Nutrition

, Volume 56, Issue 2, pp 819–830 | Cite as

Metabolic syndrome and selenium during gestation and lactation

  • Fátima Nogales
  • M. Luisa Ojeda
  • Paulina Muñoz del Valle
  • Alejandra Serrano
  • M. Luisa Murillo
  • Olimpia Carreras Sánchez
Original Contribution

Abstract

Purpose

Selenium (Se) has a dual role in metabolic syndrome (MS) development as it has an antioxidant action against both “good” and “bad” reactive oxygen species. This study evaluates Se body profile in dams which present MS during gestation and lactation, in order to elucidate a normal dietary Se’s implication in this pathology.

Method

Rats were randomized into control (C) and fructose (F) groups. The rich fructose diet (65 %) during gestation and lactation periods induced MS in dams. Se body distribution was determined by atomic absorption spectrophotometry, and the hepatic activity of the four antioxidant enzymes and the bimolecular oxidation were determined by spectrophotometry. The cardiac activity was monitored using the indirect tail occlusion method. Lipid and glucidic profile was also analyzed.

Results

Despite the fact that the diet supplied has 0.1 ppm of Se, the minimal dietary requirement for rats, F dams ate less amount of food, and therefore, they had lower Se retention. However, they had normal levels of Se in serum and milk. Dams with MS had Se depletion in heart and muscle joint to hypertension and a lower heart rate, and Se repletion in liver and kidney. Despite the increase in hepatic glutathione peroxidase (GPx) and catalase activity found, lipid oxidation occurred—probably because superoxide dismutase activity was diminished. In heart, the activity and expression of the selenoprotein GPx1 were decreased.

Conclusion

With these results, it is not possible to elucidate whether a dietary Se supplementation or a Se-restricted diet are good for MS; because despite the fact that GPx activity is increased in liver, it is also found, for the first time, that heart Se deposits are significantly decreased during MS.

Keywords

Metabolic syndrome Selenium Gestation Lactation 

Notes

Acknowledgments

The authors acknowledge the grants from Andalusian Regional Government for its support to CTS-193 research group.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

References

  1. 1.
    Day C (2007) Metabolic syndrome, or What you will: definitions and epidemiology. Diab Vasc Dis Res 4(1):32–38CrossRefGoogle Scholar
  2. 2.
    Zou M, Arentson EJ, Teegarden D, Koser SL, Onyskow L, Donkin SS (2012) Fructose consumption during pregnancy and lactation induces fatty liver and glucose intolerance in rats. Nutr Res 32(8):588–598CrossRefGoogle Scholar
  3. 3.
    Harreiter J, Dovjak G, Kautzky-Willer A (2014) Gestational diabetes mellitus and cardiovascular risk after pregnancy. Womens Health (Lond Engl) 10(1):91–108CrossRefGoogle Scholar
  4. 4.
    Duntas LH, Benvenga S (2015) Selenium: an element for life. Endocrine 48(3):756–775CrossRefGoogle Scholar
  5. 5.
    Seale LA, Hashimoto AC, Kurokawa S, Gilman CL, Seyedali A, Bellinger FP, Raman AV, Berry MJ (2012) Disruption of the selenocysteine lyase-mediated selenium recycling pathway leads to metabolic syndrome in mice. Mol Cell Biol 32(20):4141–4154CrossRefGoogle Scholar
  6. 6.
    Arnaud J, de Lorgeril M, Akbaraly T, Salen P, Arnout J, Cappuccio FP, van Dongen MC, Donati MB, Krogh V, Siani A, Iacoviello L (2012) European Collaborative Group of the IMMIDIET Project. “Gender differences in copper, zinc and selenium status in diabetic-free metabolic syndrome European population—the IMMIDIET study”. Nutr Metab Cardiovasc Dis 22(6):517–524CrossRefGoogle Scholar
  7. 7.
    Zhou J, Huang K, Lei XG (2013) Selenium and diabetes–evidence from animal studies. Free Radic Biol Med 65:1548–1556CrossRefGoogle Scholar
  8. 8.
    Rayman MP, Stranges S (2013) Epidemiology of selenium and type 2 diabetes: can we make sense of it? Free Radic Biol Med 65:1557–1564CrossRefGoogle Scholar
  9. 9.
    Brigelius-Flohé R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta 1830(5):3289–3303CrossRefGoogle Scholar
  10. 10.
    Pepper MP, Vatamaniuk MZ, Yan X, Roneker CA, Lei XG (2011) Impacts of dietary selenium deficiency on metabolic phenotypes of diet-restricted GPX1-overexpressing mice. Antioxid Redox Signal 14(3):383–390CrossRefGoogle Scholar
  11. 11.
    Mueller AS, Bosse AC, Most E, Klomann SD, Schneider S, Pallauf J (2009) Regulation of the insulin antagonistic protein tyrosinephosphatase1B by dietary Se studied in growing rats. J Nutr Biochem 20:235–247CrossRefGoogle Scholar
  12. 12.
    McClung JP, Roneker CA, Mu W, Lisk DJ, Langlais P, Liu F, Lei XG (2004) Development of insulin resistance and obesity in mice overexpressing cellular glutathione peroxidase. Proc Natl Acad Sci USA 101(24):8852–8857CrossRefGoogle Scholar
  13. 13.
    Steinbrenner H (2013) Interference of selenium and selenoproteins with the insulin-regulated carbohydrate and lipid metabolism. Free Radic Biol Med 65:1538–1547CrossRefGoogle Scholar
  14. 14.
    Stapleton SR (2000) Selenium: an insulin-mimetic. Cell Mol Life Sci 57(13–14):1874–1879CrossRefGoogle Scholar
  15. 15.
    Wang X, Zhang W, Chen H, Liao N, Wang Z, Zhang X, Hai C (2014) High selenium impairs hepatic insulin sensitivity through opposite regulation of ROS. Toxicol Lett 224(1):16–23CrossRefGoogle Scholar
  16. 16.
    Subramanian MG (1995) Effects of chronic alcohol administration on lactational performance in the rat. Alcohol 12:137–143CrossRefGoogle Scholar
  17. 17.
    Lawrence RA, Burk RF (1996) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952–958CrossRefGoogle Scholar
  18. 18.
    Worthington DJ, Rosemeyer MH (1974) Human glutathione reductase: purification of the crystalline enzyme from erythrocytes. Eur J Biochem 48:167–177CrossRefGoogle Scholar
  19. 19.
    Fridovich I (1985) Cytochrome C. In: Greenwald RA (ed) Handbook of methods for oxygen radical research. CRC Press, Boca Raton, FLorida, pp 213–215Google Scholar
  20. 20.
    Beers RF Jr, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140Google Scholar
  21. 21.
    Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431CrossRefGoogle Scholar
  22. 22.
    Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357–363CrossRefGoogle Scholar
  23. 23.
    Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with Folin phenol reagent. J Biol Chem 1:265–275Google Scholar
  24. 24.
    Gomez-Amores L, Mate A, Miguel-Carrasco JL, Jimenez L, Jos A, Camean A, Revilla E, Santa-María C, Vázquez CM (2007) L-carnitine attenuates oxidative stress in hypertensive rats. J Nutr Biochem 18:533–540CrossRefGoogle Scholar
  25. 25.
    Kotronen A, Westerbacka J, Bergholm R, Pietilainen KH, Yki-Jarvinen H (2007) Liver fat in the metabolic syndrome. J Clin Endocrinol Metab 92:3490–3497CrossRefGoogle Scholar
  26. 26.
    Sloboda DM, Li M, Patel R, Clayton ZE, Yap C, Vickers MH (2014) Early life exposure to fructose and offspring phenotype: implications for long term metabolic homeostasis. J Obes 2014:203474. doi: 10.1155/2014/203474 CrossRefGoogle Scholar
  27. 27.
    Vickers MH, Clayton ZE, Yap C, Sloboda DM (2011) Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology 152(4):1378–1387CrossRefGoogle Scholar
  28. 28.
    Li M, Reynolds CM, Sloboda DM, Gray C, Vickers MH (2015) Maternal taurine supplementation attenuates maternal fructose-induced metabolic and inflammatory dysregulation and partially reverses adverse metabolic programming in offspring. J Nutr Biochem 26(3):267–276CrossRefGoogle Scholar
  29. 29.
    Rawana S, Clark K, Zhong S, Buison A, Chackunkal S, Jen K-LC (1993) Low dose fructose ingestion during gestation and lactation affects carbohydrate metabolism in rat dams and their offspring. J Nutr 123(12):2158–2165Google Scholar
  30. 30.
    Abdulla MH, Sattar MA, Abdullah NA, Johns EJ (2013) The effect of high-fructose intake on the vasopressor response to angiotensin II and adrenergic agonists in Sprague-Dawley rats. Pak J Pharm Sci 26(4):727–732Google Scholar
  31. 31.
    Abdulla MH, Sattar MA, Abdullah NA, Johns EJ (2012) The effect of losartan and carvedilol on renal haemodynamics and altered metabolism in fructose-fed Sprague-Dawley rats. J Physiol Biochem 68(3):353–363CrossRefGoogle Scholar
  32. 32.
    Abdulla MH, Sattar MA, Johns EJ (2011) The relation between fructose-induced metabolic syndrome and altered renal haemodynamic and excretory function in the rat. Int J Nephrol 2011:934659. doi: 10.4061/2011/934659 CrossRefGoogle Scholar
  33. 33.
    Regnault TR, Gentili S, Sarr O, Toop CR, Sloboda DM (2013) Fructose, pregnancy and later life impacts. Clin Exp Pharmacol Physiol 40(11):824–837CrossRefGoogle Scholar
  34. 34.
    Cox NJ (1994) Maternal component in NIDDM transmission: how large an effect? Diabetes 43(1):166–168CrossRefGoogle Scholar
  35. 35.
    Seboussi R, Faye B, Askar M, Hassan K, Alhadrami G (2009) Effect of selenium supplementation on blood status and milk, urine, and fecal excretion in pregnant and lactating camel. Biol Trace Elem Res 128(1):45–61CrossRefGoogle Scholar
  36. 36.
    Sreeja S, Geetha R, Priyadarshini E, Bhavani K, Anuradha CV (2014) Substitution of soy protein for casein prevents oxidative modification and inflammatory response induced in rats fed high fructose diet. ISRN Inflamm 2014:641096. doi: 10.1155/2014/641096 CrossRefGoogle Scholar
  37. 37.
    Delbosc S, Paizanis E, Magous R, Araiz C, Dimo T, Cristol JP, Cros G, Azay J (2005) Involvement of oxidative stress and NADPH oxidase activation in the development of cardiovascular complications in a model of insulin resistance, the fructose-fed rat. Atherosclerosis 179(1):43–49CrossRefGoogle Scholar
  38. 38.
    Reddi AS, Bollineni JS (2001) Selenium-deficient diet induces renal oxidative stress and injury via TGF-beta1 in normal and diabetic rats. Kidney Int 59(4):1342–1353CrossRefGoogle Scholar
  39. 39.
    Jotty K, Ojeda ML, Nogales F, Murillo ML, Carreras O (2013) Selenium dietary supplementation as a mechanism to restore hepatic selenoprotein regulation in rat pups exposed to alcohol. Alcohol 47(7):545–552CrossRefGoogle Scholar
  40. 40.
    Cheng SM, Cheng YJ, Wu LY, Kuo CH, Lee YS, Wu MC, Huang CY, Ting H, Lee SD (2014) Activated apoptotic and anti-survival effects on rat hearts with fructose induced metabolic syndrome. Cell Biochem Funct 32(2):133–141CrossRefGoogle Scholar
  41. 41.
    Metes-Kosik N, Luptak I, Dibello PM, Handy DE, Tang SS, Zhi H, Qin F, Jacobsen DW, Loscalzo J, Joseph J (2012) Both selenium deficiency and modest selenium supplementation lead to myocardial fibrosis in mice via effects on redox-methylation balance. Mol Nutr Food Res 56(12):1812–1824CrossRefGoogle Scholar
  42. 42.
    Chen J (2012) An original discovery: selenium deficiency and Keshan disease (an endemic heart disease). Asia Pac J Clin Nutr 21(3):320–326Google Scholar
  43. 43.
    Xu TJ, Yuan BX, Zou YM (2011) Effect of combination of insulin and selenium on insulin signal transduction in cardiac muscle of STZ-induced diabetic rats. Yao Xue Xue Bao 46(3):274–279Google Scholar
  44. 44.
    Daniels LA (1996) Selenium metabolism and bioavailability. Biol Trace Elem Res 54(3):185–199CrossRefGoogle Scholar
  45. 45.
    Jotty K, Ojeda ML, Nogales F, Rubio JM, Murillo ML, Carreras O (2009) Selenium tissue distribution changes after ethanol exposure during gestation and lactation: selenite as a therapy. Food Chem Toxicol 47(10):2484–2489CrossRefGoogle Scholar
  46. 46.
    Stump CS, Henriksen EJ, Wei Y, Sowers JR (2006) The metabolic syndrome: role of skeletal muscle metabolism. Ann Med 38(6):389–402CrossRefGoogle Scholar
  47. 47.
    Akram M, Hamid A (2013) Mini review on fructose metabolism. Obes Res Clin Pract 7(2):e89–e94CrossRefGoogle Scholar
  48. 48.
    Fortuño A, San José G, Moreno MU, Beloqui O, Díez J, Zalba G (2006) Phagocytic NADPH oxidase overactivity underlies oxidative stress in metabolic syndrome. Diabetes 55(1):209–215CrossRefGoogle Scholar
  49. 49.
    Elnakish MT, Hassanain HH, Janssen PM, Angelos MG, Khan M (2013) Emerging role of oxidative stress in metabolic syndrome and cardiovascular diseases: important role of Rac/NADPH oxidase. J Pathol 231(3):290–300CrossRefGoogle Scholar
  50. 50.
    Feoli AM, Macagnan FE, Piovesan CH, Bodanese LC, Siqueira IR (2014) Xanthine oxidase activity is associated with risk factors for cardiovascular disease and inflammatory and oxidative status markers in metabolic syndrome: effects of a single exercise session. Oxid Med Cell Longev 2014:587083. doi: 10.1155/2014/587083 CrossRefGoogle Scholar
  51. 51.
    Armutcu F, Ataymen M, Atmaca H, Gurel A (2008) Oxidative stress markers, C-reactive protein and heat shock protein 70 levels in subjects with metabolic syndrome. Clin Chem Lab Med 46(6):785–790CrossRefGoogle Scholar
  52. 52.
    Yubero-Serrano EM, Delgado-Lista J, Peña-Orihuela P, Perez-Martinez P, Fuentes F, Marin C, Tunez I, Tinahones FJ, Perez-Jimenez F, Roche HM, Lopez-Miranda J (2013) Oxidative stress is associated with the number of components of metabolic syndrome: LIPGENE study. Exp Mol Med 45:e28. doi: 10.1038/emm.2013.53 CrossRefGoogle Scholar
  53. 53.
    Benstoem C, Goetzenich A, Kraemer S, Borosch S, Manzanares W, Hardy G, Stoppe C (2015) Selenium and its supplementation in cardiovascular disease—what do we know? Nutrients 7(5):3094–3118CrossRefGoogle Scholar
  54. 54.
    Yoshida T, Watanabe M, Engelman DT, Engelman RM, Schley JA, Maulik N, Ho YS, Oberley TD, Das DK (1996) Transgenic mice overexpressing glutathione peroxidase are resistant to myocardial ischemia reperfusion injury. J Mol Cell Cardiol 28:1759–1767CrossRefGoogle Scholar
  55. 55.
    Yoshida T, Maulik N, Engelman RM, Ho YS, Magnenat JL, Rousou JA, Flack JE, Deaton D, Das DK (1997) Glutathione peroxidase knockout mice are susceptible to myocardial ischemia reperfusion injury. Circulation 96:216–220Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Fátima Nogales
    • 1
  • M. Luisa Ojeda
    • 1
  • Paulina Muñoz del Valle
    • 1
  • Alejandra Serrano
    • 1
  • M. Luisa Murillo
    • 1
  • Olimpia Carreras Sánchez
    • 1
  1. 1.Department of Physiology, Faculty of PharmacySeville UniversitySevilleSpain

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