Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 2352594, 9 pages
https://doi.org/10.1155/2017/2352594
Research Article

Reduction of the Oxidative Stress Status Using Steviol Glycosides in a Fish Model (Cyprinus carpio)

1Laboratorio de Toxicología Ambiental, Facultad de Química, Universidad Autónoma del Estado de México, Paseo Colón Intersección Paseo Tollocan s/n, Col. Residencial Colón, 50120 Toluca, MEX, Mexico
2Centro de Investigación en Alimentación y Desarrollo, A. C. Unidad Culiacán, Carretera El Dorado Km 5.5, Col. Campo El Diez, 80110 Culiacán, SIN, Mexico
3Laboratorio de Toxicología Acuática, Departamento de Farmacia, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Unidad Profesional Adolfo López Mateos, Av. Wilfrido Massieu Esq. Cda. Miguel Stampa s/n, Delegación Gustavo A. Madero, 07738 Ciudad de México, Mexico

Correspondence should be addressed to Leobardo Manuel Gómez-Oliván; xm.xemeau@ozemogml

Received 15 December 2016; Revised 17 March 2017; Accepted 3 April 2017; Published 12 June 2017

Academic Editor: Vickram Ramkumar

Copyright © 2017 Livier Mireya Sánchez-Aceves et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Suez, T. Korem, D. Zeevi et al., “Artificial sweeteners induce glucose intolerance by altering the gut microbiota,” Nature, vol. 514, no. 7521, pp. 181–186, 2014. View at Publisher · View at Google Scholar
  2. C. Gardner, J. Wylie-Rosett, S. S. Gidding et al., “Non nutritive sweeteners: current use and health perspectives a scientific statement from the American Heart Association and the American Diabetes Association,” Diabetes care, vol. 3, no. 8, pp. 1798–1808, 2012. View at Google Scholar
  3. F. T. Lange, M. Scheurer, and H. J. Brauch, “Artificial sweeteners—a recently recognized class of emerging environmental contaminants: a review,” Analytical and Bioanalytical Chemistry, vol. 403, no. 9, pp. 2503–2518, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. V. Chatsudthipong and C. Muanprasat, “Stevioside and related compounds: therapeutic benefits beyond sweetness,” Pharmacology and Therapeutics, vol. 121, no. 1, pp. 41–54, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. Q. Yang, “Gain weight by 'going diet?' artificial sweeteners and the neurobiology of sugar cravings,” Yale Journal of Biology and Medicine, vol. 83, no. 2, pp. 101–108, 2010. View at Google Scholar · View at Scopus
  6. J. J. James, P. Thomas, D. Cavan, and D. Kerr, “Preventing childhood obesity by reducing consumption of carbonated drinks: cluster randomised controlled trial,” British Medical Journal, vol. 328, no. 7450, p. 1237, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. FDA Food and Drugs Administration, “Cyclamate (Cyclamic Acid, Calcium Cyclamate and Sodium Cyclamate) Commissioner's Decision,” http://www.fda.gov/downloads/Food/IngredientsPackagingLabeling/FoodAdditivesIngredients/UCM404344.pdf.
  8. R. Dhingra, L. Sullivan, P. F. Jacques et al., “Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community,” Circulation, vol. 116, no. 5, pp. 480–488, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. P. L. Lutsey, L. M. Steffen, and J. Stevens, “Dietary intake and the development of the metabolic syndrome: the atherosclerosis risk in communities study,” Circulation, vol. 117, no. 6, pp. 754–761, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. W. C. Winkelmayer, M. J. Stampfer, W. C. Willett, and G. C. Curhan, “Habitual caffeine intake and the risk of hypertension in women,” Journal of the American Medical Association, vol. 294, no. 18, pp. 2330–2335, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. T. I. Halldorsson, M. Strøm, S. B. Petersen, and S. F. Olsen, “Intake of artificially sweetened soft drinks and risk of preterm delivery: a prospective cohort study in 59,334 Danish pregnant women,” American Journal of Clinical Nutrition, vol. 92, no. 3, pp. 626–633, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. N. Abo Elnaga, M. I. Massoud, M. Yousef, and H. H. Mohamed, “Effect of stevia sweetener consumption as non-caloric sweetening on body weight gain and biochemical’s parameters in overweight female rats,” Annals of Agricultural Sciences, vol. 61, no. 1, pp. 155–163, 2016. View at Publisher · View at Google Scholar
  13. N.-C. Kim and A. D. Kinghorn, “Highly sweet compounds of plant origin,” Archives of Pharmacal Research, vol. 25, no. 6, pp. 725–746, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Periche, M. L. Castelló, A. Heredia, and I. Escriche, “Influence of drying method on steviol glycosides and antioxidants in Stevia rebaudiana leaves,” Food Chemistry, vol. 172, pp. 1–6, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. G. J. Gerwig, E. M. te Poele, L. Dijkhuizen, and J. P. Kamerling, “Chapter one-stevia glycosides: chemical and enzymatic modifications of their carbohydrate moieties to improve the sweet-tasting quality,” in Advances in Carbohydrate Chemistry and Biochemistry, vol. 73, pp. 1–72, 2016. View at Google Scholar
  16. M. C. Carakostas, L. L. Curry, A. C. Boileau, and D. J. Brusick, “Overview: the history, technical function and safety of rebaudioside A, a naturally occurring steviol glycoside, for use in food and beverages,” Food and Chemical Toxicology, vol. 46, no. 7, pp. S1–S10, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. S. K. Goyal and R. K. Goyal, “Stevia (Stevia rebaudiana) a bio-sweetener: a review,” International Journal of Food Sciences and Nutrition, vol. 61, no. 1, pp. 1–11, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. “Stevia Market: Global Industry Analysis and Opportunity Assessment 2014–2020,” http://www.futuremarketinsights.com/reports/global-stevia-market.
  19. J. O. Atteh, O. M. Onagbesan, K. Tona, E. Decuypere, J. M. Geuns, and J. Buyse, “Evaluation of supplementary stevia (Stevia rebaudiana, bertoni) leaves and stevioside in broiler diets: effects on feed intake, nutrient metabolism, blood parameters and growth performance,” Journal of Animal Physiology and Animal Nutrition, vol. 92, no. 6, pp. 640–649, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Boonkaewwan, C. Toskulkao, and M. Vongsakul, “Anti-inflammatory and immunomodulatory activities of stevioside and its metabolite steviol on THP-1 cells,” Journal of Agricultural and Food Chemistry, vol. 54, no. 3, pp. 785–789, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Abudula, P. B. Jeppesen, S. E. D. Rolfsen, J. Xiao, and K. Hermansen, “Rebaudioside A potently stimulates insulin secretion from isolated mouse islets: studies on the dose-, glucose-, and calcium-dependency,” Metabolism, vol. 53, no. 10, pp. 1378–1381, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. P. B. Jeppesen, S. Gregersen, C. R. Poulsen, and K. Hermansen, “Stevioside acts directly on pancreatic β cells to secrete insulin: actions independent of cyclic adenosine monophosphate and adenosine triphosphate-sensitive K+-channel activity,” Metabolism, vol. 49, no. 2, pp. 208–214, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Chan, B. Tomlinson, Y.-J. Chen, J.-C. Liu, M.-H. Hsieh, and J.-T. Cheng, “A double-blind placebo-controlled study of the effectiveness and tolerability of oral stevioside in human hypertension,” British Journal of Clinical Pharmacology, vol. 50, no. 3, pp. 215–220, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Puri and D. Sharma, “Antibacterial activity of stevioside towards food-borne pathogenic bacteria,” Engineering in Life Sciences, vol. 11, no. 3, pp. 326–329, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. H. Sies, Ed., Elsevier, 2013.
  26. A. Valavanidis, T. Vlahogianni, M. Dassenakis, and M. Scoullos, “Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants,” Ecotoxicology and Environmental Safety, vol. 64, no. 2, pp. 178–189, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. F. F. Ahmad, D. L. Cowan, and A. Y. Sun, “Detection of free radical formation in various tissues after acute carbon tetrachloride administration in gerbil,” Life Sciences, vol. 41, no. 22, pp. 2469–2475, 1987. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Ohta, K. Nishida, E. Sasaki, M. Kongo, and I. Ishiguro, “Attenuation of disrupted hepatic active oxygen metabolism with the recovery of acute liver injury in rats intoxicated with carbon tetrachloride,” Research Communications in Molecular Pathology and Pharmacology, vol. 95, no. 2, pp. 191–207, 1997. View at Google Scholar · View at Scopus
  29. F. Ozturk, M. Ucar, I. C. Ozturk, N. Vardi, and K. Batcioglu, “Carbon tetrachloride-induced nephrotoxicity and protective effect of betaine in Sprague-Dawley rats,” Urology, vol. 62, no. 2, pp. 353–356, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. N. Tirkey, S. Pilkhwal, A. Kuhad, and K. Chopra, “Hasperidin, a citrus bioflavonoid, decreases the oxidative stress produced by carbon tetrachloride in rat liver and kidney,” BMC Pharmacology, vol. 5, no. 1, article 2, pp. 1–8, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Barata, I. Varo, J. C. Navarro, S. Arun, and C. Porte, “Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds,” Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology, vol. 140, no. 2, pp. 175–186, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Dröge, “Free radicals in the physiological control of cell function,” Physiological Reviews, vol. 82, no. 1, pp. 47–95, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. H. Malekinejad, A. Alizadeh, H. Cheraghi, S. Meshkin, and F. Dardmeh, “The protective effect of liquorice plant extract on CCl4-induced hepatotoxicity in common carp (Cyprinus carpio),” Veterinary Research Forum, vol. 1, no. 3, pp. 158–164, 2012. View at Google Scholar
  34. G. Yin, L. Cao, P. Xu, G. Jeney, M. Nakao, and C. Lu, “Hepatoprotective and antioxidant effects of Glycyrrhiza glabra extract against carbon tetrachloride (CCl4)-induced hepatocyte damage in common carp (Cyprinus carpio),” Fish Physiology and Biochemistry, vol. 37, no. 1, pp. 209–216, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. R. Jia, L. Cao, J. Du, P. Xu, G. Jeney, and G. Yin, “The protective effect of silymarin on the carbon tetrachloride (CCl4)-induced liver injury in common carp (Cyprinus carpio),” In Vitro Cellular and Developmental Biology—Animal, vol. 49, no. 3, pp. 155–161, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. Z. Y. Jiang, J. V. Hunt, and S. P. Wolff, “Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein,” Analytical Biochemistry, vol. 202, no. 2, pp. 384–389, 1992. View at Publisher · View at Google Scholar · View at Scopus
  37. J. A. Buege and S. D. Aust, “Microsomal lipid peroxidation,” Methods in Enzymology, vol. 52, pp. 302–310, 1978. View at Publisher · View at Google Scholar · View at Scopus
  38. R. L. Levine, J. A. Williams, E. R. Stadtman, and E. Shacter, “Carbonyl assays for determination of oxidatively modified proteins,” Methods in Enzymology, vol. 233, pp. 346–357, 1994. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Parvez and S. Raisuddin, “Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (bloch),” Environmental Toxicology and Pharmacology, vol. 20, no. 1, pp. 112–117, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. P. C. Burcham, “Modified protein carbonyl assay detects oxidised membrane proteins: a new tool for assessing drug- and chemically-induced oxidative cell injury,” Journal of Pharmacological and Toxicological Methods, vol. 56, no. 1, pp. 18–22, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. K. A. Novoa-Luna, R. Romero-Romero, R. Natividad-Rangel et al., “Oxidative stress induced in hyalella azteca by an effluent from a NSAID-manufacturing plant in Mexico,” Ecotoxicology, vol. 25, no. 7, pp. 1288–1304, 2016. View at Publisher · View at Google Scholar · View at Scopus
  42. H. P. Misra and I. Fridovich, “The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase,” The Journal of Biological Chemistry, vol. 247, no. 10, pp. 3170–3175, 1972. View at Google Scholar · View at Scopus
  43. R. Radi, J. F. Turrens, L. Y. Chang, K. M. Bush, J. D. Crapo, and B. A. Freeman, “Detection of catalase in rat heart mitochondria,” The Journal of Biological Chemistry, vol. 266, no. 32, pp. 22028–22034, 1991. View at Publisher · View at Google Scholar · View at Scopus
  44. M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Shukla, A. Mehta, P. Mehta, and V. K. Bajpai, “Antioxidant ability and total phenolic content of aqueous leaf extract of stevia rebaudiana bert,” Experimental and Toxicologic Pathology, vol. 64, pp. 807–811, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. A. F. Hernández, M. Lacasaña, F. Gil, M. Rodríguez-Barranco, A. Pla, and O. López-Guarnido, “Evaluation of pesticide-induced oxidative stress from a gene-environment interaction perspective,” Toxicology, vol. 307, pp. 95–102, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Sureda, S. Tejada, A. Boxsa, and S. Deudero, “Polycyclic aromatic hydrocarbon levels and measures of oxidative stress in the mediterranean endemic bivalve Pinna nobilis exposed to the Don Pedro oil spill,” Marine Pollution Bulletin, vol. 71, no. 1-2, pp. 69–73, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Espín, E. Martínez-López, M. León-Ortega, J. E. Martínez, and A. J. García-Fernández, “Oxidative stress biomarkers in eurasian eagle owls (Bubo bubo) in three different scenarios of heavy metal exposure,” Environmental Research, vol. 131, pp. 131–134, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. L. M. Gómez-Oliván, M. Galar-Martínez, H. Islas-Flores, S. García-Medina, and N. Sanjuan-Reyes, “DNA damage and oxidative stress induced by acetylsalicylic acid in Daphnia magna,” Comparative Biochemistry and Physiology Part—C: Toxicology and Pharmacology, vol. 164, pp. 21–26, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Galar-Martínez, L. M. Gómez-Oliván, A. Amaya-Chávez, C. Razo-Estrada, and S. García-Medina, “Oxidative stress induced on cyprinus carpio by contaminants present in the water and sediment of madín reservoir,” Journal of Environmental Science and Health—Part A Toxic/Hazardous Substances and Environmental Engineering, vol. 45, no. 2, pp. 155–160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Sanjuan-Reyes, L. M. Gómez-Oliván, M. Galar-Martínez et al., “Effluent from an NSAID-manufacturing plant in Mexico induces oxidative stress on Cyprinus carpio,” Water, Air, and Soil Pollution, vol. 224, no. 9, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Zhu, Z. Shen, J. Liu et al., “The ROS-mediated activation of STAT-3/VEGF signaling is involved in the 27-hydroxycholesterol-induced angiogenesis in human breast cancer cells,” Toxicology Letters, vol. 264, pp. 79–86, 2016. View at Publisher · View at Google Scholar
  53. R. V. Roy, P. Pratheeshkumar, Y.-O. Son et al., “Different roles of ROS and Nrf2 in Cr(VI)-induced inflammatory responses in normal and Cr(VI)-transformed cells,” Toxicology and Applied Pharmacology, vol. 307, pp. 81–90, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Belaidi, J. Morand, E. Gras, J. L. Pépin, and D. Godin-Ribuot, “Targeting the ROS-HIF-1-endothelin axis as a therapeutic approach for the treatment of obstructive sleep apnea-related cardiovascular complications,” Pharmacology Therapeutics, vol. 168, pp. 1–11, 2016. View at Google Scholar
  55. I. S. Kim, M. Yang, O. H. Lee, and S.-N. Kang, “The antioxidant activity and the bioactive compound content of Stevia rebaudiana water extracts,” LWT—Food Science and Technology, vol. 44, no. 5, pp. 1328–1332, 2011. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Morelli, S. Russo-Volpe, N. Bruno, and R. L. Scalzo, “Fenton-dependent damage to carbohydrates: free radical scavenging activity of some simple sugars,” Journal of Agricultural and Food Chemistry, vol. 51, no. 25, pp. 7418–7425, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Nishizawa, Y. Yabuta, and S. Shigeoka, “Galactinol and raffinose constitute a novel function to protect plants from oxidative damage,” Plant Physiology, vol. 147, no. 3, pp. 1251–1263, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Hajihashemi and J. M. C. Geuns, “Radical scavenging activity of steviol glycosides, steviol glucuronide, hydroxytyrosol, metformin, aspirin and leaf extract of Stevia rebaudiana,” Free Radicals and Antioxidants, vol. 3, pp. 34–41, 2013. View at Publisher · View at Google Scholar
  59. R. M. Martínez-Alvarez, A. E. Morales, and A. Sanz, “Antioxidant defenses in fish: biotic and abiotic factors,” Reviews in Fish Biology and Fisheries, vol. 15, no. 1-2, pp. 75–88, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. S. Ozden, B. Catalgol, S. Gezginci-Oktayoglu, P. Arda-Pirincci, S. Bolkent, and B. Alpertunga, “Methiocarb-induced oxidative damage following subacute exposure and the protective effects of vitamin E and taurine in rats,” Food and Chemical Toxicology, vol. 47, no. 7, pp. 1676–1684, 2009. View at Publisher · View at Google Scholar · View at Scopus
  61. H.-H. Wang, T.-M. Hung, J. Wei, and A.-N. Chiang, “Fish oil increases antioxidant enzyme activities in macrophages and reduces atherosclerotic lesions in apoE-knockout mice,” Cardiovascular Research, vol. 61, no. 1, pp. 169–176, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. S. A. Levine and J. H. Reinhardt, “Biochemical-pathology initiated by free radicals, oxidant chemicals, and therapeutic drugs in the etiology of chemical hypersensitivity disease,” Journal of Orthomolecular Psychiatry, vol. 12, no. 3, pp. 166–183, 1983. View at Google Scholar · View at Scopus
  63. T. Vlahogianni, M. Dassenakis, M. J. Scoullos, and A. Valavanidis, “Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals' pollution in coastal areas from the saronikos gulf of greece,” Marine Pollution Bulletin, vol. 54, no. 9, pp. 1361–1371, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. R. van der Oost, J. Beyer, and N. P. E. Vermeulen, “Fish bioaccumulation and biomarkers in environmental risk assessment: a review,” Environmental Toxicology and Pharmacology, vol. 13, no. 2, pp. 57–149, 2003. View at Publisher · View at Google Scholar
  65. T. V. Bagnyukova, O. I. Chahrak, and V. I. Lushchak, “Coordinated response of goldfish antioxidant defenses to environmental stress,” Aquatic Toxicology, vol. 78, no. 4, pp. 325–331, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Holvoet, A. Rull, A. García-Heredia et al., “Stevia-derived compounds attenuate the toxic effects of ectopic lipid accumulation in the liver of obese mice: a transcriptomic and metabolomic study,” Food and Chemical Toxicology, vol. 77, pp. 22–33, 2015. View at Publisher · View at Google Scholar · View at Scopus
  67. T. Fiaschi, F. Magherini, T. Gamberi, P. A. Modesti, and A. Modesti, “Adiponectin as a tissue regenerating hormone: more than a metabolic function,” Cellular and Molecular Life Sciences, vol. 71, no. 10, pp. 1917–1925, 2014. View at Publisher · View at Google Scholar
  68. J. M. C. Geuns and T. Struyf, “Radical scavenging activity of steviol glycosides and steviol glucuronide,” in Proceedings of the 4th EUSTAS Stevia Symposium, Stevia, Science no Fiction, J. M. C. Geuns, Ed., pp. 191–207, KU Leuven, Leuven, Belgium, 2010.
  69. B. Geeraert, F. Crombé, M. Hulsmans, N. Benhabilès, J. M. Geuns, and P. Holvoet, “Stevioside inhibits atherosclerosis by improving insulin signaling and antioxidant defense in obese insulin-resistant mice,” International Journal of Obesity, vol. 34, no. 3, pp. 569–577, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Stoyanova, J. Geuns, É. Hideg, and W. Van den Ende, “The food additives inulin and stevioside counteract oxidative stress,” International Journal of Food Sciences and Nutrition, vol. 62, no. 3, pp. 207–214, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. W. Jira, G. Spiteller, and A. Richter, “Increased levels of lipid oxidation products in low density lipoproteins of patients suffering from rheumatoid arthritis,” Chemistry and Physics of Lipids, vol. 87, no. 1, pp. 81–89, 1997. View at Publisher · View at Google Scholar · View at Scopus