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BioMed Research International
Volume 2014 (2014), Article ID 878062, 14 pages
Prooxidant Effects of Verbascoside, a Bioactive Compound from Olive Oil Mill Wastewater, on In Vitro Developmental Potential of Ovine Prepubertal Oocytes and Bioenergetic/Oxidative Stress Parameters of Fresh and Vitrified Oocytes
1Section of Veterinary Clinics and Animal Production, Department of Emergency and Organ Transplantation (DETO), University of Bari “Aldo Moro”, Strada Provincial Casamassima Km 3, Valenzano, 70010 Bari, Italy
2Obstetric and Gynecological Section, Department of Veterinary Medicine, Via Vienna 2, 07100 Sassari, Italy
3Department of Basic Medical Sciences, Neurosciences and Sense Organs, University of Bari “Aldo Moro”, Piazza Giulio Cesare, 70124 Bari, Italy
4Institute of Translational Pharmacology (IFT), National Research Council (CNR), Via Fosso del Cavaliere No. 100, 00133 Rome, Italy
5Institute of Sciences of Food Production (ISPA), National Research Council (CNR), Via G. Amendola 122/O, 70126 Bari, Italy
6Department of Food Science, 745 Agriculture Mall Drive, West Lafayette, IN 47907, USA
Received 10 June 2013; Revised 3 December 2013; Accepted 8 December 2013; Published 25 February 2014
Academic Editor: Maha Zaki Rizk
Copyright © 2014 M. E. Dell'Aquila 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.
- A. Cardinali, N. Cicco, V. Linsalata et al., “Biological activity of high molecular weight phenolics from olive mill wastewater,” Journal of Agricultural and Food Chemistry, vol. 58, no. 15, pp. 8585–8590, 2010.
- A. Cardinali, S. Pati, F. Minervini, I. D'Antuono, V. Linsalata, and V. Lattanzio, “Verbascoside, isoverbascoside, and their derivatives recovered from olive mill wastewater as possible food antioxidants,” Journal of Agricultural and Food Chemistry, vol. 60, no. 7, pp. 1822–1829, 2012.
- L. G. Korkina, E. V. Mikhal'chik, M. V. Suprun, S. Pastore, and R. Dal Toso, “Molecular mechanisms underlying wound healing and anti-inflammatory properties of naturally occurring biotechnologically produced phenylpropanoid glycosides,” Cellular and Molecular Biology, vol. 53, no. 5, pp. 84–91, 2007.
- E. Esposito, E. Mazzon, I. Paterniti et al., “PPAR-contributes to the anti-inflammatory activity of verbascoside in a model of inflammatory bowel disease in mice,” PPAR Research, vol. 2010, Article ID 917312, 10 pages, 2010.
- E. Esposito, R. Dal Toso, G. Pressi, P. Bramanti, R. Meli, and S. Cuzzocrea, “Protective effect of verbascoside in activated C6 glioma cells: possible molecular mechanisms,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 381, no. 1, pp. 93–105, 2010.
- L. Speranza, S. Franceschelli, M. Pesce et al., “Antiinflammatory effects in THP-1 cells treated with verbascoside,” Phytotherapy Research, vol. 24, no. 9, pp. 1398–1404, 2010.
- V. A. Kostyuk, A. I. Potapovich, T. O. Suhan, C. De Luca, and L. G. Korkina, “Antioxidant and signal modulation properties of plant polyphenols in controlling vascular inflammation,” European Journal of Pharmacology, vol. 658, no. 2-3, pp. 248–256, 2011.
- T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, no. 6809, pp. 239–247, 2000.
- P. S. Brookes, A.-L. Levonen, S. Shiva, P. Sarti, and V. M. Darley-Usmar, “Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species,” Free Radical Biology and Medicine, vol. 33, no. 6, pp. 755–764, 2002.
- A. Agarwal and S. S. R. Allamaneni, “Role of free radicals in female reproductive diseases and assisted reproduction,” Reproductive BioMedicine Online, vol. 9, no. 3, pp. 338–347, 2004.
- A. Agarwal, T. M. Said, M. A. Bedaiwy, J. Banerjee, and J. G. Alvarez, “Oxidative stress in an assisted reproductive techniques setting,” Fertility and Sterility, vol. 86, no. 3, pp. 503–512, 2006.
- E. Cadenas and K. J. A. Davies, “Mitochondrial free radical generation, oxidative stress, and aging,” Free Radical Biology and Medicine, vol. 29, no. 3-4, pp. 222–230, 2000.
- E. Cadenas, “Mitochondrial free radical production and cell signaling,” Molecular Aspects of Medicine, vol. 25, no. 1-2, pp. 17–26, 2004.
- P. G. Winyard, C. J. Moody, and C. Jacob, “Oxidative activation of antioxidant defence,” Trends in Biochemical Sciences, vol. 30, no. 8, pp. 453–461, 2005.
- P. S. Brookes, Y. Yoon, J. L. Robotham, M. W. Anders, and S.-S. Sheu, “Calcium, ATP, and ROS: a mitochondrial love-hate triangle,” American Journal of Physiology: Cell Physiology, vol. 287, no. 4, pp. C817–C833, 2004.
- R. Dumollard, J. Carroll, M. R. Duchen, K. Campbell, and K. Swann, “Mitochondrial function and redox state in mammalian embryos,” Seminars in Cell and Developmental Biology, vol. 20, no. 3, pp. 346–353, 2009.
- L.-Y. Wang, D.-H. Wang, X.-Y. Zou, and C.-M. Xu, “Mitochondrial functions on oocytes and preimplantation embryos,” Journal of Zhejiang University B, vol. 10, no. 7, pp. 483–492, 2009.
- U. Eichenlaub-Ritter, M. Wieczorek, S. Lüke, and T. Seidel, “Age related changes in mitochondrial function and new approaches to study redox regulation in mammalian oocytes in response to age or maturation conditions,” Mitochondrion, vol. 11, no. 5, pp. 783–796, 2011.
- J. Van Blerkom, “Mitochondrial function in the human oocyte and embryo and their role in developmental competence,” Mitochondrion, vol. 11, no. 5, pp. 797–813, 2011.
- B. Ambruosi, G. M. Lacalandra, A. I. Iorga et al., “Cytoplasmic lipid droplets and mitochondrial distribution in equine oocytes: implications on oocyte maturation, fertilization and developmental competence after ICSI,” Theriogenology, vol. 71, no. 7, pp. 1093–1104, 2009.
- F. W. Nicholas, “Genetic improvement through reproductive technology,” Animal Reproduction Science, vol. 42, no. 1–4, pp. 205–214, 1996.
- K. M. Morton, “Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes,” Reproduction in Domestic Animals, vol. 43, pp. 137–143, 2008.
- L. Ayensu-Coker, D. Bauman, S. R. Lindheim, and L. Breech, “Fertility preservation in pediatric, adolescent and young adult female cancer patients,” Pediatrics Endocrinology Review, vol. 10, no. 1, pp. 174–187, 2012.
- D. E. Reichman, O. K. Davis, N. Zaninovic, Z. Rosenwaks, and D. E. Goldschlag, “Fertility preservation using controlled ovarian hyperstimulation and oocyte cryopreservation in a premenarcheal female with myelodysplastic syndrome,” Fertility and Sterility, vol. 98, no. 5, pp. 1225–1228, 2012.
- K. E. Dillon and C. R. Gracia, “Pediatric and young adult patients and oncofertility,” Current Treatment Options in Oncology, vol. 13, no. 2, pp. 1–13, 2012.
- D. Dorji, Y. Ohkubo, K. Miyoshi, and M. Yoshida, “Gene expression profile differences in embryos derived from prepubertal and adult Japanese Black cattle during in vitro development,” Reproduction, Fertility and Development, vol. 24, no. 2, pp. 370–381, 2012.
- W. F. Rall and G. M. Fahy, “Ice-free cryopreservation of mouse embryos at −196°C by vitrification,” Nature, vol. 313, no. 6003, pp. 573–575, 1985.
- W. F. Rall, “Factors affecting the survival of mouse embryos cryopreserved by vitrification,” Cryobiology, vol. 24, no. 5, pp. 387–402, 1987.
- G. Vajta, “Vitrification of the oocytes and embryos of domestic animals,” Animal Reproduction Science, vol. 60-61, pp. 357–364, 2000.
- J. Liebermann, F. Nawroth, V. Isachenko, E. Isachenko, G. Rahimi, and M. J. Tucker, “Potential importance of vitrification in reproductive medicine,” Biology of Reproduction, vol. 67, no. 6, pp. 1671–1680, 2002.
- B. Fuller, S. Paynter, and P. Watson, “Cryopreservation of human gametes and embryos,” in Life in the Frozen State, B. Fuller, N. Lane, and E. Benson, Eds., pp. 505–541, CRC Press, Boca Raton, Fla, USA, 2004.
- J. L. Albarracín, R. Morató, C. Rojas, and T. Mogas, “Effects of vitrification in open pulled straws on the cytology of in vitro matured prepubertal and adult bovine oocytes,” Theriogenology, vol. 63, no. 3, pp. 890–901, 2005.
- F. Berlinguer, S. Succu, F. Mossa et al., “Effects of trehalose co-incubation on in vitro matured prepubertal ovine oocyte vitrification,” Cryobiology, vol. 55, no. 1, pp. 27–34, 2007.
- S. Succu, G. G. Leoni, F. Berlinguer et al., “Effect of vitrification solutions and cooling upon in vitro matured prepubertal ovine oocytes,” Theriogenology, vol. 68, no. 1, pp. 107–114, 2007.
- G. Fasano, F. Moffa, J. Dechène, Y. Englert, and I. Demeestere, “Vitrification of in vitro matured oocytes collected from antral follicles at the time of ovarian tissue cryopreservation,” Reproductive Biology and Endocrinology, vol. 9, article 150, 2011.
- M. G. Catalá, D. Izquierdo, S. Uzbekova et al., “Brilliant Cresyl Blue stain selects largest oocytes with highest mitochondrial activity, maturation-promoting factor activity and embryo developmental competence in prepubertal sheep,” Reproduction, vol. 142, no. 4, pp. 517–527, 2011.
- P. Pawlak, A. Cieslak, E. Warzych et al., “No single way to explain cytoplasmic maturation of oocytes from prepubertal and cyclic gilts,” Theriogenology, vol. 78, no. 9, pp. 2020–2030, 2012.
- S. Ledda, L. Bogliolo, G. Leoni, and S. Naitana, “Cell coupling and maturation-promoting factor activity in in vitro-matured prepubertal and adult sheep oocytes,” Biology of Reproduction, vol. 65, no. 1, pp. 247–252, 2001.
- L. Bogliolo, F. Ariu, G. Leoni, S. Uccheddu, and D. Bebbere, “High hydrostatic pressure treatment improves the quality of in vitro-produced ovine blastocysts,” Reproduction, Fertility and Development, vol. 23, no. 6, pp. 809–817, 2011.
- N. A. Martino, G. M. Lacalandra, M. Filioli Uranio et al., “Oocyte mitochondrial bioenergy potential and oxidative stress: within-/between-subject, in vivo versus in vitro maturation, and age-related variations in a sheep model,” Fertility and Sterility, vol. 97, no. 3, pp. 720–728, 2012.
- L. Bogliolo, F. Ariu, S. Fois et al., “Morphological and biochemical analysis of immature ovine oocytes vitrified with or without cumulus cells,” Theriogenology, vol. 68, no. 8, pp. 1138–1149, 2007.
- F. Berlinguer, G. G. Leoni, S. Succu et al., “Exogenous melatonin positively influences follicular dynamics, oocyte developmental competence and blastocyst output in a goat model,” Journal of Pineal Research, vol. 46, no. 4, pp. 383–391, 2009.
- H. R. Tervit, D. G. Whittingham, and L. E. Rowson, “Successful culture in vitro of sheep and cattle ova,” Journal of Reproduction and Fertility, vol. 30, no. 3, pp. 493–497, 1972.
- S. K. Walker, J. L. Hill, D. O. Kleemann, and C. D. Nancarrow, “Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations,” Biology of Reproduction, vol. 55, no. 3, pp. 703–708, 1996.
- S. Ledda, L. Bogliolo, P. Calvia, G. Leoni, and S. Naitana, “Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes,” Journal of Reproduction and Fertility, vol. 109, no. 1, pp. 73–78, 1997.
- J. Liu, S. Tang, W. Xu, Y. Wang, B. Yin, and Y. Zhang, “Detrimental effects of antibiotics on mouse embryos in chromatin integrity, apoptosis and expression of zygotically activated genes,” Zygote, vol. 19, no. 2, pp. 137–145, 2011.
- B. Ambruosi, M. Uranio, A. M. Sardanelli et al., “in vitro acute exposure to DEHP affects oocyte meiotic maturation, energy and oxidative stress parameters in a large animal model,” PLoS One, vol. 6, no. 11, Article ID e27452, 2011.
- M. Poot, Y.-Z. Zhang, J. A. Krämer et al., “Analysis of mitochondrial morphology and function with novel fixable fluorescent stains,” Journal of Histochemistry and Cytochemistry, vol. 44, no. 12, pp. 1363–1372, 1996.
- H. Torner, K.-P. Brüssow, H. Alm et al., “Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depends on the stage of pre-ovulatory maturation,” Theriogenology, vol. 61, no. 9, pp. 1675–1689, 2004.
- L. Valentini, A. I. Iorga, T. De Santis et al., “Mitochondrial distribution patterns in canine oocytes as related to the reproductive cycle stage,” Animal Reproduction Science, vol. 117, no. 1-2, pp. 166–177, 2010.
- H. W. Yang, K. J. Hwang, H. C. Kwon, H. S. Kim, K. W. Choi, and K. S. Oh, “Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos,” Human Reproduction, vol. 13, no. 4, pp. 998–1002, 1998.
- A. V. Kuznetsov, I. Kehrer, A. V. Kozlov et al., “Mitochondrial ROS production under cellular stress: comparison of different detection methods,” Analytical and Bioanalytical Chemistry, vol. 400, no. 8, pp. 2383–2390, 2011.
- H. Torner, H. Alm, W. Kanitz et al., “Effect of initial cumulus morphology on meiotic dynamic and status of mitochondria in horse oocytes during IVM,” Reproduction in Domestic Animals, vol. 42, no. 2, pp. 176–183, 2007.
- S. L. Wakefield, M. Lane, S. J. Schulz, M. L. Hebart, J. G. Thompson, and M. Mitchell, “Maternal supply of omega-3 polyunsaturated fatty acids alter mechanisms involved in oocyte and early embryo development in the mouse,” American Journal of Physiology: Endocrinology and Metabolism, vol. 294, no. 2, pp. E425–E434, 2008.
- M. E. Dell'Aquila, B. Ambruosi, T. De Santis, and Y. S. Cho, “Mitochondrial distribution and activity in human mature oocytes: gonadotropin-releasing hormone agonist versus antagonist for pituitary down-regulation,” Fertility and Sterility, vol. 91, no. 1, pp. 249–255, 2009.
- 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.
- R. F. Beers Jr. and I. W. Sizer, “A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase,” The Journal of biological chemistry, vol. 195, no. 1, pp. 133–140, 1952.
- H. Ukeda, D. Kawana, S. Maeda, and M. Sawamura, “Spectrophotometric assay for superoxide dismutase based on the reduction of highly water-soluble tetrazolium salts by xanthine-xanthine oxidase,” Bioscience, Biotechnology and Biochemistry, vol. 63, no. 3, pp. 485–488, 1999.
- J. M. McCord and I. Fridovich, “Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein),” Journal of Biological Chemistry, vol. 244, no. 22, pp. 6049–6055, 1969.
- J. Hong, H. Lu, X. Meng, J.-H. Ryu, Y. Hara, and C. S. Yang, “Stability, cellular uptake, biotransformation, and efflux of tea polyphenol (−)-epigallocatechin-3-gallate in HT-29 human colon adenocarcinoma cells,” Cancer Research, vol. 62, no. 24, pp. 7241–7246, 2002.
- P. Bellion, M. Olk, F. Will et al., “Formation of hydrogen peroxide in cell culture media by apple polyphenols and its effect on antioxidant biomarkers in the colon cell line HT-29,” Molecular Nutrition and Food Research, vol. 53, no. 10, pp. 1226–1236, 2009.
- L. H. Long, A. Hoi, and B. Halliwell, “Instability of, and generation of hydrogen peroxide by, phenolic compounds in cell culture media,” Archives of Biochemistry and Biophysics, vol. 501, no. 1, pp. 162–169, 2010.
- Z. Qiusheng, Z. Yuntao, Z. Rongliang, G. Dean, and L. Changling, “Effects of verbascoside and luteolin on oxidative damage in brain of heroin treated mice,” Pharmazie, vol. 60, no. 7, pp. 539–543, 2005.
- L. Lenoir, A. Rossary, J. Joubert-Zakeyh et al., “Lemon verbena infusion consumption attenuates oxidative stress in dextran sulfate sodium-induced colitis in the rat,” Digestive Diseases and Sciences, vol. 56, no. 12, pp. 3534–3545, 2011.
- A. Mestre-Alfaro, M. D. Ferrer, A. Sureda et al., “Phytoestrogens enhance antioxidant enzymes after swimming exercise and modulate sex hormone plasma levels in female swimmers,” European Journal of Applied Physiology, vol. 111, no. 9, pp. 2281–2294, 2011.
- M. B. Crosby, J. Svenson, G. S. Gilkeson, and T. K. Nowling, “A novel PPAR response element in the murine iNOS promoter,” Molecular Immunology, vol. 42, no. 11, pp. 1303–1310, 2005.
- G. D. Girnun, F. E. Domann, S. A. Moore, and M. E. C. Robbins, “Identification of a functional peroxisome proliferator-activated receptor response element in the rat catalase promoter,” Molecular Endocrinology, vol. 16, no. 12, pp. 2793–2801, 2002.
- E. Gray, M. Ginty, K. Kemp, N. Scolding, and A. Wilkins, “The PPAR-gamma agonist pioglitazone protects cortical neurons from inflammatory mediators via improvement in peroxisomal function,” Journal of Neuroinflammation, vol. 9, article 63, 2012.
- X.-M. Zhao, W.-H. Du, D. Wang et al., “Recovery of mitochondrial function and endogenous antioxidant systems in vitrified bovine oocytes during extended in vitro culture,” Molecular Reproduction and Development, vol. 78, no. 12, pp. 942–950, 2011.
- S. Vertuani, E. Beghelli, E. Scalambra et al., “Activity and stability studies of verbascoside, a novel antioxidant, in dermo-cosmetic and pharmaceutical topical formulations,” Molecules, vol. 16, no. 8, pp. 7068–7080, 2011.
- H. Bergmann, D. Rogoll, W. Scheppach, R. Melcher, and E. Richling, “The Ussing type chamber model to study the intestinal transport and modulation of specific tight-junction genes using a colonic cell line,” Molecular Nutrition and Food Research, vol. 53, no. 10, pp. 1211–1225, 2009.
- S. Sang, I. Yang, B. Buckley, C.-T. Ho, and C. S. Yang, “Autoxidative quinone formation in vitro and metabolite formation in vivo from tea polyphenol (−)-epigallocatechin-3-gallate: studied by real-time mass spectrometry combined with tandem mass ion mapping,” Free Radical Biology and Medicine, vol. 43, no. 3, pp. 362–371, 2007.
- A. P. Neilson, B. J. Song, T. N. Sapper, J. A. Bomser, and M. G. Ferruzzi, “Tea catechin auto-oxidation dimers are accumulated and retained by Caco-2 human intestinal cells,” Nutrition Research, vol. 30, no. 5, pp. 327–340, 2010.
- T. Kawada, R. Asano, K. Makino, and T. Sakuno, “Synthesis of isoacteoside, a dihydroxyphenylethyl glycoside,” Journal of Wood Science, vol. 48, no. 6, pp. 512–515, 2002.
- A. Cardinali, V. Linsalata, V. Lattanzio, and M. G. Ferruzzi, “Verbascosides from olive mill waste water: assessment of their bioaccessibility and Intestinal uptake using an in vitro digestion/Caco-2 model system,” Journal of Food Science, vol. 76, no. 2, pp. H48–H54, 2011.
- J. B. Vaidyanathan and T. Walle, “Cellular uptake and efflux of the tea favonoid (−)-epicatechin-3-gallate in the human intestinal cell Line caco-2,” Journal of Pharmacology and Experimental Therapeutics, vol. 307, no. 2, pp. 745–752, 2003.
- A. P. Neilson, J. C. George, E. M. Janle et al., “Influence of chocolate matrix composition on cocoa flavan-3-ol bioaccessibility in vitro and bioavailability in humans,” Journal of Agricultural and Food Chemistry, vol. 57, no. 20, pp. 9418–9426, 2009.
- C. M. Peters, R. J. Green, E. M. Janle, and M. G. Ferruzzi, “Formulation with ascorbic acid and sucrose modulates catechin bioavailability from green tea,” Food Research International, vol. 43, no. 1, pp. 95–102, 2010.
- L. Funes, S. Fernández-Arroyo, O. Laporta et al., “Correlation between plasma antioxidant capacity and verbascoside levels in rats after oral administration of lemon verbena extract,” Food Chemistry, vol. 117, no. 4, pp. 589–598, 2009.
- A. Cardinali, F. Rotondo, F. Minervini et al., “Assessment of verbascoside absorption in human colonic tissues using the Ussing chamber model,” Food Research International, vol. 54, pp. 132–138, 2013.
- E. M. Odiatou, A. L. Skaltsounis, and A. I. Constantinou, “Identification of the factors responsible for the in vitro pro-oxidant and cytotoxic activities of the olive polyphenols oleuropein and hydroxytyrosol,” Cancer Letters, vol. 330, no. 1, pp. 113–121, 2013.