Reactive oxygen species and anti-oxidant defences in swine follicular fluids
Giuseppina Basini A B , Bussolati Simona A , Sujen Eleonora Santini A and Francesca Grasselli AA Dipartimento di Produzioni Animali, Biotecnologie Veterinarie, Qualità e Sicurezza degli Alimenti – Sezione di Fisiologia Veterinaria, Via del Taglio 8, Università degli Studi di Parma, 43100, Parma, Italy.
B Corresponding author. Email: basini@unipr.it
Reproduction, Fertility and Development 20(2) 269-274 https://doi.org/10.1071/RD07147
Submitted: 6 September 2007 Accepted: 19 November 2007 Published: 4 January 2008
Abstract
A growing body of evidence indicates that the pro-oxidant/anti-oxidant balance inside the ovarian follicle plays an important role in folliculogenesis. Therefore, the aim of the present study was to assess the redox status of follicular fluids collected from different-sized swine follicles. We quantified the most important reactive oxygen species (ROS), namely superoxide anion (O2–), hydrogen peroxide and hydroperoxides (ROOH); in addition, we examined the activity of the detoxifying enzymes superoxide dismutase, catalase (CAT) and glutathione peroxidase and the total non-enzymatic antioxidant capacity as determined by the ferric-reducing anti-oxidant power assay. Our data demonstrate that oxidative stress does not affect follicle growth because O2– levels do not change during follicle development, whereas concentrations of H2O2 and ROOH are reduced (P < 0.05). Surprisingly, all non-enzymatic and enzymatic scavengers examined in the present study, except for CAT, demonstrated reduced activity during follicle development (P < 0.05). Taken together, these results suggest that other factors could be involved in ROS detoxification during follicle development.
Acknowledgements
This work was supported by a FIL University of Parma grant and a ‘Programma di Ricerca di Rilevante Interesse Nazionale’ of the Ministero dell’Istruzione dell’Università e della Ricerca.
Agarwal, A. , Saleh, R. A. , and Badaiwy, M. A. (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 79, 829–843.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Angelucci, S. , Ciavardelli, D. , Di Giuseppe, F. , Eleuterio, E. , Sulpizio, M. , Tiboni, G. M. , Giampietro, F. , Palombo, P. , and Di Ilio, C. (2006). Protome analysis of human follicular fluid. Biochim. Biophys. Acta 1764, 1775–1785.
| PubMed |
Basini, G. , Bianco, F. , Grasselli, F. , Tirelli, M. , Bussolati, S. , and Tamanini, C. (2004a). The effects of reduced oxygen tension on swine granulosa cell. Regul. Pept. 120, 69–75.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Basini, G. , Grasselli, F. , Bianco, F. , Tirelli, M. , and Tamanini, C. (2004b). Effect of reduced oxygen tension on reactive oxygen species production and activity of antioxidant enzymes in swine granulosa cells. Biofactors 20, 61–69.
| PubMed |
Basini, G. , Bussolati, S. , Santini, S. E. , Bianchi, F. , Careri, M. , Mangia, A. , Musci, M. , and Grasselli, F. (2007). Antiangiogenesis in swine ovarian follicle: A potential role for 2-methoxyestradiol. Steroids 72, 660–665.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Benzie, I. F. , and Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal. Biochem. 239, 70–76.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Canbolat, O. , Fandrey, J. , and Jelkmann, W. (1998). Effects of modulators of the production and degradation of hydrogen peroxide on erythropoietin synthesis. Respir. Physiol. 114, 175–183.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Carbone, M. C. , Tatone, C. , Delle Monache, S. , Marci, R. , Caserta, D. , Colonna, R. , and Amicarelli, F. (2003). Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Mol. Hum. Reprod. 9, 639–643.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cassano, E. , Tosto, L. , Balestrieri, M. , Zicarelli, L. , and Abrescia, P. (1999). Antioxidant defense in the follicular fluid of water buffalo. Cell. Physiol. Biochem. 9, 106–116.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fallgren, A. B. , Mathisen, G. H. , Maehlen, J. , Blomhoff, R. , and Paulsen, R. E. (2007). Preconditioning with estradiol abolishes its neuroprotection in cerebellar neurons. Biochem. Biophys. Res. Commun. 352, 966–972.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grasselli, F. , Basini, G. , Bussolati, S. , and Tamanini, C. (2002). Effects of VEGF and bFGF on proliferation and production of steroids and nitric oxide in porcine granulosa cells. Reprod. Domest. Anim. 37, 362–368.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Grasselli, F. , Basini, G. , Tirelli, M. , Cavalli, V. , Bussolanti, S. , and Tamanini, C. (2003). Angiogenic activity of porcine granulosa cells co-cultured with endothelial cells in a microcarrier-based three-dimensional fibrin gel. J. Physiol. Pharmacol. 54, 361–370.
| PubMed |
Grasselli, F. , Basini, G. , Bussolati, S. , and Bianco, F. (2005). Cobalt chloride, a hypoxia-mimicking agent, modulates redox status and functional parameters of cultured swine granulosa cells. Reprod. Fertil. Dev. 17, 715–720.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Harsem, N. K. , Braekke, K. , and Staff, A. C. (2006). Augmented oxidative stress as well as antioxidant capacity in maternal circulation in preeclampsia. Eur. J. Obstet. Gynecol. Reprod. Biol. 128, 209–215.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jancar, N. , Kopitar, A. N. , Ihan, A. , Klun, I. V. , and Bokal, E. V. (2007). Effect of apoptosis and reactive oxygen species production in human granulosa cells on oocyte fertilization and blastocyst development. J. Assist. Reprod. Genet. 24, 91–97.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kroll, S. L. , and Czyzyk-Krzeska, M. F. (1998). Role of H2O2 and heme-containing O2 sensors in hypoxic regulation of tyrosine hydroxylase gene expression. Am. J. Physiol. Cell Physiol. 274, C167–C174.
Lenzi, A. , Gandini, L. , Lombardo, F. , Picardo, M. , Maresca, V. , Panfili, E. , Tramer, F. , Boitani, C. , and Dondero, F. (2002). Polyunsaturated fatty acids of germ cell membranes, glutathione and blutathione-dependent enzyme-PHGPx: from basic to clinic. Contraception 65, 301–304.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
MacLeod, J. (1943). The role of oxygen in the metabolism and mobility of human spermatozoa. Am. J. Physiol. 138, 512–518.
Menezo, Y. J. , Russo, G. , Tosti, E. , Mouatassim, S. E. , and Benkhalifa, M. (2007). Expression profile of genes coding for DNA repair in human oocytes using pangenomic microarrays, with a special focus on ROS linked decays. J. Assist. Reprod. Genet. ,, in press
| PubMed |
Pellegrini, N. , Serafini, M. , Colombi, B. , Del Rio, D. , Salvatore, S. , Bianchi, M. , and Brighenti, F. (2003). Total antioxidant capacity of plant foods, beverages and oils consumed in Italy assessed by three different in vitro assays. J. Nutr. 133, 2812–2819.
| PubMed |