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Antioxidant activities and lipid peroxidation status in human follicular fluid: age-dependent change

Published online by Cambridge University Press:  29 April 2021

H. Debbarh Open the ORCID record for H. Debbarh [Opens in a new window] ,
N. Louanjli ,
S. Aboulmaouahib ,
M. Jamil Open the ORCID record for M. Jamil [Opens in a new window] ,
L. Ahbbas ,
I. Kaarouch ,
O. Sefrioui  and
R. Cadi
H. Debbarh*
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology, Department of Biology Ain Chock Faculty of Sciences, Hassan II University, Casablanca, Morocco
N. Louanjli
Affiliation:
Anfa Fertility Center, Private Clinic of In Vitro Fertilization and Endoscopic Surgery, Casablanca, Morocco Labomac IVF Center and Clinical Laboratory Medicine, Casablanca, Morocco
S. Aboulmaouahib
Affiliation:
Anfa Fertility Center, Private Clinic of In Vitro Fertilization and Endoscopic Surgery, Casablanca, Morocco
M. Jamil
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology, Department of Biology Ain Chock Faculty of Sciences, Hassan II University, Casablanca, Morocco
L. Ahbbas
Affiliation:
Anfa Fertility Center, Private Clinic of In Vitro Fertilization and Endoscopic Surgery, Casablanca, Morocco
I. Kaarouch
Affiliation:
Anfa Fertility Center, Private Clinic of In Vitro Fertilization and Endoscopic Surgery, Casablanca, Morocco
O. Sefrioui
Affiliation:
Anfa Fertility Center, Private Clinic of In Vitro Fertilization and Endoscopic Surgery, Casablanca, Morocco
R. Cadi
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology, Department of Biology Ain Chock Faculty of Sciences, Hassan II University, Casablanca, Morocco
*
Author for correspondence: H. Debbarh. Laboratory of Molecular Genetic Physiopathology and Biotechnology, Department of Biology Ain Chock Faculty of Sciences, Hassan II University, Casablanca, Morocco. E-mail: debbarhhasnae2017@gmail.com
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Summary

Maternal age is a significant factor influencing in vitro fertilization (IVF) outcomes. Oxidative stress (OS) is one of the major causes of age-related cellular and molecular damage. The purpose of this work was to investigate the correlation between maternal age with intrafollicular antioxidants and OS markers in follicular fluid (FF), and also to determine the OS status in patients of advanced age. This study was a prospective study including 201 women undergoing IVF whose age was between 24 and 45 years old. FF samples were obtained from mature follicles at the time of oocyte retrieval. After treatment of FF, lipid peroxidation levels (MDA) and enzyme activities such as superoxide dismutase (SOD), catalase (CAT), glutathione reductase (GR) and glutathione (GSH) level were evaluated using spectrophotometry. The results indicated that the age cutoff point for increasing the MDA level was fixed at 37 years, allowing the study to be differentiated into two age groups. Group I included patients whose age was less than 37 years, and group II included patients whose age was greater than or equal 37 years. Statistical analysis revealed that MDA and GSH levels and GR activity were significantly higher in group II compared with group I. The SOD and CAT activities were significantly less in group II compared with group I. We concluded that from 37 years old a reproductive ageing was accompanied by a change in the antioxidant pattern in FF that impaired reactive oxygen species scavenging efficiency.

Keywords

Antioxidant enzymesMaternal ageLipid peroxidation
Type
Research Article
Information
Zygote , Volume 29 , Issue 6 , December 2021 , pp. 490 - 494
Copyright
© Ain Chock Faculty of Sciences, Hassan II University, Casablanca, Morocco., 2021. Published by Cambridge University Press

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References

Aebi, H (1984). [13] Catalase in vitro. Methods Enzymol 105, 121–6.CrossRefGoogle Scholar
Agarwal, A, Gupta, S and Sharma, R (2005). Oxidative stress and its implications in female infertility–a clinician’s perspective. Reprod Biomed Online 11, 641–50.CrossRefGoogle Scholar
Aitken, RJ and Clarkson, JS (1988). Significance of reactive oxygen species and antioxidants in defining the efficacy of sperm preparation techniques. J Androl 9, 367–76.CrossRefGoogle ScholarPubMed
Attaran, M, Pasqualotto, E, Falcone, T, Goldberg, JM, Miller, KF, Agarwal, A and Sharma, RK (2000). The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med 45, 314–20.Google ScholarPubMed
Borowiecka, M, Wojsiat, J, Polac, I, Radwan, M, Radwan, P and Zbikowska, HM (2012). Oxidative stress markers in follicular fluid of women undergoing in vitro fertilization and embryo transfer. Syst Biol Reprod Med 58, 301–5.CrossRefGoogle ScholarPubMed
Bradford, MM (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2), 248–54.CrossRefGoogle ScholarPubMed
Burton, GJ, Hempstock, J and Jauniaux, E (2003). Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed 6, 84–96.CrossRefGoogle ScholarPubMed
Carbone, MC, Tatone, C, Monache, SD, 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, 639–43.CrossRefGoogle ScholarPubMed
Di Ilio, C, Polidoro, G, Arduini, A, Muccini, A and Federici, G (1983). Glutathione peroxidase, glutathione reductase, glutathione S-transferase, and γ-glutamyl transpeptidase activities in the human early pregnancy placenta. Biochem Med 29, 143–8.CrossRefGoogle ScholarPubMed
Dröge, W (2002). Free radicals in the physiological control of cell function. Physiol Rev 82, 47–95.CrossRefGoogle ScholarPubMed
Elizur, SE, Lebovitz, O, Orvieto, R, Dor, J and Zan-Bar, T (2014). Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. Gynecol Endocrinol 30, 705–7.CrossRefGoogle ScholarPubMed
Ferrero, H, Delgado-Rosas, F, Garcia-Pascual, CM, Monterde, M, Zimmermann, RC, Simón, C and Gómez, R (2012). Efficiency and purity provided by the existing methods for the isolation of luteinized granulosa cells: a comparative study. Hum Reprod 27, 1781–9.CrossRefGoogle ScholarPubMed
Fridovich, I (1986). Biological effects of the superoxide radical. Arch Biochem Biophys 247, 1–11.CrossRefGoogle ScholarPubMed
Friedman, CI, Danforth, DR, Herbosa-Encarnacion, C, Arbogast, L, Alak, BM and Seifer, DB (1997). Follicular fluid vascular endothelial growth factor concentrations are elevated in women of advanced reproductive age undergoing ovulation induction. Fertil Steril 68, 607–12.CrossRefGoogle ScholarPubMed
Han, X, Song, X, Yu, F and Chen, L (2017). A ratiometric fluorescent probe for imaging and quantifying anti-apoptotic effects of GSH under temperature stress. Chem Sci 8, 6991–7002.CrossRefGoogle ScholarPubMed
Harman, D (1984). Free radical theory of aging: the ‘free radical’ diseases. AGE 7, 111–31.CrossRefGoogle Scholar
Hensley, K, Robinson, KA, Gabbita, SP, Salsman, S and Floyd, RA (2000). Reactive oxygen species, cell signaling, and cell injury. Free Radical Bio Med 28, 1456–62.CrossRefGoogle ScholarPubMed
Ighodaro, OM and Akinloye, OA (2018). First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54, 287–93.CrossRefGoogle Scholar
Lambrinoudaki, IV, Augoulea, A, Christodoulakos, GE, Economou, EV, Kaparos, G, Kontoravdis, A and Creatsas, G (2009). Measurable serum markers of oxidative stress response in women with endometriosis. Fertil Steril 91, 46–50.CrossRefGoogle ScholarPubMed
Lenzi, A, Gandini, L, Lombardo, F, Picardo, M, Maresca, V, Panfili, E and Dondero, F (2002). Polyunsaturated fatty acids of germ cell membranes, glutathione and glutathione-dependent enzyme-PHGPx: from basic to clinic. Contraception 65, 301–4.CrossRefGoogle Scholar
Liu, L, Trimarchi, JR and Keefe, DL (2000). Involvement of mitochondria in oxidative stress- induced cell death in mouse zygotes. Biol Reprod 62, 1745–53.CrossRefGoogle ScholarPubMed
Oktay, K, Turan, V, Bedoschi, G, Pacheco, FS and Moy, F (2015). Fertility preservation success subsequent to concurrent aromatase inhibitor treatment and ovarian stimulation in women with breast cancer. J Clin Oncol 33, 2424.CrossRefGoogle ScholarPubMed
Ottolenghi, C, Uda, M, Hamatani, T, Crisponi, L, Garcia, JE, Ko, M and Forabosco, A (2004). Aging of oocyte, ovary, and human reproduction. Annal NY Acad Sci 1034, 117–31.CrossRefGoogle ScholarPubMed
Oyawoye, O, Abdel Gadir, A, Garner, A, Constantinovici, N, Perrett, C and Hardiman, P (2003). Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: relationship to outcome. Hum Reprod 18, 2270–4.CrossRefGoogle Scholar
Pacella, L, Zander-Fox, DL, Armstrong, DT and Lane, M (2012). Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment. Fertil Steril 98, 4.CrossRefGoogle ScholarPubMed
Palhares, MB, Romão, GS, Da Broi, MG, Martins, WDP and Jordão, AA (2012). Serum and follicular oxidative stress biomarkers levels and response to controlled ovarian hyperstimulation (COH) in IVF cycles. Fertil Steril 98, S241.CrossRefGoogle Scholar
Paoletti, F, Aldinucci, D, Mocali, A and Caparrini, A (1986). A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Anal Biochem 154, 536–41.CrossRefGoogle ScholarPubMed
Pasqualotto, EB, Agarwal, A, Sharma, RK, Izzo, VM, Pinotti, JA, Joshi, NJ and Rose, BI (2004). Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril, 81, 973–6.CrossRefGoogle ScholarPubMed
Paszkowski, T, Traub, AI, Robinson, SY and McMaster, D (1995). Selenium dependent glutathione peroxidase activity in human follicular fluid. Clin Chim Acta 236, 173–80.CrossRefGoogle ScholarPubMed
Pella, R, Suárez-Cunza, S, Orihuela, P, Escudero, F, Pérez, Y, García, M and Romero, S (2020). Oxidative balance in follicular fluid of ART patients of advanced maternal age and blastocyst formation. JBRA Assist Reprod 24, 296.Google ScholarPubMed
Piette, C, De Mouzon, J, Bachelot, A and Spira, A (1990). In-vitro fertilization: influence of women’s age on pregnancy rates. Hum Reprod 5, 56–9.CrossRefGoogle ScholarPubMed
Sadraie, SH, Saito, H, Kaneko, T, Saito, T and Hiroi, M (2000). Effects of aging on ovarian fecundity in terms of the incidence of apoptotic granulosa cells. J Assist Reprod Genetic 17, 168–73.CrossRefGoogle ScholarPubMed
Saikat, KJ, Narendra, BK, Ratna, C, Baidyanath, C and Koel, C (2010) Upper control limit of reactive oxygen species in follicular fluid beyond which viable embryo formation is not favorable. Reprod Toxicol 29, 447–51Google Scholar
Samokyszyn, VM and Marnett, LJ (1990). Inhibition of microsomal lipid peroxidation by 13-cis-retinoic acid. Methods Enzymol 190(C), 281–8.CrossRefGoogle ScholarPubMed
Scandalios, JG (2005). Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38, 995–1014.CrossRefGoogle ScholarPubMed
Şimşek, M, Nazirolu, M, Şimşek, H, Cay, M, Aksakal, M and Kumru, S (1998). Blood plasma levels of lipoperoxides, glutathione peroxidase, beta carotene, vitamin A and E in women with habitual abortion. Cell Biochem Funct 16, 227–31.3.0.CO;2-M>CrossRefGoogle Scholar
Tatone, C, Carbone, MC, Falone, S, Aimola, P, Giardinelli, A, Caserta, D and Amicarelli, F (2006). Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod 12, 655–60.CrossRefGoogle ScholarPubMed
Van Blerkom, J, Antczak, M and Schrader, R (1997). The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels. Hum Reprod 12, 1047–55.CrossRefGoogle ScholarPubMed
Wdowiak, A (2015). Comparing antioxidant enzyme levels in follicular fluid in ICSI-treated patients. Gynecol Obstet Fertil 43(7–8), 515–21.CrossRefGoogle ScholarPubMed
Weckbecker, G and Cory, JG (1988). Ribonucleotide reductase activity and growth of glutathione-depleted mouse leukemia L1210 cells in vitro . Cancer Lett 40, 257–64.CrossRefGoogle ScholarPubMed
Wiener-Megnazi, Z, Vardi, L, Lissak, A, Shnizer, S, Reznick, AZ, Ishai, D and Dirnfeld, M (2004). Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization. Fertil Steril 82, 1171–6.CrossRefGoogle ScholarPubMed
Zelko, IN, Mariani, TJ and Folz, RJ (2002). Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radical Biol Med 33, 337–49.CrossRefGoogle Scholar
Zeron, Y, Ocheretny, A, Kedar, O, Borochov, A, Sklan, D and Arav, A (2001). Seasonal changes in bovine fertility: relation to developmental competence of oocytes, membrane properties and fatty acid composition of follicles. Reproduction 121, 447–54.CrossRefGoogle ScholarPubMed