Skip to main content
Top
Published in: Journal of Ovarian Research 1/2017

Open Access 01-12-2017 | Review

Follicular Fluid redox involvement for ovarian follicle growth

Authors: Cláudia Freitas, Ana Catarina Neto, Liliana Matos, Elisabete Silva, Ângela Ribeiro, João Luís Silva-Carvalho, Henrique Almeida

Published in: Journal of Ovarian Research | Issue 1/2017

Login to get access

Abstract

As the human ovarian follicle enlarges in the course of a regular cycle or following controlled ovarian stimulation, the changes in its structure reveal the oocyte environment composed of cumulus oophorus cells and the follicular fluid (FF).
In contrast to the dynamic nature of cells, the fluid compartment appears as a reservoir rich in biomolecules. In some aspects, it is similar to the plasma, but it also exhibits differences that likely relate to its specific localization around the oocyte. The chemical composition indicates that the follicular fluid is able to detect and buffer excessive amounts of reactive oxygen species, employing a variety of antioxidants, some of them components of the intracellular milieu.
An important part is played by albumin through specific cysteine residues. But the fluid contains other molecules whose cysteine residues may be involved in sensing and buffering the local oxidative conditions. How these molecules are recruited and regulated to intervene such process is unknown but it is a critical issue in reproduction.
In fact, important proteins in the FF, that regulate follicle growth and oocyte quality, exhibit cysteine residues at specific points, whose untoward oxidation would result in functional loss. Therefore, preservation of controlled oxidative conditions in the FF is a requirement for the fine-tuned oocyte maturation process. In contrast, its disturbance enhances the susceptibility to the establishment of reproductive disorders that would require the intervention of reproductive medicine technology.
Literature
1.
go back to reference Gougeon A. Dynamics of human follicular growth: morphologic, dynamic, and functional aspects. Ovary. 2004;2:25–43.CrossRef Gougeon A. Dynamics of human follicular growth: morphologic, dynamic, and functional aspects. Ovary. 2004;2:25–43.CrossRef
2.
go back to reference Eppig JJ, et al. In: Leung PCK, Adashi EY, editors. CHAPTER 7 - Regulation of Mammalian Oocyte Maturation A2, The Ovary. Second ed. San Diego: Academic Press; 2004. p. 113–29. Eppig JJ, et al. In: Leung PCK, Adashi EY, editors. CHAPTER 7 - Regulation of Mammalian Oocyte Maturation A2, The Ovary. Second ed. San Diego: Academic Press; 2004. p. 113–29.
3.
go back to reference Zeleznik AJ. CHAPTER 3 - Dynamics of Primate Follicular Growth: A Physiological Perspective A2. In: Adashi EY, Leung PCK, editors. The Ovary. Second ed. San Diego: Academic Press; 2004. p. 45–53.CrossRef Zeleznik AJ. CHAPTER 3 - Dynamics of Primate Follicular Growth: A Physiological Perspective A2. In: Adashi EY, Leung PCK, editors. The Ovary. Second ed. San Diego: Academic Press; 2004. p. 45–53.CrossRef
4.
go back to reference Albertini DF, Rider V. Patterns of intercellular connectivity in the mammalian cumulus-oocyte complex. Microsc Res Tech. 1994;27(2):125–33.PubMedCrossRef Albertini DF, Rider V. Patterns of intercellular connectivity in the mammalian cumulus-oocyte complex. Microsc Res Tech. 1994;27(2):125–33.PubMedCrossRef
5.
go back to reference Albertini DF, et al. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53.PubMedCrossRef Albertini DF, et al. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction. 2001;121(5):647–53.PubMedCrossRef
6.
go back to reference Li R, et al. Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod. 2000;63(3):839–45.PubMedCrossRef Li R, et al. Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod. 2000;63(3):839–45.PubMedCrossRef
7.
go back to reference Russell DL, et al. Bidirectional communication between cumulus cells and the oocyte: Old hands and new players? Theriogenology. 2016;86(1):62–8.PubMedCrossRef Russell DL, et al. Bidirectional communication between cumulus cells and the oocyte: Old hands and new players? Theriogenology. 2016;86(1):62–8.PubMedCrossRef
8.
go back to reference Ozawa M, et al. Cumulus cell-enclosed oocytes acquire a capacity to synthesize GSH by FSH stimulation during in vitro maturation in pigs. J Cell Physiol. 2010;222(2):294–301.PubMedCrossRef Ozawa M, et al. Cumulus cell-enclosed oocytes acquire a capacity to synthesize GSH by FSH stimulation during in vitro maturation in pigs. J Cell Physiol. 2010;222(2):294–301.PubMedCrossRef
9.
go back to reference Mori T, Amano T, Shimizu H. Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol Reprod. 2000;62(4):913–9.PubMedCrossRef Mori T, Amano T, Shimizu H. Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol Reprod. 2000;62(4):913–9.PubMedCrossRef
10.
go back to reference Tatemoto H, et al. Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol Reprod. 2004;71(4):1150–7.PubMedCrossRef Tatemoto H, et al. Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol Reprod. 2004;71(4):1150–7.PubMedCrossRef
11.
go back to reference Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during In vitro maturation: role of cumulus cells. Biol Reprod. 2000;63(3):805–10.PubMedCrossRef Tatemoto H, Sakurai N, Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during In vitro maturation: role of cumulus cells. Biol Reprod. 2000;63(3):805–10.PubMedCrossRef
12.
go back to reference Matos L, et al. Superoxide dismutase expression in human cumulus oophorus cells. Mol Hum Reprod. 2009;15(7):411–9.PubMedCrossRef Matos L, et al. Superoxide dismutase expression in human cumulus oophorus cells. Mol Hum Reprod. 2009;15(7):411–9.PubMedCrossRef
13.
go back to reference Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A. 2002;99(5):2890–4.PubMedPubMedCentralCrossRef Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A. 2002;99(5):2890–4.PubMedPubMedCentralCrossRef
14.
go back to reference Gilchrist RB, et al. Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation. J Cell Sci. 2006;119(Pt 18):3811–21.PubMedCrossRef Gilchrist RB, et al. Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation. J Cell Sci. 2006;119(Pt 18):3811–21.PubMedCrossRef
15.
go back to reference Juengel JL, McNatty KP. The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum Reprod Update. 2005;11(2):143–60.PubMed Juengel JL, McNatty KP. The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum Reprod Update. 2005;11(2):143–60.PubMed
16.
go back to reference Laitinen M, et al. A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev. 1998;78(1–2):135–40.PubMedCrossRef Laitinen M, et al. A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev. 1998;78(1–2):135–40.PubMedCrossRef
17.
go back to reference Peng J, et al. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci U S A. 2013;110(8):E776–85.PubMedPubMedCentralCrossRef Peng J, et al. Growth differentiation factor 9:bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc Natl Acad Sci U S A. 2013;110(8):E776–85.PubMedPubMedCentralCrossRef
18.
go back to reference Mottershead DG, et al. Cumulin, an Oocyte-secreted Heterodimer of the Transforming Growth Factor-beta Family, Is a Potent Activator of Granulosa Cells and Improves Oocyte Quality. J Biol Chem. 2015;290(39):24007–20.PubMedPubMedCentralCrossRef Mottershead DG, et al. Cumulin, an Oocyte-secreted Heterodimer of the Transforming Growth Factor-beta Family, Is a Potent Activator of Granulosa Cells and Improves Oocyte Quality. J Biol Chem. 2015;290(39):24007–20.PubMedPubMedCentralCrossRef
19.
go back to reference Dong J, et al. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383(6600):531–5.PubMedCrossRef Dong J, et al. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 1996;383(6600):531–5.PubMedCrossRef
20.
go back to reference Elvin JA, et al. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol. 1999;13(6):1035–48.PubMedCrossRef Elvin JA, et al. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol. 1999;13(6):1035–48.PubMedCrossRef
21.
go back to reference Yan C, et al. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001;15(6):854–66.PubMedCrossRef Yan C, et al. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol. 2001;15(6):854–66.PubMedCrossRef
22.
go back to reference Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14(2):159–77.PubMedCrossRef Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008;14(2):159–77.PubMedCrossRef
23.
go back to reference Sugiura K, et al. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development. 2007;134(14):2593–603.PubMedCrossRef Sugiura K, et al. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development. 2007;134(14):2593–603.PubMedCrossRef
24.
go back to reference Dragovic RA, et al. Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology. 2005;146(6):2798–806.PubMedCrossRef Dragovic RA, et al. Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology. 2005;146(6):2798–806.PubMedCrossRef
25.
go back to reference Su YQ, et al. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development. 2008;135(1):111–21.PubMedCrossRef Su YQ, et al. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development. 2008;135(1):111–21.PubMedCrossRef
26.
go back to reference Sutton-McDowall ML, et al. Redox and anti-oxidant state within cattle oocytes following in vitro maturation with bone morphogenetic protein 15 and follicle stimulating hormone. Mol Reprod Dev. 2015;82(4):281–94.PubMedCrossRef Sutton-McDowall ML, et al. Redox and anti-oxidant state within cattle oocytes following in vitro maturation with bone morphogenetic protein 15 and follicle stimulating hormone. Mol Reprod Dev. 2015;82(4):281–94.PubMedCrossRef
27.
go back to reference Diaz FJ, Wigglesworth K, Eppig JJ. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci. 2007;120(Pt 8):1330–40.PubMedCrossRef Diaz FJ, Wigglesworth K, Eppig JJ. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci. 2007;120(Pt 8):1330–40.PubMedCrossRef
28.
go back to reference Wigglesworth K, et al. Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod. 2015;92(1):23.PubMedCrossRef Wigglesworth K, et al. Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod. 2015;92(1):23.PubMedCrossRef
29.
30.
31.
go back to reference Balaban B, Urman B. Effect of oocyte morphology on embryo development and implantation. Reprod BioMed Online. 2006;12(5):608–15.PubMedCrossRef Balaban B, Urman B. Effect of oocyte morphology on embryo development and implantation. Reprod BioMed Online. 2006;12(5):608–15.PubMedCrossRef
32.
go back to reference Ambekar AS, et al. Proteomic analysis of human follicular fluid: a new perspective towards understanding folliculogenesis. J Proteome. 2013;87:68–77.CrossRef Ambekar AS, et al. Proteomic analysis of human follicular fluid: a new perspective towards understanding folliculogenesis. J Proteome. 2013;87:68–77.CrossRef
33.
go back to reference Kushnir MM, et al. Exploratory study of the association of steroid profiles in stimulated ovarian follicular fluid with outcomes of IVF treatment. J Steroid Biochem Mol Biol. 2016;162:126–33.PubMedCrossRef Kushnir MM, et al. Exploratory study of the association of steroid profiles in stimulated ovarian follicular fluid with outcomes of IVF treatment. J Steroid Biochem Mol Biol. 2016;162:126–33.PubMedCrossRef
34.
go back to reference Angelucci S, et al. Proteome analysis of human follicular fluid. Biochim Biophys Acta. 2006;1764(11):1775–85.PubMedCrossRef Angelucci S, et al. Proteome analysis of human follicular fluid. Biochim Biophys Acta. 2006;1764(11):1775–85.PubMedCrossRef
35.
go back to reference Twigt J, et al. Proteomic analysis of the microenvironment of developing oocytes. Proteomics. 2012;12(9):1463–71.PubMedCrossRef Twigt J, et al. Proteomic analysis of the microenvironment of developing oocytes. Proteomics. 2012;12(9):1463–71.PubMedCrossRef
36.
go back to reference Hanrieder J, et al. Proteomic analysis of human follicular fluid using an alternative bottom-up approach. J Proteome Res. 2008;7(1):443–9.PubMedCrossRef Hanrieder J, et al. Proteomic analysis of human follicular fluid using an alternative bottom-up approach. J Proteome Res. 2008;7(1):443–9.PubMedCrossRef
37.
go back to reference Jiang JY, et al. Follicular microvasculature in the porcine ovary. Cell Tissue Res. 2002;310(1):93–101.PubMedCrossRef Jiang JY, et al. Follicular microvasculature in the porcine ovary. Cell Tissue Res. 2002;310(1):93–101.PubMedCrossRef
38.
go back to reference Schweigert FJ, et al. Peptide and protein profiles in serum and follicular fluid of women undergoing IVF. Hum Reprod. 2006;21(11):2960–8.PubMedCrossRef Schweigert FJ, et al. Peptide and protein profiles in serum and follicular fluid of women undergoing IVF. Hum Reprod. 2006;21(11):2960–8.PubMedCrossRef
39.
go back to reference Bianchi L, et al. A methodological and functional proteomic approach of human follicular fluid en route for oocyte quality evaluation. J Proteome. 2013;90:61–76.CrossRef Bianchi L, et al. A methodological and functional proteomic approach of human follicular fluid en route for oocyte quality evaluation. J Proteome. 2013;90:61–76.CrossRef
40.
go back to reference Espey LL. Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol Reprod. 1994;50(2):233–8.PubMedCrossRef Espey LL. Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction. Biol Reprod. 1994;50(2):233–8.PubMedCrossRef
42.
go back to reference Duan J, Kasper DL. Oxidative depolymerization of polysaccharides by reactive oxygen/nitrogen species. Glycobiology. 2011;21(4):401–9.PubMedCrossRef Duan J, Kasper DL. Oxidative depolymerization of polysaccharides by reactive oxygen/nitrogen species. Glycobiology. 2011;21(4):401–9.PubMedCrossRef
43.
go back to reference Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. 4th Ed., New York: Oxford University Press Inc; 2007. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine. 4th Ed., New York: Oxford University Press Inc; 2007.
44.
go back to reference Naskalski JW, Bartosz G. Oxidative modifications of protein structures. Adv Clin Chem. 2000;35:161–253.PubMedCrossRef Naskalski JW, Bartosz G. Oxidative modifications of protein structures. Adv Clin Chem. 2000;35:161–253.PubMedCrossRef
45.
go back to reference Mary J, et al. Enzymatic reactions involved in the repair of oxidized proteins. Exp Gerontol. 2004;39(8):1117–23.PubMedCrossRef Mary J, et al. Enzymatic reactions involved in the repair of oxidized proteins. Exp Gerontol. 2004;39(8):1117–23.PubMedCrossRef
46.
47.
go back to reference Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem. 2001;276(42):38388–93.PubMedCrossRef Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu, Zn-SOD in mitochondria. J Biol Chem. 2001;276(42):38388–93.PubMedCrossRef
48.
go back to reference Weisiger RA, Fridovich I. Mitochondrial superoxide dismutase. Site of synthesis and intramitochondrial localization. J Biol Chem. 1973;248(13):4793–6.PubMed Weisiger RA, Fridovich I. Mitochondrial superoxide dismutase. Site of synthesis and intramitochondrial localization. J Biol Chem. 1973;248(13):4793–6.PubMed
51.
go back to reference Mates JM, Perez-Gomez C, Nunez de Castro I. Antioxidant enzymes and human diseases. Clin Biochem. 1999;32(8):595–603.PubMedCrossRef Mates JM, Perez-Gomez C, Nunez de Castro I. Antioxidant enzymes and human diseases. Clin Biochem. 1999;32(8):595–603.PubMedCrossRef
52.
go back to reference Arthur JR. The glutathione peroxidases. Cell Mol Life Sci. 2000;57(13–14):1825–35.PubMed Arthur JR. The glutathione peroxidases. Cell Mol Life Sci. 2000;57(13–14):1825–35.PubMed
53.
go back to reference Chaudiere J, Ferrari-Iliou R. Intracellular antioxidants: from chemical to biochemical mechanisms. Food Chem Toxicol. 1999;37(9–10):949–62.PubMedCrossRef Chaudiere J, Ferrari-Iliou R. Intracellular antioxidants: from chemical to biochemical mechanisms. Food Chem Toxicol. 1999;37(9–10):949–62.PubMedCrossRef
54.
go back to reference Turunen M, Olsson J, Dallner G. Metabolism and function of coenzyme Q. Biochim Biophys Acta. 2004;1660(1–2):171–99.PubMedCrossRef Turunen M, Olsson J, Dallner G. Metabolism and function of coenzyme Q. Biochim Biophys Acta. 2004;1660(1–2):171–99.PubMedCrossRef
55.
go back to reference Kand’ar R, Zakova P, Muzakova V. Monitoring of antioxidant properties of uric acid in humans for a consideration measuring of levels of allantoin in plasma by liquid chromatography. Clin Chim Acta. 2006;365(1–2):249–56.PubMedCrossRef Kand’ar R, Zakova P, Muzakova V. Monitoring of antioxidant properties of uric acid in humans for a consideration measuring of levels of allantoin in plasma by liquid chromatography. Clin Chim Acta. 2006;365(1–2):249–56.PubMedCrossRef
56.
go back to reference Wu G, et al. Glutathione metabolism and its implications for health. J Nutr. 2004;134(3):489–92.PubMed Wu G, et al. Glutathione metabolism and its implications for health. J Nutr. 2004;134(3):489–92.PubMed
57.
go back to reference Levine M. New concepts in the biology and biochemistry of ascorbic acid. N Engl J Med. 1986;314(14):892–902.PubMedCrossRef Levine M. New concepts in the biology and biochemistry of ascorbic acid. N Engl J Med. 1986;314(14):892–902.PubMedCrossRef
58.
go back to reference Rumsey SC, Levine M. Absorption, transport, and disposition of ascorbic acid in humans. J Nutr Biochem. 1998;9(3):116–30.CrossRef Rumsey SC, Levine M. Absorption, transport, and disposition of ascorbic acid in humans. J Nutr Biochem. 1998;9(3):116–30.CrossRef
59.
go back to reference Alej, et al. The Exogenous Antioxidants, in Oxidative Stress and Chronic Degenerative Diseases - A Role for Antioxidants. Rijeka: InTech; 2013. Ch. 0. Alej, et al. The Exogenous Antioxidants, in Oxidative Stress and Chronic Degenerative Diseases - A Role for Antioxidants. Rijeka: InTech; 2013. Ch. 0.
60.
go back to reference Joshi R, et al. Free radical scavenging behavior of folic acid: evidence for possible antioxidant activity. Free Radic Biol Med. 2001;30(12):1390–9.PubMedCrossRef Joshi R, et al. Free radical scavenging behavior of folic acid: evidence for possible antioxidant activity. Free Radic Biol Med. 2001;30(12):1390–9.PubMedCrossRef
61.
go back to reference Sies H. Total antioxidant capacity: appraisal of a concept. J Nutr. 2007;137(6):1493–5.PubMed Sies H. Total antioxidant capacity: appraisal of a concept. J Nutr. 2007;137(6):1493–5.PubMed
62.
go back to reference Sundaresan M, et al. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 1995;270(5234):296–9.PubMedCrossRef Sundaresan M, et al. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 1995;270(5234):296–9.PubMedCrossRef
65.
go back to reference Biswas S, Chida AS, Rahman I. Redox modifications of protein-thiols: emerging roles in cell signaling. Biochem Pharmacol. 2006;71(5):551–64.PubMedCrossRef Biswas S, Chida AS, Rahman I. Redox modifications of protein-thiols: emerging roles in cell signaling. Biochem Pharmacol. 2006;71(5):551–64.PubMedCrossRef
66.
go back to reference Ghezzi P, Chan P. Redox Proteomics Applied to the Thiol Secretome. Antioxid Redox Signal. 2017;26(7):299–312.PubMedCrossRef Ghezzi P, Chan P. Redox Proteomics Applied to the Thiol Secretome. Antioxid Redox Signal. 2017;26(7):299–312.PubMedCrossRef
67.
go back to reference Janssen-Heininger YM, et al. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med. 2008;45(1):1–17.PubMedPubMedCentralCrossRef Janssen-Heininger YM, et al. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med. 2008;45(1):1–17.PubMedPubMedCentralCrossRef
68.
go back to reference Boronat S, Domenech A, Hidalgo E. Proteomic Characterization of Reversible Thiol Oxidations in Proteomes and Proteins. Antioxid Redox Signal. 2017;26(7):329–44.PubMedCrossRef Boronat S, Domenech A, Hidalgo E. Proteomic Characterization of Reversible Thiol Oxidations in Proteomes and Proteins. Antioxid Redox Signal. 2017;26(7):329–44.PubMedCrossRef
70.
go back to reference Choi YS, et al. Alteration in the intrafollicular thiol-redox system in infertile women with endometriosis. Reproduction. 2015;149(2):155–62.PubMedCrossRef Choi YS, et al. Alteration in the intrafollicular thiol-redox system in infertile women with endometriosis. Reproduction. 2015;149(2):155–62.PubMedCrossRef
71.
go back to reference Sabatini L, et al. Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization. Fertil Steril. 1999;72(6):1027–34.PubMedCrossRef Sabatini L, et al. Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization. Fertil Steril. 1999;72(6):1027–34.PubMedCrossRef
72.
go back to reference Carbone MC, et al. Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Mol Hum Reprod. 2003;9(11):639–43.PubMedCrossRef Carbone MC, et al. Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes. Mol Hum Reprod. 2003;9(11):639–43.PubMedCrossRef
73.
go back to reference Kishi I, et al. Thioredoxin, an antioxidant redox protein, in ovarian follicles of women undergoing in vitro fertilization. Endocr J. 2016;63(1):9–20.PubMedCrossRef Kishi I, et al. Thioredoxin, an antioxidant redox protein, in ovarian follicles of women undergoing in vitro fertilization. Endocr J. 2016;63(1):9–20.PubMedCrossRef
74.
go back to reference Da Broi MG, et al. Increased concentration of 8-hydroxy-2′-deoxyguanosine in follicular fluid of infertile women with endometriosis. Cell Tissue Res. 2016;366(1):231–42. Da Broi MG, et al. Increased concentration of 8-hydroxy-2′-deoxyguanosine in follicular fluid of infertile women with endometriosis. Cell Tissue Res. 2016;366(1):231–42.
75.
go back to reference Otsuki J, et al. The influence of the redox state of follicular fluid albumin on the viability of aspirated human oocytes. Syst Biol Reprod Med. 2012;58(3):149–53.PubMedCrossRef Otsuki J, et al. The influence of the redox state of follicular fluid albumin on the viability of aspirated human oocytes. Syst Biol Reprod Med. 2012;58(3):149–53.PubMedCrossRef
76.
go back to reference Elizur SE, et al. Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. Gynecol Endocrinol. 2014;30(10):705–7.PubMedCrossRef Elizur SE, et al. Reactive oxygen species in follicular fluid may serve as biochemical markers to determine ovarian aging and follicular metabolic age. Gynecol Endocrinol. 2014;30(10):705–7.PubMedCrossRef
77.
go back to reference Kushnir MM, et al. Protein and steroid profiles in follicular fluid after ovarian hyperstimulation as potential biomarkers of IVF outcome. J Proteome Res. 2012;11(10):5090–100.PubMedCrossRef Kushnir MM, et al. Protein and steroid profiles in follicular fluid after ovarian hyperstimulation as potential biomarkers of IVF outcome. J Proteome Res. 2012;11(10):5090–100.PubMedCrossRef
79.
go back to reference Bedaiwy MA, et al. Effect of follicular fluid oxidative stress parameters on intracytoplasmic sperm injection outcome. Gynecol Endocrinol. 2012;28(1):51–5.PubMedCrossRef Bedaiwy MA, et al. Effect of follicular fluid oxidative stress parameters on intracytoplasmic sperm injection outcome. Gynecol Endocrinol. 2012;28(1):51–5.PubMedCrossRef
80.
go back to reference Pasqualotto EB, et al. Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril. 2004;81(4):973–6.PubMedCrossRef Pasqualotto EB, et al. Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril. 2004;81(4):973–6.PubMedCrossRef
81.
go back to reference Das S, et al. Reactive oxygen species level in follicular fluid--embryo quality marker in IVF? Hum Reprod. 2006;21(9):2403–7.PubMedCrossRef Das S, et al. Reactive oxygen species level in follicular fluid--embryo quality marker in IVF? Hum Reprod. 2006;21(9):2403–7.PubMedCrossRef
82.
go back to reference Palini S, et al. Influence of ovarian stimulation for IVF/ICSI on the antioxidant defence system and relationship to outcome. Reprod BioMed Online. 2014;29(1):65–71.PubMedCrossRef Palini S, et al. Influence of ovarian stimulation for IVF/ICSI on the antioxidant defence system and relationship to outcome. Reprod BioMed Online. 2014;29(1):65–71.PubMedCrossRef
83.
go back to reference Hashemitabar M, et al. A proteomic analysis of human follicular fluid: comparison between younger and older women with normal FSH levels. Int J Mol Sci. 2014;15(10):17518–40.PubMedPubMedCentralCrossRef Hashemitabar M, et al. A proteomic analysis of human follicular fluid: comparison between younger and older women with normal FSH levels. Int J Mol Sci. 2014;15(10):17518–40.PubMedPubMedCentralCrossRef
84.
go back to reference Watson WH, et al. Differential Regulation of the Extracellular Cysteine/Cystine Redox State (EhCySS) by Lung Fibroblasts from Young and Old Mice. Oxidative Med Cell Longev. 2016;2016:1561305.CrossRef Watson WH, et al. Differential Regulation of the Extracellular Cysteine/Cystine Redox State (EhCySS) by Lung Fibroblasts from Young and Old Mice. Oxidative Med Cell Longev. 2016;2016:1561305.CrossRef
85.
go back to reference Takeo S, et al. Age-associated deterioration in follicular fluid induces a decline in bovine oocyte quality. Reprod Fertil Dev. 2016. doi:10.1071/RD15228. Takeo S, et al. Age-associated deterioration in follicular fluid induces a decline in bovine oocyte quality. Reprod Fertil Dev. 2016. doi:10.​1071/​RD15228.
86.
go back to reference Jozwik M, et al. Oxidative stress markers in preovulatory follicular fluid in humans. Mol Hum Reprod. 1999;5(5):409–13.PubMedCrossRef Jozwik M, et al. Oxidative stress markers in preovulatory follicular fluid in humans. Mol Hum Reprod. 1999;5(5):409–13.PubMedCrossRef
87.
go back to reference Attaran M, et al. The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med. 2000;45(5):314–20.PubMed Attaran M, et al. The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med. 2000;45(5):314–20.PubMed
89.
go back to reference Bjelakovic G, Nikolova D, Gluud C. Meta-regression analyses, meta-analyses, and trial sequential analyses of the effects of supplementation with beta-carotene, vitamin A, and vitamin E singly or in different combinations on all-cause mortality: do we have evidence for lack of harm? PLoS One. 2013;8(9):e74558.PubMedPubMedCentralCrossRef Bjelakovic G, Nikolova D, Gluud C. Meta-regression analyses, meta-analyses, and trial sequential analyses of the effects of supplementation with beta-carotene, vitamin A, and vitamin E singly or in different combinations on all-cause mortality: do we have evidence for lack of harm? PLoS One. 2013;8(9):e74558.PubMedPubMedCentralCrossRef
90.
go back to reference Lin J, et al. Vitamins C and E and beta carotene supplementation and cancer risk: a randomized controlled trial. J Natl Cancer Inst. 2009;101(1):14–23.PubMedPubMedCentralCrossRef Lin J, et al. Vitamins C and E and beta carotene supplementation and cancer risk: a randomized controlled trial. J Natl Cancer Inst. 2009;101(1):14–23.PubMedPubMedCentralCrossRef
92.
go back to reference Zhao H, et al. Metabolism alteration in follicular niche: The nexus among intermediary metabolism, mitochondrial function, and classic polycystic ovary syndrome. Free Radic Biol Med. 2015;86:295–307.PubMedCrossRef Zhao H, et al. Metabolism alteration in follicular niche: The nexus among intermediary metabolism, mitochondrial function, and classic polycystic ovary syndrome. Free Radic Biol Med. 2015;86:295–307.PubMedCrossRef
93.
go back to reference Gupta S, et al. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril. 2008;90(2):247–57.PubMedCrossRef Gupta S, et al. Pathogenic mechanisms in endometriosis-associated infertility. Fertil Steril. 2008;90(2):247–57.PubMedCrossRef
94.
go back to reference Da Broi MG, Navarro PA. Oxidative stress and oocyte quality: ethiopathogenic mechanisms of minimal/mild endometriosis-related infertility. Cell Tissue Res. 2016;364(1):1–7.PubMedCrossRef Da Broi MG, Navarro PA. Oxidative stress and oocyte quality: ethiopathogenic mechanisms of minimal/mild endometriosis-related infertility. Cell Tissue Res. 2016;364(1):1–7.PubMedCrossRef
95.
go back to reference Carvalho LF, et al. Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet. 2012;286(4):1033–40.PubMedCrossRef Carvalho LF, et al. Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet. 2012;286(4):1033–40.PubMedCrossRef
96.
go back to reference Regiani T, et al. Follicular fluid alterations in endometriosis: label-free proteomics by MS(E) as a functional tool for endometriosis. Syst Biol Reprod Med. 2015;61(5):263–76.PubMedCrossRef Regiani T, et al. Follicular fluid alterations in endometriosis: label-free proteomics by MS(E) as a functional tool for endometriosis. Syst Biol Reprod Med. 2015;61(5):263–76.PubMedCrossRef
97.
go back to reference Liu F, et al. The expression and role of oxidative stress markers in the serum and follicular fluid of patients with endometriosis. Clin Exp Obstet Gynecol. 2013;40(3):372–6.PubMed Liu F, et al. The expression and role of oxidative stress markers in the serum and follicular fluid of patients with endometriosis. Clin Exp Obstet Gynecol. 2013;40(3):372–6.PubMed
98.
go back to reference Singh AK, et al. Markers of oxidative stress in follicular fluid of women with endometriosis and tubal infertility undergoing IVF. Reprod Toxicol. 2013;42:116–24.PubMedCrossRef Singh AK, et al. Markers of oxidative stress in follicular fluid of women with endometriosis and tubal infertility undergoing IVF. Reprod Toxicol. 2013;42:116–24.PubMedCrossRef
99.
go back to reference Lo Turco EG, et al. Proteomic analysis of follicular fluid from women with and without endometriosis: new therapeutic targets and biomarkers. Mol Reprod Dev. 2013;80(6):441–50.PubMed Lo Turco EG, et al. Proteomic analysis of follicular fluid from women with and without endometriosis: new therapeutic targets and biomarkers. Mol Reprod Dev. 2013;80(6):441–50.PubMed
100.
go back to reference Giorgi VS, et al. N-Acetyl-Cysteine and l-Carnitine Prevent Meiotic Oocyte Damage Induced by Follicular Fluid From Infertile Women With Mild Endometriosis. Reprod Sci. 2016;23(3):342–51.PubMedCrossRef Giorgi VS, et al. N-Acetyl-Cysteine and l-Carnitine Prevent Meiotic Oocyte Damage Induced by Follicular Fluid From Infertile Women With Mild Endometriosis. Reprod Sci. 2016;23(3):342–51.PubMedCrossRef
101.
go back to reference Ozkaya MO, Naziroglu M. Multivitamin and mineral supplementation modulates oxidative stress and antioxidant vitamin levels in serum and follicular fluid of women undergoing in vitro fertilization. Fertil Steril. 2010;94(6):2465–6.PubMedCrossRef Ozkaya MO, Naziroglu M. Multivitamin and mineral supplementation modulates oxidative stress and antioxidant vitamin levels in serum and follicular fluid of women undergoing in vitro fertilization. Fertil Steril. 2010;94(6):2465–6.PubMedCrossRef
102.
go back to reference Kazemi A, Ramezanzadeh F, Nasr-Esfahani MH. The relations between dietary antioxidant vitamins intake and oxidative stress in follicular fluid and ART outcomes. Iran J Reprod Med. 2015;13(9):533–40.PubMedPubMedCentral Kazemi A, Ramezanzadeh F, Nasr-Esfahani MH. The relations between dietary antioxidant vitamins intake and oxidative stress in follicular fluid and ART outcomes. Iran J Reprod Med. 2015;13(9):533–40.PubMedPubMedCentral
103.
go back to reference Santanam N, Zoneraich N, Parthasarathy S. Myeloperoxidase as a Potential Target in Women With Endometriosis Undergoing IVF. Reprod Sci. 2017;24(4):619–26.PubMedCrossRef Santanam N, Zoneraich N, Parthasarathy S. Myeloperoxidase as a Potential Target in Women With Endometriosis Undergoing IVF. Reprod Sci. 2017;24(4):619–26.PubMedCrossRef
104.
go back to reference Szymanski W, Kazdepka-Zieminska A. Effect of homocysteine concentration in follicular fluid on a degree of oocyte maturity. Ginekol Pol. 2003;74(10):1392–6.PubMed Szymanski W, Kazdepka-Zieminska A. Effect of homocysteine concentration in follicular fluid on a degree of oocyte maturity. Ginekol Pol. 2003;74(10):1392–6.PubMed
105.
go back to reference Piomboni P, et al. Protein modification as oxidative stress marker in follicular fluid from women with polycystic ovary syndrome: the effect of inositol and metformin. J Assist Reprod Genet. 2014;31(10):1269–76.PubMedPubMedCentralCrossRef Piomboni P, et al. Protein modification as oxidative stress marker in follicular fluid from women with polycystic ovary syndrome: the effect of inositol and metformin. J Assist Reprod Genet. 2014;31(10):1269–76.PubMedPubMedCentralCrossRef
106.
107.
go back to reference Castro JP, et al. Actin carbonylation: from cell dysfunction to organism disorder. J Proteome. 2013;92:171–80.CrossRef Castro JP, et al. Actin carbonylation: from cell dysfunction to organism disorder. J Proteome. 2013;92:171–80.CrossRef
Metadata
Title
Follicular Fluid redox involvement for ovarian follicle growth
Authors
Cláudia Freitas
Ana Catarina Neto
Liliana Matos
Elisabete Silva
Ângela Ribeiro
João Luís Silva-Carvalho
Henrique Almeida
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2017
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/s13048-017-0342-3

Other articles of this Issue 1/2017

Journal of Ovarian Research 1/2017 Go to the issue