The Implications of Insufficient Zinc on the Generation of Oxidative Stress Leading to Decreased Oocyte Quality.
Infertility
Nitric oxide synthase
Oocyte
Oxidative stress
Reactive oxygen species
Zinc finger protein
Journal
Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249
Informations de publication
Date de publication:
07 2023
07 2023
Historique:
received:
12
12
2022
accepted:
07
03
2023
medline:
3
7
2023
pubmed:
16
3
2023
entrez:
15
3
2023
Statut:
ppublish
Résumé
Zinc is a transition metal that displays wide physiological implications ranging from participation in hundreds of enzymes and proteins to normal growth and development. In the reproductive tract of both sexes, zinc maintains a functional role in spermatogenesis, ovulation, fertilization, normal pregnancy, fetal development, and parturition. In this work, we review evidence to date regarding the importance of zinc in oocyte maturation and development, with emphasis on the role of key zinc-binding proteins, as well as examine the effects of zinc and reactive oxygen species (ROS) on oocyte quality and female fertility. We summarize our current knowledge about the participation of zinc in the developing oocyte bound to zinc finger proteins as well as loosely bound zinc ion in the intracellular and extracellular environments. These include aspects related to (1) the impact of zinc deficiency and overwhelming production of ROS under inflammatory conditions on the offset of the physiological antioxidant machinery disturbing biomolecules, proteins, and cellular processes, and their role in contributing to further oxidative stress; (2) the role of ROS in modulating damage to proteins containing zinc, such as zinc finger proteins and nitric oxide synthases (NOS), and expelling the zinc resulting in loss of protein function; and (3) clarify the different role of oxidative stress and zinc deficiency in the pathophysiology of infertility diseases with special emphasis on endometriosis-associated infertility.
Identifiants
pubmed: 36920672
doi: 10.1007/s43032-023-01212-0
pii: 10.1007/s43032-023-01212-0
doi:
Substances chimiques
Reactive Oxygen Species
0
Zinc
J41CSQ7QDS
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2069-2078Informations de copyright
© 2023. The Author(s), under exclusive licence to Society for Reproductive Investigation.
Références
Garner TB, Hester JM, Carothers A, Diaz FJ. Role of zinc in female reproduction. Biol Reprod. 2021;104(5):976–94. https://doi.org/10.1093/biolre/ioab023 .
doi: 10.1093/biolre/ioab023
pubmed: 33598687
pmcid: 8599883
McClung JP. Iron, zinc, and physical performance. Biol Trace Elem Res. 2019;188(1):135–9. https://doi.org/10.1007/s12011-018-1479-7 .
doi: 10.1007/s12011-018-1479-7
pubmed: 30112658
Fallah A, Mohammad-Hasani A, Colagar AH. Zinc is an essential element for male fertility: a review of Zn roles in men’s health, germination, sperm quality, and fertilization. J Reprod Infertil. 2018;19(2):69–81.
pubmed: 30009140
pmcid: 6010824
Sanna A, Firinu D, Zavattari P, Valera P. Zinc status and autoimmunity: a systematic review and meta-analysis. Nutrients. 2018;10(1):68 https://doi.org/10.3390/nu10010068 .
Skalny AV, Aschner M, Tinkov AA. Zinc. Adv Food Nutr Res. 2021;96:251–310. https://doi.org/10.1016/bs.afnr.2021.01.003
Li J, Chen H, Gou M, Tian C, Wang H, Song X, et al. Molecular features of polycystic ovary syndrome revealed by transcriptome analysis of oocytes and cumulus cells. Front Cell Dev Biol. 2021;9:735684. https://doi.org/10.3389/fcell.2021.735684 .
doi: 10.3389/fcell.2021.735684
pubmed: 34552933
pmcid: 8450412
Qiao J, Feng HL. Extra- and intra-ovarian factors in polycystic ovary syndrome: impact on oocyte maturation and embryo developmental competence. Hum Reprod Update. 2011;17(1):17–33. https://doi.org/10.1093/humupd/dmq032 .
doi: 10.1093/humupd/dmq032
pubmed: 20639519
Camp OG, Bai D, Goud PT, Diamond MP, Abu-Soud HM. A novel theory implicating hypochlorous acid as the primary generator of angiogenesis, infertility, and free iron in endometriosis. F&S Reviews. 2022;3(2):146–56. https://doi.org/10.1016/j.xfnr.2022.02.001 .
doi: 10.1016/j.xfnr.2022.02.001
Wessels I, Maywald M, Rink L. Zinc as a gatekeeper of immune function. Nutrients. 2017;9(12):1286. https://doi.org/10.3390/nu9121286 .
Hennigar SR, Lieberman HR, Fulgoni VL 3rd, McClung JP. Serum zinc concentrations in the US population are related to sex, age, and time of blood draw but not dietary or supplemental zinc. J Nutr. 2018;148(8):1341–51. https://doi.org/10.1093/jn/nxy105 .
doi: 10.1093/jn/nxy105
pubmed: 29947812
Hennigar SR, Kelley AM, McClung JP. Metallothionein and zinc transporter expression in circulating human blood cells as biomarkers of zinc status: a systematic review. Adv Nutr. 2016;7(4):735–46. https://doi.org/10.3945/an.116.012518 .
doi: 10.3945/an.116.012518
pubmed: 27422508
pmcid: 4942874
Eide DJ. The oxidative stress of zinc deficiency. Metallomics. 2011;3(11):1124–9. https://doi.org/10.1039/c1mt00064k .
doi: 10.1039/c1mt00064k
pubmed: 21789324
Kloubert V, Rink L. Zinc as a micronutrient and its preventive role of oxidative damage in cells. Food & Function. 2015;6(10):3195–204. Epub 2015/08/20. https://doi.org/10.1039/c5fo00630a . PubMed PMID: 26286461.
Lee SR. Critical role of zinc as either an antioxidant or a prooxidant in cellular systems. Oxid Med Cell Longev. 2018;2018:9156285. https://doi.org/10.1155/2018/9156285 .
doi: 10.1155/2018/9156285
pubmed: 29743987
pmcid: 5884210
Sethuram R, Bai D, Abu-Soud HM. Potential role of zinc in the COVID-19 disease process and its probable impact on reproduction. Reprod Sci. 2022;29(1):1–6. https://doi.org/10.1007/s43032-020-00400-6 .
doi: 10.1007/s43032-020-00400-6
pubmed: 33415646
Cassandri M, Smirnov A, Novelli F, Pitolli C, Agostini M, Malewicz M, et al. Zinc-finger proteins in health and disease. Cell Death Discov. 2017;3:17071. https://doi.org/10.1038/cddiscovery.2017.71 .
doi: 10.1038/cddiscovery.2017.71
pubmed: 29152378
pmcid: 5683310
Krishna SS, Majumdar I, Grishin NV. Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 2003;31(2):532–50. https://doi.org/10.1093/nar/gkg161 .
doi: 10.1093/nar/gkg161
pubmed: 12527760
pmcid: 140525
Miloch A, Krezel A. Metal binding properties of the zinc finger metallome–insights into variations in stability. Metallomics. 2014;6(11):2015–24. https://doi.org/10.1039/c4mt00149d .
doi: 10.1039/c4mt00149d
pubmed: 25109667
Kluska K, Adamczyk J, Krężel A. Metal binding properties, stability and reactivity of zinc fingers. Coord Chem Rev. 2018;367:18–64. https://doi.org/10.1016/j.ccr.2018.04.009 .
doi: 10.1016/j.ccr.2018.04.009
Colvin RA, Holmes WR, Fontaine CP, Maret W. Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis. Metallomics. 2010;2(5):306–17. https://doi.org/10.1039/b926662c .
doi: 10.1039/b926662c
pubmed: 21069178
Singh AK, Chattopadhyay R, Chakravarty B, Chaudhury K. Markers of oxidative stress in follicular fluid of women with endometriosis and tubal infertility undergoing IVF. Reprod Toxicol. 2013;42:116–24. https://doi.org/10.1016/j.reprotox.2013.08.005 .
doi: 10.1016/j.reprotox.2013.08.005
pubmed: 23994512
Yahfoufi ZA, Bai D, Khan SN, Chatzicharalampous C, Kohan-Ghadr HR, Morris RT, et al. Glyphosate induces metaphase II oocyte deterioration and embryo damage by zinc depletion and overproduction of reactive oxygen species. Toxicology. 2020;439:152466. https://doi.org/10.1016/j.tox.2020.152466 .
doi: 10.1016/j.tox.2020.152466
pubmed: 32315717
Nikbakht R, Mohammadjafari R, Rajabalipour M, Moghadam MT. Evaluation of oocyte quality in Polycystic ovary syndrome patients undergoing ART cycles. Fertil Res Pract. 2021;7(1):2. https://doi.org/10.1186/s40738-020-00094-z .
doi: 10.1186/s40738-020-00094-z
pubmed: 33397466
pmcid: 7784377
Aldhaheri SR, Jeelani R, Kohan-Ghadr HR, Khan SN, Mikhael S, Washington C, et al. Dimercapto-1-propanesulfonic acid (DMPS) induces metaphase II mouse oocyte deterioration. Free Radic Biol Med. 2017;112:445–51. https://doi.org/10.1016/j.freeradbiomed.2017.08.015 .
doi: 10.1016/j.freeradbiomed.2017.08.015
pubmed: 28844937
He M, Zhang T, Yang Y, Wang C. Mechanisms of oocyte maturation and related epigenetic regulation. Front Cell Dev Biol. 2021;9:654028. https://doi.org/10.3389/fcell.2021.654028 .
doi: 10.3389/fcell.2021.654028
pubmed: 33842483
pmcid: 8025927
Bernhardt ML, Kong BY, Kim AM, O’Halloran TV, Woodruff TK. A zinc-dependent mechanism regulates meiotic progression in mammalian oocytes. Biol Reprod. 2012;86(4):114. https://doi.org/10.1095/biolreprod.111.097253 .
doi: 10.1095/biolreprod.111.097253
pubmed: 22302686
pmcid: 3338659
Mehlmann LM. Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction. 2005;130(6):791–9. https://doi.org/10.1530/rep.1.00793 .
doi: 10.1530/rep.1.00793
pubmed: 16322539
Gershon E, Maimon I, Galiani D, Elbaz M, Karasenti S, Dekel N. High cGMP and low PDE3A activity are associated with oocyte meiotic incompetence. Cell Cycle. 2019;18(20):2629–40. https://doi.org/10.1080/15384101.2019.1652472 .
doi: 10.1080/15384101.2019.1652472
pubmed: 31401933
pmcid: 6773239
Shuhaibar LC, Egbert JR, Norris RP, Lampe PD, Nikolaev VO, Thunemann M, et al. Intercellular signaling via cyclic GMP diffusion through gap junctions restarts meiosis in mouse ovarian follicles. Proc Natl Acad Sci U S A. 2015;112(17):5527–32. https://doi.org/10.1073/pnas.1423598112 .
doi: 10.1073/pnas.1423598112
pubmed: 25775542
pmcid: 4418852
Granot I, Dekel N. Phosphorylation and expression of connexin-43 ovarian gap junction protein are regulated by luteinizing hormone. J Biol Chem. 1994;269(48):30502–9.
doi: 10.1016/S0021-9258(18)43842-2
pubmed: 7982967
Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, et al. Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development. 2008;135(19):3229–38. https://doi.org/10.1242/dev.025494 .
doi: 10.1242/dev.025494
pubmed: 18776144
Zhang W, Colman RW. Conserved amino acids in metal-binding motifs of PDE3A are involved in substrate and inhibitor binding. Blood. 2000;95(11):3380–6.
doi: 10.1182/blood.V95.11.3380
pubmed: 10828019
Vaccari S, Weeks JL 2nd, Hsieh M, Menniti FS, Conti M. Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod. 2009;81(3):595–604. https://doi.org/10.1095/biolreprod.109.077768 .
doi: 10.1095/biolreprod.109.077768
pubmed: 19474061
pmcid: 2731981
Fan H-Y, Sun Q-Y. Chapter 12 Oocyte meiotic maturation. Ovary. 2019:181–203. https://doi.org/10.1016/B978-0-12-813209-8.00012-1
Tripathi A, Kumar KV, Chaube SK. Meiotic cell cycle arrest in mammalian oocytes. J Cell Physiol. 2010;223(3):592–600. https://doi.org/10.1002/jcp.22108 .
doi: 10.1002/jcp.22108
pubmed: 20232297
Prasad S, Tiwari M, Koch B, Chaube SK. Morphological, cellular and molecular changes during postovulatory egg aging in mammals. J Biomed Sci. 2015;22:36. https://doi.org/10.1186/s12929-015-0143-1 .
doi: 10.1186/s12929-015-0143-1
pubmed: 25994054
pmcid: 4440248
Madgwick S, Jones KT. How eggs arrest at metaphase II: MPF stabilisation plus APC/C inhibition equals Cytostatic Factor. Cell Div. 2007;2:4. https://doi.org/10.1186/1747-1028-2-4 .
doi: 10.1186/1747-1028-2-4
pubmed: 17257429
pmcid: 1794241
Kim AM, Bernhardt ML, Kong BY, Ahn RW, Vogt S, Woodruff TK, et al. Zinc sparks are triggered by fertilization and facilitate cell cycle resumption in mammalian eggs. ACS Chem Biol. 2011;6(7):716–23. https://doi.org/10.1021/cb200084y .
doi: 10.1021/cb200084y
pubmed: 21526836
pmcid: 3171139
Wu JM, Zelinski MB, Ingram DK, Ottinger MA. Ovarian aging and menopause: current theories, hypotheses, and research models. Exp Biol Med (Maywood). 2005;230(11):818–28. https://doi.org/10.1177/153537020523001106 .
doi: 10.1177/153537020523001106
pubmed: 16339746
Xi X, Zou Q, Wei Y, Chen Y, Wang X, Lv D, et al. Dynamic changes of DNA methylation and transcriptome expression in porcine ovaries during aging. BioMed Res Int. 2019;2019:8732023. https://doi.org/10.1155/2019/8732023 .
doi: 10.1155/2019/8732023
pubmed: 31781648
pmcid: 6874880
Malhi PS, Adams GP, Mapletoft RJ, Singh J. Superovulatory response in a bovine model of reproductive aging. Anim Reprod Sci. 2008;109(1–4):100–9. https://doi.org/10.1016/j.anireprosci.2007.12.002 .
doi: 10.1016/j.anireprosci.2007.12.002
pubmed: 18374524
Uliani RC, Conley AJ, Corbin CJ, Friso AM, Maciel LFS, Alvarenga MA. Anti-Müllerian hormone and ovarian aging in mares. J Endocrinol. 2019;240(2):147–56. https://doi.org/10.1530/joe-18-0391 .
doi: 10.1530/joe-18-0391
pubmed: 30400031
Nichols SM, Bavister BD, Brenner CA, Didier PJ, Harrison RM, Kubisch HM. Ovarian senescence in the rhesus monkey (Macaca mulatta). Hum Reprod (Oxford, England). 2005;20(1):79–83. https://doi.org/10.1093/humrep/deh576 .
doi: 10.1093/humrep/deh576
Mendoza AD, Sue A, Antipova O, Vogt S, Woodruff TK, Wignall SM, et al. Dynamic zinc fluxes regulate meiotic progression in Caenorhabditis elegans†. Biol Reprod. 2022;107(2):406–18. https://doi.org/10.1093/biolre/ioac064 .
doi: 10.1093/biolre/ioac064
pubmed: 35466369
pmcid: 9902257
Que EL, Bleher R, Duncan FE, Kong BY, Gleber SC, Vogt S, et al. Quantitative mapping of zinc fluxes in the mammalian egg reveals the origin of fertilization-induced zinc sparks. Nat Chem. 2015;7(2):130–9. https://doi.org/10.1038/nchem.2133 .
doi: 10.1038/nchem.2133
pubmed: 25615666
Kim AM, Vogt S, O’Halloran TV, Woodruff TK. Zinc availability regulates exit from meiosis in maturing mammalian oocytes. Nat Chem Biol. 2010;6(9):674–81. https://doi.org/10.1038/nchembio.419 .
doi: 10.1038/nchembio.419
pubmed: 20693991
pmcid: 2924620
Celik O, Celik N, Gungor S, Haberal ET, Aydin S. Selective regulation of oocyte meiotic events enhances progress in fertility preservation methods. Biochem Insights. 2015;8:11–21. https://doi.org/10.4137/BCI.S28596 .
doi: 10.4137/BCI.S28596
pubmed: 26417205
pmcid: 4577271
Tian X, Diaz FJ. Zinc depletion causes multiple defects in ovarian function during the periovulatory period in mice. Endocrinology. 2012;153(2):873–86. https://doi.org/10.1210/en.2011-1599 .
doi: 10.1210/en.2011-1599
pubmed: 22147014
Kong BY, Duncan FE, Que EL, Kim AM, O’Halloran TV, Woodruff TK. Maternally-derived zinc transporters ZIP6 and ZIP10 drive the mammalian oocyte-to-egg transition. Mol Hum Reprod. 2014;20(11):1077–89. https://doi.org/10.1093/molehr/gau066 .
doi: 10.1093/molehr/gau066
pubmed: 25143461
pmcid: 4209882
Zhang N, Duncan FE, Que EL, O’Halloran TV, Woodruff TK. The fertilization-induced zinc spark is a novel biomarker of mouse embryo quality and early development. Sci Rep. 2016;6:22772. https://doi.org/10.1038/srep22772 .
doi: 10.1038/srep22772
pubmed: 26987302
pmcid: 4796984
Tian X, Diaz FJ. Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development. Dev Biol. 2013;376(1):51–61. https://doi.org/10.1016/j.ydbio.2013.01.015 .
doi: 10.1016/j.ydbio.2013.01.015
pubmed: 23348678
pmcid: 3601821
Jeon Y, Yoon JD, Cai L, Hwang SU, Kim E, Zheng Z, et al. Supplementation of zinc on oocyte in vitro maturation improves preimplatation embryonic development in pigs. Theriogenology. 2014;82(6):866–74. https://doi.org/10.1016/j.theriogenology.2014.06.021 .
doi: 10.1016/j.theriogenology.2014.06.021
pubmed: 25091527
Jablonka-Shariff A, Olson LM. The role of nitric oxide in oocyte meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology. 1998;139(6):2944–54. https://doi.org/10.1210/endo.139.6.6054 .
doi: 10.1210/endo.139.6.6054
pubmed: 9607805
Tranguch S, Steuerwald N, Huet-Hudson YM. Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biol Reprod. 2003;68(5):1538–44. https://doi.org/10.1095/biolreprod.102.009282 .
doi: 10.1095/biolreprod.102.009282
pubmed: 12606428
Khorram O. Nitric oxide and its role in blastocyst implantation. Rev Endocr Metab Disord. 2002;3(2):145–9. https://doi.org/10.1023/a:1015459029397 .
doi: 10.1023/a:1015459029397
pubmed: 12007291
Nishikimi A, Matsukawa T, Hoshino K, Ikeda S, Kira Y, Sato EF, et al. Localization of nitric oxide synthase activity in unfertilized oocytes and fertilized embryos during preimplantation development in mice. Reproduction. 2001;122(6):957–63. https://doi.org/10.1530/rep.0.1220957 .
doi: 10.1530/rep.0.1220957
pubmed: 11732991
Goud AP, Goud PT, Diamond MP, Abu-Soud HM. Nitric oxide delays oocyte aging. Biochemistry. 2005;44(34):11361–8. https://doi.org/10.1021/bi050711f .
doi: 10.1021/bi050711f
pubmed: 16114873
Abu-Soud HM, Stuehr DJ. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc Natl Acad Sci U S A. 1993;90(22):10769–72. https://doi.org/10.1073/pnas.90.22.10769 .
doi: 10.1073/pnas.90.22.10769
pubmed: 7504282
pmcid: 47859
Raman CS, Li H, Martasek P, Kral V, Masters BS, Poulos TL. Crystal structure of constitutive endothelial nitric oxide synthase: a paradigm for pterin function involving a novel metal center. Cell. 1998;95(7):939–50. https://doi.org/10.1016/s0092-8674(00)81718-3 .
doi: 10.1016/s0092-8674(00)81718-3
pubmed: 9875848
Stuehr DJ. Mammalian nitric oxide synthases. Biochim Biophys Acta. 1999;1411(2–3):217–30. https://doi.org/10.1016/s0005-2728(99)00016-x .
doi: 10.1016/s0005-2728(99)00016-x
pubmed: 10320659
Goud AP, Goud PT, Diamond MP, Gonik B, Abu-Soud HM. Activation of the cGMP signaling pathway is essential in delaying oocyte aging in diabetes mellitus. Biochemistry. 2006;45(38):11366–78. https://doi.org/10.1021/bi060910e .
doi: 10.1021/bi060910e
pubmed: 16981697
Goud PT, Goud AP, Diamond MP, Gonik B, Abu-Soud HM. Nitric oxide extends the oocyte temporal window for optimal fertilization. Free Radic Biol Med. 2008;45(4):453–9. https://doi.org/10.1016/j.freeradbiomed.2008.04.035 .
doi: 10.1016/j.freeradbiomed.2008.04.035
pubmed: 18489913
pmcid: 3786211
Ignarro LJ. Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: a unique transduction mechanism for transcellular signaling. Pharmacol Toxicol. 1990;67(1):1–7. https://doi.org/10.1111/j.1600-0773.1990.tb00772.x .
doi: 10.1111/j.1600-0773.1990.tb00772.x
pubmed: 1975691
Denninger JW, Marletta MA. Guanylate cyclase and the .NO/cGMP signaling pathway. Biochim Biophys Acta. 1999;1411(2–3):334–50. https://doi.org/10.1016/s0005-2728(99)00024-9 .
doi: 10.1016/s0005-2728(99)00024-9
pubmed: 10320667
Camp OG, Bai D, Awonuga A, Goud PT, Abu-Soud HM. Hypochlorous acid facilitates inducible nitric oxide synthase subunit dissociation: the link between heme destruction, disturbance of the zinc-tetrathiolate center, and the prevention by melatonin. Nitric Oxide. 2022;124:32–8. https://doi.org/10.1016/j.niox.2022.04.006 .
doi: 10.1016/j.niox.2022.04.006
pubmed: 35513289
Foster MW, Hess DT, Stamler JS. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med. 2009;15(9):391–404. https://doi.org/10.1016/j.molmed.2009.06.007 .
doi: 10.1016/j.molmed.2009.06.007
pubmed: 19726230
pmcid: 3106339
Banerjee J, Shaeib F, Maitra D, Saed GM, Dai J, Diamond MP, et al. Peroxynitrite affects the cumulus cell defense of metaphase II mouse oocytes leading to disruption of the spindle structure in vitro. Fertil Steril. 2013;100(2):578-84.e1. https://doi.org/10.1016/j.fertnstert.2013.04.030 .
doi: 10.1016/j.fertnstert.2013.04.030
pubmed: 23721714
Shaeib F, Khan SN, Ali I, Thakur M, Saed MG, Dai J, et al. The defensive role of cumulus cells against reactive oxygen species insult in metaphase II mouse oocytes. Reprod Sci. 2016;23(4):498–507. https://doi.org/10.1177/1933719115607993 .
doi: 10.1177/1933719115607993
pubmed: 26468254
Thakur M, Shaeib F, Khan SN, Kohan-Ghadr HR, Jeelani R, Aldhaheri SR, et al. Galactose and its metabolites deteriorate metaphase II mouse oocyte quality and subsequent embryo development by disrupting the spindle structure. Sci Rep. 2017;7(1):231. https://doi.org/10.1038/s41598-017-00159-y .
doi: 10.1038/s41598-017-00159-y
pubmed: 28331195
pmcid: 5427935
Goud AP, Goud PT, Diamond MP, Gonik B, Abu-Soud HM. Reactive oxygen species and oocyte aging: role of superoxide, hydrogen peroxide, and hypochlorous acid. Free Radic Biol Med. 2008;44(7):1295–304. https://doi.org/10.1016/j.freeradbiomed.2007.11.014 .
doi: 10.1016/j.freeradbiomed.2007.11.014
pubmed: 18177745
Cetica PD, Pintos LN, Dalvit GC, Beconi MT. Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life. 2001;51(1):57–64. https://doi.org/10.1080/15216540119253 .
doi: 10.1080/15216540119253
pubmed: 11419698
Cetica PD, Pintos LN, Dalvit GC, Beconi MT. Effect of lactate dehydrogenase activity and isoenzyme localization in bovine oocytes and utilization of oxidative substrates on in vitro maturation. Theriogenology. 1999;51(3):541–50. https://doi.org/10.1016/s0093-691x(99)00008-4 .
doi: 10.1016/s0093-691x(99)00008-4
pubmed: 10729040
Ferre-Pujol P, Nguyen XK, Nagahara T, Bui TTM, Wakai T, Funahashi H. Removal of cumulus cells around 20 h after the start of in vitro maturation improves the meiotic competence of porcine oocytes via reduction in cAMP and cGMP levels. J Reprod Dev. 2019;65(2):177–82. https://doi.org/10.1262/jrd.2018-130 .
doi: 10.1262/jrd.2018-130
pubmed: 30745497
pmcid: 6473111
Beckman JS, Chen J, Ischiropoulos H, Crow JP. Oxidative chemistry of peroxynitrite. Methods Enzymol. 1994;233:229–40. https://doi.org/10.1016/s0076-6879(94)33026-3 .
doi: 10.1016/s0076-6879(94)33026-3
pubmed: 8015460
Li MS, Adesina SE, Ellis CL, Gooch JL, Hoover RS, Williams CR. NADPH oxidase-2 mediates zinc deficiency-induced oxidative stress and kidney damage. Am J Physiol Cell Physiol. 2017;312(1):C47–55. https://doi.org/10.1152/ajpcell.00208.2016 .
doi: 10.1152/ajpcell.00208.2016
pubmed: 27806940
Olechnowicz J, Tinkov A, Skalny A, Suliburska J. Zinc status is associated with inflammation, oxidative stress, lipid, and glucose metabolism. J Physiol Sci. 2018;68(1):19–31. https://doi.org/10.1007/s12576-017-0571-7 .
doi: 10.1007/s12576-017-0571-7
pubmed: 28965330
Goud PT, Goud AP, Najafi T, Gonik B, Diamond MP, Saed GM, et al. Direct real-time measurement of intra-oocyte nitric oxide concentration in vivo. PLoS One. 2014;9(6):e98720. https://doi.org/10.1371/journal.pone.0098720 .
doi: 10.1371/journal.pone.0098720
pubmed: 24887331
pmcid: 4041775
Huber KL, Hardy JA. Mechanism of zinc-mediated inhibition of caspase-9. Protein Sci. 2012;21(7):1056–65. https://doi.org/10.1002/pro.2090 .
doi: 10.1002/pro.2090
pubmed: 22573662
pmcid: 3403442
Velazquez-Delgado EM, Hardy JA. Zinc-mediated allosteric inhibition of caspase-6. J Biol Chem. 2012;287(43):36000–11. https://doi.org/10.1074/jbc.M112.397752 .
doi: 10.1074/jbc.M112.397752
pubmed: 22891250
pmcid: 3476268
Maret W, Jacob C, Vallee BL, Fischer EH. Inhibitory sites in enzymes: zinc removal and reactivation by thionein. Proc Natl Acad Sci U S A. 1999;96(5):1936–40. https://doi.org/10.1073/pnas.96.5.1936 .
doi: 10.1073/pnas.96.5.1936
pubmed: 10051573
pmcid: 26715
Eron SJ, MacPherson DJ, Dagbay KB, Hardy JA. Multiple mechanisms of zinc-mediated inhibition for the apoptotic caspases-3, -6, -7, and -8. ACS Chem Biol. 2018;13(5):1279–90. https://doi.org/10.1021/acschembio.8b00064 .
doi: 10.1021/acschembio.8b00064
pubmed: 29364645
pmcid: 5959779
Searle AJF, Tomasi A. Hydroxyl free radical production in iron-cysteine solutions and protection by zinc. J Inorg Biochem. 1982;17(2):161–6. https://doi.org/10.1016/S0162-0134(00)80085-9 .
doi: 10.1016/S0162-0134(00)80085-9
Powell SR. The antioxidant properties of zinc. J Nutr. 2000;130(5S Suppl):1447S-S1454. https://doi.org/10.1093/jn/130.5.1447S .
doi: 10.1093/jn/130.5.1447S
pubmed: 10801958
Girotti AW, Thomas JP, Jordan JE. Inhibitory effect of zinc(II) on free radical lipid peroxidation in erythrocyte membranes. J Free Radic Biol Med. 1985;1(5–6):395–401. https://doi.org/10.1016/0748-5514(85)90152-7 .
doi: 10.1016/0748-5514(85)90152-7
pubmed: 3841804
Shoji S, Muto Y, Ikeda M, He F, Tsuda K, Ohsawa N, et al. The zinc-binding region (ZBR) fragment of Emi2 can inhibit APC/C by targeting its association with the coactivator Cdc20 and UBE2C-mediated ubiquitylation. FEBS Open Bio. 2014;4:689–703. https://doi.org/10.1016/j.fob.2014.06.010 .
doi: 10.1016/j.fob.2014.06.010
pubmed: 25161877
pmcid: 4141206
Jia JL, Han YH, Kim HC, Ahn M, Kwon JW, Luo Y, et al. Structural basis for recognition of Emi2 by Polo-like kinase 1 and development of peptidomimetics blocking oocyte maturation and fertilization. Sci Rep. 2015;5:14626. https://doi.org/10.1038/srep14626 .
doi: 10.1038/srep14626
pubmed: 26459104
pmcid: 4602232
Zhao MH, Kim NH, Cui XS. Zinc depletion activates porcine metaphase II oocytes independently of the protein kinase C pathway. In Vitro Cell Dev Biol Anim. 2014;50(10):945–51. https://doi.org/10.1007/s11626-014-9784-8 .
doi: 10.1007/s11626-014-9784-8
pubmed: 25107407
Suzuki T, Yoshida N, Suzuki E, Okuda E, Perry AC. Full-term mouse development by abolishing Zn2+-dependent metaphase II arrest without Ca2+ release. Development. 2010;137(16):2659–69. https://doi.org/10.1242/dev.049791 .
doi: 10.1242/dev.049791
pubmed: 20591924
Hubner C, Haase H. Interactions of zinc- and redox-signaling pathways. Redox Biol. 2021;41:101916. https://doi.org/10.1016/j.redox.2021.101916 .
doi: 10.1016/j.redox.2021.101916
pubmed: 33662875
pmcid: 7937829
Marla SS, Lee J, Groves JT. Peroxynitrite rapidly permeates phospholipid membranes. Proc Natl Acad Sci U S A. 1997;94(26):14243–8. https://doi.org/10.1073/pnas.94.26.14243 .
doi: 10.1073/pnas.94.26.14243
pubmed: 9405597
pmcid: 24925
Podrez EA, Abu-Soud HM, Hazen SL. Myeloperoxidase-generated oxidants and atherosclerosis. Free Radic Biol Med. 2000;28(12):1717–25. https://doi.org/10.1016/s0891-5849(00)00229-x .
doi: 10.1016/s0891-5849(00)00229-x
pubmed: 10946213
Banerjee J, Maitra D, Diamond MP, Abu-Soud HM. Melatonin prevents hypochlorous acid-induced alterations in microtubule and chromosomal structure in metaphase-II mouse oocytes. J Pineal Res. 2012;53(2):122–8. https://doi.org/10.1111/j.1600-079X.2012.00977.x .
doi: 10.1111/j.1600-079X.2012.00977.x
pubmed: 22304486
Zondervan KT, Becker CM, Koga K, Missmer SA, Taylor RN, Vigano P. Endometriosis Nat Rev Dis Primers. 2018;4(1):9. https://doi.org/10.1038/s41572-018-0008-5 .
doi: 10.1038/s41572-018-0008-5
pubmed: 30026507
Alvarado-Diaz CP, Nunez MT, Devoto L, Gonzalez-Ramos R. Iron overload-modulated nuclear factor kappa-B activation in human endometrial stromal cells as a mechanism postulated in endometriosis pathogenesis. Fertil Steril. 2015;103(2):439–47. https://doi.org/10.1016/j.fertnstert.2014.10.046 .
doi: 10.1016/j.fertnstert.2014.10.046
pubmed: 25500022
Xiu-li W, Su-ping H, Hui-hua D, Zhi-xue Y, Shi-long F, Pin-hong L. NF-kappaB decoy oligonucleotides suppress RANTES expression and monocyte chemotactic activity via NF-kappaB inactivation in stromal cells of ectopic endometrium. J Clin Immunol. 2009;29(3):387–95. https://doi.org/10.1007/s10875-009-9274-z .
doi: 10.1007/s10875-009-9274-z
pubmed: 19172384
Taniguchi F, Harada T, Miyakoda H, Iwabe T, Deura I, Tagashira Y, et al. TAK1 activation for cytokine synthesis and proliferation of endometriotic cells. Mol Cell Endocrinol. 2009;307(1–2):196–204. https://doi.org/10.1016/j.mce.2009.04.012 .
doi: 10.1016/j.mce.2009.04.012
pubmed: 19410630
Kim KH, Lee EN, Park JK, Lee JR, Kim JH, Choi HJ, et al. Curcumin attenuates TNF-alpha-induced expression of intercellular adhesion molecule-1, vascular cell adhesion molecule-1 and proinflammatory cytokines in human endometriotic stromal cells. Phytother Res. 2012;26(7):1037–47. https://doi.org/10.1002/ptr.3694 .
doi: 10.1002/ptr.3694
pubmed: 22183741
Veillat V, Lavoie CH, Metz CN, Roger T, Labelle Y, Akoum A. Involvement of nuclear factor-kappaB in macrophage migration inhibitory factor gene transcription up-regulation induced by interleukin- 1 beta in ectopic endometrial cells. Fertil Steril. 2009;91(5 Suppl):2148–56. https://doi.org/10.1016/j.fertnstert.2008.05.017 .
doi: 10.1016/j.fertnstert.2008.05.017
pubmed: 18710704
Cao WG, Morin M, Metz C, Maheux R, Akoum A. Stimulation of macrophage migration inhibitory factor expression in endometrial stromal cells by interleukin 1, beta involving the nuclear transcription factor NFkappaB. Biol Reprod. 2005;73(3):565–70. https://doi.org/10.1095/biolreprod.104.038331 .
doi: 10.1095/biolreprod.104.038331
pubmed: 15901641
Ohama Y, Harada T, Iwabe T, Taniguchi F, Takenaka Y, Terakawa N. Peroxisome proliferator-activated receptor-gamma ligand reduced tumor necrosis factor-alpha-induced interleukin-8 production and growth in endometriotic stromal cells. Fertil Steril. 2008;89(2):311–7. https://doi.org/10.1016/j.fertnstert.2007.03.061 .
doi: 10.1016/j.fertnstert.2007.03.061
pubmed: 17555752
Lebovic DI, Chao VA, Martini JF, Taylor RN. IL-1beta induction of RANTES (regulated upon activation, normal T cell expressed and secreted) chemokine gene expression in endometriotic stromal cells depends on a nuclear factor-kappaB site in the proximal promoter. J Clin Endocrinol Metab. 2001;86(10):4759–64. https://doi.org/10.1210/jcem.86.10.7890 .
doi: 10.1210/jcem.86.10.7890
pubmed: 11600537
Sakamoto Y, Harada T, Horie S, Iba Y, Taniguchi F, Yoshida S, et al. Tumor necrosis factor-alpha-induced interleukin-8 (IL-8) expression in endometriotic stromal cells, probably through nuclear factor-kappa B activation: gonadotropin-releasing hormone agonist treatment reduced IL-8 expression. J Clin Endocrinol Metab. 2003;88(2):730–5. https://doi.org/10.1210/jc.2002-020666 .
doi: 10.1210/jc.2002-020666
pubmed: 12574206
Liu Y, Wang J, Zhang X. An update on the multifaceted role of NF-kappaB in endometriosis. Int J Biol Sci. 2022;18(11):4400–13. https://doi.org/10.7150/ijbs.72707 .
doi: 10.7150/ijbs.72707
pubmed: 35864971
pmcid: 9295070
Ozaki Y, Ohashi T, Kume S. Potentiation of neutrophil function by recombinant DNA-produced interleukin 1a. J Leukoc Biol. 1987;42(6):621–7. https://doi.org/10.1002/jlb.42.6.621 .
doi: 10.1002/jlb.42.6.621
pubmed: 3500253
Berkow RL, Wang D, Larrick JW, Dodson RW, Howard TH. Enhancement of neutrophil superoxide production by preincubation with recombinant human tumor necrosis factor. J Immunol. 1987;139(11):3783–91.
doi: 10.4049/jimmunol.139.11.3783
pubmed: 2824615
Kocyigit A, Gur S, Erel O, Gurel MS. Associations among plasma selenium, zinc, copper, and iron concentrations and immunoregulatory cytokine levels in patients with cutaneous leishmaniasis. Biol Trace Elem Res. 2002;90(1–3):47–55. https://doi.org/10.1385/BTER:90:1-3:47 .
doi: 10.1385/BTER:90:1-3:47
pubmed: 12666825
Uzzo RG, Leavis P, Hatch W, Gabai VL, Dulin N, Zvartau N, et al. Zinc inhibits nuclear factor-kappa B activation and sensitizes prostate cancer cells to cytotoxic agents. Clin Cancer Res. 2002;8(11):3579–83.
pubmed: 12429649
Kim CH, Kim JH, Moon SJ, Chung KC, Hsu CY, Seo JT, et al. Pyrithione, a zinc ionophore, inhibits NF-kappaB activation. Biochem Biophys Res Commun. 1999;259(3):505–9. https://doi.org/10.1006/bbrc.1999.0814 .
doi: 10.1006/bbrc.1999.0814
pubmed: 10364448
Ho E, Quan N, Tsai YH, Lai W, Bray TM. Dietary zinc supplementation inhibits NFkappaB activation and protects against chemically induced diabetes in CD1 mice. Exp Biol Med (Maywood). 2001;226(2):103–11. https://doi.org/10.1177/153537020122600207 .
doi: 10.1177/153537020122600207
pubmed: 11446433
Otsu K, Ikeda Y, Fujii J. Accumulation of manganese superoxide dismutase under metal-depleted conditions: proposed role for zinc ions in cellular redox balance. Biochem J. 2004;377(Pt 1):241–8. https://doi.org/10.1042/BJ20030935 .
doi: 10.1042/BJ20030935
pubmed: 14531733
pmcid: 1223854
Goud PT, Goud AP, Joshi N, Puscheck E, Diamond MP, Abu-Soud HM. Dynamics of nitric oxide, altered follicular microenvironment, and oocyte quality in women with endometriosis. Fertil Steril. 2014;102(1):151-9.e5. https://doi.org/10.1016/j.fertnstert.2014.03.053 .
doi: 10.1016/j.fertnstert.2014.03.053
pubmed: 24825428
Hsu AL, Townsend PM, Oehninger S, Castora FJ. Endometriosis may be associated with mitochondrial dysfunction in cumulus cells from subjects undergoing in vitro fertilization-intracytoplasmic sperm injection, as reflected by decreased adenosine triphosphate production. Fertil Steril. 2015;103(2):347-52.e1. https://doi.org/10.1016/j.fertnstert.2014.11.002 .
doi: 10.1016/j.fertnstert.2014.11.002
pubmed: 25516080
Mate G, Bernstein LR, Torok AL. Endometriosis is a cause of infertility. Does reactive oxygen damage to gametes and embryos play a key role in the pathogenesis of infertility caused by endometriosis? Front Endocrinol (Lausanne). 2018;9:725. https://doi.org/10.3389/fendo.2018.00725 .
doi: 10.3389/fendo.2018.00725
pubmed: 30555421
Xu B, Guo N, Zhang XM, Shi W, Tong XH, Iqbal F, et al. Oocyte quality is decreased in women with minimal or mild endometriosis. Sci Rep. 2015;5:10779. https://doi.org/10.1038/srep10779 .
doi: 10.1038/srep10779
pubmed: 26022105
pmcid: 4448226
Jiang H, He X, Wang S, Jia J, Wan Y, Wang Y, et al. A microtubule-associated zinc finger protein, BuGZ, regulates mitotic chromosome alignment by ensuring Bub3 stability and kinetochore targeting. Dev Cell. 2014;28(3):268–81. https://doi.org/10.1016/j.devcel.2013.12.013 .
doi: 10.1016/j.devcel.2013.12.013
pubmed: 24462186
pmcid: 3927447
Soubry A, Staes K, Parthoens E, Noppen S, Stove C, Bogaert P, et al. The transcriptional repressor Kaiso localizes at the mitotic spindle and is a constituent of the pericentriolar material. PLoS One. 2010;5(2):e9203. https://doi.org/10.1371/journal.pone.0009203 .
doi: 10.1371/journal.pone.0009203
pubmed: 20169156
pmcid: 2821401