The possible involvement of oxidative stress in the oocyte ageing process in goldfish Carassius auratus (Linnaeus, 1758)

. 2019 Jul 18 ; 9 (1) : 10469. [epub] 20190718

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31320670
Odkazy

PubMed 31320670
PubMed Central PMC6639355
DOI 10.1038/s41598-019-46895-1
PII: 10.1038/s41598-019-46895-1
Knihovny.cz E-zdroje

Decreasing egg quality following oocyte ageing is a major restricting factor for the breeding programs. The mechanisms behind this process has not yet been clarified. To examine the possible involvement of oxidative stress in the oocyte ageing process, the relative mRNA abundance of specific transcripts were determined in oocytes collected from 6 females and incubated in vitro for 18 hours post stripping at 20 °C in goldfish Carassius auratus. During the 18 hour-post-stripping ageing of the oocytes, relative mRNA levels of candidate transcripts involved in oxidative injury, mitochondrial function and stress response, cell cycles, apoptosis, reproduction and germ line speciation and developmental competence were measured by real-time PCR. None of the relative mRNA abundance of the examined genes were significantly altered through oocyte ageing. In addition, the amount of thiobarbituric acid reactive substances (TBARS), an indicator of lipid peroxidation, did not change over time following stripping. The activity of the antioxidant enzymes also remained constant during oocyte ageing. The results of the current study indicated that oxidative stress unlikely plays a role as an initiator or promotor in the progress of oocyte ageing in goldfish.

Zobrazit více v PubMed

Liang X, Ma J, Schatten H, Sun Q. Epigenetic changes associated with oocyte aging. Sci. China. Life. Sci. 2012;55(8):670–676. doi: 10.1007/s11427-012-4354-3. PubMed DOI

Lahnsteiner F, Urbanyi B, Horvath A, Weismann T. Bio-markers for egg quality determination in cyprinid fish. Aquaculture. 2001;195:331–352. doi: 10.1016/S0044-8486(00)00550-0. DOI

Samarin AM, et al. Effects of post-ovulatory oocyte ageing and temperature on egg quality in kutum Rutilus frisii kutum. World. Appl. Sci. J. 2011;15(1):14–18.

Flajshans M, Kohlmann K, Rab P. Autotriploid tench Tinca tinca (L.) larvae obtained by fertilization of eggs previously subjected to postovulatory ageing in vitro and in vivo. J. Fish Biol. 2007;71:868–876. doi: 10.1111/j.1095-8649.2007.01557.x. DOI

Aegerter S, Jalabert B. Effects of post ovulatory oocyte ageing and temperature on egg quality and on the occurrence of triploid fry in rainbow trout Oncorhynchus mykiss. Aquaculture. 2004;231:59–71. doi: 10.1016/j.aquaculture.2003.08.019. DOI

Bonnet E, Fostier A, Bobe J. Characterization of rainbow trout egg quality: a case study using four different breeding protocols, with emphasis on the incidence of embryonic malformations. Theriogenology. 2007;67:786–794. doi: 10.1016/j.theriogenology.2006.10.008. PubMed DOI

Samarin AM, et al. In vitro storage of unfertilized eggs of the Eurasian perch and its effect on egg viability rates and the occurrence of larval malformations. Animal. 2017;11(1):78–83. doi: 10.1017/S1751731116001361. PubMed DOI

Tarin JJ, Perez-Albala S, Perez-Hoyos P, Cano A. Postovulatory aging of oocytes decreases reproductive fitness and longevity of offspring. Biol. Reprod. 2002;66:495–499. doi: 10.1095/biolreprod66.2.495. PubMed DOI

Liang XW, et al. The effects of postovulatory aging of mouse oocytes on methylation and expression of imprinted genes at midterm gestation. Mol. Hum. Reprod. 2011;17:562–567. doi: 10.1093/molehr/gar018. PubMed DOI

Liang XW, et al. Loss of methylation imprint of Snrpn in postovulatory aging mouse oocyte. Biochem. Biophys. Res. Commun. 2008;371:16–21. doi: 10.1016/j.bbrc.2008.03.105. PubMed DOI

Minami N, Suzuki T, Tsukamoto S. Zygotic gene activation and maternal factors in mammals. J. Reprod. Dev. 2007;53:707–715. doi: 10.1262/jrd.19029. PubMed DOI

Yoshida N, Brahmajisyula M, Shoji S, Amanai M, Perry AC. Epigenetic discrimination by mouse metaphase II oocytes mediated asymmetric chromatin remodelling independently of meiotic exit. Dev. Biol. 2007;301:464–477. doi: 10.1016/j.ydbio.2006.08.006. PubMed DOI

Samarin AM, Policar T, Lahnsteiner F. Fish oocyte ageing and its effect on egg quality. Rev. Fish. Sci. Aquac. 2015;23:302–314. doi: 10.1080/23308249.2015.1053560. DOI

Zuccotti M, Merico V, Cecconi S, Redi CA, Garagna S. What does it take to make a developmentally competent mammalian egg? Hum. Reprod. Update. 2011;17:525–540. doi: 10.1093/humupd/dmr009. PubMed DOI

Bonnet E, Fostier A, Bobe J. Microarray-based analysis of fish egg quality after natural or controlled ovulation. BMC Genomics. 2007;8:55. doi: 10.1186/1471-2164-8-55. PubMed DOI PMC

Aegerter S, Jalabert B, Bobe J. MessengerRNAstockpile of cyclin B, insulin-like growth factor I, insulin-like growth factor II, insulinlike growth factor receptor Ib, and p53 in the rainbow trout oocyte in relation with developmental competence. Mol. Reprod. Dev. 2004;67:127–135. doi: 10.1002/mrd.10384. PubMed DOI

Aegerter S, Jalabert B, Bobe J. Large scale real-time PCR analysis of mRNA abundance in rainbow trout eggs in relationship with egg quality and postovulatory ageing. Mol. Reprod. Dev. 2005;72:377–385. doi: 10.1002/mrd.20361. PubMed DOI

Mommens M, et al. Maternal gene expression in Atlantic halibut (Hippoglossus hippoglossus L.) and its relation to egg quality. BMC Res Notes. 2010;3:138. doi: 10.1186/1756-0500-3-138. PubMed DOI PMC

Ma H, et al. MicroRNA expression profiles from eggs of different qualities associated with post-ovulatory ageing in rainbow trout (Oncorhynchus mykiss) BMC Genomics. 2015;16:201. doi: 10.1186/s12864-015-1400-0. PubMed DOI PMC

Lord T, Nixon B, Jones KT, Aitken RJ. Melatonin prevents postovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro. Biol. Reprod. 2013;88:1–9. doi: 10.1095/biolreprod.112.106450. PubMed DOI

Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013;146:217–227. doi: 10.1530/REP-13-0111. PubMed DOI

Takahashi T, Takahashi E, Igarashi H, Tezuka N, Kurachi H. Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol. Reprod. Dev. 2003;66:143–152. doi: 10.1002/mrd.10341. PubMed DOI

Tarin JJ, Perez-Albala S, Cano A. Consequences on offspring of abnormal function in ageing gametes. Hum. Reprod. Update. 2000;6:532–549. doi: 10.1093/humupd/6.6.532. PubMed DOI

Samarin AM, et al. mRNA abundance changes during in vitro oocyte ageing in African catfish Clarias gariepinus (Burchell, 1822) Aquac. Res. 2018;49:1037–1045. doi: 10.1111/are.13552. DOI

Kikuchi K, Naito K, Noguchi J, Kaneko H, Tojo H. Maturation/M-phase promoting factor regulates aging of porcine oocytes matured in vitro. Cloning Stem Cells. 2002;4:211–222. doi: 10.1089/15362300260339494. PubMed DOI

Formacion MJ, Venkatesh B, Tan CH, Lam TJ. Overripening of ovulated eggs in goldfish, Carassius auratus: II. Possible involvement of postovulatory follicles and steroids. Fish Physiol. Biochem. 1995;14(3):237–246. doi: 10.1007/BF00004314. PubMed DOI

Grondahl ML, et al. Gene expression profiles of single human mature oocytes in relation to age. Hum. Reprod. 2010;25(4):957–68. doi: 10.1093/humrep/deq014. PubMed DOI

Steuerwald NM, Bermudez MG, Wells D, Munne S, Cohen J. Maternal age-related differential global expression profiles observed in human oocytes. Reprod. Biomed. Online. 2007;14:700–708. doi: 10.1016/S1472-6483(10)60671-2. PubMed DOI

Pan H, O’Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and develop¬ment in vitro. Dev. Biol. 2005;286:493–506. doi: 10.1016/j.ydbio.2005.08.023. PubMed DOI

Hamatani T, et al. Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 2004;13(19):2263–2278. doi: 10.1093/hmg/ddh241. PubMed DOI

Esponda, P. & Dıaz, H. Age-induced apoptosis and activation of heat shock protein HSP70 in mammalian oocytes. Signalling and Apoptosis, PP-184a (2006).

Verbeke P, Fonager J, Clark BF, Rattan SI. Heat shock response and ageing: mechanisms and applications. Cell Biol. Int. 2001;25:845–857. doi: 10.1006/cbir.2001.0789. PubMed DOI

Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC. A fraction of yeast Cu, Zn superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria: a physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 2001;276:38084–9. PubMed

Pechenino AS, Brown TR. Superoxide dismutase in the prostate lobes of aging Brown Norway rats. Prostate. 2006;66:522–35. doi: 10.1002/pros.20364. PubMed DOI

Wesson DE, Elliott SJ. The H2O2-generating enzyme, xanthine oxidase, decreases luminal Ca2+ content of the IP3- sensitive Ca2+ store in vascular endothelial cells. Microcirculation. 1995;2:195–203. doi: 10.3109/10739689509146767. PubMed DOI

Schallreuter KU, Gibbons NC, Zothner C, Abou Elloof MM, Wood JM. Hydrogen peroxide-mediated oxidative stress disrupts calcium binding on calmodulin: more evidence for oxidative stress in vitiligo. Biochem. Biophys. Res. Commun. 2007;360:70–75. doi: 10.1016/j.bbrc.2007.05.218. PubMed DOI

Takahashi T, et al. Poor embryo development in mouse oocytes aged in vitro is associated with impaired calcium homeostasis. Biol. Reprod. 2009;80:493–502. doi: 10.1095/biolreprod.108.072017. PubMed DOI

Xu Z, Abbott A, Kopf GS, Schultz RM, Ducibella T. Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-triphosphate sensitivity. Biol. Reprod. 1997;57:743–750. doi: 10.1095/biolreprod57.4.743. PubMed DOI

Ma W, et al. Reduced expression of MAD2, BCL2, and MAP kinase activity in pig oocytes after in vitro aging are associated with defects in sister chromatid segregation during meiosis II and embryo fragmentation after activation. Biol. Reprod. 2005;72:373–383. doi: 10.1095/biolreprod.104.030999. PubMed DOI

Carnevali O, Mosconi G, Cardinali M, Meiri I, Polzonetti-Magni A. Molecular components related to egg viability in the gilthead sea bream, Sparus aurata. Mol. Reprod. Dev. 2001;58(3):330–5. doi: 10.1002/1098-2795(200103)58:3<330::AID-MRD11>3.0.CO;2-7. PubMed DOI

Raz E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 2000;1(3):reviews1017. doi: 10.1186/gb-2000-1-3-reviews1017. PubMed DOI PMC

Nikolic, A., Volarevic, V., Armstrong, L., Lako, M. & Stojkovic, M. Primordial germ cells: current knowledge and perspectives. Stem Cells Int. 1741072 (2016). PubMed PMC

Tzung KW, et al. Early Depletion of Primordial Germ Cells in Zebrafish Promotes Testis Formation. Stem Cell Reports. 2015;4(1):61–73. doi: 10.1016/j.stemcr.2014.10.011. PubMed DOI PMC

Liu W, et al. Complete depletion of primordial germ cells in an All-female fish leads to Sex-biased gene expression alteration and sterile All-male occurrence. BMC Genomics. 2015;16:971. doi: 10.1186/s12864-015-2130-z. PubMed DOI PMC

Houseweart MK, et al. Cathepsin B but not cathepsins L or S contributes to the pathogenesis of Unverricht-Lundborg progressive myoclonus epilepsy (EPM1) J. Neurobiol. 2003;56(4):315–327. doi: 10.1002/neu.10253. PubMed DOI

Kågedal K, Johansson U, Öllinger K. The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J. 2001;15:1592–1594. doi: 10.1096/fj.00-0708fje. PubMed DOI

Samarin AM, et al. Alteration of mRNA abundance, oxidation products and antioxidant enzyme activities during oocyte ageing in common carp Cyprinus carpio. PLoS One. 2019;14(2):e0212694. doi: 10.1371/journal.pone.0212694. PubMed DOI PMC

Abe K, Inoue A, Suzuki MG, Aoki F. Global gene silencing is caused by the dissociation of RNA polymerase II from DNA in mouse oocytes. J. Reprod. Dev. 2010;56:502–507. doi: 10.1262/jrd.10-068A. PubMed DOI

Clarke HJ. Post-transcriptional control of gene expression during mouse oogenesis. Results. Probl. Cell. Differ. 2012;55:1–21. doi: 10.1007/978-3-642-30406-4_1. PubMed DOI

Weill L, Belloc E, Bava FA, Mendez R. Translational control by changes in poly(A) tail length: recycling mRNAs. Nat. Struct. Mol. Biol. 2012;19:577–585. doi: 10.1038/nsmb.2311. PubMed DOI

Dankert D, et al. Pre- and postovulatory aging of murine oocytes affect the transcript level and poly(A) tail length of maternal effect genes. PLoS One. 2014;9:e108907. doi: 10.1371/journal.pone.0108907. PubMed DOI PMC

Wilson VL, Jones PA. DNA methylation decreases in aging but not in immortal cells. Science. 1983;220:1055–1057. doi: 10.1126/science.6844925. PubMed DOI

Crary-Dooley FK, et al. A comparison of existing global DNA methylation assays to low-coverage whole-genome bisulfite sequencing for epidemiological studies. Epigenetics. 2017;12:206–214. doi: 10.1080/15592294.2016.1276680. PubMed DOI PMC

McCauley BS, Dang W. Histone methylation and aging: lessons learned from model systems. Biochem. Biophys. Acta. 2014;1839(12):1454–62. PubMed PMC

Xu Y, Zhang JJ, Grifo JA, Krey LC. DNA methylation patterns in human tripronucleate zygotes. Mol. Hum. Reprod. 2004;11:167–171. doi: 10.1093/molehr/gah145. PubMed DOI

Ge ZJ, Schatten H, Zhang CL, Sun QY. Oocyte ageing and epigenetics. Reproduction. 2015;149:R103–R114. doi: 10.1530/REP-14-0242. PubMed DOI PMC

Kjorsvik E, Mangor-Jensen A, Holmefjord I. Egg quality in fishes. Adv. Mar. boil. 1990;26:71–113. doi: 10.1016/S0065-2881(08)60199-6. DOI

Brooks S, Tyler CR, Sumpter JP. Egg quality in fish: what makes a good egg? Rev. Fish. Biol. Fisher. 1997;7:387–416. doi: 10.1023/A:1018400130692. DOI

Flanagan JM, et al. Intra-and interindividual epigenetic variation in human germ cells. Am. J. Hum. Genet. 2006;79:67–84. doi: 10.1086/504729. PubMed DOI PMC

Goldberg AD, Allis CD, Bernstein E. Epigenetics: a landscape takes shape. Cell. 2007;128:635–638. doi: 10.1016/j.cell.2007.02.006. PubMed DOI

Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 2003;33:245–254. doi: 10.1038/ng1089. PubMed DOI

Fauvel C, Suquet M, Cosson J. Evaluation of fish sperm quality. J. Appl. Ichthyol. 2010;26:636–643. doi: 10.1111/j.1439-0426.2010.01529.x. DOI

Koressaar T, Remm M. Enhancements and modifications of primer design program Primer3. Bioinformatics. 2007;23(10):1289–1291. doi: 10.1093/bioinformatics/btm091. PubMed DOI

Untergasser A, et al. Primer3 - new capabilities and interfaces. Nucleic Acids Res. 2012;40(15):e115. doi: 10.1093/nar/gks596. PubMed DOI PMC

Smith PK, et al. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985;150:76–85. doi: 10.1016/0003-2697(85)90442-7. PubMed DOI

Claiborne, A. Catalase activity. In Greenwall, R. A. (Ed.), CRC handbook of methods in oxygen radical research (pp. 283–284). Boca Raton, FL: CRC Press (1985).

Nishikimi M, Rao NA, Yagi K. The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem. Biophys. Res. Commun. 1972;46:849–854. doi: 10.1016/S0006-291X(72)80218-3. PubMed DOI

Mohandas J, Marshall JJ, Duggin GG, Horvath JS, Tiller DJ. Differential distribution of glutathione and glutathione-related enzymes in rabbit kidney - possible implications in analgesic nephropathy. Biochem. Pharmacol. 1984;33:1801–1807. doi: 10.1016/0006-2952(84)90353-8. PubMed DOI

Cribb AE, Leeder JS, Spielberg SP. Use of a microplate reader in an assay of glutathione-reductase using 5,5′-dithiobis (2-nitrobenzoic acid) Anal. Biochem. 1989;183:195–196. doi: 10.1016/0003-2697(89)90188-7. PubMed DOI

Li P, et al. Evaluating the impacts of osmotic and oxidative stress on common carp (Cyprinus carpio L.) sperm caused by cryopreservation techniques. Biol. Reprod. 2010;83:852–858. doi: 10.1095/biolreprod.110.085852. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...