Oocyte ageing is the most important factor affecting egg quality of several fish species after ovulation. Oxidative stress has been proposed as the initiator of the oocyte ageing process in other vertebrates. To identify the role of oxidative stress and apoptosis on the progress of oocyte ageing in the common carp Cyprinus carpio, changes in the relative mRNA abundance of selected transcripts were examined. The possible alteration in the oxidation status of the oocytes during ageing was also studied. In addition, the activity of antioxidant enzymes during oocyte ageing was evaluated. Oocytes from 6 females were incubated in vivo for 14 hours post-ovulation (HPO) and in vitro for 10 hours post-stripping (HPS) at 20°C before fertilization. Hatching rates were over 65% up to 4-6 HPO, finally dropping to 1.3% at 12-14 HPO.Hatching rates were over 65% up to 4-6 HPO, finally dropping to 1.3% at 12-14 HPO. Hatching rates were more than 70% for the eggs stored in vitro up to 6 HPS and then decreased to 21.3% at 10 HPS. The results demonstrated no significant changes in the relative mRNA levels of oxidative stress-related genes or genes involved in the cell cycle during the progress of oocyte ageing in common carp. Additionally, the amount of TBARS and carbonyls did not change as time elapsed following ovulation. The apoptosis-related genes however, were significantly altered following the prolonged time interval between ovulation and fertilization. The lack of response of both activities of antioxidant enzymes and oxidation products during oocyte ageing strengthens the conclusion that oxidative stress is unlikely to be a main factor determining the progress of oocyte ageing in common carp. However, an increase in the mRNA abundance of apoptosis-related genes demonstrates that apoptotic pathway might be involved in the progress of oocyte ageing.

Department of Molecular Sciences Swedish University of Agricultural Sciences Uppsala Sweden

Nofima Ås Norway

University of South Bohemia in Ceske Budejovice Faculty of Fisheries and Protection of Waters South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Research Institute of Fish Culture and Hydrobiology Vodňany Czech Republic

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Schultz GA, Heyner S. Gene expression in pre-implantation mammalian embryos. Mutat Res. 1992; 296: 17–31. PubMed

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

Torres-Padilla ME, Bannister AJ, Hurd PJ, Kouzarides T, Zernicka-Goetz M. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int J Dev Biol. 2006; 50: 455–461. 10.1387/ijdb.052073mt 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. 10.1016/j.ydbio.2006.08.006 PubMed DOI

Lam TJ, Nagahama Y, Chan K, Hoar WS. Overripe eggs and post-ovulatory corpora lutea in the three spined stickleback. Can J Zool. 1978; 56: 2029–2036.

McEvoy (Barton) L.-A. Ovulatory rhythms and over-ripening of eggs in cultivated turbot, Scophthalmus maximus L. J Fish Biol. 1984; 24: 437–448.

Rime H, Guitton N, Pineau C, Bonnet E, Bobe J, Jalabert B. Post-ovulatory ageing and egg quality: A proteomic analysis of rainbow trout coelomic fluid. Reprod Biol Endocrinol. 2004; 2: 26–36. 10.1186/1477-7827-2-26 PubMed DOI PMC

Bobe J, Labbe C. Egg and sperm quality in fish. Gen Comp Endocrinol. 2010; 165: 535–548. 10.1016/j.ygcen.2009.02.011 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.

Lahnsteiner F, Urbanyi B, Horvath A, Weismann T. Biomarkers for egg quality determination in cyprinid fish. Aquaculture. 2001; 195: 331–352.

Samarin AM, Gela D, Bytyutskyy D, Policar T. Determination of the best post-ovulatory stripping time for the common carp, Cyprinus carpio. J Appl Ichthyol. 2015; 31(2): 51–55.

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.

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. 10.1016/j.theriogenology.2006.10.008 PubMed DOI

Samarin AM, Żarski D, Palińska-Żarska K, Krejszeff S, Blecha M, Kucharczyk D, 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. 10.1017/S1751731116001361 PubMed DOI

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.

Samarin AM, Blecha M, Uzhytchak M, Bytyutskyy D, Żarski D, Flajshans M, et al. Post-ovulatory and post-stripping oocyte ageing in northern pike, Esox lucius (Linnaeus, 1758), and its effect on egg viability rates and the occurrence of larval malformations and ploidy anomalies. Aquaculture. 2016; 450: 431–438.

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. 10.1093/humupd/dmr009 PubMed DOI

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. 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 post-ovulatory ageing. Mol Reprod Dev. 2005; 72: 377–385. 10.1002/mrd.20361 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 10.1186/1471-2164-8-55 PubMed DOI PMC

Mommens M, Fernandes JM, Bizuayehu TT, Bolla SL, Johnston IA, Babiak I. Maternal gene expression in Atlantic halibut (Hippoglossus hippoglossus L.) and its relation to egg quality. BMC Res Notes. 2010; 3: 138 10.1186/1756-0500-3-138 PubMed DOI PMC

Ma H, Weber GM, Hostuttler MA, Wei H, Wang L, Yao J. MicroRNA expression profiles from eggs of different qualities associated with post-ovulatory ageing in rainbow trout (Oncorhynchus mykiss). BMC Genomics. 2015; 16: 201 10.1186/s12864-015-1400-0 PubMed DOI PMC

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

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. 10.1002/mrd.10341 PubMed DOI

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. 10.1095/biolreprod.112.105957 PubMed DOI

Dean RT, Gieseg S, Davies MJ. Reactive species and their accumulation on radical-damaged proteins. Trends Biochem Sci. 1993; 18: 437–441. PubMed

Headlam HA, Davies MJ. Markers of protein oxidation: different oxidants give rise to variable yields of bound and released carbonyl products. Free Radic Biol Med. 2004; 36: 1175–1184. 10.1016/j.freeradbiomed.2004.02.017 PubMed DOI

Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol. 2007; 47: 143–183. 10.1146/annurev.pharmtox.47.120505.105122 PubMed DOI

Mok HJ, Shin H, Lee JW, Lee GK, Suh CS, Kim KP, et al. Age-associated lipidome changes in metaphase II mouse oocytes. PLoS ONE. 2016; 11(2): e0148577 10.1371/journal.pone.0148577 PubMed DOI PMC

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(3): 211–222. 10.1089/15362300260339494 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. PubMed

Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, et al. Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet. 2004; 13(19): 2263–2278. 10.1093/hmg/ddh241 PubMed DOI

Horvath L, Tamas G. Common Carp, part 1: mass production of eggs and early fry 1st ed Rome: Food and Agriculture Organization of the United Nations; 1985.

Komrakova M, Holtz W. Factors responsible for successful chilled storage of unfertilized rainbow trout (Oncorhynchus mykiss) eggs. Aquaculture. 2009; 286: 156–163.

Babiak I, Dabrowski K. Refrigeration of rainbow trout gametes and embryos. J Exp Zool A Comp Exp Biol. 2003; 300(2): 140–151. 10.1002/jez.a.10319 PubMed DOI

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

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012; 40(15): e115 10.1093/nar/gks596 PubMed DOI PMC

Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985; 150: 76–85. PubMed

Claiborne A. Catalase activity In: Greenwall RA, editor. CRC handbook of methods for oxygen radical research. Boca Raton: CRC Press; 1985. pp. 283–284.

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. PubMed

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. PubMed

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. PubMed

Li P, Li ZH, Dzyuba B, Hulak M, Rodina M, Linhart O. 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. 10.1095/biolreprod.110.085852 PubMed DOI

Oliver C, Ahn B, Moerman E, Goldstein S, Stadtman E. Age-related changes in oxidized proteins. J Biol Chem. 1987; 262: 5488–5491. PubMed

Lord T, Aitken RJ. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction. 2013; 146: 217–227. PubMed

Esponda P, Diaz H. Age-induced apoptosis and activation of heat shock protein HSP70 in mammalian oocytes. Signaling and Apoptosis. 2006; PP–184a.

Boerjan ML, de Boer P. First cell cycle of zygotes of the mouse derived from oocytes aged postovulation in vivo and fertilized in vivo. Mol Reprod Dev. 1990; 25: 155–163. 10.1002/mrd.1080250208 PubMed DOI

Yang HW, Hwang KJ, Kwon HC, Kim HS, Choi KW, Oh KS. Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod. 1998; 13: 998–1002. PubMed

Samarin AM, Sampels S, Policar T, Rodina M, Hematyar N, Samarin AM. mRNA abundance changes during in vitro oocyte ageing in African catfish Clarias gariepinus (Burchell, 1822). Aquac Res. 2018; 49: 1037–1045.

Raz E. The function and regulation of vasa-like genes in germ-cell development. Genome Biol. 2000; 1(3): reviews1017.1–1017.6. PubMed PMC

Nikolic A, Volarevic V, Armstrong L, Lako M, Stojkovic M. Primordial Germ Cells: Current Knowledge and Perspectives. Stem Cells Int. 2016; 2016: 1741072 10.1155/2016/1741072 PubMed DOI PMC

Saffman E, Lasko P. Germline development in vertebrates and invertebrates. Cell Mol Life Sci. 1999; 55: 1141–1163. PubMed PMC

Tzung KW, Goto R, Saju JM, Sreenivasan R, Saito T, Arai K, et al. Early depletion of primordial germ cells in zebrafish promotes testis formation. Stem Cell Reports. 2015; 4(1): 61–73. 10.1016/j.stemcr.2014.10.011 PubMed DOI PMC

Liu W, Li SZ, Li Z, Wang Y, Li XY, Zhong JX, 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 10.1186/s12864-015-2130-z PubMed DOI PMC

Ma W, Zhang D, Hou Y, Li YH, Sun QY, Sun XF, 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. 10.1095/biolreprod.104.030999 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. PubMed

Takai Y, Matikainen T, Juriscova A, Kim MR, Trbovich AM, Fujita E, et al. Caspase-12 compensates for lack of caspase-2 and caspase-3 in female germ cells. Apoptosis. 2007; 12: 791–800. 10.1007/s10495-006-0022-z PubMed DOI

Perez GI, Juriscova A, Matikainen T, Morityama T, Kim MR, Takai Y, et al. A central role for ceramide in the age-related acceleration of apoptosis in the female germline. FASEB J. 2005; 19: 860–862. 10.1096/fj.04-2903fje PubMed DOI

Fujino Y, Ozaki K, Yamamasu S, Ito F, Matsuoka I, Hayashi E, et al. DNA fragmentation of oocytes in aged mice. Hum Reprod. 1996; 11: 1480–1483. PubMed

Takahashi T, Igarashi H, Amita M, Hara S, Matsuo K, Kurachi H. Molecular mechanism of poor embryo development in postovulatory aged oocytes: Mini review. J Obstet Gynaecol Res. 2013; 39: 1431–1439. 10.1111/jog.12111 PubMed DOI

Gordo AC, Rodrigues P, Kurokawa M. Intracellular calcium oscillations signal apoptosis rather than activation in in vitro aged mouse eggs. Biol Reprod. 2002; 66: 1828–1837. PubMed

Li M, Baumeister P, Roy B, Phan T, Foti D, Luo S, et al. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol Cell Biol. 2000; 20: 5096–5106. PubMed PMC

Cleary ML, Smith SD, Sklar J. Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14;18) translocation. Cell. 1986; 47 (1): 19–28. PubMed

Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science. 1984; 226 (4678): 1097–1099. PubMed

Houseweart MK, Pennacchio LA, Vilaythong A, Peters C, Noebels JL, Myers RM. Cathepsin B but not cathepsins L or S contributes to the pathogenesis of Unverricht-Lundborg progressive myoclonus epilepsy (EPM1). J Neurobiol. 2003; 56(4): 315–27. 10.1002/neu.10253 PubMed DOI

Kågedal K, Johansson U, Ollinger K. The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J. 2001; 15: 1592–1594. PubMed

Butt AJ, Firth SM, Baxter RC. The IGF axis and programmed cell death. Immunol Cell Biol. 1999; 77: 256–262. 10.1046/j.1440-1711.1999.00822.x PubMed DOI

Huang JC, Yan LY, Lei ZL, Miao YL, Shi LH, Yang JW, et al. Changes in histone acetylation during postovulatory aging of mouse oocyte. Biol Reprod. 2007; 77: 666–670. 10.1095/biolreprod.107.062703 PubMed DOI

Liang XW, Zhu JQ, Miao YL, Liu JH, Wei L, Lu SS, et al. Loss of methylation imprint of Snrpn in postovulatory aging mouse oocyte. Biochem Biophys Res Commun. 2008; 371(1): 16–21. 10.1016/j.bbrc.2008.03.105 PubMed DOI

Liang XW, Ge ZI, Wei L, Guo L, Han ZM, Schatten H, et al. The effects of postovulatory aging of mouse oocytes on methylation and expression of imprinted genes at mid-term gestation. Mol Hum Reprod. 2011; 17: 562–567. 10.1093/molehr/gar018 PubMed DOI

Mayer W, Nivelelai A, Walter J, Fundele R, Haaf T. Demethylation of the zygotic paternal genome. Nature. 2000; 403: 501–502. 10.1038/35000654 PubMed DOI

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