Histone Acetylation Dynamics during In Vivo and In Vitro Oocyte Aging in Common Carp Cyprinus carpio
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
20-01251S
Grantová Agentura České Republiky
LRI CENAKVA LM2018099; Biodiversity (CZ.02.1.01/0.0/0.0/ 16_025/0007370)
Ministry of Education, Youth and Sports of the Czech Republic, projects: LRI CENAKVA LM2018099, Biodiversity (CZ.02.1.01/0.0/0.0/ 16_025/0007370)
046/2020/Z
Grant Agency of the University of South Bohemia in České Budějovice
PubMed
34204879
PubMed Central
PMC8199789
DOI
10.3390/ijms22116036
PII: ijms22116036
Knihovny.cz E-zdroje
- Klíčová slova
- Cyprinus carpio, egg quality, epigenetics, histone acetyltransferase, histone modifications, post-ovulatory aging,
- MeSH
- acetylace MeSH
- histonacetyltransferasy genetika MeSH
- histony genetika MeSH
- kapři genetika růst a vývoj MeSH
- oocyty růst a vývoj metabolismus MeSH
- posttranslační úpravy proteinů genetika MeSH
- stárnutí genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- histonacetyltransferasy MeSH
- histony MeSH
Aging is the most critical factor that influences the quality of post-ovulatory oocytes. Age-related molecular pathways remain poorly understood in fish oocytes. In this study, we examined the effect of oocyte aging on specific histone acetylation in common carp Cyprinus carpio. The capacity to progress to the larval stage in oocytes that were aged for 28 h in vivo and in vitro was evaluated. Global histone modifications and specific histone acetylation (H3K9ac, H3K14ac, H4K5ac, H4K8ac, H4K12ac, and H4K16ac) were investigated during oocyte aging. Furthermore, the activity of histone acetyltransferase (HAT) was assessed in fresh and aged oocytes. Global histone modifications did not exhibit significant alterations during 8 h of oocyte aging. Among the selected modifications, H4K12ac increased significantly at 28 h post-stripping (HPS). Although not significantly different, HAT activity exhibited an upward trend during oocyte aging. Results of our current study indicate that aging of common carp oocytes for 12 h results in complete loss of egg viability rates without any consequence in global and specific histone modifications. However, aging oocytes for 28 h led to increased H4K12ac. Thus, histone acetylation modification as a crucial epigenetic mediator may be associated with age-related defects, particularly in oocytes of a more advanced age.
CBIO Aarhus University Centre for Circular Bioeconomy 8000 Aarhus Denmark
Department of Food Science Aarhus University Agro Food Park 48 8200 Aarhus Denmark
Zobrazit více v PubMed
Petri T., Dankert D., Demond H., Wennemuth G., Horsthemke B., Grummer R. In vitro postovulatory oocyte aging affects H3K9 trimethylation in two-cell embryos after IVF. Ann. Anat. 2020;227:151424. doi: 10.1016/j.aanat.2019.151424. PubMed DOI
Reading B., Andersen L., Ryu Y.-W., Mushirobira Y., Todo T., Hiramatsu N. Oogenesis and Egg Quality in Finfish: Yolk Formation and Other Factors Influencing Female Fertility. Fishes. 2018;3:45. doi: 10.3390/fishes3040045. 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
Samarin A.M., 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
Flanagan J.M., Popendikyte V., Pozdniakovaite N., Sobolev M., Assadzadeh A., Schumacher A., Zangeneh M., Lau L., Virtanen C., Wang S.C., 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 A.D., Allis C.D., Bernstein E. Epigenetics: A landscape takes shape. Cell. 2007;128:635–638. doi: 10.1016/j.cell.2007.02.006. PubMed DOI
Bobe J., Labbe C. Egg and sperm quality in fish. Gen. Comp. Endocrinol. 2010;165:535–548. doi: 10.1016/j.ygcen.2009.02.011. PubMed DOI
Gonzalo S. Epigenetic alterations in aging. J. Appl. Physiol. 2010;109:586–597. doi: 10.1152/japplphysiol.00238.2010. PubMed DOI PMC
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. doi: 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 Genom. 2007;8:55. doi: 10.1186/1471-2164-8-55. PubMed DOI PMC
Mommens M., Fernandes J.M., Bizuayehu T.T., Bolla S.L., Johnston I.A., Babiak I. 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., Weber G.M., Hostuttler M.A., 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 Genom. 2015;16:201. doi: 10.1186/s12864-015-1400-0. PubMed DOI PMC
Bizuayehu T.T., Mommens M., Sundaram A.Y.M., Dhanasiri A.K.S., Babiak I. Postovulatory maternal transcriptome in Atlantic salmon and its relation to developmental potential of embryos. BMC Genom. 2019;20:315. doi: 10.1186/s12864-019-5667-4. PubMed DOI PMC
Samarin A.M., Samarin A.M., Ostbye T.K., Ruyter B., Sampels S., Burkina V., Blecha M., Policar T. The possible involvement of oxidative stress in the oocyte ageing process in goldfish Carassius auratus (Linnaeus, 1758) Sci. Rep. 2019;9:10469. doi: 10.1038/s41598-019-46895-1. PubMed DOI PMC
Liang X., Ma J., Schatten H., Sun Q. Epigenetic changes associated with oocyte aging. Sci. China Life Sci. 2012;55:670–676. doi: 10.1007/s11427-012-4354-3. PubMed DOI
Ge Z.J., Schatten H., Zhang C.L., Sun Q.Y. Oocyte ageing and epigenetics. Reproduction. 2015;149:R103–R114. doi: 10.1530/REP-14-0242. PubMed DOI PMC
Heinzmann J., Mattern F., Aldag P., Bernal-Ulloa S.M., Schneider T., Haaf T., Niemann H. Extended in vitro maturation affects gene expression and DNA methylation in bovine oocytes. Mol. Hum. Reprod. 2015;21:770–782. doi: 10.1093/molehr/gav040. PubMed DOI
Cui M.S., Wang X.L., Tang D.W., Zhang J., Liu Y., Zeng S.M. Acetylation of H4K12 in porcine oocytes during in vitro aging: Potential role of ooplasmic reactive oxygen species. Theriogenology. 2011;75:638–646. doi: 10.1016/j.theriogenology.2010.09.031. PubMed DOI
Huang J.C., Yan L.Y., Lei Z.L., Miao Y.L., Shi L.H., Yang J.W., Wang Q., Ouyang Y.C., Sun Q.Y., Chen D.Y. Changes in histone acetylation during postovulatory aging of mouse oocyte. Biol. Reprod. 2007;77:666–670. doi: 10.1095/biolreprod.107.062703. PubMed DOI
Labbé C., Robles V., Herraez M.P. Epigenetics in fish gametes and early embryo. Aquaculture. 2017;472:93–106. doi: 10.1016/j.aquaculture.2016.07.026. DOI
Bannister A.J., Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–395. doi: 10.1038/cr.2011.22. PubMed DOI PMC
Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–260. doi: 10.1038/38444. PubMed DOI
Rothbart S.B., Strahl B.D. Interpreting the language of histone and DNA modifications. Biochim. Biophys. Acta. 2014;1839:627–643. doi: 10.1016/j.bbagrm.2014.03.001. PubMed DOI PMC
Gavazzo P., Vergani L., Mascetti G.C., Nicolini C. Effects of histone acetylation on chromatin structure. J. Cell. Biochem. 1997;64:466–475. doi: 10.1002/(SICI)1097-4644(19970301)64:3<466::AID-JCB13>3.0.CO;2-E. PubMed DOI
Turner B.M. Histone acetylation and an epigenetic code. Bioessays. 2000;22:836–845. doi: 10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X. PubMed DOI
Kurdistani S.K., Grunstein M. Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell Biol. 2003;4:276–284. doi: 10.1038/nrm1075. PubMed DOI
Shahbazian M.D., Grunstein M. Functions of Site-Specific Histone Acetylation and Deacetylation. Annu. Rev. Biochem. 2007;76:75–100. doi: 10.1146/annurev.biochem.76.052705.162114. PubMed DOI
Zhang G.M., Gu C.H., Zhang Y.L., Sun H.Y., Qian W.P., Zhou Z.R., Wan Y.J., Jia R.X., Wang L.Z., Wang F. Age-associated changes in gene expression of goat oocytes. Theriogenology. 2013;80:328–336. doi: 10.1016/j.theriogenology.2013.04.019. PubMed DOI
Linhart O., Kudo S., Billard R., Slechta V., Mikodina E.V. Morphology, Composition and Fertilization of Carp Eggs—A Review. Aquaculture. 1995;129:75–93. doi: 10.1016/0044-8486(94)00230-L. DOI
Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature. 2000;403:41–45. doi: 10.1038/47412. PubMed DOI
Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705. doi: 10.1016/j.cell.2007.02.005. PubMed DOI
Bloushtain-Qimron N., Yao J., Shipitsin M., Maruyama R., Polyak K. Epigenetic patterns of embryonic and adult stem cells. Cell Cycle. 2009;8:809–817. doi: 10.4161/cc.8.6.7938. PubMed DOI
Wang N., Tilly J.L. Epigenetic status determines germ cell meiotic commitment in embryonic and postnatal mammalian gonads. Cell Cycle. 2010;9:339–349. doi: 10.4161/cc.9.2.10447. PubMed DOI PMC
Gu L., Wang Q., Sun Q.Y. Histone modifications during mammalian oocyte maturation: Dynamics, regulation and functions. Cell Cycle. 2010;9:1942–1950. doi: 10.4161/cc.9.10.11599. PubMed DOI
Cunliffe V.T. Histone modifications in zebrafish development. Methods Cell Biol. 2016;135:361–385. doi: 10.1016/bs.mcb.2016.05.005. PubMed DOI
Turner B.M. Defining an epigenetic code. Nat. Cell. Biol. 2007;9:2–6. doi: 10.1038/ncb0107-2. PubMed DOI
Xing X., Zhang J., Wu T., Zhang J., Wang Y., Su J., Zhang Y. SIRT1 reduces epigenetic and non-epigenetic changes to maintain the quality of postovulatory aged oocytes in mice. Exp. Cell Res. 2021;399:112421. doi: 10.1016/j.yexcr.2020.112421. PubMed DOI
Liu N., Wu Y.G., Lan G.C., Sui H.S., Ge L., Wang J.Z., Liu Y., Qiao T.W., Tan J.H. Pyruvate prevents aging of mouse oocytes. Reproduction. 2009;138:223–234. doi: 10.1530/REP-09-0122. PubMed DOI
Trapphoff T., Heiligentag M., Dankert D., Demond H., Deutsch D., Frohlich T., Arnold G.J., Grummer R., Horsthemke B., Eichenlaub-Ritter U. Postovulatory aging affects dynamics of mRNA, expression and localization of maternal effect proteins, spindle integrity and pericentromeric proteins in mouse oocytes. Hum. Reprod. 2016;31:133–149. doi: 10.1093/humrep/dev279. PubMed DOI PMC
Samarin A.M., Samarin A.M., Ostbye T.K., Ruyter B., Sampels S., Burkina V., Blecha M., Gela D., Policar T. Alteration of mRNA abundance, oxidation products and antioxidant enzyme activities during oocyte ageing in common carp Cyprinus carpio. PLoS ONE. 2019;14:e0212694. doi: 10.1371/journal.pone.0212694. PubMed DOI PMC
Shang W.-H., Hori T., Westhorpe F.G., Godek K.M., Toyoda A., Misu S., Monma N., Ikeo K., Carroll C.W., Takami Y., et al. Acetylation of histone H4 lysine 5 and 12 is required for CENP-A deposition into centromeres. Nat. Commun. 2016;7:13465. doi: 10.1038/ncomms13465. PubMed DOI PMC
Régnier V., Vagnarelli P., Fukagawa T., Zerjal T., Burns E., Trouche D., Earnshaw W., Brown W. CENP-A Is Required for Accurate Chromosome Segregation and Sustained Kinetochore Association of BubR1. Mol. Cell. Biol. 2005;25:3967–3981. doi: 10.1128/MCB.25.10.3967-3981.2005. PubMed DOI PMC
Ruan K., Yamamoto T.G., Asakawa H., Chikashige Y., Kimura H., Masukata H., Haraguchi T., Hiraoka Y. Histone H4 acetylation required for chromatin decompaction during DNA replication. Sci. Rep. 2015;5:12720. doi: 10.1038/srep12720. PubMed DOI PMC
Demond H., Dankert D., Grümmer R., Horsthemke B. Preovulatory oocyte aging in mice affects fertilization rate and embryonic genome activation. bioRxiv. 2017 doi: 10.1101/209437. DOI
Schulz K.N., Harrison M.M. Mechanisms regulating zygotic genome activation. Nat. Rev. Genet. 2019;20:221–234. doi: 10.1038/s41576-018-0087-x. PubMed DOI PMC
Sato Y., Hilbert L., Oda H., Wan Y., Heddleston J.M., Chew T.L., Zaburdaev V., Keller P., Lionnet T., Vastenhouw N., et al. Histone H3K27 acetylation precedes active transcription during zebrafish zygotic genome activation as revealed by live-cell analysis. Development. 2019;146 doi: 10.1242/dev.179127. PubMed DOI PMC
Li X.Y., Harrison M.M., Villalta J.E., Kaplan T., Eisen M.B. Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition. eLife. 2014;3:e03737. doi: 10.7554/eLife.03737. PubMed DOI PMC
Jiang G.J., Wang K., Miao D.Q., Guo L., Hou Y., Schatten H., Sun Q.Y. Protein profile changes during porcine oocyte aging and effects of caffeine on protein expression patterns. PLoS ONE. 2011;6:e28996. doi: 10.1371/journal.pone.0028996. PubMed DOI PMC
Zhang T., Zhou Y., Li L., Wang H.H., Ma X.S., Qian W.P., Shen W., Schatten H., Sun Q.Y. SIRT1, 2, 3 protect mouse oocytes from postovulatory aging. Aging. 2016;8:685–696. doi: 10.18632/aging.100911. PubMed DOI PMC
Hamatani T., Falco G., Carter M.G., Akutsu H., Stagg C.A., Sharov A.A., Dudekula D.B., VanBuren V., Ko M.S. Age-associated alteration of gene expression patterns in mouse oocytes. Hum. Mol. Genet. 2004;13:2263–2278. doi: 10.1093/hmg/ddh241. PubMed DOI
Samarin A.M., Gela D., Bytyutskyy D., Policar T. Determination of the best post-ovulatory stripping time for the common carp (Cyprinus carpio Linnaeus, 1758) J. Appl. Ichthyol. 2015;31:51–55. doi: 10.1111/jai.12855. DOI
Horváth L., Tamás G., Coche A. Common Carp: Mass Production of Eggs and Early Fry. Food and Agriculture Organization of the United Nations; Rome, Italy: 1985. p. 44.
Wu N., Yue H.M., Chen B., Gui J.F. Histone H2A has a novel variant in fish oocytes. Biol Reprod. 2009;81:275–283. doi: 10.1095/biolreprod.108.074955. PubMed DOI
Shechter D., Dormann H.L., Allis C.D., Hake S.B. Extraction, purification and analysis of histones. Nat. Protoc. 2007;2:1445–1457. doi: 10.1038/nprot.2007.202. PubMed DOI
Green G.R., Do D.P. Purification and analysis of variant and modified histones using 2D PAGE. Methods Mol. Biol. 2009;464:285–302. doi: 10.1007/978-1-60327-461-6_16. PubMed DOI