Histone Acetylation Dynamics during In Vivo and In Vitro Oocyte Aging in Common Carp Cyprinus carpio

. 2021 Jun 03 ; 22 (11) : . [epub] 20210603

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34204879

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

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.

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace