The central role of pyruvate metabolism on the epigenetic maturation and transcriptional profile of bovine oocytes

in Reproduction
Authors:
João Vitor Alcantara da Silva Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

Search for other papers by João Vitor Alcantara da Silva in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0002-3030-6356
,
Jessica Ispada Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

Search for other papers by Jessica Ispada in
Current site
Google Scholar
PubMed
Close
,
Ricardo Perecin Nociti Department of Veterinary Medicine, Faculty of Animal Sciences and Food Engineering, University of São Paulo, Pirassununga, SP, Brazil

Search for other papers by Ricardo Perecin Nociti in
Current site
Google Scholar
PubMed
Close
,
Aldcejam Martins da Fonseca Junior Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

Search for other papers by Aldcejam Martins da Fonseca Junior in
Current site
Google Scholar
PubMed
Close
,
Camila Bruna de Lima Département des Sciences Animales, Laval University, Canada

Search for other papers by Camila Bruna de Lima in
Current site
Google Scholar
PubMed
Close
,
Erika Cristina dos Santos Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

Search for other papers by Erika Cristina dos Santos in
Current site
Google Scholar
PubMed
Close
,
Marcos Roberto Chiaratti Department of Genetics and Evolution, Federal University of Sao Carlos, Sao Carlos, SP, Brazil

Search for other papers by Marcos Roberto Chiaratti in
Current site
Google Scholar
PubMed
Close
, and
Marcella Pecora Milazzotto Laboratory of Embryonic Metabolism and Epigenetics, Center of Natural and Human Sciences, Federal University of ABC, Santo Andre, SP, Brazil

Search for other papers by Marcella Pecora Milazzotto in
Current site
Google Scholar
PubMed
Close
https://orcid.org/0000-0003-0933-3066

Correspondence should be addressed to M P Milazzotto; Email: marcella.milazzotto@ufabc.edu.br
Restricted access
Rent on DeepDyve

Sign up for journal news

In brief

Pyruvate metabolism is one of the main metabolic pathways during oocyte maturation. This study demonstrates that pyruvate metabolism also regulates the epigenetic and molecular maturation in bovine oocytes.

Abstract

Pyruvate, the final product of glycolysis, undergoes conversion into acetyl-CoA within the mitochondria of oocytes, serving as a primary fuel source for the tricarboxylic acid (TCA) cycle. The citrate generated in the TCA cycle can be transported to the cytoplasm and converted back into acetyl-CoA. This acetyl-CoA can either fuel lipid synthesis or act as a substrate for histone acetylation. This study aimed to investigate how pyruvate metabolism influences lysine 9 histone 3 acetylation (H3K9ac) dynamics and RNA transcription in bovine oocytes during in vitro maturation (IVM). Bovine cumulus–oocyte complexes were cultured in vitro for 24 h, considering three experimental groups: Control (IVM medium only), DCA (IVM supplemented with sodium dichloroacetate, a stimulant of pyruvate oxidation into acetyl-CoA), or IA (IVM supplemented with sodium iodoacetate, a glycolysis inhibitor). The results revealed significant alterations in oocyte metabolism in both treatments, promoting the utilization of lipids as an energy source. These changes during IVM affected the dynamics of H3K9ac, subsequently influencing the oocyte's transcriptional activity. In the DCA and IA groups, a total of 148 and 356 differentially expressed genes were identified, respectively, compared to the control group. These findings suggest that modifications in pyruvate metabolism trigger the activation of metabolic pathways, particularly lipid metabolism, changing acetyl-CoA availability and H3K9ac levels, ultimately impacting the mRNA content of in vitro matured bovine oocytes.

 

  • Collapse
  • Expand
  • Agarwal A, Gupta S & & Sharma RK 2005 Role of oxidative stress in female reproduction. Reproductive Biology and Endocrinology 3 28. (https://doi.org/10.1186/1477-7827-3-28)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Akiyama T, Nagata M & & Aoki F 2006 Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. PNAS 103 73397344. (https://doi.org/10.1073/pnas.0510946103)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Almansa-Ordonez A, Bellido R, Vassena R, Barragan M & & Zambelli F 2020 Oxidative stress in reproduction: a mitochondrial perspective. Biology 9 269. (https://doi.org/10.3390/biology9090269)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Biagi CAO, Cury SS, Alves CP, Rabhi N, Silva WA, Farmer SR, Carvalho RF & & Batista ML 2021 Multidimensional single-nuclei RNA-seq reconstruction of adipose tissue reveals adipocyte plasticity underlying thermogenic response. Cells 10 3073. (https://doi.org/10.3390/cells10113073)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Cheng F, Lienlaf M, Perez-Villarroel P, Wang HW, Lee C, Woan K, Woods D, Knox T, Bergman J, Pinilla-Ibarz J, et al.2014 Divergent roles of histone deacetylase 6 (HDAC6) and histone deacetylase 11 (HDAC11) on the transcriptional regulation of IL10 in antigen presenting cells. Molecular Immunology 60 4453. (https://doi.org/10.1016/j.molimm.2014.02.019)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dalbiès-Tran R & & Mermillod P 2003 Use of heterologous complementary DNA array screening to analyze bovine oocyte transcriptome and its evolution during in vitro maturation. Biology of Reproduction 68 252261. (https://doi.org/10.1095/biolreprod.102.007872)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • De Andrade F & & Poehland R 2021 Lipid metabolism in bovine oocytes and early embryos under in vivo, in vitro, and stress conditions. International Journal of Molecular Sciences 22 3421. (https://doi.org/10.3390/ijms22073421)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • De Gelder J, De Gussem K, Vandenabeele P & & Moens L 2007 Reference database of Raman spectra of biological molecules. Journal of Raman Spectroscopy 38 11331147. (https://doi.org/10.1002/jrs.1734)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M & & Gingeras TR 2013 STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29 1521. (https://doi.org/10.1093/bioinformatics/bts635)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dode MAN, Dufort I, Massicotte L & & Sirard M-A 2006. Quantitative expression of candidate genes for developmental competence in bovine two-cell embryos. Molecular Reproduction and Development 73 288297. (https://doi.org/10.1002/mrd.20427)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ & & Robker RL 2010 Beta-oxidation is essential for mouse oocyte developmental competence and early embryo Development1. Biology of Reproduction 83 909918. (https://doi.org/10.1095/biolreprod.110.084145)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fair T, Carter F, Park S, Evans ACO & & Lonergan P 2007 Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68 S91S97. (https://doi.org/10.1016/j.theriogenology.2007.04.018)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Friis RM, Wu BP, Reinke SN, Hockman DJ, Sykes BD & & Schultz MC 2009 A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Research 37 39693980. (https://doi.org/10.1093/nar/gkp270)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ge H-S, Li X-H, Zhang F, Chen H, Xi H-T, Huang JY, Zhu C-F & & Lv J-Q 2013 Suppression of mitochondrial oxidative phosphorylation on in vitro maturation, fertilization and developmental competence of oocytes. Beijing Da Xue Xue Bao. Yi Xue Ban = Journal of Peking University. Health Sciences 45 864868.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gujral P, Mahajan V, Lissaman AC & & Ponnampalam AP 2020 Histone acetylation and the role of histone deacetylases in normal cyclic endometrium. Reproductive Biology and Endocrinology 18 84. (https://doi.org/10.1186/s12958-020-00637-5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • He M, Zhang T, Yang Y & & Wang C 2021 Mechanisms of oocyte maturation and related epigenetic regulation. Frontiers in Cell and Developmental Biology 9 654028. (https://doi.org/10.3389/fcell.2021.654028)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Huang WJ, Wang YC, Chao SW, Yang CY, Chen LC, Lin MH, Hou WC, Chen MY, Lee TL, Yang P, et al.2012 Synthesis and biological evaluation of Ortho-aryl N-Hydroxycinnamides as potent histone deacetylase (HDAC) 8 isoform-selective inhibitors. ChemMedChem 7 18151824. (https://doi.org/10.1002/cmdc.201200300)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Karaz S, Courgeon M, Lepetit H, Bruno E, Pannone R, Tarallo A, Thouzé F, Kerner P, Vervoort M, Causeret F, et al.2016 Neuronal fate specification by the Dbx1 transcription factor is linked to the evolutionary acquisition of a novel functional domain. EvoDevo 7 18. (https://doi.org/10.1186/s13227-016-0055-5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Latham T, Mackay L, Sproul D, Karim M, Culley J, Harrison DJ, Hayward L, Langridge-Smith P, Gilbert N & & Ramsahoye BH 2012 Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression. Nucleic Acids Research 40 47944803. (https://doi.org/10.1093/nar/gks066)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liao Y, Smyth GK & & Shi W 2014 featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30 923930. (https://doi.org/10.1093/bioinformatics/btt656)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Liao Y, Smyth GK & & Shi W 2019 The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Research 47 e47. (https://doi.org/10.1093/nar/gkz114)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lipinska P, Sell-Kubiak E, Pawlak P, Madeja ZE & & Warzych E 2021 Response of bovine cumulus–oocytes complexes to energy pathway inhibition during in vitro maturation. Genes 12 838. (https://doi.org/10.3390/genes12060838)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Love MI, Huber W & & Anders S 2014 Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15 550. (https://doi.org/10.1186/s13059-014-0550-8)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Luciano AM, Lodde V, Franciosi F, Tessaro I, Corbani D & & Modina S 2012 Large-scale chromatin morpho-functional changes during mammalian oocyte growth and differentiation. European Journal of Histochemistry 56 e37e37. (https://doi.org/10.4081/ejh.2012.e37)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Luo W & & Brouwer C 2013 Pathview: an R/bioconductor package for pathway-based data integration and visualization. Bioinformatics 29 18301831. (https://doi.org/10.1093/bioinformatics/btt285)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ma P & & Schultz RM 2013 Histone deacetylase 2 (HDAC2) regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse. PLoS Genetics 9 e1003377. (https://doi.org/10.1371/journal.pgen.1003377)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Matsuhashi T, Hishiki T, Zhou H, Ono T, Kaneda R, Iso T, Yamaguchi A, Endo J, Katsumata Y, Atsushi A, et al.2015 Activation of pyruvate dehydrogenase by dichloroacetate has the potential to induce epigenetic remodeling in the heart. Journal of Molecular and Cellular Cardiology 82 116124. (https://doi.org/10.1016/j.yjmcc.2015.02.021)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • McDonnell E, Crown SB, Fox DB, Kitir B, Ilkayeva OR, Olsen CA, Grimsrud PA & & Hirschey MD 2016 Lipids reprogram metabolism to become a major carbon source for histone acetylation. Cell Reports 17 14631472. (https://doi.org/10.1016/j.celrep.2016.10.012)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • McPherson NO, Zander-Fox D & & Lane M 2014 Stimulation of mitochondrial embryo metabolism by dichloroacetic acid in an aged mouse model improves embryo development and viability. Fertility and Sterility 101 14581466. (https://doi.org/10.1016/j.fertnstert.2013.12.057)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Michelakis ED, Webster L & & Mackey JR 2008 Dichloroacetate (DCA) as a potential metabolic-targeting therapy for cancer. British Journal of Cancer 99 989994. (https://doi.org/10.1038/sj.bjc.6604554)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Michelakis ED, Sutendra G, Dromparis P, Webster L, Haromy A, Niven E, Maguire C, Gammer TL, Mackey JR, Fulton D, et al.2010 Metabolic modulation of glioblastoma with dichloroacetate. Science Translational Medicine 2 31ra3431ra34. (https://doi.org/10.1126/scitranslmed.3000677)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mihalas BP, De Iuliis GN, Redgrove KA, McLaughlin EA & & Nixon B 2017 The lipid peroxidation product 4-hydroxynonenal contributes to oxidative stress-mediated deterioration of the ageing oocyte. Scientific Reports 7 6247. (https://doi.org/10.1038/s41598-017-06372-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Morgan M, Much C, DiGiacomo M, Azzi C, Ivanova I, Vitsios DM, Pistolic J, Collier P, Moreira PN, Benes V, et al.2017 mRNA 3’ uridylation and poly(A) tail length sculpt the mammalian maternal transcriptome. Nature 548 347351. (https://doi.org/10.1038/nature23318)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Moussaieff A, Rouleau M, Kitsberg D, Cohen M, Levy G, Barasch D, Nemirovski A, Shen-Orr S, Laevsky I, Amit M, et al.2015 Glycolysis-mediated changes in acetyl-CoA and histone acetylation control the early differentiation of embryonic stem cells. Cell Metabolism 21 392402. (https://doi.org/10.1016/j.cmet.2015.02.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ng H-H & & Bird A 1999 DNA methylation and chromatin modification. Current Opinion in Genetics and Development 9 158163. (https://doi.org/10.1016/S0959-437X(9980024-0)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • O’Doherty AM, Magee DA, O’Shea LC, Forde N, Beltman ME, Mamo S & & Fair T 2015 DNA methylation dynamics at imprinted genes during bovine pre-implantation embryo development. BMC Developmental Biology 15 13. (https://doi.org/10.1186/s12861-015-0060-2)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ordoñez-Leon EA, Merchant H, Medrano A, Kjelland M & & Romo S 2014 Lipid droplet analysis using in vitro bovine oocytes and embryos. Reproduction in Domestic Animals 49 306314. (https://doi.org/10.1111/rda.12275)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ploplis VA, Carmeliet P, Vazirzadeh S, Van Vlaenderen I, Moons L, Plow EF & & Collen D 1995 Effects of disruption of the plasminogen gene on thrombosis, growth, and health in mice. Circulation 92 25852593. (https://doi.org/10.1161/01.cir.92.9.2585)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pontelo TP, Rodrigues SAD, Kawamoto TS, Leme LO, Gomes ACMM, Zangeronimo MG, Franco MM & & Dode MAN 2020 Histone acetylation during the in vitro maturation of bovine oocytes with different levels of competence. Reproduction, Fertility, and Development 32 690696. (https://doi.org/10.1071/RD19218)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pontelo TP, Franco MM, Kawamoto TS, Caixeta FMC, de Oliveira Leme L, Kussano NR, Zangeronimo MG & & Dode MAN 2021 Histone deacetylase inhibitor during in vitro maturation decreases developmental capacity of bovine oocytes. PLoS One 16 e0247518. (https://doi.org/10.1371/journal.pone.0247518)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K & & Tesfaye D 2011 Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genomics 12 57. (https://doi.org/10.1186/1471-2164-12-57)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reverter A & & Chan EKF 2008 Combining partial correlation and an information theory approach to the reversed engineering of gene co-expression networks. Bioinformatics 24 24912497. (https://doi.org/10.1093/bioinformatics/btn482)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reverter A, Hudson NJ, Nagaraj SH, Pérez-Enciso M & & Dalrymple BP 2010 Regulatory impact factors: unraveling the transcriptional regulation of complex traits from expression data. Bioinformatics 26 896904. (https://doi.org/10.1093/bioinformatics/btq051)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reyes JM, Chitwood JL & & Ross PJ 2015 RNA-seq profiling of single bovine oocyte transcript abundance and its modulation by cytoplasmic polyadenylation. Molecular Reproduction and Development 82 103114. (https://doi.org/10.1002/mrd.22445)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Robinson MD, McCarthy DJ & & Smyth GK 2010 edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 139140. (https://doi.org/10.1093/bioinformatics/btp616)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rosca MG, Vazquez EJ, Chen Q, Kerner J, Kern TS & & Hoppel CL 2012 Oxidation of fatty acids is the source of increased mitochondrial reactive oxygen species production in kidney cortical tubules in early diabetes. Diabetes 61 20742083. (https://doi.org/10.2337/db11-1437)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Santos ÉC dos, Martinho HS, Annes K, da Silva T, Soares CA, Leite RF & & Milazzotto MP 2016. Raman-based noninvasive metabolic profile evaluation of in vitro bovine embryos. Journal of Biomedical Optics 21 075002. (https://doi.org/10.1117/1.JBO.21.7.075002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Saraiva NZ, Oliveira CS, Almeida NNC, Figueiró MR, Quintão CCR & & Garcia JM 2022 Epigenetic modifiers during in vitro maturation as a strategy to increase oocyte competence in bovine. Theriogenology 187 95101. (https://doi.org/10.1016/j.theriogenology.2022.04.014)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sarwar Z, Saad M, Saleem M, Husnain A, Riaz A & & Ahmad N 2020 Effect of follicle size on oocytes recovery rate, quality, and in-vitro developmental competence in Bos indicus Cows. Animal Reproduction 17 e20200011. (https://doi.org/10.1590/1984-3143-AR2020-0011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sharma S, Poetz F, Bruer M, Ly-Hartig TBN, Schott J, Séraphin B & & Stoecklin G 2016 Acetylation-dependent control of global poly(A) RNA degradation by CBP/P300 and HDAC1/2. Molecular Cell 63 927938. (https://doi.org/10.1016/j.molcel.2016.08.030)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Song JL & & Wessel GM 2005 How to make an egg: transcriptional regulation in oocytes. Differentiation; Research in Biological Diversity 73 117. (https://doi.org/10.1111/j.1432-0436.2005.07301005.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Su YQ, You-Qiang KS & & Eppig JJ 2009 Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Seminars in Reproductive Medicine 27 3242. (https://doi.org/10.1055/s-0028-1108008)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sugimura S, Matoba S, Hashiyada Y, Aikawa Y, Ohtake M, Matsuda H, Kobayashi S, Konishi K & & Imai K 2012 Oxidative phosphorylation-linked respiration in individual bovine oocytes. Journal of Reproduction and Development 58 636641. (https://doi.org/10.1262/jrd.2012-082)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sutton ML, Gilchrist RB & & Thompson JG 2003 Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Human Reproduction Update 9 3548. (https://doi.org/10.1093/humupd/dmg009)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB & & Thompson JG 2012 Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of follicle-stimulating hormone and bone morphogenetic Protein 151. Biology of Reproduction 87 87. (https://doi.org/10.1095/biolreprod.112.102061)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tan M, van Tol HTA, Mokry M, Stout TAE & & Roelen BAJ 2020 Microinjection induces changes in the transcriptome of bovine oocytes. Scientific Reports 10 11211. (https://doi.org/10.1038/s41598-020-67603-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Turathum B, Gao E-M & & Chian R-C 2021 The function of cumulus cells in oocyte growth and maturation and in subsequent ovulation and fertilization. Cells 10 2292. (https://doi.org/10.3390/cells10092292)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Turner BM 2002 Cellular memory and the histone code. Cell 111 285291. (https://doi.org/10.1016/S0092-8674(0201080-2)

  • Wassarman PM, Liu C & & Litscher ES 1996 Constructing the mammalian egg zona Pellucida: some new pieces of an old puzzle. Journal of Cell Science 109 20012004. (https://doi.org/10.1242/jcs.109.8.2001)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR & & Thompson CB 2009 ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324 10761080. (https://doi.org/10.1126/science.1164097)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wen J, Wang GL, Yuan H-J, Zhang J, Xie H-L, Gong S, Han X & & Tan JH 2020 Effects of glucose metabolism pathways on nuclear and cytoplasmic maturation of pig oocytes. Scientific Reports 10 2782. (https://doi.org/10.1038/s41598-020-59709-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wu X, Hu S, Wang L, Li Y & & Yu H 2020 Dynamic changes of histone acetylation and methylation in bovine oocytes, zygotes, and preimplantation embryos. Journal of Experimental Zoology 334 245256. (https://doi.org/10.1002/jez.b.22943)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Xie HL, Hong-Li Y-BW, Jiao GZ, Kong DL, Li Q, Li H, Zheng LL & & Tan JH 2016 Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes. Scientific Reports 6 20764. (https://doi.org/10.1038/srep20764)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yanes O, Clark J, Wong DM, Patti GJ, Sanchez-Ruiz A, Benton HP, Trauger SA, Desponts C, Ding S & & Siuzdak G 2010 Metabolic oxidation regulates embryonic stem cell differentiation. Nature Chemical Biology 6 411417. (https://doi.org/10.1038/nchembio.364)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yu G, Wang L-G, Han Y & & He QY 2012 clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16 284287. (https://doi.org/10.1089/omi.2011.0118)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yucel N, Wang YX, Mai T, Porpiglia E, Lund PJ, Markov G, Garcia BA, Bendall SC, Angelo M & & Blau HM 2019 Glucose metabolism drives histone acetylation landscape transitions that dictate muscle stem cell function. Cell Reports 27 39393955.e6. (https://doi.org/10.1016/j.celrep.2019.05.092)

    • PubMed
    • Search Google Scholar
    • Export Citation