1,164
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Genome-wide methylation profile of mitochondrial DNA across bovine preimplantation development

, , & ORCID Icon
Article: 2241010 | Received 25 Apr 2023, Accepted 11 Jul 2023, Published online: 31 Jul 2023

References

  • Jansen RP. Origin and persistence of the mitochondrial genome. Hum Reprod. 2000;15(Suppl 2):1–13. doi: 10.1093/humrep/15.suppl_2.1
  • Chakrabarty RP, Chandel NS. Beyond ATP, new roles of mitochondria. The Biochemist. 2022;44(4):2–8. doi: 10.1042/bio_2022_119
  • Boore JL. Animal mitochondrial genomes. Nucleic acids res. 1999;27(8):1767–1780. doi: 10.1093/nar/27.8.1767
  • Rorbach J, Minczuk M. The post-transcriptional life of mammalian mitochondrial RNA. Biochem J. 2012;444(3):357–373. doi: 10.1042/BJ20112208
  • Minocherhomji S, Tollefsbol TO, Singh KK. Mitochondrial regulation of epigenetics and its role in human diseases. Epigenetics. 2012;7(4):326–334. doi: 10.4161/epi.19547
  • Chiaratti MR, Garcia BM, Carvalho KF, et al. Oocyte mitochondria: role on fertility and disease transmission. Anim Reprod. 2018;15(3):231–238. doi: 10.21451/1984-3143-AR2018-0069
  • Nishimura Y, Yoshinari T, Naruse K, et al. Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc Nat Acad Sci. 2006;103(5):1382–1387. doi: 10.1073/pnas.0506911103
  • Babayev E, Seli E. Oocyte mitochondrial function and reproduction. Curr Opin Obstet Gynecol. 2015;27(3):175–181. doi: 10.1097/GCO.0000000000000164
  • May-Panloup P, Boguenet M, El Hachem H, et al. Embryo and its mitochondria. Antioxidants. 2021;10(2):139. doi: 10.3390/antiox10020139
  • WARZYCH E, LIPINSKA P. Energy metabolism of follicular environment during oocyte growth and maturation. J Reprod Dev. 2020;66(1):1–7. doi: 10.1262/jrd.2019-102
  • Chaput C, Sirard MA. Embryonic response to high beta-hydroxybutyrate (BHB) levels in postpartum dairy cows. Domest Anim Endocrinol. 2020;72:106431. doi: 10.1016/j.domaniend.2019.106431
  • Cagnone G, Sirard M-A. The embryonic stress response to in vitro culture: insight from genomic analysis. Reproduction. 2016;152(6):R247–R261. doi: 10.1530/REP-16-0391
  • de Lima CB, dos Santos ÉC, Ispada J, et al. The dynamics between in vitro culture and metabolism: embryonic adaptation to environmental changes. Sci Rep. 2020;10(1): Article 1. doi: 10.1038/s41598-020-72221-1
  • Hufnagel A, Grant ID, Aiken CEM. Glucose and oxygen in the early intrauterine environment and their role in developmental abnormalities. Seminars In Cell & Developmental Biology. 2022;131:25–34. doi: 10.1016/j.semcdb.2022.03.041
  • el Hajj N, Haaf T. Epigenetic disturbances in in vitro cultured gametes and embryos: implications for human assisted reproduction. Fertil Sterility. 2013;99(3):632–641. doi: 10.1016/j.fertnstert.2012.12.044
  • FC Lopes A. Mitochondrial metabolism and DNA methylation: a review of the interaction between two genomes. Clin Epigenetics. 2020;12(1):182. doi: 10.1186/s13148-020-00976-5
  • Milazzotto MP, Lima CBD, Fonseca Junior AMD, et al. Erasing gametes to write blastocysts: metabolism as the new player in epigenetic reprogramming. Anim Reprod. 2020;17(3):e20200015. doi: 10.1590/1984-3143-ar2020-0015
  • Ross PJ, Canovas S. Mechanisms of epigenetic remodelling during preimplantation development. Reprod Fertil Dev. 2016;28(1–2):25–40. doi: 10.1071/RD15365
  • Milazzotto MP, Lima CBD, Ispada J, et al. Metabolism-epigenetic interactions on in vitro produced embryos. Reprod Fertil Dev. 2022;35(2):84–97. doi: 10.1071/RD22203
  • Stoccoro A, Coppedè F. Mitochondrial DNA methylation and human diseases. Int J Mol Sci. 2021;22(9):4594. Article 9. doi: 10.3390/ijms22094594
  • Sirard M-A. Distribution and dynamics of mitochondrial DNA methylation in oocytes, embryos and granulosa cells. Sci Rep. 2019;9(1):1–10. doi: 10.1038/s41598-019-48422-8
  • de Lima CB, Sirard M-A. Mitoepigenetics: methylation of mitochondrial DNA is strand-biased in bovine oocytes and embryos. Reproduct Domestic Animals. 2020;55(10):1455–1458. doi: 10.1111/rda.13786
  • Parrish JJ, Susko-Parrish J, Winer MA, et al. Capacitation of bovine sperm by heparin. Biol Reprod. 1988;38(5):1171–1180. doi: 10.1095/biolreprod38.5.1171
  • Santos ÉCD, Fonseca Junior AMD, Lima CBD, et al. Less is more: reduced nutrient concentration during in vitro culture improves embryo production rates and morphophysiology of bovine embryos. Theriogenology. 2021;173:37–47. doi: 10.1016/j.theriogenology.2021.07.010
  • Podlesniy P, Trullas R. Absolute measurement of gene transcripts with Selfie-digital PCR. 2017;Sci Rep. 7(1): Article 1. doi: 10.1038/s41598-017-08270-w
  • Cao K, Lv W, Wang X, et al. Hypermethylation of hepatic mitochondrial ND6 provokes systemic insulin resistance. Adv Sci. 2021;8(11):2004507. Weinheim, Baden-Wurttemberg, Germany. doi: 10.1002/advs.202004507
  • Mishra M, Kowluru RA. Epigenetic modification of mitochondrial DNA in the development of diabetic retinopathy. Invest Ophthalmol Visual Sci. 2015;56(9):5133–5142. doi: 10.1167/iovs.15-16937
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England). 2014;30(15):2114–2120. doi: 10.1093/bioinformatics/btu170
  • Krueger F, Andrews SR. Bismark: A flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics (Oxford, England). 2011;27(11):1571–1572. doi: 10.1093/bioinformatics/btr167
  • Akalin A, Kormaksson M, Li S, et al. methylKit: A comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome bio. 2012;13(10):R87. doi: 10.1186/gb-2012-13-10-r87
  • R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2022. https://www.R-project.org/
  • Patil V, Cuenin C, Chung F, et al. Human mitochondrial DNA is extensively methylated in a non-CpG context. Nucleic Acids Res. 2019;47(19):10072–10085. doi: 10.1093/nar/gkz762
  • Goldsmith C, Rodríguez-Aguilera JR, El-Rifai I, et al. Low biological fluctuation of mitochondrial CpG and non-CpG methylation at the single-molecule level. Sci Rep. 2021;11(1): Article 1. 10.1038/s41598-021-87457-8
  • Liu B, Du Q, Chen L, et al. CpG methylation patterns of human mitochondrial DNA. Sci Rep. 2016;6(1): Article 1. 10.1038/srep23421
  • Zeng Y, Chen T. DNA methylation reprogramming during mammalian development. Genes (Basel). 2019;10(4):257. doi: 10.3390/genes10040257
  • Nagaraj R, Sharpley MS, Chi F, et al. Nuclear Localization of Mitochondrial TCA Cycle Enzymes as a Critical Step in Mammalian Zygotic Genome Activation. Cell. 2017;168(1–2):210–223.e11. doi: 10.1016/j.cell.2016.12.026
  • Hamatani T, MSh K, Yamada M et al, Global gene expression profiling of preimplantation embryos. Hum Cell. 2006;19:98–117. doi: 10.1111/j.1749-0774.2006.00018.x
  • Jeanblanc M, Salvaing J, Mason K. et al. Embryonic genome activation. Gynecologie, Obstetrique et Fertilite. 2008;36:1126–1132. doi: 10.1016/j.gyobfe.2008.07.015
  • Gardner DK, Harvey AJ. Blastocyst metabolism. Reprod Fertil Dev. 2015;27(4):638–654. doi: 10.1071/RD14421
  • Lane M, Gardner DK. Mitochondrial Malate-Aspartate Shuttle Regulates Mouse Embryo Nutrient Consumption. J Biol Chem. 2005;280(18):18361–18367. doi: 10.1074/jbc.M500174200
  • Facucho-Oliveira JM, St John JC. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev. 2009;5(2):140–158. doi: 10.1007/s12015-009-9058-0
  • St John JC, Facucho-Oliveira J, Jiang Y, et al. Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Human Reproduction Update. 2010;16(5):488–509. doi: 10.1093/humupd/dmq002
  • Ebert KM, Liem H, Hecht NB. Mitochondrial DNA in the mouse preimplantation embryo. J Reprod Fertil. 1988;82(1):145–149. doi: 10.1530/jrf.0.0820145
  • El Shourbagy SH, Spikings EC, Freitas M, et al. Mitochondria directly influence fertilisation outcome in the pig. Reproduction. 2006;131(2):233–245. doi: 10.1530/rep.1.00551
  • Kameyama Y, Filion F, Yoo JG, et al. Characterization of mitochondrial replication and transcription control during rat early development in vivo and in vitro. Reproduction. 2007;133(2):423–432. doi: 10.1530/REP-06-0263
  • Filograna R, Mennuni M, Alsina D, et al. Mitochondrial DNA copy number in human disease: the more the better? FEBS Lett. 2021;595(8):976–1002. doi: 10.1002/1873-3468.14021
  • Kowal K, Tkaczyk A, Ząbek T, et al. Comparative analysis of CpG sites and islands distributed in mitochondrial DNA of model organisms. Animals (Basel). 2020;10(4):665. doi: 10.3390/ani10040665
  • Bogenhagen DF. Mitochondrial DNA nucleoid structure. Biochim Biophys Acta Gene Regul Mech. 2012;1819(9–10):914–920. doi: 10.1016/j.bbagrm.2011.11.005
  • D’Souza AR, Minczuk M, Garone C, et al. Mitochondrial transcription and translation: overview. Essays Biochem. 2018;62(3):309–320. doi: 10.1042/EBC20170102
  • Taanman J-W. The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta Bioenerg. 1999;1410(2):103–123. doi: 10.1016/S0005-2728(98)00161-3
  • Shayevitch R, Askayo D, Keydar I, et al. The importance of DNA methylation of exons on alternative splicing. RNA. 2018;24(10):1351–1362. doi: 10.1261/rna.064865.117
  • Armstrong DA, Green BB, Blair BA, et al. Maternal smoking during pregnancy is associated with mitochondrial DNA methylation. Environ Epigenet. 2016;2(3):dvw020. doi: 10.1093/eep/dvw020
  • Jia L, Li J, He B, et al. Abnormally activated one-carbon metabolic pathway is associated with mtDNA hypermethylation and mitochondrial malfunction in the oocytes of polycystic gilt ovaries. Sci Rep. 2016;6(1):1–11. doi: 10.1038/srep19436
  • Novielli C, Mandò C, Tabano S, et al. Mitochondrial DNA content and methylation in fetal cord blood of pregnancies with placental insufficiency. Placenta. 2017;55:63–70. doi: 10.1016/j.placenta.2017.05.008
  • Yue Y, Ren L, Zhang C, et al. Mitochondrial genome undergoes de novo DNA methylation that protects mtDNA against oxidative damage during the peri-implantation window. Proc Natl Acad Sci USA. 2022;119(30):e2201168119. doi: 10.1073/pnas.2201168119