Differentially methylated regions identified in bovine embryos are not observed in adulthood
Luna Nascimento Vargas; Allice Rodrigues Ferreira Nochi; Paloma Soares de Castro; Andrielle Thainar Mendes Cunha; Thainara Christie Ferreira Silva; Roberto Coiti Togawa; Márcia Marques Silveira; Alexandre Rodrigues Caetano; Maurício Machaim Franco
Abstract
Keywords
References
Almeida DL, Pavanello A, Saavedra LP, Pereira TS, Castro-Prado MAA, Mathias PCF. Environmental monitoring and the developmental origins of health and disease. J Dev Orig Health Dis. 2019;10(6):608-15.
Canovas S, Ross PJ, Kelsey G, Coy P. DNA Methylation in Embryo Development: Epigenetic Impact of ART (Assisted Reproductive Technologies). BioEssays. 2017;39(11):1700106.
Capra E, Lazzari B, Turri F, Cremonesi P, Portela AMR, Ajmone-Marsan P, Stella A, Pizzi F. Epigenetic analysis of high and low motile sperm populations reveals methylation variation in satellite regions within the pericentromeric position and in genes functionally related to sperm DNA organization and maintenance in Bos taurus. BMC Genomics. 2019;20(1):940.
Carlin G, Chaumontet C, Blachier F, Barbillon P, Darcel N, Blais A, Delteil C, Guillin FM, Blat S, van der Beek EM, Kodde A, Tome D, Davila AM. Maternal high-protein diet during pregnancy modifies rat offspring body weight and insulin signalling but not macronutrient preference in adulthood. Nutrients. 2019;11(1):96.
Carvalho JO, Michalczechen‐Lacerda VA, Sartori R, Rodrigues FC, Bravim O, Franco MM, Dode MA. The methylation patterns of the IGF2 and IGF2R genes in bovine spermatozoa are not affected by flow‐cytometric sex sorting. Mol Reprod Dev. 2012;79(2):77-84.
Cropley JE, Suter CM, Beckman KB, Martin DIK. Germ-line epigenetic modification of the murine Avy allele by nutritional supplementation. Proc Natl Acad Sci USA. 2006;103(46):17308-12.
Daniels TE, Sadovnikoff AI, Ridout KK, Lesseur C, Marsit CJ, Tyrka AR. Associations of maternal diet and placenta leptin methylation. Mol Cell Endocrinol. 2020;505:110739.
Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. The H19 methylation imprint is erased and re‐established differentially on the parental alleles during male germ cell development. Hum Mol Genet. 2000;9(19):2885-94.
Dean W, Santos F, Stojkovic M, Zakhartchenko V, Walter J, Wolf J, Reik W. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA. 2001;98(24):13734-8.
Devos J, Behrouzi A, Paradis F, Straathof C, Li C, Colazo M, Block H, Fitzsimmons C. Genetic potential for residual feed intake and diet fed during early- to mid-gestation influences post-natal DNA methylation of imprinted genes in muscle and liver tissues in beef cattle. J Anim Sci. 2021;99(5):skab140.
Duan JE, Jiang ZC, Alqahtani F, Mandoiu I, Dong H, Zheng X, Marjani SL, Chen J, Tian XC. Methylome dynamics of bovine gametes and in vivo early embryos. Front Genet. 2019;10:512.
Estrada-Cortes E, Ortiz W, Rabaglino MB, Block J, Rae O, Jannaman EA, Xiao Y, Hansen PJ. Choline acts during preimplantation development of the bovine embryo to program postnatal growth and alter muscle DNA methylation. FASEB J. 2021;35(10):e21926.
Fagundes NS, Michalczechen-Lacerda VA, Caixeta ES, Machado GM, Rodrigues FC, Melo EO, Dode MA, Franco MM. Methylation status in the intragenic differentially methylated region of the IGF2 locus in Bos taurus indicus oocytes with different developmental competencies. Mol Hum Reprod. 2011;17(2):85-91.
Finer S, Iqbal MS, Lowe R, Ogunkolade BW, Pervin S, Mathews C, Smart M, Alam DS, Hitman GA. Is famine exposure during developmental life in rural Bangladesh associated with a metabolic and epigenetic signature in young adulthood? A historical cohort study. BMJ Open. 2016;6(11):e011768.
Garrido N, Cruz F, Egea RR, Simon C, Sadler-Riggleman I, Beck D, Nilsson E, Ben Maamar M, Skinner MK. Sperm DNA methylation epimutation biomarker for paternal offspring autism susceptibility. Clin Epigenetics. 2021;13(1):6.
Ge ZJ, Luo SM, Lin F, Liang QX, Huang L, Wei YC, Hou Y, Han ZM, Schatten H, Sun QY. DNA methylation in oocytes and liver of female mice and their offspring: effects of high-fat-diet-induced obesity. Environ Health Perspect. 2014;122(2):159-64.
Greenberg MVC, Bourc’his D. The diverse roles of DNA methylation in mammalian development and disease. Nat Rev Mol Cell Biol. 2019;20(10):590-607.
Guo H, Zhu P, Yan L, Li R, Hu B, Lian Y, Yan J, Ren X, Lin S, Li J, Jin X, Shi X, Liu P, Wang X, Wang W, Wei Y, Li X, Guo F, Wu X, Fan X, Yong J, Wen L, Xie SX, Tang F, Qiao J. The DNA methylation landscape of human early embryos. Nature. 2014;511(7511):606-10.
Guo Y, Wang Z, Chen L, Tang L, Wen S, Liu Y, Yuan J. Diet induced maternal obesity affects offspring gut microbiota and persists into young adulthood. Food Funct. 2018;9(8):4317-27.
Ivanova E, Canovas S, Garcia-Martinez S, Romar R, Lopes JS, Rizos D, Sanchez-Calabuig MJ, Krueger F, Andrews S, Perez-Sanz F, Kelsey G, Coy P. DNA methylation changes during preimplantation development reveal inter-species differences and reprogramming events at imprinted genes. Clin Epigenetics. 2020;12(1):64.
Kafri T, Ariel M, Brandeis M, Shemer R, Urven L, McCarrey J, Cedar H, Razin A. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 1992;6(5):705-14.
Kang Y-K, Koo D-B, Park J-S, Choi Y-H, Chung A-S, Lee K-K, Han Y-M. Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet. 2001;28(2):173-7.
Knight AK, Park HJ, Hausman DB, Fleming JM, Bland VL, Rosa G, Kennedy EM, Caudill MA, Malysheva O, Kauwell GPA, Sokolow A, Fisher S, Smith AK, Bailey LB. Association between one-carbon metabolism indices and DNA methylation status in maternal and cord blood. Sci Rep. 2018;8(1):16873.
Kropp J, Carrillo JA, Namous H, Daniels A, Salih SM, Song J, Khatib H. Male fertility status is associated with DNA methylation signatures in sperm and transcriptomic profiles of bovine preimplantation embryos. BMC Genomics. 2017;18(1):280.
Kumaki Y, Oda M, Okano M. QUMA: quantification tool for methylation analysis. Nucleic Acids Res. 2008;36(Suppl 2):W170-5.
Kupers LK, Fernandez-Barres S, Nounu A, Friedman C, Fore R, Mancano G, Dabelea D, Rifas-Shiman SL, Mulder RH, Oken E, Johnson L, Bustamante M, Jaddoe VWV, Hivert MF, Starling AP, de Vries JHM, Sharp GC, Vrijheid M, Felix JF. Maternal Mediterranean diet in pregnancy and newborn DNA methylation: a meta-analysis in the PACE Consortium. Epigenetics. 2022;17(11):1419-31.
Lapehn S, Paquette AG. The placental epigenome as a molecular link between prenatal exposures and fetal health outcomes through the DOHaD hypothesis. Curr Environ Health Rep. 2022;9:490-501.
Lee J, Inoue K, Ono R, Ogonuki N, Kohda T, Kaneko-Ishino T, Ogura A, Ishino F. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development. 2002;129(8):1807-17.
Li L-C, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics. 2002;18(11):1427-31. vailable
Liu L, Amorin R, Moriel P, DiLorenzo N, Lancaster PA, Penagaricano F. Maternal methionine supplementation during gestation alters alternative splicing and DNA methylation in bovine skeletal muscle. BMC Genomics. 2021;22(1):780.
Lujan S, Caroppo E, Niederberger C, Arce JC, Sadler-Riggleman I, Beck D, Nilsson E, Skinner MK. Sperm DNA Methylation Epimutation Biomarkers for Male Infertility and FSH Therapeutic Responsiveness. Sci Rep. 2019;9(1):16786.
MacDonald WA, Mann MR. Epigenetic regulation of genomic imprinting from germ line to preimplantation. Mol Reprod Dev. 2014;81(2):126-40.
Mahajan A, Sapehia D, Thakur S, Mohanraj PS, Bagga R, Kaur J. Effect of imbalance in folate and vitamin B12 in maternal/parental diet on global methylation and regulatory miRNAs. Sci Rep. 2019;9(1):17602.
Mao J, Pennington KA, Talton OO, Schulz LC, Sutovsky M, Lin Y, Sutovsky P. In utero and postnatal exposure to high fat, high sucrose diet suppressed testis apoptosis and reduced sperm count. Sci Rep. 2018;8(1):7622.
Martinez D, Pentinat T, Ribo S, Daviaud C, Bloks VW, Cebria J, Villalmanzo N, Kalko SG, Ramon-Krauel M, Diaz R, Plosch T, Tost J, Jimenez-Chillaron JC. In utero undernutrition in male mice programs liver lipid metabolism in the second-generation offspring involving altered Lxra DNA methylation. Cell Metab. 2014;19(6):941-51.
Moreno-Fernandez J, Ochoa JJ, Lopez-Frias M, Diaz-Castro J. Impact of early nutrition, physical activity and sleep on the fetal programming of disease in the pregnancy: a narrative review. Nutrients. 2020;12(12):3900.
Nasri F, Gharesi-Fard B, Namavar Jahromi B, Farazi-Fard MA, Banaei M, Davari M, Ebrahimi S, Anvar Z. Sperm DNA methylation of H19 imprinted gene and male infertility. Andrologia. 2017;49(10):e12766.
Nochi ARF, Vargas LN, Sartori R, Junior RG, Araujo DB, Figueiredo RA, Togawa RC, Costa MMC, Grynberg P, Mendonca AS, Kussano NR, Pivato I, Silva BDM, Spricigo JFW, Leme LO, da Silva JP, Caetano AR, Dode MAN, Franco MM. Low levels of sulfur and cobalt during the pre- and periconceptional periods affect the oocyte yield of donors and the DNA methylome of preimplantation bovine embryos. J Dev Orig Health Dis. 2022;13(2):231-43.
Noya A, Ripoll G, Casasus I, Sanz A. Long-term effects of early maternal undernutrition on the growth, physiological profiles, carcass and meat quality of male beef offspring. Res Vet Sci. 2021;142:1-11.
Obata Y, Kaneko-Ishino T, Koide T, Takai Y, Ueda T, Domeki I, Shiroishi T, Ishino F, Kono T. Disruption of primary imprinting during oocyte growth leads to the modified expression of imprinted genes during embryogenesis. Development. 1998;125(8):1553-60.
Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J. Active demethylation of the paternal genome in the mouse zygote. Curr Biol. 2000;10(8):475-8.
Pedrana G, Viotti H, Lombide P, Cavestany D, Martin GB, Vickers MH, Sloboda DM. Maternal undernutrition during pregnancy and lactation affects testicular morphology, the stages of spermatogenic cycle, and the testicular IGF-I system in adult offspring. J Dev Orig Health Dis. 2020;11(5):473-83.
Proudhon C, Duffie R, Ajjan S, Cowley M, Iranzo J, Carbajosa G, Saadeh H, Holland ML, Oakey RJ, Rakyan VK, Schulz R, Bourc’his D. Protection against de novo methylation is instrumental in maintaining parent-of-origin methylation inherited from the gametes. Mol Cell. 2012;47(6):909-20.
Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science. 2001;293(5532):1089-93.
Roseboom T, de Rooij S, Painter R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006;82(8):485-91.
Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet. 2008;9(2):129-40.
Serrano-Perez B, Molina E, Noya A, Lopez-Helguera I, Casasus I, Sanz A, Villalba D. Maternal nutrient restriction in early pregnancy increases the risk of late embryo loss despite no effects on peri-implantation interferon-stimulated genes in suckler beef cattle. Res Vet Sci. 2020;128:69-75.
Silveira MM, Bayão HXS, dos Santos Mendonça A, Borges NA, Vargas LN, Caetano AR, Rumpf R, Franco MM. DNA methylation profile at a satellite region is associated with aberrant placentation in cloned calves. Placenta. 2018;70:25-33.
Silver MJ, Saffari A, Kessler NJ, Chandak GR, Fall CHD, Issarapu P, Dedaniya A, Betts M, Moore SE, Routledge MN, Herceg Z, Cuenin C, Derakhshan M, James PT, Monk D, Prentice AM. Environmentally sensitive hotspots in the methylome of the early human embryo. eLife. 2022;11:e72031.
Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG, Young LE. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA. 2007;104(49):19351-6.
Skvortsova K, Iovino N, Bogdanovic O. Functions and mechanisms of epigenetic inheritance in animals. Nat Rev Mol Cell Biol. 2018;19(12):774-90.
Smallwood SA, Kelsey G. De novo DNA methylation: a germ cell perspective. Trends Genet. 2012;28(1):33-42.
Stevens ME, Maidens PM, Robinson ES, Vandeberg JL, Pedersen RA, Monk M. DNA methylation in the developing marsupial embryo. Development. 1988;103(4):719-24.
Thakur A, Mackin SJ, Irwin RE, O’Neill KM, Pollin G, Walsh C. Widespread recovery of methylation at gametic imprints in hypomethylated mouse stem cells following rescue with DNMT3A2. Epigenetics Chromatin. 2016;9(1):53.
Tobi EW, Slieker RC, Stein AD, Suchiman HE, Slagboom PE, van Zwet EW, Heijmans BT, Lumey LH. Early gestation as the critical time-window for changes in the prenatal environment to affect the adult human blood methylome. Int J Epidemiol. 2015;44(4):1211-23.
Toschi P, Capra E, Anzalone DA, Lazzari B, Turri F, Pizzi F, Scapolo PA, Stella A, Williams JL, Marsan PA, Loi P. Maternal peri-conceptional undernourishment perturbs offspring sperm methylome. Reproduction. 2020;159(5):513-23.
Wadhwa PD, Buss C, Entringer S, Swanson JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009;27(5):358-68.
Wang X, Lan X, Radunz AE, Khatib H. Maternal nutrition during pregnancy is associated with differential expression of imprinted genes and DNA methyltranfereases in muscle of beef cattle offspring. J Anim Sci. 2015;93(1):35-40.
Xie R, Sun Y, Wu J, Huang S, Jin G, Guo Z, Zhang Y, Liu T, Liu X, Cao X, Wang B, Cao H. Maternal high fat diet alters gut microbiota of offspring and exacerbates DSS-induced colitis in adulthood. Front Immunol. 2018;9:2608.
Xu R, Li C, Liu X, Gao S. Insights into epigenetic patterns in mammalian early embryos. Protein Cell. 2021;12(1):7-28.
Zglejc-Waszak K, Waszkiewicz EM, Franczak A. Periconceptional undernutrition affects the levels of DNA methylation in the peri-implantation pig endometrium and in embryos. Theriogenology. 2019;123:185-93.
Zhang S, Chen X, Wang F, An X, Tang B, Zhang X, Sun L, Li Z. Aberrant DNA methylation reprogramming in bovine SCNT preimplantation embryos. Sci Rep. 2016;6(1):1-11.
Zhang Q, Xiao X, Zheng J, Li M, Yu M, Ping F, Wang T, Wang X. Maternal high-fat diet disturbs the DNA methylation profile in the brown adipose tissue of offspring mice. Front Endocrinol (Lausanne). 2021a;12:705827.
Zhang Z, Xu J, Lyu S, Xin X, Shi Q, Huang Y, Yu X, Zhu X, Li Z, Wang X, Lang L, Xu Z, Wang E. Whole-genome DNA methylation dynamics of sheep preimplantation embryo investigated by single-cell DNA methylome sequencing. Front Genet. 2021b;12:753144.
Zhou F, Wang R, Yuan P, Ren Y, Mao Y, Li R, Lian Y, Li J, Wen L, Yan L, Qiao J, Tang F. Reconstituting the transcriptome and DNA methylome landscapes of human implantation. Nature. 2019;572:660-4.
Zhu P, Guo H, Ren Y, Hou Y, Dong J, Li R, Lian Y, Fan X, Hu B, Gao Y, Wang X, Wei Y, Liu P, Yan J, Ren X, Yuan P, Yuan Y, Yan Z, Wen L, Yan L, Qiao J, Tang F. Single-cell DNA methylome sequencing of human preimplantation embryos. Nat Genet. 2018;50(1):12-9.
Submitted date:
08/08/2022
Accepted date:
02/14/2023
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