DNA甲基化在猪胚胎发育过程中的研究进展

doi:10.11843/j.issn.0366-6964.2022.10.002

Abstract

Abstract: Embryonic development in pigs requires a series of crucial physiological stages such as fertilization, cleavage, hatching, morphological transformation, implantation, and cellular differentiation. While a tightly regulated and accurately directed genome is a determining condition for normal embryonic development, recent studies have revealed that appropriate DNA methylation modification also plays an essential role in this process. DNA methylation is a wide and crucial epigenetic modification that does not alter the primary sequence of DNA. However, it contains heritable information and plays an indispensable role in the transcriptional regulation of genes. DNA methylation appears to be a highly dynamic process, influenced by maternal nutrition and developmental conditions in porcine embryonic development. This review describes the effects of DNA methylation on embryonic development from three aspects:early embryonic development, somatic cell nuclear transfer and maternal nutrition during pregnancy, in order to provide references for further research on the mechanism of DNA methylation in porcine embryos during development and to improve the viability of cloned embryos.

Key words: pig, DNA methylation, embryonic development, somatic cell nuclear transfer, pregnancy nutrition, imprinting genes

CLC Number:

S828.2

GAN Jianyu, ZHANG Xin, CAI Gengyuan, HONG Linjun, HUANG Sixiu. Research Progress of DNA Methylation during Porcine Embryonic Development[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(10): 3287-3295.

References 82

[1]	PRATHER R S, LORSON M, ROSS J W, et al.Genetically engineered pig models for human diseases[J].Annu Rev Anim Biosci, 2013, 1:203-219.
[2]	BICK J T, FLÖTER V L, ROBINSON M D, et al.Small RNA-seq analysis of single porcine blastocysts revealed that maternal estradiol-17beta exposure does not affect miRNA isoform (isomiR) expression[J].BMC Genomics, 2018, 19(1):590.
[3]	BAZER F W, JOHNSON G A.Pig blastocyst-uterine interactions[J].Differentiation, 2014, 87(1-2):52-65.
[4]	BIDARIMATH M, TAYADE C.Pregnancy and spontaneous fetal loss:A pig perspective[J].Mol Reprod Dev, 2017, 84(9):856-869.
[5]	WU G, BAZER F W, WALLACE J M, et al.BOARD-INVITED REVIEW:Intrauterine growth retardation:implications for the animal sciences[J].J Anim Sci, 2006, 84(9):2316-2337.
[6]	POPE W F.Uterine asynchrony:A cause of embryonic loss[J].Biol Reprod, 1988, 39(5):999-1003.
[7]	EGGER G, LIANG G N, APARICIO A, et al.Epigenetics in human disease and prospects for epigenetic therapy[J].Nature, 2004, 429(6990):457-463.
[8]	JAENISCH R, BIRD A.Epigenetic regulation of gene expression:How the genome integrates intrinsic and environmental signals[J].Nat Genet, 2003, 33 Suppl:245-254.
[9]	FENG S H, JACOBSEN S E, REIK W.Epigenetic reprogramming in plant and animal development[J].Science, 2010, 330(6004):622-627.
[10]	ALBERIO R.Regulation of cell fate decisions in early mammalian embryos[J].Annu Rev Anim Biosci, 2020, 8:377-393.
[11]	ARRELL V L, DAY B N, PRATHER R S.The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa:quantitative and qualitative aspects of protein synthesis[J].Biol Reprod, 1991, 44(1):62-68.
[12]	BAZER F W, SPENCER T E, JOHNSON G A, et al.Uterine receptivity to implantation of blastocysts in mammals[J].Front Biosci (Schol Ed), 2011, 3(2):745-767.
[13]	TAYADE C, BLACK G P, FANG Y, et al.Differential gene expression in endometrium, endometrial lymphocytes, and trophoblasts during successful and abortive embryo implantation[J].J Immunol, 2006, 176(1):148-156.
[14]	KACZMAREK M M, NAJMULA J, GUZEWSKA M M, et al.miRNAs in the peri-implantation period:Contribution to embryo-maternal communication in pigs[J].Int J Mol Sci, 2020, 21(6):2229.
[15]	胡群, 叶南, 史泽宇, 等.猪妊娠过程中胎盘发育及其调控基因研究进展[J].中国畜牧兽医, 2018, 45(6):1633-1638.HU Q, YE N, SHI Z Y, et al.Research advance on placenta development and its regulated genes in pig[J].China Animal Husbandry & Veterinary Medicine, 2018, 45(6):1633-1638.(in Chinese)
[16]	LAW J A, JACOBSEN S E.Establishing, maintaining and modifying DNA methylation patterns in plants and animals[J].Nat Rev Genet, 2010, 11(3):204-220.
[17]	BESTOR T H.The DNA methyltransferases of mammals[J].Hum Mol Genet, 2000, 9(16):2395-2402.
[18]	LI Y, ZHANG Z, CHEN J, et al.Stella safeguards the oocyte methylome by preventing de novo methylation mediated by DNMT1[J].Nature, 2018, 564(7734):136-140.
[19]	SCHNEIDER E, PLIUSHCH G, EL HAJJ N, et al.Spatial, temporal and interindividual epigenetic variation of functionally important DNA methylation patterns[J].Nucleic Acids Res, 2010, 38(12):3880-3890.
[20]	MEDVEDEVA Y A, KHAMIS A M, KULAKOVSKIY I V, et al.Effects of cytosine methylation on transcription factor binding sites[J].BMC Genomics, 2014, 15:119.
[21]	DURCOVA-HILLS G, HAJKOVA P, SULLIVAN S, et al.Influence of sex chromosome constitution on the genomic imprinting of germ cells[J].Proc Natl Acad Sci U S A, 2006, 103(30):11184-11188.
[22]	VARLEY K E, GERTZ J, BOWLING K M, et al.Dynamic DNA methylation across diverse human cell lines and tissues[J].Genome Res, 2013, 23(3):555-567.
[23]	LI M Z, WU H L, LUO Z G, et al.An atlas of DNA methylomes in porcine adipose and muscle tissues[J].Nat Commun, 2012, 3:850.
[24]	GOWHER H, JELTSCH A.Enzymatic properties of recombinant Dnmt3a DNA methyltransferase from mouse:the enzyme modifies DNA in a non-processive manner and also methylates non-CpA sites[J].J Mol Biol, 2001, 309(5):1201-1208.
[25]	RAMSAHOYE B H, BINISZKIEWICZ D, LYKO F, et al.Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a[J].Proc Natl Acad Sci U S A, 2000, 97(10):5237-5242.
[26]	LAURENT L, WONG E, LI G L, et al.Dynamic changes in the human methylome during differentiation[J].Genome Res, 2010, 20(3):320-331.
[27]	LISTER R, PELIZZOLA M, DOWEN R H, et al.Human DNA methylomes at base resolution show widespread epigenomic differences[J].Nature, 2009, 462(7271):315-322.
[28]	SANTOS F, HENDRICH B, REIK W, et al.Dynamic reprogramming of DNA methylation in the early mouse embryo[J].Dev Biol, 2002, 241(1):172-182.
[29]	LEE H J, HORE T A, REIK W.Reprogramming the methylome:Erasing memory and creating diversity[J].Cell Stem Cell, 2014, 14(6):710-719.
[30]	LI E.Chromatin modification and epigenetic reprogramming in mammalian development[J].Nat Rev Genet, 2002, 3(9):662-673.
[31]	SMITH Z D, CHAN M M, MIKKELSEN T S, et al.A unique regulatory phase of DNA methylation in the early mammalian embryo[J].Nature, 2012, 484(7394):339-344.
[32]	KAFRI T, ARIEL M, BRANDEIS M, et al.Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line[J].Genes Dev, 1992, 6(5):705-714.
[33]	MONK M, BOUBELIK M, LEHNERT S.Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development[J].Development, 1987, 99(3):371-382.
[34]	FULKA J, FULKA H, SLAVIK T, et al.DNA methylation pattern in pig in vivo produced embryos[J].Histochem Cell Biol, 2006, 126(2):213-217.
[35]	JEONG Y S, YEO S, PARK J S, et al.DNA methylation state is preserved in the sperm-derived pronucleus of the pig zygote[J].Int J Dev Biol, 2007, 51(8):707-714.
[36]	ZHU Q F, SANG F, WITHEY S, et al.Specification and epigenomic resetting of the pig germline exhibit conservation with the human lineage[J].Cell Rep, 2021, 34(6):108735.
[37]	HYLDIG S M W, OSTRUP O, VEJLSTED M, et al.Changes of DNA methylation level and spatial arrangement of primordial germ cells in embryonic day 15 to embryonic day 28 pig embryos[J].Biol Reprod, 2011, 84(6):1087-1093.
[38]	GÓMEZ-REDONDO I, PLANELLS B, CÁNOVAS S, et al.Genome-wide DNA methylation dynamics during epigenetic reprogramming in the porcine germline[J].Clin Epigenet, 2021, 13(1):27.
[39]	REIK W.Stability and flexibility of epigenetic gene regulation in mammalian development[J].Nature, 2007, 447(7143):425-432.
[40]	HAJKOVA P, JEFFRIES S J, LEE C, et al.Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway[J].Science, 2010, 329(5987):78-82.
[41]	MORGAN H D, DEAN W, COKER H A, et al.Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues:implications for epigenetic reprogramming[J].J Biol Chem, 2004, 279(50):52353-52360.
[42]	POPP C, DEAN W, FENG S H, et al.Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency[J].Nature, 2010, 463(7284):1101-1105.
[43]	GUIBERT S, FORNÉ T, WEBER M.Global profiling of DNA methylation erasure in mouse primordial germ cells[J].Genome Res, 2012, 22(4):633-641.
[44]	LUO Z G, ZHANG K, CHEN L, et al.Molecular characterization and tissue expression profile of the Dnmts gene family in pig[J].J Integr Agric, 2017, 16(6):1367-1374.
[45]	SHARIF J, MUTO M, TAKEBAYASHI S I, et al.The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA[J].Nature, 2007, 450(7171):908-912.
[46]	OKANO M, XIE S P, LI E.Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases[J]. Nat Genet, 1998, 19(3):219-220.
[47]	WION D, CASADESÚS J.N6-methyl-adenine:An epigenetic signal for DNA-protein interactions[J].Nat Rev Microbiol, 2006, 4(3):183-192.
[48]	RATEL D, RAVANAT J L, BERGER F, et al.N6-methyladenine:the other methylated base of DNA[J].Bioessays, 2006, 28(3):309-315.
[49]	HE S M, ZHANG G Q, WANG J J, et al.6 mA-DNA-binding factor Jumu controls maternal-to-zygotic transition upstream of Zelda[J].Nat Commun, 2019, 10(1):2219.
[50]	LIU J Z, ZHU Y X, LUO G Z, et al.Abundant DNA 6 mA methylation during early embryogenesis of zebrafish and pig[J].Nat Commun, 2016, 7:13052.
[51]	FERNANDES S B, GROVA N, ROTH S, et al.N6-methyladenine in eukaryotic DNA:Tissue distribution, early embryo development, and neuronal toxicity[J].Front Genet, 2021, 12:657171.
[52]	LI Z, ZHAO S, NELAKANTI R V, et al.N6-methyladenine in DNA antagonizes SATB1 in early development[J].Nature, 2020, 583(7817):625-630.
[53]	WU T P, WANG T, SEETIN M G, et al.DNA methylation on N6-adenine in mammalian embryonic stem cells[J].Nature, 2016, 532(7599):329-333.
[54]	BOULIAS K, GREER E L.Means, mechanisms and consequences of adenine methylation in DNA[J].Nat Rev Genet, 2022, 23(7):411-428.
[55]	ZHU Q F, STÖGER R, ALBERIO R.A Lexicon of DNA modifications:Their roles in embryo development and the germline[J].Front Cell Dev Biol, 2018, 6:24.
[56]	ZHAO J G, WHYTE J, PRATHER R S.Effect of epigenetic regulation during swine embryogenesis and on cloning by nuclear transfer[J].Cell Tissue Res, 2010, 341(1):13-21.
[57]	PRATHER R S, SHEN M D, DAI Y F.Genetically modified pigs for medicine and agriculture[J].Biotechnol Genet Eng Rev, 2008, 25:245-265.
[58]	LIU Y, LI J, LØVENDAHL P, et al.In vitro manipulation techniques of porcine embryos:A meta-analysis related to transfers, pregnancies and piglets[J].Reprod Fertil Dev, 2015, 27(3):429-439.
[59]	DESHMUKH R S, ØSTRUP O, ØSTRUP E, et al.DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer[J].Epigenetics, 2011, 6(2):177-187.
[60]	SONG X X, LIU Z H, HE H B, et al.Dnmt1s in donor cells is a barrier to SCNT-mediated DNA methylation reprogramming in pigs[J].Oncotarget, 2017, 8(21):34980-34991.
[61]	WANG X W, SHI J S, CAI G Y, et al.Overexpression of MBD3 improves reprogramming of cloned pig embryos[J].Cell Reprogram, 2019, 21(5):221-228.
[62]	LI Z C, HE X Y, CHEN L W, et al.Bone marrow mesenchymal stem cells are an attractive donor cell type for production of cloned pigs as well as genetically modified cloned pigs by somatic cell nuclear transfer[J].Cell Reprogram, 2013, 15(5):459-470.
[63]	ZHAI Y H, LI W, ZHANG Z R, et al.Epigenetic states of donor cells significantly affect the development of somatic cell nuclear transfer (SCNT) embryos in pigs[J].Mol Reprod Dev, 2018, 85(1):26-37.
[64]	HUAN Y J, ZHU J, HUANG B, et al.Trichostatin A rescues the disrupted imprinting induced by somatic cell nuclear transfer in pigs[J].PLoS One, 2015, 10(5):e0126607.
[65]	XU W H, LI Z C, YU B, et al.Effects of DNMT1 and HDAC inhibitors on gene-specific methylation reprogramming during porcine somatic cell nuclear transfer[J].PLoS One, 2013, 8(5):e64705.
[66]	ZHAI Y H, ZHANG M, AN X L, et al.TRIM28 maintains genome imprints and regulates development of porcine SCNT embryos[J].Reproduction, 2021, 161(4):411-424.
[67]	YU D W, WANG J, ZOU H Y, et al.Silencing of retrotransposon-derived imprinted gene RTL1 is the main cause for postimplantational failures in mammalian cloning[J].Proc Natl Acad Sci U S A, 2018, 115(47):E11071-E11080.
[68]	WANG P, LI X P, CAO L H, et al.MicroRNA-148a overexpression improves the early development of porcine somatic cell nuclear transfer embryos[J].PLoS One, 2017, 12(6):e0180535.
[69]	QU J D, WANG X Y, JIANG Y J, et al.Optimizing 5-aza-2'-deoxycytidine treatment to enhance the development of porcine cloned embryos by inhibiting apoptosis and improving DNA methylation reprogramming[J].Res Vet Sci, 2020, 132:229-236.
[70]	JEONG P S, YANG H J, PARK S H, et al.Combined chaetocin/trichostatin A treatment improves the epigenetic modification and developmental competence of porcine somatic cell nuclear transfer embryos[J].Front Cell Dev Biol, 2021, 9:709574.
[71]	ZHAI Y H, ZHANG Z R, YU H, et al.Dynamic methylation changes of DNA and H3K4 by RG108 improve epigenetic reprogramming of somatic cell nuclear transfer embryos in pigs[J].Cell Physiol Biochem, 2018, 50(4):1376-1397.
[72]	JIN J X, LEE S, TAWEECHAIPAISANKUL A, et al.The HDAC inhibitor LAQ824 enhances epigenetic reprogramming and in vitro development of porcine SCNT embryos[J].Cell Physiol Biochem, 2017, 41(3):1255-1266.
[73]	JEONG P S, SIM B W, PARK S H, et al.Chaetocin improves pig cloning efficiency by enhancing epigenetic reprogramming and autophagic activity[J].Int J Mol Sci, 2020, 21(14):4836.
[74]	WATERLAND R A.Assessing the effects of high methionine intake on DNA methylation[J].J Nutr, 2006, 136(6 Suppl):1706S-1710S.
[75]	ZGLEJC K, FRANCZAK A.Peri-conceptional under-nutrition alters the expression of TRIM28 and ZFP57 in the endometrium and embryos during peri-implantation period in domestic pigs[J].Reprod Domest Anim, 2017, 52(4):542-550.
[76]	ALTMANN S, MURANI E, SCHWERIN M, et al.Maternal dietary protein restriction and excess affects offspring gene expression and methylation of non-SMC subunits of condensin I in liver and skeletal muscle[J].Epigenetics, 2012, 7(3):239-252.
[77]	OSTER M, TRAKOOLJUL N, REYER H, et al.Sex-specific muscular maturation responses following prenatal exposure to methylation-related micronutrients in pigs[J].Nutrients, 2017, 9(1):74.
[78]	FRANCZAK A, ZGLEJC-WASZAK K, MARTYNIAK M, et al.Peri-conceptional nutritional restriction alters transcriptomic profile in the peri-implantation pig embryos[J].Anim Reprod Sci, 2018, 197:305-316.
[79]	ZGLEJC-WASZAK K, WASZKIEWICZ E M, FRANCZAK A.Periconceptional undernutrition affects the levels of DNA methylation in the peri-implantation pig endometrium and in embryos[J].Theriogenology, 2019, 123:185-193.
[80]	FRANCZAK A, ZGLEJC K, WASZKIEWICZ E, et al.Periconceptional undernutrition affects in utero methyltransferase expression and steroid hormone concentrations in uterine flushings and blood plasma during the peri-implantation period in domestic pigs[J].Reprod Fertil Dev, 2017, 29(8):1499-1508.
[81]	LI Z C, YUE Z M, AO Z, et al.Maternal dietary supplementation of arginine increases the ratio of total cloned piglets born to total transferred cloned embryos by improving the pregnancy rate of recipient sows[J].Anim Reprod Sci, 2018, 196:211-218.
[82]	CEDAR H, BERGMAN Y.Linking DNA methylation and histone modification:Patterns and paradigms[J].Nat Rev Genet, 2009, 10(5):295-304.

Research Progress of DNA Methylation during Porcine Embryonic Development

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