综述 REVIEW

丙酮酸对猪早期胚胎发育的影响

  • 闵昌国 ,
  • 车东升 ,
  • 张天芮
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  • 吉林农业大学动物科学技术学院, 动物生产及产品质量安全教育部重点实验室, 吉林省动物营养与饲料科学重点实验室, 吉林省生猪产业技术科技创新中心, 长春 130118
闵昌国(1994-),男,安徽六安人,硕士研究生,从事动物营养代谢调控。E-mail:935355275@qq.com

收稿日期: 2020-09-09

  网络出版日期: 2021-04-15

基金资助

国家重点研发项目(2017YFD0502004)

Effects of Pyruvate on Early Embryonic Development in Pigs

  • MIN Changguo ,
  • CHE Dongsheng ,
  • ZHANG Tianrui
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  • Jilin Provincial Swine Industry Technical Innovation Center, Jilin Provincial Key Lab of Animal Nutrition and Feed Science, Key Lab of Animal Production, Product Quality, and Security, Ministry of Education, College of Animal Science and Technology, Jilin Agricultural University, Changchun 130118, China

Received date: 2020-09-09

  Online published: 2021-04-15

Supported by

 

摘要

在哺乳动物中,早期胚胎发育阻滞一般发生在胚胎由输卵管向子宫角转移的时期,此时输卵管液中的物质对早期胚胎发育尤为重要,如葡萄糖、乳糖、丙酮酸。丙酮酸是大多数能量物质在代谢过程中的中间产物,在抗氧化、间接调节信号等过程中都发挥着重要作用,并且是卵母细胞和合子能够直接利用的主要能量底物。此外,早期胚胎发育阻滞时期恰好是母源-合子基因过渡时期,此时发生的基因组重编程也离不开丙酮酸的参与。本文综述了丙酮酸对哺乳动物早期胚胎发育的影响,推测了丙酮酸在猪早期胚胎合子基因组激活中的作用。

本文引用格式

闵昌国 , 车东升 , 张天芮 . 丙酮酸对猪早期胚胎发育的影响[J]. 动物营养学报, 2021 , 33(4) : 1832 -1840 . DOI: 10.3969/j.issn.1006-267x.2021.04.004

Abstract

In mammals, the early embryo development retardation usually occurs when the embryo is transferred from the oviduct to the uterine horn. At this time, the substances in the oviduct fluid are particularly important for the early embryonic development, such as glucose, lactose and pyruvate. Pyruvate is an intermediate product of most energy substances in the process of metabolism, and it is the main energy substrate that oocytes and zygotes can use directly, and plays a role in antioxidant and indirect signal regulation. In addition, the development retardation period of early embryogenesis happens to be the transition period between maternal and zygote genes. At this time, the genome reprogramming cannot be separated from pyruvate. Therefore, this paper reviews the effects of pyruvate on the development of mammalian early embryos, and speculates the role of pyruvate in the activation of zygote genome in pig early embryos.

参考文献

[1] GEISERT R D,SCHMITT R A M.Early embryonic survival in the pig:can it be improved?[J].Journal of Animal Science,2002,80(E-Suppl_1):E54-E65.
[2] NASR-ESFAHANI M H,AITKEN J R,JOHNSON M H.Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo[J].Development,1990,109(2):501-507.
[3] QUINN P,HARLOW G M.The effect of oxygen on the development of preimplantation mouse embryos in vitro[J].Journal of Experimental Zoology,1978,206(1):73-80.  
[4] TADROS W,LIPSHITZ H D.The maternal-to-zygotic transition:a play in two acts[J].Development,2009,136(18):3033-3042.  
[5] KAGEYAMA S,GUNJI W,NAKASATO M,et al.Analysis of transcription factor expression during oogenesis and preimplantation development in mice[J].Zygote,2007,15(2):117-128.  
[6] MANES C,LAI N C.Nonmitochondrial oxygen utilization by rabbit blastocysts and surface production of superoxide radicals[J].Journal of Reproducfion and Fertility,1995,104(1):69-75.  
[7] BRINSTER R T.Studies on the development of mouse embyros in vitro. Ⅱ.The effect of energy source[J].Journal of Experimental Zoology,2004,158(1):59-68.
[8] BROWN J J G,WHITTINGHAM D G.The roles of pyruvate,lactate and glucose during preimplantation development of embryos from F1 hybrid mice in vitro[J].Development,1991,112(1):99-105.
[9] HOPPER S,SEGAL H L.Comparative properties of glutamic-alanine transaminase from several sources[J].Archives of Biochemistry and Biophysics,1964,105(3):501-505.  
[10] MENDES-MOURÃO J,HALESTRAP A,CRISP D M,et al.The involvement of mitochondrial pyruvate transport in the pathways of gluconeogenesis from serine and alanine in isolated rat and mouse liver cells[J].FEBS Letters,1975,53(1):29-32.  
[11] DAWSON D M,GOODFRIEND T L,KAPLAN N O,et al.Lactic dehydrogenases:functions of the two types rates of synthesis of the two major forms can be correlated with metabolic differentiation[J].Science,1964,143(3609):929-933.  
[12] BIGGERS J D,WHITTINGHAM D G,DONAHUE R P.The pattern of energy metabolism in the mouse oöcyte and zygote[J].Proceedings of the National Academy of Sciences of the United States of America,1967,58(2):560-567.  
[13] GESHI M,TAKENOUCHI N,YAMAUCHI N,et al.Effects of sodium pyruvate in nonserum maturation medium on maturation,fertilization,and subsequent development of bovine oocytes with or without cumulus cells[J].Biology of Reproduction,2000,63(6):1730-1734.  
[14] CHUNG S J,LEE S H,LEE Y J,et al.Pyruvate protection against endothelial cytotoxicity induced by blockade of glucose uptake[J].Journal of Biochemistry and Molecular Biology,2004,37(2):239-245.
[15] DOWNS S M,HUMPHERSON P G,LEESE H J.Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus[J].Molecular Reproduction and Development,2000,62(1):113-123.
[16] O'FALLON J V,WRIGHT R W,Jr.Pyruvate revisited:a non-metabolic role for pyruvate in preimplantation embryo development[J].Theriogenology,1995,43(1):288.
[17] MORALES H,TILQUIN P J,REES J F,et al.Pyruvate prevents peroxide-induced injury of in vitro preimplantation bovine embryos[J].Molecular Reproduction and Development,1999,52(2):149-157.  
[18] KANG Y H,CHUNG S J,KANG I J,et al.Intramitochondrial pyruvate attenuates hydrogen peroxide-induced apoptosis in bovine pulmonary artery endothelium[J].Molecular and Cellular Biochemistry,2001,216(1):37-46.
[19] DE LAMIRANDE E,GAGNON C.Reactive oxygen species and human spermatozoa.Ⅱ.Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility[J].Journal of Andrology,1992,13(5):379-386.
[20] LEE Y J,KANG I J,BÜNGER R,et al.Mechanisms of pyruvate inhibition of oxidant-induced apoptosis in human endothelial cells[J].Microvascular Research,2003,66(2):91-101.  
[21] KASHIWAGI A,NISHIO Y,ASAHINA T,et al.Pyruvate improves deleterious effects of high glucose on activation of pentose phosphate pathway and glutathione redox cycle in endothelial cells[J].Diabetes,1997,46(12):2088-2095.  
[22] CARAFOLI E.Calcium signaling:a tale for all seasons[J].Proceedings of the National Academy of Sciences of the United States of America,2002,99(3):1115-1122.  
[23] BAKOWSKI D,PAREKH A B.Regulation of store-operated calcium channels by the intermediary metabolite pyruvic acid[J].Current Biology,2007,17(12):1076-1081.  
[24] MUALLEM S.Calcium signaling:pyruvate and CRAC meet at the crossroads[J].Current Biology,2007,17(14):R549-R551.
[25] YAN L,YANG M,GUO H,et al.Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells[J].Nature Structural & Molecular Biology,2013,20:1131-1139.
[26] DE SOUSA P A,WATSON A J,SCHULTZ R M.Transient expression of a translation initiation factor is conservatively associated with embryonic gene activation in murine and bovine embryos[J].Biology of Reproduction,1998,59(4):969-977.  
[27] MAGNANI L,JOHNSON C M,CABOT R A.Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential[J].Reproduction,Fertility and Development,2008,20(7):818-825.  
[28] FAVETTA L A,JOHN E J,St.,KING W A,et al.High levels of p66shc and intracellular ROS in permanently arrested early embryos[J].Free Radical Biology and Medicine,2007,42(8):1201-1210.  
[29] ROMEK M,GAJDA B,KRZYSZTOFOWICZ E,et al.Lipid content of non-cultured and cultured pig embryo[J].Reproduction in Domestic Animals,2009,44(1):24-32.  
[30] XUE L,CAI J Y,MA J,et al.Global expression profiling reveals genetic programs underlying the developmental divergence between mouse and human embryogenesis[J].BMC Genomics,2013,14:568.
[31] DAHL J A,JUNG I,AANES H,et al.Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition[J].Nature,2016,537(7621):548-552.  
[32] LEE M T,BONNEAU A R,TAKACS C M,et al.Nanog,Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition[J].Nature,2013,503(7476):360-364.  
[33] AOSHIMA K,INOUE E,SAWA H,et al.Paternal H3K4 methylation is required for minor zygotic gene activation and early mouse embryonic development[J].EMBO Reports,2015,16(7):803-812.  
[34] DEKKER J,MIRNY L.The 3D genome as moderator of chromosomal communication[J].Cell,2016,164(6):1110-1121.  
[35] FRASER R,LIN C J.Epigenetic reprogramming of the zygote in mice and men:on your marks,get set,go![J].Reproduction,2016,152(6):R211-R222.
[36] HACKETT J A,SURANI M A.DNA methylation dynamics during the mammalian life cycle[J].Philosophical Transactions of the Royal Society B:Biological Sciences,2013,368(1609):20110328.
[37] ZHANG B J,ZHENG H,HUANG B,et al.Allelic reprogramming of the histone modification H3K4me3 in early mammalian development[J].Nature,2016,537(7621):553-557.  
[38] AKIYAMA T,NAGATA M,AOKI F.Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice[J].Proceedings of the National Academy of Sciences of the United States of America,2006,103(19):7339-7344.  
[39] MA P P,SCHULTZ R M.Histone deacetylase 1(HDAC1) regulates histone acetylation,development,and gene expression in preimplantation mouse embryos[J].Developmental Biology,2008,319(1):110-120.  
[40] EBERHARTER A,BECKER P B.Histone acetylation:a switch between repressive and permissive chromatin:second in review series on chromatin dynamics[J].EMBO Reports,2002,3(3):224-229.  
[41] GRUNSTEIN M.Histone acetylation in chromatin structure and transcription[J].Nature,1997,389(6649):349-352.  
[42] SHOGREN-KNAAK M,ISHⅡ H,SUN J M,et al.Histone H4-K16 acetylation controls chromatin structure and protein interactions[J].Science,2006,311(5762):844-847.  
[43] BANNISTER A J,KOUZARIDES T.Regulation of chromatin by histone modifications[J].Cell Research,2011,21(3):381-395.  
[44] AGARWAL A,SAID T M,BEDAIWY M A,et al.Oxidative stress in an assisted reproductive techniques setting[J].Fertility and Sterility,2006,86(3):503-512.  
[45] LAN K C,LIN Y C,CHANG Y C,et al.Limited relationships between reactive oxygen species levels in culture media and zygote and embryo development[J].Journal of Assisted Reproduction and Genetics,2018,36(2):325-334.
[46] AGARWAL A,SALEH R A,BEDAIWY M A.Role of reactive oxygen species in the pathophysiology of human reproduction[J].Fertility and Sterility,2003,79(4):829-843.  
[47] GUERIN P,EL MOUATASSIM S,MÉNÉZO Y.Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings[J].Human Reproduction Update,2001,7(2):175-189.  
[48] LEE T H,LEE M S,LIU C H,et al.The association between microenvironmental reactive oxygen species and embryo development in assisted reproduction technology cycles[J].Reproductive Sciences,2012,19(7):725-732.  
[49] BEDAIWY M A,MAHFOUZ R Z,GOLDBERG J M,et al.Relationship of reactive oxygen species levels in day 3 culture media to the outcome of in vitro fertilization/intracytoplasmic sperm injection cycles[J].Fertility and Sterility,2010,94(6):2037-2042.  
[50] MARTÍN-ROMERO F J,MIGUEL-LASOBRAS E M,DOMÍNGUEZ-ARROYO J A,et al.Contribution of culture media to oxidative stress and its effect on human oocytes[J].Reproductive BioMedicine Online,2008,17(5):652-661.  
[51] BEDAIWY M A,FALCONE T,MOHAMED M S,et al.Differential growth of human embryos in vitro:role of reactive oxygen species[J].Fertility and Sterility,2004,82(3):593-600.  
[52] PASZKOWSKI T,CLARKE R N.Fertilization and early embryology:antioxidative capacity of preimplantation embryo culture medium declines following the incubation of poor quality embryos[J].Human Reproduction,1996,11(11):2493-2495.  
[53] BAUMEISTER P,HUEBNER T,REITER M,et al.Reduction of oxidative DNA fragmentation by ascorbic acid,zinc and N-acetylcysteine in nasal mucosa tissue cultures[J].Anticancer Research,2009,29(11):4571-4574.
[54] NEGRE-SALVAYRE A,SALVAYRE R,AUGÉ N,et al.Hyperglycemia and glycation in diabetic complications[J].Antioxidants & Redox Signaling,2009,11(12):3071-3109.  
[55] EBERT R,ULMER M,ZECK S,et al.Selenium supplementation restores the antioxidative capacity and prevents cell damage in bone marrow stromal cells in vitro[J].Stem Cells,2006,24(5):1226-1235.  
[56] TRABER M G,ATKINSON J.Vitamin E,antioxidant and nothing more[J].Free Radical Biology and Medicine,2007,43(1):4-15.  
[57] RUSHWORTH G F,MEGSON I L.Existing and potential therapeutic uses for N-acetylcysteine:the need for conversion to intracellular glutathione for antioxidant benefits[J].Pharmacology & Therapeutics,2014,141(2):150-159.  
[58] MANDL J,SZARKA A,BÁNHEGYI G.Vitamin C:update on physiology and pharmacology[J].British Journal of Pharmacology,2009,157(7):1097-1110.  
[59] BABICH H,LIEBLING E J,BURGER R F,et al.Choice of DMEM,formulated with or without pyruvate,plays an important role in assessing the in vitro cytotoxicity of oxidants and prooxidant nutraceuticals[J].In Vitro Cellular & Developmental Biology-Animal,2009,45(5/6):226-233.
[60] LONG L H,HALLIWELL B.Artefacts in cell culture:pyruvate as a scavenger of hydrogen peroxide generated by ascorbate or epigallocatechin gallate in cell culture media[J].Biochemical and Biophysical Research Communications,2009,388(4):700-704.  
[61] WANG X F,PEREZ E,LIU R,et al.Pyruvate protects mitochondria from oxidative stress in human neuroblastoma SK-N-SH cells[J].Brain Research,2007,1132:1-9.
[62] TEJERO-TALDO M I,CAFFREY J L,SUN J,et al.Antioxidant properties of pyruvate mediate its potentiation of β-adrenergic inotropism in stunned myocardium[J].Journal of Molecular and Cellular Cardiology,1999,31(10):1863-1872.  
[63] BRADLEY J,SWANN K.Mitochondria and lipid metabolism in mammalian oocytes and early embryos[J].The International Journal of Developmental Biology,2019,63(3/4/5):93-103.
[64] DUMOLLARD R,CAMPBELL K,HALET G,et al.Regulation of cytosolic and mitochondrial ATP levels in mouse eggs and zygotes[J].Developmental Biology,2008,316(2):431-440.  
[65] HO H C,GRANISH K A,SUAREZ S S.Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and Not CAMP[J].Developmental Biology,2002,250(1):208-217.  
[66] DEMOTT R P,SUAREZ S S.Hyperactivated sperm progress in the mouse oviduct[J].Biology of Reproduction,1992,46(5):779-785.  
[67] STAUSS C R,VOTTA T J,SUAREZ S S.Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida[J].Biology of Reproduction,1995,53(6):1280-1285.  
[68] DE AGOSTINI LOSANO J D,DE SOUZA RAMOS ANGRIMANI D,LEITE R F,et al.Spermatic mitochondria:role in oxidative homeostasis,sperm function and possible tools for their assessment[J].Zygote,2018,26(4):251-260.  
[69] HOSHI K,TSUKIKAWA S,SATO A.Importance of Ca2+,K+ and glucose in the medium for sperm penetration through the human zona pellucida[J].The Tohoku Journal of Experimental Medicine,1991,165(2):99-104.  
[70] WILLIAMS A C,FORD W C L.The role of glucose in supporting motility and capacitation in human spermatozoa[J].Journal of Andrology,2001,22(4):680-695.
[71] MUKAI C,OKUNO M.Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement[J].Biology of Reproduction,2004,71(2):540-547.  
[72] HERENG T H,ELGSTØEN K B P,CEDERKVIST F H,et al.Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa[J].Human Reproduction,2011,26(12):3249-3263.  
[73] LANE M,GARDNER D K.Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo[J].Biology of Reproduction,2000,62(1):16-22.  
[74] BARBEHENN E K,WALES R G,LOWRY O H.Measurement of metabolites in single preimplantation embryos;a new means to study metabolic control in early embryos[J].Journal of Embryology & Experimental Morphology,1978,43:29-46.
[75] BRINSTER R L.Incorporation of carbon from glucose and pyruvate into the preimplantation mouse embryo[J].Experimental Cell Research,1969,58(1):153-158.  
[76] BAUMANN C G,MORRIS D G,SREENAN J M,et al.The quiet embryo hypothesis:molecular characteristics favoring viability[J].Molecular Reproduction & Development,2010,74(10):1345-1353.
[77] COCKBURN K,ROSSANT J.Making the blastocyst:lessons from the mouse[J].Journal of Clinical Investigation,2010,120(4):995-1003.  
[78] LI L,ZHENG P,DEAN J.Maternal control of early mouse development[J].Development,2010,137(6):859-870.  
[79] HARDIVILLÉ S,HART G W.Nutrient regulation of signaling,transcription,and cell physiology by O-GlcNAcylation[J].Cell Metabolism,2014,20(2):208-213.  
[80] MARTINEZ-PASTOR B,COSENTINO C,MOSTOSLAVSKY R.A tale of metabolites:the cross-talk between chromatin and energy metabolism[J].Cancer Discovery,2013,3(5):497-501.  
[81] PATEL M S,KOROTCHKINA L G.Regulation of mammalian pyruvate dehydrogenase complex by phosphorylation:complexity of multiple phosphorylation sites and kinases[J].Experimental & Molecular Medicine,2001,33(4):191-197.  
[82] PATEL M S,NEMERIA N S,FUREY W,et al.The pyruvate dehydrogenase complexes:structure-based function and regulation[J].Journal of Biological Chemistry,2014,289(24) 16615-16623.
[83] NAGARAJ R,SHARPLEY M S,CHI F,et al.Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation[J].Cell,2017,168(1/2):210-223.
[84] ZHOU W J,NIU Y J,NIE Z W,et al.Nuclear accumulation of pyruvate dehydrogenase alpha 1 promotes histone acetylation and is essential for zygotic genome activation in porcine embryos[J].Biochimica et Biophysica Acta:Molecular Cell Research,2020,1867(4):118648.
[85] LI Y X,TANG Z R,LI T J,et al.Pyruvate is an effective substitute for glutamate in regulating porcine nitrogen excretion[J].Journal of Animal Science,2018,96(9):3804-3814.  
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