|
|
|
| Research Progress on Histone Lactylation in Animal Reproductive Development |
| XIA Yi, WANG Zhi-Chao, SHI Zhen-Hu, WANG Xin, ZHANG Yun-Hai*, CAO Zu-Bing* |
| Anhui Provincial Key Laboratory of Local Livestock and Poultry, Genetical Resource Conservation and Breeding/College of Animal Science and Technology, Anhui Agricultural University, Hefei 230036, China |
|
|
|
|
Abstract Epigenetic modification plays an important role in a series of reproductive developments such as spermatogenesis, oogenesis, early embryonic development, embryo implantation, and stem cells. Histone lactylation, as a newly discovered epigenetic modification that links cellular metabolism with epigenetic regulation, is gradually deepening the study of its mechanism of action in animal reproductive development. In this paper, the latest research progress on histone lactylation were summarized, focusing on the close relationship between histone lactylation and other apparent modifications, the writer, reader and eraser of histone lactylation modifications, and the role of histone lactylation in animal reproductive development. This paper systematically reviewed the research progress of histone lactylation modification in animal repro-ductive development, provides a theoretical basis for a deeper understanding of the molecular regulatory mechanisms of reproductive development.
|
|
Received: 08 October 2024
|
|
|
|
Corresponding Authors:
*yunhaizhang@ahau.edu.cn; zubingcao@ahau.edu.cn
|
|
|
|
[1] 张梦雅, 闫业联, 汪薪, 等. 2023. m6A甲基化调控哺乳动物配子成熟和胚胎发育的研究进展[J]. 农业生物技术学报, 31(07): 1534-1546.
(Zhang M Y, Yan Y L, Wang X, et al.2023. Research progress on m6A methylation regulation of mammalian gamete maturation and embryonic development[J]. Journal of Agricultural Biotechnology, 31(07): 1534-1546.)
[2] An Y, Duan H.2022. The role of m6A RNA methylation in cancer metabolism[J]. Molecular Cancer, 21(1): 14.
[3] Arthur S A, Blaydes J P, Houghton F D.2019. Glycolysis regulates human embryonic stem cell self-renewal under hypoxia through HIF-2alpha and the glycolytic sensors CTBPs[J]. Stem Cell Reports, 12(4): 728-742.
[4] Bermejo-Alvarez P, Lonergan P, Rizos D, et al.2010. Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis[J]. Reproductive Biomedicine Online, 20(3): 341-349.
[5] Bragança J, Eloranta J J, Bamforth S D, et al.2003. Physical and functional interactions among AP-2 transcription factors, p300/CREB-binding protein, and CITED2[J]. Journal of Biological Chemistry, 278(18): 16021-16029.
[6] Bröhm A, Schoch T, Dukatz M, et al.2022. Methylation of recombinant mononucleosomes by DNMT3A demonstrates efficient linker DNA methylation and a role of H3K36me3[J]. Communications Biology, 5(1): 192.
[7] Brooks G A.2020. Lactate as a fulcrum of metabolism[J]. Redox Biology, 35: 101454.
[8] Brown J J. Whittingham D G.1991. The roles of pyruvate, lactate and glucose during preimplantation development of embryos from F1 hybrid mice in vitro[J]. Development, 112(1): 99-105.
[9] Cai S, Quan S, Yang G, et al.2021. Nutritional status impacts epigenetic regulation in early embryo development: A scoping review[J]. Advances in Nutrition, 12(5): 1877-1892.
[10] Certo M, Llibre A, Lee W, et al.2022. Understanding lactate sensing and signalling[J]. Trends in Endocrinology & Metabolism, 33(10): 722-735.
[11] Dai S K, Liu P P, Li X, et al.2022. Dynamic profiling and functional interpretation of histone lysine crotonylation and lactylation during neural development[J]. Development, 149(14): 10.
[12] Dai W, Wu G, Liu K, et al.2023. Lactate promotes myogenesis via activating H3K9 lactylation-dependent up-regulation of Neu2 expression[J]. Journal of Cachexia Sarcopenia and Muscle, 14(6): 2851-2865.
[13] Dai X, Lv X, Thompson E W, et al.2022. Histone lactylation: Epigenetic mark of glycolytic switch[J]. Trends in Genetics, 38(2): 124-127.
[14] Dong H, Zhang J, Zhang H, et al.2022. YiaC and CobB regulate lysine lactylation in Escherichia coli[J]. Nature Communications, 13(1): 6628.
[15] Ebrahimi M, Forouzesh M, Raoufi S, et al.2020. Differentiation of human induced pluripotent stem cells into erythroid cells[J]. Stem Cell Research & Therapy, 11(1): 483.
[16] Finley L, Gendron J, Miguel-Aliaga I, et al.2023. Integrating the dynamic and energetic fields of metabolism and development[J]. Development, 150(20): dev202424.
[17] Fu Y, Yu J, Li F, et al.2022. Oncometabolites drive tumorigenesis by enhancing protein acylation: From chromosomal remodelling to nonhistone modification[J]. Journal of Experimental & Clinical Cancer Research, 41(1): 144.
[18] Gaffney D O, Jennings E Q, Anderson C C, et al.2020. Non-enzymatic lysine lactoylation of glycolytic enzymes[J]. Cell Chemical Biology, 27(2): 206-213.
[19] Galle E, Wong C W, Ghosh A, et al.2022. H3K18 lactylation marks tissue-specific active enhancers[J]. Genome Biology, 23(1): 207.
[20] Gardner D K.2015. Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion?[J]. Bioessays, 37(4): 364-371.
[21] Gu C, Liu S, Wu Q, et al.2019. Integrative single-cell analysis of transcriptome, DNA methylome and chromatin accessibility in mouse oocytes[J]. Cell Research, 29(2):110-123.
[22] Guo F, Yan L, Guo H, et al.2015. The transcriptome and DNA methylome landscapes of human primordial germ cells[J]. Cell, 161(6): 1437-1452.
[23] He Y, Zheng C C, Yang J, et al.2023. Lysine butyrylation of HSP90 regulated by KAT8 and HDAC11 confers chemoresistance[J]. Cell Discovery, 9(1): 74.
[24] Heintzman N D, Hon G C, Hawkins R D, et al.2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression[J]. Nature, 459(7243): 108-112.
[25] Hu X, Huang X, Yang Y, et al.2024. Dux activates metabolism-lactylation-MET network during early iPSC reprogramming with Brg1 as the histone lactylation reader[J]. Nucleic Acids Research, 52(10): 5529-5548.
[26] Huang H, Zhang D, Wang Y, et al.2018. Lysine benzoylation is a histone mark regulated by SIRT2[J]. Nature Communications, 9(1): 3374.
[27] Hussain S, Aleksic J, Blanco S, et al.2013. Characterizing 5-methylcytosine in the mammalian epitranscriptome[J]. Genome Biology, 14(11): 215.
[28] Ibrahim L, Stanton C, Nutsch K, et al.2023. Succinylation of a KEAP1 sensor lysine promotes NRF2 activation[J]. Cell Chemical Biology, 30(10): 1295-1302.
[29] Jin J, Bai L, Wang D, et al.2023. SIRT3-dependent delactylation of cyclin E2 prevents hepatocellular carcinoma growth[J]. EMBO Reports, 24(5): e56052.
[30] Kebede A F, Nieborak A, Shahidian L Z, et al.2017. Histone propionylation is a mark of active chromatin[J]. Nature Structural & Molecular Biology, 24(12): 1048-1056.
[31] Krisher R L. Bavister B D.1999. Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence[J]. Molecular Reproduction and Development, 53(1): 19-26.
[32] Lane M, Gardner D K.2000. Lactate regulates pyruvate uptake and metabolism in the preimplantation mouse embryo[J]. Biology of Reproduction, 62(1): 16-22.
[33] Latham T, Mackay L, Sproul D, et al.2012. Lactate, a product of glycolytic metabolism, inhibits histone deacetylase activity and promotes changes in gene expression[J]. Nucleic Acids Research, 40(11): 4794-4803.
[34] Lee G S, Kim H S, Hyun S H, et al.2003. Improved developmental competence of cloned porcine embryos with different energy supplements and chemical activation[J]. Molecular Reproduction and Development, 66(1): 17-23.
[35] Lee M, Kim B, Kim V N.2014. Emerging roles of RNA modification: m6A and u-tail[J]. Cell, 158(5): 980-987.
[36] Li J, Hou W, Zhao Q, et al.2024. Lactate regulates major zygotic genome activation by H3K18 lactylation in mammals[J]. National Science Review, 11(2): nwad295.
[37] Li J, Lu L, Liu L, et al.2023. HDAC1/2/3 are major histone desuccinylases critical for promoter desuccinylation[J]. Cell Discovery, 9(1): 85.
[38] Li L, Chen K, Wang T, et al.2020. Glis1 facilitates induction of pluripotency via an epigenome-metabolome-epigenome signalling cascade[J]. Nature Metabolism, 2(9):882-892.
[39] Li L, Sun S, Wu Y, et al.2023. Lactate and protein lactylation: The ugly duckling of energy as the sculpture artist of proteins[J]. Science Bulletin (Beijing), 68(21): 2510-2514.
[40] Liberti M V, Locasale J W.2020. Histone lactylation: A new role for glucose metabolism[J]. Trends in Biochemical Sciences, 45(3): 179-182.
[41] Lin J, Ji Z, Di Z, et al.2022. Overexpression of Tfap2a in mouse oocytes impaired spindle and chromosome organization[J]. International Journal of Molecular Sciences, 23(22): 14376.
[42] Liu C, Wu J, Zhu J, et al.2009. Lactate inhibits lipolysis in fat cells through activation of an orphan G-protein-coupled receptor, GPR81[J]. Journal of Biological Chemistry, 284(5): 2811-2822.
[43] Liu X, Zhang Y, Li W, et al.2022. Lactylation, an emerging hallmark of metabolic reprogramming: current progress and open challenges[J]. Frontiers in Cell and Developmental Biology, 10: 972020.
[44] Calero L M, Marinaro F, Fernández-Hernández P, et al.2024. Characterization of preovulatory follicular fluid secretome and its effects on equine oocytes during in vitro maturation[J]. Research in Veterinary Science, 171:105222,.
[45] Ma L, Gao Z, Wu J, et al.2021. Co-condensation between transcription factor and coactivator p300 modulates transcriptional bursting kinetics[J]. Molecular Cell, 81(8): 1682-1697.
[46] Mahmoud A I.2023. Metabolic switches during development and regeneration[J]. Development, 150(20): edv202008.
[47] Martin B J E, Brind'Amour J, Kuzmin A, et al.2021. Transcription shapes genome-wide histone acetylation patterns[J]. Nature Communications, 12(1): 210.
[48] Mathieu J, Ruohola-Baker H.2017. Metabolic remodeling during the loss and acquisition of pluripotency[J]. Development, 144(4): 541-551.
[49] Merkuri F, Rothstein M, Simoes-Costa M.2024. Histone lactylation couples cellular metabolism with developmental gene regulatory networks[J]. Nature Communications, 15(1): 90.
[50] Milazzotto M P, Ispada J, de Lima C B.2022. Metabolism-epigenetic interactions on in vitro produced embryos[J]. Reproduction Fertility and Development, 35(2): 84-97.
[51] Müller J, Radej J, Horak J, et al.2023. Lactate: The fallacy of oversimplification[J]. Biomedicines, 11(12): 3192.
[52] Nagaraj R, Sharpley M S, Chi F, et al.2017. Nuclear localization of mitochondrial TCA cycle enzymes as a critical step in mammalian zygotic genome activation[J]. Cell, 168(1-2): 210-223.
[53] Neto F T, Bach P V, Najari B B, et al.2016. Spermatogenesis in humans and its affecting factors[J]. Seminars in Cell & Developmental Biology, 59: 10-26.
[54] Niu Z, Chen C, Wang S, et al.2024. HBO1 catalyzes lysine lactylation and mediates histone H3K9la to regulate gene transcription[J]. Nature Communications, 15(1):3561.
[55] Redel B K, Brown A N, Spate L D, et al.2012. Glycolysis in preimplantation development is partially controlled by the Warburg Effect[J]. Molecular Reproduction and Development, 79(4): 262-271.
[56] Roshandel E, Parkhideh S, Ghaffari Nazari H, et al.2021. Pre-and post-transplant serum lactate dehydrogenase levels as a predictive marker for patient survival and engraftment in allogeneic hematopoietic stem cell transplant recipients[J]. Reports of Biochemistry and Molecular Biology, 10(2): 204-215.
[57] Sharpley M S, Chi F, Hoeve J T, et al.2021. Metabolic plasticity drives development during mammalian embryogenesis[J]. Developmental Cell, 56(16): 2329-2347.
[58] Srivastava S, Kumar S, Bhatt R, et al.2023. Lysine acetyltransferases (KATs) in disguise: Diseases implications[J]. Journal of Biochemistry, 173(6): 417-433.
[59] Sun L, Zhang Y, Yang B, et al.2023. Lactylation of METTL16 promotes cuproptosis via m6A-modification on FDX1 mRNA in gastric cancer[J]. Nature Communications, 14(1): 6523.
[60] Tian Q. Zhou L Q.2022. Lactate activates germline and cleavage embryo genes in mouse embryonic stem cells[J]. Cells, 11(3): 548.
[61] Tomczak W, Winkler-Lach W, Tomczyk-Socha M, et al.2023. Advancements in ocular regenerative therapies[J]. Biology-Basel, 12(5): 737.
[62] Uysal F, Ozturk S, Akkoyunlu G.2017. DNMT1, DNMT3A and DNMT3B proteins are differently expressed in mouse oocytes and early embryos[J]. Journal of Molecular Histology, 48(5-6): 417-426.
[63] Vander Heiden M G, Cantley L C, Thompson C B.2009. Understanding the Warburg effect: The metabolic requirements of cell proliferation[J]. Science, 324(5930):1029-1033.
[64] Venturas M, Shah J S, Yang X, et al.2022. Metabolic state of human blastocysts measured by fluorescence lifetime imaging microscopy[J]. Human Reproduction, 37(3): 411-427.
[65] Watson A J, Natale D R, Barcroft L C.2004. Molecular regulation of blastocyst formation[J]. Animal Reproduction Science, 82-83: 583-592.
[66] Wei W, Liu X, Chen J, et al.2017. Class I histone deacetylases are major histone decrotonylases: Evidence for critical and broad function of histone crotonylation in transcription[J]. Cell Research, 27(7): 898-915.
[67] Wei Y, Pan B, Qin J, et al.2024. The walnut-derived peptide TW-7 improves mouse parthenogenetic embryo development of vitrified MⅡ oocytes potentially by promoting histone lactylation[J]. Journal of Animal Science and Biotechnology, 15(1): 86.
[68] Wilding M, Fiorentino A, De Simone M L, et al.2002. Energy substrates, mitochondrial membrane potential and human preimplantation embryo division[J]. Reproductive Biomedicine Online, 5(1): 39-42.
[69] Wu Y, Chen Z, Xie G, et al.2022. RNA m1A methylation regulates glycolysis of cancer cells through modulating ATP5D[J]. Proceedings of the National Academy of Sciences of the USA, 119(28): e2119038119.
[70] Xie B, Zhang M, Li J, et al.2024. KAT8-catalyzed lactylation promotes eEF1A2-mediated protein synthesis and colorectal carcinogenesis[J]. Proceedings of the National Academy of Sciences of the USA, 121(8): e2314128121.
[71] Xie Y, Hu H, Liu M, et al.2022. The role and mechanism of histone lactylation in health and diseases[J]. Frontiers in Genetics, 13: 949252.
[72] Xin Q, Wang H, Li Q, et al.2022. Lactylation: A passing fad or the future of posttranslational modification[J]. Inflammation, 45(4): 1419-1429.
[73] Xu R, Li C, Liu X, et al.2021. Insights into epigenetic patterns in mammalian early embryos[J]. Protein & Cell, 12(1): 7-28.
[74] Yang F, Li B, Yang Y, et al.2019. Leptin enhances glycolysis via OPA1-mediated mitochondrial fusion to promote mesenchymal stem cell survival[J]. International Journal of Molecular Medicine, 44(1): 301-312.
[75] Yang Q, Liu J, Wang Y, et al.2022. A proteomic atlas of ligand-receptor interactions at the ovine maternal-fetal interface reveals the role of histone lactylation in uterine remodeling[J]. Journal of Biological Chemistry, 298(1):101456.
[76] Yang W, Wang P, Cao P, et al.2021. Hypoxic in vitro culture reduces histone lactylation and impairs pre-implantation embryonic development in mice[J]. Epigenetics & Chromatin, 14(1): 57.
[77] Yang Y H, Wang Q C, Kong J, et al.2023. Global profiling of lysine lactylation in human lungs[J]. Proteomics, 23(15): e2200437.
[78] Yi X D, Zhanf Y N, Xiao S, et al.2019. Role and regulatory mechanism of glycometabolism of Sertoli cells in spermatogenesis[J]. National Journal of Andrology, 25(10): 923-927.
[79] Yu J, Chai P, Xie M, et al.2021. Histone lactylation drives oncogenesis by facilitating m6A reader protein YTHDF2 expression in ocular melanoma[J]. Genome Biology, 22(1): 85.
[80] Yu S, Zhou C, He J, et al.2022. BMP4 drives primed to naïve transition through PGC-like state[J]. Nature Communications, 13(1): 2756.
[81] Zhang D, Tang Z, Huang H, et al.2019. Metabolic regulation of gene expression by histone lactylation[J]. Nature, 574(7779): 575-580.
[82] Zhang X, Liu Y, Wang N.2024. Multifaceted roles of histone lysine lactylation in meiotic gene dynamics and recombination[J]. BioRxiv, 12: 5827.
[83] Zhang X, Mao Y, Wang B, et al.2019. Screening, expression, purification and characterization of CoA-transferases for lactoyl-CoA generation[J]. Journal of Industrial Microbiology & Biotechnology, 46(7): 899-909.
[84] Zhang Y, Sun Z, Jia J, et al.2021. Overview of histone modification[J]. Advances in Experimental Medicine and Biology, 1283: 1-16.
[85] Zhao J, Yao K, Yu H, et al.2021. Metabolic remodelling during early mouse embryo development[J]. Nature Metabolism, 3(10): 1372-1384.
[86] Zhao S S, Liu J, Wu Q C, et al.2023. Role of histone lactylation interference RNA m6A modification and immune microenvironment homeostasis in pulmonary arterial hypertension[J]. Frontiers in Cell and Developmental Biology, 11: 1268646.
[87] Zong Z, Xie F, Wang S, et al.2024. Alanyl-tRNA synthetase, AARS1, is a lactate sensor and lactyltransferase that lactylates p53 and contributes to tumorigenesis[J]. Cell, 187(10): 2375-2392.
[88] Zu H, Li C, Dai C, et al.2022. SIRT2 functions as a histone delactylase and inhibits the proliferation and migration of neuroblastoma cells[J]. Cell Discovery, 8(1): 54. |
|
|
|
