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| Research Progress on Improvement in Development of Porcine Somatic Cell Nuclear Transfer Embryos by Histone Deacetylase Inhibitors |
| YAN Chao1,2, CHEN Zhi-Long2, PENG Cui-Ting2, XIE Hao2, ZHANG Cai-Yong2, ZHAO Yu-Lan2, QI Lin2, LIU Yong-Gang1,*, TANG Zhong-Lin2,3,4,5,* |
1 College of Animal Science and Technology, Yunnan Agricultural University, Kunming 650201, China;
2 Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, China;
3 Kunpeng Institute of Modern Agriculture at Foshan, Foshan 528226, China;
4 Shenzhen Branch Center of Guangdong Laboratory of Lingnan Modern Agricultural Science and Technology, Shenzhen 518000, China;
5 Key Laboratory of Livestock and Poultry Biohistology, Ministry of Agriculture and Rural Development, Shenzhen 518000, China |
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Abstract Somatic cell nuclear transfer (SCNT) has been widely used in protecting endangered species, propagating better varieties and treating diseases. Histone acetylase is an important epigenetic mark regulating the development of early embryo in pig (Sus scrofa), and its correct obliteration and reconstruction are the basis of the embryonic development. With the development of low input next generation sequencing, many studies found that a variety of abnormal epigenetic modification have been found during the reprogramming of somatic cell nuclear transfer embryos. Histone acetylase modification is an important factor that leads to the development block of porcine somatic cell nuclear transfer embryos. In recent years, some small molecule compounds of histone deacetylase inhibitors have been gradually discovered for the improvement of abnormal modification level of histone acetylase during embryonic development. This paper reviews the studies of the effects and mechanisms of histone deacetylase inhibitors on the development of porcine somatic cell nuclear transfer embryos, which provides reference for improving the cloning efficiency in pig.
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Received: 14 April 2024
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Corresponding Authors:
* tangzhonglin@caas.cn;Liuyg4567@163.com
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[1] 孙俊铭, 崔奎青, 李志鹏, 等. 2018. SAHA处理对猪手工克隆胚胎体外发育潜能的影响[J]. 黑龙江畜牧兽医, (05):104-108.
(Sun J M, Cui K Q, Li Z P, et al. 2018. Effects of SAHA on the developmental potential of porcine handmade cloned embryos in vitro[J]. Heilongjiang Animal Science and Veterinary Medicine, (05):104-108.)
[2] 周娜汝. 2013. 猪体细胞克隆胚胎着床前发育期间H3K27乙酰化重编程规律研究[D]. 硕士学位论文, 安徽农业大学, 导师: 张运海, pp. 36-41.
(Zhou N N.2013. Reprogramming dynamics of histone H3 lysine 27 acetylation during pre-implantation of pig somatic cloned embryos[D]. Thesis for M.S., Anhui Agricultural University, Supervisor: Zhang Y H, pp. 36-41.)
[3] Agrawal H, Selokar N L, Saini M, et al.2018a. Epigenetic alteration of donor cells with histone deacetylase inhibitor m-carboxycinnamic acid bishydroxymide improves the in vitro developmental competence of buffalo (Bubalus bubalis) cloned embryos[J]. Cellular Reprogramming, 20(1): 76-88.
[4] Agrawal H, Selokar N L, Saini M, et al.2018b. m-carboxycinnamic acid bishydroxamide improves developmental competence, reduces apoptosis and alters epigenetic status and gene expression pattern in cloned buffalo (Bubalus bubalis) embryos[J]. Reproduction in Domestic Animals, 53(4): 986-996.
[5] Avery L B, Bumpus N N.2014. Valproic acid is a novel activator of AMP-activated protein kinase and decreases liver mass, hepatic fat accumulation, and serum glucose in obese mice[J]. Molecular Pharmacology, 85(1): 1-10.
[6] Bali P, George P, Cohen P, et al.2004. Superior activity of the combination of histone deacetylase inhibitor LAQ824 and the FLT-3 kinase inhibitor PKC412 against human acute myelogenous leukemia cells with mutant FLT-3[J]. Clinical Cancer Research, 10(15): 4991-4997.
[7] Bass A, El-zoghbi M S, Nageeb E M, et al. 2021. Comprehensive review for anticancer hybridized multitargeting HDAC inhibitors[J]. European Journal of Medicinal Chemistry, 2021: 209112904.
[8] Buckton L K, Rahimi M N, Mcalpine S R.2021. Cyclic peptides as drugs for intracellular targets: The next frontier in peptide therapeutic development[J]. Chemistry, 27(5): 1487-1513.
[9] Buggy J J, Cao Z A, Bass K E, et al.2006. CRA-024781: A novel synthetic inhibitor of histone deacetylase enzymes with antitumor activity in vitro and in vivo[J]. Molecular Cancer Therapeutics, 5(5): 1309-1317.
[10] Bui H T, Wakayama S, Kishigami S, et al.2010. Effect of trichostatin A on chromatin remodeling, histone modifications, DNA replication, and transcriptional activity in cloned mouse embryos[J]. Biology of Reproduction, 83(3): 454-463.
[11] Catley L, Weisberg E, Tai Y T, et al.2003. NVP-LAQ824 is a potent novel histone deacetylase inhibitor with significant activity against multiple myeloma[J]. Blood, 102(7): 2615-2622.
[12] Cervera R P, Marti-Gutierrez N, Escorihuela E, et al.2009. Trichostatin A affects histone acetylation and gene expression in porcine somatic cell nucleus transfer embryos[J]. Theriogenology, 72(8):1097-1100.
[13] Cong P, Zhu K, Ji Q, et al.2013. Effects of trichostatin A on histone acetylation and methylation characteristics in early porcine embryos after somatic cell nuclear transfer[J]. Animal Science Journal, 84(9): 639-649.
[14] Cousens L S, Gallwitz D, Alberts B M.1979. Different accessibilities in chromatin to histone acetylase[J]. Journal of Biological Chemistry, 254(5): 1716-1723.
[15] de Macedo M P, Glanzenr W G, Gutierrez K, et al.2022. Simultaneous inhibition of histone deacetylases and RNA synthesis enables totipotency reprogramming in pig SCNT embryos[J]. Journal of Biological Chemistry, 23(22): 14142.
[16] Dokmanovic M, Marks P A.2005. Prospects: Histone deacetylase inhibitors[J]. Journal of Cellular Biochemistry, 96(2): 293-304.
[17] Emmett M J, Lazar M A.2019. Integrative regulation of physiology by histone deacetylase[J]. Nature Reviews Molecular Cell Biology, 20(2): 102-115.
[18] Fang X, Xia W, Cao H, et al.2020. Effect of supplementation of Zebularine and Scriptaid on efficiency of in vitro developmental competence of ovine somatic cell nuclear transferred embryos[J]. Animal Biotechnology, 31(2): 155-163.
[19] Feng R, Oton A, Mapara M Y, et al.2007. The histone deacetylase inhibitor, PXD101, potentiates bortezomib-induced anti-multiple myeloma effect by induction of oxidative stress and DNA damage[J]. British Journal of Haematology, 139(3): 385-397.
[20] Feng T, Qi X, Zou H, et al.2022. TSA activates pluripotency factors in porcine recloned embryos[J]. Genes (Basel), 13(4): 649.
[21] Fournel M, Bonfits C, Hou Y, et al.2008. MGCD0103, a novel isotype-selective histone deacetylase inhibitor, has broad spectrum antitumor activity in vitro and in vivo[J]. Molecular Cancer Therapeutics, 7(4): 759-768.
[22] Hrzenjak A, Moinfar F, Kremser M L.et al.2010. Histone deacetylase inhibitor vorinostat suppresses the growth of uterine sarcomas in vitro and in vivo[J]. Molecular Cancer, 2010: 949.
[23] Huber K, Doyon G, Plaks J, et al.2011. Inhibitors of histone deacetylases: Correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells[J]. Journal of Biological Chemistry, 286(25): 22211-22218.
[24] Jackson B L, Shafique S, Natale B V, et al.2024. Investigating the effects of valproic acid on placental epigenetic modifications and development in the CD-1 mouse model[J]. Reproductive Toxicology, 124: 108551.
[25] Jeong P S, Yang H J, Park S H, et al.2021. Combined chaetocin/trichostatin A treatment improves the epigenetic modification and developmental competence of porcine somatic cell nuclear transfer embryos[J]. Frontiers in Cell and Developmental Biology, 9: 709574.
[26] Jin J X, Kang J D, Li S, et al.2015. PXD101 significantly improves nuclear reprogramming and the in vitro developmental competence of porcine SCNT embryos[J]. Biochemical and Biophysical Research Communications, 456(1): 156-161.
[27] Jin J X, Lee S, Taweechaipaisankul A, et al.2017a. The HDAC inhibitor LAQ824 enhances epigenetic reprogramming and in vitro development of porcine SCNT embryos[J]. Cellular Physiology and Biochemistry, 41(3): 1255-1266.
[28] Jin J X, Li S, Gao Q S, et al.2013. Significant improvement of pig cloning efficiency by treatment with LBH589 after somatic cell nuclear transfer[J]. Theriogenology, 80(6): 630-635.
[29] Jin J X, Li S, Hong Y, et al.2014. CUDC-101, a histone deacetylase inhibitor, improves the in vitro and in vivo developmental competence of somatic cell nuclear transfer pig embryos[J]. Theriogenology, 81(4): 572-578.
[30] Jin L, Guo Q, Zhu H Y, et al.2017b. Histone deacetylase inhibitor M344 significantly improves nuclear reprogramming, blastocyst quality, and in vitro developmental capacity of cloned pig embryos[J]. Journal of Animal Science, 95(3): 1388-1395.
[31] Jin L, Zhu H Y, Guo Q, et al.2017c. Effect of histone acetylation modification with MGCD0103, a histone deacetylase inhibitor, on nuclear reprogramming and the developmental competence of porcine somatic cell nuclear transfer embryos[J]. Theriogenology, 87: 298-305.
[32] Jin L, Zhu H Y, Guo Q, et al.2016. PCI-24781 can improve in vitro and in vivo developmental capacity of pig somatic cell nuclear transfer embryos[J]. Biotechnology Letters, 38(9): 1433-1441.
[33] Kang J, Li S, Lu Y, et al.2013. Valproic acid improved in vitro development of pig cloning embryos but did not improve survival of cloned pigs to adulthood[J]. Theriogenology, 79(2): 306-311. e1.
[34] Katusic-Bojanac A, Plazibat M, Himelreich-Peric M, et al.2022. Valproate targets mammalian gastrulation impairing neural tissue differentiation and development of the placental source in vitro[J]. International Journal of Molecular Sciences, 23(16): 8861.
[35] Knoche S M, Brumfield G L, Goetz B T, et al.2022. The histone deacetylase inhibitor M344 as a multifaceted therapy for pancreatic cancer[J]. PLOS ONE, 17(9): e0273518.
[36] Legoff L, Dali O, De La Mata S E, et al.2021. Histone deacetylase inhibition leads to regulatory histone mark alterations and impairs meiosis in oocytes[J]. Epigenetics Chromatin, 14(1): 39.
[37] Li G, Zhang X, Wang H, et al.2020. Increasing CRISPR/Cas9-mediated homology-directed DNA repair by histone deacetylase inhibitors[J]. International Journal of Biochemistry & Cell Biology, 125: 105790.
[38] Li J, Svarcova O, Viliemoes K, et al.2008. High in vitro development after somatic cell nuclear transfer and trichostatin A treatment of reconstructed porcine embryos[J]. Theriogenology, 70(5): 800-808.
[39] Li W, Zheng H, Yang Y, et al.2022. A diverse English keyword search reveals the value of scriptaid treatment for porcine embryo development following somatic cell nuclear transfer[J]. Reproduction, Fertility and Development, 34(11): 798-803.
[40] Li Y, Seto E.2016. HDACs and HDAC inhibitors in cancer development and therapy[J]. Cold Spring Harbor perspectives in medicine, 6(10): a026831.
[41] Lin T, Sun L, Lee J E, et al2020. Changes of histone H3 lysine 23 acetylation and methylation in porcine somatic cells, oocytes and preimplantation embryos[J]. Theriogenology, 148: 162-173.
[42] Liu L, Liu Y, Gao F, et al.2012a. Embryonic development and gene expression of porcine SCNT embryos treated with sodium butyrate[J]. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 318(3): 224-334.
[43] Liu L, Song G, Gao F, et al.2012b. Transient exposure to sodium butyrate after germinal vesicle breakdown improves meiosis but not developmental competence in pig oocytes[J]. Cell Biology International, 36(5): 483-490.
[44] Liu Z, Cai Y, Wang Y, et al.2018. Cloning of macaque monkeys by somatic cell nuclear transfer[J]. Cell, 172(4): 881-887.e7.
[45] Luo Z B, Jin L, Guo Q, et al.2018. Cotreatment with RepSox and LBH589 improves the in vitro developmental competence of porcine somatic cell nuclear transfer embryos[J]. Reproduction, Fertility and Development, 30(10): 1342-1351.
[46] Mao J, Zhao M T, Whitworth K M, et al.2015. Oxamflatin treatment enhances cloned porcine embryo development and nuclear reprogramming[J]. Cellular Reprogramming, 17(1): 28-40.
[47] Matoba S, Zhang Y.2018. Somatic cell nuclear transfer reprogramming: Mechanisms and applications[J]. Cell Stem Cell, 23(4): 471-485.
[48] Mcclure J J, Li X, Chou C J.2018. Advances and challenges of HDAC inhibitors in cancer therapeutics[J]. Advances in Cancer Research, 138: 183-211.
[49] Meissner A, Jaenisch R.2006. Mammalian nuclear transfer[J]. Developmental Dynamics, 23(9): 2460-2469.
[50] Miyoshi K, Mori H, Mizobe Y, et al.2010. Valproic acid enhances in vitro development and Oct-3/4 expression of miniature pig somatic cell nuclear transfer embryos[J]. Cellular Reprogramming, 12(1): 67-74.
[51] Oogura A, Inoue K, Wakayama T.2013. Recent advancements in cloning by somatic cell nuclear transfer[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1609): 20110329.
[52] Park S J, Park H J, Koo O J, et al.2012. Oxamflatin improves developmental competence of porcine somatic cell nuclear transfer embryos[J]. Cellular Reprogramming, 14(5): 398-406.
[53] Plumb J A, Finn P W, Williams R J, et al.2003. Pharmacodynamic response and inhibition of growth of human tumor xenografts by the novel histone deacetylase inhibitor PXD101[J]. Molecular Cancer Therapeutics, 2(8): 721-728.
[54] Qiu X, Li N, Xiao X, et al.2017. Effects of embryo aggregation and PXD101 on the in vitro development of mouse somatic cell nuclear transfer embryos[J]. Cellular Reprogramming, 19(6): 337-343.
[55] Qiu X, Xiao X, Ren A, et al.2020. Effects of PXD101 and embryo aggregation on the in vitro development of mouse parthenogenetic embryos[J]. Cellular Reprogramming, 22(1): 14-21.
[56] Richon V M, Emiliani S, Verdin E, et al.1998. A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases[J]. Proceedings of the National Academy of Sciences of the USA, 95(6): 3003-3007.
[57] Ruan D, Peng J, Wang X, et al.2018. XIST derepression in active X chromosome hinders pig somatic cell nuclear transfer[J]. Stem Cell Reports, 10(2): 494-508.
[58] Samiec M, Romanek J, Lipinski D, et al.2019. Expression of pluripotency-related genes is highly dependent on trichostatin A‐assisted epigenomic modulation of porcine mesenchymal stem cells analysed for apoptosis and subsequently used for generating cloned embryos[J]. Animal Science Journal, 90(9): 1127-1141.
[59] Scuto A, Kirschbaum M, Kowolik C, et al.2008. The novel histone deacetylase inhibitor, LBH589, induces expression of DNA damage response genes and apoptosis in Ph-acute lymphoblastic leukemia cells[J]. Blood, 111(10): 5093-5100.
[60] Shao R, Suzuki T, Suyama M, et al.2024. The impact of selective HDAC inhibitors on the transcriptome of early mouse embryos[J]. BMC Genomics, 25(1): 143.
[61] Song Y, Hai T, Wang Y, et al.2014. Epigenetic reprogramming, gene expression and in vitro development of porcine SCNT embryos are significantly improved by a histone deacetylase inhibitor--m-carboxycinnamic acid bishydroxamide (CBHA)[J]. Protein Cell, 5(5): 382-393.
[62] Su G H, Sohn T A, Ryu B, et al.2000. A novel histone deacetylase inhibitor identified by high-throughput transcriptional screening of a compound library[J]. Cancer Research, 60(12): 3137-3142.
[63] Sun H, Mediwala S N, Szafran A T, et al.2016. CUDC-101, a novel inhibitor of full-length androgen receptor (flAR) and androgen receptor variant 7 (AR-V7) activity: Mechanism of action and in vivo efficacy[J]. Hormones & Cancer, 7(3): 196-210.
[64] Sun J M, Cui K Q, Li Z P, et al.2017. Suberoylanilide hydroxamic acid, a novel histone deacetylase inhibitor, improves the development and acetylation level of miniature porcine handmade cloning embryos[J]. Reproduction in Domestic Animals, 52(5): 763-774.
[65] Vigushin D M, Ali S, Pace P E, et al.2001. Trichostatin A is a histone deacetylase inhibitor with potent antitumor activity against breast cancer in vivo[J]. Clinical Cancer Research, 7(4): 971-976.
[66] Volmar C H, Salah-Uddin H, Janczura K J, et al.2017. M344 promotes nonamyloidogenic amyloid precursor protein processing while normalizing Alzheimer's disease genes and improving memory[J]. Proceedings of the National Academy of Sciences of the USA, 114(43): E9135-E9144.
[67] Wang X F, Xie S M, Guo S M, et al.2020. Dynamic pattern of histone H3 core acetylation in human early embryos[J]. Cell Cycle, 19(17): 2226-2234.
[68] Wood M, Rymarchyk S, Zheng S, et al.2018. Trichostatin A inhibits deacetylation of histone H3 and p53 by SIRT6[J]. Archives of Biochemistry and Biophysics, 638: 8-17.
[69] Wu K, Fan D, Zhao H, et al.2023. Dynamics of histone acetylation during human early embryogenesis[J]. Cell Discovery, 9(1): 29.
[70] Xu W S, Parmigiani R B, Marks P A.2007. Histone deacetylase inhibitors: Molecular mechanisms of action[J]. Oncogene, 26(37): 5541-5552.
[71] Yang G, Zhang L, Liu W, et al.2021. Dux-Mediated corrections of aberrant H3K9ac during 2-cell genome activation optimize efficiency of somatic cell nuclear transfer[J]. Cell Stem Cell, 28(1): 150-163.e5.
[72] Yang Y, Jia W, Luo Z, et al.2024. VGLL1 cooperates with TEAD4 to control human trophectoderm lineage specification[J]. Nature Communications, 15(1): 583.
[73] Yoon S, Eom G H.2016. HDAC and HDAC inhibitor: From cancer to cardiovascular diseases[J]. Chonnam Medical Journal, 52(1): 1-11.
[74] Yu M F, Wang J L, Yi J M., et al.2019. Sodium butyrate interrupts the maturation of oocytes and enhances the development of preimplantation embryos[J]. PLOS ONE, 14(7): e0220479.
[75] Zarei M, Shamaghdari B, Vahabi Z, et al.2022. Epigenetic reprogramming in cloned mouse embryos following treatment with DNA methyltransferase and histone deacetylase inhibitors[J]. Systems Biology in Reproductive Medicine, 68(3): 227-238.
[76] Zhao C, Dong H, Xu Q, et al.2020. Histone deacetylase (HDAC) inhibitors in cancer: a patent review[J]. Expert Opinion on Therapeutic Patents, 30(4): 263-274.
[77] Zhao J, Hao Y, Ross J W, et al.2010. Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos[J]. Cellular Reprogramming, 12(1): 75-83.
[78] Zhao L, Long C, Zhao G, et al.2022. Reprogramming barriers in bovine cells nuclear transfer revealed by single-cell RNA-seq analysis[J]. Journal of Cellular and Molecular Medicine, 26(18): 4792-4804.
[79] Zhou N, Cao Z, Wu R, et al.2014. Dynamic changes of histone H3 lysine 27 acetylation in pre-implantational pig embryos derived from somatic cell nuclear transfer[J]. Animal Reproduction Science, 148(3-4): 153-163. |
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