Differential effects of trichostatin A on mouse embryogenesis and development

in Reproduction
Authors:
Cheng Peng Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, First Hospital, Jilin University, Changchun, China

Search for other papers by Cheng Peng in
Current site
Google Scholar
PubMed
Close
,
Zhuo Lv New Hope Fertility Center, New York, USA

Search for other papers by Zhuo Lv in
Current site
Google Scholar
PubMed
Close
,
Tang Hai State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Chaoyang, Beijing, China

Search for other papers by Tang Hai in
Current site
Google Scholar
PubMed
Close
,
Xiangpeng Dai Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, First Hospital, Jilin University, Changchun, China

Search for other papers by Xiangpeng Dai in
Current site
Google Scholar
PubMed
Close
, and
Qi Zhou Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, First Hospital, Jilin University, Changchun, China
State Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Chaoyang, Beijing, China

Search for other papers by Qi Zhou in
Current site
Google Scholar
PubMed
Close

Correspondence should be addressed to X Dai or Q Zhou; Email: daixiangpeng@jlu.edu.cn or zhouqi@ioz.ac.cn
Restricted access
Rent on DeepDyve

Sign up for journal news

Trichostatin A (TSA), a histone deacetylase (HDAC) inhibitor, can significantly improve the reprogramming efficiency of somatic cells. However, whether TSA has a detrimental effect on other kinds of embryos is largely unknown because of the lack of integrated analysis of the TSA effect on natural fertilized embryos. To investigate the effect of TSA on mouse embryo development, we analyzed preimplantation and post-implantation development of in vivo, in vitro fertilized, and parthenogenetic embryos treated with TSA at different concentrations and durations. In vivo fertilized embryos appeared to be the most sensitive to TSA treatment among the three groups, and the blastocyst formation rate decreased sharply as TSA concentration and treatment time increased. TSA treatment also reduced the livebirth rate for in vivo fertilized embryos from 56.59 to 38.33% but did not significantly affect postnatal biological functions such as the pups’ reproductive performance and their ability for spatial learning and memory. Further analysis indicated that the acetylation level of H3K9 and H4K5 was enhanced by TSA treatment at low concentrations, while DNA methylation appeared to be also disturbed by TSA treatment only at high concentration. Thus, our data indicates that TSA has different effects on preimplantation embryonic development depending on the nature of the embryo’s reproductive origin, the TSA concentration and treatment time, whereas the effect of TSA at the indicated concentration on postnatal function was minor.

 

  • Collapse
  • Expand
  • Akiyama T, Nagata M & Aoki F 2006 Inadequate histone deacetylation during oocyte meiosis causes aneuploidy and embryo death in mice. PNAS 103 73397344. (https://doi.org/10.1073/pnas.0510946103)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Aoki E & Schultz RM 1999 DNA replication in the 1-cell mouse embryo: stimulatory effect of histone acetylation. Zygote 7 165172. (https://doi.org/10.1017/s0967199499000532)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Azuma R, Miyamoto K, Oikawa M, Yamada M & Anzai M 2018 Combinational treatment of trichostatin A and vitamin C improves the efficiency of cloning mice by somatic cell nuclear transfer. Journal of Visualized Experiments: JoVE 134 57036. (https://doi.org/10.3791/57036)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chang HY, Xie RX, Zhang L, Fu LZ, Zhang CT, Chen HH, Wang ZQ, Zhang Y & Quan FS 2019 Overexpression of miR-101-2 in donor cells improves the early development of Holstein cow somatic cell nuclear transfer embryos. Journal of Dairy Science 102 46624673. (https://doi.org/10.3168/jds.2018-15072)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Chen H, Zhang L, Guo Z, Wang Y, He R, Qin Y, Quan F & Zhang Y 2015 Improving the development of early bovine somatic-cell nuclear transfer embryos by treating adult donor cells with vitamin C. Molecular Reproduction and Development 82 867879. (https://doi.org/10.1002/mrd.22531)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Dai X, Hao J, Hou XJ, Hai T, Fan Y, Yu Y, Jouneau A, Wang L & Zhou Q 2010 Somatic nucleus reprogramming is significantly improved by m-carboxycinnamic acid bishydroxamide, a histone deacetylase inhibitor. Journal of Biological Chemistry 285 3100231010. (https://doi.org/10.1074/jbc.M110.136085)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Enright BP, Kubota C, Yang X & Tian XC 2003 Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2'-deoxycytidine. Biology of Reproduction 69 896901. (https://doi.org/10.1095/biolreprod.103.017954)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Falkenberg KJ & Johnstone RW 2014 Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nature Reviews: Drug Discovery 13 673691. (https://doi.org/10.1038/nrd4360)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Frew AJ, Johnstone RW & Bolden JE 2009 Enhancing the apoptotic and therapeutic effects of HDAC inhibitors. Cancer Letters 280 125133. (https://doi.org/10.1016/j.canlet.2009.02.042)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gao R, Wang C, Gao Y, Xiu W, Chen J, Kou X, Zhao Y, Liao Y, Bai D & Qiao Z et al.2018 Inhibition of aberrant DNA Re-methylation improves post-implantation development of somatic cell nuclear transfer embryos. Cell Stem Cell 23 426435.e5. (https://doi.org/10.1016/j.stem.2018.07.017)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gurvich N, Berman MG, Wittner BS, Gentleman RC, Klein PS & Green JB 2005 Association of valproate-induced teratogenesis with histone deacetylase inhibition in vivo. FASEB Journal 19 11661168. (https://doi.org/10.1096/fj.04-3425fje)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hai T, Hao J, Wang L, Jouneau A & Zhou Q 2011 Pluripotency maintenance in mouse somatic cell nuclear transfer embryos and its improvement by treatment with the histone deacetylase inhibitor TSA. Cell Reprogram 13 475. (https://doi.org/10.1089/cell.2010.0042)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Huang J, Zhang H, Yao J, Qin G, Wang F, Wang X, Luo A, Zheng Q, Cao C & Zhao J 2016 BIX-01294 increases pig cloning efficiency by improving epigenetic reprogramming of somatic cell nuclei. Reproduction 151 3949. (https://doi.org/10.1530/REP-15-0460)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Inoue K, Oikawa M, Kamimura S, Ogonuki N, Nakamura T, Nakano T, Abe K & Ogura A 2015 Trichostatin A specifically improves the aberrant expression of transcription factor genes in embryos produced by somatic cell nuclear transfer. Scientific Reports 5 10127. (https://doi.org/10.1038/srep10127)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kelly WK, O'Connor OA & Marks PA 2002 Histone deacetylase inhibitors: from target to clinical trials. Expert Opinion on Investigational Drugs 11 16951713. (https://doi.org/10.1517/13543784.11.12.1695)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kim EY, Park MJ, Park HY, Noh EJ, Noh EH, Park KS, Lee JB, Jeong CJ, Riu KZ & Park SP 2012 Improved cloning efficiency and developmental potential in bovine somatic cell nuclear transfer with the oosight imaging system. Cell Reprogram 14 305311. (https://doi.org/10.1089/cell.2011.0103)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kim G, Roy PK, Fang X, Hassan BM & Cho J 2019 Improved preimplantation development of porcine somatic cell nuclear transfer embryos by caffeine treatment. Journal of Veterinary Science 20 e31. (https://doi.org/10.4142/jvs.2019.20.e31)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kishigami S, Mizutani E, Ohta H, Hikichi T, Thuan NV, Wakayama S, Bui H-T & Wakayama T 2006 aSignificant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochemical and Biophysical Research Communications 340 183189. (https://doi.org/10.1016/j.bbrc.2005.11.164)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kishigami S, Ohta H, Mizutani E, Wakayama S, Bui H-T, Thuan NV, Hikichi T, Suetsugu R & Wakayama T 2006 bHarmful or not: trichostatin A treatment of embryos generated by ICSI or ROSI. Central European Journal of Biology 1 376385.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ma P & Schultz RM 2008 Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Developmental Biology 319 110120. (https://doi.org/10.1016/j.ydbio.2008.04.011)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ma J, Svoboda P, Schultz RM & Stein P 2001 Regulation of zygotic gene activation in the preimplantation mouse embryo: global activation and repression of gene expression. Biology of Reproduction 64 17131721. (https://doi.org/10.1095/biolreprod64.6.1713)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Marks PA, Miller T & Richon VM 2003 Histone deacetylases. Current Opinion in Pharmacology 3 344351. (https://doi.org/10.1016/s1471-4892(0300084-5)

  • Mei S, Ho AD & Mahlknecht U 2004 Role of histone deacetylase inhibitors in the treatment of cancer. International Journal of Oncology 25 15091519. (https://doi.org/10.3892/ijo.25.6.1509)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Menegola E, Di Renzo F, Broccia ML, Prudenziati M, Minucci S, Massa V & Giavini E 2005 Inhibition of histone deacetylase activity on specific embryonic tissues as a new mechanism for teratogenicity. Birth Defects Research: Part B, Developmental and Reproductive Toxicology 74 392398. (https://doi.org/10.1002/bdrb.20053)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Morales Torres C, Wu MY, Hobor S, Wainwright EN, Martin MJ, Patel H, Grey W, Gronroos E, Howell S & Carvalho J et al.2020 Selective inhibition of cancer cell self-renewal through a Quisinostat-histone H1.0 axis. Nature Communications 11 1792. (https://doi.org/10.1038/s41467-020-15615-z)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Morris R 1984 Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods 11 4760. (https://doi.org/10.1016/0165-0270(8490007-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ogura A, Inoue K, Takano K, Wakayama T & Yanagimachi R 2000 Birth of mice after nuclear transfer by electrofusion using tail tip cells. Molecular Reproduction and Development 57 5559. (https://doi.org/10.1002/1098-2795(200009)57:1<55::AID-MRD8>3.0.CO;2-W)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Papaioannou VE & Ebert KM 1988 The preimplantation pig embryo: cell number and allocation to trophectoderm and inner cell mass of the blastocyst in vivo and in vitro. Development 102 793803. (https://doi.org/10.1242/dev.102.4.793)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Qiu X, You H, Xiao X, Li N & Li Y 2017 Effects of trichostatin A and PXD101 on the in vitro development of mouse somatic cell nuclear transfer embryos. Cell Reprogram 19 19. (https://doi.org/10.1089/cell.2016.0030)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rybouchkin A, Kato Y & Tsunoda Y 2006 Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biology of Reproduction 74 10831089. (https://doi.org/10.1095/biolreprod.105.047456)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Saini M, Selokar NL, Revey T, Singla SK, Chauhan MS, Palta P & Madan P 2014 Trichostatin A alters the expression of cell cycle controlling genes and microRNAs in donor cells and subsequently improves the yield and quality of cloned bovine embryos in vitro. Theriogenology 82 10361042. (https://doi.org/10.1016/j.theriogenology.2014.07.027)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Santos F, Peters AH, Otte AP, Reik W & Dean W 2005 Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Developmental Biology 280 225236. (https://doi.org/10.1016/j.ydbio.2005.01.025)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Song X, Wu JQ, Yu XF, Yang XS & Yang Y 2018 Trichostatin a inhibits proliferation of triple negative breast cancer cells by inducing cell cycle arrest and apoptosis. Neoplasma 65 898906. (https://doi.org/10.4149/neo_2018_181212N476)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Spinaci M, Seren E & Mattioli M 2004 Maternal chromatin remodeling during maturation and after fertilization in mouse oocytes. Molecular Reproduction and Development 69 215221. (https://doi.org/10.1002/mrd.20117)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Szyf M 2005 DNA methylation and demethylation as targets for anticancer therapy. Biochemistry. Biokhimiia 70 533549. (https://doi.org/10.1007/s10541-005-0147-7)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tonegawa S, Li Y, Erzurumlu RS, Jhaveri S, Chen C, Goda Y, Paylor R, Silva AJ, Kim JJ & Wehner JM 1995 The gene knockout technology for the analysis of learning and memory, and neural development. Progress in Brain Research 105 314. (https://doi.org/10.1016/s0079-6123(0863279-3)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tsuji N & Kobayashi M 1978 Trichostatin C, a glucopyranosyl hydroxamate. Journal of Antibiotics 31 939944. (https://doi.org/10.7164/antibiotics.31.939)

  • Tsuji N, Kobayashi M, Nagashima K, Wakisaka Y & Koizumi K 1976 A new antifungal antibiotic, trichostatin. Journal of Antibiotics 29 16. (https://doi.org/10.7164/antibiotics.29.1)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • van Soom A, Ysebaert MT & de Kruif A 1997 Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Molecular Reproduction and Development 47 4756. (https://doi.org/10.1002/(SICI)1098-2795(199705)47:1<47::AID-MRD7>3.0.CO;2-Q)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wakayama T & Yanagimachi R 2001 Effect of cytokinesis inhibitors, DMSO and the timing of oocyte activation on mouse cloning using cumulus cell nuclei. Reproduction 122 4960. (https://doi.org/10.1530/rep.0.1220049)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wakayama T, Perry AC, Zuccotti M, Johnson KR & Yanagimachi R 1998 Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394 369374. (https://doi.org/10.1038/28615)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wakayama S, Cibelli JB & Wakayama T 2003 Effect of timing of the removal of oocyte chromosomes before or after injection of somatic nucleus on development of NT embryos. Cloning and Stem Cells 5 181189. (https://doi.org/10.1089/153623003769645848)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Wang P, Li X, Cao L, Huang S, Li H, Zhang Y, Yang T, Jiang J & Shi D 2017 MicroRNA-148a overexpression improves the early development of porcine somatic cell nuclear transfer embryos. PLoS ONE 12 e0180535. (https://doi.org/10.1371/journal.pone.0180535)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yoshida M, Kijima M, Akita M & Beppu T 1990 Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. Journal of Biological Chemistry 265 1717417179. (https://doi.org/10.1016/S0021-9258(1744885-X)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zeng F & Schultz RM 2005 RNA transcript profiling during zygotic gene activation in the preimplantation mouse embryo. Developmental Biology 283 4057. (https://doi.org/10.1016/j.ydbio.2005.03.038)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zeng F, Baldwin DA & Schultz RM 2004 Transcript profiling during preimplantation mouse development. Developmental Biology 272 483496. (https://doi.org/10.1016/j.ydbio.2004.05.018)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhao LW, Yang XY, Guan PF, Fu J, Li H, Zhou YY, Huang SZ, Zeng YT & Zeng FY 2009 Improved efficiency of bovine somatic cell nuclear transfer by optimizing operational procedures. Journal of Reproduction and Development 55 542546. (https://doi.org/10.1262/jrd.20123)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhou Q, Renard JP, Le Friec G, Brochard V, Beaujean N, Cherifi Y, Fraichard A & Cozzi J 2003 Generation of fertile cloned rats by regulating oocyte activation. Science 302 1179. (https://doi.org/10.1126/science.1088313)

    • PubMed
    • Search Google Scholar
    • Export Citation