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Effect of epigenetic modification with trichostatin A and S-adenosylhomocysteine on developmental competence and POU5F1–EGFP expression of interspecies cloned embryos in dog

Published online by Cambridge University Press:  15 October 2014

M. Mousai ,
S.M. Hosseini ,
M. Hajian ,
F. Jafarpour ,
V. Asgari ,
M. Forouzanfar  and
M.H. Nasr-Esfahani
M. Mousai
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran.
S.M. Hosseini
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran.
M. Hajian
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran.
F. Jafarpour
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran.
V. Asgari
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran.
M. Forouzanfar
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran.
M.H. Nasr-Esfahani*
Affiliation:
Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran. Department of Embryology, Reproductive Biomedicine Center, Royan Institute for Reproductive Biomedicine, ACECR, Tehran, Iran.
*
All correspondence to: M.H. Nasr-Esfahani. Department of Reproductive Biotechnology at Reproductive Biomedicine Research Center, Royan Institute for Biotechnology, ACECR, Isfahan, Iran. Tel: +98 311 9515699. Fax: +98 311 9515687. e-mail: mh.nasr-esfahani@royaninstitute.org
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Summary

Adult canine fibroblasts stably transfected with either cytomegalovirus (CMV) or POU5F1 promoter-driven enhanced green fluorescent protein (EGFP) were used to investigate if pre-treatment of these donor cells with two epigenetic drugs [trichostatin A (TSA), or S-adenosylhomocysteine (SAH)] can improve the efficiency of interspecies somatic cell nuclear transfer (iSCNT). Fluorescence-activated cell sorting (FACS), analyses revealed that TSA, but not SAH, treatment of both transgenic and non-transgenic fibroblasts significantly increased acetylation levels compared with untreated relatives. The expression levels of Bcl2 and P53 were significantly affected in TSA-treated cells compared with untreated cells, whereas SAH treatment had no significant effect on cell apoptosis. Irrespective of epigenetic modification, dog/bovine iSCNT embryos had overall similar rates of cleavage and development to 8–16-cell and morula stages in non-transgenic groups. For transgenic reconstructed embryos, however, TSA and SAH could significantly improve development to 8–16-cell and morula stages compared with control. Even though, irrespective of cell transgenesis and epigenetic modification, none of the iSCNT embryos developed to the blastocyst stage. The iSCNT embryos carrying CMV–EGFP expressed EGFP at all developmental stages (2-cell, 4-cell, 8–16-cell, and morula) without mosaicism, while no POU5F1–EGFP signal was observed in any stage of developing iSCNT embryos irrespective of TSA/SAH epigenetic modifications. These results indicated that bovine oocytes partially remodel canine fibroblasts and that TSA and SAH have marginal beneficial effects on this process.

Keywords

DogEpigenetic modificationInterspecies somatic cell nuclear transferPOU5F1
Type
Research Article
Information
Zygote , Volume 23 , Issue 5 , October 2015 , pp. 758 - 770
Copyright
Copyright © Cambridge University Press 2014 

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References

Asgari, V., Hosseini, S.M., Ostadhosseini, S., Hajian, M., Azhdari, Z.T., Mosaie, M. & Nasr-Esfahani, M.H. (2012). Specific activation requirements of in vitro-matured sheep oocytes following vitrification-warming. Mol. Reprod. Dev. 79, 434–44.CrossRefGoogle ScholarPubMed
Chastant-Maillard, S., Chebrout, M., Thoumire, S., Saint-Dizier, M., Chodkiewicz, M. & Reynaud, K. (2010). Embryo biotechnology in the dog: a review. Reprod. Fertil Dev. 22, 1049–56.Google ScholarPubMed
Chastant-Maillard, S.A.B., Viaris de Lesegno, C.C., Thoumire, S.B., Chebrout, M.B. & Reynaud, K.B. (2011). Transcription genome activation in canine embryos collected in vivo. Reprod. Fertil. Dev. 24, 146.CrossRefGoogle Scholar
Cui, X.S., Xu, Y.N., Shen, X.H., Zhang, L.Q., Zhang, J.B. & Kim, N.H. (2011). Trichostatin A modulates apoptotic-related gene expression and improves embryo viability in cloned bovine embryos. Cell. Reprogram. 13, 179–89.CrossRefGoogle ScholarPubMed
Dominko, T., Mitalipova, M., Haley, B., Beyhan, Z., Memili, E., McKusick, B. & First, N.L. (1999). Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. Biol. Reprod. 60, 1496–1502.CrossRefGoogle ScholarPubMed
Enright, B.P., Kubota, C., Yang, X. & Tian, X.C. (2003). Epigenetic characteristics and development of embryos cloned from donor cells treated by trichostatin A or 5-aza-2′-deoxycytidine. Biol. Reprod. 69, 896–901.CrossRefGoogle ScholarPubMed
Ghorbani, R., Emamzadeh, A., Khazaie, Y., Dormiani, K., Ghaedi, K., Rabbani, M., Foruzanfar, M., Karbalaie, K., Karamali, F., Lachinani, L., Kiani-Esfahani, K., Nematollahi, M. & Nasr-Esfahani, M.H. (2012). Constructing a mouse Oct4 Promoter/EGFP vector, as a whole-cellular reporter to monitor the pluripotent state of cells. Avicenna J. Med. Biotech. 5, 2–9.Google Scholar
Hasiwa, N., Bailey, J., Clausing, P., Daneshian, M., Eileraas, M., Farkas, S., Gyertyán, I., Hubrecht, R., Kobel, W., Krummenacher, G., Leist, M., Lohi, H., Miklósi, A., Ohl, F., Olejniczak, K., Schmitt, G., Sinnett-Smith, P., Smith, D., Wagner, K., Yager, J.D., Zurlo, J. & Hartung, T. (2011). Critical evaluation of the use of dogs in biomedical research and testing in Europe. ALTEX 28, 326–40.CrossRefGoogle ScholarPubMed
Hong, S.G., Kim, M.K., Jang, G., Oh, H.J., Park, J.E., Kang, J.T., Koo, O.J., Kim, T., Kwon, M.S., Koo, B.C., Ra, J.C., Kim, D.Y., Ko, C. & Lee, B.C. (2009). Generation of red fluorescent protein transgenic dogs. Genesis 47, 314–22.CrossRefGoogle ScholarPubMed
Hong, S.G., Oh, H.J., Park, J.E., Kim, M.J., Kim, G.A., Koo, O.J., Jang, G. & Lee, B.C. (2012). Production of transgenic canine embryos using interspecies somatic cell nuclear transfer. Zygote 20, 67–72.CrossRefGoogle ScholarPubMed
Hosseini, S.M., Hajian, M., Moulavi, F., Shahverdi, A.H. & Nasr-Esfahani, M.H. (2006). Optimized combined electrical and chemical activation of in vitro matured bovine oocytes. Anim Reprod. Sci. 108, 122–33.CrossRefGoogle Scholar
Hosseini, S.M., Moulavi, F., Hajian, M. & Abedi, P. (2008). Highly efficient in vitro production of bovine blastocysts in cell-free sequential synthetic oviductal fluid vs. TCM199 Vero cell co-culture system. Int. J. Fertil. Steril. 2, 66–73.Google Scholar
Hosseini, SM., Hajian, M., Forouzanfar, M., Moulavi, F., Abedi, P., Asgari, V., Tanhaei, S., Abbasi, H., Jafarpour, F., Ostadhosseini, S., Karamali, F., Karbaliaie, K., Baharvand, H. & Nasr-Esfahani, M.H. (2012). Enucleated ovine oocyte supports human somatic cells reprogramming back to the embryonic stage. Cell. Reprogram. 14, 155–63.CrossRefGoogle Scholar
Iager, A.E., Ragina, N.P., Ross, P.J., Beyhan, Z., Cunniff, K., Rodriguez, R.M. & Cibelli, J.B. (2008). Trichostatin A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning Stem Cells 10, 371–9.CrossRefGoogle ScholarPubMed
Jafari, S., Hosseini, M.S., Hajian, M., Forouzanfar, M., Jafarpour, F., Abedi, P., Ostadhosseini, S., Abbasi, H., Gourabi, H., Shahverdi, A.H., Dizaj, A.V., Anjomshoaa, M., Haron, W., Noorshariza, N., Yakub, H. & Nasr-Esfahani, M.H. (2011a). Improved in vitro development of cloned bovine embryos using S-adenosylhomocysteine, a non-toxic epigenetic modifying reagent. Mol. Reprod. Dev. 78, 576–84.CrossRefGoogle ScholarPubMed
Jafari, S., Hosseini, S.M., Hajian, M., Forouzanfar, M., Jafarpour, F., Abedi, P., Ostadhosseini, S., Abbasi, H., Gourabi, H., Shahverdi, A.H., Vosough, A.D., Anjomshoaa, M., Haron, A.W., Nordin, N., Yaakub, H. & Nasr-Esfahani, M.H. (2011b). Epigenetic modification does not determine the time of POU5F1 transcription activation in cloned bovine embryos. J. Assist. Reprod. Genet. 28, 1119–27.CrossRefGoogle Scholar
Jafarpour, F., Hosseini, S.M., Hajian, M., Forouzanfar, M., Ostadhosseini, S., Abedi, P., Gholami, S., Ghaedi, K., Gourabi, H., Shahverdi, A.H., Vosough, A.D. & Nasr-Esfahani, M.H. (2011a). Somatic cell-induced hyperacetylation, but not hypomethylation, positively and reversibly affects the efficiency of in vitro cloned blastocyst production in bovine. Cell. Reprogram. 13, 483–93.CrossRefGoogle ScholarPubMed
Jafarpour, F., Hosseini, S.M., Hajian, M., Forouzanfar, M., Abedi, P., Hosseini, L., Ostadhosseini, S., Gholami, S. & Nasr-Esfhani, M.H. (2011b). Developmental competence and pluripotency gene expression of cattle cloned embryos derived from donor cells treated with 5-aza-2′-deoxycytidine. Int. J. Fertil. Steril. 4, 148–55.Google Scholar
Jeon, B.G., Coppola, G., Perrault, S.D., Rho, G.J., Betts, D. & King, W.A. (2008). S-adenosylhomocysteine treatment of adult female fibroblasts alters X-chromosome inactivation and improves in vitro embryo development after somatic cell nuclear transfer. Reproduction 135, 815–28.CrossRefGoogle ScholarPubMed
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, NV., Wakayama, S., Bui, H.T. & Wakayama, T. (2005). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–9.CrossRefGoogle ScholarPubMed
Lee, B.C., Kim, M.K., Jang, G., Oh, H.J., Yuda, F., Kim, H.J., Hossein, M.S., Kim, J.J., Kang, S.K., Schatten, G. & Hwang, W.S. (2005). Dogs cloned from adult somatic cells. Nature 4, 641.CrossRefGoogle Scholar
Liu, H.S., Jan, M.S., Chou, C.K., Chen, P.H. & Ke, N.J. (1999). Is green fluorescent protein toxic to the living cells? Biochem. Biophys. Res. Commun. 260, 712–7.CrossRefGoogle Scholar
Loi, P., Ptak, G., Barboni, B., Fulka, J. Jr., Cappai, P. & Clinton, M. (2001). Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat. Biotechnol. 19, 962–4.CrossRefGoogle ScholarPubMed
Loi, P., Modlinski, J.A. & Ptak, G. (2011). Interspecies somatic cell nuclear transfer, a salvage tool seeking first aid. Theriogenology 15, 217–28.CrossRefGoogle Scholar
Moulavi, F., Hosseini, S.M., Ashtiani, S.K., Shahverdi, A. & Nasr-Esfahani, M.H. (2006). Can Vero cell co-culture improve in-vitro maturation of bovine oocytes? Reprod. Biomed. Online 13, 404–11.CrossRefGoogle ScholarPubMed
Moulavi, F., Hosseini, S.M., Hajian, M., Forouznfar, M., Asgari, V. & Nasr-Esfahani, M.H. (2013). Nuclear transfer technique affects mRNA abundance, developmental competence, and cell fate of the reconstituted sheep oocytes. Reproduction 145, 345–55.CrossRefGoogle ScholarPubMed
Murakami, M., Otoi, T., Wongsrikeao, P., Agung, B., Sambuu, R. & Suzuki, T. (2005). Development of interspecies cloned embryos in yak and dog. Cloning Stem Cells 7, 77–81.CrossRefGoogle ScholarPubMed
Nasr-Esfahani, M.H., Hosseini, S.M., Hajian, M., Forouzanfar, M., Ostadhosseini, S., Abedi, P., Khazaie, Y., Dormiani, K., Ghaedi, K., Forozanfar, M., Gourabi, H., Shahverdi, A.H., Vosough, A.D. & Vojgani, H. (2011). Development of an optimized zona-free method of somatic cell nuclear transfer in the goat. Cell. Reprogram. 13, 157–70.CrossRefGoogle ScholarPubMed
Noggle, S., Fung, H.L., Gore, A., Martinez, H., Satriani, K.C., Prosser, R., Oum, K., Paull, D., Druckenmiller, S., Freeby, M., Greenberg, E., Zhang, K., Goland, R., Sauer, M.V., Leibel, R.L. & Egli, D. (2011). Human oocytes reprogram somatic cells to a pluripotent state. Nature 5, 70–5.CrossRefGoogle Scholar
Oback, B., Wiersema, A.T., Gaynor, P., Laible, G., Tucker, F.C., Oliver, J.E., Miller, A.L., Troskie, H.E., Wilson, K.L., Forsyth, J.T., Berg, M.C., Cockrem, K., McMillan, V., Tervit, H.R. & Wells, D.N. (2003). Cloned bovine derived from a novel zona-free embryo reconstruction system. Cloning Stem Cells 5, 3–12.CrossRefGoogle ScholarPubMed
Prunuske, A.J., Liu, J., Elgort, S., Joseph, J., Dasso, M. & Ullman, K.S. (2006). Nuclear envelope breakdown is coordinated by both Nup358/RanBP2 and Nup153, two nucleoporins with zinc finger modules. Mol. Biol. Cell 17, 760–9.CrossRefGoogle ScholarPubMed
Shi, W., Hoeflich, A., Flaswinkel, H., Stojkovic, M., Wolf, E. & Zakhartchenko, V. (2003). Induction of a senescent-like phenotype does not confer the ability of bovine immortal cells to support the development of nuclear transfer embryos. Biol. Reprod. 69, 301–9.CrossRefGoogle Scholar
Sirard, M.A. (2010). Activation of the embryonic genome. Soc. Reprod. Fertil. Suppl. 67, 145–58.Google ScholarPubMed
Srirattana, K., Imsoonthornruksa, S., Laowtammathron, C., Sangmalee, A., Tunwattana, W., Thongprapai, T., Chaimongkol, C., Ketudat-Cairns, M. & Parnpai, R. (2012). Full-term development of gaur–bovine interspecies somatic cell nuclear transfer embryos, effect of trichostatin A treatment. Cell. Reprogram. 14, 248–57.CrossRefGoogle ScholarPubMed
Sutter, N.B. & Ostrander, E.A. (2004). Dog star rising: the canine genetic system. Nat. Rev. Genet. 5, 900–10.CrossRefGoogle ScholarPubMed
Sylvestre, E.L., Pennetier, S., Bureau, M., Robert, C. & Sirard, M.A. (2010). Investigating the potential of genes preferentially expressed in oocyte to induce chromatin remodeling in somatic cells. Cell. Reprogram. 12, 519–28.CrossRefGoogle ScholarPubMed
Tecirlioglu, R.T., Guo, J. & Trounson, A.O. (2006). Interspecies somatic cell nuclear transfer and preliminary data for horse-cow/mouse iSCNT. Stem Cell Rev. 2, 277–87.CrossRefGoogle ScholarPubMed
Tian, X.C., Park, J., Bruno, R., French, R., Jiang, L. & Prather, R.S. (2009). Altered gene expression in cloned piglets. Reprod. Fertil. Dev. 21, 60–6.CrossRefGoogle ScholarPubMed
Vajta, G., Peura, T.T., Holm, P., Paldi, A., Greve, T., Trounson, A.O. & Callesen, H. (2000). New method for culture of zona-included or zona-free embryos: the Well of the Well (WOW) system. Mol. Reprod. Dev. 55, 256–64.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Vallée, M., Aiba, K., Piao, Y., Palin, M.F., Ko, M.S. & Sirard, M.A. (2008). Comparative analysis of oocyte transcript profiles reveals a high degree of conservation among species. Reproduction 135, 439–48.CrossRefGoogle ScholarPubMed
Wilbe, M., Jokinen, P., Truvé, K., Seppala, E.H., Karlsson, E.K., Biagi, T., Hughes, A., Bannasch, D., Andersson, G., Hansson-Hamlin, H., Lohi, H. & Lindblad-Toh, K. (2010). Genome-wide association mapping identifies multiple loci for a canine SLE-related disease complex. Nat. Genet. 42, 250–4.CrossRefGoogle ScholarPubMed