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Effect of cryopreservation and in vitro culture of bovine fibroblasts on histone acetylation levels and in vitro development of hand-made cloned embryos

Published online by Cambridge University Press:  07 July 2010

Liliana Chacón ,
Martha C. Gómez ,
Jill A. Jenkins ,
Staley P. Leibo ,
Gemechu Wirtu ,
Betsy L. Dresser  and
C. Earle Pope
Liliana Chacón
Affiliation:
Audubon Center for Research of Endangered Species, New Orleans, Louisiana, USA. School of Veterinarian Medicine, Colombian National University, Bogotá, Colombia.
Martha C. Gómez*
Affiliation:
Audubon Center for Research of Endangered Species, 14001 River Road, New Orleans, Louisiana, USA. Audubon Center for Research of Endangered Species, New Orleans, Louisiana, USA.
Jill A. Jenkins
Affiliation:
National Wetlands Research Center, US Geological Survey, Lafayette, Louisiana, USA.
Staley P. Leibo
Affiliation:
Audubon Center for Research of Endangered Species, New Orleans, Louisiana, USA. Department of Biological Sciences, University of New Orleans, New Orleans, Louisiana, USA.
Gemechu Wirtu
Affiliation:
Audubon Center for Research of Endangered Species, New Orleans, Louisiana, USA.
Betsy L. Dresser
Affiliation:
Audubon Center for Research of Endangered Species, New Orleans, Louisiana, USA. Department of Biological Sciences, University of New Orleans, New Orleans, Louisiana, USA.
C. Earle Pope
Affiliation:
Audubon Center for Research of Endangered Species, New Orleans, Louisiana, USA.
*
All correspondence to: Martha C. Gómez. Audubon Center for Research of Endangered Species, 14001 River Road, New Orleans, Louisiana, USA. Tel: +504 398 3159. Fax: +504 391 7707. e-mail: mgomez@auduboninstitute.org
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Summary

In this study, the relative acetylation levels of histone 3 in lysine 9 (H3K9ac) in cultured and cryopreserved bovine fibroblasts was measured and we determined the influence of the epigenetic status of three cultured (C1, C2 and C3) donor cell lines on the in vitro development of reconstructed bovine embryos. Results showed that cryopreservation did not alter the overall acetylation levels of H3K9 in bovine fibroblasts analysed immediately after thawing (frozen/thawed) compared with fibroblasts cultured for a period of time after thawing. However, reduced cleavage rates were noted in embryos reconstructed with fibroblasts used immediately after thawing. Cell passage affects the levels of H3K9ac in bovine fibroblasts, decreasing after P1 and donor cells with lower H3K9ac produced a greater frequency of embryo development to the blastocyst stage. Cryopreservation did not influence the total cell and ICM numbers, or the ICM/TPD ratios of reconstructed embryos. However, the genetic source of donor cells did influence the total number of cells and the trophectoderm cell numbers, and the cell passage influenced the total ICM cell numbers.

Keywords

BovineEmbryoFibroblastsHistone acetylationSCNT
Type
Research Article
Information
Zygote , Volume 19 , Issue 3 , August 2011 , pp. 255 - 264
Copyright
Copyright © Cambridge University Press 2010

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References

Al-Rostum, F., Bhojwani, S., Poehland, R., Becker, F., Viergutz, T., Brunner, R. & Kanitz, W. (2007). Effect of somatic cell donor on bovine nuclear transfer efficiency. 23rd Annual Meeting A.E.T.E. 7–8th September, Alghero, Sardinia.Google Scholar
Alberio, R., Johnson, A.D., Stick, R. & Campbell, K.H. (2005). Differential nuclear remodeling of mammalian somatic cells by Xenopus laevis oocyte and egg cytoplasm. Exp. Cell Res. 307, 131–41.CrossRefGoogle ScholarPubMed
Allegrucci, C., Way's., Thurston A., Denning, C.N., Priddle, H., Mummery, C.L., Ward-van Oostwaard, D., Andrews, P.W., Stojkovic, M., Smith, N., Parkin, T., Jones, M.E., Warren, G., Yu, L., Brena, R.M., Plass, C. & Young, L.E. (2007). Restriction landmark genome scanning identifies culture-induced DNA methylation instability in the human embryonic stem cell epigenome. Hum. Mol. Genet. 16, 1253–68.CrossRefGoogle ScholarPubMed
Allis, C.D., Jenuwein, T. & Reinberg, D. (2007). Overview and Concepts. In Epigenetics (eds. Allis, C.D., Jenuwein, T., Reinberg, D. & Caparros, M.L..) p. 25. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Amasino, R. (2004). Vernalization, competence and the epigenetic memory of winter. Plant Cell 16, 2553–9.CrossRefGoogle ScholarPubMed
Antequera, F., Boyes, J. & Bird, A. (1990). High levels of de novo methylation and altered chromatin structure at CpG islands in cell lines. Cell 62, 503–14.CrossRefGoogle ScholarPubMed
Beyhan, Z., Forsberg, E.J., Eilertsen, K.J., Kent-First, M. & First, N.L. (2007). Gene expression in bovine nuclear transfer embryos in relation to donor cell efficiency in producing live offspring. Mol. Reprod. Dev. 74, 18–27.CrossRefGoogle ScholarPubMed
Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6–21.CrossRefGoogle ScholarPubMed
Boiani, M., Eckardt, S., Leu, N.A., Scholer, H.R. & McLaughlin, K.J. (2003). Pluripotency deficit in clones overcome by clone–clone aggregation: epigenetic complementation? EMBO J. 22, 5304–12.CrossRefGoogle ScholarPubMed
Boquest, A.C., Day, B.N. & Prather, R.S. (1999). Flow cytometric cell cycle analysis of cultured porcine fetal fibroblast cells. Biol. Reprod. 60, 1013–9.CrossRefGoogle ScholarPubMed
Bordignon, V., Clarke, H.J. & Smith, L.C. (2001). Factors controlling the loss of immunoreactive somatic histone H1 from blastomere nuclei in oocyte cytoplasm: a potential marker of nuclear reprogramming. Dev. Biol. 233, 192–203.CrossRefGoogle ScholarPubMed
Bourc'his, D., Le Bourhis, D., Patin, D., Niveleau, A., Comizzoli, P., Renard, J.P. & Viegas-Pequignot, E. (2001). Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Curr. Biol. 11, 1542–6.CrossRefGoogle ScholarPubMed
Chacón, L, Gómez, M.C., Jenkins, J.A., Leibo, S.P., Wirtu, G., Dresser, B.L. & Pope, C.E. (2009). Production of bovine cloned embryos with donor cells frozen at a slow cooling rate in a conventional freezer (−20 °C). Zygote 17, 341–51.CrossRefGoogle Scholar
Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E. & Reik, W. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc. Natl. Acad. Sci. USA 98, 13734–8.CrossRefGoogle ScholarPubMed
Doherty, A.S., Mann, M.R., Tremblay, K.D., Bartolomei, M.S. & Schultz, R.M. (2000). Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526–35.CrossRefGoogle ScholarPubMed
Enright, B.P., Jeong, B.S., Yang, X. & Tian, X.C. (2003a). Epigenetic characteristics of bovine donor cells for nuclear transfer: levels of histone acetylation. Biol. Reprod. 69, 1525–30.CrossRefGoogle ScholarPubMed
Enright, B.P., Kubota, C., Yang, X. & Tian, X.C. (2003b). 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
Fauque, P., Jouannet, P., Lesaffre, C., Ripoche, M.A., Dandolo, L., Vaiman, D. & Jammes, H. (2007). Assisted Reproductive Technology affects developmental kinetics, H19 imprinting control region methylation and H19 gene expression in individual mouse embryos. BMC Dev. Biol. 7, 116.CrossRefGoogle ScholarPubMed
Fischle, W., Wang, Y., Jacobs, S.A., Kim, Y., Allis, C.D. & Khorasanizadeh, S. (2003). Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by polycomb and HP1 chromodomains. Genes Dev. 17, 1870–81.CrossRefGoogle Scholar
Fleming, T.P., Kwong, W.Y., Porter, R., Ursell, E., Fesenko, I., Wilkins, A., Miller, D.J., Watkins, A.J. & Eckert, J.J. (2004). The embryo and its future. Biol. Reprod. 71, 1046–54.CrossRefGoogle ScholarPubMed
Fuks, F., Hurd, P.J., Wolf, D., Nan, X., Bird, A.P. & Kouzarides, T. (2003). The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035–40.CrossRefGoogle ScholarPubMed
Gómez, M.C., Pope, C.E., Kutner, R.H., Ricks, D.M., Lyons, L.A., Ruhe, M., Dumas, C., Lyons, J., López, M., Dresser, B.L. & Reiser, J. (2008). Nuclear transfer of Sand Cat cells in to enucleated domestic cat oocytes is affected by cryopreservation of donor cells. Cloning Stem Cells 10, 469–84.CrossRefGoogle ScholarPubMed
Hayes, O., Rodriguez, L.L., Gonzalez, A., Falcon, V., Aguilar, A. & Castro, F.O. (2005). Effect of cryopreservation on fusion efficiency and in vitro development into blastocysts of bovine cell lines used in somatic cell cloning. Zygote 13, 277–82.CrossRefGoogle ScholarPubMed
Holm, P., Booth, P.J., Schmidt, M.H., Greve, T. & Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum-proteins. Theriogenology 52, 683–700.CrossRefGoogle ScholarPubMed
Kang, Y.K., Koo, D.B., Park, J.S., Choi, Y.H., Chung, A.S., Lee, K.K. & Han, Y.M. (2001). Aberrant methylation of donor genome in cloned bovine embryos. Nat. Genet. 28, 173–7.CrossRefGoogle ScholarPubMed
Kang, Y.K., Park, J.S., Koo, D.B., Choi, Y.H., Kim, S.U., Lee, K.K. & Han, Y.M. (2002). Limited demethylation leaves mosaic-type methylation states in cloned bovine pre-implantation embryos. EMBO J. 21, 1092–100.CrossRefGoogle ScholarPubMed
Kato, Y., Tani, T. & Tsunoda, Y. (2000). Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J. Reprod. Fertil. 120, 231–7.CrossRefGoogle ScholarPubMed
Ke, Q., Davidson, T., Chen, H., Kluz, T. & Costa, M. (2006). Alterations of histone modifications and transgene silencing by nickel chloride. Carcinogenesis 27, 1481–8.CrossRefGoogle ScholarPubMed
Kikyo, N., Wade, P.A., Guschin, D., Ge, H. & Wolffe, A.P. (2000). Active remodeling of somatic nuclei in egg cytoplasm by the nucleosomal ATPase ISWI. Science 289, 2360–2.CrossRefGoogle ScholarPubMed
Kishi, M., Itagaki, Y., Takakura, R., Sudo, T. & Teranishi, M. (2003). Effect of polyethylene glycol and dimethyl sulfoxide on the fusion of bovine nuclear transfer using mammary gland epithelial cells. Cloning Stem Cells 5, 43–9.CrossRefGoogle ScholarPubMed
Koo, D.B., Kang, Y.K., Choi, Y.H., Park, J.S., Kim, H.N., Oh, K.B., Son, D.S., Park, H., Lee, K.K. & Han, Y.M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol. Reprod. 67, 487–92.CrossRefGoogle ScholarPubMed
Lachner, M., O'Sullivan, R.J. & Jenuwein, T. (2003). An epigenetic road map for histone lysine methylation. J. Cell Sci. 116, 2117–24.CrossRefGoogle ScholarPubMed
Li, T., Vu, T.H., Ulaner, G.A., Littman, E., Ling, J.Q., Chen, H.L., Hu, J.F., Behr, B., Giudice, L. & Hoffman, A.R. (2005). IVF results in de novo DNA methylation and histone methylation at an Igf2-H19 imprinting epigenetic switch. Mol. Hum. Reprod. 11, 631–40.CrossRefGoogle ScholarPubMed
Luger, K., Rechsteiner, T.J., Flaus, A.J., Waye, M.M. & Richmond, T.J. (1997). Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol 272, 301–11.CrossRefGoogle ScholarPubMed
Mastromonaco, G.F., Perrault, S.D., Betts, D.H. & King, W.A. (2006). Role of chromosome stability and telomere length in the production of viable cell lines for somatic cell nuclear transfer. BMC Dev. Biol. 6, 41 [abs].CrossRefGoogle ScholarPubMed
Noer, A. (2008). Histone h3 modifications associated with differentiation and long-term culture of mesenchymal adipose stem cells. Stem Cells Dev. 18, 725–36.CrossRefGoogle Scholar
Pnueli, L., Edry, I., Cohen, M. & Kassir, Y. (2004). Glucose and nitrogen regulate the switch from histone deacetylation to acetylation for expression of early meiosis-specific genes in budding yeast. Mol. Cell Biol. 24, 5197–208.CrossRefGoogle ScholarPubMed
Poehland, R., Al-Rostum, F., Becker, F., Viergutz, T., Brunner, R.M., Kanitz, W. & Bhojwani, S. (2007). Donor cell lines considerably affect the outcome of somatic nuclear transfer in the case of bovines. J. Reprod. Dev. 53, 737–48.CrossRefGoogle ScholarPubMed
Powell, A.M., Talbot, N.C., Wells, K.D., Kerr, D.E., Pursel, V.G. & Wall, R.J. (2004). Cell donor influences success of producing cattle by somatic cell nuclear transfer. Biol. Reprod. 71, 210–6.CrossRefGoogle ScholarPubMed
Rice, J.C. & Allis, C.D. (2001). Histone methylation versus histone acetylation: new insights into epigenetic regulation. Curr. Opin. Cell Biol. 13, 263–73.CrossRefGoogle ScholarPubMed
Roh, S., Shim, H., Hwang, W.S. & Yoon, J.T. (2000). In vitro development of green fluorescent protein (GFP) transgenic bovine embryos after nuclear transfer using different cell cycles and passages of fetal fibroblasts. Reprod. Fertil. Dev. 12, 1–6.CrossRefGoogle ScholarPubMed
Ross, P.J., Beyhan, Z. & Cibelli, J. (2007). Somatic cell nuclear transfer in cattle. J. Anim. Sci. 85 (Suppl 2), 117 [abs].Google Scholar
Santos, F., Zakhartchenko, V., Stojkovic, M., Peters, A., Jenuwein, T., Wolf, E., Reik, W. & Dean, W. (2003). Epigenetic marking correlates with developmental potential in cloned bovine preimplantation embryos. Curr. Biol. 13, 1116–21.CrossRefGoogle ScholarPubMed
Schiltz, R.L., Mizzen, C.A., Vassilev, A., Cook, R.G., Allis, C.D. & Nakatani, Y. (1999). Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J. Biol. Chem. 274, 1189–92.CrossRefGoogle ScholarPubMed
Shao, G.B., Ding, H.M., Gong, A.H. & Xiao, D.S. (2008). Inheritance of histone H3 methylation in reprogramming of somatic nuclei following nuclear transfer. J. Reprod. Dev. 54, 233–8.CrossRefGoogle ScholarPubMed
Spencer, T.E., Jenster, G., Burcin, M.M., Allis, C.D., Zhou, J., Mizzen, C.A., McKenna, N.J., Onate, S.A., Tsai, S.Y., Tsai, M.J. & O'Malley, B.W. (1997). Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389, 194–8.CrossRefGoogle ScholarPubMed
Strahl, B.D. & Allis, C.D. (2000). The language of covalent histone modifications. Nature 403, 41–5.CrossRefGoogle ScholarPubMed
Thompson, J.G. (1997). Comparison between in vivo-derived and in vitro-produced pre-elongation embryos from domestic ruminants. Reprod. Fertil. Dev. 9, 341–54.CrossRefGoogle ScholarPubMed
Turner, B.M. (2000). Histone acetylation and an epigenetic code. Bioessays 22, 836–45.3.0.CO;2-X>CrossRefGoogle Scholar
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
Vajta, G., Lewis, I.M., Hyttel, P., Thouas, G.A. & Trounson, A.O. (2001). Somatic cell cloning without micromanipulators. Cloning 3, 89–95.CrossRefGoogle ScholarPubMed
Vajta, G., Maddox-Hyttel, P., Skou, C.T., Tecirlioglu, R.T., Peura, T.T., Lai, L., Murphy, C.N., Prather, R.S., Kragh, P.M. & Callesen, H. (2005). Highly efficient and reliable chemically assisted enucleation method for hand made cloning in cattle. Reprod. Fertil. Dev. 17, 791–7.CrossRefGoogle ScholarPubMed
Van Soom, A., Ysebaert, M.T. & 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. Mol. Reprod. Dev. 47, 47–56.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Vignon, X, Le Bourhis, D., Laloy, E., Lavergne, Y, Servely, J.L, Richard, C., Renard, J.P. & Heyman, Y. (2003). A comparison of the development of bovine embryos cloned from fibroblasts of two different genetic origins. In Proceedings for the 9th Scientific Meeting of the European Embryo Transfer Association (AETE). 12–13th September, Rostock, Germany, 221, Abstract.Google Scholar
Walker, S.K., Hartwich, K.M. & Seamark, R.F. (1996). The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 45, 111–20.CrossRefGoogle Scholar
Wee, G., Koo, D.B., Song, B.S., Kim, J.S., Kang, M.J., Moon, S.J., Kang, Y.K., Lee, K.K. & Han, Y.M. (2006). Inheritable histone H4 acetylation of somatic chromatins in cloned embryos. J. Biol. Chem. 281, 6048–57.CrossRefGoogle ScholarPubMed
Wells, K.D. (2000). Simple, efficient stain for differential staining of trophectoderm and inner cell mass cells. Genetically Engineering and Cloning Animals: Science, Society and Industry. Park City, Utah, USA. 2 (3), 115 [abs].Google Scholar
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.CrossRefGoogle ScholarPubMed
Wu, J., Wang, S.H., Potter, D., Liu, J.C., Smith, L.T., Wu, Y.Z., Huang, T.H. & Plass, C. (2007). Diverse histone modifications on histone 3 lysine 9 and their relation to DNA methylation in specifying gene silencing. BMC Genomics 8, 131–9.CrossRefGoogle ScholarPubMed
Yang, F., Hao, R., Kessler, B., Brem, G., Wolf, E. & Zakhartchenko, V. (2007). Rabbit somatic cell cloning: effects of donor cell type, histone acetylation status and chimeric embryo complementation. Reproduction 133, 219–30.CrossRefGoogle ScholarPubMed
Yang, J., Yang, S., Beaujean, N., Niu, Y., He, X., Xie, Y., Tang, X., Wang, L., Zhou, Q. & Ji, W. (2006). Epigenetic marks in cloned rhesus monkey embryos: comparison with counterparts produced in vitro. Biol. Reprod. 76, 36–42.CrossRefGoogle Scholar
Young, L.E., Sinclair, K.D. & Wilmut, I. (1998). Large offspring syndrome in cattle and sheep. Rev. Reprod. 3, 155–63.CrossRefGoogle ScholarPubMed
Young, L.E., Fernandes, K., McEvoy, T.G., Butterwith, S.C., Gutierrez, C.G., Carolan, C., Broadbent, P.J., Robinson, J.J., Wilmut, I. & Sinclair, K.D. (2001). Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153–4.CrossRefGoogle ScholarPubMed
Zakhartchenko, V., Yang, F., Hao, R. & Wolf, E. (2007). Rabbit cloning: histone acetylation status of donor cells and cloned embryos. Reprod. Fert. Dev. 19, 168 [abs].CrossRefGoogle Scholar