Hostname: page-component-8448b6f56d-dnltx Total loading time: 0 Render date: 2024-04-23T21:20:59.530Z Has data issue: false hasContentIssue false

Multiple histone site epigenetic modifications in nuclear transfer and in vitro fertilized bovine embryos

Published online by Cambridge University Press:  08 July 2010

Xia Wu
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Yan Li
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Lian Xue
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Lingling Wang
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Yongli Yue
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Kehan Li
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Shorgan Bou
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Guang-Peng Li*
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China. The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
Haiquan Yu*
Affiliation:
The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China. The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China.
*
All correspondence to: Haiquan Yu and Guang-Peng Li. The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China. Tel: +86 471 4992495. Fax: +86 471 4995071. e-mail: haiquan_yu@yahoo.com and guangpengli@yahoo.com
All correspondence to: Haiquan Yu and Guang-Peng Li. The Key Laboratory of Mammalian Reproductive Biology and Biotechnology of the Ministry of Education, Inner Mongolia University, Hohhot 010021, China. Tel: +86 471 4992495. Fax: +86 471 4995071. e-mail: haiquan_yu@yahoo.com and guangpengli@yahoo.com

Summary

During mammalian embryonic development, DNA methylation and histone modifications are important in gene expression regulation and epigenetic reprogramming. In cloned embryos, high levels of DNA methylation and abnormal demethylation were widely observed during the preimplantation period. Little is known whether there is a difference in histone modifications between in vitro fertilization (IVF) and cloned embryos during preimplantation development. In the present study, the distributions and intensity patterns of acetylations in H3 lysine 9, 18 and H4 lysine 8, 5 and tri-methyl lysine 4 and dimethyl-lysine 9 in histone H3 were compared in cloned and IVF bovine preimplantation embryos by using indirect immunofluorescence and scanning confocal microscopy. The results showed that the acetylation and methylation levels of H3K9ac, H3K18ac, H4K5ac, H4K8ac, H3K4me3 and H3K9me2 were abnormally high in the cloned embryos from the pronuclear to the 8-cell stage. H4K8ac and H4K5ac in the cloned embryos were particularly abnormal when compared with the IVF controls. At the blastocyst stage differences dissipated between cloned and IVF embryos and the distribution and intensity patterns of all histone modifications showed no obvious difference. These results suggest that somatic cells in recipient oocytes produced aberrant histone modifications at multiple sites before the donor cell genome is activated. After zygotic genome activation, distributions and intensity patterns of histone modifications were comparable with both cloned and IVF embryos.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adenot, P.G., Mercier, Y., Renard, J.P. & Thompson, E.M. (1997). Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124, 4615–25.CrossRefGoogle ScholarPubMed
Arney, K.L., Bao, S., Bannister, A.J., Kouzarides, T. & Surani, M.A. (2002). Histone methylation defines epigenetic asymmetry in the mouse zygote. Int. J. Dev. Biol. 46, 317–20.Google ScholarPubMed
Beaujean, N., Hartshorne, G., Cavilla, J., Taylor, J., Gardner, J., Wilmut, I., Meehan, R. & Young, L. (2004). Non-conservation of mammalian preimplantation methylation dynamics. Curr. Biol. 14, R2667.CrossRefGoogle ScholarPubMed
Bernstein, B.E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D.K., Huebert, D.J., McMahon, S., Karlsson, E.K., Kulbokas, E.J., 3rd, Gingeras, T.R., Schreiber, S.L. & Lander, E.S. (2005). Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169–81.CrossRefGoogle ScholarPubMed
Bertos, N.R., Wang, A.H. & Yang, X.J. (2001). Class II histone deacetylases: structure, function and regulation. Biochem. Cell. Biol. 79, 243–52.CrossRefGoogle ScholarPubMed
Biel, M., Wascholowski, V. & Giannis, A. (2005). Epigenetics—an epicenter of gene regulation: histones and histone-modifying enzymes. Angew. Chem. Int. Ed. Engl. 44, 3186–216.CrossRefGoogle ScholarPubMed
Bjerling, P., Silverstein, R.A., Thon, G., Caudy, A., Grewal, S. & Ekwall, K. (2002). Functional divergence between histone deacetylases in fission yeast by distinct cellular localization and in vivo specificity. Mol. Cell. Biol. 22, 2170–81.CrossRefGoogle ScholarPubMed
Brackett, B.G. & Oliphant, G. (1975). Capacitation of rabbit spermatozoa in vitro. Biol. Reprod. 12, 260–74.CrossRefGoogle ScholarPubMed
Brevini, T.A., Cillo, F., Antonini, S., Tosetti, V. & Gandolfi, F. (2007). Temporal and spatial control of gene expression in early embryos of farm animals. Reprod. Fertil. Dev. 19, 3542.CrossRefGoogle ScholarPubMed
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, 1373413738.CrossRefGoogle ScholarPubMed
Dean, W., Santos, F. & Reik, W. (2003). Epigenetic reprogramming in early mammalian development and following somatic nuclear transfer. Semin. Cell. Dev. Biol. 14, 93100.CrossRefGoogle ScholarPubMed
Fulka, H., Mrazek, M., Tepla, O. & Fulka, J. Jr. (2004). DNA methylation pattern in human zygotes and developing embryos. Reproduction 128, 703–8.CrossRefGoogle ScholarPubMed
Fulka, J., Fulka, H., Slavik, T., Okada, K. & Fulka, J. Jr (2006). DNA methylation pattern in pig in vivo produced embryos. Histochem. Cell. Biol. 126, 213–7.CrossRefGoogle ScholarPubMed
Grant, P.A., Eberharter, A., John, S., Cook, R.G., Turner, B.M. & Workman, J.L. (1999). Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 274, 5895–900.CrossRefGoogle ScholarPubMed
Gurdon, J.B., Laskey, R.A., De Robertis, E.M. & Partington, G.A. (1979). Reprogramming of transplanted nuclei in amphibia. Int. Rev. Cytol. 9, 161–78.CrossRefGoogle Scholar
Holker, M., Petersen, B., Hassel, P., Kues, W.A., Lemme, E., Lucas-Hahn, A. & Niemann, H. (2005). Duration of in vitro maturation of recipient oocytes affects blastocyst development of cloned porcine embryos. Cloning Stem Cells 7, 3544.CrossRefGoogle ScholarPubMed
Huang, J.C., Lei, Z.L., Shi, L.H., Miao, Y.L., Yang, J.W., Ouyang, Y.C., Sun, Q.Y. & Chen, D.Y. (2007). Comparison of histone modifications in in vivo and in vitro fertilization mouse embryos. Biochem. Biophys. Res. Commun. 354, 7783.CrossRefGoogle ScholarPubMed
Kim, J.M., Ogura, A., Nagata, M. & Aoki, F. (2002). Analysis of the mechanism for chromatin remodeling in embryos reconstructed by somatic nuclear transfer. Biol. Reprod. 67, 760–6.CrossRefGoogle ScholarPubMed
Kim, J.M., Liu, H., Tazaki, M., Nagata, M. & Aoki, F. (2003). Changes in histone acetylation during mouse oocyte meiosis. J. Cell. Biol. 162, 3746.CrossRefGoogle ScholarPubMed
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N.V., Wakayama, S., Bui, H.T. & Wakayama, T. (2006). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–9.CrossRefGoogle ScholarPubMed
Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693705.CrossRefGoogle ScholarPubMed
Kurdistani, S.K., Tavazoie, S. & Grunstein, M. (2004). Mapping global histone acetylation patterns to gene expression. Cell 117, 721–33.CrossRefGoogle ScholarPubMed
Lachner, M. & Jenuwein, T. (2002). The many faces of histone lysine methylation. Curr. Opin. Cell. Biol. 14, 286–98.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
Lepikhov, K. & Walter, J. (2004). Differential dynamics of histone H3 methylation at positions K4 and K9 in the mouse zygote. BMC Dev. Biol. 4, 12.CrossRefGoogle ScholarPubMed
Liu, H., Kim, J.M. & Aoki, F. (2004). Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131, 2269–80.CrossRefGoogle ScholarPubMed
Liu, X.Y., Mal, S.F., Miao, D.Q., Liu, D.J., Bao, S. & Tan, J.H. (2005). Cortical granules behave differently in mouse oocytes matured under different conditions. Hum. Reprod. 20, 3402–13.CrossRefGoogle ScholarPubMed
Marmorstein, R. & Roth, S.Y. (2001). Histone acetyltransferases: function, structure and catalysis. Curr. Opin. Genet. Dev. 11, 155–61.CrossRefGoogle ScholarPubMed
Martin, C. & Zhang, Y. (2005). The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell. Biol. 6, 838–49.CrossRefGoogle ScholarPubMed
McGraw, S., Robert, C., Massicotte, L. & Sirard, M.A. (2003). Quantification of histone acetyltransferase and histone deacetylase transcripts during early bovine embryo development. Biol. Reprod. 68, 383–9.CrossRefGoogle ScholarPubMed
Meissner, A. & Jaenisch, R. (2006). Mammalian nuclear transfer. Dev. Dyn. 235, 2460–9.CrossRefGoogle ScholarPubMed
Mizzen, C.A. & Allis, C.D. (1998). Linking histone acetylation to transcriptional regulation. Cell. Mol. Life Sci. 54, 620.CrossRefGoogle ScholarPubMed
Noma, K., Allis, C.D. & Grewal, S.I. (2001). Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science 293, 1150–5.CrossRefGoogle Scholar
O'Neill, L.P. & Turner, B.M. (1995). Histone H4 acetylation distinguishes coding regions of the human genome from heterochromatin in a differentiation-dependent but transcription-independent manner. EMBO J. 14, 3946–57.CrossRefGoogle Scholar
Park, J.S., Jeong, Y.S., Shin, S.T., Lee, K.K. & Kang, Y.K. (2007). Dynamic DNA methylation reprogramming: active demethylation and immediate remethylation in the male pronucleus of bovine zygotes. Dev. Dyn. 236, 2523–33.CrossRefGoogle ScholarPubMed
Pereira, D.C., Dode, M.A. & Rumpf, R. (2005). Evaluation of different culture systems on the in vitro production of bovine embryos. Theriogenology 63, 1131–41.CrossRefGoogle ScholarPubMed
Rybouchkin, A., Kato, Y. & Tsunoda, Y. (2006). Role of histone acetylation in reprogramming of somatic nuclei following nuclear transfer. Biol. Reprod. 74, 1083–9.CrossRefGoogle ScholarPubMed
Santos-Rosa, H., Schneider, R., Bannister, A.J., Sherriff, J., Bernstein, B.E., Emre, N.C., Schreiber, S.L., Mellor, J. & Kouzarides, T. (2002). Active genes are tri-methylated at K4 of histone H3. Nature 419, 407–11.CrossRefGoogle ScholarPubMed
Santos, F. & Dean, W. (2004). Epigenetic reprogramming during early development in mammals. Reproduction 127, 643–51.CrossRefGoogle ScholarPubMed
Santos, F., Hendrich, B., Reik, W. & Dean, W. (2002). Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172–82.CrossRefGoogle ScholarPubMed
Santos, F., Peters, A.H., Otte, A.P., Reik, W. & Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225–36.CrossRefGoogle ScholarPubMed
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
Sarmento, O.F., Digilio, L.C., Wang, Y., Perlin, J., Herr, J.C., Allis, C.D. & Coonrod, S.A. (2004). Dynamic alterations of specific histone modifications during early murine development. J. Cell Sci. 117, 4449–59.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
Schultz, R.M. (1993). Regulation of zygotic gene activation in the mouse. Bioessays 15, 531–8.CrossRefGoogle ScholarPubMed
Shi, L.H., Ai, J.S., Ouyang, Y.C., Huang, J.C., Lei, Z.L., Wang, Q., Yin, S., Han, Z.M., Sun, Q.Y. & Chen, D.Y. (2008). Trichostatin A and nuclear reprogramming of cloned rabbit embryos. J. Anim. Sci. 86, 1106–13.CrossRefGoogle ScholarPubMed
Solter, D. (2000). Mammalian cloning: advances and limitations. Nat. Rev. Genet. 1, 199207.CrossRefGoogle ScholarPubMed
Stallcup, M.R. (2001). Role of protein methylation in chromatin remodeling and transcriptional regulation. Oncogene 20, 3014–20.CrossRefGoogle ScholarPubMed
Stein, P., Worrad, D.M., Belyaev, N.D., Turner, B.M. & Schultz, R.M. (1997). Stage-dependent redistributions of acetylated histones in nuclei of the early preimplantation mouse embryo. Mol. Reprod. Dev. 47, 421–9.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Suteevun, T., Parnpai, R., Smith, S.L., Chang, C.C., Muenthaisong, S. & Tian, X.C. (2006). Epigenetic characteristics of cloned and in vitro-fertilized swamp buffalo (Bubalus bubalis) embryos. J. Anim. Sci. 84, 2065–71.CrossRefGoogle ScholarPubMed
Turner, B.M. (1991). Histone acetylation and control of gene expression. J. Cell Sci. 99, 1320.CrossRefGoogle ScholarPubMed
Turner, B.M. (1998). Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell. Mol. Life Sci. 54, 2131.CrossRefGoogle ScholarPubMed
Valls, E., Sanchez-Molina, S. & Martinez-Balbas, M.A. (2005). Role of histone modifications in marking and activating genes through mitosis. J. Biol. Chem. 280, 42592–600.CrossRefGoogle ScholarPubMed
van der Heijden, G.W., Derijck, A.A., Ramos, L., Giele, M., van der Vlag, J. & de Boer, P. (2006). Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev. Biol. 298, 458–69.CrossRefGoogle Scholar
Vigneault, C., McGraw, S., Massicotte, L. & Sirard, M.A. (2004). Transcription factor expression patterns in bovine in vitro-derived embryos prior to maternal-zygotic transition. Biol. Reprod. 70, 1701–9.CrossRefGoogle ScholarPubMed
Wang, F., Kou, Z., Zhang, Y. & Gao, S. (2007). Dynamic reprogramming of histone acetylation and methylation in the first cell cycle of cloned mouse embryos. Biol. Reprod. 77, 1007–16.CrossRefGoogle ScholarPubMed
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, 810–13.CrossRefGoogle ScholarPubMed
Worrad, D.M., Turner, B.M. & Schultz, R.M. (1995). Temporally restricted spatial localization of acetylated isoforms of histone H4 and RNA polymerase II in the 2-cell mouse embryo. Development 121, 2949–59.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Wells, D., Herrmann, D., Miller, A., Oliver, J., Tervit, R. & Niemann, H. (2001). Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biol. Reprod. 65, 309–17.CrossRefGoogle ScholarPubMed
Yan, C. & Boyd, D.D. (2006). Histone H3 acetylation and H3 K4 methylation define distinct chromatin regions permissive for transgene expression. Mol. Cell. Biol. 26, 6357–71.CrossRefGoogle ScholarPubMed
Yang, J., Yang, S., Beaujean, N., Niu, Y., He, X., Xie, Y., Tang, X., Wang, L., Zhou, Q. & Ji, W. (2007). Epigenetic marks in cloned rhesus monkey embryos: comparison with counterparts produced in vitro. Biol. Reprod. 76, 3642.CrossRefGoogle Scholar