Differential developmental requirements for individual histone H3K9 methyltransferases in cleavage-stage porcine embryos
Ki-Eun Park A , Christine M. Johnson A , Xin Wang A and Ryan A. Cabot A B
+ Author Affiliations
- Author Affiliations
A Department of Animal Sciences, Purdue University, West Lafayette, IN 47907, USA.
B Corresponding author. Email: rcabot@purdue.edu
Reproduction, Fertility and Development 23(4) 551-560 https://doi.org/10.1071/RD10280
Submitted: 27 October 2010 Accepted: 24 November 2010 Published: 3 May 2011
Abstract
Dimethylated H3K9 is a heritable epigenetic mark that is closely linked with transcriptional silencing and known to undergo global remodelling during cleavage development. Five mammalian histone methyltransferases (HMTases), namely Suv39H1, Suv39H2, SetDB1, EHMT1 and EHMT2, have been shown to mediate the methylation of H3K9. The aim of the present study was to determine the developmental requirements of these HMTases during cleavage development in porcine embryos. We hypothesised that knockdown of the abovementioned HMTases would differentially affect porcine cleavage development. To test this hypothesis, IVM and IVF porcine oocytes were divided into one of three treatment groups, including non-injected controls, oocytes injected with a double-stranded interfering RNA molecule specific for one of the HMTases and oocytes injected with a corresponding mutated (control) double-stranded RNA molecule. Nuclei were counted in all embryos 6 days after fertilisation. Although no significant difference in total cell number was detected in embryos injected with EHMT1 and EHMT2 interfering RNAs (compared with their respective control groups), embryos injected with interfering RNAs that targeted Suv39H1, Suv39H2 and SetDB1 had significantly lower cell numbers than their respective control groups (P < 0.05). This suggests that individual HMTases differentially affect in vitro developmental potential.
Additional keywords: methylation, RNA interference (RNAi).
References
Aagaard, L., Laible, G., Selenko, P., Schmid, M., Dorn, R., Schotta, G., Kuhfittig, S., Wolf, A., Lebersorger, A., Singh, P. B., Reuter, G., and Jenuwein, T. (1999). Functional mammalian homologues of the Drosophila PEV modifier Su(var)3–9 encode centromere-associated proteins which complex with the heterochromatin component M31. EMBO J. 18, 1923–1938.| Functional mammalian homologues of the Drosophila PEV modifier Su(var)3–9 encode centromere-associated proteins which complex with the heterochromatin component M31.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXivVyks7o%3D&md5=757a480f0130088470a3ca7a7c18536cCAS | 10202156PubMed |
Abeydeera, L. R., and Day, B. N. (1997). Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified tris-buffered medium with frozen–thawed ejaculated spermatozoa. Biol. Reprod. 57, 729–734.
| Fertilization and subsequent development in vitro of pig oocytes inseminated in a modified tris-buffered medium with frozen–thawed ejaculated spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmtFCqs7c%3D&md5=178f00798c971759ada0079842a4a43dCAS | 9314573PubMed |
Abeydeera, L. R., Wang, W. H., Prather, R. S., and Day, B. N. (1998). Maturation in vitro of pig oocytes in protein-free media: fertilization and subsequent embryo development in vitro. Biol. Reprod. 58, 1316–1320.
| Maturation in vitro of pig oocytes in protein-free media: fertilization and subsequent embryo development in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivFCrtLc%3D&md5=289989dffb0cc19a7f85ab825677856dCAS | 9603270PubMed |
Allfrey, V. G., Faulkner, R., and Mirsky, A. E. (1964). Acetylation and methylation of histones and their possible role in regulation of RNA synthesis. Proc. Natl Acad. Sci. USA 51, 786–794.
| Acetylation and methylation of histones and their possible role in regulation of RNA synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2cXktlekurg%3D&md5=6d0c53ea3ad69d442dae42979ac1bd2aCAS |
Berger, S. L. (2002). Histone modifications in transcriptional regulation. Curr. Opin. Genet. Dev. 12, 142–148.
| Histone modifications in transcriptional regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVCnsb4%3D&md5=917a38bc1310c3bdcac9fcef08a3ef9cCAS | 11893486PubMed |
Bouniol, C., Nguyen, E., and Debey, P. (1995). Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp. Cell Res. 218, 57–62.
| Endogenous transcription occurs at the 1-cell stage in the mouse embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlsFShsLc%3D&md5=b62363ce76ce8225df1991d4f9d8dbdfCAS | 7537698PubMed |
de la Cruz, X., Lois, S., Sanchez-Molina, S., and Martinez-Balbas, M. A. (2005). Do protein motifs read the histone code? Bioessays 27, 164–175.
| Do protein motifs read the histone code?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Citbc%3D&md5=c5cbf75ed5ee239f13d564eba9770fdaCAS | 15666348PubMed |
Dodge, J. E., Kang, Y. K., Beppu, H., Lei, H., and Li, E. (2004). Histone H3-K9 methyltransferase ESET is essential for early development. Mol. Cell. Biol. 24, 2478–2486.
| Histone H3-K9 methyltransferase ESET is essential for early development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitVWqt7o%3D&md5=a4cabef6cb711708428ce320937bad8eCAS | 14993285PubMed |
Jarrell, V. L., Day, B. N., and Prather, R. S. (1991). The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis. Biol. Reprod. 44, 62–68.
| The transition from maternal to zygotic control of development occurs during the 4-cell stage in the domestic pig, Sus scrofa: quantitative and qualitative aspects of protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlvFCrsw%3D%3D&md5=1c08b1e57cffd28fd1498a76628e0bc6CAS | 2015352PubMed |
Jeong, Y. S., Yeo, S., Park, J. S., Lee, K. K., and Kang, Y. K. (2007). Gradual development of a genome wide H3-K9 trimethylation pattern in paternally derived pig pronucleus. Dev. Dyn. 236, 1509–1516.
| Gradual development of a genome wide H3-K9 trimethylation pattern in paternally derived pig pronucleus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvFOhsbc%3D&md5=11bb7a03bbc196bf103965622c7f229bCAS | 17474127PubMed |
Lee, D. Y., Teyssier, C., Strahl, B. D., and Stallcup, M. R. (2005). Role of protein methylation in regulation of transcription. Endocr. Rev. 26, 147–170.
| Role of protein methylation in regulation of transcription.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslGjsbc%3D&md5=f2f05aa88e863501a9ea151f3ea8b6c6CAS | 15479858PubMed |
Liu, H., Kim, J. M., and Aoki, F. (2004). Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos. Development 131, 2269–2280.
| Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlGrtrs%3D&md5=ca2c9be327ec9d22a3192f637ca1b98dCAS | 15102709PubMed |
Magnani, L., and Cabot, R. A. (2008). In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development. Mol. Reprod. Dev. 75, 1726–1735.
| In vitro and in vivo derived porcine embryos possess similar, but not identical, patterns of Oct4, Nanog, and Sox2 mRNA expression during cleavage development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlyqsrzN&md5=9bd804b19fe8a1891dc1c13ca1e27088CAS | 18425776PubMed |
Magnani, L., Johnson, C. M., and Cabot, R. A. (2008). Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential. Reprod. Fertil. Dev. 20, 818–825.
| Expression of eukaryotic elongation initiation factor 1A differentially marks zygotic genome activation in biparental and parthenogenetic porcine embryos and correlates with in vitro developmental potential.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWmsb7N&md5=2405b763ed0e72c380ab51d21d234904CAS | 18842184PubMed |
Memili, E., and First, N. L. (1999). Control of gene expression at the onset of bovine embryonic development. Biol. Reprod. 61, 1198–1207.
| Control of gene expression at the onset of bovine embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmvFertrw%3D&md5=7760844012475a6ef00dafc5750e0194CAS | 10529265PubMed |
Morgan, H. D., Santos, F., Green, K., Dean, W., and Reik, W. (2005). Epigenetic reprogramming in mammals. Hum. Mol. Genet. 14, R47–R58.
| Epigenetic reprogramming in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsFeksb4%3D&md5=e05605cb13d90a91ba2717ce31de5fb4CAS | 15809273PubMed |
O’Carroll, D., Scherthan, H., Peters, A. H., Opravil, S., Haynes, A. R., Laible, G., Rea, S., Schmid, M., Lebersorger, A., Jerratsch, M., Sattler, L., Mattei, M. G., Denny, P., Brown, S. D., Schweizer, D., and Jenuwein, T. (2000). Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression. Mol. Cell. Biol. 20, 9423–9433.
| Isolation and characterization of Suv39h2, a second histone H3 methyltransferase gene that displays testis-specific expression.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2Fnsl2ntQ%3D%3D&md5=12d4958963947545d3280578dd149296CAS | 11094092PubMed |
Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dan, W., Reik, W., and Walter, J. (2000). Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475–478.
| Active demethylation of the paternal genome in the mouse zygote.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislyltLo%3D&md5=c64dd510d97ac2bf7b122c276f0260f0CAS | 10801417PubMed |
Park, K. E., Johnson, C. M., Magnani, L., Wang, X., Biancardi, M. N., and Cabot, R. A. (2010). Global H3K9 dimethylation status is not affected by transcription, translation, or DNA replication in porcine zygotes. Mol. Reprod. Dev. 77, 420–429.
| Global H3K9 dimethylation status is not affected by transcription, translation, or DNA replication in porcine zygotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFKqtrs%3D&md5=331c893c9641e5fde389ad278bfbb60dCAS | 20108327PubMed |
Perreault, S. D. (1992). Chromatin remodeling in mammalian zygotes. Mutat. Res. 296, 43–55.
| 1:STN:280:DyaK3s%2FmtlSjug%3D%3D&md5=b3163376c7660c2d8d6ba88f46f7cb96CAS | 1279407PubMed |
Peters, A. H. F. M., O’Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schöfer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A., Opravil, S., Doyle, M., Sibilia, M., and Jenuwein, T. (2001). Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323–337.
| Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVKhsb4%3D&md5=612f739d8ac9f671c00192bd29ab023eCAS | 11701123PubMed |
Sega, M. F., Lee, K., Machaty, Z., and Cabot, R. (2007). Pronuclear stage porcine embryos do not possess a strict asymmetric distribution of lysine 9 dimethylation of histone H3 based solely on parental origin. Mol. Reprod. Dev. 74, 2–7.
| Pronuclear stage porcine embryos do not possess a strict asymmetric distribution of lysine 9 dimethylation of histone H3 based solely on parental origin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yjsb%2FP&md5=3fdb5abd4b3ffb6bff4dea2b002562a3CAS | 16941674PubMed |
Sif, S. (2004). ATP-dependent nucleosome remodeling complexes: enzymes tailored to deal with chromatin. J. Cell. Biochem. 91, 1087–1098.
| ATP-dependent nucleosome remodeling complexes: enzymes tailored to deal with chromatin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1yntr4%3D&md5=3b63823f9755a4cfbc598e9714752225CAS | 15048866PubMed |
Strahl, B. D., and Allis, C. D. (2000). The language of covalent histone modifications. Nature 403, 41–45.
| The language of covalent histone modifications.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7gt1arsQ%3D%3D&md5=67a4b55cbaf0cb43de121a8cc1dc899dCAS | 10638745PubMed |
Tachibana, M., Sugimoto, K., Nozaki, M., Ueda, J., Ohta, T., Ohki, M., Fukuda, M., Takeda, N., Niida, H., Kato, H., and Shinkai, Y. (2002). G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev. 16, 1779–1791.
| G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Onurg%3D&md5=a2f347a5700f9ce9ef2ed66d5e742315CAS | 12130538PubMed |
Tachibana, M., Ueda, J., Fukuda, M., Takeda, N., Ohta, T., Iwanari, H., Sakihama, T., Kodama, T., Hamakubo, T., and Shinkai, Y. (2005). Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3–K9. Genes Dev. 19, 815–826.
| Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3–K9.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1OjtLc%3D&md5=7c78f4c9021fc545864cc4ae9229144bCAS | 15774718PubMed |
Turner, B. M. (2000). Histone acetylation and an epigenetic code. Bioessays 22, 836–845.
| Histone acetylation and an epigenetic code.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslShtbs%3D&md5=9b171cd1ae6c970ede00f97313461a2cCAS | 10944586PubMed |
van der Heijden, G. W., Dieker, J. W., Derijck, A. A., Muller, S., Berden, J. H., Braat, D. D., van der Vlag, J., and de Boer, P. (2005). Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech. Dev. 122, 1008–1022.
| Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntVGjtr4%3D&md5=937fa685e602d70039dff54b28e55a79CAS | 15922569PubMed |
Wagschal, A., Sutherland, H. G., Woodfine, K., Henckel, A., Chebli, K., Schulz, R., Oakey, R. J., Bickmore, W. A., and Feil, R. (2008). G9a histone methyltransferase contributes to imprinting in the mouse placenta. Mol. Cell. Biol. 28, 1104–1113.
| G9a histone methyltransferase contributes to imprinting in the mouse placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWqu70%3D&md5=8f294f817a9afa809fc460fd8502d17fCAS | 18039842PubMed |
Whitworth, K. M., Agca, C., Kim, J. G., Patel, R. V., Springer, G. K., Bivens, N., Forrester, L. J., Mathialagan, N., Green, J. A., and Prather, R. S. (2005). Transcriptional profiling of pig embryogenesis by using a 15K member unigene set specific for pig reproductive tissues and embryos. Biol. Reprod. 72, 1437–1451.
| Transcriptional profiling of pig embryogenesis by using a 15K member unigene set specific for pig reproductive tissues and embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXksFGqsbg%3D&md5=0c5732aad64cb33497f1ec1443aa93fcCAS | 15703372PubMed |
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I. M., and Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–119.
| Birth of piglets derived from porcine zygotes cultured in a chemically defined medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht1yksQ%3D%3D&md5=1222cf9263515655d52deba5e03ac896CAS | 11751272PubMed |
Yuan, P., Han, J., Guo, G., Orlov, Y. L., Huss, M., Loh, Y. H., Yaw, L. P., Robson, P., Lim, B., and Ng, H. H. (2009). Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23, 2507–2520.
| Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVSmtLfK&md5=932c685692b5ae13aec54e22eec27058CAS | 19884257PubMed |
