Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T17:40:03.072Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of peptidylarginine deiminase 4 (PAD4) in pig parthenogenetic preimplantation embryonic development

Published online by Cambridge University Press:  13 July 2012

Manjula Brahmajosyula  and
Masashi Miyake
Manjula Brahmajosyula
Affiliation:
Department of Bioresource Science, Graduate School of Agricultural Science, Kobe University, 1–1 Rokkodai-cho, Nada-ku, Kobe 657–8501, Japan.
Masashi Miyake*
Affiliation:
Department of Bioresource Science, Graduate School of Agricultural Science, Kobe University, 1–1 Rokkodai-cho, Nada-ku, Kobe 657–8501, Japan. Organization of Advanced Science and Technology, Kobe University, 1–1 Rokkodai-cho, Nada-ku, Kobe 657–8501, Japan.
*
All correspondence to: Masashi Miyake. Department of Bioresource Science, Graduate School of Agricultural Science, Kobe University, 1–1 Rokkodai-cho, Nada-ku, Kobe 657–8501, Japan. Tel: +81 78 803 5807. Fax: +81 78 803 6581. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Arginine modification to citrulline (citrullination) is catalyzed by peptidylarginine deiminases (PADs) and one of the isomers PAD4 is shown to be involved in the gene regulation. In our previous paper we studied the localization and expression of PAD4 and the target of PAD4 in mammalian gametes and preimplantation embryos. In this study the role of PAD4 was examined in the pig diploid parthenogenetic preimplantation embryonic development. Knockdown of PAD4 by RNAi resulted in delayed development. Inhibition of PAD4 by a potent PAD4 inhibitor Cl-amidine from the time of activation for 24 h resulted in developmental arrest at the first cleavage. Inhibition at the later stages of development resulted in delayed or arrested development. A shorter exposure to Cl-amidine for 6 h at any stage of growth resulted in slow development. Thus, this study suggests that PAD4 activity is essential for the normal development of the embryos.

Keywords

DevelopmentPAD4PreimplantationPig parthenotesRNAi
Type
Research Article
Information
Zygote , Volume 21 , Issue 4 , November 2013 , pp. 385 - 393
Copyright
Copyright © Cambridge University Press 2012 

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

Bachvarova, R. (1985). Gene expression during oogenesis and oocyte development in mammals. Dev. Biol. 1, 453–24.Google ScholarPubMed
Balint, B.L., Szanto, A., Madi, A., Bauer, U.M., Gabor, P., Benko, S., Puskas, L.G., Davies, P.J. & Nagy, L. (2005). Arginine methylation provides epigenetic transcription memory for retinoid-induced differentiation in myeloid cells. Mol. Cell. Biol. 25, 5648–63.CrossRefGoogle ScholarPubMed
Bolton, V.N., Oades, P.J. & Johnson, M.H. (1984). The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryo. J. Embryol. Exp. Morph. 179, 139–63.Google Scholar
Brahmajosyula, M & Miyake, M. (2011). Localization and expression of peptidylarginine deiminase 4 (PAD4) in mammalian oocytes and preimplantation embryos. Zygote 30, 1–11.Google Scholar
Braunstein, M., Rose, A.B., Holmes, S.G., Allis, C.D. & Broach, J.R. (1993). Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev. 7, 592–4.CrossRefGoogle ScholarPubMed
Causey, C.P. & Thompson, P.R. (2008). An improved synthesis of haloaceteamidine-based inactivators of protein arginine deiminase 4 (PAD4). Tetrahedron Lett. 49, 4383–5.CrossRefGoogle ScholarPubMed
Cuthbert, G.L., Daujat, S., Snowden, A.W., Erdjument-Bromage, H., Hagiwara, T., Yamada, M., Schneider, R., Gregory, P.D., Tempst, P., Bannister, A.J.et al. (2004). Histone deimination antagonizes arginine methylation. Cell 118, 545–53.CrossRefGoogle ScholarPubMed
Gyorgy, B., Toth, E., Tarcsa, E., Falus, A. & Buzas, E.I. (2006). Citrullination: a posttranslational modification in health and disease. Int. J. Biochem. Cell. Biol. 38, 1662–77.CrossRefGoogle ScholarPubMed
Hebbes, T.R., Thorne, A.W. & Crane-Robinson, C. (1988). A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 7, 1395–402.CrossRefGoogle ScholarPubMed
Hebbes, T.R., Clayton, A.L., Thorne, A.W. & Crane-Robinson, C. (1994). Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J 13, 1823–30.CrossRefGoogle ScholarPubMed
Jeppesen, P. & Turner, B.M. (1993). The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74, 281–9.CrossRefGoogle ScholarPubMed
Johnson, M.H. (1981). The molecular and cellular basis of preimplantation mouse development. Biol. Rev. Camb. Philos. Soc. 56, 463–98.CrossRefGoogle ScholarPubMed
Kawamura, Y., Uchijima, Y., Horike, N., Tonami, K., Nishiyama, K., Amano, T., Asano, T., Kurihara, Y. & Kurihara, H. (2010). Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest. J. Clin. Invest. 120, 2817–28.CrossRefGoogle ScholarPubMed
Kornberg, R.D. & Lorch, Y. (1999). Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285–94.CrossRefGoogle ScholarPubMed
Li, P., Yao, H., Zhangm, Z., Li, M., Luo, Y., Thompson, P.R., Gilmourm, D.S. & Wang, Y. (2008). Regulation of p53 target gene expression by peptidylarginine deiminase 4. Mol. Cell. Biol. 28, 4745–58.CrossRefGoogle ScholarPubMed
Li, P., Wang, D., Yao, H., Doret, P., Hao, G., Shen, Q., Qiu, H., Zhang, X., Wang, Y., Chen, G. & Wang, Y. (2010). Coordination of PAD4 and HDAC2 in the regulation of p53-target gene expression. Oncogene 29, 3153–62CrossRefGoogle ScholarPubMed
Loos, T., Opdenakker, G., Van, D.J. & Proost, P. (2009). Citrullination of CXCL8 increases this chemokine's ability to mobilize neutrophils into the blood circulation. Haematologica 94, 1346–53.CrossRefGoogle ScholarPubMed
Luger, K., Mäder, A.W., Richmondm, R.K., Sargent, D.F. & Richmond, T.J. (1997). Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 389, 251–60.CrossRefGoogle Scholar
Pritzker, L.B., Joshi, S., Gowan, J.J., Harauz, G. & Moscarello, M.A. (2000). Deimination of myelin basic protein: I. Effect of deimination of arginyl residues of myelin basic protein on its structure and susceptibility to digestion by cathepsin D. Biochemistry 39, 5374–81.CrossRefGoogle ScholarPubMed
Proost, P., Loos, T., Mortier, A., Schutyser, E., Gouwy, M., Noppen, S., Dillen, C., Ronsse, I., Conings, R., Struyf, S., Opdenakker, G., Maudgal, P.C. & Van, D.J. (2008). Citrullination of CXCL8 by peptidylarginine deiminase alters receptor usage, prevents proteolysis, and dampens tissue inflammation. J. Exp. Med. 205, 2085–97.CrossRefGoogle ScholarPubMed
Stein, P., Svoboda, P., Anger, M. & Schultz, R.M. (2003). RNAi: mammalian oocytes do it without RNA-dependent RNA polymerase. RNA 9, 187–92.CrossRefGoogle Scholar
Stein, P. (2009). Microinjection of dsRNA into mouse one-cell embryos. Cold Spring Harbor Prot (1), 5133.CrossRefGoogle Scholar
Svoboda, P., Stein, P., Filipowicz, W. & Schultz, R.M. (2004). Lack of homologous sequence-specific DNA methylation in response to stable dsRNA expression in mouse oocytes. Nucleic Acids Res. 32, 3601–6.CrossRefGoogle ScholarPubMed
Tarcsa, E., Marekov, L.N., Mei, G., Melino, G., Lee, S.C. & Steinert, P.M. (1996). Protein unfolding by peptidylarginine deaminase: substrate specificity and structural relationships of the natural substrates trichohyalin and filaggrin. J. Biol. Chem. 271, 30709–16.CrossRefGoogle Scholar
Wang, Y., Wysocka, J., Sayegh, J., Lee, Y.H., Perlin, J.R., Leonelli, L., Sonbuchner, L.S., McDonald, C.H., Cook, R.G., Dou, Y.et al. (2004). Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306, 279–83.CrossRefGoogle ScholarPubMed
Wang, Y., Li, M., Stadler, S., Correll, S., Li, P., Wang, D., Hayama, R., Leonelli, L., Han, H., Grigoryev, S.A., Allis, C.D. & Coonrod, S.A. (2009). Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205–13.CrossRefGoogle ScholarPubMed
Yao, H., Li, P., Venters, B.J., Zheng, S., Thompson, P.R., Pugh, B.F. & Wang, Y. (2008). Histone Arg modifications and p53 regulate the expression of OKL38, a mediator of apoptosis. J. Biol. Chem. 283, 20060–8.CrossRefGoogle ScholarPubMed
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.CrossRefGoogle Scholar
Zimmermann, U. & Vienken, J. (1982). Electric field-induced cell-to-cell fusion. J. Membr. Biol. 67, 165–82.CrossRefGoogle ScholarPubMed