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Specific activation of the hb4 gene in the Xenopus oocyte through a Nobox-binding element located at the proximal promoter sequence

Published online by Cambridge University Press:  28 June 2019

Masanori Nakamigawa ,
Takumi Kondo  and
Mitsugu Maéno Open the ORCID record for Mitsugu Maéno [Opens in a new window]
Masanori Nakamigawa
Affiliation:
Graduate School of Science and Technology;
Takumi Kondo
Affiliation:
Graduate School of Science and Technology;
Mitsugu Maéno
Affiliation:
Institute of Science and Technology, Niigata University, 8050 Ikarashi-2, Nishi-ku, Niigata 950-2181, Japan
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Summary

We isolated and characterized Xenopus tropicalis hb4 flanking DNA and showed that the −3076/+29 sequence was able to drive stage-specific transcription in the developmental process. Transgenic reporter analysis indicated that green fluorescent protein was expressed in the ovaries of female frogs at 3 months of age and in both the ovaries and testis of frogs at 6 months of age. A series of experiments with deletion of the flanking sequence and a subsequent luciferase reporter assay revealed that there were two positive regulatory regions and that the most proximal sequence of the promoter region had a certain level of transcriptional activity in oocytes. Subsequently, we showed that a conserved sequence containing Nobox-binding element (NBE) was essential for transcriptional activation and that Nobox expressed in the ovary had a crucial role in hb4 transcription through the NBE sequence.

Keywords

Linker histoneLuciferaseMaternal geneTransgenic frogTranscription

Information

Type
Research Article
Information
Zygote , Volume 27 , Issue 4 , August 2019 , pp. 195 - 202
Copyright
© Cambridge University Press 2019 

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References

Cho, H and Wolffe, AP (1994) Xenopus laevis B4, an intron-containing oocyte-specific linker histone-encoding gene. Gene 143, 233–238.Google ScholarPubMed
Choi, Y, Qin, Y, Berger, MF, Ballow, DJ, Bulyk, ML and Rajkovic, A (2007) Microarray analyses of newborn mouse ovaries lacking Nobox. Biol Reprod 77, 312–319.CrossRefGoogle ScholarPubMed
Dimitrov, S, Almouzni, G, Dasso, M and Wolffe, AP (1993) Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. Dev Biol 160, 214–227.CrossRefGoogle ScholarPubMed
Dworkin-Rastl, E, Kandolf, H and Smith, RC (1994) The maternal histone H1 variant, H1M (B4 protein), is the predominant H1 histone in Xenopus pregastrula embryos. Dev Biol 161, 425–439.CrossRefGoogle Scholar
Hansson, MD, Rzeznicka, K, Rosenbäck, M, Hansson, M and Sirijovski, N (2008) PCR-mediated deletion of plasmid DNA. Anal Biochem 375, 373–375.CrossRefGoogle ScholarPubMed
Huntriss, J, Gosden, R, Hinkins, M, Oliver, B, Miller, D, Rutherford, AJ and Picton, HM (2002) Isolation, characterization and expression of the human factor in the germline alpha (FIGLA) gene in ovarian follicles and oocytes. Mol Hum Reprod 8, 1087–1095.CrossRefGoogle ScholarPubMed
Ishida, M, Okazaki, E, Tsukamoto, S, Kimura, K, Aizawa, A, Kito, S, Imai, H and Minami, N (2013) The promoter of the oocyte-specific gene, Oog1, functions in both male and female meiotic germ cells in transgenic mice. PLoS One 8, e68686.CrossRefGoogle ScholarPubMed
Jullien, J, Astrand, C, Halley-Stott, RP, Garrett, N and Gurdon, JB (2010) Characterization of somatic cell nuclear reprogramming by oocytes in which a linker histone is required for pluripotency gene reactivation. Proc Natl Acad Sci USA 107, 5483–5488.CrossRefGoogle ScholarPubMed
Jullien, J, Miyamoto, K, Pasque, V, Allen, GE, Bradshaw, CR, Garrett, NJ, Halley-Stott, RP, Kimura, H, Ohsumi, K and Gurdon, JB (2014) Hierarchical molecular events driven by oocyte-specific factors lead to rapid and extensive reprogramming. Mol Cell 55, 524–536.CrossRefGoogle ScholarPubMed
Lim, JC, Kurihara, S, Tamaki, R, Mashima, Y and Maéno, M (2014) Expression and localization of Rdd proteins in Xenopus embryo. Anat Cell Bio 47, 18–27.CrossRefGoogle ScholarPubMed
Maki, N, Suetsugu-Maki, R, Sano, S, Nakamura, K, Nishimura, O, Tarui, H, Del Rio-Tsonis, K, Ohsumi, K, Agata, K and Tsonis, PA (2010) Oocyte-type linker histone B4 is required for transdifferentiation of somatic cells in vivo. FASEB J 24, 3462–4367.CrossRefGoogle ScholarPubMed
Ogino, H Fisher, M and Grainger, RM (2008) Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. Development 135, 249–258.CrossRefGoogle ScholarPubMed
Rajkovic, A, Pangas, SA, Ballow, D, Suzumori, N and Matzuk, MM (2004) NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305, 1157–1159.CrossRefGoogle ScholarPubMed
Saeki, H, Ohsumi, K, Aihara, H, Ito, T, Hirose, S, Ura, K and Kaneda, Y (2005) Linker histone variants control chromatin dynamics during early embryogenesis. Proc Natl Acad Sci USA 102, 5697–5702.CrossRefGoogle ScholarPubMed
Sandelin, A, Alkema, W, Engström, P, Wasserman, WW and Lenhard, B (2004) JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acid Res 32, 91–94.CrossRefGoogle ScholarPubMed
Smith, RC, Dworkin-Rastl, E and Dworkin, MB (1988) Expression of a histone H1-like protein is restricted to early Xenopus development. Genes Dev 2, 1284–1295.CrossRefGoogle ScholarPubMed
Steinbach, OC, Wolffe, AP and Rupp, RA (1997) Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature 389, 395–399.CrossRefGoogle ScholarPubMed
Stewart, D, Tomita, A, Shi, YB and Wong, J (2006) Chromatin immunoprecipitation for studying transcriptional regulation in Xenopus oocytes and tadpoles. Methods Mol Biol 322, 165–181.CrossRefGoogle ScholarPubMed
Suzumori, N, Yan, C, Matzuk, MM and Rajkovic, A (2002) Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes. Mech Dev 111, 137–141.CrossRefGoogle ScholarPubMed
Tafuri, SR and Wolffe, AP (1990) Xenopus Y-box transcription factors: molecular cloning, functional analysis and developmental regulation. Proc Natl Acad Sci USA 87, 9028–9032.Google ScholarPubMed
Tanaka, M, Hennebold, JD, Macfarlane, J and Adashi, EY (2001) A mammalian oocyte-specific linker histone gene H1oo: homology with the genes for the oocyte-specific cleavage stage histone (cs-H1) of sea urchin and the B4/H1M histone of the frog. Development 128, 655–664.CrossRefGoogle ScholarPubMed
Tsunemoto, K, Anzai, M, Matsuoka, T, Tokoro, M, Shin, SW, Amano, T, Mitani, T, Kato, H, Hosoi, Y, Saeki, K, Iritani, A and Matsumoto, K (2008) Cis-acting elements (E-box and NBE) in the promoter region of three maternal genes (histone H1oo, nucleoplasmin 2 and zygote arrest 1) are required for oocyte-specific gene expression in the mouse. Mol Reprod Dev 75, 1104–1108.CrossRefGoogle ScholarPubMed
van Dongen, WM, Moorman, AF and Destrée, OH (1983) The accumulation of the maternal pool of histone H1A during oogenesis in Xenopus laevis. Cell Differ 12, 257–264.CrossRefGoogle ScholarPubMed
Yan, C, Elvin, JA, Lin, YN, Hadsell, LA, Wang, J, DeMayo, FJ and Matzuk, MM (2006) Regulation of growth differentiation factor 9 expression in oocytes in vivo: a key role of the E-box. Biol Reprod 74, 999–1006.Google Scholar
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