Regulation of Tjp1 mRNA by CPEB2 for tight junction assembly in mouse blastocyst

in Reproduction
Authors:
Yelin JeongDivision of Animal and Dairy Sciences, College of Agriculture and Life Sciences, Chungnam National University, Korea, Republic of Korea

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Seulah LeeDivision of Animal and Dairy Sciences, College of Agriculture and Life Sciences, Chungnam National University, Korea, Republic of Korea

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Inchul ChoiDivision of Animal and Dairy Sciences, College of Agriculture and Life Sciences, Chungnam National University, Korea, Republic of Korea

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https://orcid.org/0000-0001-5011-2658
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Correspondence should be addressed to I Choi; Email: icchoi@cnu.ac.kr
DOI:
https://doi.org/10.1530/REP-21-0227
Volume/Issue:
Volume 163: Issue 4
Page Range:
233–240
Article Type:
Research Article
Online Publication Date:
24 Feb 2022
Copyright:
© Society for Reproduction and Fertility 2022
Restricted access

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Cytoplasmic polyadenylation element-binding protein 2 (CPEB2) is an mRNA-binding protein that regulates the cytoplasmic polyadenylation of mRNA and is required for tight junction (TJ) assembly in the trophectoderm epithelium during porcine preimplantation development. However, the regulatory mechanism underlying TJ assembly by CPEB2 has not been examined. The aim of this study was to elucidate how Cpeb2 regulates the subcellular localisation and stabilisation of Tjp1 mRNA for TJ biogenesis during mouse preimplantation. CPEB2 was detected in nuclei during the early stages of development and was localised at apical cell membranes from the morula stage onwards. In the Cpeb2 knockdown (KD), we observed reduced blastocyst formation with impaired TJs, defective inner cell mass development in the blastocyst outgrowth assay, and loss of pregnancy after embryo transfer. More importantly, Tjp1 mRNA was localised apically in the outer cells of control morulae but not in the Cpeb2 KD embryos, indicating that CPEB2 mediated the translocalisation of Tjp1 mRNA from the nuclei. Finally, in the control embryos, the length of the Tjp1 mRNA poly (A) tail was varied, while only a single peak was detected in the Cpeb2 KD embryos. These findings suggest that the binding of CPEB2 to the cytoplasmic polyadenylation element in the 3'-UTR can confer stability on Tjp1 mRNA and translational regulation. In summary, we demonstrated for the first time that CPEB2 mediates Tjp1 mRNA stabilisation and subcellular localisation for TJ assembly during mouse blastocyst formation.

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Alarcon VB 2010 Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse Embryo1. Biology of Reproduction 83 347–358. (https://doi.org/10.1095/biolreprod.110.084400)

    • Search Google Scholar
    • Export Citation

  • Balda MS & Matter K 2008 Tight junctions at a glance. Journal of Cell Science 121 3677–3682. (https://doi.org/10.1242/jcs.023887)

  • Choi I, Carey TS, Wilson CA & Knott JG 2012 Transcription factor AP-2γ is a core regulator of tight junction biogenesis and cavity formation during mouse early embryogenesis. Development 139 4623–4632. (https://doi.org/10.1242/dev.086645)

    • Search Google Scholar
    • Export Citation

  • Cockburn K & Rossant J 2010 Making the blastocyst: lessons from the mouse. Journal of Clinical Investigation 120 995–1003. (https://doi.org/10.1172/JCI41229)

    • Search Google Scholar
    • Export Citation

  • Dodge JE, Kang YK, Beppu H, Lei H & Li E 2004 Histone H3-K9 methyltransferase ESET is essential for early development. Molecular and Cellular Biology 24 2478–2486. (https://doi.org/10.1128/MCB.24.6.2478-2486.2004)

    • Search Google Scholar
    • Export Citation

  • Eckert JJ & Fleming TP 2008 Tight junction biogenesis during early development. Biochimica et Biophysica Acta 1778 717–728. (https://doi.org/10.1016/j.bbamem.2007.09.031)

    • Search Google Scholar
    • Export Citation

  • Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, Gústafsdóttir SM, Østman A & Landegren U 2002 Protein detection using proximity-dependent DNA ligation assays. Nature Biotechnology 20 473–477. (https://doi.org/10.1038/nbt0502-473)

    • Search Google Scholar
    • Export Citation

  • González-Mariscal L, Domínguez-Calderón A, Raya-Sandino A, Ortega-Olvera JM, Vargas-Sierra O & Martínez-Revollar G 2014 Tight junctions and the regulation of gene expression. Seminars in Cell and Developmental Biology 36 213–223. (https://doi.org/10.1016/j.semcdb.2014.08.009)

    • Search Google Scholar
    • Export Citation

  • Jeong Y & Choi I 2019 Tight junction assembly ensures maintenance of pregnancy during embryogenesis in a mouse model. Journal of Animal Reproduction and Biotechnology 34 318–321. (https://doi.org/10.12750/JARB.34.4.318)

    • Search Google Scholar
    • Export Citation

  • Jeong Y, Ock SA, Yoo JG, Yu DY & Choi I 2019 The Cxadr–Adam10 complex plays pivotal roles in tight junction integrity and early trophoblast development in mice. Molecular Reproduction and Development 86 1628–1638. (https://doi.org/10.1002/mrd.23250)

    • Search Google Scholar
    • Export Citation

  • Katsuno T, Umeda K, Matsui T, Hata M, Tamura A, Itoh M, Takeuchi K, Fujimori T, Nabeshima Y & Noda T et al.2008 Deficiency of zonula occludens-1 causes embryonic lethal phenotype associated with defected yolk sac angiogenesis and apoptosis of embryonic cells. Molecular Biology of the Cell 19 2465–2475. (https://doi.org/10.1091/mbc.e07-12-1215)

    • Search Google Scholar
    • Export Citation

  • Kwon J, Jeong SM, Choi I & Kim NH 2016a ADAM10 is involved in cell junction assembly in early porcine embryo development. PLoS ONE 11 e0152921. (https://doi.org/10.1371/journal.pone.0152921)

    • Search Google Scholar
    • Export Citation

  • Kwon JW, Kim NH & Choi I 2016b CXADR is required for AJ and TJ assembly during porcine blastocyst formation. Reproduction 151 297–304. (https://doi.org/10.1530/REP-15-0397)

    • Search Google Scholar
    • Export Citation

  • Kwon J, Park S, Seong MJ, Choi I & Kim NH 2019 Cytoplasmic polyadenylation element binding protein 2 (CPEB2) is required for tight-junction assembly for establishment of porcine trophectoderm epithelium. Reproduction, Fertility, and Development 31 412–419. (https://doi.org/10.1071/RD18098)

    • Search Google Scholar
    • Export Citation

  • Lee SH, Kwon JW, Choi I & Kim NH 2015 Expression and function of transcription factor AP-2γ in early embryonic development of porcine parthenotes. Reproduction, Fertility, and Development 28 1197–1205. (https://doi.org/10.1071/RD14198)

    • Search Google Scholar
    • Export Citation

  • Moriwaki K, Tsukita S & Furuse M 2007 Tight junctions containing claudin 4 and 6 are essential for blastocyst formation in preimplantation mouse embryos. Developmental Biology 312 509–522. (https://doi.org/10.1016/j.ydbio.2007.09.049)

    • Search Google Scholar
    • Export Citation

  • Nagaoka K, Udagawa T & Richter JD 2012 CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nature Communications 3 675. (https://doi.org/10.1038/ncomms1678)

    • Search Google Scholar
    • Export Citation

  • Prochazkova B, Komrskova P & Kubelka M 2018 CPEB2 is necessary for proper porcine meiotic maturation and embryonic development. International Journal of Molecular Sciences 19 3138. (https://doi.org/10.3390/ijms19103138)

    • Search Google Scholar
    • Export Citation

  • Richter JD 2007 CPEB: a life in translation. Trends in Biochemical Sciences 32 279–285. (https://doi.org/10.1016/j.tibs.2007.04.004)

  • Saitou M, Furuse M, Sasaki H, Schulzke JD, Fromm M, Takano H, Noda T & Tsukita S 2000 Complex phenotype of mice lacking occludin, a component of tight junction strands. Molecular Biology of the Cell 11 4131–4142. (https://doi.org/10.1091/mbc.11.12.4131)

    • Search Google Scholar
    • Export Citation

  • Sheth B, Nowak RL, Anderson R, Kwong WY, Papenbrock T & Fleming TP 2008 Tight junction protein ZO-2 expression and relative function of ZO-1 and ZO-2 during mouse blastocyst formation. Experimental Cell Research 314 3356–3368. (https://doi.org/10.1016/j.yexcr.2008.08.021)

    • Search Google Scholar
    • Export Citation

  • Watson AJ & Barcroft LC 2001 Regulation of blastocyst formation. Frontiers in Bioscience 6 D708–D730. (https://doi.org/10.2741/watson)

  • Yuan P, Han J, Guo G, Orlov YL, Huss M, Loh YH, Yaw LP, Robson P, Lim B & Ng HH 2009 Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes and Development 23 2507–2520. (https://doi.org/10.1101/gad.1831909)

    • Search Google Scholar
    • Export Citation