Involvement of Nlrp9a/b/c in mouse preimplantation development

in Reproduction
Authors:
Satoko Kanzaki Laboratory of Stem Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan
Research and Development Department, Prima Meat Packers Ltd Ibaraki Research Center, Ibaraki, Japan

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Shiori Tamura Laboratory of Stem Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Toshiaki Ito Laboratory of Stem Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Mizuki Wakabayashi Laboratory of Stem Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Koji Saito Division of Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Shigeki Kato Research and Development Department, Prima Meat Packers Ltd Ibaraki Research Center, Ibaraki, Japan

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Yasutaka Ohta Division of Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Yoichi Sekita Laboratory of Stem Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Tohru Kimura Laboratory of Stem Cell Biology, Department of Biosciences, Kitasato University School of Science, Kanagawa, Japan

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Correspondence should be addressed to T Kimura; Email: tkimura@Kitasato-u.ac.jp

*(S Kanzaki and S Tamura contributed equally to this work)

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Nucleotide-binding oligomerization domain, leucine-rich repeat and pyrin domain-containing proteins (NRLPs) are central components of the inflammasome. Accumulating evidence has shown that a reproductive clade of NRLPs is predominantly expressed in oocyte to cleavage stage embryos and participates in mammalian preimplantation development as a component of a multiprotein complex known as the subcortical maternal complex (SCMC). Nlrp9s belong to the reproductive class of NLRPs; Nlrp9b is unique in acting as an inflammasome against rotavirus in intestines. Here we generated mice carrying mutations in all three members of the Nlrp9a/b/c gene (Nlrp9 triple mutant (TMut) mice). When crossed with WT males, the Nlrp9 TMut females were fertile, but deliveries with fewer pups were increased in the mutants. Consistent with this, blastocyst development was retarded and lethality to the preimplantation embryos increased in the Nlrp9 TMut females in vivo. Under in vitro culture conditions, the fertilized eggs from the Nlrp9 TMut females exhibited developmental arrest at the two-cell stage, accompanied by asymmetric cell division. By contrast, double-mutant (DMut) oocytes (any genetic combination) did not exhibit the two-cell block in vitro, showing the functional redundancy of Nlrp9a/b/c. Finally, Nlrp9 could bind to components of the SCMC. These results show that Nlrp9 functions as an immune or reproductive NLRP in a cell-type-dependent manner.

 

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  • Biggers JD 1998 Reflections on the culture of the preimplantation embryo. International Journal of Developmental Biology 42 879884.

  • Dang-Nguyen TQ & Torres-Padilla ME 2015 How cells build totipotency and pluripotency: nuclear, chromatin and transcriptional architecture. Current Opinion in Cell Biology 34 915. (https://doi.org/10.1016/j.ceb.2015.04.006)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Docherty LE, Rezwan FI, Poole RL, Turner CLS, Kivuva E, Maher ER, Smithson SF, Hamilton-Shield JP, Patalan M & Gizewska M et al.2015 Mutations in NLRP5 are associated with reproductive wastage and multilocus imprinting disorders in humans. Nature Communications 6 8086. (https://doi.org/10.1038/ncomms9086)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Esposito G, Vitale AM, Leijten FPJ, Strik AM, Koonen-Reemst AMCB, Yurttas P, Robben TJAA, Coonrod S & Gossen JA 2007 Peptidylarginine deiminase (PAD) 6 is essential for oocyte cytoskeletal sheet formation and female fertility. Molecular and Cellular Endocrinology 273 2531. (https://doi.org/10.1016/j.mce.2007.05.005)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Gao Z, Zhang X, Yu X, Qin D, Xiao Y, Yu Y, Xiang Y, Nie X, Lu X & Liu W et al.2018 Zbed3 participates in the subcortical maternal complex and regulates the distribution of organelles. Journal of Molecular Cell Biology 10 7488. (https://doi.org/10.1093/jmcb/mjx035)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Hashimoto M & Takemoto T 2015 Electroporation enables the efficient mRNA delivery into the mouse zygotes and facilitates CRISPR/Cas9-based genome editing. Scientific Reports 5 11315. (https://doi.org/10.1038/srep11315)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kosugi M, Otani M, Kikkawa Y, Itakura Y, Sakai K, Ito T, Toyoda M, Sekita Y & Kimura T 2020 Mutations of histone demethylase genes encoded by X and Y chromosomes, Kdm5c and Kdm5d, lead to noncompaction cardiomyopathy in mice. Biochemical and Biophysical Research Communications. (https://doi.org/10.1016/j.bbrc.2020.02.043)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Leung CY & Zernicka-Goetz M 2015 Mapping the journey from totipotency to lineage specification in the mouse embryo. Current Opinion in Genetics and Development 34 7176. (https://doi.org/10.1016/j.gde.2015.08.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Li L, Baibakov B & Dean J 2008 A subcortical maternal complex essential for preimplantation mouse embryogenesis. Developmental Cell 15 416425. (https://doi.org/10.1016/j.devcel.2008.07.010)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Lu X, Gao Z, Qin D & Li L 2017 A maternal functional module in the mammalian oocyte-to-embryo transition. Trends in Molecular Medicine 23 10141023. (https://doi.org/10.1016/j.molmed.2017.09.004)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mahadevan S, Sathappan V, Utama B, Lorenzo I, Kaskar K & Van Den Veyver IB 2017 Maternally expressed NLRP2 links the subcortical maternal complex (SCMC) to fertility, embryogenesis and epigenetic reprogramming. Scientific Reports 7 44667. (https://doi.org/10.1038/srep44667)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ohsugi M, Zheng P, Baibakov B, Li L & Dean J 2008 Maternally derived FILIA-MATER complex localizes asymmetrically in cleavage-stage mouse embryos. Development 135 259269. (https://doi.org/10.1242/dev.011445)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Parry DA, Logan CV, Hayward BE, Shires M, Landolsi H, Diggle C, Carr I, Rittore C, Touitou I & Philibert L et al.2011 Mutations causing familial biparental hydatidiform mole implicate C6orf221 as a possible regulator of genomic imprinting in the human oocyte. American Journal of Human Genetics 89 451458. (https://doi.org/10.1016/j.ajhg.2011.08.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Peng H, Lin X, Liu F, Wang C & Zhang W 2015 NLRP9B protein is dispensable for oocyte maturation and early embryonic development in the mouse. Journal of Reproduction and Development 61 559564. (https://doi.org/10.1262/jrd.2015-050)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Pétrilli V, Dostert C, Muruve DA & Tschopp J 2007 The inflammasome: a danger sensing complex triggering innate immunity. Current Opinion in Immunology 19 615622. (https://doi.org/10.1016/j.coi.2007.09.002)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Qin D, Gao Z, Xiao Y, Zhang X, Ma H, Yu X, Nie X, Fan N, Wang X & Ouyang Y et al.2019 The subcortical maternal complex protein Nlrp4f is involved in cytoplasmic lattice formation and organelle distribution. Development 146. (https://doi.org/10.1242/dev.183616)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rathinam VAK & Fitzgerald KA 2016 Inflammasome complexes: emerging mechanisms and effector functions. Cell 165 792800. (https://doi.org/10.1016/j.cell.2016.03.046)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Reddy R, Akoury E, Phuong Nguyen NM, Abdul-Rahman OA, Dery C, Gupta N, Daley WP, Ao A, Landolsi H & Ann Fisher R et al.2013 Report of four new patients with protein-truncating mutations in C6orf221/KHDC3L and colocalization with NLRP7. European Journal of Human Genetics 21 957964. (https://doi.org/10.1038/ejhg.2012.274)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Rezaei M, Nguyen NMP, Foroughinia L, Dash P, Ahmadpour F, Verma IC, Slim R & Fardaei M 2016 Two novel mutations in the KHDC3L gene in Asian patients with recurrent hydatidiform mole. Human Genome Variation 3 16027. (https://doi.org/10.1038/hgv.2016.27)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Sakai K, Ito C, Wakabayashi M, Kanzaki S, Ito T, Takada S, Toshimori K, Sekita Y & Kimura T 2019 Usp26 mutation in mice leads to defective spermatogenesis depending on genetic background. Scientific Reports 9 13757. (https://doi.org/10.1038/s41598-019-50318-6)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Schultz RM, Stein P & Svoboda P 2018 The oocyte-to-embryo transition in mouse: past, present, and future. Biology of Reproduction 99 160174. (https://doi.org/10.1093/biolre/ioy013)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tashiro F, Kanai-Azuma M, Miyazaki S, Kato M, Tanaka T, Toyoda S, Yamato E, Kawakami H, Miyazaki T & Miyazaki JI 2010 Maternal-effect gene Ces5/Ooep/Moep19/Floped is essential for oocyte cytoplasmic lattice formation and embryonic development at the maternal-zygotic stage transition. Genes to Cells 15 813828. (https://doi.org/10.1111/j.1365-2443.2010.01420.x)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tian X, Pascal G & Monget P 2009 Evolution and functional divergence of NLRP genes in mammalian reproductive systems. BMC Evolutionary Biology 9 202. (https://doi.org/10.1186/1471-2148-9-202)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Tong ZB, Gold L, Pfeifer KE, Dorward H, Lee E, Bondy CA, Dean J & Nelson LM 2000 Mater, a maternal effect gene required for early embryonic development in mice. Nature Genetics 26 267268. (https://doi.org/10.1038/81547)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yu XJ, Yi Z, Gao Z, Qin D, Zhai Y, Chen X, Ou-Yang Y, Wang ZB, Zheng P & Zhu MS et al.2014 The subcortical maternal complex controls symmetric division of mouse zygotes by regulating F-actin dynamics. Nature Communications 5 4887. (https://doi.org/10.1038/ncomms5887)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Yue F, Cheng Y, Breschi A, Vierstra J, Wu W, Ryba T, Sandstrom R, Ma Z, Davis C & Pope BD et al.2014 A comparative encyclopedia of DNA elements in the mouse genome. Nature 515 355364. (https://doi.org/10.1038/nature13992)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zheng P & Dean J 2009 Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. PNAS 106 74737478. (https://doi.org/10.1073/pnas.0900519106)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Zhu S, Ding S, Wang P, Wei Z, Pan W, Palm NW, Yang Y, Yu H, Li HB & Wang G et al.2017 Nlrp9b inflammasome restricts rotavirus infection in intestinal epithelial cells. Nature 546 667670. (https://doi.org/10.1038/nature22967)

    • PubMed
    • Search Google Scholar
    • Export Citation