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Maternal SMCHD1 regulates Hox gene expression and patterning in the mouse embryo

Author

Listed:
  • Natalia Benetti

    (WEHI
    The University of Melbourne)

  • Quentin Gouil

    (WEHI
    The University of Melbourne)

  • Andres Tapia del Fierro

    (WEHI
    The University of Melbourne)

  • Tamara Beck

    (WEHI)

  • Kelsey Breslin

    (WEHI)

  • Andrew Keniry

    (WEHI
    The University of Melbourne)

  • Edwina McGlinn

    (Monash University
    Monash University)

  • Marnie E. Blewitt

    (WEHI
    The University of Melbourne)

Abstract

Parents transmit genetic and epigenetic information to their offspring. Maternal effect genes regulate the offspring epigenome to ensure normal development. Here we report that the epigenetic regulator SMCHD1 has a maternal effect on Hox gene expression and skeletal patterning. Maternal SMCHD1, present in the oocyte and preimplantation embryo, prevents precocious activation of Hox genes post-implantation. Without maternal SMCHD1, highly penetrant posterior homeotic transformations occur in the embryo. Hox genes are decorated with Polycomb marks H2AK119ub and H3K27me3 from the oocyte throughout early embryonic development; however, loss of maternal SMCHD1 does not deplete these marks. Therefore, we propose maternal SMCHD1 acts downstream of Polycomb marks to establish a chromatin state necessary for persistent epigenetic silencing and appropriate Hox gene expression later in the developing embryo. This is a striking role for maternal SMCHD1 in long-lived epigenetic effects impacting offspring phenotype.

Suggested Citation

  • Natalia Benetti & Quentin Gouil & Andres Tapia del Fierro & Tamara Beck & Kelsey Breslin & Andrew Keniry & Edwina McGlinn & Marnie E. Blewitt, 2022. "Maternal SMCHD1 regulates Hox gene expression and patterning in the mouse embryo," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32057-x
    DOI: 10.1038/s41467-022-32057-x
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    1. Shifeng Xue & Thanh Thao Nguyen Ly & Raunak S. Vijayakar & Jingyi Chen & Joel Ng & Ajay S. Mathuru & Frederique Magdinier & Bruno Reversade, 2022. "HOX epimutations driven by maternal SMCHD1/LRIF1 haploinsufficiency trigger homeotic transformations in genetically wildtype offspring," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Michal R. Gdula & Tatyana B. Nesterova & Greta Pintacuda & Jonathan Godwin & Ye Zhan & Hakan Ozadam & Michael McClellan & Daniella Moralli & Felix Krueger & Catherine M. Green & Wolf Reik & Skirmantas, 2019. "The non-canonical SMC protein SmcHD1 antagonises TAD formation and compartmentalisation on the inactive X chromosome," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    3. Andrew Keniry & Natasha Jansz & Linden J. Gearing & Iromi Wanigasuriya & Joseph Chen & Christian M. Nefzger & Peter F. Hickey & Quentin Gouil & Joy Liu & Kelsey A. Breslin & Megan Iminitoff & Tamara B, 2022. "BAF complex-mediated chromatin relaxation is required for establishment of X chromosome inactivation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Chen-Yu Wang & David Colognori & Hongjae Sunwoo & Danni Wang & Jeannie T. Lee, 2019. "PRC1 collaborates with SMCHD1 to fold the X-chromosome and spread Xist RNA between chromosome compartments," Nature Communications, Nature, vol. 10(1), pages 1-18, December.
    5. Xiaoyu Liu & Chenfei Wang & Wenqiang Liu & Jingyi Li & Chong Li & Xiaochen Kou & Jiayu Chen & Yanhong Zhao & Haibo Gao & Hong Wang & Yong Zhang & Yawei Gao & Shaorong Gao, 2016. "Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos," Nature, Nature, vol. 537(7621), pages 558-562, September.
    6. Gabriel M. Hauswirth & Victoria C. Garside & Lisa S. F. Wong & Heidi Bildsoe & Jan Manent & Yi-Cheng Chang & Christian M. Nefzger & Jaber Firas & Joseph Chen & Fernando J. Rossello & Jose M. Polo & Ed, 2022. "Breaking constraint of mammalian axial formulae," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Laurie A. Boyer & Kathrin Plath & Julia Zeitlinger & Tobias Brambrink & Lea A. Medeiros & Tong Ihn Lee & Stuart S. Levine & Marius Wernig & Adriana Tajonar & Mridula K. Ray & George W. Bell & Arie P. , 2006. "Polycomb complexes repress developmental regulators in murine embryonic stem cells," Nature, Nature, vol. 441(7091), pages 349-353, May.
    8. Azusa Inoue & Lan Jiang & Falong Lu & Tsukasa Suzuki & Yi Zhang, 2017. "Maternal H3K27me3 controls DNA methylation-independent imprinting," Nature, Nature, vol. 547(7664), pages 419-424, July.
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    1. Andres Tapia del Fierro & Bianca den Hamer & Natalia Benetti & Natasha Jansz & Kelan Chen & Tamara Beck & Hannah Vanyai & Alexandra D. Gurzau & Lucia Daxinger & Shifeng Xue & Thanh Thao Nguyen Ly & Ir, 2023. "SMCHD1 has separable roles in chromatin architecture and gene silencing that could be targeted in disease," Nature Communications, Nature, vol. 14(1), pages 1-22, December.

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