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Inability to switch from ARID1A-BAF to ARID1B-BAF impairs exit from pluripotency and commitment towards neural crest formation in ARID1B-related neurodevelopmental disorders

Author

Listed:
  • Luca Pagliaroli

    (Thomas Jefferson University)

  • Patrizia Porazzi

    (Thomas Jefferson University)

  • Alyxandra T. Curtis

    (Thomas Jefferson University)

  • Chiara Scopa

    (Thomas Jefferson University)

  • Harald M. M. Mikkers

    (Leiden University Medical Center)

  • Christian Freund

    (Leiden University Medical Center)

  • Lucia Daxinger

    (Leiden University Medical Center (LUMC))

  • Sandra Deliard

    (The Wistar Institute)

  • Sarah A. Welsh

    (The Wistar Institute)

  • Sarah Offley

    (The Wistar Institute)

  • Connor A. Ott

    (Thomas Jefferson University)

  • Bruno Calabretta

    (Thomas Jefferson University)

  • Samantha A. Brugmann

    (Divisions of Developmental Biology and Plastic Surgery, Department of Pediatrics at Cincinnati Children’s Hospital Medical Center)

  • Gijs W. E. Santen

    (Leiden University Medical Center)

  • Marco Trizzino

    (Thomas Jefferson University)

Abstract

Subunit switches in the BAF chromatin remodeler are essential during development. ARID1B and its paralog ARID1A encode for mutually exclusive BAF subunits. De novo ARID1B haploinsufficient mutations cause neurodevelopmental disorders, including Coffin-Siris syndrome, which is characterized by neurological and craniofacial features. Here, we leveraged ARID1B+/− Coffin-Siris patient-derived iPSCs and modeled cranial neural crest cell (CNCC) formation. We discovered that ARID1B is active only during the first stage of this process, coinciding with neuroectoderm specification, where it is part of a lineage-specific BAF configuration (ARID1B-BAF). ARID1B-BAF regulates exit from pluripotency and lineage commitment by attenuating thousands of enhancers and genes of the NANOG and SOX2 networks. In iPSCs, these enhancers are maintained active by ARID1A-containing BAF. At the onset of differentiation, cells transition from ARID1A- to ARID1B-BAF, eliciting attenuation of the NANOG/SOX2 networks and triggering pluripotency exit. Coffin-Siris patient cells fail to perform the ARID1A/ARID1B switch, and maintain ARID1A-BAF at the pluripotency enhancers throughout all stages of CNCC formation. This leads to persistent NANOG/SOX2 activity which impairs CNCC formation. Despite showing the typical neural crest signature (TFAP2A/SOX9-positive), ARID1B-haploinsufficient CNCCs are also aberrantly NANOG-positive. These findings suggest a connection between ARID1B mutations, neuroectoderm specification and a pathogenic mechanism for Coffin-Siris syndrome.

Suggested Citation

  • Luca Pagliaroli & Patrizia Porazzi & Alyxandra T. Curtis & Chiara Scopa & Harald M. M. Mikkers & Christian Freund & Lucia Daxinger & Sandra Deliard & Sarah A. Welsh & Sarah Offley & Connor A. Ott & Br, 2021. "Inability to switch from ARID1A-BAF to ARID1B-BAF impairs exit from pluripotency and commitment towards neural crest formation in ARID1B-related neurodevelopmental disorders," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26810-x
    DOI: 10.1038/s41467-021-26810-x
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    References listed on IDEAS

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    1. Victor Heurtier & Nick Owens & Inma Gonzalez & Florian Mueller & Caroline Proux & Damien Mornico & Philippe Clerc & Agnes Dubois & Pablo Navarro, 2019. "The molecular logic of Nanog-induced self-renewal in mouse embryonic stem cells," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    2. Jovylyn Gatchalian & Shivani Malik & Josephine Ho & Dong-Sung Lee & Timothy W. R. Kelso & Maxim N. Shokhirev & Jesse R. Dixon & Diana C. Hargreaves, 2018. "A non-canonical BRD9-containing BAF chromatin remodeling complex regulates naive pluripotency in mouse embryonic stem cells," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    3. Svetlana O. Dodonova & Fangjie Zhu & Christian Dienemann & Jussi Taipale & Patrick Cramer, 2020. "Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function," Nature, Nature, vol. 580(7805), pages 669-672, April.
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    1. Mingyi Zhang & Tingwei Guo & Fei Pei & Jifan Feng & Junjun Jing & Jian Xu & Takahiko Yamada & Thach-Vu Ho & Jiahui Du & Prerna Sehgal & Yang Chai, 2024. "ARID1B maintains mesenchymal stem cell quiescence via inhibition of BCL11B-mediated non-canonical Activin signaling," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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