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Single-cell transcriptomics uncovers a non-autonomous Tbx1-dependent genetic program controlling cardiac neural crest cell development

Author

Listed:
  • Christopher Bono

    (Albert Einstein College of Medicine)

  • Yang Liu

    (Albert Einstein College of Medicine)

  • Alexander Ferrena

    (Albert Einstein College of Medicine
    Albert Einstein College of Medicine)

  • Aneesa Valentine

    (Albert Einstein College of Medicine)

  • Deyou Zheng

    (Albert Einstein College of Medicine
    Albert Einstein College of Medicine
    Albert Einstein College of Medicine)

  • Bernice E. Morrow

    (Albert Einstein College of Medicine
    Albert Einstein College of Medicine)

Abstract

Disruption of cardiac neural crest cells (CNCCs) results in congenital heart disease, yet we do not understand the cell fate dynamics as these cells differentiate to vascular smooth muscle cells. Here we performed single-cell RNA-sequencing of NCCs from the pharyngeal apparatus with the heart in control mouse embryos and when Tbx1, the gene for 22q11.2 deletion syndrome, is inactivated. We uncover three dynamic transitions of pharyngeal NCCs expressing Tbx2 and Tbx3 through differentiated CNCCs expressing cardiac transcription factors with smooth muscle genes. These transitions are altered non-autonomously by loss of Tbx1. Further, inactivation of Tbx2 and Tbx3 in early CNCCs results in aortic arch branching defects due to failed smooth muscle differentiation. Loss of Tbx1 interrupts mesoderm to CNCC cell-cell communication with upregulation and premature activation of BMP signaling and reduced MAPK signaling, as well as alteration of other signaling, and failed dynamic transitions of CNCCs leading to disruption of aortic arch artery formation and cardiac outflow tract septation.

Suggested Citation

  • Christopher Bono & Yang Liu & Alexander Ferrena & Aneesa Valentine & Deyou Zheng & Bernice E. Morrow, 2023. "Single-cell transcriptomics uncovers a non-autonomous Tbx1-dependent genetic program controlling cardiac neural crest cell development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37015-9
    DOI: 10.1038/s41467-023-37015-9
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    1. Yuichiro Arima & Sachiko Miyagawa-Tomita & Kazuhiro Maeda & Rieko Asai & Daiki Seya & Maryline Minoux & Filippo M. Rijli & Koichi Nishiyama & Ki-Sung Kim & Yasunobu Uchijima & Hisao Ogawa & Yukiko Kur, 2012. "Preotic neural crest cells contribute to coronary artery smooth muscle involving endothelin signalling," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
    2. Suoqin Jin & Christian F. Guerrero-Juarez & Lihua Zhang & Ivan Chang & Raul Ramos & Chen-Hsiang Kuan & Peggy Myung & Maksim V. Plikus & Qing Nie, 2021. "Inference and analysis of cell-cell communication using CellChat," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    3. Elizabeth A. Lindsay & Francesca Vitelli & Hong Su & Masae Morishima & Tuong Huynh & Tiziano Pramparo & Vesna Jurecic & George Ogunrinu & Helen F. Sutherland & Peter J. Scambler & Allan Bradley & Anto, 2001. "Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice," Nature, Nature, vol. 410(6824), pages 97-101, March.
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