Impaired Human Cardiac Cell Development due to NOTCH1 Deficiency

  • Shiqiao Ye
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Cankun Wang
    Department of Biomedical Informatics (C.W., Q.M.), The Ohio State University College of Medicine, Columbus, OH.
  • Zhaohui Xu
    Department of Pediatrics (Z.X., V.G., M.-T.Z.), The Ohio State University College of Medicine, Columbus, OH.
  • Hui Lin
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Xiaoping Wan
    Department of Physiology and Cell Biology (X.W., A.R.-N., I.D., M.-T.Z.), The Ohio State University College of Medicine, Columbus, OH.
  • Yang Yu
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Subhodip Adhicary
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Joe Z. Zhang
    Stanford Cardiovascular Institute (J.Z.Z., Y.Z., C.L., J.C.W.), Stanford University School of Medicine, Stanford, CA.
  • Yang Zhou
    Stanford Cardiovascular Institute (J.Z.Z., Y.Z., C.L., J.C.W.), Stanford University School of Medicine, Stanford, CA.
  • Chun Liu
    Stanford Cardiovascular Institute (J.Z.Z., Y.Z., C.L., J.C.W.), Stanford University School of Medicine, Stanford, CA.
  • Matthew Alonzo
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Jianli Bi
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Angelina Ramirez-Navarro
    Department of Physiology and Cell Biology (X.W., A.R.-N., I.D., M.-T.Z.), The Ohio State University College of Medicine, Columbus, OH.
  • Isabelle Deschenes
    Department of Physiology and Cell Biology (X.W., A.R.-N., I.D., M.-T.Z.), The Ohio State University College of Medicine, Columbus, OH.
  • Qin Ma
    Department of Biomedical Informatics (C.W., Q.M.), The Ohio State University College of Medicine, Columbus, OH.
  • Vidu Garg
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).
  • Joseph C. Wu
    Stanford Cardiovascular Institute (J.Z.Z., Y.Z., C.L., J.C.W.), Stanford University School of Medicine, Stanford, CA.
  • Ming-Tao Zhao
    Center for Cardiovascular Research, The Abigail Wexner Research Institute, Nationwide Children’s Hospital, Columbus, OH (S.Y., H.L., Y.Y., S.A., M.A., J.B., V.G., M.-T.Z.).

書誌事項

公開日
2023-01-20
権利情報
  • https://creativecommons.org/licenses/by-nc-nd/4.0/
DOI
  • 10.1161/circresaha.122.321398
公開者
Ovid Technologies (Wolters Kluwer Health)

この論文をさがす

説明

<jats:sec> <jats:title>Background:</jats:title> <jats:p> <jats:italic>NOTCH1</jats:italic> pathogenic variants are implicated in multiple types of congenital heart defects including hypoplastic left heart syndrome, where the left ventricle is underdeveloped. It is unknown how <jats:italic>NOTCH1</jats:italic> regulates human cardiac cell lineage determination and cardiomyocyte proliferation. In addition, mechanisms by which <jats:italic>NOTCH1</jats:italic> pathogenic variants lead to ventricular hypoplasia in hypoplastic left heart syndrome remain elusive. </jats:p> </jats:sec> <jats:sec> <jats:title>Methods:</jats:title> <jats:p> CRISPR (Clustered Regularly Interspaced Short Palindromic Repeats)/Cas9 genome editing was utilized to delete <jats:italic>NOTCH1</jats:italic> in human induced pluripotent stem cells. Cardiac differentiation was carried out by sequential modulation of WNT signaling, and <jats:italic>NOTCH1</jats:italic> knockout and wild-type differentiating cells were collected at day 0, 2, 5, 10, 14, and 30 for single-cell RNA-seq. </jats:p> </jats:sec> <jats:sec> <jats:title>Results:</jats:title> <jats:p> Human <jats:italic>NOTCH1</jats:italic> knockout induced pluripotent stem cells are able to generate functional cardiomyocytes and endothelial cells, suggesting that NOTCH1 is not required for mesoderm differentiation and cardiovascular development in vitro. However, disruption of NOTCH1 blocks human ventricular-like cardiomyocyte differentiation but promotes atrial-like cardiomyocyte generation through shortening the action potential duration. <jats:italic>NOTCH1</jats:italic> deficiency leads to defective proliferation of early human cardiomyocytes, and transcriptomic analysis indicates that pathways involved in cell cycle progression and mitosis are downregulated in <jats:italic>NOTCH1</jats:italic> knockout cardiomyocytes. Single-cell transcriptomic analysis reveals abnormal cell lineage determination of cardiac mesoderm, which is manifested by the biased differentiation toward epicardial and second heart field progenitors at the expense of first heart field progenitors in <jats:italic>NOTCH1</jats:italic> knockout cell populations. </jats:p> </jats:sec> <jats:sec> <jats:title>Conclusions:</jats:title> <jats:p> <jats:italic>NOTCH1</jats:italic> is essential for human ventricular-like cardiomyocyte differentiation and proliferation through balancing cell fate determination of cardiac mesoderm and modulating cell cycle progression. Because first heart field progenitors primarily contribute to the left ventricle, we speculate that pathogenic <jats:italic>NOTCH1</jats:italic> variants lead to biased differentiation of first heart field progenitors, blocked ventricular-like cardiomyocyte differentiation, and defective cardiomyocyte proliferation, which collaboratively contribute to left ventricular hypoplasia in hypoplastic left heart syndrome. </jats:p> </jats:sec>

収録刊行物

  • Circulation Research

    Circulation Research 132 (2), 187-204, 2023-01-20

    Ovid Technologies (Wolters Kluwer Health)

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