IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43999-1.html
   My bibliography  Save this article

A patterned human primitive heart organoid model generated by pluripotent stem cell self-organization

Author

Listed:
  • Brett Volmert

    (Michigan State University
    Michigan State University)

  • Artem Kiselev

    (Michigan State University
    Michigan State University
    Michigan State University)

  • Aniwat Juhong

    (Michigan State University
    Michigan State University)

  • Fei Wang

    (Washington University in Saint Louis)

  • Ashlin Riggs

    (Michigan State University
    Michigan State University)

  • Aleksandra Kostina

    (Michigan State University
    Michigan State University)

  • Colin O’Hern

    (Michigan State University
    Michigan State University)

  • Priyadharshni Muniyandi

    (Michigan State University
    Michigan State University)

  • Aaron Wasserman

    (Michigan State University
    Michigan State University)

  • Amanda Huang

    (Michigan State University
    Michigan State University)

  • Yonatan Lewis-Israeli

    (Michigan State University
    Michigan State University)

  • Vishal Panda

    (Michigan State University
    Michigan State University)

  • Sudin Bhattacharya

    (Michigan State University
    Michigan State University)

  • Adam Lauver

    (Michigan State University)

  • Sangbum Park

    (Michigan State University
    Michigan State University
    Michigan State University)

  • Zhen Qiu

    (Michigan State University
    Michigan State University)

  • Chao Zhou

    (Washington University in Saint Louis)

  • Aitor Aguirre

    (Michigan State University
    Michigan State University)

Abstract

Pluripotent stem cell-derived organoids can recapitulate significant features of organ development in vitro. We hypothesized that creating human heart organoids by mimicking aspects of in utero gestation (e.g., addition of metabolic and hormonal factors) would lead to higher physiological and anatomical relevance. We find that heart organoids produced using this self-organization-driven developmental induction strategy are remarkably similar transcriptionally and morphologically to age-matched human embryonic hearts. We also show that they recapitulate several aspects of cardiac development, including large atrial and ventricular chambers, proepicardial organ formation, and retinoic acid-mediated anterior-posterior patterning, mimicking the developmental processes found in the post-heart tube stage primitive heart. Moreover, we provide proof-of-concept demonstration of the value of this system for disease modeling by exploring the effects of ondansetron, a drug administered to pregnant women and associated with congenital heart defects. These findings constitute a significant technical advance for synthetic heart development and provide a powerful tool for cardiac disease modeling.

Suggested Citation

  • Brett Volmert & Artem Kiselev & Aniwat Juhong & Fei Wang & Ashlin Riggs & Aleksandra Kostina & Colin O’Hern & Priyadharshni Muniyandi & Aaron Wasserman & Amanda Huang & Yonatan Lewis-Israeli & Vishal , 2023. "A patterned human primitive heart organoid model generated by pluripotent stem cell self-organization," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43999-1
    DOI: 10.1038/s41467-023-43999-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43999-1
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43999-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Yonatan R. Lewis-Israeli & Aaron H. Wasserman & Mitchell A. Gabalski & Brett D. Volmert & Yixuan Ming & Kristen A. Ball & Weiyang Yang & Jinyun Zou & Guangming Ni & Natalia Pajares & Xanthippi Chatzis, 2021. "Self-assembling human heart organoids for the modeling of cardiac development and congenital heart disease," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    2. Donald M. Bers, 2002. "Cardiac excitation–contraction coupling," Nature, Nature, vol. 415(6868), pages 198-205, January.
    3. Daniel Dimitrov & Dénes Türei & Martin Garrido-Rodriguez & Paul L. Burmedi & James S. Nagai & Charlotte Boys & Ricardo O. Ramirez Flores & Hyojin Kim & Bence Szalai & Ivan G. Costa & Alberto Valdeoliv, 2022. "Comparison of methods and resources for cell-cell communication inference from single-cell RNA-Seq data," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Lucia M. Moreira & Abhijit Takawale & Mohit Hulsurkar & David A. Menassa & Agne Antanaviciute & Satadru K. Lahiri & Neelam Mehta & Neil Evans & Constantinos Psarros & Paul Robinson & Alexander J. Spar, 2020. "Paracrine signalling by cardiac calcitonin controls atrial fibrogenesis and arrhythmia," Nature, Nature, vol. 587(7834), pages 460-465, November.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Guillermo Serrano & Nerea Berastegui & Aintzane Díaz-Mazkiaran & Paula García-Olloqui & Carmen Rodriguez-Res & Sofia Huerga-Dominguez & Marina Ainciburu & Amaia Vilas-Zornoza & Patxi San Martin-Uriz &, 2024. "Single-cell transcriptional profile of CD34+ hematopoietic progenitor cells from del(5q) myelodysplastic syndromes and impact of lenalidomide," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Sina Schumacher & Max Fernkorn & Michelle Marten & Rui Chen & Yung Su Kim & Ivan Bedzhov & Christian Schröter, 2024. "Tissue-intrinsic beta-catenin signals antagonize Nodal-driven anterior visceral endoderm differentiation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Erick Armingol & Hratch M. Baghdassarian & Cameron Martino & Araceli Perez-Lopez & Caitlin Aamodt & Rob Knight & Nathan E. Lewis, 2022. "Context-aware deconvolution of cell–cell communication with Tensor-cell2cell," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Quanxia Lyu & Shu Gong & Jarmon G. Lees & Jialiang Yin & Lim Wei Yap & Anne M. Kong & Qianqian Shi & Runfang Fu & Qiang Zhu & Ash Dyer & Jennifer M. Dyson & Shiang Y. Lim & Wenlong Cheng, 2022. "A soft and ultrasensitive force sensing diaphragm for probing cardiac organoids instantaneously and wirelessly," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Hongyan Gao & Zhien Wang & Feiyu Yang & Xiaoyu Wang & Siqi Wang & Quan Zhang & Xiaomeng Liu & Yubing Sun & Jing Kong & Jun Yao, 2024. "Graphene-integrated mesh electronics with converged multifunctionality for tracking multimodal excitation-contraction dynamics in cardiac microtissues," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    6. Zhuoxuan Li & Tianjie Wang & Pentao Liu & Yuanhua Huang, 2023. "SpatialDM for rapid identification of spatially co-expressed ligand–receptor and revealing cell–cell communication patterns," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    7. Roman Nikolaienko & Elisa Bovo & Daniel Kahn & Ryan Gracia & Thomas Jamrozik & Aleksey V. Zima, 2023. "Cysteines 1078 and 2991 cross-linking plays a critical role in redox regulation of cardiac ryanodine receptor (RyR)," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. David R. Ghasemi & Konstantin Okonechnikov & Anne Rademacher & Stephan Tirier & Kendra K. Maass & Hanna Schumacher & Piyush Joshi & Maxwell P. Gold & Julia Sundheimer & Britta Statz & Ahmet S. Rifaiog, 2024. "Compartments in medulloblastoma with extensive nodularity are connected through differentiation along the granular precursor lineage," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Pietro Mesirca & Jean Chemin & Christian Barrère & Eleonora Torre & Laura Gallot & Arnaud Monteil & Isabelle Bidaud & Sylvie Diochot & Michel Lazdunski & Tuck Wah Soong & Stéphanie Barrère-Lemaire & M, 2024. "Selective blockade of Cav1.2 (α1C) versus Cav1.3 (α1D) L-type calcium channels by the black mamba toxin calciseptine," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    10. Zoe Piran & Mor Nitzan, 2024. "SiFT: uncovering hidden biological processes by probabilistic filtering of single-cell data," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Sabrina Schütz & Llorenç Solé-Boldo & Carlota Lucena-Porcel & Jochen Hoffmann & Alexander Brobeil & Anke S. Lonsdorf & Manuel Rodríguez-Paredes & Frank Lyko, 2023. "Functionally distinct cancer-associated fibroblast subpopulations establish a tumor promoting environment in squamous cell carcinoma," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Zachary V. Johnson & Brianna E. Hegarty & George W. Gruenhagen & Tucker J. Lancaster & Patrick T. McGrath & Jeffrey T. Streelman, 2023. "Cellular profiling of a recently-evolved social behavior in cichlid fishes," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    13. Mariana A. Branco & Tiago P. Dias & Joaquim M. S. Cabral & Perpetua Pinto-do-Ó & Maria Margarida Diogo, 2022. "Human multilineage pro-epicardium/foregut organoids support the development of an epicardium/myocardium organoid," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    14. Maksymilian Prondzynski & Paul Berkson & Michael A. Trembley & Yashasvi Tharani & Kevin Shani & Raul H. Bortolin & Mason E. Sweat & Joshua Mayourian & Dogacan Yucel & Albert M. Cordoves & Beatrice Gab, 2024. "Efficient and reproducible generation of human iPSC-derived cardiomyocytes and cardiac organoids in stirred suspension systems," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Daniel Bormann & Michael Knoflach & Emilia Poreba & Christian J. Riedl & Giulia Testa & Cyrille Orset & Anthony Levilly & Andréa Cottereau & Philipp Jauk & Simon Hametner & Nadine Stranzl & Bahar Gola, 2024. "Single-nucleus RNA sequencing reveals glial cell type-specific responses to ischemic stroke in male rodents," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    16. Marco C. Miotto & Steven Reiken & Anetta Wronska & Qi Yuan & Haikel Dridi & Yang Liu & Gunnar Weninger & Carl Tchagou & Andrew R. Marks, 2024. "Structural basis for ryanodine receptor type 2 leak in heart failure and arrhythmogenic disorders," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Bas Loo & Simone A. Den & Nuno Araújo-Gomes & Vincent Jong & Rebecca R. Snabel & Maik Schot & José M. Rivera-Arbeláez & Gert Jan C. Veenstra & Robert Passier & Tom Kamperman & Jeroen Leijten, 2023. "Mass production of lumenogenic human embryoid bodies and functional cardiospheres using in-air-generated microcapsules," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    18. Ian Fernandes & Shunsuke Funakoshi & Homaira Hamidzada & Slava Epelman & Gordon Keller, 2023. "Modeling cardiac fibroblast heterogeneity from human pluripotent stem cell-derived epicardial cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    19. Weiyuan Li & Lu Pan & Weifeng Hong & Florent Ginhoux & Xuan Zhang & Chunjie Xiao & Xuexin Li, 2024. "A single-cell pan-cancer analysis to show the variability of tumor-infiltrating myeloid cells in immune checkpoint blockade," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    20. E. Koncina & M. Nurmik & V. I. Pozdeev & C. Gilson & M. Tsenkova & R. Begaj & S. Stang & A. Gaigneaux & C. Weindorfer & F. Rodriguez & M. Schmoetten & E. Klein & J. Karta & V. S. Atanasova & K. Grzyb , 2023. "IL1R1+ cancer-associated fibroblasts drive tumor development and immunosuppression in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43999-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.