IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34730-7.html
   My bibliography  Save this article

Human multilineage pro-epicardium/foregut organoids support the development of an epicardium/myocardium organoid

Author

Listed:
  • Mariana A. Branco

    (Universidade de Lisboa
    Universidade de Lisboa)

  • Tiago P. Dias

    (Universidade de Lisboa
    Universidade de Lisboa)

  • Joaquim M. S. Cabral

    (Universidade de Lisboa
    Universidade de Lisboa)

  • Perpetua Pinto-do-Ó

    (Universidade do Porto
    Universidade do Porto)

  • Maria Margarida Diogo

    (Universidade de Lisboa
    Universidade de Lisboa)

Abstract

The epicardium, the outer epithelial layer that covers the myocardium, derives from a transient organ known as pro-epicardium, crucial during heart organogenesis. The pro-epicardium develops from lateral plate mesoderm progenitors, next to septum transversum mesenchyme, a structure deeply involved in liver embryogenesis. Here we describe a self-organized human multilineage organoid that recreates the co-emergence of pro-epicardium, septum transversum mesenchyme and liver bud. Additionally, we study the impact of WNT, BMP and retinoic acid signaling modulation on multilineage organoid specification. By co-culturing these organoids with cardiomyocyte aggregates, we generated a self-organized heart organoid comprising an epicardium-like layer that fully surrounds a myocardium-like tissue. These heart organoids recapitulate the impact of epicardial cells on promoting cardiomyocyte proliferation and structural and functional maturation. Therefore, the human heart organoids described herein, open the path to advancing knowledge on how myocardium-epicardium interaction progresses during heart organogenesis in healthy or diseased settings.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34730-7
    DOI: 10.1038/s41467-022-34730-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34730-7
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-34730-7?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. Lei Yang & Mark H. Soonpaa & Eric D. Adler & Torsten K. Roepke & Steven J. Kattman & Marion Kennedy & Els Henckaerts & Kristina Bonham & Geoffrey W. Abbott & R. Michael Linden & Loren J. Field & Gordo, 2008. "Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population," Nature, Nature, vol. 453(7194), pages 524-528, May.
    2. 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.
    3. Chen-Leng Cai & Jody C. Martin & Yunfu Sun & Li Cui & Lianchun Wang & Kunfu Ouyang & Lei Yang & Lei Bu & Xingqun Liang & Xiaoxue Zhang & William B. Stallcup & Christopher P. Denton & Andrew McCulloch , 2008. "A myocardial lineage derives from Tbx18 epicardial cells," Nature, Nature, vol. 454(7200), pages 104-108, July.
    4. Lu Han & Praneet Chaturvedi & Keishi Kishimoto & Hiroyuki Koike & Talia Nasr & Kentaro Iwasawa & Kirsten Giesbrecht & Phillip C. Witcher & Alexandra Eicher & Lauren Haines & Yarim Lee & John M. Shanno, 2020. "Single cell transcriptomics identifies a signaling network coordinating endoderm and mesoderm diversification during foregut organogenesis," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    5. Jun Jie Tan & Jacques P. Guyette & Kenji Miki & Ling Xiao & Gurbani Kaur & Tong Wu & Liye Zhu & Katrina J. Hansen & King-Hwa Ling & David J. Milan & Harald C. Ott, 2021. "Human iPS-derived pre-epicardial cells direct cardiomyocyte aggregation expansion and organization in vitro," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    6. T. Yvanka de Soysa & Sanjeev S. Ranade & Satoshi Okawa & Srikanth Ravichandran & Yu Huang & Hazel T. Salunga & Amelia Schricker & Antonio del Sol & Casey A. Gifford & Deepak Srivastava, 2019. "Single-cell analysis of cardiogenesis reveals basis for organ-level developmental defects," Nature, Nature, vol. 572(7767), pages 120-124, August.
    7. Kacey Ronaldson-Bouchard & Stephen P. Ma & Keith Yeager & Timothy Chen & LouJin Song & Dario Sirabella & Kumi Morikawa & Diogo Teles & Masayuki Yazawa & Gordana Vunjak-Novakovic, 2018. "Advanced maturation of human cardiac tissue grown from pluripotent stem cells," Nature, Nature, vol. 556(7700), pages 239-243, April.
    8. Henning Kempf & Ruth Olmer & Alexandra Haase & Annika Franke & Emiliano Bolesani & Kristin Schwanke & Diana Robles-Diaz & Michelle Coffee & Gudrun Göhring & Gerald Dräger & Oliver Pötz & Thomas Joos &, 2016. "Bulk cell density and Wnt/TGFbeta signalling regulate mesendodermal patterning of human pluripotent stem cells," Nature Communications, Nature, vol. 7(1), pages 1-13, December.
    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. 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.
    2. 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.
    3. Mao Mao & Xiaoli Qu & Yabo Zhang & Bingsong Gu & Chen Li & Rongzhi Liu & Xiao Li & Hui Zhu & Jiankang He & Dichen Li, 2023. "Leaf-venation-directed cellular alignment for macroscale cardiac constructs with tissue-like functionalities," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Ryan J. Smith & Hongpan Zhang & Shengen Shawn Hu & Theodora Yung & Roshane Francis & Lilian Lee & Mark W. Onaitis & Peter B. Dirks & Chongzhi Zang & Tae-Hee Kim, 2022. "Single-cell chromatin profiling of the primitive gut tube reveals regulatory dynamics underlying lineage fate decisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Emmanuel Ekow Asmah & Francis Kwaw Andoh & Edem Titriku, 2020. "Trade misinvoicing effects on tax revenue in sub‐Saharan Africa: The role of tax holidays and regulatory quality," Annals of Public and Cooperative Economics, Wiley Blackwell, vol. 91(4), pages 649-672, December.
    6. 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.
    7. Karin D. Prummel & Helena L. Crowell & Susan Nieuwenhuize & Eline C. Brombacher & Stephan Daetwyler & Charlotte Soneson & Jelena Kresoja-Rakic & Agnese Kocere & Manuel Ronner & Alexander Ernst & Zahra, 2022. "Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    8. Wei Feng & Abha Bais & Haoting He & Cassandra Rios & Shan Jiang & Juan Xu & Cindy Chang & Dennis Kostka & Guang Li, 2022. "Single-cell transcriptomic analysis identifies murine heart molecular features at embryonic and neonatal stages," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Nevin Witman & Chikai Zhou & Timm Häneke & Yao Xiao & Xiaoting Huang & Eduarde Rohner & Jesper Sohlmér & Niels Grote Beverborg & Miia L. Lehtinen & Kenneth R. Chien & Makoto Sahara, 2023. "Placental growth factor exerts a dual function for cardiomyogenesis and vasculogenesis during heart development," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Tao Zhuang & Mei-Hua Chen & Ruo-Xi Wu & Jing Wang & Xi-De Hu & Ting Meng & Ai-Hua Wu & Yan Li & Yong-Feng Yang & Yu Lei & Dong-Hua Hu & Yan-Xiu Li & Li Zhang & Ai-Jun Sun & Wei Lu & Guan-Nan Zhang & J, 2024. "ALKBH5-mediated m6A modification of IL-11 drives macrophage-to-myofibroblast transition and pathological cardiac fibrosis in mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    11. Dorota Zawada & Jessica Kornherr & Anna B. Meier & Gianluca Santamaria & Tatjana Dorn & Monika Nowak-Imialek & Daniel Ortmann & Fangfang Zhang & Mark Lachmann & Martina Dreßen & Mariaestela Ortiz & Vi, 2023. "Retinoic acid signaling modulation guides in vitro specification of human heart field-specific progenitor pools," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. Lu Han & Yongxia Wu & Kun Fang & Sean Sweeney & Ulyss K. Roesner & Melodie Parrish & Khushbu Patel & Tom Walter & Julia Piermattei & Anthony Trimboli & Julia Lefler & Cynthia D. Timmers & Xue-Zhong Yu, 2023. "The splanchnic mesenchyme is the tissue of origin for pancreatic fibroblasts during homeostasis and tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    13. Andrea B. Alber & Hector A. Marquez & Liang Ma & George Kwong & Bibek R. Thapa & Carlos Villacorta-Martin & Jonathan Lindstrom-Vautrin & Pushpinder Bawa & Feiya Wang & Yongfeng Luo & Laertis Ikonomou , 2023. "Directed differentiation of mouse pluripotent stem cells into functional lung-specific mesenchyme," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    14. Jeremy Lotto & Rebecca Cullum & Sibyl Drissler & Martin Arostegui & Victoria C. Garside & Bettina M. Fuglerud & Makenna Clement-Ranney & Avinash Thakur & T. Michael Underhill & Pamela A. Hoodless, 2023. "Cell diversity and plasticity during atrioventricular heart valve EMTs," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    15. Andrea Toth & Paranthaman Kannan & John Snowball & Matthew Kofron & Joseph A. Wayman & James P. Bridges & Emily R. Miraldi & Daniel Swarr & William J. Zacharias, 2023. "Alveolar epithelial progenitor cells require Nkx2-1 to maintain progenitor-specific epigenomic state during lung homeostasis and regeneration," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    16. Norika Liu & Naofumi Kawahira & Yasuhiro Nakashima & Haruko Nakano & Akiyasu Iwase & Yasunobu Uchijima & Mei Wang & Sean M. Wu & Susumu Minamisawa & Hiroki Kurihara & Atsushi Nakano, 2023. "Notch and retinoic acid signals regulate macrophage formation from endocardium downstream of Nkx2-5," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    17. Shunsuke Tanigawa & Etsuko Tanaka & Koichiro Miike & Tomoko Ohmori & Daisuke Inoue & Chen-Leng Cai & Atsuhiro Taguchi & Akio Kobayashi & Ryuichi Nishinakamura, 2022. "Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    18. Gayan I. Balasooriya & David L. Spector, 2022. "Allele-specific differential regulation of monoallelically expressed autosomal genes in the cardiac lineage," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    19. 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.
    20. Elena Astanina & Gabriella Doronzo & Davide Corà & Francesco Neri & Salvatore Oliviero & Tullio Genova & Federico Mussano & Emanuele Middonti & Edoardo Vallariello & Chiara Cencioni & Donatella Valdem, 2022. "The TFEB-TGIF1 axis regulates EMT in mouse epicardial cells," Nature Communications, Nature, vol. 13(1), pages 1-20, 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:13:y:2022:i:1:d:10.1038_s41467-022-34730-7. 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.