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Spatiotemporal single-cell RNA sequencing of developing chicken hearts identifies interplay between cellular differentiation and morphogenesis

Author

Listed:
  • Madhav Mantri

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University
    Computational Biology Ph.D. Program, Cornell University)

  • Gaetano J. Scuderi

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University)

  • Roozbeh Abedini-Nassab

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University
    University of Neyshabur)

  • Michael F. Z. Wang

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University
    Computational Biology Ph.D. Program, Cornell University)

  • David McKellar

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University)

  • Hao Shi

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University)

  • Benjamin Grodner

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University)

  • Jonathan T. Butcher

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University)

  • Iwijn De Vlaminck

    (Nancy E. and Peter C. Meinig School of Biomedical Engineering, Cornell University)

Abstract

Single-cell RNA sequencing is a powerful tool to study developmental biology but does not preserve spatial information about tissue morphology and cellular interactions. Here, we combine single-cell and spatial transcriptomics with algorithms for data integration to study the development of the chicken heart from the early to late four-chambered heart stage. We create a census of the diverse cellular lineages in developing hearts, their spatial organization, and their interactions during development. Spatial mapping of differentiation transitions in cardiac lineages defines transcriptional differences between epithelial and mesenchymal cells within the epicardial lineage. Using spatially resolved expression analysis, we identify anatomically restricted expression programs, including expression of genes implicated in congenital heart disease. Last, we discover a persistent enrichment of the small, secreted peptide, thymosin beta-4, throughout coronary vascular development. Overall, our study identifies an intricate interplay between cellular differentiation and morphogenesis.

Suggested Citation

  • Madhav Mantri & Gaetano J. Scuderi & Roozbeh Abedini-Nassab & Michael F. Z. Wang & David McKellar & Hao Shi & Benjamin Grodner & Jonathan T. Butcher & Iwijn De Vlaminck, 2021. "Spatiotemporal single-cell RNA sequencing of developing chicken hearts identifies interplay between cellular differentiation and morphogenesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-21892-z
    DOI: 10.1038/s41467-021-21892-z
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    Cited by:

    1. Lin Wei Tung & Elena Groppa & Hesham Soliman & Bruce Lin & Chihkai Chang & Chun Wai Cheung & Morten Ritso & David Guo & Lucas Rempel & Sarthak Sinha & Christine Eisner & Julyanne Brassard & Kelly McNa, 2023. "Spatiotemporal signaling underlies progressive vascular rarefaction in myocardial infarction," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Lulu Shang & Xiang Zhou, 2022. "Spatially aware dimension reduction for spatial transcriptomics," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    3. Honglei Ren & Benjamin L. Walker & Zixuan Cang & Qing Nie, 2022. "Identifying multicellular spatiotemporal organization of cells with SpaceFlow," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Aditi Sahu & Kivanc Kose & Lukas Kraehenbuehl & Candice Byers & Aliya Holland & Teguru Tembo & Anthony Santella & Anabel Alfonso & Madison Li & Miguel Cordova & Melissa Gill & Christi Fox & Salvador G, 2022. "In vivo tumor immune microenvironment phenotypes correlate with inflammation and vasculature to predict immunotherapy response," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. Carter Allen & Yuzhou Chang & Brian Neelon & Won Chang & Hang J. Kim & Zihai Li & Qin Ma & Dongjun Chung, 2023. "A Bayesian multivariate mixture model for high throughput spatial transcriptomics," Biometrics, The International Biometric Society, vol. 79(3), pages 1775-1787, September.
    6. Yu Xia & Sierra Duca & Björn Perder & Friederike Dündar & Paul Zumbo & Miaoyan Qiu & Jun Yao & Yingxi Cao & Michael R. M. Harrison & Lior Zangi & Doron Betel & Jingli Cao, 2022. "Activation of a transient progenitor state in the epicardium is required for zebrafish heart regeneration," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Johannes Wirth & Nina Huber & Kelvin Yin & Sophie Brood & Simon Chang & Celia P. Martinez-Jimenez & Matthias Meier, 2023. "Spatial transcriptomics using multiplexed deterministic barcoding in tissue," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Lukas M. Weber & Arkajyoti Saha & Abhirup Datta & Kasper D. Hansen & Stephanie C. Hicks, 2023. "nnSVG for the scalable identification of spatially variable genes using nearest-neighbor Gaussian processes," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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