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In vivo clonal tracking reveals evidence of haemangioblast and haematomesoblast contribution to yolk sac haematopoiesis

Author

Listed:
  • C. Biben

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • T. S. Weber

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • K. S. Potts

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • J. Choi

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • D. C. Miles

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • A. Carmagnac

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • T. Sargeant

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • C. A. Graaf

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • K. A. Fennell

    (Peter MacCallum Cancer Centre)

  • A. Farley

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • O. J. Stonehouse

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • M. A. Dawson

    (Peter MacCallum Cancer Centre
    The University of Melbourne
    The University of Melbourne)

  • D. J. Hilton

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • S. H. Naik

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

  • S. Taoudi

    (The Walter and Eliza Hall Institute of Medical Research
    The University of Melbourne)

Abstract

During embryogenesis, haematopoietic and endothelial lineages emerge closely in time and space. It is thought that the first blood and endothelium derive from a common clonal ancestor, the haemangioblast. However, investigation of candidate haemangioblasts in vitro revealed the capacity for mesenchymal differentiation, a feature more compatible with an earlier mesodermal precursor. To date, no evidence for an in vivo haemangioblast has been discovered. Using single cell RNA-Sequencing and in vivo cellular barcoding, we have unravelled the ancestral relationships that give rise to the haematopoietic lineages of the yolk sac, the endothelium, and the mesenchyme. We show that the mesodermal derivatives of the yolk sac are produced by three distinct precursors with dual-lineage outcomes: the haemangioblast, the mesenchymoangioblast, and a previously undescribed cell type: the haematomesoblast. Between E5.5 and E7.5, this trio of precursors seeds haematopoietic, endothelial, and mesenchymal trajectories.

Suggested Citation

  • C. Biben & T. S. Weber & K. S. Potts & J. Choi & D. C. Miles & A. Carmagnac & T. Sargeant & C. A. Graaf & K. A. Fennell & A. Farley & O. J. Stonehouse & M. A. Dawson & D. J. Hilton & S. H. Naik & S. T, 2023. "In vivo clonal tracking reveals evidence of haemangioblast and haematomesoblast contribution to yolk sac haematopoiesis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35744-x
    DOI: 10.1038/s41467-022-35744-x
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    1. Andrea Ventura & David G. Kirsch & Margaret E. McLaughlin & David A. Tuveson & Jan Grimm & Laura Lintault & Jamie Newman & Elizabeth E. Reczek & Ralph Weissleder & Tyler Jacks, 2007. "Restoration of p53 function leads to tumour regression in vivo," Nature, Nature, vol. 445(7128), pages 661-665, February.
    2. Elisa Gomez Perdiguero & Kay Klapproth & Christian Schulz & Katrin Busch & Emanuele Azzoni & Lucile Crozet & Hannah Garner & Celine Trouillet & Marella F. de Bruijn & Frederic Geissmann & Hans-Reimer , 2015. "Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors," Nature, Nature, vol. 518(7540), pages 547-551, February.
    3. Hanna M. Eilken & Shin-Ichi Nishikawa & Timm Schroeder, 2009. "Continuous single-cell imaging of blood generation from haemogenic endothelium," Nature, Nature, vol. 457(7231), pages 896-900, February.
    4. Weike Pei & Thorsten B. Feyerabend & Jens Rössler & Xi Wang & Daniel Postrach & Katrin Busch & Immanuel Rode & Kay Klapproth & Nikolaus Dietlein & Claudia Quedenau & Wei Chen & Sascha Sauer & Stephan , 2017. "Polylox barcoding reveals haematopoietic stem cell fates realized in vivo," Nature, Nature, vol. 548(7668), pages 456-460, August.
    5. Christophe Lancrin & Patrycja Sroczynska & Catherine Stephenson & Terry Allen & Valerie Kouskoff & Georges Lacaud, 2009. "The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage," Nature, Nature, vol. 457(7231), pages 892-895, February.
    6. Michael J. Chen & Tomomasa Yokomizo & Brandon M. Zeigler & Elaine Dzierzak & Nancy A. Speck, 2009. "Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter," Nature, Nature, vol. 457(7231), pages 887-891, February.
    7. Alejo E. Rodriguez-Fraticelli & Samuel L. Wolock & Caleb S. Weinreb & Riccardo Panero & Sachin H. Patel & Maja Jankovic & Jianlong Sun & Raffaele A. Calogero & Allon M. Klein & Fernando D. Camargo, 2018. "Clonal analysis of lineage fate in native haematopoiesis," Nature, Nature, vol. 553(7687), pages 212-216, January.
    8. Gemma Swiers & Claudia Baumann & John O’Rourke & Eleni Giannoulatou & Stephen Taylor & Anagha Joshi & Victoria Moignard & Cristina Pina & Thomas Bee & Konstantinos D. Kokkaliaris & Momoko Yoshimoto & , 2013. "Early dynamic fate changes in haemogenic endothelium characterized at the single-cell level," Nature Communications, Nature, vol. 4(1), pages 1-10, December.
    9. Tara L. Huber & Valerie Kouskoff & H. Joerg Fehling & James Palis & Gordon Keller, 2004. "Haemangioblast commitment is initiated in the primitive streak of the mouse embryo," Nature, Nature, vol. 432(7017), pages 625-630, December.
    10. Blanca Pijuan-Sala & Jonathan A. Griffiths & Carolina Guibentif & Tom W. Hiscock & Wajid Jawaid & Fernando J. Calero-Nieto & Carla Mulas & Ximena Ibarra-Soria & Richard C. V. Tyser & Debbie Lee Lian H, 2019. "A single-cell molecular map of mouse gastrulation and early organogenesis," Nature, Nature, vol. 566(7745), pages 490-495, February.
    11. Jianlong Sun & Azucena Ramos & Brad Chapman & Jonathan B. Johnnidis & Linda Le & Yu-Jui Ho & Allon Klein & Oliver Hofmann & Fernando D. Camargo, 2014. "Clonal dynamics of native haematopoiesis," Nature, Nature, vol. 514(7522), pages 322-327, October.
    12. Antonio Scialdone & Yosuke Tanaka & Wajid Jawaid & Victoria Moignard & Nicola K. Wilson & Iain C. Macaulay & John C. Marioni & Berthold Göttgens, 2016. "Resolving early mesoderm diversification through single-cell expression profiling," Nature, Nature, vol. 535(7611), pages 289-293, July.
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