IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-022-35744-x.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35744-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35744-x?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. 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. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    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. Mina N. F. Morcos & Congxin Li & Clara M. Munz & Alessandro Greco & Nicole Dressel & Susanne Reinhardt & Katrin Sameith & Andreas Dahl & Nils B. Becker & Axel Roers & Thomas Höfer & Alexander Gerbaule, 2022. "Fate mapping of hematopoietic stem cells reveals two pathways of native thrombopoiesis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Yu-Jung Tseng & Yuki Kageyama & Rebecca L. Murdaugh & Ayumi Kitano & Jong Hwan Kim & Kevin A. Hoegenauer & Jonathan Tiessen & Mackenzie H. Smith & Hidetaka Uryu & Koichi Takahashi & James F. Martin & , 2024. "Increased iron uptake by splenic hematopoietic stem cells promotes TET2-dependent erythroid regeneration," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Ran Wang & Xianfa Yang & Jiehui Chen & Lin Zhang & Jonathan A. Griffiths & Guizhong Cui & Yingying Chen & Yun Qian & Guangdun Peng & Jinsong Li & Liantang Wang & John C. Marioni & Patrick P. L. Tam & , 2023. "Time space and single-cell resolved tissue lineage trajectories and laterality of body plan at gastrulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. 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.
    5. Trent D. Hall & Hyunjin Kim & Mahmoud Dabbah & Jacquelyn A. Myers & Jeremy Chase Crawford & Antonio Morales-Hernandez & Claire E. Caprio & Pramika Sriram & Emilia Kooienga & Marta Derecka & Esther A. , 2022. "Murine fetal bone marrow does not support functional hematopoietic stem and progenitor cells until birth," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Grigorios Georgolopoulos & Nikoletta Psatha & Mineo Iwata & Andrew Nishida & Tannishtha Som & Minas Yiangou & John A. Stamatoyannopoulos & Jeff Vierstra, 2021. "Discrete regulatory modules instruct hematopoietic lineage commitment and differentiation," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    7. Ritsuko Nakai & Takafumi Yokota & Masahiro Tokunaga & Mikiro Takaishi & Tomomasa Yokomizo & Takao Sudo & Henyun Shi & Yoshiaki Yasumizu & Daisuke Okuzaki & Chikara Kokubu & Sachiyo Tanaka & Katsuyoshi, 2024. "A newly identified gene Ahed plays essential roles in murine haematopoiesis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Natthakan Thongon & Feiyang Ma & Andrea Santoni & Matteo Marchesini & Elena Fiorini & Ashley Rose & Vera Adema & Irene Ganan-Gomez & Emma M. Groarke & Fernanda Gutierrez-Rodrigues & Shuaitong Chen & P, 2021. "Hematopoiesis under telomere attrition at the single-cell resolution," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    9. Qiang Zhao & Young-Min Han & Ping Song & Zhixue Liu & Zuyi Yuan & Ming-Hui Zou, 2022. "Endothelial cell-specific expression of serine/threonine kinase 11 modulates dendritic cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    10. Patrick Coulombe & Grace Cole & Amanda Fentiman & Jeremy D. K. Parker & Eric Yung & Misha Bilenky & Lemlem Degefie & Patrick Lac & Maggie Y. M. Ling & Derek Tam & R. Keith Humphries & Aly Karsan, 2023. "Meis1 establishes the pre-hemogenic endothelial state prior to Runx1 expression," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. B. Edginton-White & A. Maytum & S. G. Kellaway & D. K. Goode & P. Keane & I. Pagnuco & S. A. Assi & L. Ames & M. Clarke & P. N. Cockerill & B. Göttgens & J. B. Cazier & C. Bonifer, 2023. "A genome-wide relay of signalling-responsive enhancers drives hematopoietic specification," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    12. D. M. Jeziorska & E. A. J. Tunnacliffe & J. M. Brown & H. Ayyub & J. Sloane-Stanley & J. A. Sharpe & B. C. Lagerholm & C. Babbs & A. J. H. Smith & V. J. Buckle & D. R. Higgs, 2022. "On-microscope staging of live cells reveals changes in the dynamics of transcriptional bursting during differentiation," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    13. Geethika Arekatla & Stavroula Skylaki & David Corredor Suarez & Hartland Jackson & Denis Schapiro & Stefanie Engler & Markus Auler & German Camargo Ortega & Simon Hastreiter & Andreas Reimann & Dirk L, 2024. "Identification of an embryonic differentiation stage marked by Sox1 and FoxA2 co-expression using combined cell tracking and high dimensional protein imaging," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Zaniah N. Gonzalez Galofre & Alastair M. Kilpatrick & Madalena Marques & Diana Sá da Bandeira & Telma Ventura & Mario Gomez Salazar & Léa Bouilleau & Yvan Marc & Ana B. Barbosa & Fiona Rossi & Mariana, 2024. "Runx1+ vascular smooth muscle cells are essential for hematopoietic stem and progenitor cell development in vivo," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Kristoffer Sølvsten Burgdorf & Niels Grarup & Johanne Marie Justesen & Marie Neergaard Harder & Daniel Rinse Witte & Torben Jørgensen & Annelli Sandbæk & Torsten Lauritzen & Sten Madsbad & Torben Hans, 2011. "Studies of the Association of Arg72Pro of Tumor Suppressor Protein p53 with Type 2 Diabetes in a Combined Analysis of 55,521 Europeans," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-6, January.
    16. Brian DeVeale & Leqian Liu & Ryan Boileau & Jennifer Swindlehurst-Chan & Bryan Marsh & Jacob W. Freimer & Adam Abate & Robert Blelloch, 2022. "G1/S restriction point coordinates phasic gene expression and cell differentiation," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    17. Shambhu Yadav & Markus Waldeck-Weiermair & Fotios Spyropoulos & Roderick Bronson & Arvind K. Pandey & Apabrita Ayan Das & Alexander C. Sisti & Taylor A. Covington & Venkata Thulabandu & Shari Caplan &, 2023. "Sensory ataxia and cardiac hypertrophy caused by neurovascular oxidative stress in chemogenetic transgenic mouse lines," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Javier Rodríguez-Ubreva & Anna Arutyunyan & Marc Jan Bonder & Lucía Del Pino-Molina & Stephen J. Clark & Carlos de la Calle-Fabregat & Luz Garcia-Alonso & Louis-François Handfield & Laura Ciudad & Edu, 2022. "Single-cell Atlas of common variable immunodeficiency shows germinal center-associated epigenetic dysregulation in B-cell responses," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    19. Luke Simpson & Andrew Strange & Doris Klisch & Sophie Kraunsoe & Takuya Azami & Daniel Goszczynski & Triet Minh & Benjamin Planells & Nadine Holmes & Fei Sang & Sonal Henson & Matthew Loose & Jennifer, 2024. "A single-cell atlas of pig gastrulation as a resource for comparative embryology," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    20. Daniel H Rapoport & Tim Becker & Amir Madany Mamlouk & Simone Schicktanz & Charli Kruse, 2011. "A Novel Validation Algorithm Allows for Automated Cell Tracking and the Extraction of Biologically Meaningful Parameters," PLOS ONE, Public Library of Science, vol. 6(11), pages 1-16, November.

    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_s41467-022-35744-x. 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.