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A human neural crest model reveals the developmental impact of neuroblastoma-associated chromosomal aberrations

Author

Listed:
  • Ingrid M. Saldana-Guerrero

    (The University of Sheffield
    The University of Sheffield
    The University of Sheffield)

  • Luis F. Montano-Gutierrez

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Katy Boswell

    (The University of Sheffield
    The University of Sheffield)

  • Christoph Hafemeister

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Evon Poon

    (The Institute of Cancer Research (ICR) & Royal Marsden NHS Trust)

  • Lisa E. Shaw

    (Medical University of Vienna)

  • Dylan Stavish

    (The University of Sheffield
    The University of Sheffield)

  • Rebecca A. Lea

    (The University of Sheffield
    The University of Sheffield)

  • Sara Wernig-Zorc

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Eva Bozsaky

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Irfete S. Fetahu

    (St. Anna Children’s Cancer Research Institute (CCRI)
    Department of Neurology, Division of Neuropathology and Neurochemistry)

  • Peter Zoescher

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Ulrike Pötschger

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Marie Bernkopf

    (St. Anna Children’s Cancer Research Institute (CCRI)
    Labdia Labordiagnostik GmbH)

  • Andrea Wenninger-Weinzierl

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Caterina Sturtzel

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Celine Souilhol

    (The University of Sheffield
    The University of Sheffield
    Sheffield Hallam University)

  • Sophia Tarelli

    (The University of Sheffield
    The University of Sheffield)

  • Mohamed R. Shoeb

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Polyxeni Bozatzi

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Magdalena Rados

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Maria Guarini

    (CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Michelle C. Buri

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Wolfgang Weninger

    (Medical University of Vienna)

  • Eva M. Putz

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Miller Huang

    (Cancer and Blood Disease Institutes, and The Saban Research Institute
    University of Southern California)

  • Ruth Ladenstein

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Peter W. Andrews

    (The University of Sheffield)

  • Ivana Barbaric

    (The University of Sheffield
    The University of Sheffield)

  • George D. Cresswell

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Helen E. Bryant

    (The University of Sheffield)

  • Martin Distel

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Louis Chesler

    (The Institute of Cancer Research (ICR) & Royal Marsden NHS Trust)

  • Sabine Taschner-Mandl

    (St. Anna Children’s Cancer Research Institute (CCRI))

  • Matthias Farlik

    (Medical University of Vienna)

  • Anestis Tsakiridis

    (The University of Sheffield
    The University of Sheffield)

  • Florian Halbritter

    (St. Anna Children’s Cancer Research Institute (CCRI))

Abstract

Early childhood tumours arise from transformed embryonic cells, which often carry large copy number alterations (CNA). However, it remains unclear how CNAs contribute to embryonic tumourigenesis due to a lack of suitable models. Here we employ female human embryonic stem cell (hESC) differentiation and single-cell transcriptome and epigenome analysis to assess the effects of chromosome 17q/1q gains, which are prevalent in the embryonal tumour neuroblastoma (NB). We show that CNAs impair the specification of trunk neural crest (NC) cells and their sympathoadrenal derivatives, the putative cells-of-origin of NB. This effect is exacerbated upon overexpression of MYCN, whose amplification co-occurs with CNAs in NB. Moreover, CNAs potentiate the pro-tumourigenic effects of MYCN and mutant NC cells resemble NB cells in tumours. These changes correlate with a stepwise aberration of developmental transcription factor networks. Together, our results sketch a mechanistic framework for the CNA-driven initiation of embryonal tumours.

Suggested Citation

  • Ingrid M. Saldana-Guerrero & Luis F. Montano-Gutierrez & Katy Boswell & Christoph Hafemeister & Evon Poon & Lisa E. Shaw & Dylan Stavish & Rebecca A. Lea & Sara Wernig-Zorc & Eva Bozsaky & Irfete S. F, 2024. "A human neural crest model reveals the developmental impact of neuroblastoma-associated chromosomal aberrations," Nature Communications, Nature, vol. 15(1), pages 1-25, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47945-7
    DOI: 10.1038/s41467-024-47945-7
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    as
    1. Tim Groningen & Nurdan Akogul & Ellen M. Westerhout & Alvin Chan & Nancy E. Hasselt & Danny A. Zwijnenburg & Marloes Broekmans & Peter Stroeken & Franciska Haneveld & Gerrit K. J. Hooijer & C. Dilara , 2019. "A NOTCH feed-forward loop drives reprogramming from adrenergic to mesenchymal state in neuroblastoma," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Bieke Decaesteker & Amber Louwagie & Siebe Loontiens & Fanny De Vloed & Sarah-Lee Bekaert & Juliette Roels & Suzanne Vanhauwaert & Sara De Brouwer & Ellen Sanders & Alla Berezovskaya & Geertrui Deneck, 2023. "SOX11 regulates SWI/SNF complex components as member of the adrenergic neuroblastoma core regulatory circuitry," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Xiaotu Ma & Yu Liu & Yanling Liu & Ludmil B. Alexandrov & Michael N. Edmonson & Charles Gawad & Xin Zhou & Yongjin Li & Michael C. Rusch & John Easton & Robert Huether & Veronica Gonzalez-Pena & Mark , 2018. "Pan-cancer genome and transcriptome analyses of 1,699 paediatric leukaemias and solid tumours," Nature, Nature, vol. 555(7696), pages 371-376, March.
    4. Koen Van den Berge & Hector Roux de Bézieux & Kelly Street & Wouter Saelens & Robrecht Cannoodt & Yvan Saeys & Sandrine Dudoit & Lieven Clement, 2020. "Trajectory-based differential expression analysis for single-cell sequencing data," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    5. Wouter Meuleman & Alexander Muratov & Eric Rynes & Jessica Halow & Kristen Lee & Daniel Bates & Morgan Diegel & Douglas Dunn & Fidencio Neri & Athanasios Teodosiadis & Alex Reynolds & Eric Haugen & Je, 2020. "Index and biological spectrum of human DNase I hypersensitive sites," Nature, Nature, vol. 584(7820), pages 244-251, August.
    6. Cécile Thirant & Agathe Peltier & Simon Durand & Amira Kramdi & Caroline Louis-Brennetot & Cécile Pierre-Eugène & Margot Gautier & Ana Costa & Amandine Grelier & Sakina Zaïdi & Nadège Gruel & Irène Ji, 2023. "Reversible transitions between noradrenergic and mesenchymal tumor identities define cell plasticity in neuroblastoma," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Carles A. Boix & Benjamin T. James & Yongjin P. Park & Wouter Meuleman & Manolis Kellis, 2021. "Regulatory genomic circuitry of human disease loci by integrative epigenomics," Nature, Nature, vol. 590(7845), pages 300-307, February.
    8. Myrthala Moreno-Smith & Giorgio Milazzo & Ling Tao & Baharan Fekry & Bokai Zhu & Mahmoud A. Mohammad & Simone Giacomo & Roshan Borkar & Karthik Reddy Kami Reddy & Mario Capasso & Sanjeev A. Vasudevan , 2021. "Restoration of the molecular clock is tumor suppressive in neuroblastoma," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    9. Jan J. Molenaar & Jan Koster & Danny A. Zwijnenburg & Peter van Sluis & Linda J. Valentijn & Ida van der Ploeg & Mohamed Hamdi & Johan van Nes & Bart A. Westerman & Jennemiek van Arkel & Marli E. Ebus, 2012. "Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes," Nature, Nature, vol. 483(7391), pages 589-593, March.
    10. Irfete S. Fetahu & Wolfgang Esser-Skala & Rohit Dnyansagar & Samuel Sindelar & Fikret Rifatbegovic & Andrea Bileck & Lukas Skos & Eva Bozsaky & Daria Lazic & Lisa Shaw & Marcus Tötzl & Dora Tarlungean, 2023. "Single-cell transcriptomics and epigenomics unravel the role of monocytes in neuroblastoma bone marrow metastasis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
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