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Dynamics of genome architecture and chromatin function during human B cell differentiation and neoplastic transformation

Author

Listed:
  • Roser Vilarrasa-Blasi

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)
    Facultat de Medicina, Universitat de Barcelona)

  • Paula Soler-Vila

    (CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST))

  • Núria Verdaguer-Dot

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

  • Núria Russiñol

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

  • Marco Stefano

    (CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST))

  • Vicente Chapaprieta

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

  • Guillem Clot

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)
    Centro de Investigación Biomédica en Red de Cáncer (CIBERONC))

  • Irene Farabella

    (CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST))

  • Pol Cuscó

    (Gastrointestinal and Endocrine Tumors Group, Vall d’Hebron Institute of Oncology (VHIO))

  • Marta Kulis

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

  • Xabier Agirre

    (Centro de Investigación Biomédica en Red de Cáncer (CIBERONC)
    Universidad de Navarra)

  • Felipe Prosper

    (Centro de Investigación Biomédica en Red de Cáncer (CIBERONC)
    Universidad de Navarra
    Clínica Universidad de Navarra, Universidad de Navarra)

  • Renée Beekman

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS))

  • Silvia Beà

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)
    Centro de Investigación Biomédica en Red de Cáncer (CIBERONC))

  • Dolors Colomer

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)
    Centro de Investigación Biomédica en Red de Cáncer (CIBERONC)
    Hematopathology Section, Hospital Clinic of Barcelona)

  • Hendrik G. Stunnenberg

    (Radboud University)

  • Ivo Gut

    (CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
    Universitat Pompeu Fabra (UPF))

  • Elias Campo

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)
    Facultat de Medicina, Universitat de Barcelona
    Centro de Investigación Biomédica en Red de Cáncer (CIBERONC))

  • Marc A. Marti-Renom

    (CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST)
    Universitat Pompeu Fabra (UPF)
    Institució Catalana de Recerca i Estudis Avançats (ICREA)
    Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST))

  • José Ignacio Martin-Subero

    (Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS)
    Facultat de Medicina, Universitat de Barcelona
    Centro de Investigación Biomédica en Red de Cáncer (CIBERONC)
    Institució Catalana de Recerca i Estudis Avançats (ICREA))

Abstract

To investigate the three-dimensional (3D) genome architecture across normal B cell differentiation and in neoplastic cells from different subtypes of chronic lymphocytic leukemia and mantle cell lymphoma patients, here we integrate in situ Hi-C and nine additional omics layers. Beyond conventional active (A) and inactive (B) compartments, we uncover a highly-dynamic intermediate compartment enriched in poised and polycomb-repressed chromatin. During B cell development, 28% of the compartments change, mostly involving a widespread chromatin activation from naive to germinal center B cells and a reversal to the naive state upon further maturation into memory B cells. B cell neoplasms are characterized by both entity and subtype-specific alterations in 3D genome organization, including large chromatin blocks spanning key disease-specific genes. This study indicates that 3D genome interactions are extensively modulated during normal B cell differentiation and that the genome of B cell neoplasias acquires a tumor-specific 3D genome architecture.

Suggested Citation

  • Roser Vilarrasa-Blasi & Paula Soler-Vila & Núria Verdaguer-Dot & Núria Russiñol & Marco Stefano & Vicente Chapaprieta & Guillem Clot & Irene Farabella & Pol Cuscó & Marta Kulis & Xabier Agirre & Felip, 2021. "Dynamics of genome architecture and chromatin function during human B cell differentiation and neoplastic transformation," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-020-20849-y
    DOI: 10.1038/s41467-020-20849-y
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    Cited by:

    1. Milad Mokhtaridoost & Jordan J. Chalmers & Marzieh Soleimanpoor & Brandon J. McMurray & Daniella F. Lato & Son C. Nguyen & Viktoria Musienko & Joshua O. Nash & Sergio Espeso-Gil & Sameen Ahmed & Kate , 2024. "Inter-chromosomal contacts demarcate genome topology along a spatial gradient," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Laureano Tomás-Daza & Llorenç Rovirosa & Paula López-Martí & Andrea Nieto-Aliseda & François Serra & Ainoa Planas-Riverola & Oscar Molina & Rebecca McDonald & Cedric Ghevaert & Esther Cuatrecasas & Do, 2023. "Low input capture Hi-C (liCHi-C) identifies promoter-enhancer interactions at high-resolution," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Hannah L. Harris & Huiya Gu & Moshe Olshansky & Ailun Wang & Irene Farabella & Yossi Eliaz & Achyuth Kalluchi & Akshay Krishna & Mozes Jacobs & Gesine Cauer & Melanie Pham & Suhas S. P. Rao & Olga Dud, 2023. "Chromatin alternates between A and B compartments at kilobase scale for subgenic organization," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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