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CTCF loss has limited effects on global genome architecture in Drosophila despite critical regulatory functions

Author

Listed:
  • Anjali Kaushal

    (University of Lausanne)

  • Giriram Mohana

    (University of Lausanne)

  • Julien Dorier

    (University of Lausanne)

  • Isa Özdemir

    (University of Lausanne)

  • Arina Omer

    (The Center for Genome Architecture, Baylor College of Medicine)

  • Pascal Cousin

    (University of Lausanne)

  • Anastasiia Semenova

    (University of Lausanne)

  • Michael Taschner

    (University of Lausanne)

  • Oleksandr Dergai

    (University of Lausanne)

  • Flavia Marzetta

    (University of Lausanne
    Vital-IT, SIB Swiss Institute of Bioinformatics)

  • Christian Iseli

    (University of Lausanne)

  • Yossi Eliaz

    (The Center for Genome Architecture, Baylor College of Medicine
    University of Houston
    Rice University)

  • David Weisz

    (The Center for Genome Architecture, Baylor College of Medicine)

  • Muhammad Saad Shamim

    (The Center for Genome Architecture, Baylor College of Medicine
    Rice University
    Medical Scientist Training Program, Baylor College of Medicine)

  • Nicolas Guex

    (University of Lausanne)

  • Erez Lieberman Aiden

    (The Center for Genome Architecture, Baylor College of Medicine
    Rice University
    Department of Molecular and Human Genetics, Baylor College of Medicine
    Rice University)

  • Maria Cristina Gambetta

    (University of Lausanne)

Abstract

Vertebrate genomes are partitioned into contact domains defined by enhanced internal contact frequency and formed by two principal mechanisms: compartmentalization of transcriptionally active and inactive domains, and stalling of chromosomal loop-extruding cohesin by CTCF bound at domain boundaries. While Drosophila has widespread contact domains and CTCF, it is currently unclear whether CTCF-dependent domains exist in flies. We genetically ablate CTCF in Drosophila and examine impacts on genome folding and transcriptional regulation in the central nervous system. We find that CTCF is required to form a small fraction of all domain boundaries, while critically controlling expression patterns of certain genes and supporting nervous system function. We also find that CTCF recruits the pervasive boundary-associated factor Cp190 to CTCF-occupied boundaries and co-regulates a subset of genes near boundaries together with Cp190. These results highlight a profound difference in CTCF-requirement for genome folding in flies and vertebrates, in which a large fraction of boundaries are CTCF-dependent and suggest that CTCF has played mutable roles in genome architecture and direct gene expression control during metazoan evolution.

Suggested Citation

  • Anjali Kaushal & Giriram Mohana & Julien Dorier & Isa Özdemir & Arina Omer & Pascal Cousin & Anastasiia Semenova & Michael Taschner & Oleksandr Dergai & Flavia Marzetta & Christian Iseli & Yossi Eliaz, 2021. "CTCF loss has limited effects on global genome architecture in Drosophila despite critical regulatory functions," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-21366-2
    DOI: 10.1038/s41467-021-21366-2
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    Cited by:

    1. Varvara Lukyanchikova & Miroslav Nuriddinov & Polina Belokopytova & Alena Taskina & Jiangtao Liang & Maarten J. M. F. Reijnders & Livio Ruzzante & Romain Feron & Robert M. Waterhouse & Yang Wu & Chunh, 2022. "Anopheles mosquitoes reveal new principles of 3D genome organization in insects," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    2. Thais Ealo & Victor Sanchez-Gaya & Patricia Respuela & María Muñoz-San Martín & Elva Martin-Batista & Endika Haro & Alvaro Rada-Iglesias, 2024. "Cooperative insulation of regulatory domains by CTCF-dependent physical insulation and promoter competition," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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