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

Anjali Kaushal, Giriram Mohana, Julien Dorier, Isa Özdemir, Arina Omer, Pascal Cousin, Anastasiia Semenova, Michael Taschner, Oleksandr Dergai, Flavia Marzetta, Christian Iseli, Yossi Eliaz, David Weisz, Muhammad Saad Shamim, Nicolas Guex, Erez Lieberman Aiden () and Maria Cristina Gambetta ()
Additional contact information
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
Christian Iseli: University of Lausanne
Yossi Eliaz: The Center for Genome Architecture, Baylor College of Medicine
David Weisz: The Center for Genome Architecture, Baylor College of Medicine
Muhammad Saad Shamim: The Center for Genome Architecture, Baylor College of Medicine
Nicolas Guex: University of Lausanne
Erez Lieberman Aiden: The Center for Genome Architecture, Baylor College of Medicine
Maria Cristina Gambetta: University of Lausanne

Nature Communications, 2021, vol. 12, issue 1, 1-16

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-21366-2

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