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Different NIPBL requirements of cohesin-STAG1 and cohesin-STAG2

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  • Dácil Alonso-Gil

    (Chromosome Dynamics Group, Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO))

  • Ana Cuadrado

    (Chromosome Dynamics Group, Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO))

  • Daniel Giménez-Llorente

    (Chromosome Dynamics Group, Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO))

  • Miriam Rodríguez-Corsino

    (Chromosome Dynamics Group, Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO))

  • Ana Losada

    (Chromosome Dynamics Group, Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO))

Abstract

Cohesin organizes the genome through the formation of chromatin loops. NIPBL activates cohesin’s ATPase and is essential for loop extrusion, but its requirement for cohesin loading is unclear. Here we have examined the effect of reducing NIPBL levels on the behavior of the two cohesin variants carrying STAG1 or STAG2 by combining a flow cytometry assay to measure chromatin-bound cohesin with analyses of its genome-wide distribution and genome contacts. We show that NIPBL depletion results in increased cohesin-STAG1 on chromatin that further accumulates at CTCF positions while cohesin-STAG2 diminishes genome-wide. Our data are consistent with a model in which NIPBL may not be required for chromatin association of cohesin but it is for loop extrusion, which in turn facilitates stabilization of cohesin-STAG2 at CTCF positions after being loaded elsewhere. In contrast, cohesin-STAG1 binds chromatin and becomes stabilized at CTCF sites even under low NIPBL levels, but genome folding is severely impaired.

Suggested Citation

  • Dácil Alonso-Gil & Ana Cuadrado & Daniel Giménez-Llorente & Miriam Rodríguez-Corsino & Ana Losada, 2023. "Different NIPBL requirements of cohesin-STAG1 and cohesin-STAG2," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36900-7
    DOI: 10.1038/s41467-023-36900-7
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    References listed on IDEAS

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    1. Georg A. Busslinger & Roman R. Stocsits & Petra van der Lelij & Elin Axelsson & Antonio Tedeschi & Niels Galjart & Jan-Michael Peters, 2017. "Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl," Nature, Nature, vol. 544(7651), pages 503-507, April.
    2. Armelle Lengronne & Yuki Katou & Saori Mori & Shihori Yokobayashi & Gavin P. Kelly & Takehiko Itoh & Yoshinori Watanabe & Katsuhiko Shirahige & Frank Uhlmann, 2004. "Cohesin relocation from sites of chromosomal loading to places of convergent transcription," Nature, Nature, vol. 430(6999), pages 573-578, July.
    3. Wibke Schwarzer & Nezar Abdennur & Anton Goloborodko & Aleksandra Pekowska & Geoffrey Fudenberg & Yann Loe-Mie & Nuno A Fonseca & Wolfgang Huber & Christian H. Haering & Leonid Mirny & Francois Spitz, 2017. "Two independent modes of chromatin organization revealed by cohesin removal," Nature, Nature, vol. 551(7678), pages 51-56, November.
    4. Yan Li & Judith H. I. Haarhuis & Ángela Sedeño Cacciatore & Roel Oldenkamp & Marjon S. Ruiten & Laureen Willems & Hans Teunissen & Kyle W. Muir & Elzo Wit & Benjamin D. Rowland & Daniel Panne, 2020. "The structural basis for cohesin–CTCF-anchored loops," Nature, Nature, vol. 578(7795), pages 472-476, February.
    5. Patricia Garcia & Rita Fernandez-Hernandez & Ana Cuadrado & Ignacio Coca & Antonio Gomez & Maria Maqueda & Ana Latorre-Pellicer & Beatriz Puisac & Feliciano J. Ramos & Juan Sandoval & Manel Esteller &, 2021. "Disruption of NIPBL/Scc2 in Cornelia de Lange Syndrome provokes cohesin genome-wide redistribution with an impact in the transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    6. Yasuto Murayama & Frank Uhlmann, 2014. "Biochemical reconstitution of topological DNA binding by the cohesin ring," Nature, Nature, vol. 505(7483), pages 367-371, January.
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