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Interphase chromosomes of the Aedes aegypti mosquito are liquid crystalline and can sense mechanical cues

Author

Listed:
  • Vinícius G. Contessoto

    (Rice University
    UNESP - Univ. Estadual Paulista, Departamento de Física)

  • Olga Dudchenko

    (Rice University
    Baylor College of Medicine)

  • Erez Lieberman Aiden

    (Rice University
    Baylor College of Medicine)

  • Peter G. Wolynes

    (Rice University
    Rice University
    Rice University
    Rice University)

  • José N. Onuchic

    (Rice University
    Rice University
    Rice University
    Rice University)

  • Michele Pierro

    (Northeastern University
    Northeastern University)

Abstract

We use data-driven physical simulations to study the three-dimensional architecture of the Aedes aegypti genome. Hi-C maps exhibit both a broad diagonal and compartmentalization with telomeres and centromeres clustering together. Physical modeling reveals that these observations correspond to an ensemble of 3D chromosomal structures that are folded over and partially condensed. Clustering of the centromeres and telomeres near the nuclear lamina appears to be a necessary condition for the formation of the observed structures. Further analysis of the mechanical properties of the genome reveals that the chromosomes of Aedes aegypti, by virtue of their atypical structural organization, are highly sensitive to the deformation of the nuclei. This last finding provides a possible physical mechanism linking mechanical cues to gene regulation.

Suggested Citation

  • Vinícius G. Contessoto & Olga Dudchenko & Erez Lieberman Aiden & Peter G. Wolynes & José N. Onuchic & Michele Pierro, 2023. "Interphase chromosomes of the Aedes aegypti mosquito are liquid crystalline and can sense mechanical cues," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35909-2
    DOI: 10.1038/s41467-023-35909-2
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    References listed on IDEAS

    as
    1. Benjamin J. Matthews & Olga Dudchenko & Sarah B. Kingan & Sergey Koren & Igor Antoshechkin & Jacob E. Crawford & William J. Glassford & Margaret Herre & Seth N. Redmond & Noah H. Rose & Gareth D. Weed, 2018. "Improved reference genome of Aedes aegypti informs arbovirus vector control," Nature, Nature, vol. 563(7732), pages 501-507, November.
    2. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    3. Jumana AlHaj Abed & Jelena Erceg & Anton Goloborodko & Son C. Nguyen & Ruth B. McCole & Wren Saylor & Geoffrey Fudenberg & Bryan R. Lajoie & Job Dekker & Leonid A. Mirny & C.-ting Wu, 2019. "Highly structured homolog pairing reflects functional organization of the Drosophila genome," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
    4. 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.
    5. Martin Franke & Daniel M. Ibrahim & Guillaume Andrey & Wibke Schwarzer & Verena Heinrich & Robert Schöpflin & Katerina Kraft & Rieke Kempfer & Ivana Jerković & Wing-Lee Chan & Malte Spielmann & Bernd , 2016. "Formation of new chromatin domains determines pathogenicity of genomic duplications," Nature, Nature, vol. 538(7624), pages 265-269, October.
    6. Martin Falk & Yana Feodorova & Natalia Naumova & Maxim Imakaev & Bryan R. Lajoie & Heinrich Leonhardt & Boris Joffe & Job Dekker & Geoffrey Fudenberg & Irina Solovei & Leonid A. Mirny, 2019. "Heterochromatin drives compartmentalization of inverted and conventional nuclei," Nature, Nature, vol. 570(7761), pages 395-399, June.
    7. Esteban Dodero-Rojas & Luiza G Ferreira & Vitor B P Leite & José N Onuchic & Vinícius G Contessoto, 2020. "Modeling Chikungunya control strategies and Mayaro potential outbreak in the city of Rio de Janeiro," PLOS ONE, Public Library of Science, vol. 15(1), pages 1-13, January.
    8. Guang Shi & Lei Liu & Changbong Hyeon & D. Thirumalai, 2018. "Interphase human chromosome exhibits out of equilibrium glassy dynamics," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    9. Martin Falk & Yana Feodorova & Natalia Naumova & Maxim Imakaev & Bryan R. Lajoie & Heinrich Leonhardt & Boris Joffe & Job Dekker & Geoffrey Fudenberg & Irina Solovei & Leonid A. Mirny, 2019. "Publisher Correction: Heterochromatin drives compartmentalization of inverted and conventional nuclei," Nature, Nature, vol. 572(7771), pages 22-22, August.
    10. William A. Flavahan & Yotam Drier & Brian B. Liau & Shawn M. Gillespie & Andrew S. Venteicher & Anat O. Stemmer-Rachamimov & Mario L. Suvà & Bradley E. Bernstein, 2016. "Insulator dysfunction and oncogene activation in IDH mutant gliomas," Nature, Nature, vol. 529(7584), pages 110-114, January.
    11. Elphège P. Nora & Bryan R. Lajoie & Edda G. Schulz & Luca Giorgetti & Ikuhiro Okamoto & Nicolas Servant & Tristan Piolot & Nynke L. van Berkum & Johannes Meisig & John Sedat & Joost Gribnau & Emmanuel, 2012. "Spatial partitioning of the regulatory landscape of the X-inactivation centre," Nature, Nature, vol. 485(7398), pages 381-385, May.
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