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Cytoplasmic control of intranuclear polarity by human cytomegalovirus

Author

Listed:
  • Dean J. Procter

    (Northwestern University)

  • Colleen Furey

    (Northwestern University)

  • Arturo G. Garza-Gongora

    (Northwestern University)

  • Steven T. Kosak

    (Northwestern University)

  • Derek Walsh

    (Northwestern University)

Abstract

Despite its size and rigidity, the cell nucleus can be moved or reorganized by cytoskeletal filaments under various conditions (for example, during viral infection)1–11. Moreover, whereas chromatin organizes into non-random domains12, extensive heterogeneity at the single-cell level13 means that precisely how and why nuclei reorganize remains an area of intense investigation. Here we describe convolutional neural network-based automated cell classification and analysis pipelines, which revealed the extent to which human cytomegalovirus generates nuclear polarity through a virus-assembled microtubule-organizing centre. Acetylation of tubulin enables microtubules emanating from this centre to rotate the nucleus by engaging cytoplasmically exposed dynein-binding domains in the outer nuclear membrane protein nesprin-2G, which polarizes the inner nuclear membrane protein SUN1. This in turn creates intranuclear polarity in emerin, and thereby controls nuclear actin filaments that spatially segregate viral DNA from inactive histones and host DNA, maximizing virus replication. Our findings demonstrate the extent to which viruses can control the nucleus from the cytoplasm.

Suggested Citation

  • Dean J. Procter & Colleen Furey & Arturo G. Garza-Gongora & Steven T. Kosak & Derek Walsh, 2020. "Cytoplasmic control of intranuclear polarity by human cytomegalovirus," Nature, Nature, vol. 587(7832), pages 109-114, November.
  • Handle: RePEc:nat:nature:v:587:y:2020:i:7832:d:10.1038_s41586-020-2714-x
    DOI: 10.1038/s41586-020-2714-x
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    Cited by:

    1. Nathan Meade & Helen K. Toreev & Ram P. Chakrabarty & Charles R. Hesser & Chorong Park & Navdeep S. Chandel & Derek Walsh, 2023. "The poxvirus F17 protein counteracts mitochondrially orchestrated antiviral responses," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Alessandro Poli & Fabrizio A. Pennacchio & Andrea Ghisleni & Mariagrazia Gennaro & Margaux Lecacheur & Paulina Nastały & Michele Crestani & Francesca M. Pramotton & Fabio Iannelli & Galina Beznusenko , 2023. "PIP4K2B is mechanoresponsive and controls heterochromatin-driven nuclear softening through UHRF1," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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