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Four-dimensional nuclear speckle phase separation dynamics regulate proteostasis.

William Dion1, Heather Ballance1, Jane Lee1

  • 1Aging Institute of UPMC, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.

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|January 5, 2022
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Summary
This summary is machine-generated.

A conserved XBP1s-SON axis drives a 12-hour ultradian rhythm in nuclear speckle liquid-liquid phase separation (LLPS), impacting proteostasis and offering a potential chrono-therapeutic target.

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Area of Science:

  • Cell biology
  • Molecular biology
  • Chronobiology

Background:

  • Biological processes are controlled by spatial (phase separation) and temporal (biorhythms) mechanisms.
  • The integration of these four-dimensional controls remains poorly understood.

Purpose of the Study:

  • To identify the mechanisms integrating spatial and temporal regulation of biological processes.
  • To investigate the role of the XBP1s-SON axis in mammalian ultradian rhythms.

Main Methods:

  • Identification of the evolutionarily conserved XBP1s-SON axis.
  • Analysis of nuclear speckle liquid-liquid phase separation (LLPS) dynamics.
  • Correlation of Son gene expression with proteostasis across the mouse lifespan.

Main Results:

  • The XBP1s-SON axis establishes a cell-autonomous 12-hour ultradian rhythm of nuclear speckle LLPS, independent of circadian and cell cycle clocks.
  • Elevated SON levels promote diffuse nuclear speckles, enhance chromatin interaction, and amplify the unfolded protein response, protecting against proteome stress.
  • Reduced SON levels exhibit opposite effects, highlighting a temporal regulation of proteostasis.

Conclusions:

  • The nuclear speckle LLPS, modulated by the XBP1s-SON axis, represents a novel ultradian rhythm impacting proteostasis.
  • This temporal regulation of proteostasis suggests nuclear speckle LLPS as a potential chrono-therapeutic target for proteostasis-related diseases.