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Direct ionic stress sensing and mitigation by the transcription factor NFAT5.

Chandni B Khandwala1, Parijat Sarkar1, H Broder Schmidt1

  • 1Departments of Biochemistry and Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA.

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Animal cells possess a novel mechanism to detect and manage ionic stress using the NFAT5 protein. This protein

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Area of Science:

  • Cellular Biology
  • Molecular Mechanisms
  • Environmental Stress Response

Background:

  • Climate change-induced rising temperatures and water scarcity elevate cellular ionic strength, causing ionic stress.
  • Ionic stress disrupts essential cellular functions, including protein, organelle, and genome integrity.
  • Existing knowledge lacks a clear understanding of how animal cells sense and mitigate intracellular ionic stress.

Purpose of the Study:

  • To identify and characterize the molecular mechanism by which animal cells sense and respond to intracellular ionic strength.
  • To elucidate the role of the NFAT5 protein in mediating cellular adaptation to ionic stress.
  • To compare the animal cell response to ionic stress with known mechanisms in other organisms, such as yeast.

Main Methods:

  • Investigated the function of the transcription factor NFAT5 and its C-terminal prion-like domain (PLD) in sensing ionic strength.
  • Utilized in vitro assays to observe the formation of condensates by the purified NFAT5 PLD under varying ionic strengths.
  • Employed yeast models to assess the sufficiency of human NFAT5 in reconstituting a transcriptional response to ionic stress.

Main Results:

  • Identified NFAT5 as a direct sensor of intracellular ionic strength, utilizing its C-terminal prion-like domain (PLD).
  • Demonstrated that the NFAT5 PLD is essential and sufficient for coordinating an adaptive gene expression program via BRD4 recruitment.
  • Showcased the ability of purified NFAT5 PLD to form condensates in vitro at elevated ionic strengths and human NFAT5 to rescue yeast ionic stress response.

Conclusions:

  • NFAT5 acts as a single-protein sensor for intracellular ionic strength in animal cells.
  • The NFAT5 PLD directly regulates transcription through ion-sensitive conformational changes to maintain ionic homeostasis.
  • This mechanism represents a distinct pathway for ionic stress mitigation compared to the yeast high osmolarity glycerol pathway.