An HSF1-JMJD6-HSP feedback circuit promotes cell adaptation to proteotoxic stress

Proc Natl Acad Sci U S A. 2024 Jul 16;121(29):e2313370121. doi: 10.1073/pnas.2313370121. Epub 2024 Jul 10.

Abstract

Heat Shock Factor 1 (HSF1) is best known as the master transcriptional regulator of the heat-shock response (HSR), a conserved adaptive mechanism critical for protein homeostasis (proteostasis). Combining a genome-wide RNAi library with an HSR reporter, we identified Jumonji domain-containing protein 6 (JMJD6) as an essential mediator of HSF1 activity. In follow-up studies, we found that JMJD6 is itself a noncanonical transcriptional target of HSF1 which acts as a critical regulator of proteostasis. In a positive feedback circuit, HSF1 binds and promotes JMJD6 expression, which in turn reduces heat shock protein 70 (HSP70) R469 monomethylation to disrupt HSP70-HSF1 repressive complexes resulting in enhanced HSF1 activation. Thus, JMJD6 is intricately wired into the proteostasis network where it plays a critical role in cellular adaptation to proteotoxic stress.

Keywords: HSF1; JMJD6; proteostasis.

MeSH terms

  • Adaptation, Physiological
  • Feedback, Physiological
  • HEK293 Cells
  • HSP70 Heat-Shock Proteins* / genetics
  • HSP70 Heat-Shock Proteins* / metabolism
  • Heat Shock Transcription Factors* / genetics
  • Heat Shock Transcription Factors* / metabolism
  • Heat-Shock Response* / physiology
  • Humans
  • Jumonji Domain-Containing Histone Demethylases* / genetics
  • Jumonji Domain-Containing Histone Demethylases* / metabolism
  • Proteostasis* / physiology
  • Proteotoxic Stress

Substances

  • Heat Shock Transcription Factors
  • HSF1 protein, human
  • Jumonji Domain-Containing Histone Demethylases
  • HSP70 Heat-Shock Proteins