HSF1 is required for cellular adaptation to daily temperature fluctuations

• Published in: Scientific reports 2024-09, Vol.14 (1), p.21361-16, Article 21361
• Main Authors: Takii, Ryosuke, Fujimoto, Mitsuaki, Pandey, Akanksha, Jaiswal, Kritika, Shearwin-Whyatt, Linda, Grutzner, Frank, Nakai, Akira
• Format: Article
• Language: English
• Subjects: 631/45; 631/80; Adaptation; Adaptation, Physiological - genetics; Animals; Cell Proliferation; Cell Survival - genetics; Chickens - genetics; Ectopic expression; Egg laying; Fluctuations; Gene regulation; Heat; Heat resistance; Heat shock; Heat shock factors; Heat shock proteins; Heat shock transcription factor; Heat Shock Transcription Factors - genetics; Heat Shock Transcription Factors - metabolism; Heat-Shock Proteins - genetics; Heat-Shock Proteins - metabolism; Heat-Shock Response - genetics; Heat-Shock Response - physiology; High temperature; HSF1 protein; Humanities and Social Sciences; Humans; Mice; multidisciplinary; Null cells; Proteins; Science; Science (multidisciplinary); Temperature; Temperature fluctuation; Temperature requirements; Transcription; Vertebrate; Vertebrates
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-024-72415-x

The heat shock response (HSR) is a universal mechanism of cellular adaptation to elevated temperatures and is regulated by heat shock transcription factor 1 (HSF1) or HSF3 in vertebrate endotherms, such as humans, mice, and chickens. We here showed that HSF1 and HSF3 from egg-laying mammals (monotremes), with a low homeothermic capacity, equally possess a potential to maximally induce the HSR, whereas either HSF1 or HSF3 from birds have this potential. Therefore, we focused on cellular adaptation to daily temperature fluctuations and found that HSF1 was required for the proliferation and survival of human cells under daily temperature fluctuations. The ectopic expression of vertebrate HSF1 proteins, but not HSF3 proteins, restored the resistance in HSF1-null cells, regardless of the induction of heat shock proteins. This function was associated with the up-regulation of specific HSF1-target genes. These results indicate the distinct role of HSF1 in adaptation to thermally fluctuating environments and suggest association of homeothermic capacity with functional diversification of vertebrate HSF genes.