Reprogramming of the transcriptome after heat stress mediates heat hormesis in Caenorhabditis elegans

Abstract

Transient stress experiences not only trigger acute stress responses, but can also have long-lasting effects on cellular functions. In Caenorhabditis elegans, a brief exposure to heat shock during early adulthood extends lifespan and improves stress resistance, a phenomenon known as heat hormesis. Here, we investigated the prolonged effect of hormetic heat stress on the transcriptome of worms and found that the canonical heat shock response is followed by a profound transcriptional reprogramming in the post-stress period. This reprogramming relies on the endoribonuclease ENDU-2 but not the heat shock factor 1. ENDU-2 co-localizes with chromatin and interacts with RNA polymerase II, enabling specific regulation of transcription after the stress period. Failure to activate the post-stress response does not affect the resistance of animals to heat shock but eliminates the beneficial effects of hormetic heat stress. In summary, our work discovers that the RNA-binding protein ENDU-2 mediates the long-term impacts of transient heat stress via reprogramming transcriptome after stress exposure.

Expression of Truncated Products at the 5′-Terminal Region of RIPK2 and Evolutive Aspects that Support Their Biological Importance

“…Hyperthermic stress effects have been studied in many organisms, and cell line models. The examples include clinical responses in humans ( Wetsel 2011 ; Cui and Sinoway 2014 ), transcriptome alterations in Caenorhabditis elegans ( Xu, et al 2023 ), Drosophila, yeast, mouse, human (reviewed by ( Pessa, et al 2024 )), and in cancer cells ( Scutigliani, et al 2022 ). In contrast, cold-shock stress has been less well investigated, and little is known about the underlying mechanisms involved in responses to hypothermia, which can occur as a response to a drug, disease or exposure to the cold.…”

Icariin Improves Stress Resistance and Extends Lifespan in Caenorhabditis elegans through hsf-1 and daf-2-Driven Hormesis

“…Hormesis in aging suggests that moderate stress can confer physiological benefits by activating protective mechanisms within cells and organisms. This response to stressors, whether physical, physiological, biological, or nutritional, triggers a cascade of processes that influence adaptation and longevity, collectively referred to as the stress response [ 40 , 41 , 57 ]. In C. elegans , various types of stressors induce hormesis, interacting with the metabolome, transcriptome, and proteome, respectively.…”

“…In C. elegans , various types of stressors induce hormesis, interacting with the metabolome, transcriptome, and proteome, respectively. Brief exposure to heat shock during early adulthood extends the lifespan of worms and enhances resistance to high levels of stressors [ 57 ]. Hypoxic stress in worms is another example of hormesis, particularly induced in mild doses and associated with the gustatory sensory system [ 58 ].…”

“…Its modulation is associated with certain late-life diseases linked to aging, such as metabolic disturbances and obesity. The HSF-1 is an evolutionarily conserved protein linked to the response to different stressors [ 57 , 63 ]. Furthermore, HSF-1 is associated with the maintenance of proteostasis integrity and the regulation of mitochondrial function during the aging process [ 64 ].…”

A laser‐Engraved Wearable Electrochemical Sensing Patch for Heat Stress Precise Individual Management of Horse

“…[ 1 , 2 , 3 ] Normally, the animals present limited adaptability to environmental temperatures, rendering them vulnerable to heat stress when exposed to temperatures beyond their tolerance limits. [ 4 , 5 , 6 ] Heat stress reveals adverse influence on the psychological and physiological of animals, and potentially endangering their health in husbandry breeding. [ 7 , 8 ] Especially, as a specific mammalian species, the horses are prone to heat stress due to their limited capacity for self‐temperature regulation, which can result in various physiological disruptions, including elevated body temperature, increased respiratory rate, dehydration, and impaired immune function.…”