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1 Department of Physiology, The Hebrew University, Hadassah Medical School, Jerusalem, Israel
2 Division of Physiology, The Hebrew University, Hadassah Dental Medicine, Jerusalem, Israel
3 Department of Zoology and Genetics, Iowa State University, Ames, Iowa, USA
4 Department of Physiology, The Hebrew University, Hadassah Medical School, Jerusalem, Israel; Division of Physiology, The Hebrew University, Hadassah Dental Medicine, Jerusalem, Israel
* To whom correspondence should be addressed. E-mail: horowitz{at}cc.huji.ac.il.
Chronic exposure to environmental heat improves tolerance via heat acclimation (AC). Our previous data on mammals indicate that reprogramming the expression of genes coding for stress proteins and energy-metabolism enzymes plays a major role. Knowledge of pathways leading to AC is limited. For their identification, we established a Caenorhabditis elegans AC model and tested mutants in which signaling pathways pertinent to acclimatory responses are mutated. AC attained by maintaining adult C. elegans at 25°C for 18 hrs enhanced heat endurance of wild-type worms subjected to heat-stress (35°C) and conferred protection against hypoxia and cadmium. Survival curves demonstrated that both daf-2 (insulin receptor pathway) showing enhanced heat tolerance and daf-16 loss-of-function (a transcription factor mediating DAF-2 signaling) mutants benefit from AC, suggesting that the insulin receptor pathway does not mediate AC. In contrast, the hif-1 (hypoxia inducible factor) loss-of-function strain did not show acclimation, and non-acclimated vhl-1 and egl-9 mutants (overexpressing HIF-1) had greater heat endurance than the wild-type. Like mammals, HIF-1 and HSP72 levels increased in the wild-type AC nematodes. HSP72 upregulation in AC hif-1 mutants was also observed; however, it was insufficient to improve heat/stress tolerance, suggesting that HIF-1 upregulation is essential for acclimation, while HSP72 upregulation in the absence of HIF-1 is inadequate. We conclude that HIF-1 upregulation is both an evolutionarily conserved and a necessary component of heat acclimation. The known targets of HIF-1 imply that metabolic adaptations are essential for AC-dependent tolerance to heat and heavy metals, in addition to their known role in hypoxic adaptation.
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