Research ArticleCell Biology

Olfactory experience primes the heat shock transcription factor HSF-1 to enhance the expression of molecular chaperones in C. elegans

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Sci. Signal.  17 Oct 2017:
Vol. 10, Issue 501, eaan4893
DOI: 10.1126/scisignal.aan4893

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Learning the smell of danger

The best way to prevent pathogen-induced cellular damage is to avoid becoming infected. If that is not possible, being prepared to fight damage is the next-best option. Ooi and Prahlad found that previous experience of the odor of a pathogenic bacterium enhanced the pathogen avoidance response of the nematode Caenorhabditis elegans. In addition, this experience enhanced heat shock factor 1 (HSF-1) target gene expression when animals encountered the pathogen, thus increasing survival. Olfactory experience of the pathogen odor alone caused HSF-1 to accumulate at genomic loci enriched for RNA polymerase II. These responses required serotonergic signaling, which is important for learning and memory. The activation of HSF-1 and chaperone expression has been considered an autonomous reaction of cells to protein damage. Instead, the authors show that in C. elegans, olfactory learning can initiate HSF-1–dependent chaperone gene expression systemically in anticipation of a proteotoxic encounter.

Abstract

Learning, a process by which animals modify their behavior as a result of experience, enables organisms to synthesize information from their surroundings to acquire resources and avoid danger. We showed that a previous encounter with only the odor of pathogenic bacteria prepared Caenorhabditis elegans to survive exposure to the pathogen by increasing the heat shock factor 1 (HSF-1)–dependent expression of genes encoding molecular chaperones. Experience-mediated enhancement of chaperone gene expression required serotonin, which primed HSF-1 to enhance the expression of molecular chaperone genes by promoting its localization to RNA polymerase II–enriched nuclear loci, even before transcription occurred. However, HSF-1–dependent chaperone gene expression was stimulated only if and when animals encountered the pathogen. Thus, learning equips C. elegans to better survive environmental dangers by preemptively and specifically initiating transcriptional mechanisms throughout the whole organism that prepare the animal to respond rapidly to proteotoxic agents. These studies provide one plausible basis for the protective role of environmental enrichment in disease.

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