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Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans

Abstract

Animals cope with environmental changes by altering behavioral strategy. Environmental information is generally received by sensory neurons in the neural circuit that generates behavior. However, although environmental temperature inevitably influences an animal's entire body, the mechanism of systemic temperature perception remains largely unknown. We show here that systemic temperature signaling induces a change in a memory-based behavior in C. elegans. During behavioral conditioning, non-neuronal cells as well as neuronal cells respond to cultivation temperature through a heat-shock transcription factor that drives newly identified gene expression dynamics. This systemic temperature signaling regulates thermosensory neurons non-cell-autonomously through the estrogen signaling pathway, producing thermotactic behavior. We provide a link between systemic environmental recognition and behavioral plasticity in the nervous system.

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Figure 1: The essential role of HSF-1 in a memory-based behavior revealed by genome-wide microarray analyses.
Figure 2: Characterization of thermotaxis behavior of hsf-1 mutants.
Figure 3: Thermotaxis controlled by HSF-1 downstream signaling.
Figure 4: Cell-specific rescue of defective thermotactic behavior in hsf-1 mutants.
Figure 5: Genetic interactions between HSF-1 signaling and the genes that act in the thermotactic neural circuit.
Figure 6: Regulation of the thermosensory neurons by the HSF-1 signaling.
Figure 7: Effect of estradiol application on thermotaxis.
Figure 8: HSF-1 signaling acts through estrogen signaling to regulate the AFD thermosensory neurons.

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Acknowledgements

We thank N. Hisamoto (Nagoya University), T. Mizuno (Nagoya University) and K. Matsumoto (Nagoya University) for sharing strains; A. Fire (Stanford University School of Medicine) for pPD plasmids; Y. Iino (University of Tokyo) for the gcy-5 and gcy-7 promoters; Caenorhabditis Genetic Center, C. elegans Knockout Consortium and S. Mitani at the National Bioresource Project, Japan, for strains; K. Terauchi and T. Kondo for kindly sharing the microarray apparatus; T. Inada for kindly sharing the quantitative PCR apparatus; C. Bargmann, S. Takagi, N. Hisamoto, A. Kuhara, P. Jurado, H. Sasakura, N. Ohnishi, T. Kimata, M. Nonomura and members of the Mori laboratory for comments on this manuscript and discussion. I.M. is a Scholar of the Institute for Advanced Research in Nagoya University, Japan. This work was supported by the Core Research for Evolutional Science and Technology (CREST) Program of the Japan Science and Technology (JST) agency (to I.M.).

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T.S. designed the research, performed most experiments, analyzed data and wrote the manuscript; Y.N. performed the quantitative PCR experiments and conducted germline transformation to construct the C. elegans transgenic line; I.M. supervised the project, conducted initial identification of cells expressing the hsf-1 promoter::gfp reporter gene and wrote the manuscript.

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Correspondence to Ikue Mori.

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Supplementary Figures 1–9, Supplementary Strains and Plasmids (PDF 14251 kb)

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Sugi, T., Nishida, Y. & Mori, I. Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat Neurosci 14, 984–992 (2011). https://doi.org/10.1038/nn.2854

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