DrosophilaDH31 Neuropeptide and PDF Receptor Regulate Night-Onset Temperature Preference

Abstract

Body temperature exhibits rhythmic fluctuations over a 24 h period (Refinetti and Menaker, 1992) and decreases during the night, which is associated with sleep initiation (Gilbert et al., 2004; Kräuchi, 2007a,b). However, the underlying mechanism of this temperature decrease is largely unknown. We have previously shown that Drosophila exhibit a daily temperature preference rhythm (TPR), in which their preferred temperatures increase during the daytime and then decrease at the transition from day to night (night-onset) (Kaneko et al., 2012). Because Drosophila are small ectotherms, their body temperature is very close to that of the ambient temperature (Stevenson, 1985), suggesting that their TPR generates their body temperature rhythm. Here, we demonstrate that the neuropeptide diuretic hormone 31 (DH31) and pigmentdispersing factor receptor (PDFR) contribute to regulate the preferred temperature decrease at night-onset. We show that PDFR and tethered-DH31 expression in dorsal neurons 2 (DN2s) restore the preferred temperature decrease at night-onset, suggesting that DH31 acts on PDFR in DN2s. Notably, we previously showed that the molecular clock in DN2s is important for TPR. Although PDF (another ligand of PDFR) is a critical factor for locomotor activity rhythms, Pdf mutants exhibit normal preferred temperature decreases at night-onset. This suggests that DH31-PDFR signaling specifically regulates a preferred temperature decrease at night-onset. Thus, we propose that night-onset TPR and locomotor activity rhythms are differentially controlled not only by clock neurons but also by neuropeptide signaling in the brain.Key words: circadian rhythm; DH31; Drosophila; PDFR; temperature preference behavior; thermoregulation IntroductionBody temperature rhythm (BTR) is fundamental for maintaining homeostasis, such as in generating metabolic energy and sleep (Aschoff, 1983;Refinetti and Menaker, 1992; Kräuchi, 2002 Kräuchi, , 2007aGilbert et al., 2004;Weinert, 2010;Gerhart-Hines et al., 2013). BTR is one of the most robust circadian outputs and can affect the peripheral clocks of mammals (Brown et al., 2002;Buhr et al., 2010). The rhythmic patterns of BTR and locomotor activity rhythms are analogous. For instance, in diurnal mammals, both body temperature and locomotor activity increase during the daytime and decrease at night (Satlin et al., 1995; Weinert and Received March 23, 2016; revised Aug. 24, 2016; accepted Sept. 22, 2016. Author , and UAS-Pdfr flies, Dr. Michael Nitabach for UAS-t-Pdf, UAS-t-Dh31, UAS-t-PDF-SCR flies and the anti-DH31 antibody, and the Bloomington Drosophila Stock Center for the fly lines. We thank Drs. Christian I. Hong, Emi Nagoshi, and Haruna Kaneko, and the Hamada laboratory members for their comments and advice on this manuscript, as well as Dr. Kazuhiko Kume for advice on sleep data analysis.The authors declare no competing financial interests. Significance StatementBody temperature rhythm (BTR) is fundamental for the maintenance of functions essential for homeostasis, such as ge...

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