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A novel photic entrainment mechanism for the circadian clock in an insect: involvement of c-fos and cryptochromes.

ABSTRACT: Background:Entrainment to the environmental light cycle is an essential property of the circadian clock. Although the compound eye is known to be the major photoreceptor necessary for entrainment in many insects, the molecular mechanisms of photic entrainment remain to be explored. Results:We found that cryptochromes (crys) and c-fos mediate photic entrainment of the circadian clock in a hemimetabolous insect, the cricket Gryllus bimaculatus. We examined the effects of RNA interference (RNAi)-mediated knockdown of the cry genes, Gb'cry1 and Gb'cry2, on photic entrainment, and light-induced resetting of the circadian locomotor rhythm. Gb'cry2 RNAi accelerated entrainment for delay shifts, while Gb'cry1/ Gb'cry2 double RNAi resulted in significant lengthening of transient cycles in both advance and delay shifts, and even in entrainment failure in some crickets. Double RNAi also strongly suppressed light induced resetting. The Gb'cry-mediated phase shift or resetting of the rhythm was preceded by light-induced Gb'c-fosB expression. We also found that Gb'c-fosB, Gb'cry2 and Gb'period (Gb'per) were likely co-expressed in some optic lobe neurons. Conclusion:Based on these results, we propose a novel model for photic entrainment of the insect circadian clock, which relies on the light information perceived by the compound eye.

SUBMITTER: Kutaragi Y

PROVIDER: S-EPMC6145112 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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A novel photic entrainment mechanism for the circadian clock in an insect: involvement of <i>c-fos</i> and <i>cryptochrome</i>s.

Kutaragi Yuki Y Tokuoka Atsushi A Tomiyama Yasuaki Y Nose Motoki M Watanabe Takayuki T Bando Tetsuya T Moriyama Yoshiyuki Y Tomioka Kenji K

Zoological letters 20180918

<h4>Background</h4>Entrainment to the environmental light cycle is an essential property of the circadian clock. Although the compound eye is known to be the major photoreceptor necessary for entrainment in many insects, the molecular mechanisms of photic entrainment remain to be explored.<h4>Results</h4>We found that <i>cryptochrome</i>s (<i>cry</i>s) and <i>c-fos</i> mediate photic entrainment of the circadian clock in a hemimetabolous insect, the cricket <i>Gryllus bimaculatus</i>. We examin ...[more]

PMID: 30250749

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Project description:Inhibitor of DNA binding (Id) genes comprise a family of four helix-loop-helix (HLH) transcriptional inhibitors. Our earlier studies revealed a role for ID2 within the circadian system, contributing to input, output, and core clock function through its interaction with CLOCK and BMAL1. Here, we explore the contribution of ID4 to the circadian system using a targeted disruption of the Id4 gene. Attributes of the circadian clock were assessed by monitoring the locomotor activity of Id4-/- mice, and they revealed disturbances in its operation. Id4-mutant mice expressed a shorter circadian period length, attenuated phase shifts in responses to continuous and discrete photic cues, and an advanced phase angle of entrainment under a 12:12 light:dark cycle and under short and long photoperiods. To understand the basis for these properties, suprachiasmatic nucleus (SCN) and retinal structures were examined. Anatomical analysis reveals a smaller Id4-/- SCN in the width dimension, which is a finding consistent with its smaller brain. As a result of this feature, anterograde tracing in Id4-/- mice revealed retinal afferents innovate a disproportionally larger SCN area. The Id4-/- photic entrainment responses are unlikely to be due to an impaired function of the retinal pathways since Id4-/- retinal anatomy and function tested by pupillometry were similar to wild-type mice. Furthermore, these circadian characteristics are opposite to those exhibited by the Id2-/- mouse, suggesting an opposing influence of the ID4 protein within the circadian system; or, the absence of ID4 results in changes in the expression or activity of other members of the Id gene family. Expression analysis of the Id genes within the Id4-/- SCN revealed a time-of-day specific elevated Id1. It is plausible that the increased Id1 and/or absence of ID4 result in changes in interactions with bHLH canonical clock components or with targets upstream and/or downstream of the clock, thereby resulting in abnormal properties of the circadian clock and its entrainment.

Dataset Information

A novel photic entrainment mechanism for the circadian clock in an insect: involvement of c-fos and cryptochromes.

Publications

A novel photic entrainment mechanism for the circadian clock in an insect: involvement of <i>c-fos</i> and <i>cryptochrome</i>s.

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