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

Yuki Kutaragi1, Atsushi Tokuoka1, Yasuaki Tomiyama1, Motoki Nose1, Takayuki Watanabe2, Toshikazu Bando3, Yoshiyuki Moriyama4, Kenji Tomioka1
1Graduate School of Natural Science and Technology, Okayama University, Okayama, 700-8530, Japan
2Research Institute for Electronic Science, Hokkaido University, Sapporo, 060-0811, Japan
3Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama 700-8558, Japan
4Department of Natural Sciences, Kawasaki Medical School, Matsushima 577, Kurashiki, 701-0192, Japan

Tóm tắt

Từ khóa


Tài liệu tham khảo

Saunders DS, Steel CGH, Vafopoulou X, Lewis RD. Insect Clocks, vol. 560. Amsterdam: Elsevier 3rd ed. p. 2002.

Hardin P. Molecular mechanisms of circadian timekeeping in Drosophila. Sleep Biol Rhythms. 2009;7:235–42.

Tataroglu O, Emery P. The molecular ticks of the Drosophila circadian clock. Curr Opin Insect Sci. 2015;7:51–7.

Tomioka K, Matsumoto A. Circadian molecular clockworks in non-model insects. Curr Opin Insect Sci. 2015;7:58–64.

Blau J, Young MW. Cycling vrille expression is required for a functional Drosophila clock. Cell. 1999;99:661–71.

Cyran SA, Buchsbaum AM, Reddy KL, Lin M-C, Glossop NRJ, Hardin PE, et al. vrille, Pdp1 and dClock form a second feedback loop in the Drosophila circadian clock. Cell. 2003;112:329–41.

Kamae Y, Uryu O, Miki T, Tomioka K. The nuclear receptor genes HR3 and E75 are required for the circadian rhythm in a primitive insect. PLoS One. 2014;9:e114899.

Yoshii T, Todo T, Wülbeck C, Stanewsky R, Helfrich-Förster C. Cryptochrome is present in the compound eyes and a subset of Drosophila's clock neurons. J Comp Neurol. 2008;508:952–66.

Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, Weitz CJ, et al. Light-dependent sequentation of TIMELESS by CRYPTOCHROME. Science. 1999;285:553–6.

Lin F-J, Song W, Meyer-Bernstein E, Naidoo N, Sehgal A. Photic signaling by cryptochrome in the Drosophila circadian system. Mol Cell Biol. 2001;21:7287–94.

Emery P, So WV, Kaneko M, Hall JC, Rosbash M. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell. 1998;95:669–79.

Ishikawa T, Matsumoto A, Kato Jr. T, Togashi S, Ryo H, Ikenaga M, et al. DCRY is a Drosophila photoreceptor protein implicated in light entrainment of circadian rhythm. Gene Cells 1999;4:57–65.

Ingram KK, Kutowoi A, Wurm Y, Shoemaker D, Meier R, Bloch G. The molecular clockwork of the fire ant Solenopsis invicta. PLoS One. 2012;7:e45715.

Yuan Q, Metterville D, Briscoe AD, Reppert SM. Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol Biol Evol. 2007;24:948–55.

Langmesser S, Tallone T, Bordon A, Rusconi S, Albrecht U. Interaction of circadian clock proteins PER2 and CRY with BMAL1 and CLOCK. BMC Mol Biol. 2008;9:41.

Ye R, Selby CP, Chiou Y-Y, Ozkan-Dagliyan I, Gaddameedhi S, Sancar A. Dual modes of CLOCK:BMAL1 inhibition mediated by Cryptochrome and period proteins in the mammalian circadian clock. Genes Dev. 2016;28:1989–98.

Selby CP, Thompson C, Schmitz TM, Van Gelder RN, Sancar A. Functional redundancy of cryptochromes and classical photoreceptors for nonvisual ocular photoreception in mice. Proc Natl Acad Sci. 2000;97:14697–702.

Nathalie H, Schleicher E, Kacprzak S, Bouly J-P, Picot M, Wu W, et al. Human and Drosophila cryptochromes are light activated by flavin photoreduction in living cells. PLoS Biol. 2008;6:e160.

Tomioka K, Chiba Y. Effects of nymphal stage optic nerve severance or optic lobe removal on the circadian locomotor rhythm of the cricket. Zool Sci. 1984;1:375–82.

Yukizane M, Tomioka K. Neural pathways involved in mutual interactions between optic lobe circadian pacemakers in the cricket Gryllus bimaculatus. J Comp Physiol A. 1995;176:601–10.

Komada S, Kamae Y, Koyanagi M, Tatewaki K, Hassaneen E, Saifullah A, et al. Green-sensitive opsin is the photoreceptor for photic entrainment of an insect circadian clock. Zoological Letters. 2015;1:11.

Kutaragi Y, Miki T, Bando T, Tomioka K. Transcriptional and non-transcriptional events are involved in photic entrainment of the circadian clock in the cricket Gryllus bimaculatus. Physiol Entomol. 2016;41:358–68.

Tokuoka A, Itoh TQ, Hori S, Uryu O, Danbara Y, Nose M, et al. cryptochrome genes form an oscillatory loop independent of the per/tim loop in the circadian clockwork of the cricket Gryllus bimaculatus. Zoological Letters. 2017;3:5.

Moriyama Y, Sakamoto T, Karpova SG, Matsumoto A, Noji S, Tomioka K. RNA interference of the clock gene period disrupts circadian rhythms in the cricket Gryllus bimaculatus. J Biol Rhythm. 2008;23:308–18.

Sokolove PG, Bushell WN. The chi square periodogram: its utility for analysis of circadian rhythm. J Theor Biol. 1978;72:131–60.

Schmid B, Helfrich-Förster C, Yoshii T. A new ImageJ plug-in “ActogramJ” for chronobiological analyses. J Biol Rhythm. 2011;26:464–7.

Kaneko M, Park JH, Cheng Y, Hardin PE, Hall JC. Disruption of synaptic transmission or clock-gene-product oscillations in circadian pacemaker cells of Drosophila cause abnormal behavioral rhythms. J Neurobiol. 2000;43:207–33.

Kornhauser JM, Nelson DE, Mayo KE, Takahashi JS. Photic and circadian regulation of c-fos gene expression in hamster suprachiasmatic nucleus. Neuron. 1990;5:127–34.

Zhang L, Lear BC, Seluzicki A, Allada R. The CRYPTOCHROME photoreceptor gates PDF neuropeptide signaling to set circadian network hierarchy in Drosophila. Curr Biol. 2009;19:2050–5.

Zhu H, Yuan Q, Briscoe AD, Froy O, Casselman A, Reppert SM. The two CRYs of the butterfly. Curr Biol. 2005;15:R953–4.

Michae AK, Fribourgh JL, Gelder RNV, Partch CL. Animal cryptochromes: divergent roles in light perception, circadian timekeeping and beyond. Photochem Photobiol. 2017;93:128–40.

Spoelstra K, Albrecht U, GTJvd H, Brauer V, Daan S. Phase responses to light pulses in mice lacking functional Per or Cry genes. J Biol Rhythm. 2004;19:518–29.

Moore HAM, Whitmore D. Circadian rhythmicity and light sensitivity of the zebrafish brain. PLoS One. 2014;9:e86176.

Guillaumond F, Sage D, Deprez P, Bosler O, Becquet D, François-Bellan AM. Circadian binding activity of AP-1, a regulator of the arylalkylamine N-acetyltransferase gene in the rat pineal gland, depends on circadian Fra-2, c-Jun, and Jun-D expression and is regulated by the clock's zeitgebers. J Neurochem. 2000;75:1398–407.

Yoo S-H, Mohawk JA, Siepka SM, Shan Y, Huh SK, Hong H-K, et al. Competing E3 ubiquitin ligase govern circadian periodicity by degradation of CRY in nucleus and cytoplasm. Cell. 2013;152:1091–105.

Hirano A, Yumimoto K, Tsunematsu R, Matsumoto M, Oyama M, Kozuka-Hata H, et al. FBXL21 regulates oscillation of the circadian clock through ubiquitination and stabilization of Cryptochromes. Cell. 2013;152:1106–18.

Ozturk N, VanVickle-Chavez SJ, Akileswaran L, Van Gelder RN, Sancar A. Ramshackle (Brwd3) promotes light-induced ubiquitylation of Drosophila Cryptochrome by DDB1-CUL4-ROC1 E3 ligase complex. Proc Natl Acad Sci. 2013;110:4980–5.

Mracek P, Santoriello C, Idda ML, Pagano C, Ben-Moshe Z, Gothilf Y, et al. Regulation of per and cry genes reveals a central role for the D-box enhancer in light-dependent gene expression. PLoS One. 2012;7:e51278.

Yamaguchi S, Isejima H, Matsuo T, Okura R, Yagita K, Kobayashi M, et al. Synchronization of cellular clocks in the suprachiasmatic nucleus. Science. 2003;302:1408–12.

Kaneko M, Hall JC. Neuroanatomy of cells expressing clock genes in Drosophila: transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections. J Comp Neurol. 2000;422:66–94.

Miyasako Y, Umezaki Y, Tomioka K. Separate sets of cerebral clock neurons are responsible for light and temperature entrainment of Drosophila circadian locomotor rhythms. J Biol Rhythm. 2007;22:115–26.

Yoshii T, Hermann-Luibl C, Kistenpfennig C, Schmid B, Tomioka K, Helfrich-Förster C. Cryptochrome-dependent and -independent circadian entrainment circuits in Drosophila. J Neurosci. 2015;35:6131–41.

Golombek DA, Rosenstein RE. Physiology of circadian entrainment. Physiol Reviews. 2010;90:1063–102.

Ono D, Honma S, K-i H. Cryptochromes are critical for the development of coherent circadian rhythms in the mouse suprachiasmatic nucleus. Nat Commun. 2013;4:1666.

Evans JA, Pan H, Liu AC, Welsh DK. Cry1 −/− circadian rhythmicity depends on SCN intercellular coupling. J Biol Rhythm. 2012;27:443–52.

Inagaki N, Honma S, Ono D, Tanahashi Y, Honma K-i. Separate oscillating cell groups in mouse suprachiasmatic nucleus couple photoperiodically to the onset and end of daily activity. Proc Natl Acad Sci. 2007;104:7664–9.

Nishiitsutsuji-Uwo J, Pittendrigh CS. Central nervous system control of circadian rhythmicity in the cockroach. II. The pathway of light signals that entrain the rhythm. Z vergl Physiol. 1968;58:1–13.

Page TL. Interaction between bilaterally paired components of the cockroach circadian system. J Comp Physiol. 1978;124:225–36.