Network Dynamics Mediate Circadian Clock Plasticity

Overview

Journal Neuron

Publisher Cell Press

Specialty Neurology

Date 2017 Jan 10

PMID 28065650

Citations 36

Authors

Abdelhalim Azzi

Jennifer A Evans

Tanya Leise

Jihwan Myung

Toru Takumi

Alec J Davidson

Steven A Brown

Affiliations

Soon will be listed here.

Abstract

A circadian clock governs most aspects of mammalian behavior. Although its properties are in part genetically determined, altered light-dark environment can change circadian period length through a mechanism requiring de novo DNA methylation. We show here that this mechanism is mediated not via cell-autonomous clock properties, but rather through altered networking within the suprachiasmatic nuclei (SCN), the circadian "master clock," which is DNA methylated in region-specific manner. DNA methylation is necessary to temporally reorganize circadian phasing among SCN neurons, which in turn changes the period length of the network as a whole. Interruption of neural communication by inhibiting neuronal firing or by physical cutting suppresses both SCN reorganization and period changes. Mathematical modeling suggests, and experiments confirm, that this SCN reorganization depends upon GABAergic signaling. Our results therefore show that basic circadian clock properties are governed by dynamic interactions among SCN neurons, with neuroadaptations in network function driven by the environment.

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References

Farajnia S, van Westering T, Meijer J, Michel S . Seasonal induction of GABAergic excitation in the central mammalian clock. Proc Natl Acad Sci U S A. 2014; 111(26):9627-32. PMC: 4084452. DOI: 10.1073/pnas.1319820111. View

Malenka R, Bear M . LTP and LTD: an embarrassment of riches. Neuron. 2004; 44(1):5-21. DOI: 10.1016/j.neuron.2004.09.012. View

Zovkic I, Guzman-Karlsson M, Sweatt J . Epigenetic regulation of memory formation and maintenance. Learn Mem. 2013; 20(2):61-74. PMC: 3549063. DOI: 10.1101/lm.026575.112. View

Albus H, Vansteensel M, Michel S, Block G, Meijer J . A GABAergic mechanism is necessary for coupling dissociable ventral and dorsal regional oscillators within the circadian clock. Curr Biol. 2005; 15(10):886-93. DOI: 10.1016/j.cub.2005.03.051. View

Nagano M, Adachi A, Nakahama K, Nakamura T, Tamada M, Meyer-Bernstein E . An abrupt shift in the day/night cycle causes desynchrony in the mammalian circadian center. J Neurosci. 2003; 23(14):6141-51. PMC: 6740348. View

Nakajima Y, Yamazaki T, Nishii S, Noguchi T, Hoshino H, Niwa K . Enhanced beetle luciferase for high-resolution bioluminescence imaging. PLoS One. 2010; 5(4):e10011. PMC: 2848861. DOI: 10.1371/journal.pone.0010011. View

Brown S, Kunz D, Dumas A, Westermark P, Vanselow K, Tilmann-Wahnschaffe A . Molecular insights into human daily behavior. Proc Natl Acad Sci U S A. 2008; 105(5):1602-7. PMC: 2234191. DOI: 10.1073/pnas.0707772105. View

Evans J, Leise T, Castanon-Cervantes O, Davidson A . Intrinsic regulation of spatiotemporal organization within the suprachiasmatic nucleus. PLoS One. 2011; 6(1):e15869. PMC: 3017566. DOI: 10.1371/journal.pone.0015869. View

Nakahata Y, Kaluzova M, Grimaldi B, Sahar S, Hirayama J, Chen D . The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control. Cell. 2008; 134(2):329-40. PMC: 3526943. DOI: 10.1016/j.cell.2008.07.002. View

10.

Earnest D, Digiorgio S, Sladek C . Effects of tetrodotoxin on the circadian pacemaker mechanism in suprachiasmatic explants in vitro. Brain Res Bull. 1991; 26(5):677-82. DOI: 10.1016/0361-9230(91)90160-l. View

11.

Stevenson T, Prendergast B . Reversible DNA methylation regulates seasonal photoperiodic time measurement. Proc Natl Acad Sci U S A. 2013; 110(41):16651-6. PMC: 3799317. DOI: 10.1073/pnas.1310643110. View

12.

Liu C, Weaver D, Strogatz S, Reppert S . Cellular construction of a circadian clock: period determination in the suprachiasmatic nuclei. Cell. 1997; 91(6):855-60. DOI: 10.1016/s0092-8674(00)80473-0. View

13.

Abraham U, Granada A, Westermark P, Heine M, Kramer A, Herzel H . Coupling governs entrainment range of circadian clocks. Mol Syst Biol. 2010; 6:438. PMC: 3010105. DOI: 10.1038/msb.2010.92. View

14.

Kuleshov M, Jones M, Rouillard A, Fernandez N, Duan Q, Wang Z . Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016; 44(W1):W90-7. PMC: 4987924. DOI: 10.1093/nar/gkw377. View

15.

Herzog E, Takahashi J, Block G . Clock controls circadian period in isolated suprachiasmatic nucleus neurons. Nat Neurosci. 1999; 1(8):708-13. DOI: 10.1038/3708. View

16.

Oda G, Friesen W . A model for "splitting" of running-wheel activity in hamsters. J Biol Rhythms. 2002; 17(1):76-88. DOI: 10.1177/074873002129002357. View

17.

Yoo S, Yamazaki S, Lowrey P, Shimomura K, Ko C, Buhr E . PERIOD2::LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc Natl Acad Sci U S A. 2004; 101(15):5339-46. PMC: 397382. DOI: 10.1073/pnas.0308709101. View

18.

Noda M, Ikeda T, Suzuki H, Takeshima H, Takahashi T, Kuno M . Expression of functional sodium channels from cloned cDNA. Nature. 1986; 322(6082):826-8. DOI: 10.1038/322826a0. View

19.

Antle M, Silver R . Orchestrating time: arrangements of the brain circadian clock. Trends Neurosci. 2005; 28(3):145-51. DOI: 10.1016/j.tins.2005.01.003. View

20.

Harmar A, Marston H, Shen S, Spratt C, West K, Sheward W . The VPAC(2) receptor is essential for circadian function in the mouse suprachiasmatic nuclei. Cell. 2002; 109(4):497-508. DOI: 10.1016/s0092-8674(02)00736-5. View