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Chronobiology International
The Journal of Biological and Medical Rhythm Research
Volume 41, 2024 - Issue 6
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Original Articles

TASK-3, two-pore potassium channels, contribute to circadian rhythms in the electrical properties of the suprachiasmatic nucleus and play a role in driving stable behavioural photic entrainment

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Pages 802-816 | Received 24 Aug 2023, Accepted 19 Apr 2024, Published online: 17 May 2024

References

  • Allen CN, Nitabach MN, Colwell CS. 2017. Membrane currents, gene expression, and circadian clocks. Cold Spring Harb Perspect Biol. 9:1–16. doi: 10.1101/cshperspect.a027714.
  • Biello SM, Bonsall DR, Atkinson LA, Molyneux PC, Harrington ME, Lall GS. 2018. Alterations in glutamatergic signaling contribute to the decline of circadian photoentrainment in aged mice. Neurobiol Aging. 66:75–84. doi: 10.1016/j.neurobiolaging.2018.02.013.
  • Borsotto M, Veyssiere J, Moha Ou Maati H, Devader C, Mazella J, Heurteaux C. 2015. Targeting two-pore domain K+ channels TREK-1 and TASK-3 for the treatment of depression: a new therapeutic concept. Br J Pharmacol. 172:771–784. doi: 10.1111/bph.12953.
  • Brancaccio M, Edwards MD, Patton AP, Smyllie NJ, Chesham JE, Maywood ES, Hastings MH. 2019. Cell-autonomous clock of astrocytes drives circadian behavior in mammals. Science. 363:187–192. doi: 10.1126/science.aat4104.
  • Brickley SG, Aller MI, Sandu C, Veale EL, Alder FG, Sambi H, Mathie A, Wisden W. 2007. TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons. J Neurosci. 27:9329–9340. doi: 10.1523/JNEUROSCI.1427-07.2007.
  • Collins B, Pierre-Ferrer S, Muheim C, Lukacsovich D, Cai Y, Spinnler A, Herrera CG, Wen SA, Winterer J, Belle MDC, et al. 2020. Circadian VIPergic neurons of the suprachiasmatic nuclei sculpt the sleep-wake cycle. Neuron. 108:486–499.e5. doi: 10.1016/j.neuron.2020.08.001.
  • Colwell CS. 2011. Linking neural activity and molecular oscillations in the SCN. Nat Rev Neurosci. 12:553–569. doi: 10.1038/nrn3086.
  • Cousin MA, Veale EL, Dsouza NR, Tripathi S, Holden RG, Arelin M, Beek G, Bekheirnia MR, Beygo J, Bhambhani V, et al. 2022. Gain and loss of TASK3 channel function and its regulation by novel variation cause KCNK9 imprinting syndrome. Genome Med. 14. doi: 10.1186/s13073-022-01064-4.
  • Enyedi P, Czirják G. 2010. Molecular background of leak K + currents: two-pore domain potassium channels. Physiol Rev. 90:559–605. doi: 10.1152/physrev.00029.2009.
  • Feliciangeli S, Chatelain FC, Bichet D, Lesage F. 2015. The family of K2P channels: salient structural and functional properties. J Physiol. 593:2587–2603. doi: 10.1113/jphysiol.2014.287268.
  • Ginty DD, Kornhauser JM, Thompson MA, Bading H, Mayo KE, Takahashi JS, Greenberg ME. 1993. Regulation of CREB phosphorylation in the suprachiasmatic nucleus by light and a circadian clock. Science. 260:238–241. doi: 10.1126/science.8097062.
  • Gnatenco C, Han J, Snyder AK, Kim D. 2002. Functional expression of TREK-2 K+ channel in cultured rat brain astrocytes. Brain Res. 931:56–67. doi: 10.1016/S0006-8993(02)02261-8.
  • Han S, Yu FH, Schwartz MD, Linton JD, Bosma MM, Hurley JB, Catterall WA, De La Iglesia HO. 2012. Na V1.1 channels are critical for intercellular communication in the suprachiasmatic nucleus and for normal circadian rhythms. Proc Natl Acad Sci USA. 109. doi: 10.1073/pnas.1115729109.
  • Harvey JRMM, Plante AE, Meredith AL. 2020. Ion channels controlling circadian rhythms in suprachiasmatic nucleus excitability. Physiol Rev. 100:1415–1454.
  • Jones JR, Simon T, Lones L, Herzog ED. 2018. SCN VIP neurons are essential for normal light-mediated resetting of the circadian system. J Neurosci. 38:7986–7995. doi: 10.1523/JNEUROSCI.1322-18.2018.
  • Kim J-E, Yeo S-I, Ryu HJ, Chung CK, Kim M-J, Kang T-C. 2011. Changes in TWIK-related acid sensitive K±1 and -3 channel expressions from neurons to glia in the hippocampus of temporal lobe epilepsy patients and experimental animal model. Neurochem Res. 36:2155–2168. doi: 10.1007/s11064-011-0540-0.
  • Kudo T, Loh DH, Kuljis D, Constance C, Colwell CS. 2011. Fast delayed rectifier potassium current: critical for input and output of the circadian system. J Neurosci. 31:2746–2755. doi: 10.1523/JNEUROSCI.5792-10.2011.
  • Lalic T, Steponenaite A, Wei L, Vasudevan SR, Mathie A, Peirson SN, Lall GS, Cader MZ. 2020. TRESK is a key regulator of nocturnal suprachiasmatic nucleus dynamics and light adaptive responses. Nat Commun. 11. doi: 10.1038/s41467-020-17978-9.
  • Linden A-M, Sandu C, Aller MI, Vekovischeva OY, Rosenberg PH, Wisden W, Korpi ER. 2007. TASK-3 knockout mice exhibit exaggerated nocturnal activity, impairments in cognitive functions, and reduced sensitivity to inhalation anesthetics. J Pharmacol Exp Ther. 323:924–934. doi: 10.1124/jpet.107.129544.
  • Lu B, Su Y, Das S, Liu J, Xia J, Ren D. 2007. The Neuronal Channel NALCN contributes resting sodium permeability and is required for normal respiratory rhythm. Cell. 129:371–383. doi: 10.1016/j.cell.2007.02.041.
  • Mathie A. 2007. Neuronal two-pore-domain potassium channels and their regulation by G protein-coupled receptors. J Physiol. 578:377–385. doi: 10.1113/jphysiol.2006.121582.
  • Meijer JH, Albus H, Weidema F, Ravesloot J-H. 1993. The effects of glutamate on membrane potential and discharge rate of suprachiasmatic neurons. Brain Res. 603:284–288. doi: 10.1016/0006-8993(93)91249-R.
  • Meredith AL, Wiler SW, Miller BH, Takahashi JS, Fodor AA, Ruby NF, Aldrich RW. 2006. BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat Neurosci. 9:1041–1049. doi: 10.1038/nn1740.
  • Michel S, Itri J, Colwell CS. 2002. Excitatory mechanisms in the suprachiasmatic nucleus: the role of AMPA/KA glutamate receptors. J Neurophysiol. 88:817–828. doi: 10.1152/jn.2002.88.2.817.
  • Patton AP, Hastings MH. 2018. The suprachiasmatic nucleus. Curr Biol. 28:R816–R822. doi: 10.1016/j.cub.2018.06.052.
  • Rajan S, Preisig-Muller R, Wischmeyer E, Nehring R, Hanley PJ, Renigunta V, Musset B, Schlichthorl G, Derst C, Karschin A, et al. 2002. Interaction with 14-3-3 proteins promotes functional expression of the potassium channels TASK-1 and TASK-3. J Physiol. 545:13–26. doi: 10.1113/jphysiol.2002.027052.
  • Ramkisoensing A, Meijer JH. 2015. Synchronization of biological clock neurons by light and peripheral feedback systems promotes circadian rhythms and health. Front Neurol. 6:138217. doi: 10.3389/fneur.2015.00128.
  • Renigunta V, Schlichthorl G, Daut J. 2015. Much more than a leak: structure and function of K2P-channels. Pflugers Archiv Eur J Physiol. 467:867–894. doi: 10.1007/s00424-015-1703-7.
  • Rusznák Z, Pocsai K, Kovács I, Pór Á, Pál B, Bíró T, Szücs G. 2004. Differential distribution of TASK-1, TASK-2 and TASK-3 immunoreactivities in the rat and human cerebellum. Cell Mol Life Sci. 61:1532–1542. doi: 10.1007/s00018-004-4082-3.
  • Sans N, Petralia RS, Wang Y-X, Blahos J II, Hell JW, Wenthold RJ. 2000. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci. 20:1260–1271. doi: 10.1523/JNEUROSCI.20-03-01260.2000.
  • Sokolove PG, Bushell WN. 1978. The chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol. 72:131–160. doi: 10.1016/0022-5193(78)90022-x.
  • Sun H, Luo L, Lal B, Ma X, Chen L, Hann CL, Fulton AM, Leahy DJ, Laterra J, Li M. 2016. A monoclonal antibody against KCNK9 K+ channel extracellular domain inhibits tumour growth and metastasis. Nat Commun. 7:7. doi: 10.1038/ncomms10339.
  • Takahashi JS. 2017. Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet. 18:164–179. doi: 10.1038/nrg.2016.150.
  • Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA. 2001. CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci. 21:7491–7505. pii. doi: 10.1523/JNEUROSCI.21-19-07491.2001.
  • Van Someren EJW, Hagebeuk EEO, Lijzenga C, Scheltens P, De Rooij SEJA, Jonker C, Pot AM, Mirmiran M, Swaab DF. 1996. Circadian rest-activity rhythm disturbances in Alzheimer’s disease. Biol Psychiatry. 40:259–270. doi: 10.1016/0006-3223(95)00370-3.
  • Veale EL, Kennard LE, Sutton GL, MacKenzie G, Sandu C, Mathie A. 2007. Gα q -mediated regulation of TASK3 two-pore domain potassium channels: the role of protein kinase C. Mol Pharmacol. 71:1666–1675. doi: 10.1124/mol.106.033241.
  • Welsh DK, Takahashi JS, Kay SA. 2010. Suprachiasmatic nucleus: cell autonomy and network properties. Annu Rev Physiol. 72:551–577. doi: 10.1146/annurev-physiol-021909-135919.
  • Whitt JP, Montgomery JR, Meredith AL. 2016. BK channel inactivation gates daytime excitability in the circadian clock. Nat Commun. 7:1–13. doi: 10.1038/ncomms10837.
  • Yoshida K, Shi S, Ukai-Tadenuma M, Fujishima H, Ohno R, Ueda HR. 2018. Leak potassium channels regulate sleep duration. Proc Natl Acad Sci. 115:E9459–E9468. doi: 10.1073/pnas.1806486115.