Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Implications of Circadian Rhythm in Dopamine and Mood Regulation

  • Kim, Jeongah (Department of Brain and Cognitive Sciences, Daegu Gyeongbuk Institute of Science and Technology (DGIST)) ;
  • Jang, Sangwon (Department of Brain and Cognitive Sciences, Daegu Gyeongbuk Institute of Science and Technology (DGIST)) ;
  • Choe, Han Kyoung (Department of Brain and Cognitive Sciences, Daegu Gyeongbuk Institute of Science and Technology (DGIST)) ;
  • Chung, Sooyoung (Department of Brain and Cognitive Sciences, Scranton College, Ewha Womans University) ;
  • Son, Gi Hoon (Department of Biomedical Sciences, College of Medicine, Korea University) ;
  • Kim, Kyungjin (Department of Brain and Cognitive Sciences, Daegu Gyeongbuk Institute of Science and Technology (DGIST))
  • Received : 2017.05.02
  • Accepted : 2017.07.28
  • Published : 2017.07.31
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Abstract

Mammalian physiology and behavior are regulated by an internal time-keeping system, referred to as circadian rhythm. The circadian timing system has a hierarchical organization composed of the master clock in the suprachiasmatic nucleus (SCN) and local clocks in extra-SCN brain regions and peripheral organs. The circadian clock molecular mechanism involves a network of transcription-translation feedback loops. In addition to the clinical association between circadian rhythm disruption and mood disorders, recent studies have suggested a molecular link between mood regulation and circadian rhythm. Specifically, genetic deletion of the circadian nuclear receptor Rev-$erb{\alpha}$ induces mania-like behavior caused by increased midbrain dopaminergic (DAergic) tone at dusk. The association between circadian rhythm and emotion-related behaviors can be applied to pathological conditions, including neurodegenerative diseases. In Parkinson's disease (PD), DAergic neurons in the substantia nigra pars compacta progressively degenerate leading to motor dysfunction. Patients with PD also exhibit non-motor symptoms, including sleep disorder and neuropsychiatric disorders. Thus, it is important to understand the mechanisms that link the molecular circadian clock and brain machinery in the regulation of emotional behaviors and related midbrain DAergic neuronal circuits in healthy and pathological states. This review summarizes the current literature regarding the association between circadian rhythm and mood regulation from a chronobiological perspective, and may provide insight into therapeutic approaches to target psychiatric symptoms in neurodegenerative diseases involving circadian rhythm dysfunction.

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References

  1. Aarsland, D., Pahlhagen, S., Ballard, C.G., Ehrt, U., and Svenningsson, P. (2011). Depression in Parkinson disease--epidemiology, mechanisms and management. Nat. Rev. Neurol. 8, 35-47. https://doi.org/10.1038/nrneurol.2011.189
  2. Abarca, C., Albrecht, U., and Spanagel, R. (2002). Cocaine sensitization and reward are under the influence of circadian genes and rhythm. Proc. Natl. Acad. Sci. USA 99, 9026-9030. https://doi.org/10.1073/pnas.142039099
  3. Akhtar, R.A., Reddy, A.B., Maywood, E.S., Clayton, J.D., King, V.M., Smith, A.G., Gant, T.W., Hastings, M.H., and Kyriacou, C.P. (2002). Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus. Curr. Biol. 12, 540-550.
  4. Albrecht, U. (2013). Circadian clocks and mood-related behaviors. Handb. Exp. Pharmacol. 217, 227-239.
  5. Albrecht, U. (2017). Molecular mechanisms in mood regulation involving the circadian clock. Front Neurol. 8, 30.
  6. Amir, S., and Stewart, J. (2009). Motivational modulation of rhythms of the expression of the clock protein PER2 in the limbic forebrain. Biol. Psychiatry 65, 829-834. https://doi.org/10.1016/j.biopsych.2008.12.019
  7. Balsalobre, A., Damiola, F., and Schibler, U. (1998). A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell 93, 929-937. https://doi.org/10.1016/S0092-8674(00)81199-X
  8. Banerjee, S., Wang, Y., Solt, L.A., Griffett, K., Kazantzis, M., Amador, A., El-Gendy, B.M., Huitron-Resendiz, S., Roberts, A.J., Shin, Y., et al. (2014). Pharmacological targeting of the mammalian clock regulates sleep architecture and emotional behaviour. Nat. Commun. 5, 5759. https://doi.org/10.1038/ncomms6759
  9. Bedrosian, T.A., and Nelson, R.J. (2013). Sundowning syndrome in aging and dementia: research in mouse models. Exp. Neurol. 243, 67-73. https://doi.org/10.1016/j.expneurol.2012.05.005
  10. Bjorklund, A., and Dunnett, S.B. (2007). Dopamine neuron systems in the brain: an update. Trends Neurosci. 30, 194-202. https://doi.org/10.1016/j.tins.2007.03.006
  11. Bliwise, D.L., Watts, R.L., Watts, N., Rye, D.B., Irbe, D., and Hughes, M. (1995). Disruptive nocturnal behavior in Parkinson's disease and Alzheimer's disease. J. Geriatr. Psychiatry Neurol. 8, 107-110. https://doi.org/10.1177/089198879500800206
  12. Braak, H., Del Tredici, K., Rüb, U., de Vos, R.A., Jansen Steur, E.N., and Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging. 24, 197-211. https://doi.org/10.1016/S0197-4580(02)00065-9
  13. Brichta, L., and Greengard, P. (2014). Molecular determinants of selective dopaminergic vulnerability in Parkinson's disease: an update. Front Neuroanat. 8, 152.
  14. Brown, R.G., Landau, S., Hindle, J.V., Playfer, J., Samuel, M., Wilson, K.C., Hurt, C.S., Anderson, R.J., Carnell, J., Dickinson, L., et al. (2011). Depression and anxiety related subtypes in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 82, 803-809. https://doi.org/10.1136/jnnp.2010.213652
  15. Bunger, M.K., Wilsbacher, L.D., Moran, S.M., Clendenin, C., Radcliffe, L.A., Hogenesch, J.B., Simon, M.C., Takahashi, J.S., and Bradfield, C.A. (2000). Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103, 1009-1017. https://doi.org/10.1016/S0092-8674(00)00205-1
  16. Burn, D.J. (2002). Beyond the iron mask; towards better recognition and treatment of depression associated with Parkinson's disease. Mov. Disord. 17, 445-454. https://doi.org/10.1002/mds.10114
  17. Cebrian, C., and Prensa, L. (2010). Basal ganglia and thalamic input from neurons located within the ventral tier cell cluster region of the substantia nigra pars compacta in the rat. J. Comp. Neurol. 518, 1283-1300.
  18. Chaudhuri, K.R., and Schapira, A.H. (2009). Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 8, 464-474. https://doi.org/10.1016/S1474-4422(09)70068-7
  19. Cheng, H.C., Ulane, C.M., and Burke, R.E. (2010). Clinical progression in Parkinson disease and the neurobiology of axons. Ann. Neurol. 67, 715-725. https://doi.org/10.1002/ana.21995
  20. Chung, S., Lee, E.J., Yun, S., Choe, H.K., Park, S.B., Son, H.J., Kim, K.S., Dluzen, D.E., Lee. I., Hwang, O., et al. (2014). Impact of circadian nuclear receptor REV-ERB${\alpha}$ on midbrain dopamine production and mood regulation. Cell 157, 858-868. https://doi.org/10.1016/j.cell.2014.03.039
  21. Colavito, V., Tesoriero, C., Wirtu, A.T., Grassi-Zucconi, G., and Bentivoglio, M. (2015). Limbic thalamus and state-dependent behavior: The paraventricular nucleus of the thalamic midline as a node in circadian timing and sleep/wake-regulatory networks. Neurosci. Biobehav. Rev. 54, 3-17. https://doi.org/10.1016/j.neubiorev.2014.11.021
  22. Dauer, W., and Przedborski, S. (2003). Parkinson's disease: mechanisms and models. Neuron 39, 889-909. https://doi.org/10.1016/S0896-6273(03)00568-3
  23. Dibner, C., Schibler, U., and Albrecht, U. (2010). The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549. https://doi.org/10.1146/annurev-physiol-021909-135821
  24. Dominguez-Lopez, S., Howell, R.D., Lopez-Canul, M.G., Leyton, M., and Gobbi, G. (2014). Electrophysiological characterization of dopamine neuronal activity in the ventral tegmental area across the light-dark cycle. Synapse 68, 454-467. https://doi.org/10.1002/syn.21757
  25. Dulcis, D., Jamshidi, P., Leutgeb, S., and Spitzer, N.C. (2013). Neurotransmitter switching in the adult brain regulates behavior. Science 340, 449-453. https://doi.org/10.1126/science.1234152
  26. Easton, A., Arbuzova, J., and Turek, F.W. (2003). The circadian Clock mutation increases exploratory activity and escape-seeking behavior. Genes Brain Behav. 2,11-19. https://doi.org/10.1034/j.1601-183X.2003.00002.x
  27. Gallego, M., and Virshup, D.M. (2007). Post-translational modifications regulate the ticking of the circadian clock. Nat. Rev. Mol. Cell Biol. 8, 139-148. https://doi.org/10.1038/nrm2106
  28. Gekakis, N., Staknis, D., Nguyen, H.B., Davis, F.C., Wilsbacher, L.D., King, D.P., Takahashi, J.S., and Weitz, C.J. (1998). Role of the CLOCK protein in the mammalian circadian mechanism. Science 280, 1564-1569. https://doi.org/10.1126/science.280.5369.1564
  29. Gloston, G.F., Yoo, S.H., and Chen, Z. (2017). Clock-enhancing small molecules and potential applications in chronic diseases and aging. Front Neurol. 8, 100.
  30. Grace, A.A. (2016). Dysregulation of the dopamine system in the pathophysiology of schizophrenia and depression. Nat. Rev. Neurosci. 17, 524-532. https://doi.org/10.1038/nrn.2016.57
  31. Guillaumond, F., Dardente, H., Giguère, V., and Cermakian, N. (2005). Differential control of Bmal1 circadian transcription by REVERB and ROR nuclear receptors. J. Biol. Rhythms. 20, 391-403. https://doi.org/10.1177/0748730405277232
  32. Halliday, G.M., Li, Y.W., Blumbergs, P.C., Joh, T.H., Cotton, R.G., Howe, P.R., Blessing, W.W., and Geffen, L.B. (1990). Neuropathology of immunohistochemically identified brainstem neurons in Parkinson's disease. Ann. Neurol. 27, 373-385. https://doi.org/10.1002/ana.410270405
  33. Hampp, G., Ripperger, J.A., Houben, T., Schmutz, I., Blex, C., Perreau-Lenz, S., Brunk, I., Spanagel, R., Ahnert-Hilger, G., Meijer, J.H., et al. (2008). Regulation of monoamine oxidase A by circadianclock components implies clock influence on mood. Curr. Biol. 18, 678-683. https://doi.org/10.1016/j.cub.2008.04.012
  34. Heuer, A., Smith, G.A., Lelos, M.J., Lane, E.L., and Dunnett, S.B. (2012). Unilateral nigrostriatal 6-hydroxydopamine lesions in mice I: motor impairments identify extent of dopamine depletion at three different lesion sites. Behav. Brain Res. 228, 30-43. https://doi.org/10.1016/j.bbr.2011.11.027
  35. Hikosaka, O. (2010). The habenula: from stress evasion to valuebased decision-making. Nat. Rev. Neurosci. 11, 503-513. https://doi.org/10.1038/nrn2866
  36. Hyman, S.E., and Malenka, R.C. (2001). Addiction and the brain: the neurobiology of compulsion and its persistence. Nat. Rev. Neurosci. 2, 695-703. https://doi.org/10.1038/35094560
  37. Johnsson, A., Engelmann, W., Pflug, B., and Klemke, W. (1983). Period lengthening of human circadian rhythms by lithium carbonate, a prophylactic for depressive disorders. Int. J. Chronobiol. 8, 129-147.
  38. Kim, H.J., Park, S.Y., Cho, Y.J., Hong, K.S., Cho, J.Y., Seo, S.Y., Lee, D.H., and Jeon, B.S. (2009). Nonmotor symptoms in de novo Parkinson disease before and after dopaminergic treatment. J. Neurol. Sci. 287, 200-204. https://doi.org/10.1016/j.jns.2009.07.026
  39. King, D.P., Zhao, Y., Sangoram, A.M., Wilsbacher, L.D., Tanaka, M., Antoch, M.P., Steeves, T.D., Vitaterna, M.H., Kornhauser, J.M., Lowrey, P.L., et al. (1997). Positional cloning of the mouse circadian clock gene. Cell 89, 641-653. https://doi.org/10.1016/S0092-8674(00)80245-7
  40. Kojetin, D., Wang, Y., Kamenecka, T.M., and Burris, T.P. (2011). Identification of SR8278, a synthetic antagonist of the nuclear heme receptor REV-ERB. ACS Chem. Biol. 6, 131-134. https://doi.org/10.1021/cb1002575
  41. Kripke, D.F., Nievergelt, C.M., Joo, E., Shekhtman, T., and Kelsoe, J.R. (2009). Circadian polymorphisms associated with affective disorders. J. Circadian Rhythms. 7, 2. https://doi.org/10.1186/1740-3391-7-2
  42. Kume, K., Zylka, M.J., Sriram, S., Shearman, L.P., Weaver, D.R., Jin, X., Maywood, E.S., Hastings, M.H., and Reppert, S.M. (1999). mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193-205. https://doi.org/10.1016/S0092-8674(00)81014-4
  43. Lauretti, E., Di Meco, A., Merali, S., and Pratico, D. (2017). Circadian rhythm dysfunction: a novel environmental risk factor for Parkinson's disease. Mol. Psychiatry 22, 280-286. https://doi.org/10.1038/mp.2016.47
  44. Leentjens, A.F., Scholtissen, B., Vreeling, F.W., and Verhey, F.R. (2006). The serotonergic hypothesis for depression in Parkinson's disease: an experimental approach. Neuropsychopharmacology 31, 1009-1015. https://doi.org/10.1038/sj.npp.1300914
  45. Li, J.Z., Bunney, B.G., Meng, F., Hagenauer, M.H., Walsh, D.M., Vawter, M.P., Evans, S.J., Choudary, P.V., Cartagena, P., Barchas, J.D., et al. (2013). Circadian patterns of gene expression in the human brain and disruption in major depressive disorder. Proc. Natl. Acad. Sci. USA 110, 9950-9955. https://doi.org/10.1073/pnas.1305814110
  46. Luo, A.H., and Aston-Jones, G. (2009). Circuit projection from suprachiasmatic nucleus to ventral tegmental area: a novel circadian output pathway. Eur. J. Neurosci. 29, 748-760. https://doi.org/10.1111/j.1460-9568.2008.06606.x
  47. Mansour, H.A., Wood, J., Logue, T., Chowdari, K.V., Dayal, M., Kupfer, D.J., Monk, T.H., Devlin, B., and Nimgaonkar, V.L. (2006). Association study of eight circadian genes with bipolar I disorder, schizoaffective disorder and schizophrenia. Genes Brain Behav. 5, 150-157. https://doi.org/10.1111/j.1601-183X.2005.00147.x
  48. McCarthy, M.J., and Welsh, D.K. (2012). Cellular circadian clocks in mood disorders. J. Biol. Rhythms 27, 339-352. https://doi.org/10.1177/0748730412456367
  49. McClung, C.A. (2007). Circadian genes, rhythms and the biology of mood disorders. Pharmacol. Ther. 114, 222-232. https://doi.org/10.1016/j.pharmthera.2007.02.003
  50. McClung, C.A., Sidiropoulou, K., Vitaterna, M., Takahashi, J.S., White, F.J., Cooper, D.C., and Nestler, E.J. (2005). Regulation of dopaminergic transmission and cocaine reward by the Clock gene. Proc. Natl. Acad. Sci. USA 102, 9377-9381. https://doi.org/10.1073/pnas.0503584102
  51. Musiek, E.S. (2015). Circadian clock disruption in neurodegenerative diseases: cause and effect? Front Pharmacol. 27, 6-29.
  52. Nestler, E.J., and Carlezon, W.A. Jr. (2006). The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59, 1151-1159. https://doi.org/10.1016/j.biopsych.2005.09.018
  53. Panda, S., Antoch, M.P., Miller, B.H., Su, A.I., Schook, A.B., Straume, M., Schultz, P.G., Kay, S.A., Takahashi, J.S., and Hogenesch, J.B. (2002). Coordinated transcription of key pathways in the mouse by the circadian clock. Cell 109, 307-320. https://doi.org/10.1016/S0092-8674(02)00722-5
  54. Preitner, N., Damiola, F., Lopez-Molina, L., Zakany, J., Duboule, D., Albrecht, U., and Schibler, U. (2002). The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 110, 251-260. https://doi.org/10.1016/S0092-8674(02)00825-5
  55. Renard, C.E., Fiocco, A.J., Clenet, F., Hascoet, M., and Bourin, M. (2001). Is dopamine implicated in the antidepressant-like effects of selective serotonin reuptake inhibitors in the mouse forced swimming test? Psychopharmacology 159, 42-50. https://doi.org/10.1007/s002130100836
  56. Richard, I.H., Frank, S., McDermott, M.P., Wang, H., Justus, A.W., LaDonna, K.A., and Kurlan, R. (2004). The ups and downs of Parkinson disease: a prospective study of mood and anxiety fluctuations. Cogn. Behav. Neurol. 17, 201-207.
  57. Roedter, A., Winkler, C., Samii, M., Walter, G.F., Brandis, A., and Nikkhah, G. (2001). Comparison of unilateral and bilateral intrastriatal 6-hydroxydopamine-induced axon terminal lesions: evidence for interhemispheric functional coupling of the two nigrostriatal pathways. J. Comp. Neurol. 432, 217-229. https://doi.org/10.1002/cne.1098
  58. Roybal, K., Theobold, D., Graham, A., DiNieri, J.A., Russo, S.J., Krishnan, V., Chakravarty, S., Peevey, J., Oehrlein, N., Birnbaum, S., et al. (2007). Mania-like behavior induced by disruption of CLOCK. Proc. Natl. Acad. Sci. USA 104, 6406-6411. https://doi.org/10.1073/pnas.0609625104
  59. Russo, S.J., and Nestler, E.J. (2013). The brain reward circuitry in mood disorders. Nat. Rev. Neurosci. 14, 609-625.
  60. Shearman, L.P., Sriram, S., Weaver, D.R., Maywood, E.S., Chaves, I., Zheng, B., Kume, K., Lee, C.C., van der Horst, G.T., Hastings, M.H., et al. (2000). Interacting molecular loops in the mammalian circadian clock. Science 288, 1013-1019. https://doi.org/10.1126/science.288.5468.1013
  61. Solt, L.A., Wang, Y., Banerjee, S., Hughes, T., Kojetin, D.J., Lundasen, T., Shin, Y., Liu, J., Cameron, M.D., Noel, R., et al. (2012). Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 485, 62-68. https://doi.org/10.1038/nature11030
  62. Soria, V., Martinez-Amoros, E., Escaramis, G., Valero, J., Perez-Egea, R., Garcia, C., Gutierrez-Zotes, A., Puigdemont, D., Bayes, M., Crespo, J.M., et al. (2010). Differential association of circadian genes with mood disorders: CRY1 and NPAS2 are associated with unipolar major depression and CLOCK and VIP with bipolar disorder. Neuropsychopharmacology 35, 1279-1289. https://doi.org/10.1038/npp.2009.230
  63. Sprouse, J., Braselton, J., and Reynolds, L. (2006). Fluoxetine modulates the circadian biological clock via phase advances of suprachiasmatic nucleus neuronal firing. Biol. Psychiatry 60, 896-899. https://doi.org/10.1016/j.biopsych.2006.03.003
  64. Storch, K.F., Lipan, O., Leykin, I., Viswanathan, N., Davis, F.C., Wong, W.H., and Weitz, C.J. (2002). Extensive and divergent circadian gene expression in liver and heart. Nature 417, 78-83. https://doi.org/10.1038/nature744
  65. Videnovic, A., and Willis, G.L. (2016). Circadian system - A novel diagnostic and therapeutic target in Parkinson's disease? Mov. Disord. 31, 260-269. https://doi.org/10.1002/mds.26509
  66. Videnovic, A., Lazar, A.S., Barker, R.A., and Overeem, S. (2014). 'The clocks that time us'--circadian rhythms in neurodegenerative disorders. Nat. Rev. Neurol. 10, 683-693. https://doi.org/10.1038/nrneurol.2014.206
  67. Volkow, N.D., Wang, G.J., Kollins, S.H., Wigal, T.L., Newcorn, J.H., Telang, F., Fowler, J.S., Zhu, W., Logan, J., and Ma, Y. (2009). Evaluating dopamine reward pathway in ADHD: clinical implications. JAMA 302, 1084-1091. https://doi.org/10.1001/jama.2009.1308
  68. Watabe-Uchida, M., Zhu, L., Ogawa, S.K., Vamanrao, A., and Uchida, N. (2012). Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74, 858-873. https://doi.org/10.1016/j.neuron.2012.03.017
  69. Webb, I.C., Baltazar, R.M., Wang, X., Pitchers, K.K., Coolen, L.M., and Lehman, M.N. (2009). Diurnal variations in natural and drug reward, mesolimbic tyrosine hydroxylase, and clock gene expression in the male rat. J. Biol. Rhythms 24, 465-476. https://doi.org/10.1177/0748730409346657
  70. Weber, M., Lauterburg, T., Tobler, I., and Burgunder, J.M. (2004). Circadian patterns of neurotransmitter related gene expression in motor regions of the rat brain. Neurosci. Lett. 358, 17-20. https://doi.org/10.1016/j.neulet.2003.12.053
  71. Weintraub, D., Morales, K.H., Moberg, P.J., Bilker, W.B., Balderston, C., Duda, J.E., Katz, I.R., and Stern, M.B. (2005). Antidepressant studies in Parkinson's disease: a review and meta-analysis. Mov. Disord. 20, 1161-1169. https://doi.org/10.1002/mds.20555
  72. Wirz-Justice, A. (2006). Biological rhythm disturbances in mood disorders. Int. Clin. Psychopharmacol. 21 Suppl 4, S11-S15.
  73. Wise, R.A. (1998). Drug-activation of brain reward pathways. Drug Alcohol. Depend. 51, 13-22. https://doi.org/10.1016/S0376-8716(98)00063-5
  74. Wulff, K., Gatti, S., Wettstein, J.G., and Foster, R.G. (2010). Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nat. Rev. Neurosci. 11, 589-599.
  75. Yadid, G., Overstreet, D.H., and Zangen, A. (2001). Limbic dopaminergic adaptation to a stressful stimulus in a rat model of depression. Brain Res. 896, 43-47. https://doi.org/10.1016/S0006-8993(00)03248-0
  76. Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R., Ueda, M., Block, G.D., Sakaki, Y., Menaker, M., and Tei H. (2000). Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682-685. https://doi.org/10.1126/science.288.5466.682
  77. Yin, L., and Lazar, M.A. (2005). The orphan nuclear receptor $Reverb{\alpha}$ recruits the N-CoR/histone Deacetylase 3 corepressor to regulate the circadian Bmal1 gene. Mol. Endocrinol. 19, 1452-1459. https://doi.org/10.1210/me.2005-0057
  78. Yin, L., Wang, J., Klein, P.S., and Lazar, M.A. (2006). Nuclear receptor Rev-erbalpha is a critical lithium-sensitive component of the circadian clock. Science 311, 1002-1005. https://doi.org/10.1126/science.1121613
  79. Zarow, C, Lyness, S.A., Mortimer, J.A., and Chui, H.C. (2003). Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch. Neurol. 60, 337-341. https://doi.org/10.1001/archneur.60.3.337
  80. Zhang, R., Lahens, N.F., Balance, H.I., Hughes, M.E., and Hogenesch, J.B. (2014). A circadian gene expression atlas in mammals: implications for biology and medicine. Proc. Natl. Acad. Sci. USA 111, 16219-16224. https://doi.org/10.1073/pnas.1408886111
  81. Zhao, X., Hirota, T., Han, X., Cho, H., Chong, L.W., Lamia, K., Liu, S., Atkins, A.R., Banayo, E., Liddle, C., et al. (2016). Circadian amplitude regulation via FBXW7-targeted REV-$ERB{\alpha}$ degradation. Cell 165, 1644-1657. https://doi.org/10.1016/j.cell.2016.05.012
  82. Zheng, B., Larkin, D.W., Albrecht, U., Sun, Z.S., Sage, M., Eichele, G., Lee, C.C., and Bradley, A. (1999). The mPer2 gene encodes a functional component of the mammalian circadian clock. Nature 400, 169-173. https://doi.org/10.1038/22118
  83. Zheng, B., Albrecht, U., Kaasik, K., Sage, M., Lu, W., Vaishnav, S., Li, Q., Sun, Z.S., Eichele, G., Bradley, A., et al. (2001). Nonredundant roles of the mPer1 and mPer2 genes in the mammalian circadian clock. Cell 105, 683-694. https://doi.org/10.1016/S0092-8674(01)00380-4
  84. Zhu, B., Gates, L.A., Stashi, E., Dasgupta, S., Gonzales, N., Dean, A., Dacso, C.C., York, B., and O'Malley, B.W. (2015). Coactivatordependent oscillation of chromatin accessibility dictates circadian gene amplitude via REV-ERB loading. Mol. Cell 60, 769-783. https://doi.org/10.1016/j.molcel.2015.10.024

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  7. Sex Differences in Patterns of Sleep Disorders Among Hospitalizations With Parkinson’s Disease: 2004-2014 Nationwide Inpatient Sample vol.83, pp.5, 2017, https://doi.org/10.1097/psy.0000000000000949
  8. Recent Progress in Non-motor Features of Parkinson’s Disease with a Focus on Circadian Rhythm Dysregulation vol.37, pp.7, 2017, https://doi.org/10.1007/s12264-021-00711-x
  9. Fullerene-Filtered Light Spectrum and Fullerenes Modulate Emotional and Pain Processing in Mice vol.13, pp.11, 2017, https://doi.org/10.3390/sym13112004