Circadian clock disruption in neurodegenerative diseases: Cause and effect?

Frontiers in Pharmacology

Volumn 6, Issue FEB, 2015, Pages

  Musiek, Erik S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer disease; Bmal1; Circadian clock; Huntington disease; Neurodegeneration; Per2

Indexed keywords

PER2 PROTEIN; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK;

ALZHEIMER DISEASE; ARTICLE; BEHAVIOR THERAPY; BMAL1 GENE; CIRCADIAN RHYTHM; CLOCK GENE; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DISEASE EXACERBATION; GENE FUNCTION; HUMAN; HUNTINGTON CHOREA; NONHUMAN; OSCILLATION; PARKINSON DISEASE; PATHOGENESIS; PROTEIN DNA BINDING; PROTEIN FUNCTION; SLEEP; SUPRACHIASMATIC NUCLEUS;

EID: 84926505629     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2015.00029     Document Type: Article

References (73)

1. An, S., Harang, R., Meeker, K., Granados-Fuentes, D., Tsai, C. A., Mazuski, C., et al. (2013). A neuropeptide speeds circadian entrainment by reducing intercellular synchrony. Proc. Natl. Acad. Sci. U.S.A. 110, E4355-E4361. doi: 10.1073/pnas.1307088110
2. Aton, S. J., Colwell, C. S., Harmar, A. J., Waschek, J., and Herzog, E. D. (2005). Vasoactive intestinal polypeptide mediates circadian rhythmicity and synchrony in mammalian clock neurons. Nat. Neurosci. 8, 476-483. doi: 10.1038/nn1419
3. Aziz, N. A., Anguelova, G. V., Marinus, J., Lammers, G. J., and Roos, R. A. (2010). Sleep and circadian rhythm alterations correlate with depression and cognitive impairment in Huntington's disease. Parkinsonism Relat. Disord. 16, 345-350. doi: 10.1016/j.parkreldis.2010.02.009
4. Bae, K., Jin, X., Maywood, E. S., Hastings, M. H., Reppert, S. M., and Weaver, D. R. (2001). Differential functions of mPer1, mPer2, and mPer3 in the SCN circadian clock. Neuron 30, 525-536. doi: 10.1016/S0896-6273(01)00302-6
5. Bass, J., and Takahashi, J. S. (2010). Circadian integration of metabolism and energetics. Science 330, 1349-1354. doi: 10.1126/science.1195027
6. Beal, M. F., Ferrante, R. J., Henshaw, R., Matthews, R. T., Chan, P. H., Kowall, N. W., et al. (1995). 3-Nitropropionic acid neurotoxicity is attenuated in copper/zinc superoxide dismutase transgenic mice. J. Neurochem. 65, 919-922. doi: 10.1046/j.1471-4159.1995.65020919.x
7. Beaver, L. M., Klichko, V. I., Chow, E. S., Kotwica-Rolinska, J., Williamson, M., Orr, W. C., et al. (2012). Circadian regulation of glutathione levels and biosynthesis in Drosophila melanogaster. PLoS ONE 7:e50454. doi: 10.1371/journal.pone.0050454
8. Breen, D. P., Vuono, R., Nawarathna, U., Fisher, K., Shneerson, J. M., Reddy, A. B., et al. (2014). Sleep and circadian rhythm regulation in early Parkinson disease. JAMA Neurol. 71, 589-595. doi: 10.1001/jamaneurol.2014.65
9. Cai, Y., Liu, S., Sothern, R. B., Xu, S., and Chan, P. (2010). Expression of clock genes Per1 and Bmal1 in total leukocytes in health and Parkinson's disease. Eur. J. Neurol. 17, 550-554. doi: 10.1111/j.1468-1331.2009.02848.x
10. Cermakian, N., Lamont, E. W., Boudreau, P., and Boivin, D. B. (2011). Circadian clock gene expression in brain regions of Alzheimer's disease patients and control subjects. J. Biol. Rhythms 26, 160-170. doi: 10.1177/0748730410395732
11. Chen, H. F., Huang, C. Q., You, C., Wang, Z. R., and Si-Qing, H. (2013a). Polymorphism of CLOCK gene rs 4580704 C > G is associated with susceptibility of Alzheimer's disease in a Chinese population. Arch. Med. Res. 44, 203-207. doi: 10.1016/j.arcmed.2013.01.002
12. Chen, Q., Huang, C. Q., Hu, X. Y., Li, S. B., and Zhang, X. M. (2013b). Functional CLOCK gene rs1554483 G/C polymorphism is associated with susceptibility to Alzheimer's disease in the Chinese population. J. Int. Med. Res. 41, 340-346. doi: 10.1177/0300060513476430
13. Chen, K. F., Possidente, B., Lomas, D. A., and Crowther, D. C. (2014). The central molecular clock is robust in the face of behavioural arrhythmia in a Drosophila model of Alzheimer's disease. Dis. Model. Mech. 7, 445-458. doi: 10.1242/dmm.014134
14. Chen, Z., Yoo, S. H., Park, Y. S., Kim, K. H., Wei, S., Buhr, E., et al. (2012). Identification of diverse modulators of central and peripheral circadian clocks by high-throughput chemical screening. Proc. Natl. Acad. Sci. U.S.A. 109, 101-106. doi: 10.1073/pnas.1118034108
15. Cho, K. (2001). Chronic 'jet lag' produces temporal lobe atrophy and spatial cognitive deficits. Nat. Neurosci. 4, 567-568. doi: 10.1038/88384
16. Cho, K., Ennaceur, A., Cole, J. C., and Suh, C. K. (2000). Chronic jet lag produces cognitive deficits. J. Neurosci. 20, 1-5.
17. Coogan, A. N., Schutova, B., Husung, S., Furczyk, K., Baune, B. T., Kropp, P., et al. (2013). The circadian system in Alzheimer's disease: disturbances, mechanisms, and opportunities. Biol. Psychiatry 74, 333-339. doi: 10.1016/j.biopsych.2012.11.021
18. De Bruyne, J. P., Weaver, D. R., and Reppert, S. M. (2007). CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat. Neurosci. 10, 543-545. doi: 10.1038/nn1884
19. Duncan, M. J., Smith, J. T., Franklin, K. M., Beckett, T. L., Murphy, M. P., St Clair, D. K., et al. (2012). Effects of aging and genotype on circadian rhythms, sleep, and clock gene expression in APPxPS1 knock-in mice, a model for Alzheimer's disease. Exp. Neurol. 236, 249-258. doi: 10.1016/j.expneurol.2012.05.011
20. Evans, J. A., and Davidson, A. J. (2013). Health consequences of circadian disruption in humans and animal models. Prog. Mol. Biol. Transl. Sci. 119, 283-323. doi: 10.1016/B978-0-12-396971-2.00010-5
21. Fahrenkrug, J., Popovic, N., Georg, B., Brundin, P., and Hannibal, J. (2007). Decreased VIP and VPAC2 receptor expression in the biological clock of the R6/2 Huntington's disease mouse. J. Mol. Neurosci. 31, 139-148. doi: 10.1385/JMN/31:02:139
22. Farajnia, S., Michel, S., Deboer, T., Vanderleest, H. T., Houben, T., Rohling, J. H., et al. (2012). Evidence for neuronal desynchrony in the aged suprachiasmatic nucleus clock. J. Neurosci. 32, 5891-5899. doi: 10.1523/JNEUROSCI.0469-12.2012
23. Gajula Balija, M. B., Griesinger, C., Herzig, A., Zweckstetter, M., and Jackle, H. (2011). Pre-fibrillar a-synuclein mutants cause Parkinson's disease-like non-motor symptoms in Drosophila. PLoS ONE 6:e24701. doi: 10.1371/journal.pone.0024701
24. Gibson, E. M., Wang, C., Tjho, S., Khattar, N., and Kriegsfeld, L. J. (2010). Experimental 'jet lag' inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters. PLoS ONE 5:e15267. doi: 10.1371/journal.pone.0015267
25. Hatfield, C. F., Herbert, J., Van Someren, E. J., Hodges, J. R., and Hastings, M. H. (2004). Disrupted daily activity/rest cycles in relation to daily cortisol rhythms of home-dwelling patients with early Alzheimer's dementia. Brain 127, 1061-1074. doi: 10.1093/brain/awh129
26. Hirota, T., Lee, J. W., Lewis, W. G., Zhang, E. E., Breton, G., Liu, X., et al. (2010). High-throughput chemical screen identifies a novel potent modulator of cellular circadian rhythms and reveals CKIa as a clock regulatory kinase. PLoS Biol. 8:e1000559. doi: 10.1371/journal.pbio.1000559
27. Hu, K., Van Someren, E. J., Shea, S. A., and Scheer, F. A. (2009). Reduction of scale invariance of activity fluctuations with aging and Alzheimer's disease: involvement of the circadian pacemaker. Proc. Natl. Acad. Sci. U.S.A. 106, 2490-2494. doi: 10.1073/pnas.0806087106
28. Huang, Y., Potter, R., Sigurdson, W., Santacruz, A., Shih, S., Ju, Y. E., et al. (2012). Effects of age and amyloid deposition on Aß dynamics in the human central nervous system. Arch. Neurol. 69, 51-58. doi: 10.1001/archneurol.2011.235
29. Ju, Y. E., Lucey, B. P., and Holtzman, D. M. (2014). Sleep and Alzheimer disease pathology-a bidirectional relationship. Nat. Rev. Neurol. 10, 115-119. doi: 10.1038/nrneurol.2013.269
30. Ju, Y. E., Mcleland, J. S., Toedebusch, C. D., Xiong, C., Fagan, A. M., Duntley, S. P., et al. (2013). Sleep quality and preclinical Alzheimer disease. JAMA Neurol. 70, 587-593. doi: 10.1001/jamaneurol.2013.2334
31. Kang, J. E., Lim, M. M., Bateman, R. J., Lee, J. J., Smyth, L. P., Cirrito, J. R., et al. (2009). Amyloid-ß dynamics are regulated by orexin and the sleep-wake cycle. Science 326, 1005-1007. doi: 10.1126/science.1180962
32. Karatsoreos, I. N., Bhagat, S., Bloss, E. B., Morrison, J. H., and Mcewen, B. S. (2011). Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc. Natl. Acad. Sci. U.S.A. 108, 1657-1662. doi: 10.1073/pnas.1018375108
33. Koike, N., Yoo, S. H., Huang, H. C., Kumar, V., Lee, C., Kim, T. K., et al. (2012). Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 338, 349-354. doi: 10.1126/science.1226339
34. Kott, J., Leach, G., and Yan, L. (2012). Direction-dependent effects of chronic "jet-lag" on hippocampal neurogenesis. Neurosci. Lett. 515, 177-180. doi: 10.1016/j.neulet.2012.03.048
35. Krishnan, N., Davis, A. J., and Giebultowicz, J. M. (2008). Circadian regulation of response to oxidative stress in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 374, 299-303. doi: 10.1016/j.bbrc.2008.07.011
36. Krishnan, N., Kretzschmar, D., Rakshit, K., Chow, E., and Giebultowicz, J. M. (2009). The circadian clock gene period extends healthspan in aging Drosophila melanogaster. Aging (Albany NY) 1, 937-948.
37. Krishnan, N., Rakshit, K., Chow, E. S., Wentzell, J. S., Kretzschmar, D., and Giebultowicz, J. M. (2012). Loss of circadian clock accelerates aging in neurodegeneration-prone mutants. Neurobiol. Dis. 45, 1129-1135. doi: 10.1016/j.nbd.2011.12.034
38. Kudo, T., Loh, D. H., Truong, D., Wu, Y., and Colwell, C. S. (2011a). Circadian dysfunction in a mouse model of Parkinson's disease. Exp. Neurol. 232, 66-75. doi: 10.1016/j.expneurol.2011.08.003
39. Kudo, T., Schroeder, A., Loh, D. H., Kuljis, D., Jordan, M. C., Roos, K. P., et al. (2011b). Dysfunctions in circadian behavior and physiology in mouse models of Huntington's disease. Exp. Neurol. 228, 80-90. doi: 10.1016/j.expneurol.2010.12.011
40. Kudo, T., Tahara, Y., Gamble, K. L., Mcmahon, D. G., Block, G. D., and Colwell, C. S. (2013). Vasoactive intestinal peptide produces long-lasting changes in neural activity in the suprachiasmatic nucleus. J. Neurophysiol. 110, 1097-1106. doi: 10.1152/jn.00114.2013
41. Laposky, A., Easton, A., Dugovic, C., Walisser, J., Bradfield, C., and Turek, F. (2005). Deletion of the mammalian circadian clock gene BMAL1/Mop3 alters baseline sleep architecture and the response to sleep deprivation. Sleep 28, 395-409.
42. Lim, A. S., Kowgier, M., Yu, L., Buchman, A. S., and Bennett, D. A. (2013a). Sleep fragmentation and the risk of incident Alzheimer's disease and cognitive decline in older persons. Sleep 36, 1027-1032. doi: 10.5665/sleep.2802
43. Lim, A. S., Myers, A. J., Yu, L., Buchman, A. S., Duffy, J. F., De Jager, P. L., et al. (2013b). Sex difference in daily rhythms of clock gene expression in the aged human cerebral cortex. J. Biol. Rhythms 28, 117-129. doi: 10.1177/0748730413478552
44. Lim, A. S., Srivastava, G. P., Yu, L., Chibnik, L. B., Xu, J., Buchman, A. S., et al. (2014). 24-hour rhythms of DNA methylation and their relation with rhythms of RNA expression in the human dorsolateral prefrontal cortex. PLoS Genet. 10:e1004792. doi: 10.1371/journal.pgen.1004792
45. Long, D. M., Blake, M. R., Dutta, S., Holbrook, S. D., Kotwica-Rolinska, J., Kretzschmar, D., et al. (2014). Relationships between the circadian system and Alzheimer's disease-like symptoms in Drosophila. PLoS ONE 9:e106068. doi: 10.1371/journal.pone.0106068
46. Maywood, E. S., Fraenkel, E., Mcallister, C. J., Wood, N., Reddy, A. B., Hastings, M. H., et al. (2010). Disruption of peripheral circadian timekeeping in a mouse model of Huntington's disease and its restoration by temporally scheduled feeding. J. Neurosci. 30, 10199-10204. doi: 10.1523/JNEUROSCI.1694-10.2010
47. Mohawk, J. A., Green, C. B., and Takahashi, J. S. (2012). Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 35, 445-462. doi: 10.1146/annurev-neuro-060909-153128
48. Mongrain, V., La Spada, F., Curie, T., and Franken, P. (2011). Sleep loss reduces the DNA-binding of BMAL1, CLOCK, and NPAS2 to specific clock genes in the mouse cerebral cortex. PLoS ONE 6:e26622. doi: 10.1371/journal.pone.0026622
49. Morton, A. J., Wood, N. I., Hastings, M. H., Hurelbrink, C., Barker, R. A., and Maywood, E. S. (2005). Disintegration of the sleep-wake cycle and circadian timing in Huntington's disease. J. Neurosci. 25, 157-163. doi: 10.1523/JNEUROSCI.3842-04.2005
50. Musiek, E. S., Lim, M. M., Yang, G., Bauer, A. Q., Qi, L., Lee, Y., et al. (2013). Circadian clock proteins regulate neuronal redox homeostasis and neurodegeneration. J. Clin. Invest. 123, 5389-5400. doi: 10.1172/JCI70317
51. Niwa, F., Kuriyama, N., Nakagawa, M., and Imanishi, J. (2011). Circadian rhythm of rest activity and autonomic nervous system activity at different stages in Parkinson's disease. Auton. Neurosci. 165, 195-200. doi: 10.1016/j.autneu.2011.07.010
52. Pallier, P. N., Maywood, E. S., Zheng, Z., Chesham, J. E., Inyushkin, A. N., Dyball, R., et al. (2007). Pharmacological imposition of sleep slows cognitive decline and reverses dysregulation of circadian gene expression in a transgenic mouse model of Huntington's disease. J. Neurosci. 27, 7869-7878. doi: 10.1523/JNEUROSCI.0649-07.2007
53. Pallier, P. N., and Morton, A. J. (2009). Management of sleep/wake cycles improves cognitive function in a transgenic mouse model of Huntington's disease. Brain Res. 1279, 90-98. doi: 10.1016/j.brainres.2009.03.072
54. Peter-Derex, L., Yammine, P., Bastuji, H., and Croisile, B. (2014). Sleep and Alzheimer's disease. Sleep Med. Rev. 19C, 29-38. doi: 10.1016/j.smrv.2014.03.007
55. Rakshit, K., and Giebultowicz, J. M. (2013). Cryptochrome restores dampened circadian rhythms and promotes healthspan in aging Drosophila. Aging Cell 12, 752-762. doi: 10.1111/acel.12100
56. Roh, J. H., Huang, Y., Bero, A. W., Kasten, T., Stewart, F. R., Bateman, R. J., et al. (2012). Disruption of the sleep-wake cycle and diurnal fluctuation of ß-amyloid in mice with Alzheimer's disease pathology. Sci. Transl. Med. 4, 150ra122. doi: 10.1126/scitranslmed.3004291
57. Schnell, A., Chappuis, S., Schmutz, I., Brai, E., Ripperger, J. A., Schaad, O., et al. (2014). The nuclear receptor REV-ERBa regulates Fabp7 and modulates adult hippocampal neurogenesis. PLoS ONE 9:e99883. doi: 10.1371/journal.pone.0099883
58. Skene, D. J., and Swaab, D. F. (2003). Melatonin rhythmicity: effect of age and Alzheimer's disease. Exp. Gerontol. 38, 199-206. doi: 10.1016/S0531-5565(02)00198-5
59. Spira, A. P., Gamaldo, A. A., An, Y., Wu, M. N., Simonsick, E. M., Bilgel, M., et al. (2013). Self-reported sleep and ß-amyloid deposition in community-dwelling older adults. JAMA Neurol. 70, 1537-1543. doi: 10.1001/jamaneurol.2013.4258
60. Sterniczuk, R., Dyck, R. H., Laferla, F. M., and Antle, M. C. (2010). Characterization of the 3xTg-AD mouse model of Alzheimer's disease: part 1. Circadian changes. Brain Res. 1348, 139-148. doi: 10.1016/j.brainres.2010.05.013
61. Swaab, D. F., Fliers, E., and Partiman, T. S. (1985). The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia. Brain Res. 342, 37-44. doi: 10.1016/0006-8993(85)91350-2
62. Tranah, G. J., Blackwell, T., Stone, K. L., Ancoli-Israel, S., Paudel, M. L., Ensrud, K. E., et al. (2011). Circadian activity rhythms and risk of incident dementia and mild cognitive impairment in older women. Ann. Neurol. 70, 722-732. doi: 10.1002/ana.22468
63. Valnegri, P., Khelfaoui, M., Dorseuil, O., Bassani, S., Lagneaux, C., Gianfelice, A., et al. (2011). A circadian clock in hippocampus is regulated by interaction between oligophrenin-1 and Rev-erba. Nat. Neurosci. 14, 1293-1301. doi: 10.1038/nn.2911
64. Videnovic, A., and Golombek, D. (2013). Circadian and sleep disorders in Parkinson's disease. Exp. Neurol. 243, 45-56. doi: 10.1016/j.expneurol.2012.08.018
65. Videnovic, A., Lazar, A. S., Barker, R. A., and Overeem, S. (2014a). 'The clocks that time us'-circadian rhythms in neurodegenerative disorders. Nat. Rev. Neurol. 10, 683-693. doi: 10.1038/nrneurol.2014.206
66. Videnovic, A., Noble, C., Reid, K. J., Peng, J., Turek, F. W., Marconi, A., et al. (2014b). Circadian melatonin rhythm and excessive daytime sleepiness in Parkinson disease. JAMA Neurol. 71, 463-469. doi: 10.1001/jamaneurol.2013.6239
67. Wisor, J. P., Edgar, D. M., Yesavage, J., Ryan, H. S., Mccormick, C. M., Lapustea, N., et al. (2005). Sleep and circadian abnormalities in a transgenic mouse model of Alzheimer's disease: a role for cholinergic transmission. Neuroscience 131, 375-385. doi: 10.1016/j.neuroscience.2004.11.018
68. Witting, W., Kwa, I. H., Eikelenboom, P., Mirmiran, M., and Swaab, D. F. (1990). Alterations in the circadian rest-activity rhythm in aging and Alzheimer's disease. Biol. Psychiatry 27, 563-572. doi: 10.1016/0006-3223(90)90523-5
69. Wu, Y. H., Fischer, D. F., Kalsbeek, A., Garidou-Boof, M. L., Van Der Vliet, J., Van Heijningen, C., et al. (2006). Pineal clock gene oscillation is disturbed in Alzheimer's disease, due to functional disconnection from the "master clock." FASEB J. 20, 1874-1876. doi: 10.1096/fj.05-4446fje
70. Yamaguchi, Y., Suzuki, T., Mizoro, Y., Kori, H., Okada, K., Chen, Y., et al. (2013). Mice genetically deficient in vasopressin V1a and V1b receptors are resistant to jet lag. Science 342, 85-90. doi: 10.1126/science.1238599
71. Yang, Y. K., Peng, X. D., Li, Y. H., Wang, Z. R., Chang-Quan, H., Hui, W., et al. (2013). The polymorphism of CLOCK gene 3111T/C C>T is associated with susceptibility of Alzheimer disease in Chinese population. J. Investig. Med. 61, 1084-1087. doi: 10.231/JIM.0b013e31829f91c0
72. Zhang, R., Lahens, N. F., Ballance, 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. U.S.A. 111, 16219-16224. doi: 10.1073/pnas.1408886111
73. Zhou, J. N., Hofman, M. A., and Swaab, D. F. (1995). VIP neurons in the human SCN in relation to sex, age, and Alzheimer's disease. Neurobiol. Aging 16, 571-576. doi: 10.1016/0197-4580(95)00043-E