Circadian Clock Gene Expression in Brain Regions of Alzheimer ’s Disease Patients and Control Subjects
Abstract
Circadian oscillators have been observed throughout the rodent brain. In the human brain, rhythmic expression of clock genes has been reported only in the pineal gland, and little is known about their expression in other regions. The investigators sought to determine whether clock gene expression could be detected and whether it varies as a function of time of day in the bed nucleus of the stria terminalis (BNST) and cingulate cortex, areas known to be involved in decision making and motivated behaviors, as well as in the pineal gland, in the brains of Alzheimer’s disease (AD) patients and aged controls. Relative expression levels of PERIOD1 ( PER1 ), PERIOD2 ( PER2), and Brain and muscle Arnt-like protein-1 (BMAL1) were detected by quantitative PCR in all 3 brain regions. A harmonic regression model revealed significant 24-h rhythms of PER1 in the BNST of AD subjects. A significant rhythm of PER2 was found in the cingulate cortex and BNST of control subjects and in all 3 regions of AD patients. In controls, BMAL1 did not show a diurnal rhythm in the cingulate cortex but significantly varied with time of death in the pineal and BNST and in all 3 regions for AD patients . Notable differences in the phase of clock gene rhythms and phase relationships between genes and regions were observed in the brains of AD compared to those of controls. These results indicate the presence of multiple circadian oscillators in the human brain and suggest altered synchronization among these oscillators in the brain of AD patients.
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Individuals with AD still show cycling clock gene expression in multiple brain regions but lose typical phase coherence within and across regions.
“although individuals with AD still show cycling clock gene expression in multiple brain regions, they lose typical phase coherence within and across regions263”
From Rhythms of life: circadian disruption and brain disorders across the lifespan (2019) · cites this paper as [263]
Cites
Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., Vogel, F. S., Hughes, J. P., Belle, G. V., Berg, L., et al. (1991) · Neurology · doi:10.1212/wnl.41.4.479 · Cited by 4,961 · see citing works
Yoo, S.-H., Yamazaki, S., Lowrey, P. L., Shimomura, K., Ko, C. H., Buhr, E. D., Siepka, S. M., Hong, H.-K., Oh, W. J., Yoo, O. J., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308709101 · Cited by 2,329 · see citing works
Shao, J., & Tu, D. (1995) · Springer Series in Statistics · doi:10.1007/978-1-4612-0795-5 · Cited by 1,985 · see citing works
The suprachiasmatic nucleus of the human brain in relation to sex, age and senile dementia
Swaab, D. F., Fliers, E., & Partiman, T. S. (1985) · Brain Research · doi:10.1016/0006-8993(85)91350-2 · Cited by 847 · see citing works
Circadian Expression of Clock Genes in Human Oral Mucosa and Skin
Bjarnason, G. A., Jordan, R. C., Wood, P. A., Li, Q., Lincoln, D. W., Sothern, R. B., Hrushesky, W. J. M., & Ben‐David, Y. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64135-1 · Cited by 379 · see citing works
Sleep problems in the community elderly as predictors of death and nursing home placement
Pollak, C. P., PERLICK, D. A., Linsner, J. P., Wenston, J., & Hsieh, F. (1990) · Journal of Community Health · doi:10.1007/bf01321316 · Cited by 350 · see citing works
Sleep and quantitative EEG in neurodegenerative disorders
Petit, D., Gagnon, J., Fantini, M. L., Ferini‐Strambi, L., & Montplaisir, J. Y. (2004) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2004.02.001 · Cited by 349 · see citing works
Guilding, C., & Piggins, H. D. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05581.x · Cited by 348 · see citing works
Circadian clock genes oscillate in human peripheral blood mononuclear cells
Boivin, D. B., James, F. O., Wu, A., Cho-Park, P. F., Xiong, H., & Sun, Z. S. (2003) · Blood · doi:10.1182/blood-2003-03-0779 · Cited by 340 · see citing works
Self-citationSleep, EEG and mental function changes in senile dementia of the Alzheimer's type
Prinz, P. N., VITALIANO, P. P., Vitiello, M. V., Bokan, J. A., Raskind, M. A., Peskind, E. R., & Gerber, C. J. (1982) · Neurobiology of Aging · doi:10.1016/0197-4580(82)90024-0 · Cited by 324 · see citing works
Sakamoto, K., Nagase, T., Fukui, H., Horikawa, K., Okada, T., Tanaka, H., Sato, K. Z., Miyake, Y., Ohara, O., Kako, K., et al. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.42.27039 · Cited by 300 · see citing works
Microarray analysis of postmortem temporal cortex from patients with schizophrenia
Aston, C., Jiang, L., & Sokolov, B. P. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20208 · Cited by 283 · see citing works
Mishima, K., Tozawa, T., Satoh, K., Matsumoto, Y., Hishikawa, Y., & Okawa, M. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00510-6 · Cited by 269 · see citing works
Pathologic Evaluation of the Human Suprachiasmatic Nucleus in Severe Dementia
Stopa, E. G., Volicer, L., Kuo-Leblanc, V., Harper, D., Lathi, D., Tate, B., & Satlin, A. (1999) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199901000-00004 · Cited by 265 · see citing works
Oishi, K., Sakamoto, K., Okada, T., Nagase, T., & Ishida, N. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9779 · Cited by 257 · see citing works
Lamont, E. W., Robinson, B., Stewart, J., & Amir, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500901102 · Cited by 256 · see citing works
VIP neurons in the human SCN in relation to sex, age, and Alzheimer's disease
Zhou, J. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)00043-e · Cited by 243 · see citing works
Bonanni, E., Maestri, M., Tognoni, G., Fabbrini, M., Nucciarone, B., Manca, M. L., Gori, S., Iudice, A., & Murri, L. (2005) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2005.00462.x · Cited by 213 · see citing works
Disturbance of Endogenous Circadian Rhythm in Aging and Alzheimer Disease
Harper, D. G., Volicer, L., Stopa, E. G., McKee, A. C., Nitta, M., & Satlin, A. (2005) · American Journal of Geriatric Psychiatry · doi:10.1176/appi.ajgp.13.5.359 · Cited by 199 · see citing works
Characterization of the 3xTg-AD mouse model of Alzheimer's disease: Part 1. Circadian changes
Sterniczuk, R., Dyck, R. H., LaFerla, F. M., & Antle, M. C. (2010) · Brain Research · doi:10.1016/j.brainres.2010.05.013 · Cited by 198 · see citing works
Guo, H., Brewer, J. M., Lehman, M. N., & Bittman, E. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4676-05.2006 · Cited by 180 · see citing works
Quantification of mRNA degradation as possible indicator of postmortem interval—a pilot study
Bauer, M., Gramlich, I., Polzin, S., & Patzelt, D. (2003) · Legal Medicine · doi:10.1016/j.legalmed.2003.08.001 · Cited by 179 · see citing works
Masubuchi, S., Honma, S., Abe, H., Ishizaki, K., Namihira, M., Ikeda, M., & Honma, K. (2000) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2000.01313.x · Cited by 177 · see citing works
Wu, Y., Fischer, D. F., Kalsbeek, A., Garidou, M., van der Vliet, J., Heijningen, C. L. V., Liu, R., Zhou, J., & Swaab, D. F. (2006) · The FASEB Journal · doi:10.1096/fj.05-4446fje · Cited by 175 · see citing works
Amir, S., Lamont, E. W., Robinson, B., & Stewart, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4488-03.2004 · Cited by 175 · see citing works
Forebrain oscillators ticking with different clock hands
Feillet, C. A., Mendoza, J., Albrecht, U., Pévet, P., & Challet, É. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2007.09.010 · Cited by 170 · see citing works
Archer, S. N., Viola, A., Kyriakopoulou, V., von Schantz, M., & Dijk, D. (2008) · SLEEP · doi:10.1093/sleep/31.5.608 · Cited by 156 · see citing works
Bianchetti, A., Scuratti, A., Zanetti, O. O., Binetti, G. G., Frisoni, G. B., Magni, E., & Trabucchi, M. (1995) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000106930 · Cited by 145 · see citing works
Evening exposure to blue light stimulates the expression of the clock gene <i>PER2</i> in humans
Cajochen, C., Jud, C., Münch, M., Kobialka, S., Wirz‐Justice, A., & Albrecht, U. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04613.x · Cited by 144 · see citing works
Independent Circadian Oscillations ofPeriod1in Specific Brain AreasIn VivoandIn Vitro
Abraham, U., Prior, J. L., Granados‐Fuentes, D., Piwnica-Worms, D. R., & Herzog, E. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2225-05.2005 · Cited by 124 · see citing works
Steeves, T. D. L., King, D. P., Zhao, Y., Sangoram, A. M., Du, F., Bowcock, A. M., Moore, R. Y., & Takahashi, J. S. (1999) · Genomics · doi:10.1006/geno.1998.5675 · Cited by 123 · see citing works
Dementia severity and Lewy bodies affect circadian rhythms in Alzheimer disease
Harper, D. G., Stopa, E. G., McKee, A. C., Satlin, A., Fish, D., & Volicer, L. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2003.04.009 · Cited by 121 · see citing works
Clock Genes Display Rhythmic Expression in Human Hearts
Leibetseder, V. J., Humpeler, S., Svoboda, M., Schmid, D., Thalhammer, T., Zuckermann, A. O., Marktl, W., & Ekmekçioğlu, C. (2009) · Chronobiology International · doi:10.1080/07420520902924939 · Cited by 121 · see citing works
From circadian clock gene expression to pathologies
Lamont, E. W., James, F. O., Boivin, D. B., & Cermakian, N. (2007) · Sleep Medicine · doi:10.1016/j.sleep.2006.11.002 · Cited by 120 · see citing works
Self-citationOlfactory bulb neurons express functional, entrainable circadian rhythms
Granados‐Fuentes, D., Saxena, M. T., Prolo, L. M., Aton, S. J., & Herzog, E. D. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03117.x · Cited by 117 · see citing works
Atypical patterns of circadian clock gene expression in human peripheral blood mononuclear cells
Teboul, M., Barrat-Petit, M.-A., Li, X. M., Claustrat, B., Formento, J., Delaunay, F., Lévi, F., & Milano, G. A. (2005) · Journal of Molecular Medicine · doi:10.1007/s00109-005-0697-6 · Cited by 106 · see citing works
Diurnal and Seasonal Rhythms of Neuronal Activity in the Suprachiasmatic Nucleus of Humans
Hofman, M. A., & Swaab, D. F. (1993) · Journal of Biological Rhythms · doi:10.1177/074873049300800402 · Cited by 102 · see citing works
High stability of mRNAs postmortem and protocols for their assessment by RT-PCR
Yasojima, K., McGeer, E. G., & McGeer, P. L. (2001) · Brain Research Protocols · doi:10.1016/s1385-299x(01)00119-2 · Cited by 97 · see citing works
James, F. O., Boivin, D. B., Charbonneau, S., Bélanger, V., & Cermakian, N. (2007) · Chronobiology International · doi:10.1080/07420520701800736 · Cited by 90 · see citing works
Self-citationExpression profiles of 10 circadian clock genes in human peripheral blood mononuclear cells
Kusanagi, H., Hida, A., Satoh, K., Echizenya, M., Shimizu, T., Pendergast, J. S., Yamazaki, S., & Mishima, K. (2008) · Neuroscience Research · doi:10.1016/j.neures.2008.01.012 · Cited by 89 · see citing works
Takimoto, M., Hamada, A., Tomoda, A., Ohdo, S., Ohmura, T., Sakato, H., Kawatani, J., Jodoi, T., Nakagawa, H., Terazono, H., et al. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00126.2005 · Cited by 78 · see citing works
Human Intestinal Circadian Clock: Expression of Clock Genes in Colonocytes Lining the Crypt
Pardini, L., Kaeffer, B., Trubuil, A., Bourreille, A., & Galmiche, J. ‐. (2005) · Chronobiology International · doi:10.1080/07420520500395011 · Cited by 59 · see citing works
Nishide, S., Honma, S., Nakajima, Y., Ikeda, M., Baba, K., Ohmiya, Y., & Honma, K. (2006) · Genes to Cells · doi:10.1111/j.1365-2443.2006.01015.x · Cited by 58 · see citing works
Abe, H., Honma, S., Namihira, M., Masubuchi, S., & Honma, K.-I. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01732.x · Cited by 58 · see citing works
Vosko, A. M., Hagenauer, M. H., Hummer, D. L., & Lee, T. M. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90392.2008 · Cited by 45 · see citing works
Luboshitzky, R., Shen‐Orr, Z., Tzischichinsky, O., Maldonado, M., Herer, P., & Lavie, P. (2001) · Chronobiology International · doi:10.1081/cbi-100103973 · Cited by 40 · see citing works
Ramanathan, C., Stowie, A. C., Smale, L., & Nunez, A. A. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.07.053 · Cited by 36 · see citing works
Expression profiles of PERIOD1, 2, and 3 in peripheral blood mononuclear cells from older subjects
Hida, A., Kusanagi, H., Satoh, K., Kato, T., Matsumoto, Y., Echizenya, M., Shimizu, T., Higuchi, S., & Mishima, K. (2008) · Life Sciences · doi:10.1016/j.lfs.2008.10.012 · Cited by 30 · see citing works
Day–night expression patterns of clock genes in the human pineal gland
Ackermann, K., Dehghani, F., Bux, R., Kauert, G. F., & Stehle, J. H. (2007) · Journal of Pineal Research · doi:10.1111/j.1600-079x.2007.00461.x · Cited by 26 · see citing works
Wu, Yh, Fischer, Df, Kalsbcck, Garidou-Boof, van, der, Vliet, Heijningen, et al. (2006) · 中国生物学文摘 · Cited by 12 · see citing works
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Leng, Y., Musiek, E. S., Hu, K., Cappuccio, F. P., & Yaffe, K. S. (2019) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30461-7 · Cited by 660 · see citing works
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Fishbein, A. B., Knutson, K. L., & Zee, P. C. (2021) · Journal of Clinical Investigation · doi:10.1172/jci148286 · Cited by 468 · see citing works
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Videnović, A., Lázár, A. S., Barker, R. A., & Overeem, S. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.206 · Cited by 373 · see citing works
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Wright, K. P., Lowry, C. A., & LeBourgeois, M. K. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00050 · Cited by 209 · see citing works
Schroeder, A., & Colwell, C. S. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.09.002 · Cited by 190 · see citing works
GROUP investigators, Børglum, A. D., Demontis, D., Grove, J., Pallesen, J., Hollegaard, M. V., Pedersen, C. B., Hedemand, A., Mattheisen, M., Uitterlinden, A., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.2 · Cited by 186 · see citing works
The trouble with circadian clock dysfunction: Multiple deleterious effects on the brain and body
Zelinski, E. L., Deibel, S. H., & McDonald, R. J. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.01.007 · Cited by 174 · see citing works
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Holth, J. K., Patel, T. K., & Holtzman, D. M. (2016) · Neurobiology of Sleep and Circadian Rhythms · doi:10.1016/j.nbscr.2016.08.002 · Cited by 165 · see citing works
Zhou, Y., Xu, J., Hou, Y., Leverenz, J. B., Kallianpur, A. R., Mehra, R., Liu, Y., Yu, H., Pieper, A. A., Jehi, L. E., et al. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00850-3 · Cited by 160 · see citing works
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Coogan, A. N., Schutová, B., Husung, S., Furczyk, K., Baune, B. T., Kropp, P. A., Häßler, F., & Thome, J. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.11.021 · Cited by 158 · see citing works
Ramkisoensing, A., & Meijer, J. H. (2015) · Frontiers in Neurology · doi:10.3389/fneur.2015.00128 · Cited by 152 · see citing works
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Cuesta, M., Cermakian, N., & Boivin, D. B. (2014) · The FASEB Journal · doi:10.1096/fj.14-265686 · Cited by 125 · see citing works
Self-citationGuarnieri, B., & Sorbi, S. (2015) · European Neurology · doi:10.1159/000434629 · Cited by 122 · see citing works
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Glucocorticoid-mediated Period2 induction delays the phase of circadian rhythm
Cheon, S., Park, N., Cho, S., & Kim, K. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt307 · Cited by 119 · see citing works
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Circadian clocks and neurodegenerative diseases: time to aggregate?
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Diurnal rhythms in gene expression in the prefrontal cortex in schizophrenia
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Lecarpentier, Y., CLAES, V. A., Duthoit, G., & Hébert, J. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00429 · Cited by 99 · see citing works
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Duffy, J. F., Abbott, S. M., Burgess, H. J., Crowley, S. J., Emens, J. S., Epstein, L. J., Gamble, K. L., Hasler, B. P., Kristo, D. A., Malkani, R. G., et al. (2021) · SLEEP · doi:10.1093/sleep/zsaa281 · Cited by 98 · see citing works
Rogers-Soeder, T. S., BLACKWELL, T. L., Yaffe, K. S., Ancoli‐Israel, S., Redline, S. S., Cauley, J. A., Ensrud, K. E., Paudel, M. L., Barrett-Connor, E. L., LeBlanc, E. S., et al. (2018) · Journal of the American Geriatrics Society · doi:10.1111/jgs.15555 · Cited by 93 · see citing works
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Krishnan, H. C., & Lyons, L. C. (2015) · Learning & Memory · doi:10.1101/lm.038877.115 · Cited by 91 · see citing works
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Weissová, K., Bartoš, A., Sládek, M., Nováková, M., & Sumová, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0146200 · Cited by 79 · see citing works
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Bellanti, F., Iannelli, G., Blonda, M., Tamborra, R., Villani, R., Romano, A., Calcagnini, S., Mazzoccoli, G., Vinciguerra, M., Gaetani, S., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-160942 · Cited by 70 · see citing works
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Ni, J., Wu, Z., Meng, J., Saito, T., Saido, T. C., Qing, H., & Nakanishi, H. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1562-9 · Cited by 65 · see citing works
Sleep and hippocampal neurogenesis: Implications for Alzheimer’s disease
Kent, B. A., & Mistlberger, R. E. (2017) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2017.02.004 · Cited by 64 · see citing works
Fan, R., Peng, X., Xie, L., Dong, K., Ma, D., Xu, W., Shi, X., Zhang, S., Chen, J., Yu, X., et al. (2022) · Aging Cell · doi:10.1111/acel.13704 · Cited by 62 · see citing works
Neurobiological Functions of the Period Circadian Clock 2 Gene, Per2
Kim, M., de la Peña, J. B., Cheong, J. H., & Kim, H. J. (2017) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2017.131 · Cited by 62 · see citing works
Sleep and circadian rhythm disruption and stress intersect in Alzheimer's disease
Phan, T., & Malkani, R. G. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.10.001 · Cited by 64 · see citing works
Neural function of Bmal1: an overview
Zheng, Y., Pan, L., Wang, F., Yan, J., Wang, T., Xia, Y., Yao, L., Deng, K., Zheng, Y., Xia, X., et al. (2023) · Cell & Bioscience · doi:10.1186/s13578-022-00947-8 · Cited by 60 · see citing works
The circadian clock circuitry and the AHR signaling pathway in physiology and pathology
Anderson, G., Beischlag, T. V., Vinciguerra, M., & Mazzoccoli, G. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.02.022 · Cited by 61 · see citing works
Central and peripheral circadian clocks and their role in Alzheimer's disease
Chauhan, R., Chen, K.-F., Kent, B. A., & Crowther, D. C. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.030627 · Cited by 58 · see citing works
“Their conclusion was that the central, and indeed the secondary, brain clocks were rhythmic in healthy individuals and in those with AD, but in the latter there were marked phase shifts, indicating changes in their relative synchronization (Cermakian et al., 2011).”
BackgroundImpact of Shift Work on the Circadian Timing System and Health in Women
Kervezee, L., Shechter, A., & Boivin, D. B. (2018) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2018.04.003 · Cited by 57 · see citing works
Self-citationInteracting influences of aging and Alzheimer's disease on circadian rhythms
Duncan, M. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14358 · Cited by 55 · see citing works
Kim, E., Nohara, K., Wirianto, M., Escobedo, G., Lim, J. Y., Morales, R., Yoo, S.-H., & Chen, Z. (2021) · Biomolecules · doi:10.3390/biom11071004 · Cited by 51 · see citing works
Major depressive disorder: A loss of circadian synchrony?
Edgar, N. M., & McClung, C. A. (2013) · BioEssays · doi:10.1002/bies.201300086 · Cited by 52 · see citing works
Petrásek, T., Vojtěchová, I., Lobellová, V., Popelíková, A., Janikova, M., Brožka, H., Houdek, P., Sládek, M., Sumová, A., Krištofiková, Z., et al. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00250 · Cited by 51 · see citing works
Sleep Disturbances in MCI and AD: Neuroinflammation as a Possible Mediating Pathway
Pak, V. M., Onen, S. ‐., Bliwise, D. L., Kutner, N. G., Russell, K. L., & Onen, F. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00069 · Cited by 48 · see citing works
Mammalian circadian networks mediated by the suprachiasmatic nucleus
Lu, Q., & Kim, J. Y. (2021) · FEBS Journal · doi:10.1111/febs.16233 · Cited by 50 · see citing works
Means, J. C., Venkatesan, A., Gerdes, B. C., Fan, J.-Y., Bjes, E. S., & Price, J. L. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005171 · Cited by 48 · see citing works
CLOCK Genes and Circadian Rhythmicity in Alzheimer Disease
Thome, J., Coogan, A. N., Woods, A. G., Darie, C. C., & Häßler, F. (2011) · Journal of Aging Research · doi:10.4061/2011/383091 · Cited by 47 · see citing works
Disruption of central and peripheral circadian clocks in police officers working at night
Koshy, A., Cuesta, M., Boudreau, P., Cermakian, N., & Boivin, D. B. (2019) · The FASEB Journal · doi:10.1096/fj.201801889r · Cited by 46 · see citing works
Self-citationKinoshita, C., Okamoto, Y., Aoyama, K., & Nakaki, T. (2020) · Clocks & Sleep · doi:10.3390/clockssleep2030022 · Cited by 48 · see citing works
Astara, K., Tsimpolis, A., Kalafatakis, K., Vavougios, G. D., Xiromerisiou, G., Dardiotis, E., Christodoulou, G. N., Samara, M. T., & Lappas, A. S. (2023) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2023.111899 · Cited by 47 · see citing works
Wirianto, M., Wang, C., Kim, E., Koike, N., Gomez‐Gutierrez, R., Nohara, K., Escobedo, G., Choi, J. M., Han, C., Yagita, K., et al. (2022) · The FASEB Journal · doi:10.1096/fj.202101633r · Cited by 45 · see citing works
Skin Temperature Rhythms in Humans Respond to Changes in the Timing of Sleep and Light
Cuesta, M., Boudreau, P., Cermakian, N., & Boivin, D. B. (2017) · Journal of Biological Rhythms · doi:10.1177/0748730417702974 · Cited by 44 · see citing works
Self-citationTherapeutic Targeting of Casein Kinase 1δ/ε in an Alzheimer’s Disease Mouse Model
Adler, P., Mayne, J., Walker, K., Ning, Z., & Figeys, D. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00312 · Cited by 43 · see citing works
Amidfar, M., Garcez, M. L., & Kim, Y. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110721 · Cited by 43 · see citing works
Anderson, G., & Maes, M. H. J. (2017) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527315666161122144659 · Cited by 41 · see citing works
Deibel, S. H., Zelinski, E. L., Keeley, R. J., Kovalchuk, O., & McDonald, R. J. (2015) · Oncotarget · doi:10.18632/oncotarget.4036 · Cited by 39 · see citing works
Irregular Sleep-Wake Rhythm Disorder
Abbott, S. M., & Zee, P. C. (2015) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2015.08.005 · Cited by 40 · see citing works
Relationships between the Circadian System and Alzheimer's Disease-Like Symptoms in Drosophila
Long, D. M., Blake, M. R., Dutta, S., Holbrook, S. D., Kotwica‐Rolinska, J., Kretzschmar, D., & Giebultowicz, J. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0106068 · Cited by 39 · see citing works
Circadian Rhythms in AD Pathogenesis: a Critical Appraisal
Musiek, E. S. (2017) · Current Sleep Medicine Reports · doi:10.1007/s40675-017-0072-5 · Cited by 37 · see citing works
Circadian Rhythm Disruption and Alzheimer's Disease: The Dynamics of a Vicious Cycle
Sharma, A., Sethi, G., Tambuwala, M. M., Aljabali, A. A. A., Chellappan, D. K., Dua, K., & Goyal, R. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200429013041 · Cited by 49 · see citing works
Xue, X., Zong, W., Glausier, J. R., Kim, S.-M., Shelton, M. A., Phan, B. N., Srinivasan, C., Pfenning, A. R., Tseng, G. C., Lewis, D. A., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01894-1 · Cited by 37 · see citing works
Influence of the extracellular matrix on cell-intrinsic circadian clocks
Streuli, C. H., & Meng, Q. (2019) · Journal of Cell Science · doi:10.1242/jcs.207498 · Cited by 36 · see citing works
Fifel, K., & Videnović, A. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105029 · Cited by 35 · see citing works
Integrating Sleep and Alzheimer’s Disease Pathophysiology: Hints for Sleep Disorders Management
Proserpio, P., Arnaldi, D., Nobili, F. M., & Nobili, L. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-180041 · Cited by 34 · see citing works
Yang, Y.-K., Peng, X.-D., Li, Y., Wang, Z., Changquan, H., Hui, W., & Liu, Q. (2013) · Journal of Investigative Medicine · doi:10.2310/jim.0b013e31829f91c0 · Cited by 33 · see citing works
Kent, B. A., Michalik, M. J., Marchant, E. G., Yau, K. W., Feldman, H., Mistlberger, R. E., & Nygaard, H. B. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2019.01.010 · Cited by 33 · see citing works
Huang, S., Choi, M. H., Huang, H., Wang, X., Chang, Y. C., & Kim, J. Y. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108394 · Cited by 32 · see citing works
Sex Differences in Molecular Rhythms in the Human Cortex
Logan, R. W., Xue, X., Ketchesin, K. D., Hoffman, G. E., Roussos, P., Tseng, G. C., McClung, C. A., & Seney, M. L. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.03.005 · Cited by 30 · see citing works
Neuronal Hyperexcitability in APPSWE/PS1dE9 Mouse Models of Alzheimer’s Disease
Müller, L., Kirschstein, T., Köhling, R., Kuhla, A., & Teipel, S. J. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201540 · Cited by 27 · see citing works
Deciphering clock genes as emerging targets against aging
Zhu, Y., Liu, Y., Escames, G., Yang, Z. Z., Zhao, H., Lu, Q., Xue, C., Xu, D., Acuña-Castroviejo, D., & Yang, Y. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101725 · Cited by 31 · see citing works
Circadian Rhythm Disruption and Alzheimers Disease: The Dynamics of a Vicious Cycle
Sharma, A. (2021) · Current Neuropharmacology · doi:10.2174/18756190mta21mjaf3 · Cited by 29 · see citing works
A Dichotomous Role for FABP7 in Sleep and Alzheimer’s Disease Pathogenesis: A Hypothesis
Needham, H., Torpey, G., Flores, C. C., Davis, C. J., Vanderheyden, W. M., & Gerstner, J. R. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.798994 · Cited by 28 · see citing works
Trujillo-Rangel, W. Á., Acuña-Vaca, S., Padilla-Ponce, D. J., García-Mercado, F. G., Torres-Mendoza, B. M., Pacheco-Moisés, F. P., Escoto-Delgadillo, M., García‐Benavides, L., & Delgado-Lara, D. L. C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084401 · Cited by 27 · see citing works
Epigenetic Regulation of BMAL1 with Sleep Disturbances and Alzheimer’s Disease
Hulme, B., Didikoğlu, A., Bradburn, S., Robinson, A., Canal, M. M., Payton, A., Pendleton, N., & Murgatroyd, C. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200634 · Cited by 25 · see citing works
Synchronizing an aging brain: can entraining circadian clocks by food slow Alzheimer’s disease?
Kent, B. A. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00234 · Cited by 23 · see citing works
Barragán, S., Fernández, M. A., Rueda, C., & Peddada, S. D. (2013) · Journal of Statistical Software · doi:10.18637/jss.v054.i04 · Cited by 22 · see citing works
Commins, S., & Kirby, B. P. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104363 · Cited by 22 · see citing works
Transcription Factor Interactions in Genomic Nuclear Receptor Function
George, C. L., Lightman, S. L., & Biddie, S. C. (2011) · Epigenomics · doi:10.2217/epi.11.66 · Cited by 21 · see citing works
Rest-activity rhythms in small scale homelike care and traditional care for residents with dementia
Kok, J. S., Berg, I. J., Blankevoort, G., & Scherder, E. (2017) · BMC Geriatrics · doi:10.1186/s12877-017-0525-1 · Cited by 21 · see citing works
Urban, M. W., Lo, C.-Y., Bodinayake, K. K., Brunswick, C. A., Murakami, S., Heimann, A. C., & Kwapis, J. L. (2021) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2021.107535 · Cited by 20 · see citing works
Impact of circadian clock dysfunction on human health
Samanta, S., & Ali, S. A. (2022) · Exploration of neuroscience · doi:10.37349/en.2022.00002 · Cited by 20 · see citing works
Son, G., Neylan, T. C., & Grinberg, L. T. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-023-00695-4 · Cited by 21 · see citing works
LeVault, K. R., Tischkau, S. A., & Brewer, G. J. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150026 · Cited by 20 · see citing works
How Does Chronobiology Contribute to the Development of Diseases in Later Life
Stowe, T. A., & McClung, C. A. (2023) · Clinical Interventions in Aging · doi:10.2147/cia.s380436 · Cited by 18 · see citing works
Ibrahim, A., Högl, B., & Stefani, A. (2024) · Clinical and Translational Neuroscience · doi:10.3390/ctn8010011 · Cited by 19 · see citing works
Resetting the Aging Clock: Implications for Managing Age-Related Diseases
Nobrega, A. K. D., Luz, K. V., & Lyons, L. C. (2020) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-42667-5_9 · Cited by 18 · see citing works
Sleep as the Foundation of Brain Health
Ibrahim, A., Högl, B., & Stefani, A. (2025) · Seminars in Neurology · doi:10.1055/a-2566-4073 · Cited by 20 · see citing works
Bessi, V., Giacomucci, G., Mazzeo, S., Bagnoli, S., Padiglioni, S., Balestrini, J., Tomaiuolo, G., Piaceri, I., Carraro, M., Bracco, L., et al. (2020) · European Journal of Neurology · doi:10.1111/ene.14518 · Cited by 16 · see citing works
Can chronopharmacology improve the therapeutic management of neurological diseases?
Sion, B., & Bégou, M. (2021) · Fundamental and Clinical Pharmacology · doi:10.1111/fcp.12659 · Cited by 17 · see citing works
Shukla, M., & Vincent, B. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230314142505 · Cited by 15 · see citing works
- Authors
- Cermakian, N., Waddington Lamont, E., Boudreau, P., & Boivin, D. B.
- Affiliations
- Douglas Mental Health University Institute (CA)
- Laboratory of Molecular Chronobiology, Douglas Mental Health University Institute, Montréal (QC), Canada, Centre for Study and Treatment of Circadian Rhythms, Douglas Mental Health University Institute, Montréal (QC), Canada, Department of Psychiatry and Department of Neurology and Neurosurgery, McGill University, Montréal (QC), Canada, Department of Neuroscience, Carleton University, Ottawa (ON), Canada.
- Venue
- Journal of Biological Rhythms
- Publisher
- SAGE Publications
- Published
- 2011-03-30
- Volume
- 26
- Issue
- 2
- Pages
- 160-170
- ISSN
- 0748-7304 (ISSN-L)
- 1552-4531
- OpenAlex
- W2057817679
- Cited by
- 175
- References
- 50
- Citations by year
- 2026: 4 · 2025: 16 · 2024: 14 · 2023: 12 · 2022: 13 · 2021: 23 · 2020: 13 · 2019: 10 · 2018: 9 · 2017: 17 · 2016: 7 · 2015: 10 · 2014: 9 · 2013: 13 · 2012: 3
- FWCI
- 4.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Biological Rhythms (publishedVersion)
- PubMed (publishedVersion)
- Funders
- McGill University
- Faculty of Medicine, McGill University
- Institut de Recherche Robert-Sauvé en Santé et en Sécurité du Travail
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- clock genes, Alzheimer's disease, circadian clock, bed nucleus of the stria terminalis, cingulate cortex, pineal gland, Per1, Per2, Bmal1, brain aging
- MeSH terms
- Aged, Alzheimer Disease, Circadian Rhythm, Female, Gyrus Cinguli, Humans, Male, Pineal Gland, Septal Nuclei, Gene Expression, ARNTL Transcription Factors, Period Circadian Proteins, Circadian Clocks
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