The DOI matches its Crossref record; 50 of the 50 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Citations
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
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
Shao, J., & Tu, D. (1995) · Springer Series in Statistics · doi:10.1007/978-1-4612-0795-5 · Cited by 1,985
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
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
Guilding, C., & Piggins, H. D. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05581.x · Cited by 356
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
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
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
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
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
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
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
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
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
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
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
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 219
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 208
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
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
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
Amir, S., Lamont, E. W., Robinson, B., & Stewart, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4488-03.2004 · Cited by 179
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
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 176
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 173
Archer, S. N., Viola, A., Kyriakopoulou, V., von Schantz, M., & Dijk, D. (2008) · SLEEP · doi:10.1093/sleep/31.5.608 · Cited by 156
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
Evening exposure to blue light stimulates the expression of the clock gene PER2 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
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 124
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
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 123
Self-citationDementia 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
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
Olfactory 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
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 108
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
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
James, F. O., Boivin, D. B., Charbonneau, S., Bélanger, V., & Cermakian, N. (2007) · Chronobiology International · doi:10.1080/07420520701800736 · Cited by 90
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
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 76
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
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
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
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
Luboshitzky, R., Shen‐Orr, Z., Tzischichinsky, O., Maldonado, M., Herer, P., & Lavie, P. (2001) · Chronobiology International · doi:10.1081/cbi-100103973 · Cited by 40
Ramanathan, C., Stowie, A. C., Smale, L., & Nunez, A. A. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.07.053 · Cited by 36
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
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
Wu, Yh, Fischer, Df, Kalsbcck, Garidou-Boof, van, der, Vliet, Heijningen, et al. (2006) · 中国生物学文摘 · Cited by 12
Research works printed but not linked: 2
- Bianchetti A., 1995, Dementia, 6, 108
- 10.1097/00019442-200505000-00004 · DOI
Cited by
Sorted by citations
Mechanisms linking circadian clocks, sleep, and neurodegeneration
Musiek, E. S., & Holtzman, D. M. (2016) · Science · doi:10.1126/science.aah4968 · Cited by 878
Connections between sleep and cognition in older adults
Yaffe, K., Falvey, C. M., & Hoang, T. (2014) · The Lancet Neurology · doi:10.1016/s1474-4422(14)70172-3 · Cited by 796
Rhythms of life: circadian disruption and brain disorders across the lifespan
Logan, R. W., & McClung, C. A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0088-y · Cited by 713
Association between circadian rhythms and neurodegenerative diseases
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 677
Circadian patterns of gene expression in the human brain and disruption in major depressive disorder
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) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305814110 · Cited by 589
Metadata
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review