Real-time luminescence reporting of circadian gene expression in mammals
Open accessAbstract
Luminescence reporters have been used successfully in studies of circadian rhythms. Real-time measurements of circadian variations in gene expression were made in living cells, cultured tissues, and whole organisms. Because this technique is relatively easy and continuous noninvasive measurement from tissue cultures allows for a drastic reduction in the number of experimental animals, we believe this method will become a common technique for studying circadian rhythms. Using a multichannel recording apparatus, it may also become a powerful tool for the discovery of new drugs. In the past, measurements were done using hand-made apparatuses or by modifying commercially available equipment. We, along with other investigators, have developed user-friendly equipment for performing circadian rhythms experiments, and these systems are now available commercially. This article describes the use of luminescence reporters in circadian research and provides detailed methods used in these experiments. One of our goals in this article is to reduce experimental variability in different laboratories by proposing standard protocols.
Integrity signals
Registry
Cites
Statistics
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?
The suprachiasmatic nucleus is an autonomous oscillator and cycles even in vitro almost indefinitely.
“The SCN is an autonomous oscillator and cycles even in vitro almost indefinitely (26).”
From Role of the circadian system in cardiovascular disease (2018) · cites this paper as [26]
Cites
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
Self-citationResetting central and peripheral circadian oscillators in transgenic rats
Yamazaki, S., Numano, R., Abe, M., Hida, A., Takahashi, R.-I., Ueda, M., Block, G. D., Sakaki, Y., Menaker, M., & Tei, H. (2000) · Science · doi:10.1126/science.288.5466.682 · Cited by 1,907 · see citing works
Self-citationEntrainment of the circadian clock in the liver by feeding
Stokkan, K.-A., Yamazaki, S., Tei, H., Sakaki, Y., & Menaker, M. (2001) · Science · doi:10.1126/science.291.5503.490 · Cited by 1,800 · see citing works
Self-citationSynchronization of Cellular Clocks in the Suprachiasmatic Nucleus
Yamaguchi, S., Isejima, H., Matsuo, T., Okura, R., Yagita, K., Kobayashi, M., & Okamura, H. (2003) · Science · doi:10.1126/science.1089287 · Cited by 934 · see citing works
Differential Functions of mPer1, mPer2, and mPer3 in the SCN Circadian Clock
Bae, K., Jin, X., Maywood, E. S., Hastings, M. H., Reppert, S. M., & Weaver, D. R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00302-6 · Cited by 900 · see citing works
A transcription factor response element for gene expression during circadian night
Ueda, H. R., Chen, W., Adachi, A. A., Wakamatsu, H., Hayashi, S., Takasugi, T., Nagano, M., Nakahama, K., Suzuki, Y., Sugano, S., et al. (2002) · Nature · doi:10.1038/nature00906 · Cited by 850 · see citing works
The mPer2 gene encodes a functional component of the mammalian circadian clock
Zheng, B., Larkin, D. W., Albrecht, U., Sun, Z. S., Sage, M., Eichele, G., Lee, C. C., & Bradley, A. (1999) · Nature · doi:10.1038/22118 · Cited by 718 · see citing works
Kondo, T., Strayer, C. A., Kulkarni, R. D., Taylor, W., Ishiura, M., Golden, S. S., & Johnson, C. H. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.12.5672 · Cited by 495 · see citing works
Multiple signaling pathways elicit circadian gene expression in cultured Rat-1 fibroblasts
Balsalobre, A., Marcacci, L., & Schibler, U. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00758-2 · Cited by 485 · see citing works
A Novel Circadian Phenotype Based on Firefly Luciferase Expression in Transgenic Plants
Millar, A. J., Short, S. R., Chua, N., & Kay, S. A. (1992) · The Plant Cell · doi:10.1105/tpc.4.9.1075 · Cited by 391 · see citing works
Effects of aging on central and peripheral mammalian clocks
Yamazaki, S., Straume, M., Tei, H., Sakaki, Y., Menaker, M., & Block, G. D. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152318499 · Cited by 317 · see citing works
Self-citationZheng (1999) · doi:10.1038/22659 · Cited by 293 · see citing works
Temporal Precision in the Mammalian Circadian System: A Reliable Clock from Less Reliable Neurons
Herzog, E. D., Aton, S. J., Numano, R., Sakaki, Y., & Tei, H. (2004) · Journal of Biological Rhythms · doi:10.1177/0748730403260776 · Cited by 281 · see citing works
Novel Features of Drosophila period Transcription Revealed by Real-Time Luciferase Reporting
Brandes, C., Plautz, J. D., Stanewsky, R., et al. (1996) · Neuron · doi:10.1016/s0896-6273(00)80088-4 · Cited by 175 · see citing works
Izumo, M., Johnson, C. H., & Yamazaki, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2536313100 · Cited by 161 · see citing works
Self-citationMultiple circadian‐regulated elements contribute to cycling period gene expression in Drosophila
Stanewsky, R., Jamison, C. F., Plautz, J. D., et al. (1997) · The EMBO Journal · doi:10.1093/emboj/16.16.5006 · Cited by 155 · see citing works
E-box function in a period gene repressed by light
Vallone, D., Gondi, S. B., Whitmore, D., & Foulkes, N. S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305436101 · Cited by 149 · see citing works
Photic and circadian expression of luciferase in mPeriod1 - luc transgenic mice in vivo
Wilsbacher, L. D., Yamazaki, S., Herzog, E. D., Song, E.-J., Radcliffe, L. A., Abe, M., Block, G. D., Spitznagel, E. L., Menaker, M., & Takahashi, J. S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012248599 · Cited by 138 · see citing works
Self-citationView of a mouse clock gene ticking
Yamaguchi, S., Kobayashi, M., Mitsui, S., Ishida, Y., van der Horst, G. T. J., Suzuki, M., Shibata, S., & Okamura, H. (2001) · Nature · doi:10.1038/35055628 · Cited by 113 · see citing works
Welsh, D. K., Imaizumi, T., & Kay, S. A. (2005) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(05)93011-5 · Cited by 93 · see citing works
Tsuchiya, Y., Akashi, M., & Nishida, E. (2003) · Genes to Cells · doi:10.1046/j.1365-2443.2003.00669.x · Cited by 88 · see citing works
Visualization of mPer1 transcription in vitro
Asai, M., Yamaguchi, S., Isejima, H., Jonouchi, M., Moriya, T., Shibata, S., Kobayashi, M., & Okamura, H. (2001) · Current Biology · doi:10.1016/s0960-9822(01)00445-6 · Cited by 68 · see citing works
Circadian and light-induced expression of luciferase in Neurospora crassa
Morgan, L. W., Greene, A. V., & Bell‐Pedersen, D. (2003) · Fungal Genetics and Biology · doi:10.1016/s1087-1845(02)00562-5 · Cited by 65 · see citing works
Geusz, M. E., Fletcher, C., Block, G. D., Straume, M., Copeland, N. G., Jenkins, N. A., Kay, S. A., & Day, R. N. (1997) · Current Biology · doi:10.1016/s0960-9822(06)00334-4 · Cited by 48 · see citing works
Monitoring immediate-early gene expression through firefly luciferase imaging of HRS/J hairless mice
Collaco, A. M., & Geusz, M. E. (2003) · BMC Physiology · doi:10.1186/1472-6793-3-8 · Cited by 33 · see citing works
Oscillation of Human Period 1 (hPER1) Reporter Gene Activity in Human Neuroblastoma Cells In Vivo
Maronde, E., & Motzkus, D. (2003) · Chronobiology International · doi:10.1081/cbi-120022413 · Cited by 19 · see citing works
Bioluminescence Imaging of Gene Expression in Living Cells and Tissues
Geusz, M. E. (2001) · Springer eBooks · doi:10.1007/978-1-4614-7513-2_23 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Role of the circadian system in cardiovascular disease
Thosar, S. S., Butler, M. P., & Shea, S. A. (2018) · Journal of Clinical Investigation · doi:10.1172/jci80590 · Cited by 443 · see citing works
Scheduled exercise phase shifts the circadian clock in skeletal muscle
WOLFF, G., & ESSER, K. A. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318255cf4c · Cited by 291 · see citing works
Um, J. H., Yang, S., Yamazaki, S., Kang, H., Viollet, B., Foretz, M., & Chung, J. H. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.c700070200 · Cited by 244 · see citing works
Self-citationCircadian Rhythms, the Molecular Clock, and Skeletal Muscle
Harfmann, B. D., Schroder, E. A., & Esser, K. A. (2015) · Journal of Biological Rhythms · doi:10.1177/0748730414561638 · Cited by 211 · see citing works
High-fat diet acutely affects circadian organisation and eating behavior
Pendergast, J. S., Branecky, K. L., Yang, W., Ellacott, K. L. J., Niswender, K. D., & Yamazaki, S. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12133 · Cited by 198 · see citing works
Self-citationSelective Inhibition of Casein Kinase 1ϵ Minimally Alters Circadian Clock Period
Walton, K. M., Fisher, K., Rubitski, D., Marconi, M., Meng, Q.-J., Sládek, M., Adams, J., Bass, M., Chandrasekaran, R., Butler, T., et al. (2009) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.109.151415 · Cited by 184 · see citing works
Visualizing jet lag in the mouse suprachiasmatic nucleus and peripheral circadian timing system
Davidson, A. J., Castanon‐Cervantes, O., Leise, T. L., Molyneux, P. C., & Harrington, M. E. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06534.x · Cited by 171 · see citing works
The cardiomyocyte molecular clock, regulation of <i>Scn5a</i> , and arrhythmia susceptibility
Schroder, E. A., Lefta, M., Zhang, X., Bartos, D. C., Feng, H.-Z., Zhao, Y., Patwardhan, A., Jin, J.-P., Esser, K. A., & Delisle, B. P. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00383.2012 · Cited by 147 · see citing works
Intrinsic muscle clock is necessary for musculoskeletal health
Schroder, E. A., Harfmann, B. D., Zhang, X., Srikuea, R., England, J. H., Hodge, B. A., Wen, Y., Riley, L. A., Yu, Q., Christie, A., et al. (2015) · The Journal of Physiology · doi:10.1113/jp271436 · Cited by 145 · see citing works
McCarthy, M. J., Wei, H., Marnoy, Z., Darvish, R. M., McPhie, D. L., Cohen, B. M., & Welsh, D. K. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.90 · Cited by 137 · see citing works
Baeza-Raja, B., Eckel-Mahan, K., Zhang, L., Vagena, E., Tsigelny, I. F., Sassone-Corsi, P., Ptacek, L. J., & Akassoglou, K. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2757-12.2013 · Cited by 44 · see citing works
McCarthy, M. J., Fernandes, M., Kranzler, H. R., Covault, J. M., & Welsh, D. K. (2013) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.12106 · Cited by 32 · see citing works
Ota, S. M., Hut, R. A., Riede, S. J., Crosby, P., Suchecki, D., & Meerlo, P. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104683 · Cited by 27 · see citing works
- Authors
- Yamazaki, S., & Takahashi, J. S.
- Affiliations
- Vanderbilt University (US)
- Northwestern University (US)
- Venue
- Methods in Enzymology
- Publisher
- Elsevier
- Published
- 2005
- Volume
- 393
- Pages
- 288-301
- ISSN
- 0076-6879 (ISSN-L)
- PMC
- PMC3793321
- OpenAlex
- W1482377585
- Cited by
- 200
- References
- 27
- Citations by year
- 2026: 12 · 2025: 9 · 2024: 6 · 2023: 6 · 2022: 9 · 2021: 11 · 2020: 13 · 2019: 10 · 2018: 11 · 2017: 8 · 2016: 9 · 2015: 9 · 2014: 8 · 2013: 19 · 2012: 12
- FWCI
- 3.93
- Type
- book chapter
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Methods in enzymology on CD-ROM/Methods in enzymology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › bioluminescence and chemiluminescence research
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Keywords
- circadian rhythm, circadian gene expression, real-time monitoring, non-invasive measurement, drug discovery, standardization of protocols, animal use reduction
- MeSH terms
- Animals, Circadian Rhythm, Luciferases, Luminescent Measurements, Mice, Transgenic, Gene Expression, Animals, Genetically Modified, Tissue Culture Techniques, Mice, Rats
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
