Spatiotemporal single-cell analysis of gene expression in the mouse suprachiasmatic nucleus
Abstract
Mammalian circadian behaviors are orchestrated by the suprachiasmatic nucleus (SCN) in the ventral hypothalamus, but the number of SCN cell types and their functional roles remain unclear. We have used single-cell RNA-sequencing to identify the basic cell types in the mouse SCN and to characterize their circadian and light-induced gene expression patterns. We identified eight major cell types, with each type displaying a specific pattern of circadian gene expression. Five SCN neuronal subtypes, each with specific combinations of markers, differ in their spatial distribution, circadian rhythmicity and light responsiveness. Through a complete three-dimensional reconstruction of the mouse SCN at single-cell resolution, we obtained a standardized SCN atlas containing the spatial distribution of these subtypes and gene expression. Furthermore, we observed heterogeneous circadian gene expression between SCN neuron subtypes. Such a spatiotemporal pattern of gene regulation within the SCN may have an important function in the circadian pacemaker.
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 094 SCH Six6 Cdc14a Gaba subclass pacemaker cells are at a different phase of the circadian cycle of gene expression from the rest of the brain.
“suggesting that the pacemaker cells are at a different phase of the circadian cycle of gene expression from the rest of the brain, consistent with previous findings117”
From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [117]
Cites
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
UCSF Chimera—A visualization system for exploratory research and analysis
Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004) · Journal of Computational Chemistry · doi:10.1002/jcc.20084 · Cited by 45,260 · see citing works
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890 · see citing works
Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn923 · Cited by 14,108 · see citing works
Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N. J., Livak, K. J., Mikkelsen, T. S., & Rinn, J. L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2859 · Cited by 7,314 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Spatial reconstruction of single-cell gene expression data
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F., & Regev, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3192 · Cited by 7,055 · see citing works
Scenic: single-cell regulatory network inference and clustering.
Aibar, S., González-Blas, C. B., Moerman, T., Huynh-Thu, V. A., Imrichova, H., Hulselmans, G., Rambow, F., Marine, J.-C., Geurts, P., Aerts, J., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4463 · Cited by 6,520 · see citing works
Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W.-H., Pagès, F., Trajanoski, Z., & Galon, J. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp101 · Cited by 6,280 · see citing works
Full-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137 · see citing works
Phototransduction by retinal ganglion cells that set the circadian clock
Berson, D. M., Dunn, F. A., & Takao, M. (2002) · Science · doi:10.1126/science.1067262 · Cited by 3,629 · see citing works
Hattar, S., Liao, H.-W., Takao, M., Berson, D. M., & Yau, K.-W. (2002) · Science · doi:10.1126/science.1069609 · Cited by 2,734 · see citing works
Transcriptional architecture of the mammalian circadian clock
Takahashi, J. S. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.150 · Cited by 2,639 · see citing works
GARCÍA-ALONSO, C. R., Pérez, L. M., & Fernández, J. C. F. (2011) · Annals of Operations Research · doi:10.1007/s10479-011-0841-3 · Cited by 1,357 · see citing works
Suprachiasmatic Nucleus: Cell Autonomy and Network Properties
Welsh, D. K., Takahashi, J. S., & Kay, S. A. (2010) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021909-135919 · Cited by 1,216 · see citing works
A smart local moving algorithm for large-scale modularity-based community detection
Waltman, L., & van Eck, N. J. (2013) · The European Physical Journal B · doi:10.1140/epjb/e2013-40829-0 · Cited by 1,088 · see citing works
Hughes, M. E., Hogenesch, J. B., & Kornacker, K. (2010) · Journal of Biological Rhythms · doi:10.1177/0748730410379711 · Cited by 1,087 · see citing works
Generation of circadian rhythms in the suprachiasmatic nucleus
Hastings, M. H., Maywood, E. S., & Brancaccio, M. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0026-z · Cited by 1,065 · see citing works
Synchronization 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
Advanced CLARITY for rapid and high-resolution imaging of intact tissues
Tomer, R., Ye, L., Hsueh, B., & Deisseroth, K. (2014) · Nature Protocols · doi:10.1038/nprot.2014.123 · Cited by 842 · see citing works
Abrahamson, E. E., & Moore, R. Y. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02890-6 · Cited by 788 · see citing works
Single-Cell RNA-Seq Reveals Hypothalamic Cell Diversity
Chen, R., Wu, X., Jiang, L., & Zhang, Y. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.004 · Cited by 592 · see citing works
MetaCycle: an integrated R package to evaluate periodicity in large scale data
Wu, G., Anafi, R. C., Hughes, M. E., Kornacker, K., & Hogenesch, J. B. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw405 · Cited by 560 · see citing works
Molecular interrogation of hypothalamic organization reveals distinct dopamine neuronal subtypes
Romanov, R. A., Zeisel, A., Bakker, J., Girach, F., Hellysaz, A., Tomer, R., Alpár, A., Mulder, J., Clotman, F., Keimpema, E., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4462 · Cited by 502 · see citing works
Spontaneous Synchronization of Coupled Circadian Oscillators
Gonze, D., Bernard, S., Waltermann, C., Kramer, A., & Herzel, H. (2005) · Biophysical Journal · doi:10.1529/biophysj.104.058388 · Cited by 465 · see citing works
Maywood, E. S., Reddy, A. B., Wong, G. K. Y., O'Neill, J. S., O'Brien, J. A., McMahon, D. G., Harmar, A. J., Okamura, H., & Hastings, M. H. (2006) · Current Biology · doi:10.1016/j.cub.2006.02.023 · Cited by 438 · see citing works
Astrocytes Control Circadian Timekeeping in the Suprachiasmatic Nucleus via Glutamatergic Signaling
Brancaccio, M., Patton, A. P., Chesham, J. E., Maywood, E. S., & Hastings, M. H. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.030 · Cited by 437 · see citing works
Transcriptional Architecture of Synaptic Communication Delineates GABAergic Neuron Identity
Paul, A., Crow, M., Raudales, R., He, M., Gillis, J., & Huang, Z. J. (2017) · Cell · doi:10.1016/j.cell.2017.08.032 · Cited by 421 · see citing works
Crow, M., Paul, A., Ballouz, S., Huang, Z. J., & Gillis, J. (2018) · Nature Communications · doi:10.1038/s41467-018-03282-0 · Cited by 365 · see citing works
Cell-autonomous clock of astrocytes drives circadian behavior in mammals
Brancaccio, M., Edwards, M. D., Patton, A. P., Smyllie, N. J., Chesham, J. E., Maywood, E. S., & Hastings, M. H. (2019) · Science · doi:10.1126/science.aat4104 · Cited by 331 · see citing works
Analysis of Gene Regulatory Networks in the Mammalian Circadian Rhythm
Yan, J., Wang, H., Liu, Y., & Shao, C. (2008) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000193 · Cited by 297 · see citing works
Self-citationneuTube 1.0: A New Design for Efficient Neuron Reconstruction Software Based on the SWC Format
Feng, L., Zhao, T., & Kim, J. (2015) · eNeuro · doi:10.1523/eneuro.0049-14.2014 · Cited by 292 · see citing works
Pinkus, G. S., & SAID, J. W. (1977) · PubMed · Cited by 288 · see citing works
Inagaki, N., Honma, S., Ono, D., Tanahashi, Y., & Honma, K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607713104 · Cited by 274 · see citing works
The suprachiasmatic nuclei contain a tetrodotoxin-resistant circadian pacemaker.
Schwartz, W. J., Gross, R. A., & Morton, M. T. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.6.1694 · Cited by 258 · see citing works
Mieda, M., Ono, D., Hasegawa, E., Okamoto, H., Honma, K., Honma, S., & Sakurai, T. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.005 · Cited by 254 · see citing works
Astrocytes regulate daily rhythms in the suprachiasmatic nucleus and behavior
Tso, C.-F.-O., Simon, T., Greenlaw, A., Puri, T. A., Mieda, M., & Herzog, E. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.037 · Cited by 252 · see citing works
Barca‐Mayo, O., Pons‐Espinal, M., Follert, P., Armirotti, A., Berdondini, L., & Tonelli, D. D. P. (2017) · Nature Communications · doi:10.1038/ncomms14336 · Cited by 222 · see citing works
Cell fixation and preservation for droplet-based single-cell transcriptomics
Alles, J., Karaiskos, N., Praktiknjo, S. D., Grosswendt, S., Wahle, P., Ruffault, P.-L., Ayoub, S., Schreyer, L., Boltengagen, A., Birchmeier, C., et al. (2017) · BMC Biology · doi:10.1186/s12915-017-0383-5 · Cited by 218 · see citing works
Lee, I. T., Chang, A. S., Manandhar, M., Shan, Y., Fan, J., Izumo, M., Ikeda, Y., Motoike, T., Dixon, S., Seinfeld, J. E., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.006 · Cited by 180 · see citing works
Scalable and DiI-compatible optical clearance of the mammalian brain
Hou, B., Zhang, D., Zhao, S., Wei, M., Yang, Z., Wang, S., Wang, J., Zhang, X., Liu, B., Fan, L., et al. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00019 · Cited by 171 · see citing works
Architecture of retinal projections to the central circadian pacemaker
Fernandez, D. C., Chang, Y.-T., Hattar, S. S., & Chen, S. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523629113 · Cited by 161 · see citing works
Morin, L. P. (2007) · Journal of Biological Rhythms · doi:10.1177/0748730406296749 · Cited by 151 · see citing works
A role for androgens in regulating circadian behavior and the suprachiasmatic nucleus
Karatsoreos, I. N., Wang, A., Sasanian, J., & Silver, R. (2007) · Endocrinology · doi:10.1210/en.2007-0775 · Cited by 136 · see citing works
Hamada, T., Antle, M. C., & Silver, R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03275.x · Cited by 127 · see citing works
Entrainment of Circadian Rhythms Depends on Firing Rates and Neuropeptide Release of VIP SCN Neurons
Mazuski, C. N., Abel, J. H., Chen, S. P., Hermanstyne, T. O., Jones, J. R., Simon, T., Doyle, F. J., & Herzog, E. D. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.029 · Cited by 122 · see citing works
The Nuclear Receptor REV-ERBα Regulates Fabp7 and Modulates Adult Hippocampal Neurogenesis
Schnell, A., Chappuis, S., Schmutz, I., Brai, E., Ripperger, J. A., Schaad, O., Welzl, H., Descombes, P., Alberi, L. A., & Albrecht, U. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099883 · Cited by 104 · see citing works
Lhx1 maintains synchrony among circadian oscillator neurons of the SCN
Hatori, M., Gill, S., Mure, L. S., Goulding, M., O'Leary, D. D. M., & Panda, S. (2014) · eLife · doi:10.7554/elife.03357 · Cited by 81 · see citing works
Park, J., Zhu, H., O’Sullivan, S. J., Ogunnaike, B. A., Weaver, D. R., Schwaber, J. S., & Vadigepalli, R. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00481 · Cited by 61 · see citing works
Weaver, B. P., Zabinsky, R. A., Weaver, Y. M., Lee, E. S., Xue, D., & Han, M. (2014) · eLife · doi:10.7554/elife.04265 · Cited by 54 · see citing works
Cheng, A. H., Bouchard-Cannon, P., Hegazi, S., Lowden, C., Fung, S. W., Chiang, C., Ness, R. W., & Cheng, H. M. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.068 · Cited by 40 · see citing works
Fukuda, H., Tokuda, I. T., Hashimoto, S., & Hayasaka, N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023568 · Cited by 30 · see citing works
Cell fixation and preservation for droplet-based single-cell transcriptomicsPreprint
Alles, J., Karaiskos, N., Praktiknjo, S. D., Grosswendt, S., Wahle, P., Ruffault, P.-L., Ayoub, S., Schreyer, L., Boltengagen, A., Birchmeier, C., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/099473 · Cited by 30 · see citing works
Hannibal, J., Hundahl, C. A., Fahrenkrug, J., Rehfeld, J. F., & Friis-Hansen, L. J. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07385.x · Cited by 24 · see citing works
Angioosteohypertrophysyndrome with protein-losing enteropathy
Caplan, D. B., Herskovic, T., & Gryboski, J. D. (1969) · The Journal of Pediatrics · doi:10.1016/s0022-3476(69)80019-3 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 58 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain
Yao, Z., van Velthoven, C. T. J., Kunst, M., Zhang, M., McMillen, D., Lee, C., Jung, W., Goldy, J., Abdelhak, A., Aitken, M., et al. (2023) · Nature · doi:10.1038/s41586-023-06812-z · Cited by 1,194 · see citing works
The Glymphatic System: A Novel Component of Fundamental Neurobiology
Hablitz, L. M., & Nedergaard, M. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.0619-21.2021 · Cited by 480 · see citing works
Single-cell and spatial transcriptomics: deciphering brain complexity in health and disease
Piwecka, M., Rajewsky, N., & Rybak-Wolf, A. (2023) · Nature Reviews Neurology · doi:10.1038/s41582-023-00809-y · Cited by 320 · see citing works
HypoMap—a unified single-cell gene expression atlas of the murine hypothalamus
Steuernagel, L., Lam, B. Y. H., Klemm, P., Dowsett, G. K. C., Bauder, C. A., Tadross, J. A., Hitschfeld, T. S., del Rio Martin, A., Chen, W., de Solis, A. J., et al. (2022) · Nature Metabolism · doi:10.1038/s42255-022-00657-y · Cited by 267 · see citing works
Generation of hypothalamic arcuate organoids from human induced pluripotent stem cells
Huang, W., Wong, S. Z. H., Pather, S. R., Nguyen, P. T., Zhang, F., Zhang, D. Y., Zhang, Z., Lu, L., Fang, W., Chen, L., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.04.006 · Cited by 173 · see citing works
Defining the age-dependent and tissue-specific circadian transcriptome in male mice
Wolff, C. A., Gutierrez‐Monreal, M. A., Meng, L., Zhang, X., Douma, L. G., Costello, H. M., Douglas, C. M., Ebrahimi, E., Pham, A. T., Oliveira, A. C. D. S., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2022.111982 · Cited by 153 · see citing works
A circadian clock regulates efflux by the blood-brain barrier in mice and human cells
Zhang, S., Lahens, N. F., Yue, Z., Arnold, D. M., Pakstis, P. P., Schwarz, J. E., & Sehgal, A. (2021) · Nature Communications · doi:10.1038/s41467-020-20795-9 · Cited by 159 · see citing works
Todd, W. D., Venner, A., Anaclet, C., Broadhurst, R. Y., Luca, R. D., Bandaru, S. S., Issokson, L., Hablitz, L. M., Cravetchi, O., Arrigoni, E., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17197-2 · Cited by 142 · see citing works
A transcriptomic taxonomy of Drosophila circadian neurons around the clock
Ma, D., Przybylski, D., Abruzzi, K. C., Schlichting, M., Li, Q., Long, X., & Rosbash, M. (2021) · eLife · doi:10.7554/elife.63056 · Cited by 138 · see citing works
Self-citationMammalian circadian systems: Organization and modern life challenges
Finger, A., & Kramer, A. (2021) · Acta Physiologica · doi:10.1111/apha.13548 · Cited by 117 · see citing works
Single-cell analysis of the aging female mouse hypothalamus
Hajdarovic, K. H., Yu, D., Hassell, L.-A., Evans, S. A., Packer, S., Neretti, N., & Webb, A. E. (2022) · Nature Aging · doi:10.1038/s43587-022-00246-4 · Cited by 113 · see citing works
Synaptic connectome of the Drosophila circadian clock
Reinhard, N., Fukuda, A., Manoli, G., Derksen, E., Saito, A., Möller, G., Sekiguchi, M., Rieger, D., Helfrich‐Förster, C., Yoshii, T., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54694-0 · Cited by 110 · see citing works
Circadian VIPergic Neurons of the Suprachiasmatic Nuclei Sculpt the Sleep-Wake Cycle
Collins, B. H., Pierre-Ferrer, S., Muheim, C., Lukacsovich, D., Cai, Y., Spinnler, A., Herrera, C. G., Wen, S., Winterer, J., Belle, M. D. C., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.001 · Cited by 99 · see citing works
Self-citationCoupled network of the circadian clocks: a driving force of rhythmic physiology
Finger, A., Dibner, C., & Kramer, A. (2020) · FEBS Letters · doi:10.1002/1873-3468.13898 · Cited by 99 · see citing works
The circadian clock and metabolic homeostasis: entangled networks
de Assis, L. V. M., & Oster, H. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03800-2 · Cited by 96 · see citing works
Xu, P., Berto, S., Kulkarni, A., Jeong, B., Joseph, C., Cox, K. H., Greenberg, M. E., Kim, T.-K., Konopka, G., & Takahashi, J. S. (2021) · Neuron · doi:10.1016/j.neuron.2021.07.026 · Cited by 86 · see citing works
Defining circadian disruption in neurodegenerative disorders
Colwell, C. S. (2021) · Journal of Clinical Investigation · doi:10.1172/jci148288 · Cited by 90 · see citing works
Roles of Neuropeptides, VIP and AVP, in the Mammalian Central Circadian Clock
Ono, D., Honma, K., & Honma, S. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.650154 · Cited by 87 · see citing works
Microfluidics for Neuronal Cell and Circuit Engineering
Habibey, R., Arias, J. E. R., Striebel, J., & Busskamp, V. (2022) · Chemical Reviews · doi:10.1021/acs.chemrev.2c00212 · Cited by 86 · see citing works
Single‐cell transcriptomics of suprachiasmatic nuclei reveal a Prokineticin‐driven circadian network
Morris, E. L., Patton, A. P., Chesham, J. E., Crisp, A., Adamson, A. D., & Hastings, M. H. (2021) · The EMBO Journal · doi:10.15252/embj.2021108614 · Cited by 85 · see citing works
Neuroendocrine mechanisms underlying estrogen positive feedback and the LH surge
Kauffman, A. S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.953252 · Cited by 86 · see citing works
Cellular and molecular properties of neural progenitors in the developing mammalian hypothalamus
Zhou, X., Zhong, S., Peng, H., Liu, J., Ding, W., Sun, L., Ma, Q., Liu, Z., Chen, R., Wu, Q., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17890-2 · Cited by 77 · see citing works
Self-citationPatton, A. P., Edwards, M. D., Smyllie, N. J., Hamnett, R., Chesham, J. E., Brancaccio, M., Maywood, E. S., & Hastings, M. H. (2020) · Nature Communications · doi:10.1038/s41467-020-17110-x · Cited by 74 · see citing works
Hypertension: Causes and Consequences of Circadian Rhythms in Blood Pressure
Faraci, F. M., & Scheer, F. A. J. L. (2024) · Circulation Research · doi:10.1161/circresaha.124.323515 · Cited by 80 · see citing works
X-chromosome regulation and sex differences in brain anatomy
Raznahan, A., & Distèche, C. M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.024 · Cited by 67 · see citing works
Sleep timing and the circadian clock in mammals: Past, present and the road ahead
Sanchez, R. E. A., Kalume, F. K., & de la Iglesia, H. O. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.05.034 · Cited by 71 · see citing works
Circadian Rhythms and Astrocytes: The Good, the Bad, and the Ugly
Hastings, M. H., Brancaccio, M., Gonzalez-Aponte, M. F., & Herzog, E. D. (2023) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100322-112249 · Cited by 70 · see citing works
Inputs and Outputs of the Mammalian Circadian Clock
Starnes, A. N., & Jones, J. R. (2023) · Biology · doi:10.3390/biology12040508 · Cited by 69 · see citing works
Kim, D. W., Liu, K., Wang, Z. Q., Zhang, Y. S., Bathini, A., Brown, M. P., Lin, S. H., Washington, P. W., Sun, C., Lindtner, S., et al. (2021) · Communications Biology · doi:10.1038/s42003-020-01616-7 · Cited by 55 · see citing works
Self-citationGABAergic mechanisms in the suprachiasmatic nucleus that influence circadian rhythm
Ono, D., Honma, K., & Honma, S. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15012 · Cited by 58 · see citing works
Deciphering the spatial-temporal transcriptional landscape of human hypothalamus development
Zhou, X., Lu, Y., Zhao, F., Dong, J., Ma, W., Zhong, S., Wang, M., Wang, B., Zhao, Y., Shi, Y., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.11.009 · Cited by 58 · see citing works
Self-citationAstrocytic control of extracellular GABA drives circadian timekeeping in the suprachiasmatic nucleus
Patton, A. P., Morris, E. L., McManus, D., Wang, H., Li, Y., Chin, J. W., & Hastings, M. H. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2301330120 · Cited by 58 · see citing works
Self-citationHerb, B. R., Glover, H. J., Bhaduri, A., Colantuoni, C., Bale, T. L., Siletti, K., Linnarsson, S., Hodge, R. D., Lein, E. S., Kriegstein, A. R., et al. (2023) · Science Advances · doi:10.1126/sciadv.adf6251 · Cited by 55 · see citing works
Dopp, J., Ortega, A., Davie, K., Poovathingal, S. K., Baz, E., & Liu, S. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01549-4 · Cited by 55 · see citing works
Circadian and Sleep Metabolomics Across Species
Malik, D. M., Paschos, G. K., Sehgal, A., & Weljie, A. M. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.04.027 · Cited by 52 · see citing works
Cascade diversification directs generation of neuronal diversity in the hypothalamus
Zhang, Y.-H., Xu, M., Shi, X., Sun, X., Mu, W., Wu, H., Wang, J., Li, S., Su, P., Gong, L., et al. (2021) · Cell stem cell · doi:10.1016/j.stem.2021.03.020 · Cited by 53 · see citing works
Self-citationTimed daily exercise remodels circadian rhythms in mice
Hughes, A. T. L., Samuels, R. E., Baño‐Otálora, B., Belle, M. D. C., Wegner, S., Guilding, C., Northeast, R. C., Loudon, A. S. I., Gigg, J., & Piggins, H. D. (2021) · Communications Biology · doi:10.1038/s42003-021-02239-2 · Cited by 53 · see citing works
Sensory input, sex and function shape hypothalamic cell type development
Kaplan, H. S., Logeman, B. L., Zhang, K., Yawitz, T. A., Santiago, C., Sohail, N., Talay, M., Seo, C., Naumenko, S., Sui, S. J. H., et al. (2025) · Nature · doi:10.1038/s41586-025-08603-0 · Cited by 53 · see citing works
The Mammalian Circadian Time-Keeping System
Patton, A. P., & Hastings, M. H. (2023) · Journal of Huntington s Disease · doi:10.3233/jhd-230571 · Cited by 50 · see citing works
The Suprachiasmatic Nucleus at 50: Looking Back, Then Looking Forward
Ono, D., Weaver, D. R., Hastings, M. H., Honma, K., Honma, S., & Silver, R. (2024) · Journal of Biological Rhythms · doi:10.1177/07487304231225706 · Cited by 52 · see citing works
Bae, S., Choi, H., & Lee, D. S. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab095 · Cited by 48 · see citing works
Day-night and seasonal variation of human gene expression across tissues
Wucher, V., Sodaei, R., Amador, R., Irimia, M., & Guigó, R. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3001986 · Cited by 47 · see citing works
Cholecystokinin neurons in mouse suprachiasmatic nucleus regulate the robustness of circadian clock
Xie, L., Xiong, Y., Ma, D., Shi, K., Chen, J., Yang, Q., & Yan, J. (2023) · Neuron · doi:10.1016/j.neuron.2023.04.016 · Cited by 42 · see citing works
Self-citationCircadian rhythms and glial cells of the central nervous system
Brécier, A., Li, V. W., Smith, C. S., Halievski, K., & Ghasemlou, N. (2022) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12917 · Cited by 39 · see citing works
Circadian biology to advance therapeutics for mood disorders
Bhatnagar, A., Murray, G., & Ray, S. (2023) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2023.07.008 · Cited by 40 · see citing works
Fitzgerald, E., Parent, C. I., Kee, M. Z. L., & Meaney, M. J. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.635304 · Cited by 39 · see citing works
Disturbances of Hormonal Circadian Rhythms by Light Pollution
Zeman, M., Okuliarová, M., & Rumanova, V. S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087255 · Cited by 35 · see citing works
Deficiency of autism-related Scn2a gene in mice disrupts sleep patterns and circadian rhythms
Ma, Z., Eaton, M., Liu, Y., Zhang, J., Chen, X., Tu, X., Shi, Y., Que, Z., Wettschurack, K. W., Zhang, Z., et al. (2022) · Neurobiology of Disease · doi:10.1016/j.nbd.2022.105690 · Cited by 35 · see citing works
Understanding the aging hypothalamus, one cell at a time
Hajdarovic, K. H., Yu, D., & Webb, A. E. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.10.004 · Cited by 34 · see citing works
Berry, M. H., Moldavan, M. G., Garrett, T. R., Meadows, M. A., Cravetchi, O., White, E., Leffler, J., von Gersdorff, H., Wright, K. M., Allen, C. N., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36955-6 · Cited by 34 · see citing works
Martin, L. F., Moutal, A., Cheng, K., Washington, S. M., Calligaro, H., Goel, V., Kranz, T., Largent‐Milnes, T. M., Khanna, R., Patwardhan, A. M., et al. (2021) · Journal of Pain · doi:10.1016/j.jpain.2021.05.006 · Cited by 34 · see citing works
Daily electrical activity in the master circadian clock of a diurnal mammal
Baño‐Otálora, B., Moye, M. J., Brown, T. M., Lucas, R. J., Diekman, C. O., & Belle, M. D. C. (2021) · eLife · doi:10.7554/elife.68179 · Cited by 34 · see citing works
Ding, H., Meng, L., Liu, A. C., Gumz, M. L., Bryant, A. J., McClung, C. A., Tseng, G. C., Esser, K. A., & Huo, Z. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab224 · Cited by 33 · see citing works
Melatonin receptors, brain functions, and therapies
Oishi, A., Gbahou, F., & Jockers, R. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00022-4 · Cited by 33 · see citing works
A hypothalamic dopamine locus for psychostimulant-induced hyperlocomotion in mice
Korchynska, S., Rebernik, P., Pende, M., Boi, L., Alpár, A., Tasan, R. O., Becker, K., Balueva, K., Saghafi, S., Wulff, P., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33584-3 · Cited by 33 · see citing works
Time Will Tell: Intercellular Communication in the Plant Clock
Sorkin, M. L., & Nusinow, D. A. (2021) · Trends in Plant Science · doi:10.1016/j.tplants.2020.12.009 · Cited by 31 · see citing works
Circadian Mechanisms in Brain Fluid Biology
Vizcarra, V. S., Fame, R. M., & Hablitz, L. M. (2024) · Circulation Research · doi:10.1161/circresaha.123.323516 · Cited by 30 · see citing works
Multi-Modal Regulation of Circadian Physiology by Interactive Features of Biological Clocks
Lee, Y., & Wisor, J. P. (2021) · Biology · doi:10.3390/biology11010021 · Cited by 30 · see citing works
Circadian Rhythms in the Neuronal Network Timing the Luteinizing Hormone Surge
Tonsfeldt, K. J., Mellon, P. L., & Hoffmann, H. M. (2021) · Endocrinology · doi:10.1210/endocr/bqab268 · Cited by 34 · see citing works
Adult Mouse Retina Explants: From ex vivo to in vivo Model of Central Nervous System Injuries
Schaeffer, J., Delpech, C., Albert, F., Belin, S., & Nawabi, H. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.599948 · Cited by 30 · see citing works
Vilallongue, N., Schaeffer, J., Hesse, A.-M., Delpech, C., Blot, B., Paccard, A., Plissonnier, E., Excoffier, B., Couté, Y., Belin, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33799-4 · Cited by 29 · see citing works
Impacts of vitamin A deficiency on biological rhythms: Insights from the literature
Guo, X., Wang, H., Xu, J., & Hua, H. M. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.886244 · Cited by 28 · see citing works
Self-citationOntogenetic rules for the molecular diversification of hypothalamic neurons
Benevento, M., Hökfelt, T. G. M., & Harkany, T. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00615-3 · Cited by 28 · see citing works
Circadian and kisspeptin regulation of the preovulatory surge
Piet, R. (2023) · Peptides · doi:10.1016/j.peptides.2023.170981 · Cited by 29 · see citing works
Asano, F., Kim, S. J., Fujiyama, T., Miyoshi, C., Hotta-Hirashima, N., Asama, N., Iwasaki, K., Kakizaki, M., Mizuno, S., Mieda, M., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2218209120 · Cited by 26 · see citing works
Fighting Against the Clock: Circadian Disruption and Parkinson’s Disease
Chen, Y.-C., Wang, W., Lewis, S. J. G., & Wu, S. (2023) · Journal of Movement Disorders · doi:10.14802/jmd.23216 · Cited by 26 · see citing works
Targeting NR1D1 in organ injury: challenges and prospects
Zhang-Sun, Z.-Y., Xu, X., Escames, G., Lei, W., Zhao, L., Zhou, Y.-Z., Tian, Y., Ren, Y., Acuña-Castroviejo, D., & Yang, Y. (2023) · Military Medical Research · doi:10.1186/s40779-023-00495-3 · Cited by 38 · see citing works
Leptin receptor neurons in the dorsomedial hypothalamus input to the circadian feeding network
Tang, Q., Godschall, E., Brennan, C. D., Zhang, Q., Abraham‐Fan, R., Williams, S. P., Güngül, T. B., Onoharigho, R., Buyukaksakal, A., Salinas, R., et al. (2023) · Science Advances · doi:10.1126/sciadv.adh9570 · Cited by 32 · see citing works
Auerbach, B. J., FitzGerald, G. A., & Li, M. (2022) · Nature Communications · doi:10.1038/s41467-022-34185-w · Cited by 25 · see citing works
BDE-47 Causes Depression-like Effects in Zebrafish Larvae via a Non-Image-Forming Visual Mechanism
Cao, M., Xu, T., Zhang, H., Wei, S., Wang, H., Song, Y., Guo, X., Chen, D., & Yin, D. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c01716 · Cited by 25 · see citing works
Self-citationHuang, Y., Wang, A., Zhou, W., Li, B., Zhang, L., Rudolf, A. M., Jin, Z., Hambly, C., Wang, G., & Speakman, J. R. (2024) · Nature Communications · doi:10.1038/s41467-024-46589-x · Cited by 23 · see citing works
Energy balance drives diurnal and nocturnal brain transcriptome rhythms
van Rosmalen, L., Deota, S., Maier, G., Le, H. D., Lin, T. C., Ramasamy, R. K., Hut, R. A., & Panda, S. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113951 · Cited by 24 · see citing works
Jha, P. K., Bouâouda, H., Kalsbeek, A., & Challet, É. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.011 · Cited by 23 · see citing works
Yamaguchi, Y., Murai, I., Goto, K., Doi, S., Zhou, H., Setsu, G., Shimatani, H., Okamura, H., Miyake, T., & Doi, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-01764-8 · Cited by 23 · see citing works
Xiong, X., Hu, T., Yin, Z., Zhang, Y., Chen, F., & Lei, P. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.944283 · Cited by 24 · see citing works
Reduced VIP Expression Affects Circadian Clock Function in VIP-IRES-CRE Mice (JAX 010908)
Joye, D. A. M., Rohr, K. E., Keller, D., Inda, T., Telega, A., Pancholi, H., Carmona‐Alcocer, V., & Evans, J. A. (2020) · Journal of Biological Rhythms · doi:10.1177/0748730420925573 · Cited by 23 · see citing works
Qin, Y., Liu, Z., Gao, S., Martínez-Vasallo, C., Long, Y., Zhu, X., Liu, B., Gao, Y., Xu, X., Nohales, M. A., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-59424-8 · Cited by 23 · see citing works
Drunen, R. V., Dai, Y., Wei, H., Fekry, B., Noori, S., Shivshankar, S., Bravo, R., Zhao, Z., Yoo, S. H., Justice, N. J., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114380 · Cited by 23 · see citing works
Astrocyte Clocks and Glucose Homeostasis
Barca‐Mayo, O., & López, M. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.662017 · Cited by 23 · see citing works
Hu, S., Luo, L., & Zeng, L. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2040945 · Cited by 21 · see citing works
Bartholomai, B. M., Gladfelter, A. S., Loros, J., & Dunlap, J. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2203078119 · Cited by 21 · see citing works
Koo, K., Kim, C., Kim, H., Cho, Y., Suhito, I. R., & Kim, T. P. (2023) · Advanced Science · doi:10.1002/advs.202207084 · Cited by 21 · see citing works
Tsuno, Y., Peng, Y., Horike, S., Wang, M., Matsui, A., Yamagata, K., Sugiyama, M., Nakamura, T. J., Daikoku, T., Maejima, T., et al. (2023) · PLoS Biology · doi:10.1371/journal.pbio.3002281 · Cited by 21 · see citing works
Circadian Regulation of Apolipoproteins in the Brain: Implications in Lipid Metabolism and Disease
Lee, C., Murrell, C. E., Chu, A., & Pan, X. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242417415 · Cited by 20 · see citing works
A whole-brain single-cell atlas of circadian neural activity in mice
Yamashita, K., Kinoshita, F. L., Yoshida, S., Matsumoto, K., Mitani, T. T., Fujishima, H., Minami, Y., Morii, E., Yamada, R. G., Okada, S., et al. (2025) · Science · doi:10.1126/science.aea3381 · Cited by 23 · see citing works
Swift, J., Greenham, K., Ecker, J. R., Coruzzi, G. M., & McClung, C. R. (2021) · The Plant Journal · doi:10.1111/tpj.15589 · Cited by 20 · see citing works
High-Fat Nutritional Challenge Reshapes Circadian Signatures in Murine Extraorbital Lacrimal Glands
Zou, S., Jiao, X., Liu, J., Qi, D., Pei, X., Lu, D., Huang, S., & Li, Z. (2022) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.63.5.23 · 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
Higgs, M. J., Hill, M., John, R. M., & Isles, A. R. (2022) · BMC Genomics · doi:10.1186/s12864-022-08986-8 · Cited by 20 · see citing works
The genomic basis of temporal niche evolution in a diurnal rodent
Richardson, R., Feigin, C. Y., Baño‐Otálora, B., Johnson, M. R., Allen, A. E., Park, J., McDowell, R. J., Mereby, S. A., Lin, I., Lucas, R. J., et al. (2023) · Current Biology · doi:10.1016/j.cub.2023.06.068 · 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
Chronic sleep deprivation impairs retinal circadian transcriptome and visual function
Huang, S., Zhang, W., Xuan, S., Si, H., Huang, D., Ba, M., Qi, D., Pei, X., Lu, D., & Li, Z. (2024) · Experimental Eye Research · doi:10.1016/j.exer.2024.109907 · Cited by 20 · see citing works
Duan, J., Ngo, M. N., Karri, S. S., Tsoi, L. C., Gudjonsson, J. E., Shahbaba, B., Lowengrub, J. S., & D, B. A. M. (2024) · Nature Communications · doi:10.1038/s41467-024-48041-6 · Cited by 20 · see citing works
Daily rhythms in gene expression of the human parasite Schistosoma mansoni
Rawlinson, K. A., Reid, A. J., Lu, Z., Driguez, P., Wawer, A., Coghlan, A., Sankaranarayanan, G., Buddenborg, S. K., Soria, C. D., McCarthy, C. A., et al. (2021) · BMC Biology · doi:10.1186/s12915-021-01189-9 · Cited by 19 · see citing works
Karin, J., Bornfeld, Y., & Nitzan, M. (2023) · Nature Biotechnology · doi:10.1038/s41587-023-01663-5 · Cited by 18 · see citing works
Zong, W., Seney, M. L., Ketchesin, K. D., Gorczyca, M. T., Liu, A. C., Esser, K. A., Tseng, G. C., McClung, C. A., & Huo, Z. (2023) · Statistics in Medicine · doi:10.1002/sim.9803 · Cited by 19 · see citing works
Chen, R., Routh, B. N., Gaudet, A. D., & Fonken, L. K. (2023) · Journal of Biological Rhythms · doi:10.1177/07487304231178950 · Cited by 19 · see citing works
Circadian medicine for aging attenuation and sleep disorders: Prospects and challenges
Banerjee, S., & Ray, S. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102387 · Cited by 18 · see citing works
Evans, J. A., & Schwartz, W. J. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01659-1 · Cited by 18 · see citing works
Hamnett, R., Chesham, J. E., Maywood, E. S., & Hastings, M. H. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2015-20.2020 · Cited by 18 · see citing works
- Authors
- Wen, S., Ma, D., Zhao, M., Xie, L., Wu, Q., Gou, L., Zhu, C., Fan, Y., Wang, H., & Yan, J.
- Affiliations
- Chinese Academy of Sciences (CN)
- Corresponding author
- Yan, Jun
- Venue
- Nature Neuroscience
- Published
- 2020-02-17
- Volume
- 23
- Issue
- 3
- Pages
- 456-467
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W3005834749
- Cited by
- 328
- References
- 58
- Citations by year
- 2026: 35 · 2025: 50 · 2024: 75 · 2023: 54 · 2022: 37 · 2021: 45 · 2020: 32
- FWCI
- 21.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Science Foundation of Shanghai (16ZR1448800)
- National Natural Science Foundation of China (31571209)
- Science and Technology Commission of Shanghai Municipality (No. 2018SHZDZX05)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
- Keywords
- suprachiasmatic nucleus, circadian rhythm, circadian pacemaker, neuronal cell types, circadian gene expression, light-induced gene expression, single-cell RNA sequencing, 3D reconstruction, mice, ventral hypothalamus
- MeSH terms
- Animals, Atlases as Topic, Circadian Rhythm, Gene Expression Regulation, Light, Male, Mice, Inbred C57BL, Neurons, Photic Stimulation, Suprachiasmatic Nucleus, Gene Expression, Genomics, Mice, Circadian Rhythm Signaling Peptides and Proteins, Single-Cell Analysis
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