The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.
Circadian clock-dependent and -independent rhythmic proteomes implement distinct diurnal functions in mouse liver
Open accessAbstract
Diurnal oscillations of gene expression controlled by the circadian clock underlie rhythmic physiology across most living organisms. Although such rhythms have been extensively studied at the level of transcription and mRNA accumulation, little is known about the accumulation patterns of proteins. Here, we quantified temporal profiles in the murine hepatic proteome under physiological light-dark conditions using stable isotope labeling by amino acids quantitative MS. Our analysis identified over 5,000 proteins, of which several hundred showed robust diurnal oscillations with peak phases enriched in the morning and during the night and related to core hepatic physiological functions. Combined mathematical modeling of temporal protein and mRNA profiles indicated that proteins accumulate with reduced amplitudes and significant delays, consistent with protein half-life data. Moreover, a group comprising about one-half of the rhythmic proteins showed no corresponding rhythmic mRNAs, indicating significant translational or posttranslational diurnal control. Such rhythms were highly enriched in secreted proteins accumulating tightly during the night. Also, these rhythms persisted in clock-deficient animals subjected to rhythmic feeding, suggesting that food-related entrainment signals influence rhythms in circulating plasma factors.
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
“Similar to the reported proportion of rhythmic transcripts, it has been estimated that 6-20% of the murine proteome exhibits circadian rhythms in tissues such as the SCN (33,34) and liver (35)(36)(37).”
From Circadian rhythms, metabolism, and chrononutrition in rodents and humans (2016) · cites this paper as [36]
Citations
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482
Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · cited 4×
“(B) Protein half-lives (measured in NIH 3T3 cells) (19) are significantly longer in C1 and C2 (nonrhythmic proteins) compared with C3 and C4 (rhythmic proteins; P < 0.”
BackgroundMethodInfluentialAndromeda: A Peptide Search Engine Integrated into the MaxQuant Environment
Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., & Mann, M. (2011) · Journal of Proteome Research · doi:10.1021/pr101065j · Cited by 5,503
Central and Peripheral Circadian Clocks in Mammals
Mohawk, J. A., Green, C. B., & Takahashi, J. S. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-153128 · Cited by 2,265
Transcriptional architecture and chromatin landscape of the core circadian clock in mammals
Koike, N., Yoo, S.-H., Huang, H.-C., Kumar, V., Lee, C., Kim, T.-K., & Takahashi, J. S. (2012) · Science · doi:10.1126/science.1226339 · Cited by 1,464
Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms
Horst, G. T. J. V. D., Muijtjens, M., Kobayashi, K., Takano, R., Kanno, S.-I., Takao, M., Wit, J. D., Verkerk, A., Eker, A. P. M., Leenen, D. V., et al. (1999) · Nature · doi:10.1038/19323 · Cited by 1,402
Posttranslational Mechanisms Regulate the Mammalian Circadian Clock
Lee, C., Etchegaray, J., Cagampang, F. R. A., Loudon, A. S. I., & Reppert, S. M. (2001) · Cell · doi:10.1016/s0092-8674(01)00610-9 · Cited by 1,174
Rudic, R. D., McNamara, P., Curtis, A.-M., Boston, R. C., Panda, S., Hogenesch, J. B., & FitzGerald, G. A. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020377 · Cited by 1,059
Harmonics of Circadian Gene Transcription in Mammals
Hughes, M. E., DiTacchio, L., Hayes, K. R., Vollmers, C., Pulivarthy, S. R., Baggs, J. E., Panda, S., & Hogenesch, J. B. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000442 · Cited by 689
Cited by
Sorted by citations
Items 301–329 of 329
Rhythms in Pharmacokinetics: Absorption and Disposition
Vázquez, M., Eiraldi, R., & Maldonado, C. (2021) · Springer eBooks · doi:10.1007/978-3-030-51519-5_161-1
Ueda, H. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733755363.793558638
Gachon, F. (2018) · Biologie Aujourd hui · doi:10.1051/jbio/2018025
Rhythms in Pharmacokinetics: Absorption and Disposition
Vázquez, M., Eiraldi, R., & Maldonado, C. (2022) · Springer eBooks · doi:10.1007/978-3-030-84860-6_161
Rajavel, A. (2022) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-9595
Circadian proteomics reveal rampant tuning of post-transcriptional apparatus by Chlamydomonas clockPreprint
Jadhav, D. B., & Roy, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.28.550970
Questel, E. L., Besnard, C., Atger, F., Foucher, Y., Tollec, A., Pakulska, V., Oliveira, A. R., Cloteau, C., Gourdel, M., Nemazanyy, I., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.03.607283
Malcolm, M., Pusterla, J. M., Penazzi, L. G., Trenchi, A., Acosta-Rodríguez, V. A., Ríos, M. N., Villarreal, M. A., Guido, M. E., & Garbarino‐Pico, E. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26209943
Circadian clock: Epigenetic regulators (sirtuins), metabolism, and diseases
Meyer‐Ficca, M. L., & Meyer, R. G. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-13825-6.00303-4
Semenovykh, D., Semenovykh, K., Sládek, M., & Sumová, A. (2026) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-026-01152-8
Rôle du long ARN non codant Neat1 dans la rythmicité circadienne hypophysaire
Torres, M. (2018) · theses.fr (ABES) · doi:10.70675/0be62982z380ez416dzbc04zb92ab61b6e88
The role of the circadian transcription factor KLF10 in liver physiology
Ruberto, A. A. (2019) · theses.fr (ABES) · doi:10.70675/cb3492c2z5778z48e3za7d7zf17279fd718b
Circadian regulation of the retinal pigment epithelium–photoreceptor complex
Milićević, N. (2020) · theses.fr (ABES) · doi:10.70675/2a3b679cz473bz4c14zb33az700581cd794a
Partenaires moléculaires et fonctions circadiennes hypophysaires du long ARN non codant Neat1
Jacq, A. (2021) · theses.fr (ABES) · doi:10.70675/005fd6e8z66f0z494fz948ez8e6124d86039
Questel, E. L. (2024) · theses.fr (ABES) · doi:10.70675/fcc42711z49b5z4a0cz8169z4ba8e7c25386
Atger, F., Durand, M., Croyal, M., Chavanne, A., Questel, E. L., Foucher, Y., Besnard, C., Nemazanyy, I., Lay, S. L., Prieur, X., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.04.18.719366
Sarver, D. C., Maddahi, Y., Colwell, C. S., & Lusis, A. J. (2026) · iScience · doi:10.1016/j.isci.2026.115957
Time to rethink circadian rhythms beyond the transcriptome
Otobe, Y., & Yoshitane, H. (2026) · The Journal of Biochemistry · doi:10.1093/jb/mvag031
Questel, E. L., Besnard, C., Atger, F., Foucher, Y., Tollec, A., Pakulska, V., Oliveira, A. R., Cloteau, C., Gourdel, M., Nemazanyy, I., et al. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117774
mTOR signalling, not clock gene rhythms, organises daily physiologyPreprint
Zeng, A., Mihut, A., Anandapadamanaban, M., Goity, A., Dantas, L. L. D. B., Chew, S. Y. P., Hayter, E. A., Andersson, L. C., Smith, T. S., Pasquini, G., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.28.747564
Wang, T., Chu, Y., Li, X., Zheng, H., Feng, J., & Wang, H. (2026) · Biomolecules · doi:10.3390/biom16091289
Metadata
- Authors
- Mauvoisin, D., Wang, J., Jouffe, C., Martin, E., Atger, F., Waridel, P., Quadroni, M., Gachon, F., & Naef, F.
- Affiliations
- University of Lausanne (CH)
- SIB Swiss Institute of Bioinformatics (CH)
- Department of Pharmacology and Toxicology, University of Lausanne, CH-1005 Lausanne, Switzerland;
- The Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne and Swiss Institute of Bioinformatics, Lausanne CH-1015, Switzerland; and
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-12-16
- Volume
- 111
- Issue
- 1
- Pages
- 167-172
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3890886
- OpenAlex
- W2027410128
- Cited by
- 329
- References
- 58
- Citations by year
- 2026: 11 · 2025: 18 · 2024: 19 · 2023: 23 · 2022: 24 · 2021: 32 · 2020: 34 · 2019: 30 · 2018: 32 · 2017: 28 · 2016: 28 · 2015: 26 · 2014: 21 · 2013: 1
- FWCI
- 13.68
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- other-oa
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (130714)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Sleep and Work-Related Fatigue
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Keywords
- circadian clock, diurnal cycle, liver proteome, protein half-life, translational regulation, post-translational regulation, secreted proteins, light-dark cycle, mouse liver
- MeSH terms
- Albumins, alpha 1-Antitrypsin, Animals, Circadian Rhythm, Gene Expression Regulation, Liver, Male, Mice, Inbred C57BL, Models, Theoretical, Plasma, Protein Processing, Post-Translational, RNA, Messenger, Mass Spectrometry, Mice, Knockout, Proteome, Mice, Cryptochromes, 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