Nuclear Proteomics Uncovers Diurnal Regulatory Landscapes in Mouse Liver
Diurnal oscillations of gene expression controlled by the circadian clock and its connected feeding rhythm enable organisms to coordinate their physiologies with daily environmental cycles. While available techniques yielded crucial insights into regulation at the transcriptional level, much less is...
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| Published in | Cell metabolism Vol. 25; no. 1; pp. 102 - 117 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
10.01.2017
Elsevier Cell Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Diurnal oscillations of gene expression controlled by the circadian clock and its connected feeding rhythm enable organisms to coordinate their physiologies with daily environmental cycles. While available techniques yielded crucial insights into regulation at the transcriptional level, much less is known about temporally controlled functions within the nucleus and their regulation at the protein level. Here, we quantified the temporal nuclear accumulation of proteins and phosphoproteins from mouse liver by SILAC proteomics. We identified around 5,000 nuclear proteins, over 500 of which showed a diurnal accumulation. Parallel analysis of the nuclear phosphoproteome enabled the inference of the temporal activity of kinases accounting for rhythmic phosphorylation. Many identified rhythmic proteins were parts of nuclear complexes involved in transcriptional regulation, ribosome biogenesis, DNA repair, and the cell cycle and its potentially associated diurnal rhythm of hepatocyte polyploidy. Taken together, these findings provide unprecedented insights into the diurnal regulatory landscape of the mouse liver nucleus.
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•SILAC nuclear proteomics uncovered new diurnal regulatory landscape of mouse liver•Regulation of the diurnal nuclear proteome is mostly post-translational•Diurnal proteins regulate transcription, ribosome biogenesis, DNA repair, and cell cycle•Hepatocyte polyploidy and size oscillate diurnally
Wang et al. quantify the temporal nuclear accumulation of proteins and phosphoproteins in the mouse liver and reveal that 13% of nuclear proteins exhibit a diurnal rhythm regulated at the post-translational level through nuclear transport of protein complexes involved in transcription, DNA repair, ribosome biogenesis, cell cycle, and polyploidy. |
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| AbstractList | Diurnal oscillations of gene expression controlled by the circadian clock and its connected feeding rhythm enable organisms to coordinate their physiologies with daily environmental cycles. While available techniques yielded crucial insights into regulation at the transcriptional level, much less is known about temporally controlled functions within the nucleus and their regulation at the protein level. Here, we quantified the temporal nuclear accumulation of proteins and phosphoproteins from mouse liver by SILAC proteomics. We identified around 5,000 nuclear proteins, over 500 of which showed a diurnal accumulation. Parallel analysis of the nuclear phosphoproteome enabled the inference of the temporal activity of kinases accounting for rhythmic phosphorylation. Many identified rhythmic proteins were parts of nuclear complexes involved in transcriptional regulation, ribosome biogenesis, DNA repair, and the cell cycle and its potentially associated diurnal rhythm of hepatocyte polyploidy. Taken together, these findings provide unprecedented insights into the diurnal regulatory landscape of the mouse liver nucleus.
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SILAC nuclear proteomics uncovered new diurnal regulatory landscape of mouse liver
•
Regulation of the diurnal nuclear proteome is mostly post-translational
•
Diurnal proteins regulate transcription, ribosome biogenesis, DNA repair, and cell cycle
•
Hepatocyte polyploidy and size oscillate diurnally
Wang et al. quantify the temporal nuclear accumulation of proteins and phosphoproteins in the mouse liver and reveal that 13% of nuclear proteins exhibit a diurnal rhythm regulated at the post-translational level through nuclear transport of protein complexes involved in transcription, DNA repair, ribosome biogenesis, cell cycle, and polyploidy. Diurnal oscillations of gene expression controlled by the circadian clock and its connected feeding rhythm enable organisms to coordinate their physiologies with daily environmental cycles. While available techniques yielded crucial insights into regulation at the transcriptional level, much less is known about temporally controlled functions within the nucleus and their regulation at the protein level. Here, we quantified the temporal nuclear accumulation of proteins and phosphoproteins from mouse liver by SILAC proteomics. We identified around 5,000 nuclear proteins, over 500 of which showed a diurnal accumulation. Parallel analysis of the nuclear phosphoproteome enabled the inference of the temporal activity of kinases accounting for rhythmic phosphorylation. Many identified rhythmic proteins were parts of nuclear complexes involved in transcriptional regulation, ribosome biogenesis, DNA repair, and the cell cycle and its potentially associated diurnal rhythm of hepatocyte polyploidy. Taken together, these findings provide unprecedented insights into the diurnal regulatory landscape of the mouse liver nucleus. Diurnal oscillations of gene expression controlled by the circadian clock and its connected feeding rhythm enable organisms to coordinate their physiologies with daily environmental cycles. While available techniques yielded crucial insights into regulation at the transcriptional level, much less is known about temporally controlled functions within the nucleus and their regulation at the protein level. Here, we quantified the temporal nuclear accumulation of proteins and phosphoproteins from mouse liver by SILAC proteomics. We identified around 5,000 nuclear proteins, over 500 of which showed a diurnal accumulation. Parallel analysis of the nuclear phosphoproteome enabled the inference of the temporal activity of kinases accounting for rhythmic phosphorylation. Many identified rhythmic proteins were parts of nuclear complexes involved in transcriptional regulation, ribosome biogenesis, DNA repair, and the cell cycle and its potentially associated diurnal rhythm of hepatocyte polyploidy. Taken together, these findings provide unprecedented insights into the diurnal regulatory landscape of the mouse liver nucleus. [Display omitted] •SILAC nuclear proteomics uncovered new diurnal regulatory landscape of mouse liver•Regulation of the diurnal nuclear proteome is mostly post-translational•Diurnal proteins regulate transcription, ribosome biogenesis, DNA repair, and cell cycle•Hepatocyte polyploidy and size oscillate diurnally Wang et al. quantify the temporal nuclear accumulation of proteins and phosphoproteins in the mouse liver and reveal that 13% of nuclear proteins exhibit a diurnal rhythm regulated at the post-translational level through nuclear transport of protein complexes involved in transcription, DNA repair, ribosome biogenesis, cell cycle, and polyploidy. |
| Author | Galindo, Antonio Núñez Mauvoisin, Daniel Kussmann, Martin Naef, Felix Sizzano, Federico Atger, Florian Gachon, Frédéric Palini, Alessio Waridel, Patrice Wang, Jingkui Quadroni, Manfredo Dulić, Vjekoslav Dayon, Loïc Martin, Eva |
| AuthorAffiliation | 3 Department of Pharmacology and Toxicology, University of Lausanne, CH-1015 Lausanne, Switzerland 1 Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland 7 CNRS, UMR 5535, Institut de Génétique Moléculaire de Montpellier, 34090 Montpellier, France 4 Systems Nutrition, Metabonomics, and Proteomics, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland 2 Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland 8 School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland 5 Department of Cell Biology, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland 6 Protein Analysis Facility, University of Lausanne, CH-1015 Lausanne, Switzerland |
| AuthorAffiliation_xml | – name: 7 CNRS, UMR 5535, Institut de Génétique Moléculaire de Montpellier, 34090 Montpellier, France – name: 4 Systems Nutrition, Metabonomics, and Proteomics, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – name: 2 Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – name: 1 Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland – name: 3 Department of Pharmacology and Toxicology, University of Lausanne, CH-1015 Lausanne, Switzerland – name: 5 Department of Cell Biology, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – name: 6 Protein Analysis Facility, University of Lausanne, CH-1015 Lausanne, Switzerland – name: 8 School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland |
| Author_xml | – sequence: 1 givenname: Jingkui surname: Wang fullname: Wang, Jingkui organization: Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland – sequence: 2 givenname: Daniel surname: Mauvoisin fullname: Mauvoisin, Daniel organization: Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 3 givenname: Eva surname: Martin fullname: Martin, Eva organization: Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 4 givenname: Florian surname: Atger fullname: Atger, Florian organization: Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 5 givenname: Antonio Núñez surname: Galindo fullname: Galindo, Antonio Núñez organization: Systems Nutrition, Metabonomics, and Proteomics, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 6 givenname: Loïc surname: Dayon fullname: Dayon, Loïc organization: Systems Nutrition, Metabonomics, and Proteomics, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 7 givenname: Federico surname: Sizzano fullname: Sizzano, Federico organization: Department of Cell Biology, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 8 givenname: Alessio surname: Palini fullname: Palini, Alessio organization: Department of Cell Biology, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 9 givenname: Martin surname: Kussmann fullname: Kussmann, Martin organization: Systems Nutrition, Metabonomics, and Proteomics, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland – sequence: 10 givenname: Patrice surname: Waridel fullname: Waridel, Patrice organization: Protein Analysis Facility, University of Lausanne, CH-1015 Lausanne, Switzerland – sequence: 11 givenname: Manfredo surname: Quadroni fullname: Quadroni, Manfredo organization: Protein Analysis Facility, University of Lausanne, CH-1015 Lausanne, Switzerland – sequence: 12 givenname: Vjekoslav surname: Dulić fullname: Dulić, Vjekoslav organization: CNRS, UMR 5535, Institut de Génétique Moléculaire de Montpellier, 34090 Montpellier, France – sequence: 13 givenname: Felix surname: Naef fullname: Naef, Felix email: felix.naef@epfl.ch organization: Institute of Bioengineering, School of Life Sciences, Ecole Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland – sequence: 14 givenname: Frédéric surname: Gachon fullname: Gachon, Frédéric email: frederic.gachon@rd.nestle.com organization: Department of Diabetes and Circadian Rhythms, Nestlé Institute of Health Sciences, CH-1015 Lausanne, Switzerland |
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| PublicationCentury | 2000 |
| PublicationDate | 2017-01-10 |
| PublicationDateYYYYMMDD | 2017-01-10 |
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| PublicationPlace | United States |
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| PublicationTitle | Cell metabolism |
| PublicationTitleAlternate | Cell Metab |
| PublicationYear | 2017 |
| Publisher | Elsevier Inc Elsevier Cell Press |
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| SubjectTerms | Animals Biochemistry, Molecular Biology Cell Nucleus - metabolism Circadian Clocks - genetics Circadian Rhythm - genetics DNA Repair Gene Expression Regulation Isotope Labeling Life Sciences Liver - metabolism Mass Spectrometry Mice Mice, Knockout Nuclear Proteins - metabolism Organelle Biogenesis Phosphoproteins - metabolism Phosphorylation Polyploidy Protein Kinases - metabolism Proteome - metabolism Proteomics - methods Resource Ribosomes - metabolism Time Factors Transcription Factors - metabolism Transcription, Genetic |
| Title | Nuclear Proteomics Uncovers Diurnal Regulatory Landscapes in Mouse Liver |
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