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Mapping the nucleolar proteome reveals a spatiotemporal organization related to intrinsic protein disorder

View ORCID ProfileLovisa Stenström, Diana Mahdessian, View ORCID ProfileChristian Gnann, View ORCID ProfileAnthony J. Cesnik, View ORCID ProfileWei Ouyang, View ORCID ProfileManuel D. Leonetti, View ORCID ProfileMathias Uhlén, Sara Cuylen-Häring, Peter J. Thul, View ORCID ProfileEmma Lundberg
doi: https://doi.org/10.1101/2020.01.30.923003
Lovisa Stenström
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
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  • ORCID record for Lovisa Stenström
Diana Mahdessian
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
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Christian Gnann
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
2Chan Zuckerberg Biohub, San Francisco, CA 94158, USA
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Anthony J. Cesnik
2Chan Zuckerberg Biohub, San Francisco, CA 94158, USA
4Department of Genetics, Stanford University, Stanford, CA 94158, USA
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Wei Ouyang
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
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Manuel D. Leonetti
2Chan Zuckerberg Biohub, San Francisco, CA 94158, USA
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Mathias Uhlén
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
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Sara Cuylen-Häring
3Cell Biology and Biophysics Unit, Structural and Computational Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany
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Peter J. Thul
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
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Emma Lundberg
1Science for Life Laboratory, School of Engineering Sciences in Chemistry, Biotechnology and Health, KTH Royal Institute of Technology, SE-171 65 Stockholm, Sweden
2Chan Zuckerberg Biohub, San Francisco, CA 94158, USA
4Department of Genetics, Stanford University, Stanford, CA 94158, USA
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  • For correspondence: emma.lundberg@scilifelab.se
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Abstract

The nucleolus is essential for ribosome biogenesis and is involved in many other cellular functions. We performed a systematic spatiotemporal dissection of the human nucleolar proteome using confocal microscopy. In total, 1,318 nucleolar proteins were identified; 287 were localized to fibrillar components, and 157 were enriched along the nucleoplasmic border, indicating a potential fourth nucleolar subcompartment (nucleoli rim). We found 65 nucleolar proteins (36 uncharacterized) to relocate to the chromosomal periphery during mitosis. Interestingly, we observed temporal partitioning into two recruitment phenotypes: early (prometaphase) and late (after metaphase), suggesting phase-specific functions. We further show that expression of MKI67 is critical for this temporal partitioning. We provide the first proteome-wide analysis of intrinsic protein disorder for the human nucleolus and show that nucleolar proteins in general, and mitotic chromosome proteins in particular, have significantly higher intrinsic disorder level compared to cytosolic proteins. In summary, this study provides a comprehensive and essential resource of spatiotemporal expression data for the nucleolar proteome as part of the Human Protein Atlas.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Manuscript now including quantification of mitotic chromosome staining patterns, replicate experiments, automated classification of image patterns, and analysis of protein abundance using MS proteomics datasets.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted May 26, 2020.
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Mapping the nucleolar proteome reveals a spatiotemporal organization related to intrinsic protein disorder
Lovisa Stenström, Diana Mahdessian, Christian Gnann, Anthony J. Cesnik, Wei Ouyang, Manuel D. Leonetti, Mathias Uhlén, Sara Cuylen-Häring, Peter J. Thul, Emma Lundberg
bioRxiv 2020.01.30.923003; doi: https://doi.org/10.1101/2020.01.30.923003
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Mapping the nucleolar proteome reveals a spatiotemporal organization related to intrinsic protein disorder
Lovisa Stenström, Diana Mahdessian, Christian Gnann, Anthony J. Cesnik, Wei Ouyang, Manuel D. Leonetti, Mathias Uhlén, Sara Cuylen-Häring, Peter J. Thul, Emma Lundberg
bioRxiv 2020.01.30.923003; doi: https://doi.org/10.1101/2020.01.30.923003

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