The cell nucleus contains distinct biomolecular condensates that form at specific genetic loci, organize chromosomes in 3D space, and regulate RNA processing. Among these, Cajal bodies (CBs) require key “scaffolding” proteins for their assembly, which is not fully understood. Here, we employ proximity biotinylation, mass spectrometry, and functional screening to comprehensively identify and test the functions of CB components. We document 144 protein interactors of coilin, of which 70 were newly detected, and establish 25 players needed for CB assembly and/or maintenance. Surprisingly, the depletion of nine coilin interactors—mostly constituents of the 60S ribosome (RPLs)—increased CB number and caused subdomains defined by coilin and the survival motor neuron protein (SMN) to merge. These phenotypes were traceable to altered nuclear levels of dimethylarginine. Our data implicate RPL24 and other players in the regulation of CBs by modulating posttranslational modifications. Moreover, the prevalence of transcription factors among the identified components highlights roles for gene activity in CB assembly and nuclear positioning.
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November 27 2024
Identification of coilin interactors reveals coordinated control of Cajal body number and structure
Dahyana Arias Escayola
,
Dahyana Arias Escayola
*
(Conceptualization, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft)
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
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Chuyue Zhang
,
Chuyue Zhang
*
(Conceptualization, Formal analysis, Investigation, Validation, Visualization, Writing - review & editing)
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
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Emily Nischwitz
,
Emily Nischwitz
(Formal analysis, Investigation, Visualization)
2
Institute of Molecular Biology (IMB)
, Mainz, Germany
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Leonard Schärfen
,
Leonard Schärfen
(Formal analysis, Software, Visualization)
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
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Kerstin Dörner
,
Kerstin Dörner
(Resources)
3Department of Biology,
Institute of Biochemistry, ETH Zürich
, Zürich, Switzerland
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Korinna Straube
,
Korinna Straube
(Investigation, Methodology, Validation)
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
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Ulrike Kutay
,
Ulrike Kutay
(Resources)
3Department of Biology,
Institute of Biochemistry, ETH Zürich
, Zürich, Switzerland
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Falk Butter
,
Falk Butter
(Data curation, Supervision, Writing - review & editing)
2
Institute of Molecular Biology (IMB)
, Mainz, Germany
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Karla M. Neugebauer
(Conceptualization, Data curation, Funding acquisition, Project administration, Resources, Supervision, Writing - original draft, Writing - review & editing)
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
Correspondence to Karla M. Neugebauer: [email protected]
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Dahyana Arias Escayola
Conceptualization, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft
*
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
Chuyue Zhang
Conceptualization, Formal analysis, Investigation, Validation, Visualization, Writing - review & editing
*
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
Emily Nischwitz
Formal analysis, Investigation, Visualization
2
Institute of Molecular Biology (IMB)
, Mainz, Germany
Leonard Schärfen
Formal analysis, Software, Visualization
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
Kerstin Dörner
Resources
3Department of Biology,
Institute of Biochemistry, ETH Zürich
, Zürich, Switzerland
Korinna Straube
Investigation, Methodology, Validation
1Department of Molecular Biophysics and Biochemistry,
Yale University
, New Haven, CT, USA
Ulrike Kutay
Resources
3Department of Biology,
Institute of Biochemistry, ETH Zürich
, Zürich, Switzerland
Falk Butter
Data curation, Supervision, Writing - review & editing
2
Institute of Molecular Biology (IMB)
, Mainz, Germany
Correspondence to Karla M. Neugebauer: [email protected]
*
D. Arias Escayola and C. Zhang contributed equally to this paper.
Disclosures: The authors declare no competing interests exist.
Received:
May 18 2023
Revision Received:
October 13 2024
Accepted:
November 04 2024
Online ISSN: 1540-8140
Print ISSN: 0021-9525
Funder(s):
National Cancer Institute
Funder(s):
National Institutes of Health
- Award Id(s): P30 CA016359,S10 OD023598,U01CA200147 TCPA-2017-Neugebauer and OPAS,R01NS128358-01
© 2024 Arias Escayola et al.
2024
Arias-Escayola et al.
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
This work is licensed under a
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License
.
J Cell Biol (2025) 224 (2): e202305081.
Article history
Received:
May 18 2023
Revision Received:
October 13 2024
Accepted:
November 04 2024
Connected Content
Citation
Dahyana Arias Escayola, Chuyue Zhang, Emily Nischwitz, Leonard Schärfen, Kerstin Dörner, Korinna Straube, Ulrike Kutay, Falk Butter, Karla M. Neugebauer; Identification of coilin interactors reveals coordinated control of Cajal body number and structure. J Cell Biol 3 February 2025; 224 (2): e202305081. doi: https://doi.org/10.1083/jcb.202305081
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