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      Catalytic growth in a shared enzyme pool ensures robust control of centrosome size

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          Abstract

          Accurate regulation of centrosome size is essential for ensuring error-free cell division, and dysregulation of centrosome size has been linked to various pathologies, including developmental defects and cancer. While a universally accepted model for centrosome size regulation is lacking, prior theoretical and experimental works suggest a centrosome growth model involving autocatalytic assembly of the pericentriolar material. Here, we show that the autocatalytic assembly model fails to explain the attainment of equal centrosome sizes, which is crucial for error-free cell division. Incorporating latest experimental findings into the molecular mechanisms governing centrosome assembly, we introduce a new quantitative theory for centrosome growth involving catalytic assembly within a shared pool of enzymes. Our model successfully achieves robust size equality between maturing centrosome pairs, mirroring cooperative growth dynamics observed in experiments. To validate our theoretical predictions, we compare them with available experimental data and demonstrate the broad applicability of the catalytic growth model across different organisms, which exhibit distinct growth dynamics and size scaling characteristics.

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          Most cited references53

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          Exact stochastic simulation of coupled chemical reactions

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            Centrosome function and assembly in animal cells.

            It has become clear that the role of centrosomes extends well beyond that of important microtubule organizers. There is increasing evidence that they also function as coordination centres in eukaryotic cells, at which specific cytoplasmic proteins interact at high concentrations and important cell decisions are made. Accordingly, hundreds of proteins are concentrated at centrosomes, including cell cycle regulators, checkpoint proteins and signalling molecules. Nevertheless, several observations have raised the question of whether centrosomes are essential for many cell processes. Recent findings have shed light on the functions of centrosomes in animal cells and on the molecular mechanisms of centrosome assembly, in particular during mitosis. These advances should ultimately allow the in vitro reconstitution of functional centrosomes from their component proteins to unlock the secrets of these enigmatic organelles.
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              BioNumbers—the database of key numbers in molecular and cell biology

              BioNumbers (http://www.bionumbers.hms.harvard.edu) is a database of key numbers in molecular and cell biology—the quantitative properties of biological systems of interest to computational, systems and molecular cell biologists. Contents of the database range from cell sizes to metabolite concentrations, from reaction rates to generation times, from genome sizes to the number of mitochondria in a cell. While always of importance to biologists, having numbers in hand is becoming increasingly critical for experimenting, modeling, and analyzing biological systems. BioNumbers was motivated by an appreciation of how long it can take to find even the simplest number in the vast biological literature. All numbers are taken directly from a literature source and that reference is provided with the number. BioNumbers is designed to be highly searchable and queries can be performed by keywords or browsed by menus. BioNumbers is a collaborative community platform where registered users can add content and make comments on existing data. All new entries and commentary are curated to maintain high quality. Here we describe the database characteristics and implementation, demonstrate its use, and discuss future directions for its development.

                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                19 February 2025
                2025
                : 12
                : RP92203
                Affiliations
                [1 ] Department of Physics, Carnegie Mellon University ( https://ror.org/05x2bcf33) Pittsburgh United States
                [2 ] James Franck Institute, University of Chicago ( https://ror.org/024mw5h28) Chicago United States
                [3 ] School of Physics, Georgia Institute of Technology ( https://ror.org/01zkghx44) Atlanta United States
                Weizmann Institute of Science ( https://ror.org/0316ej306) Israel
                École Normale Supérieure - PSL ( https://ror.org/05a0dhs15) France
                Weizmann Institute of Science Israel
                University of Chicago Chicago United States
                Georgia Institute of Technology Atlanta United States
                Author information
                https://orcid.org/0000-0003-4452-7982
                https://orcid.org/0000-0001-8000-2556
                Article
                92203
                10.7554/eLife.92203
                11839165
                39968956
                479387be-a6f1-41fd-8fd3-3ceb1c795b93
                © 2023, Banerjee and Banerjee

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 31 August 2023
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: NIH R35 GM143042
                Award Recipient :
                Funded by: David Scaife Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: NSF MCB-2203601
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Cell Biology
                Physics of Living Systems
                Custom metadata
                A catalytic growth model in a shared enzyme pool explains robust centrosome size equality and size scaling, offering a unifying model for centrosome maturation dynamics across diverse organisms.
                prc

                Life sciences
                centrosome size,centrosome maturation,catalytic growth,pericentriolar material,cooperative growth,theory and modeling,c. elegans,d. melanogaster

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