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Proteome-scale Movements and Compartment Connectivity During the Eukaryotic Cell Cycle

Abstract

Cell cycle progression relies on coordinated changes in the composition and subcellular localization of the proteome. By applying two distinct convolutional neural networks on images of millions of live yeast cells, we resolved proteome-level dynamics in both concentration and localization during the cell cycle, with resolution of ∼20 subcellular localization classes. We show that a quarter of the proteome displays cell cycle periodicity, with proteins tending to be controlled either at the level of localization or concentration, but not both. Distinct levels of protein regulation are preferentially utilized for different aspects of the cell cycle, with changes in protein concentration being mostly involved in cell cycle control and changes in protein localization in the biophysical implementation of the cell cycle program. We present a resource for exploring global proteome dynamics during the cell cycle, which will aid in understanding a fundamental biological process at a systems level.

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References
1.
Tyers M, Tokiwa G, Futcher B . Comparison of the Saccharomyces cerevisiae G1 cyclins: Cln3 may be an upstream activator of Cln1, Cln2 and other cyclins. EMBO J. 1993; 12(5):1955-68. PMC: 413417. DOI: 10.1002/j.1460-2075.1993.tb05845.x. View

2.
Claus S, Jezierska S, Van Bogaert I . Protein-facilitated transport of hydrophobic molecules across the yeast plasma membrane. FEBS Lett. 2019; 593(13):1508-1527. DOI: 10.1002/1873-3468.13469. View

3.
Black L, Tollis S, Fu G, Fiche J, Dorsey S, Cheng J . G1/S transcription factors assemble in increasing numbers of discrete clusters through G1 phase. J Cell Biol. 2020; 219(9). PMC: 7480102. DOI: 10.1083/jcb.202003041. View

4.
Meitinger F, Richter H, Heisel S, Hub B, Seufert W, Pereira G . A safeguard mechanism regulates Rho GTPases to coordinate cytokinesis with the establishment of cell polarity. PLoS Biol. 2013; 11(2):e1001495. PMC: 3582507. DOI: 10.1371/journal.pbio.1001495. View

5.
Protchenko O, Rodriguez-Suarez R, Androphy R, Bussey H, Philpott C . A screen for genes of heme uptake identifies the FLC family required for import of FAD into the endoplasmic reticulum. J Biol Chem. 2006; 281(30):21445-21457. DOI: 10.1074/jbc.M512812200. View