Cell size regulation and proliferation fluctuations in single-cell derived colonies

Exponentially growing cells regulate their size by controlling their timing of division. Since two daughter cells are born as a result of this cell splitting, cell size regulation has a direct connection with cell proliferation dynamics. Recent models found more clues about this connection by sugges...

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Main Authors:	Nieto, César, Vargas García, César, Pedraza, Juan Manuel, Singh, Abhyudai
Format:	article
Language:	Inglés
Published:	Cold Spring Harbor Laboratory 2024
Subjects:	Genética vegetal y fitomejoramiento - F30 Estructura celular Propiedades biológicas Proliferación Transversal http://aims.fao.org/aos/agrovoc/c_1414 http://aims.fao.org/aos/agrovoc/c_1501 http://aims.fao.org/aos/agrovoc/c_51dd9e80
Online Access:	https://www.biorxiv.org/content/10.1101/2022.07.05.498901v1 http://hdl.handle.net/20.500.12324/39376 https://doi.org/10.1101/2022.07.05.498901

id	RepoAGROSAVIA39376
record_format	dspace
institution	Corporación Colombiana de Investigación Agropecuaria
collection	Repositorio AGROSAVIA
language	Inglés
topic	Genética vegetal y fitomejoramiento - F30 Estructura celular Propiedades biológicas Proliferación Transversal http://aims.fao.org/aos/agrovoc/c_1414 http://aims.fao.org/aos/agrovoc/c_1501 http://aims.fao.org/aos/agrovoc/c_51dd9e80
spellingShingle	Genética vegetal y fitomejoramiento - F30 Estructura celular Propiedades biológicas Proliferación Transversal http://aims.fao.org/aos/agrovoc/c_1414 http://aims.fao.org/aos/agrovoc/c_1501 http://aims.fao.org/aos/agrovoc/c_51dd9e80 Nieto, César Vargas García, César Pedraza, Juan Manuel Singh, Abhyudai Cell size regulation and proliferation fluctuations in single-cell derived colonies
description	Exponentially growing cells regulate their size by controlling their timing of division. Since two daughter cells are born as a result of this cell splitting, cell size regulation has a direct connection with cell proliferation dynamics. Recent models found more clues about this connection by suggesting that division occurs at a size-dependent rate. In this article, we propose a framework that couples the stochastic transient dynamics of both the cell size and the number of cells in the initial expansion of a single-cell-derived colony. We describe the population from the two most common perspectives. The first is known as Single Lineage: where only one cell is followed in each colony, and the second is Population Snapshots: where all cells in different colonies are followed. At a low number of cells, we propose a third perspective; Single Colony, where one tracks only cells with a common ancestor. We observe how the statistics of these three approaches are different at low numbers and how the Single Colony perspective tends to Population Snapshots at high numbers. Analyzing colony-to-colony fluctuations in the number of cells, we report an intriguing find: the extent of fluctuations first increases with time and then decreases to approach zero at large numbers of cells. In contrast, in classical size-independent proliferation models, where cell division occurs based on a pure timing mechanism, fluctuations in cell number increase monotonically over time to approach a nonzero value. We systematically study these differences and the convergence speed using different size control strategies.
format	article
author	Nieto, César Vargas García, César Pedraza, Juan Manuel Singh, Abhyudai
author_facet	Nieto, César Vargas García, César Pedraza, Juan Manuel Singh, Abhyudai
author_sort	Nieto, César
title	Cell size regulation and proliferation fluctuations in single-cell derived colonies
title_short	Cell size regulation and proliferation fluctuations in single-cell derived colonies
title_full	Cell size regulation and proliferation fluctuations in single-cell derived colonies
title_fullStr	Cell size regulation and proliferation fluctuations in single-cell derived colonies
title_full_unstemmed	Cell size regulation and proliferation fluctuations in single-cell derived colonies
title_sort	cell size regulation and proliferation fluctuations in single-cell derived colonies
publisher	Cold Spring Harbor Laboratory
publishDate	2024
url	https://www.biorxiv.org/content/10.1101/2022.07.05.498901v1 http://hdl.handle.net/20.500.12324/39376 https://doi.org/10.1101/2022.07.05.498901
work_keys_str_mv	AT nietocesar cellsizeregulationandproliferationfluctuationsinsinglecellderivedcolonies AT vargasgarciacesar cellsizeregulationandproliferationfluctuationsinsinglecellderivedcolonies AT pedrazajuanmanuel cellsizeregulationandproliferationfluctuationsinsinglecellderivedcolonies AT singhabhyudai cellsizeregulationandproliferationfluctuationsinsinglecellderivedcolonies
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spelling	RepoAGROSAVIA393762024-05-23T03:02:01Z Cell size regulation and proliferation fluctuations in single-cell derived colonies Nieto, César Vargas García, César Pedraza, Juan Manuel Singh, Abhyudai Genética vegetal y fitomejoramiento - F30 Estructura celular Propiedades biológicas Proliferación Transversal http://aims.fao.org/aos/agrovoc/c_1414 http://aims.fao.org/aos/agrovoc/c_1501 http://aims.fao.org/aos/agrovoc/c_51dd9e80 Exponentially growing cells regulate their size by controlling their timing of division. Since two daughter cells are born as a result of this cell splitting, cell size regulation has a direct connection with cell proliferation dynamics. Recent models found more clues about this connection by suggesting that division occurs at a size-dependent rate. In this article, we propose a framework that couples the stochastic transient dynamics of both the cell size and the number of cells in the initial expansion of a single-cell-derived colony. We describe the population from the two most common perspectives. The first is known as Single Lineage: where only one cell is followed in each colony, and the second is Population Snapshots: where all cells in different colonies are followed. At a low number of cells, we propose a third perspective; Single Colony, where one tracks only cells with a common ancestor. We observe how the statistics of these three approaches are different at low numbers and how the Single Colony perspective tends to Population Snapshots at high numbers. Analyzing colony-to-colony fluctuations in the number of cells, we report an intriguing find: the extent of fluctuations first increases with time and then decreases to approach zero at large numbers of cells. In contrast, in classical size-independent proliferation models, where cell division occurs based on a pure timing mechanism, fluctuations in cell number increase monotonically over time to approach a nonzero value. We systematically study these differences and the convergence speed using different size control strategies. 2024-05-22T16:15:55Z 2024-05-22T16:15:55Z 2022-07-06 2022 article Artículo científico http://purl.org/coar/resource_type/c_2df8fbb1 info:eu-repo/semantics/article https://purl.org/redcol/resource_type/ART http://purl.org/coar/version/c_970fb48d4fbd8a85 https://www.biorxiv.org/content/10.1101/2022.07.05.498901v1 2692-8205 http://hdl.handle.net/20.500.12324/39376 https://doi.org/10.1101/2022.07.05.498901 reponame:Biblioteca Digital Agropecuaria de Colombia instname:Corporación colombiana de investigación agropecuaria AGROSAVIA eng BioRxiv 1 8 [1].↵ J. M. Raser and E. K. O’shea, “Noise in gene expression: origins, consequences, and control,” Science, vol. 309, no. 5743, pp. 2010–2013, 2005.Abstract/FREE Full TextGoogle Scholar [2]. D. A. Oyarzún, J.-B. Lugagne, and G.-B. V. Stan, “Noise propagation in synthetic gene circuits for metabolic control,” ACS synthetic biology, vol. 4, no. 2, pp. 116–125, 2015.Google Scholar [3].↵ M. Hashimoto, T. Nozoe, H. Nakaoka, R. Okura, S. Akiyoshi, K. Kaneko, E. Kussell, and Y. Wakamoto, “Noise-driven growth rate gain in clonal cellular populations,” Proceedings of the National Academy of Sciences, vol. 113, no. 12, pp. 3251–3256, 2016.Abstract/FREE Full TextGoogle Scholar [4].↵ J. Masel, “Genetic drift,” Current Biology, vol. 21, no. 20, pp. R837–R838, 2011.CrossRefPubMedGoogle Scholar [5].↵ D. A. Charlebois and G. Balázsi, “Modeling cell population dynamics,” In Silico Biology, vol. 13, no. 1-2, pp. 21–39, 2019 [6].↵ C. A. Gilligan and F. van den Bosch, “Epidemiological models for invasion and persistence of pathogens,” Annu. Rev. Phytopathol., vol. 46, pp. 385–418, 2008 [7].↵ F. Lyu, M. Pan, S. Patil, J.-H. Wang, A. Matin, J. R. Andrews, and S. K. Tang, “Phenotyping antibiotic resistance with single-cell resolution for the detection of heteroresistance,” Sensors and Actuators B: Chemical, vol. 270, pp. 396–404, 2018 [8].↵ R. Lande, S. Engen, B.-E. Saether, et al., Stochastic population dynamics in ecology and conservation. Oxford University Press on Demand, 2003. [9].↵ X. Guo, K. P. T. Silva, and J. Q. Boedicker, “Single-cell variability of growth interactions within a two-species bacterial community,” Physical Biology, vol. 16, no. 3, p. 036001, 2019 [10].↵ S. Abalde-Cela, A. Gould, X. Liu, E. Kazamia, A. G. Smith, and C. Abell, “High-throughput detection of ethanol-producing cyanobacteria in a microdroplet platform,” Journal of The Royal Society Interface, vol. 12, no. 106, p. 20150216, 2015. [11].↵ D. Volfson, J. Marciniak, W. J. Blake, N. Ostroff, L. S. Tsimring, and J. Hasty, “Origins of extrinsic variability in eukaryotic gene expression,” Nature, vol. 439, no. 7078, pp. 861–864, 2006 [12].↵ L. Robert, M. Hoffmann, N. Krell, S. Aymerich, J. Robert, and M. Doumic, “Division in escherichia coliis triggered by a size-sensing rather than a timing mechanism,” BMC biology, vol. 12, no. 1, pp. 1–10, 2014 [13]. J. Lin and A. Amir, “The effects of stochasticity at the single-cell level and cell size control on the population growth,” Cell systems, vol. 5, no. 4, pp. 358–367, 2017 [14].↵ C. Nieto, C. Vargas-Garcia, and J. M. Pedraza, “Continuous rate modeling of bacterial stochastic size dynamics,” Physical Review E, vol. 104, no. 4, p. 044415, 2021 [15]. P.-Y. Ho, J. Lin, and A. Amir, “Modeling cell size regulation: From single-cell-level statistics to molecular mechanisms and population-level effects,” Annual review of biophysics, vol. 47, pp. 251–271, 2018 [16]. S. Iyer-Biswas, C. S. Wright, J. T. Henry, K. Lo, S. Burov, Y. Lin, G. E. Crooks, S. Crosson, A. R. Dinner, and N. F. Scherer, “Scaling laws governing stochastic growth and division of single bacterial cells,” Proceedings of the National Academy of Sciences, vol. 111, no. 45, pp. 15912–15917, 2014 [17].↵ K. R. Ghusinga, C. A. Vargas-Garcia, and A. Singh, “A mechanistic stochastic framework for regulating bacterial cell division,” Scientific reports, vol. 6, no. 1, pp. 1–9, 2016 [18].↵ C. Nieto, J. Arias-Castro, C. Sánchez, C. Vargas-García, and J. M. Pedraza, “Unification of cell division control strategies through continuous rate models,” Physical Review E, vol. 101, no. 2, p. 022401, 2020 [19]. C. A. Vargas-Garcia, K. R. Ghusinga, and A. Singh, “Cell size control and gene expression homeostasis in single-cells,” Current opinion in systems biology, vol. 8, pp. 109–116, 2018. [20]. M. Basan, M. Zhu, X. Dai, M. Warren, D. Sévin, Y.-P. Wang, and T. Hwa, “Inflating bacterial cells by increased protein synthesis,” Molecular systems biology, vol. 11, no. 10, p. 836, 2015 [21].↵ F. Si, G. Le Treut, J. T. Sauls, S. Vadia, P. A. Levin, and S. Jun, “Mechanistic origin of cell-size control and homeostasis in bacteria,” Current Biology, vol. 29, no. 11, pp. 1760–1770, 2019 [22].↵ P. Wang, L. Robert, J. Pelletier, W. L. Dang, F. Taddei, A. Wright, and S. Jun, “Robust growth of escherichia coli,” Current biology, vol. 20, no. 12, pp. 1099–1103, 2010. [23].↵ G. Derfel, B. Van Brunt, and G. Wake, “A cell growth model revisited,” Oxford University Research Arhive, 2009. [24].↵ N. Totis, C. Nieto, A. Küper, C. Vargas-García, A. Singh, and S. Waldherr, “A population-based approach to study the effects of growth and division rates on the dynamics of cell size statistics,” IEEE Control Systems Letters, vol. 5, no. 2, pp. 725–730, 2020 [25].↵ C. A. Nieto-Acuna, C. A. Vargas-Garcia, A. Singh, and J. M. Pedraza, “Efficient computation of stochastic cell-size transient dynamics,” BMC bioinformatics, vol. 20, no. 23, pp. 1–6, 2019. [26].↵ C. Jia, A. Singh, and R. Grima, “Cell size distribution of lineage data: analytic results and parameter inference,” Iscience, vol. 24, no. 3, p. 102220, 2021 [27].↵ J. Lin and A. Amir, “Homeostasis of protein and mrna concentrations in growing cells,” Nature communications, vol. 9, no. 1, pp. 1–11, 2018 [28].↵ F. F. Mandy, M. Bergeron, and T. Minkus, “Principles of flow cytometry,” Transfusion science, vol. 16, no. 4, pp. 303–314, 1995 [29].↵ D. Taylor, N. Verdon, P. Lomax, R. J. Allen, and S. Titmuss, “Tracking the stochastic growth of bacterial populations in microfluidic droplets [30].↵ P. Thomas, “Intrinsic and extrinsic noise of gene expression in lineage trees,” Scientific reports, vol. 9, no. 1, pp. 1–16, 2019. [31].↵ G. I. Bell and E. C. Anderson, “Cell growth and division: I. a mathematical model with applications to cell volume distributions in mammalian suspension cultures,” Biophysical journal, vol. 7, no. 4, pp. 329–351, 1967 [32].↵ A. Barizien, M. Suryateja Jammalamadaka, G. Amselem, and C. N. Baroud, “Growing from a few cells: combined effects of initial stochasticity and cell-to-cell variability,” Journal of the Royal Society Interface, vol. 16, no. 153, p. 20180935, 2019. [33].↵ S. Modi, C. A. Vargas-Garcia, K. R. Ghusinga, and A. Singh, “Analysis of noise mechanisms in cell-size control,” Biophysical journal, vol. 112, no. 11, pp. 2408–2418, 2017 [34].↵ P. Thomas, “Making sense of snapshot data: ergodic principle for clonal cell populations,” Journal of The Royal Society Interface, vol. 14, no. 136, p. 20170467, 2017. [35].↵ P. Thomas, “Analysis of cell size homeostasis at the single-cell and population level,” Frontiers in Physics, vol. 6, p. 64, 2018. [36].↵ B. Munsky and M. Khammash, “The finite state projection algorithm for the solution of the chemical master equation,” The Journal of chemical physics, vol. 124, no. 4, p. 044104, 2006. [37].↵ B. Houchmandzadeh, “General formulation of luria-delbrück distribution of the number of mutants,” Physical Review E, vol. 92, no. 1, p. 012719, 2015. [38].↵ K. B. Athreya, P. E. Ney, and P. Ney, Branching processes. Courier Corporation, 2004 [39].↵ M. Osella, E. Nugent, and M. C. Lagomarsino, “Concerted control of escherichia coli cell division,” Proceedings of the National Academy of Sciences, vol. 111, no. 9, pp. 3431–3435, 2014. [40].↵ Z. Vahdat, Z. Xu, and A. Singh, “Modeling protein concentrations in cycling cells using stochastic hybrid systems,” IFAC-PapersOnLine, vol. 54, no. 9, pp. 521–526, 2021 [41].↵ E. Kussell, R. Kishony, N. Q. Balaban, and S. Leibler, “Bacterial persistence: a model of survival in changing environments,” Genetics, vol. 169, no. 4, pp. 1807–1814, 2005. 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Cell size regulation and proliferation fluctuations in single-cell derived colonies

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