Literature DB >> 26410847

Single-cell protein dynamics reproduce universal fluctuations in cell populations.

Naama Brenner1,2, Erez Braun3,4, Anna Yoney5, Lee Susman6, James Rotella5, Hanna Salman7,8.   

Abstract

Protein variability in single cells has been studied extensively in populations, but little is known about temporal protein fluctuations in a single cell over extended times. We present here traces of protein copy number measured in individual bacteria over multiple generations and investigate their statistical properties, comparing them to previously measured population snapshots. We find that temporal fluctuations in individual cells exhibit the same properties as those previously observed in populations. Scaled fluctuations around the mean of each trace exhibit the universal distribution shape measured in populations under a wide range of conditions and in two distinct microorganisms; the mean and variance of the traces over time obey the same quadratic relation. Analyzing the individual protein traces reveals that within a cell cycle protein content increases exponentially, with a rate that varies from cycle to cycle. This leads to a compact description of the trace as a 3-variable stochastic process -exponential rate, cell cycle duration and value at the cycle start- sampled once a cycle. This description is sufficient to reproduce both universal statistical properties of the protein fluctuations. Our results show that the protein distribution shape is insensitive to sub-cycle intracellular microscopic details and reflects global cellular properties that fluctuate between generations.

Keywords:  Living systems: Biological networks

Mesh:

Substances:

Year:  2015        PMID: 26410847     DOI: 10.1140/epje/i2015-15102-8

Source DB:  PubMed          Journal:  Eur Phys J E Soft Matter        ISSN: 1292-8941            Impact factor:   1.890


  33 in total

1.  The effects of molecular noise and size control on variability in the budding yeast cell cycle.

Authors:  Stefano Di Talia; Jan M Skotheim; James M Bean; Eric D Siggia; Frederick R Cross
Journal:  Nature       Date:  2007-08-23       Impact factor: 49.962

2.  Noisy cell growth rate leads to fluctuating protein concentration in bacteria.

Authors:  Saburo Tsuru; Junya Ichinose; Akiko Kashiwagi; Bei-Wen Ying; Kunihiko Kaneko; Tetsuya Yomo
Journal:  Phys Biol       Date:  2009-06-30       Impact factor: 2.583

3.  Scaling laws governing stochastic growth and division of single bacterial cells.

Authors:  Srividya Iyer-Biswas; Charles S Wright; Jonathan T Henry; Klevin Lo; Stanislav Burov; Yihan Lin; Gavin E Crooks; Sean Crosson; Aaron R Dinner; Norbert F Scherer
Journal:  Proc Natl Acad Sci U S A       Date:  2014-10-27       Impact factor: 11.205

4.  Cellular noise regulons underlie fluctuations in Saccharomyces cerevisiae.

Authors:  Jacob Stewart-Ornstein; Jonathan S Weissman; Hana El-Samad
Journal:  Mol Cell       Date:  2012-02-24       Impact factor: 17.970

5.  Universality in stochastic exponential growth.

Authors:  Srividya Iyer-Biswas; Gavin E Crooks; Norbert F Scherer; Aaron R Dinner
Journal:  Phys Rev Lett       Date:  2014-07-07       Impact factor: 9.161

6.  Predicting stochastic gene expression dynamics in single cells.

Authors:  Jerome T Mettetal; Dale Muzzey; Juan M Pedraza; Ertugrul M Ozbudak; Alexander van Oudenaarden
Journal:  Proc Natl Acad Sci U S A       Date:  2006-04-28       Impact factor: 11.205

Review 7.  Functional roles for noise in genetic circuits.

Authors:  Avigdor Eldar; Michael B Elowitz
Journal:  Nature       Date:  2010-09-09       Impact factor: 49.962

Review 8.  Nature, nurture, or chance: stochastic gene expression and its consequences.

Authors:  Arjun Raj; Alexander van Oudenaarden
Journal:  Cell       Date:  2008-10-17       Impact factor: 41.582

9.  Collective dynamics of gene expression in cell populations.

Authors:  Elad Stolovicki; Erez Braun
Journal:  PLoS One       Date:  2011-06-15       Impact factor: 3.240

10.  Slow protein fluctuations explain the emergence of growth phenotypes and persistence in clonal bacterial populations.

Authors:  Andrea Rocco; Andrzej M Kierzek; Johnjoe McFadden
Journal:  PLoS One       Date:  2013-01-29       Impact factor: 3.240

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  13 in total

1.  Effects of cell cycle variability on lineage and population measurements of messenger RNA abundance.

Authors:  Ruben Perez-Carrasco; Casper Beentjes; Ramon Grima
Journal:  J R Soc Interface       Date:  2020-07-08       Impact factor: 4.118

2.  Mechanical bounds to transcriptional noise.

Authors:  Stuart A Sevier; David A Kessler; Herbert Levine
Journal:  Proc Natl Acad Sci U S A       Date:  2016-11-22       Impact factor: 11.205

3.  Protein concentration fluctuations in the high expression regime: Taylor's law and its mechanistic origin.

Authors:  Alberto Stefano Sassi; Mayra Garcia-Alcala; Maximino Aldana; Yuhai Tu
Journal:  Phys Rev X       Date:  2022-03-17       Impact factor: 14.417

4.  Threshold accumulation of a constitutive protein explains E. coli cell-division behavior in nutrient upshifts.

Authors:  Mia Panlilio; Jacopo Grilli; Giorgio Tallarico; Ilaria Iuliani; Bianca Sclavi; Pietro Cicuta; Marco Cosentino Lagomarsino
Journal:  Proc Natl Acad Sci U S A       Date:  2021-05-04       Impact factor: 11.205

5.  Making sense of snapshot data: ergodic principle for clonal cell populations.

Authors:  Philipp Thomas
Journal:  J R Soc Interface       Date:  2017-11       Impact factor: 4.118

6.  Cellular function given parametric variation in the Hodgkin and Huxley model of excitability.

Authors:  Hillel Ori; Eve Marder; Shimon Marom
Journal:  Proc Natl Acad Sci U S A       Date:  2018-08-15       Impact factor: 11.205

7.  Individuality and slow dynamics in bacterial growth homeostasis.

Authors:  Lee Susman; Maryam Kohram; Harsh Vashistha; Jeffrey T Nechleba; Hanna Salman; Naama Brenner
Journal:  Proc Natl Acad Sci U S A       Date:  2018-06-05       Impact factor: 11.205

8.  Non-genetic inheritance restraint of cell-to-cell variation.

Authors:  Harsh Vashistha; Maryam Kohram; Hanna Salman
Journal:  Elife       Date:  2021-02-01       Impact factor: 8.140

9.  Phenotypic delay in the evolution of bacterial antibiotic resistance: Mechanistic models and their implications.

Authors:  Martín Carballo-Pacheco; Michael D Nicholson; Elin E Lilja; Rosalind J Allen; Bartlomiej Waclaw
Journal:  PLoS Comput Biol       Date:  2020-05-29       Impact factor: 4.475

10.  Homeostasis of protein and mRNA concentrations in growing cells.

Authors:  Jie Lin; Ariel Amir
Journal:  Nat Commun       Date:  2018-10-29       Impact factor: 14.919

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