Reversible and Noisy Progression towards a Commitment Point Enables Adaptable and Reliable Cellular Decision-Making
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{"title"=>"Reversible and noisy progression towards a commitment point enables adaptable and reliable cellular Decision-Making", "type"=>"journal", "authors"=>[{"first_name"=>"Anna", "last_name"=>"Kuchina", "scopus_author_id"=>"54395518200"}, {"first_name"=>"Lorena", "last_name"=>"Espinar", "scopus_author_id"=>"54395244100"}, {"first_name"=>"Jordi", "last_name"=>"Garcia-Ojalvo", "scopus_author_id"=>"55931225400"}, {"first_name"=>"Gürol M.", "last_name"=>"Süel", "scopus_author_id"=>"6508114026"}], "year"=>2011, "source"=>"PLoS Computational Biology", "identifiers"=>{"pui"=>"362947802", "sgr"=>"81355164151", "pmid"=>"22102806", "scopus"=>"2-s2.0-81355164151", "isbn"=>"1553-7358 (Electronic)\\r1553-734X (Linking)", "doi"=>"10.1371/journal.pcbi.1002273", "issn"=>"1553734X"}, "id"=>"d9139b77-b4eb-3e26-8cf4-fa8068ed7059", "abstract"=>"Author Summary\\n Cells must continuously make decisions in response to changes in their environment. These decisions must be irreversible, to prevent cells from reverting back to unfit cellular states, but also be flexible, to allow cells to go back to their previous state upon environmental changes. Using single-cell time-lapse fluorescence microscopy, we show that these seemingly contradictory properties coexist in Bacillus subtilis cells during their progression to spore formation. We suggest, on the basis of a mathematical population model, that reversible progression towards the irreversible decision to sporulate optimizes respectively adaptability and reliability of decision-making over a broad range of changes in environmental conditions.", "link"=>"http://www.mendeley.com/research/reversible-noisy-progression-towards-commitment-point-enables-adaptable-reliable-cellular-decisionma", "reader_count"=>87, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Librarian"=>1, "Researcher"=>24, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Librarian"=>1, "Researcher"=>24, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>9, "Other"=>1, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>5}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>7, "Mathematics"=>3, "Agricultural and Biological Sciences"=>52, "Medicine and Dentistry"=>2, "Philosophy"=>1, "Neuroscience"=>1, "Physics and Astronomy"=>6, "Psychology"=>1, "Social Sciences"=>1, "Computer Science"=>7}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>6}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>52}, "Computer Science"=>{"Computer Science"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Mathematics"=>{"Mathematics"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "United States"=>4, "United Kingdom"=>3, "Slovakia"=>1, "Portugal"=>1, "Spain"=>2}, "group_count"=>7}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/713447"], "description"=>"<p><i>(A)</i> Filmstrips of phase and fluorescence image overlays of sporulating <i>B. subtilis</i> cells expressing pair-wise combinations of fluorescent proteins. For all panels, CFP fluorescence expressed from the P<sub>spoIIR</sub> promoter is colored in green. In the same cells, YFP is expressed from the P<i><sub>spo0A</sub></i> promoter (upper panel, blue), from the P<i><sub>spo0F</sub></i> promoter (middle panel, red), and as a translational fusion to SpoIIE protein (lower panel, orange). Time is indicated in hours. <i>(B)</i> Mean quantitative time traces of sporulation reporters during typical sporulation events. Dynamics of the reporters were obtained from strains expressing pair-wise combinations of indicated sporulation reporters (strains 0A-IIR, n = 33; 0F-IIR, n = 30; IIE-IIR, n = 28; strain definitions and genetic background can be found in Supporting <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002273#pcbi.1002273.s007\" target=\"_blank\">Text S2</a> and Supporting <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002273#pcbi.1002273.s004\" target=\"_blank\">Table S1</a>) and aligned in time with respect to activation of the common P<i><sub>spoIIR</sub></i> reporter (defined by P<i><sub>spoIIR</sub></i> fluorescence higher than 70% of maximum P<i><sub>spoIIR</sub></i> fluorescence at sporulation). Activities of all reporters were measured as mean fluorescence intensities in single cells. All traces have been normalized for amplitude. Dashed lines above and below the mean curves indicate standard deviation (SD). See also Supporting <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002273#pcbi.1002273.s001\" target=\"_blank\">Fig. S1</a>. <i>(C)</i> Scheme representing the temporal sequence of cellular states during the progression to sporulation, summarizing data from the plot shown in (<i>B</i>).</p>", "links"=>[], "tags"=>["sporulation", "activities", "progression", "spore"], "article_id"=>383813, "categories"=>["Biological Sciences", "Genetics"], "users"=>["Anna Kuchina", "Lorena Espinar", "Jordi García-Ojalvo", "Gürol M. Süel"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002273.g001", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Reversibility_of_sporulation_component_activities_during_the_progression_to_spore_formation_/383813", "title"=>"Reversibility of sporulation component activities during the progression to spore formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-10 01:03:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/361696", "https://ndownloader.figshare.com/files/361744", "https://ndownloader.figshare.com/files/361788", "https://ndownloader.figshare.com/files/361831", "https://ndownloader.figshare.com/files/361879", "https://ndownloader.figshare.com/files/361911", "https://ndownloader.figshare.com/files/361984"], "description"=>"<div><p>Cells must make reliable decisions under fluctuating extracellular conditions, but also be flexible enough to adapt to such changes. How cells reconcile these seemingly contradictory requirements through the dynamics of cellular decision-making is poorly understood. To study this issue we quantitatively measured gene expression and protein localization in single cells of the model organism <em>Bacillus subtilis</em> during the progression to spore formation. We found that sporulation proceeded through noisy and reversible steps towards an irreversible, all-or-none commitment point. Specifically, we observed cell-autonomous and spontaneous bursts of gene expression and transient protein localization events during sporulation. Based on these measurements we developed mathematical population models to investigate how the degree of reversibility affects cellular decision-making. In particular, we evaluated the effect of reversibility on the 1) reliability in the progression to sporulation, and 2) adaptability under changing extracellular stress conditions. Results show that reversible progression allows cells to remain responsive to long-term environmental fluctuations. In contrast, the irreversible commitment point supports reliable execution of cell fate choice that is robust against short-term reductions in stress. This combination of opposite dynamic behaviors (reversible and irreversible) thus maximizes both adaptable and reliable decision-making over a broad range of changes in environmental conditions. These results suggest that decision-making systems might employ a general hybrid strategy to cope with unpredictably fluctuating environmental conditions.</p> </div>", "links"=>[], "tags"=>["reversible", "noisy", "progression", "enables", "adaptable", "cellular", "decision-making"], "article_id"=>131499, "categories"=>["Biological Sciences", "Genetics"], "users"=>["Anna Kuchina", "Lorena Espinar", "Jordi García-Ojalvo", "Gürol M. Süel"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1002273.s001", "https://dx.doi.org/10.1371/journal.pcbi.1002273.s002", "https://dx.doi.org/10.1371/journal.pcbi.1002273.s003", "https://dx.doi.org/10.1371/journal.pcbi.1002273.s004", "https://dx.doi.org/10.1371/journal.pcbi.1002273.s005", "https://dx.doi.org/10.1371/journal.pcbi.1002273.s006", "https://dx.doi.org/10.1371/journal.pcbi.1002273.s007"], "stats"=>{"downloads"=>59, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Reversible_and_Noisy_Progression_towards_a_Commitment_Point_Enables_Adaptable_and_Reliable_Cellular_Decision_Making/131499", "title"=>"Reversible and Noisy Progression towards a Commitment Point Enables Adaptable and Reliable Cellular Decision-Making", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-11-10 00:24:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/713622"], "description"=>"<p><i>(A)</i> Filmstrips showing fluorescence (top) and phase (bottom) images of a sample sporulating cell (strain 0A-IIR) activating P<i><sub>spoIIR</sub></i> expression in the forespore (green). Phase bright spore appearance is indicated by an arrow. <i>(B)</i> Histogram presenting, in green, the distribution of time between P<i><sub>spoIIR</sub></i> activation and phase bright spore formation (n = 31, sample events highlighted by yellow boxes in the filmstrips in panel (A)), compared to sample cell cycle durations, in light grey, measured in the same cells under movie-making conditions. P<i><sub>spoIIR</sub></i> activation is measured as >60% of maximum P<i><sub>spoIIR</sub></i> fluorescence at sporulation.</p>", "links"=>[], "tags"=>["activation", "spore"], "article_id"=>383986, "categories"=>["Biological Sciences", "Genetics"], "users"=>["Anna Kuchina", "Lorena Espinar", "Jordi García-Ojalvo", "Gürol M. Süel"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002273.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Precise_timing_of_P_spoIIR_activation_prior_to_spore_formation_/383986", "title"=>"Precise timing of P<i><sub>spoIIR</sub></i> activation prior to spore formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-10 01:06:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/713563"], "description"=>"<p><i>(A)</i> 0A(5x)-IIR strain with P<i><sub>spo0A</sub></i>-CFP (blue) and P<i><sub>spoIIR</sub></i>-YFP (green). <i>(B)</i> 0F-IIR strain with P<i><sub>spo0F</sub></i>-YFP (red) and P<i><sub>spoIIR</sub></i>-CFP (green). <i>(C)</i> IIE-IIR strain showing localization of fusion protein SpoIIE-YFP (orange) and P<i><sub>spoIIR</sub></i>-CFP (green). For SpoIIE-YFP, local fluorescence measurements near the cell poles are shown. On top of each panel, cell images are shown at sample time points. The measured cell is indicated with a yellow outline.</p>", "links"=>[], "tags"=>["quantitative", "traces", "normalized", "fluorescence", "signals", "sporulation", "activities"], "article_id"=>383922, "categories"=>["Biological Sciences", "Genetics"], "users"=>["Anna Kuchina", "Lorena Espinar", "Jordi García-Ojalvo", "Gürol M. Süel"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002273.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Smoothed_quantitative_time_traces_of_normalized_fluorescence_signals_reporting_sporulation_component_activities_in_single_cells_/383922", "title"=>"Smoothed quantitative time traces of normalized fluorescence signals reporting sporulation component activities in single cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-10 01:05:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/713685"], "description"=>"<p><i>(A)</i> Schematic representation of the three models.<u><i>Irreversible-only</i></u>, top panel: Decision to sporulate is made by cells in a single step. The model comprises three cellular states: vegetative (V), decided (D) and spores (S). <i><u>Reversible-only</u></i>, middle panel: In this model vegetative cells (V) proceed toward sporulation through two intermediate states I<sub>1</sub> and I<sub>2</sub>. All transitions, including the transition to the decided state (D), are reversible. <i><u>Hybrid</u></i>, lower panel: This model combines characteristics from the two mechanisms described above. In this scenario, cells initially progress toward sporulation through intermediate states I<sub>1</sub> and I<sub>2</sub> with reversible transitions, with the irreversible final transition to the decided state (D). For all models the transition rates between sporulation stages, as well as growth and death (Ø) rates, are coupled to the stress level. For details, see Supporting <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002273#pcbi.1002273.s006\" target=\"_blank\">Text S1</a>. <i>(B)</i> Relative fitness of the hybrid model with respect to the irreversible-only and reversible-only models described in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002273#pcbi-1002273-g003\" target=\"_blank\">Fig. 3<i>A</i></a>. The blue and red lines correspond to the ratio of the total cell populations (summed over all cell states) of the hybrid model and the irreversible-only and reversible-only models, respectively. A random dichotomic variation of the environment is applied to all models, with the relative average duration of high versus low stress phases increasing in the x axis. The two insets depict sample profiles of stress for relative average durations of high stress phase equal to 0.2 and 0.8. The shaded areas in light blue and light red represent the maximum variation resulting from simultaneous random changes in all non-zero parameters of up to 20% around their baseline values given in Supporting <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002273#pcbi.1002273.s005\" target=\"_blank\">Table S2</a>. <i>(C)</i> Average fitness of the hybrid model with respect to the irreversible-only and reversible-only models obtained from a random sampling of environmental conditions. The inset shows short sample series of the average stress levels used to study the response of the three models to random stress conditions. Relative stress durations where chosen from a uniform random distribution in the range [0, 1]. The blue and red bars represent the ratio of the total cell population of the hybrid model to that of irreversible-only and reversible-only, respectively, averaged over 100 values of the relative average duration of high versus low stress scanned in (<i>B</i>). For each stress level, the models were integrated over 30 hours, in the same conditions as in (<i>B</i>). The error bars represent the maximum variation resulting from parameter changes up to 20% their baseline values, as in (<i>B</i>).</p>", "links"=>[], "tags"=>["cell-fate", "alternating"], "article_id"=>384053, "categories"=>["Biological Sciences", "Genetics"], "users"=>["Anna Kuchina", "Lorena Espinar", "Jordi García-Ojalvo", "Gürol M. Süel"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002273.g004", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mathematical_comparison_of_distinct_cell_fate_choice_dynamics_under_alternating_environmental_conditions_/384053", "title"=>"Mathematical comparison of distinct cell-fate choice dynamics under alternating environmental conditions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-10 01:07:33"}

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