Age-Dependent Transition from Cell-Level to Population-Level Control in Murine Intestinal Homeostasis Revealed by Coalescence Analysis
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{"title"=>"Age-Dependent Transition from Cell-Level to Population-Level Control in Murine Intestinal Homeostasis Revealed by Coalescence Analysis", "type"=>"journal", "authors"=>[{"first_name"=>"Zheng", "last_name"=>"Hu", "scopus_author_id"=>"57199834660"}, {"first_name"=>"Yun Xin", "last_name"=>"Fu", "scopus_author_id"=>"7404433708"}, {"first_name"=>"Anthony J.", "last_name"=>"Greenberg", "scopus_author_id"=>"7201858927"}, {"first_name"=>"Chung I.", "last_name"=>"Wu", "scopus_author_id"=>"8053335200"}, {"first_name"=>"Weiwei", "last_name"=>"Zhai", "scopus_author_id"=>"22735827300"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-84874762821", "sgr"=>"84874762821", "issn"=>"15537390", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"23468655", "doi"=>"10.1371/journal.pgen.1003326", "pui"=>"368490544"}, "id"=>"4a018cd6-e7dd-3874-ae5d-b918080cd07f", "abstract"=>"In multi-cellular organisms, tissue homeostasis is maintained by an exquisite balance between stem cell proliferation and differentiation. This equilibrium can be achieved either at the single cell level (a.k.a. cell asymmetry), where stem cells follow strict asymmetric divisions, or the population level (a.k.a. population asymmetry), where gains and losses in individual stem cell lineages are randomly distributed, but the net effect is homeostasis. In the mature mouse intestinal crypt, previous evidence has revealed a pattern of population asymmetry through predominantly symmetric divisions of stem cells. In this work, using population genetic theory together with previously published crypt single-cell data obtained at different mouse life stages, we reveal a strikingly dynamic pattern of stem cell homeostatic control. We find that single-cell asymmetric divisions are gradually replaced by stochastic population-level asymmetry as the mouse matures to adulthood. This lifelong process has important developmental and evolutionary implications in understanding how adult tissues maintain their homeostasis integrating the trade-off between intrinsic and extrinsic regulations.", "link"=>"http://www.mendeley.com/research/agedependent-transition-celllevel-populationlevel-control-murine-intestinal-homeostasis-revealed-coa", "reader_count"=>34, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Mathematics"=>3, "Agricultural and Biological Sciences"=>21, "Medicine and Dentistry"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Mathematics"=>{"Mathematics"=>3}}, "reader_count_by_country"=>{"Republic of Singapore"=>1, "United States"=>2, "United Kingdom"=>2, "Germany"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1005711"], "description"=>"*<p>: significant at 5% level,</p>**<p>: significant at 1% level.</p>", "links"=>[], "tags"=>["genetics and genomics", "developmental biology", "Evolutionary biology"], "article_id"=>666331, "categories"=>["Genetics", "Developmental Biology", "Evolutionary Biology"], "users"=>["Zheng Hu", "Yun-Xin Fu", "Anthony J. Greenberg", "Chung-I Wu", "Weiwei Zhai"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003326.t002", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Likelihood_ratio_tests_under_different_models_/666331", "title"=>"Likelihood ratio tests under different models.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-28 01:45:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/1005727"], "description"=>"a<p>: estimated for each crypt.</p>b<p>: estimated for each mice.</p>c<p>: confidence interval calculated from the non-parametric bootstrap samples.</p>", "links"=>[], "tags"=>["estimates", "asymmetric"], "article_id"=>666350, "categories"=>["Genetics", "Developmental Biology", "Evolutionary Biology"], "users"=>["Zheng Hu", "Yun-Xin Fu", "Anthony J. Greenberg", "Chung-I Wu", "Weiwei Zhai"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003326.t001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maximum_likelihood_estimates_asymmetric_division_rate_/666350", "title"=>"Maximum-likelihood estimates asymmetric division rate.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-28 01:45:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/973861"], "description"=>"<p>(A) The proportion of asymmetric and symmetric division as a function of mouse life stage. The pattern from morphogenesis are from experimental data together with the optimal control theory prediction <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003326#pgen.1003326-Itzkovitz1\" target=\"_blank\">[25]</a>. The lineage tracing evidences are from two earlier studies <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003326#pgen.1003326-LopezGarcia1\" target=\"_blank\">[23]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003326#pgen.1003326-Snippert1\" target=\"_blank\">[24]</a>. The transition from cell asymmetry to population asymmetry can take a variety of forms, including I) a fast switch similar to the Bang-Bang control, II) a linear accumulation, III) slow progression depending on the interplay between intrinsic and extrinsic signals. (B) When simulating crypt histories using curve I, II and III in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003326#pgen-1003326-g003\" target=\"_blank\">Figure 3A</a> and plotting mean pairwise divergence time between two random cells (a measurement of genealogical length), the average pairwise divergence shows very different trajectories under different transitional history.</p>", "links"=>[], "tags"=>["equilibrium"], "article_id"=>642096, "categories"=>["Genetics", "Developmental Biology", "Evolutionary Biology"], "users"=>["Zheng Hu", "Yun-Xin Fu", "Anthony J. Greenberg", "Chung-I Wu", "Weiwei Zhai"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003326.g003", "stats"=>{"downloads"=>0, "page_views"=>46, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lifelong_equilibrium_for_stem_cell_symmetric_asymmetric_divisions_/642096", "title"=>"Lifelong equilibrium for stem cell symmetric/asymmetric divisions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 12:20:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/973857"], "description"=>"<p>(A) Unweighted Pair Group Method with Arithmetic mean(UPGMA) tree <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003326#pgen.1003326-Sokal1\" target=\"_blank\">[66]</a> for the cells sampled from the two crypts at day 52. Distances were calculated using the two-step mutation model. (B) UPGMA tree for day 340. (C) Likelihood curve as a function of the proportion of asymmetric divisions for one of the crypts at day 52. (D) The same plot as panel C, but for the other crypt at day 52. (E) Likelihood curve as a function of the proportion of asymmetric divisions for one of the crypt at day 340. (F) The same plot as panel E, but for the other crypt at day 340. (G) Likelihood curve as a function of the proportion of asymmetric divisions for day 52 (combining two crypts). The horizontal dashed line marks the level of likelihood that is 1.92 units (0.5×) below the maximal value. The confidence interval (CI) for the proportion of asymmetric division rate is shown as the arrow between the two vertical dashed lines. (H). Likelihood curve as a function of the proportion of asymmetric divisions for day 340 (combining two crypts). The horizontal dashed line marks the level of likelihood that is 1.92 units below the maximal value. The confidence interval (CI) for the proportion of asymmetric division rate is shown as the arrow between the two vertical dashed lines. (I) A demonstration of the phenomena that the gene tree will increase in size as the crypt population reaches equilibrium (stationarity). The genealogical tree size (indicated as the mean pairwise divergence for two randomly picked cells) at different cell generation (generation 10, 30, 80 as well as equilibrium point) for the crypt population are shown (β = 0.4). The observed pairwise divergence for day 52 and day 340 are also plotted.</p>", "links"=>[], "tags"=>["relationships", "crypt", "cells", "asymmetric"], "article_id"=>642094, "categories"=>["Genetics", "Developmental Biology", "Evolutionary Biology"], "users"=>["Zheng Hu", "Yun-Xin Fu", "Anthony J. Greenberg", "Chung-I Wu", "Weiwei Zhai"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003326.g002", "stats"=>{"downloads"=>0, "page_views"=>52, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationships_for_the_crypt_single_cells_and_likelihood_curve_for_the_proportion_of_asymmetric_divisions_/642094", "title"=>"Phylogenetic relationships for the crypt single cells and likelihood curve for the proportion of asymmetric divisions.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 12:19:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/973855"], "description"=>"<p>(A) Anatomical structure of the intestinal crypt. The dark green cells represent stem cells and light green cells are transit-amplifying cells. There are three types of stem cells divisions (I, II and III, see main text). (B) A cartoon illustration of a coalescent process in the two deme model. One cell from stem cell deme and two cells from the transit-amplifying cell deme were sampled. Their ancestral relationship is depicted as the gene tree connecting their ancestors. (C) The state transition for the Markov Chain in one step. The current state of the chain is (m,n) and the state in the previous generation is (m′,n′). In the example here, (m,n) = (1,3) and (m′,n′) = (2,1). (D) The expected time to the most recent common ancestor for two lineages (denoted as TMRCA2) was calculated using three different approaches. The solid line is calculated using a first-step analysis of the Markov Chain. Blue squares are the results from the forward simulation and triangles are from the direct simulation following the Markov Chain.</p>", "links"=>[], "tags"=>["intestinal", "crypts", "coalescent", "processes", "two-deme"], "article_id"=>642091, "categories"=>["Genetics", "Developmental Biology", "Evolutionary Biology"], "users"=>["Zheng Hu", "Yun-Xin Fu", "Anthony J. Greenberg", "Chung-I Wu", "Weiwei Zhai"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003326.g001", "stats"=>{"downloads"=>0, "page_views"=>71, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Anatomy_of_intestinal_crypts_and_coalescent_processes_for_the_two_deme_model_/642091", "title"=>"Anatomy of intestinal crypts and coalescent processes for the two-deme model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-01 12:19:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/973866", "https://ndownloader.figshare.com/files/973869", "https://ndownloader.figshare.com/files/973871", "https://ndownloader.figshare.com/files/973873", "https://ndownloader.figshare.com/files/973875"], "description"=>"<div><p>In multi-cellular organisms, tissue homeostasis is maintained by an exquisite balance between stem cell proliferation and differentiation. This equilibrium can be achieved either at the single cell level (a.k.a. cell asymmetry), where stem cells follow strict asymmetric divisions, or the population level (a.k.a. population asymmetry), where gains and losses in individual stem cell lineages are randomly distributed, but the net effect is homeostasis. In the mature mouse intestinal crypt, previous evidence has revealed a pattern of population asymmetry through predominantly symmetric divisions of stem cells. In this work, using population genetic theory together with previously published crypt single-cell data obtained at different mouse life stages, we reveal a strikingly dynamic pattern of stem cell homeostatic control. We find that single-cell asymmetric divisions are gradually replaced by stochastic population-level asymmetry as the mouse matures to adulthood. This lifelong process has important developmental and evolutionary implications in understanding how adult tissues maintain their homeostasis integrating the trade-off between intrinsic and extrinsic regulations.</p> </div>", "links"=>[], "tags"=>["age-dependent", "cell-level", "population-level", "murine", "intestinal", "homeostasis", "revealed", "coalescence", "analysis"], "article_id"=>642099, "categories"=>["Genetics", "Developmental Biology", "Evolutionary Biology"], "users"=>["Zheng Hu", "Yun-Xin Fu", "Anthony J. Greenberg", "Chung-I Wu", "Weiwei Zhai"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003326.s001", "https://dx.doi.org/10.1371/journal.pgen.1003326.s002", "https://dx.doi.org/10.1371/journal.pgen.1003326.s003", "https://dx.doi.org/10.1371/journal.pgen.1003326.s004", "https://dx.doi.org/10.1371/journal.pgen.1003326.s005"], "stats"=>{"downloads"=>0, "page_views"=>48, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Age_Dependent_Transition_from_Cell_Level_to_Population_Level_Control_in_Murine_Intestinal_Homeostasis_Revealed_by_Coalescence_Analysis__/642099", "title"=>"Age-Dependent Transition from Cell-Level to Population-Level Control in Murine Intestinal Homeostasis Revealed by Coalescence Analysis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-03-01 12:21:52"}

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Relative Metric

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