Statistical theory of branching morphogenesis
Branching morphogenesis remains a subject of abiding interest. Although much is known about the gene regulatory programs and signaling pathways that operate at the cellular scale, it has remained unclear how the macroscopic features of branched organs, including their size, network topology and spat...
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| Veröffentlicht in: | Development, growth & differentiation Jg. 60; H. 9; S. 512 - 521 |
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| Format: | Journal Article |
| Sprache: | Englisch |
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Japan
Wiley Subscription Services, Inc
01.12.2018
John Wiley and Sons Inc |
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| ISSN: | 0012-1592, 1440-169X, 1440-169X |
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| Abstract | Branching morphogenesis remains a subject of abiding interest. Although much is known about the gene regulatory programs and signaling pathways that operate at the cellular scale, it has remained unclear how the macroscopic features of branched organs, including their size, network topology and spatial patterning, are encoded. Lately, it has been proposed that, these features can be explained quantitatively in several organs within a single unifying framework. Based on large‐scale organ reconstructions and cell lineage tracing, it has been argued that morphogenesis follows from the collective dynamics of sublineage‐restricted self‐renewing progenitor cells, localized at ductal tips, that act cooperatively to drive a serial process of ductal elongation and stochastic tip bifurcation. By correlating differentiation or cell cycle exit with proximity to maturing ducts, this dynamic results in the specification of a complex network of defined density and statistical organization. These results suggest that, for several mammalian tissues, branched epithelial structures develop as a self‐organized process, reliant upon a strikingly simple, but generic, set of local rules, without recourse to a rigid and deterministic sequence of genetically programmed events. Here, we review the basis of these findings and discuss their implications.
We review the basis of recent research activities that have developed and applied a unifying theory of branching morphogenesis in several mammalian tissues, including the mouse mammary gland epithelium, kidney and pancreas. We discuss the evidence in favor of the model, as well as the implications that these concepts have for the organization and function of ductal precursors. |
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| AbstractList | Branching morphogenesis remains a subject of abiding interest. Although much is known about the gene regulatory programs and signaling pathways that operate at the cellular scale, it has remained unclear how the macroscopic features of branched organs, including their size, network topology and spatial patterning, are encoded. Lately, it has been proposed that, these features can be explained quantitatively in several organs within a single unifying framework. Based on large-scale organ reconstructions and cell lineage tracing, it has been argued that morphogenesis follows from the collective dynamics of sublineage-restricted self-renewing progenitor cells, localized at ductal tips, that act cooperatively to drive a serial process of ductal elongation and stochastic tip bifurcation. By correlating differentiation or cell cycle exit with proximity to maturing ducts, this dynamic results in the specification of a complex network of defined density and statistical organization. These results suggest that, for several mammalian tissues, branched epithelial structures develop as a self-organized process, reliant upon a strikingly simple, but generic, set of local rules, without recourse to a rigid and deterministic sequence of genetically programmed events. Here, we review the basis of these findings and discuss their implications. Branching morphogenesis remains a subject of abiding interest. Although much is known about the gene regulatory programs and signaling pathways that operate at the cellular scale, it has remained unclear how the macroscopic features of branched organs, including their size, network topology and spatial patterning, are encoded. Lately, it has been proposed that, these features can be explained quantitatively in several organs within a single unifying framework. Based on large-scale organ reconstructions and cell lineage tracing, it has been argued that morphogenesis follows from the collective dynamics of sublineage-restricted self-renewing progenitor cells, localized at ductal tips, that act cooperatively to drive a serial process of ductal elongation and stochastic tip bifurcation. By correlating differentiation or cell cycle exit with proximity to maturing ducts, this dynamic results in the specification of a complex network of defined density and statistical organization. These results suggest that, for several mammalian tissues, branched epithelial structures develop as a self-organized process, reliant upon a strikingly simple, but generic, set of local rules, without recourse to a rigid and deterministic sequence of genetically programmed events. Here, we review the basis of these findings and discuss their implications.Branching morphogenesis remains a subject of abiding interest. Although much is known about the gene regulatory programs and signaling pathways that operate at the cellular scale, it has remained unclear how the macroscopic features of branched organs, including their size, network topology and spatial patterning, are encoded. Lately, it has been proposed that, these features can be explained quantitatively in several organs within a single unifying framework. Based on large-scale organ reconstructions and cell lineage tracing, it has been argued that morphogenesis follows from the collective dynamics of sublineage-restricted self-renewing progenitor cells, localized at ductal tips, that act cooperatively to drive a serial process of ductal elongation and stochastic tip bifurcation. By correlating differentiation or cell cycle exit with proximity to maturing ducts, this dynamic results in the specification of a complex network of defined density and statistical organization. These results suggest that, for several mammalian tissues, branched epithelial structures develop as a self-organized process, reliant upon a strikingly simple, but generic, set of local rules, without recourse to a rigid and deterministic sequence of genetically programmed events. Here, we review the basis of these findings and discuss their implications. Branching morphogenesis remains a subject of abiding interest. Although much is known about the gene regulatory programs and signaling pathways that operate at the cellular scale, it has remained unclear how the macroscopic features of branched organs, including their size, network topology and spatial patterning, are encoded. Lately, it has been proposed that, these features can be explained quantitatively in several organs within a single unifying framework. Based on large‐scale organ reconstructions and cell lineage tracing, it has been argued that morphogenesis follows from the collective dynamics of sublineage‐restricted self‐renewing progenitor cells, localized at ductal tips, that act cooperatively to drive a serial process of ductal elongation and stochastic tip bifurcation. By correlating differentiation or cell cycle exit with proximity to maturing ducts, this dynamic results in the specification of a complex network of defined density and statistical organization. These results suggest that, for several mammalian tissues, branched epithelial structures develop as a self‐organized process, reliant upon a strikingly simple, but generic, set of local rules, without recourse to a rigid and deterministic sequence of genetically programmed events. Here, we review the basis of these findings and discuss their implications. We review the basis of recent research activities that have developed and applied a unifying theory of branching morphogenesis in several mammalian tissues, including the mouse mammary gland epithelium, kidney and pancreas. We discuss the evidence in favor of the model, as well as the implications that these concepts have for the organization and function of ductal precursors. |
| Author | Hannezo, Edouard Simons, Benjamin D. |
| AuthorAffiliation | 3 Wellcome Trust Centre for Stem Cell Research University of Cambridge Cambridge UK 2 The Wellcome Trust/Cancer Research UK Gurdon Institute University of Cambridge Cambridge UK 4 Cavendish Laboratory Department of Physics University of Cambridge Cambridge UK 1 IST Austria Klosterneuburg Austria |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30357803$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1111_dgd_12590 crossref_primary_10_1016_j_cels_2024_10_005 crossref_primary_10_1016_j_semcdb_2021_07_001 crossref_primary_10_1016_j_bbagen_2023_130375 crossref_primary_10_1007_s00285_025_02189_x crossref_primary_10_1007_s10517_024_06292_9 crossref_primary_10_1088_1742_6596_1629_1_012029 crossref_primary_10_1089_scd_2021_0135 crossref_primary_10_1088_1478_3975_abd844 crossref_primary_10_1016_j_ceb_2019_07_001 |
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| Copyright | 2018 The Authors Development, Growth & Differentiation published by John Wiley & Sons Australia, Ltd on behalf of Japanese Society of Developmental Biologists 2018 The Authors Development, Growth & Differentiation published by John Wiley & Sons Australia, Ltd on behalf of Japanese Society of Developmental Biologists. 2018 Japanese Society of Developmental Biologists |
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| SubjectTerms | Animals biophysical concepts Cell cycle Cell Lineage Cell Proliferation Epithelial Cells - cytology Epithelium - growth & development Humans Kidney - cytology Kidney - growth & development mammary gland Models, Biological Morphogenesis Pancreas - cytology Pancreas - growth & development Progenitor cells Review statistical model Statistics stem cell Stem cells |
| Title | Statistical theory of branching morphogenesis |
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| Volume | 60 |
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