Global Quantification of Tissue Dynamics in the Developing Mouse Kidney
Although kidneys of equal size can vary 10-fold in nephron number at birth, discovering what regulates such variation has been hampered by a lack of quantitative parameters defining kidney development. Here we report a comprehensive, quantitative, multiscale analysis of mammalian kidney development...
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Published in | Developmental cell Vol. 29; no. 2; pp. 188 - 202 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
28.04.2014
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Subjects | |
Online Access | Get full text |
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Abstract | Although kidneys of equal size can vary 10-fold in nephron number at birth, discovering what regulates such variation has been hampered by a lack of quantitative parameters defining kidney development. Here we report a comprehensive, quantitative, multiscale analysis of mammalian kidney development in which we measure changes in cell number, compartment volumes, and cellular dynamics across the entirety of organogenesis, focusing on two key nephrogenic progenitor populations: the ureteric epithelium and the cap mesenchyme. In doing so, we describe a discontinuous developmental program governed by dynamic changes in interactions between these key cellular populations occurring within a previously unappreciated structurally stereotypic organ architecture. We also illustrate the application of this approach to the detection of a subtle mutant phenotype. This baseline program of kidney morphogenesis provides a framework for assessing genetic and environmental developmental perturbation and will serve as a gold standard for the analysis of other organs.
•A comprehensive temporospatial and multiscale profile of normal kidney development•Analysis of structural stereotypy and branch form across development•Dynamic changes in the cap and tip progenitor cell niches over time•Application of the approach to identify a subtle mutant phenotype
Short et al. describe a comprehensive, quantitative analysis of shape, cell number, and proliferation rate for key progenitor populations across mammalian kidney development. This reveals a morphogenetic program with structural stereotypy, asynchronous branching, substantial remodeling, and discontinuous nephron induction, elucidating how variation in size and nephron number may arise. |
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AbstractList | Although kidneys of equal size can vary 10-fold in nephron number at birth, discovering what regulates such variation has been hampered by a lack of quantitative parameters defining kidney development. Here we report a comprehensive, quantitative, multiscale analysis of mammalian kidney development in which we measure changes in cell number, compartment volumes, and cellular dynamics across the entirety of organogenesis, focusing on two key nephrogenic progenitor populations: the ureteric epithelium and the cap mesenchyme. In doing so, we describe a discontinuous developmental program governed by dynamic changes in interactions between these key cellular populations occurring within a previously unappreciated structurally stereotypic organ architecture. We also illustrate the application of this approach to the detection of a subtle mutant phenotype. This baseline program of kidney morphogenesis provides a framework for assessing genetic and environmental developmental perturbation and will serve as a gold standard for the analysis of other organs. Although kidneys of equal size can vary 10-fold in nephron number at birth, discovering what regulates such variation has been hampered by a lack of quantitative parameters defining kidney development. Here we report a comprehensive, quantitative, multiscale analysis of mammalian kidney development in which we measure changes in cell number, compartment volumes, and cellular dynamics across the entirety of organogenesis, focusing on two key nephrogenic progenitor populations: the ureteric epithelium and the cap mesenchyme. In doing so, we describe a discontinuous developmental program governed by dynamic changes in interactions between these key cellular populations occurring within a previously unappreciated structurally stereotypic organ architecture. We also illustrate the application of this approach to the detection of a subtle mutant phenotype. This baseline program of kidney morphogenesis provides a framework for assessing genetic and environmental developmental perturbation and will serve as a gold standard for the analysis of other organs. •A comprehensive temporospatial and multiscale profile of normal kidney development•Analysis of structural stereotypy and branch form across development•Dynamic changes in the cap and tip progenitor cell niches over time•Application of the approach to identify a subtle mutant phenotype Short et al. describe a comprehensive, quantitative analysis of shape, cell number, and proliferation rate for key progenitor populations across mammalian kidney development. This reveals a morphogenetic program with structural stereotypy, asynchronous branching, substantial remodeling, and discontinuous nephron induction, elucidating how variation in size and nephron number may arise. |
Author | McMahon, Andrew P. Hamilton, Nicholas A. Smyth, Ian M. Little, Melissa H. Ju, Adler L. Lamberton, Timothy Rumballe, Bree A. Short, Kieran M. Combes, Alexander N. Lefevre, James Georgas, Kylie M. Cairncross, Oliver |
Author_xml | – sequence: 1 givenname: Kieran M. surname: Short fullname: Short, Kieran M. organization: Department of Biochemistry and Molecular Biology, Monash University, Clayton VIC 3800, Australia – sequence: 2 givenname: Alexander N. surname: Combes fullname: Combes, Alexander N. organization: Division of Molecular Genetics and Development, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 3 givenname: James surname: Lefevre fullname: Lefevre, James organization: Division of Genomics & Computational Biology and Division of Molecular Cell Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 4 givenname: Adler L. surname: Ju fullname: Ju, Adler L. organization: Division of Molecular Genetics and Development, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 5 givenname: Kylie M. surname: Georgas fullname: Georgas, Kylie M. organization: Division of Molecular Genetics and Development, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 6 givenname: Timothy surname: Lamberton fullname: Lamberton, Timothy organization: Division of Genomics & Computational Biology and Division of Molecular Cell Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 7 givenname: Oliver surname: Cairncross fullname: Cairncross, Oliver organization: Division of Genomics & Computational Biology and Division of Molecular Cell Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 8 givenname: Bree A. surname: Rumballe fullname: Rumballe, Bree A. organization: Division of Molecular Genetics and Development, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 9 givenname: Andrew P. surname: McMahon fullname: McMahon, Andrew P. organization: Department of Stem Cell Biology and Regenerative Medicine, Broad-CIRM Center for Regenerative Medicine and Stem Cell Research, University of Southern California Keck School of Medicine, Los Angeles, CA 90089, USA – sequence: 10 givenname: Nicholas A. surname: Hamilton fullname: Hamilton, Nicholas A. organization: Division of Genomics & Computational Biology and Division of Molecular Cell Biology, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia – sequence: 11 givenname: Ian M. surname: Smyth fullname: Smyth, Ian M. email: ian.smyth@monash.edu organization: Department of Biochemistry and Molecular Biology, Monash University, Clayton VIC 3800, Australia – sequence: 12 givenname: Melissa H. surname: Little fullname: Little, Melissa H. email: m.little@imb.uq.edu.au organization: Division of Molecular Genetics and Development, Institute for Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24780737$$D View this record in MEDLINE/PubMed |
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Snippet | Although kidneys of equal size can vary 10-fold in nephron number at birth, discovering what regulates such variation has been hampered by a lack of... |
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SubjectTerms | Animals Cell Count Embryonic Stem Cells - physiology Female Gene Expression Regulation, Developmental Kidney - cytology Kidney - embryology Kidney - physiology Male Mice Mice, Inbred C57BL Mutation Nephrons - cytology Nephrons - embryology Nephrons - physiology Phenotype Pregnancy Ureter - cytology Ureter - embryology Ureter - physiology Urothelium - cytology Urothelium - embryology Urothelium - physiology |
Title | Global Quantification of Tissue Dynamics in the Developing Mouse Kidney |
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