Nephron formation adopts a novel spatial topology at cessation of nephrogenesis
Nephron number in the mammalian kidney is known to vary dramatically, with postnatal renal function directly influenced by nephron complement. What determines final nephron number is poorly understood but nephron formation in the mouse kidney ceases within the first few days after birth, presumably...
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Published in | Developmental biology Vol. 360; no. 1; pp. 110 - 122 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
01.12.2011
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Abstract | Nephron number in the mammalian kidney is known to vary dramatically, with postnatal renal function directly influenced by nephron complement. What determines final nephron number is poorly understood but nephron formation in the mouse kidney ceases within the first few days after birth, presumably due to the loss of all remaining nephron progenitors via epithelial differentiation. What initiates this event is not known. Indeed, whether nephron formation occurs in the same way at this time as during embryonic development has also not been examined. In this study, we investigate the key cellular compartments involved in nephron formation; the ureteric tip, cap mesenchyme and early nephrons; from postnatal day (P) 0 to 6 in the mouse. High resolution analyses of gene and protein expression indicate that loss of nephron progenitors precedes loss of ureteric tip identity, but show spatial shifts in the expression of cap mesenchyme genes during this time. In addition, cap mesenchymal volume and rate of proliferation decline prior to birth. Section-based 3D modeling and Optical Projection Tomography revealed a burst of ectopic nephron induction, with the formation of multiple (up to 5) nephrons per ureteric tip evident from P2. While the distal–proximal patterning of these nephrons occurred normally, their spatial relationship with the ureteric compartment was altered. We propose that this phase of nephron formation represents an acceleration of differentiation within the cap mesenchyme due to a displacement of signals within the nephrogenic niche.
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► Dramatic changes occur within the nephrogenic niche in the few days after birth. ► Loss of nephron progenitors precedes the loss of ureteric tip identity. ► Spatial shifts occur in the expression pattern of key genes in the nephrogenic zone. ► Multiple, ectopic nephrons attach to each ureteric tip during the final induction. ► We provide evidence for a gradual depletion of the nephron progenitor population. |
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AbstractList | Nephron number in the mammalian kidney is known to vary dramatically, with postnatal renal function directly influenced by nephron complement. What determines final nephron number is poorly understood but nephron formation in the mouse kidney ceases within the first few days after birth, presumably due to the loss of all remaining nephron progenitors via epithelial differentiation. What initiates this event is not known. Indeed, whether nephron formation occurs in the same way at this time as during embryonic development has also not been examined. In this study, we investigate the key cellular compartments involved in nephron formation; the ureteric tip, cap mesenchyme and early nephrons; from postnatal day (P) 0 to 6 in the mouse. High resolution analyses of gene and protein expression indicate that loss of nephron progenitors precedes loss of ureteric tip identity, but show spatial shifts in the expression of cap mesenchyme genes during this time. In addition, cap mesenchymal volume and rate of proliferation decline prior to birth. Section-based 3D modeling and Optical Projection Tomography revealed a burst of ectopic nephron induction, with the formation of multiple (up to 5) nephrons per ureteric tip evident from P2. While the distal-proximal patterning of these nephrons occurred normally, their spatial relationship with the ureteric compartment was altered. We propose that this phase of nephron formation represents an acceleration of differentiation within the cap mesenchyme due to a displacement of signals within the nephrogenic niche. Nephron number in the mammalian kidney is known to vary dramatically, with postnatal renal function directly influenced by nephron complement. What determines final nephron number is poorly understood but nephron formation in the mouse kidney ceases within the first few days after birth, presumably due to the loss of all remaining nephron progenitors via epithelial differentiation. What initiates this event is not known. Indeed, whether nephron formation occurs in the same way at this time as during embryonic development has also not been examined. In this study, we investigate the key cellular compartments involved in nephron formation; the ureteric tip, cap mesenchyme and early nephrons; from postnatal day (P) 0 to 6 in the mouse. High resolution analyses of gene and protein expression indicate that loss of nephron progenitors precedes loss of ureteric tip identity, but show spatial shifts in the expression of cap mesenchyme genes during this time. In addition, cap mesenchymal volume and rate of proliferation decline prior to birth. Section-based 3D modeling and Optical Projection Tomography revealed a burst of ectopic nephron induction, with the formation of multiple (up to 5) nephrons per ureteric tip evident from P2. While the distal–proximal patterning of these nephrons occurred normally, their spatial relationship with the ureteric compartment was altered. We propose that this phase of nephron formation represents an acceleration of differentiation within the cap mesenchyme due to a displacement of signals within the nephrogenic niche. [Display omitted] ► Dramatic changes occur within the nephrogenic niche in the few days after birth. ► Loss of nephron progenitors precedes the loss of ureteric tip identity. ► Spatial shifts occur in the expression pattern of key genes in the nephrogenic zone. ► Multiple, ectopic nephrons attach to each ureteric tip during the final induction. ► We provide evidence for a gradual depletion of the nephron progenitor population. |
Author | Rumballe, Bree A. Gilbert, Thierry Ju, Adler L. Combes, Alexander N. Little, Melissa H. Georgas, Kylie M. |
AuthorAffiliation | 1 Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane, Australia, 4072 2 Centre for Developmental Biology, UMR5547, University Paul Sabatier, Toulouse, France |
AuthorAffiliation_xml | – name: 1 Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane, Australia, 4072 – name: 2 Centre for Developmental Biology, UMR5547, University Paul Sabatier, Toulouse, France |
Author_xml | – sequence: 1 givenname: Bree A. surname: Rumballe fullname: Rumballe, Bree A. organization: Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane 4072, Australia – sequence: 2 givenname: Kylie M. surname: Georgas fullname: Georgas, Kylie M. organization: Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane 4072, Australia – sequence: 3 givenname: Alexander N. surname: Combes fullname: Combes, Alexander N. organization: Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane 4072, Australia – sequence: 4 givenname: Adler L. surname: Ju fullname: Ju, Adler L. organization: Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane 4072, Australia – sequence: 5 givenname: Thierry surname: Gilbert fullname: Gilbert, Thierry organization: Centre for Developmental Biology, UMR5547, University Paul Sabatier, Toulouse, France – sequence: 6 givenname: Melissa H. surname: Little fullname: Little, Melissa H. email: m.little@imb.uq.edu.au organization: Institute for Molecular Bioscience, The University of Queensland, St. Lucia, Brisbane 4072, Australia |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21963425$$D View this record in MEDLINE/PubMed |
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Keywords | Morphogenesis 3D modeling Ureteric tip Optical Projection Tomography Nephrogenesis Nephron induction Confocal microscopy Cap mesenchyme Gene expression Kidney development |
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Cell doi: 10.1016/j.devcel.2010.04.008 contributor: fullname: Costantini – volume: 132 start-page: 3859 issue: 17 year: 2005 ident: 10.1016/j.ydbio.2011.09.011_bb0110 article-title: Inactivation of FGF8 in early mesoderm reveals an essential role in kidney development publication-title: Development doi: 10.1242/dev.01945 contributor: fullname: Perantoni |
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Snippet | Nephron number in the mammalian kidney is known to vary dramatically, with postnatal renal function directly influenced by nephron complement. What determines... |
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SubjectTerms | 3D modeling Animals Animals, Newborn Cap mesenchyme complement Confocal microscopy Cyclin D1 - genetics Cyclin D1 - metabolism embryogenesis Female Gene expression Gene Expression Regulation, Developmental genes Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Imaging, Three-Dimensional Kidney - embryology Kidney - growth & development Kidney - physiology Kidney development Mice Models, Anatomic Models, Biological Morphogenesis Nephrogenesis Nephron induction nephrons Nephrons - embryology Nephrons - growth & development Nephrons - physiology Optical Projection Tomography Organogenesis - genetics Organogenesis - physiology Pregnancy protein synthesis renal function tomography Tomography, Optical topology Transcription Factors - genetics Transcription Factors - metabolism Ureter - embryology Ureter - growth & development Ureteric tip |
Title | Nephron formation adopts a novel spatial topology at cessation of nephrogenesis |
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