ArticlePLoS genetics2017
A SHH-FOXF1-BMP4 signaling axis regulating growth and differentiation of epithelial and mesenchymal tissues in ureter development.
Article in PLoS genetics, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 27 papers.
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Who cites it
27 citing papers in PubMed, 51 citations in OpenAlex.
- Mesenchymal WNT signaling coordinates epithelial and mesenchymal differentiation in the developing murine ureter.Cell communication and signaling : CCS · 2026Article
- Transcription factor ZEB2 is essential for ureteral smooth muscle cell differentiation.PLoS genetics · 2026Article
- In vitro generation of a ureteral organoid from pluripotent stem cells.Nature communications · 2025Article
- Ureter development and associated congenital anomalies.Nature reviews. Nephrology · 2025Review
- PPARG contributes to urothelial integrity in the murine ureter by activating the expression of Shh and superficial cell-specific genes.Development (Cambridge, England) · 2025Article
- Interplay of SHH, WNT and BMP4 signaling regulates the development of the lamina propria in the murine ureter.Development (Cambridge, England) · 2025Article
- Heterozygous variants in the teashirt zinc finger homeobox 3 (TSHZ3) gene in human congenital anomalies of the kidney and urinary tract.European journal of human genetics : EJHG · 2025Article
- Hedgehog-dependent and hedgehog-independent roles for growth arrest specific 1 in mammalian kidney morphogenesis.Development (Cambridge, England) · 2024Article
- Inferring pattern-driving intercellular flows from single-cell and spatial transcriptomics.Nature methods · 2024Article
- Keratin 5 basal cells are temporally regulated developmental and tissue repair progenitors in bladder urothelium.American journal of physiology. Renal physiology · 2024Article
- Successful reconstruction of the rat ureter by a syngeneic collagen tube with a cardiomyocyte sheet.Regenerative therapy · 2023Article
- Hedgehog signaling regulates Wolffian duct development through the primary cilium†.Biology of reproduction · 2023Article
- Stromal FOXF2 suppresses prostate cancer progression and metastasis by enhancing antitumor immunity.Nature communications · 2022Article
- Single-cell and spatial mapping Identify cell types and signaling Networks in the human ureter.Developmental cell · 2022Article
- GATA6 is a crucial factor for Myocd expression in the visceral smooth muscle cell differentiation program of the murine ureter.Development (Cambridge, England) · 2022Article
- An essential function for autocrine hedgehog signaling in epithelial proliferation and differentiation in the trachea.Development (Cambridge, England) · 2022Article
- Evaluation of PGP 9.5, NGFR, TGFβ1, FGFR1, MMP-2, AT2R2, SHH, and TUNEL in Primary Obstructive Megaureter Tissue.The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society · 2022Article
- The immune responses to differentFrontiers in immunology · 2022Review
- Disruption of a hedgehog-foxf1-rspo2 signaling axis leads to tracheomalacia and a loss of sox9+ tracheal chondrocytes.Disease models & mechanisms · 2020Article
- Loss of FOXF1 expression promotes human lung-resident mesenchymal stromal cell migration via ATX/LPA/LPA1 signaling axis.Scientific reports · 2020Article
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Authors and funding
11 authors at 1 institution in 1 country.
Funding
No grant is acknowledged in the PubMed record.
Abstract
The differentiated cell types of the epithelial and mesenchymal tissue compartments of the mature ureter of the mouse arise in a precise temporal and spatial sequence from uncommitted precursor cells of the distal ureteric bud epithelium and its surrounding mesenchyme. Previous genetic efforts identified a member of the Hedgehog (HH) family of secreted proteins, Sonic hedgehog (SHH) as a crucial epithelial signal for growth and differentiation of the ureteric mesenchyme. Here, we used conditional loss- and gain-of-function experiments of the unique HH signal transducer Smoothened (SMO) to further characterize the cellular functions and unravel the effector genes of HH signaling in ureter development. We showed that HH signaling is not only required for proliferation and SMC differentiation of cells of the inner mesenchymal region but also for survival of cells of the outer mesenchymal region, and for epithelial proliferation and differentiation. We identified the Forkhead transcription factor gene Foxf1 as a target of HH signaling in the ureteric mesenchyme. Expression of a repressor version of FOXF1 in this tissue completely recapitulated the mesenchymal and epithelial proliferation and differentiation defects associated with loss of HH signaling while re-expression of a wildtype version of FOXF1 in the inner mesenchymal layer restored these cellular programs when HH signaling was inhibited. We further showed that expression of Bmp4 in the ureteric mesenchyme depends on HH signaling and Foxf1, and that exogenous BMP4 rescued cell proliferation and epithelial differentiation in ureters with abrogated HH signaling or FOXF1 function. We conclude that SHH uses a FOXF1-BMP4 module to coordinate the cellular programs for ureter elongation and differentiation, and suggest that deregulation of this signaling axis occurs in human congenital anomalies of the kidney and urinary tract (CAKUT).
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