GDNF/Ret signaling and the development of the kidney.

Signaling by GDNF through the Ret receptor is required for normal growth of the ureteric bud during kidney development. However, the precise role of GDNF/Ret signaling in renal branching morphogenesis and the specific responses of ureteric bud cells to GDNF remain unclear. Recent studies have provided new insight into these issues. The localized expression of GDNF by the metanephric mesenchyme, together with several types of negative regulation, is important to elicit and correctly position the initial budding event from the Wolffian duct. GDNF also promotes the continued branching of the ureteric bud. However, it does not provide the positional information required to specify the pattern of ureteric bud growth and branching, as its site of synthesis can be drastically altered with minimal effects on kidney development. Cells that lack Ret are unable to contribute to the tip of the ureteric bud, apparently because GDNF-driven proliferation is required for the formation and growth of this specialized epithelial domain.

[1]  Q. Al-Awqati,et al.  Architectural patterns in branching morphogenesis in the kidney. , 1998, Kidney international.

[2]  J. Bertram,et al.  Nephron endowment and blood pressure: What do we really know? , 2004, Current hypertension reports.

[3]  Shaobing Zhang,et al.  Patterning parameters associated with the branching of the ureteric bud regulated by epithelial-mesenchymal interactions. , 2003, The International journal of developmental biology.

[4]  H. Nakagawa,et al.  Printed in U.S.A. Copyright © 1999 by The Endocrine Society Glial Cell Line-Derived Neurotropic Factor Stimulates Sertoli Cell Proliferation in the Early Postnatal Period of Rat Testis Development , 2022 .

[5]  Nobuyuki Itoh,et al.  Tube or not tube: remodeling epithelial tissues by branching morphogenesis. , 2003, Developmental cell.

[6]  S. Kato,et al.  FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. , 2000, Biochemical and biophysical research communications.

[7]  I. Fariñas,et al.  GFRα1 Is an Essential Receptor Component for GDNF in the Developing Nervous System and Kidney , 1998, Neuron.

[8]  G. Mackie,et al.  Duplex kidneys: a correlation of renal dysplasia with position of the ureteral orifice. , 1975, The Journal of urology.

[9]  E. Lai,et al.  Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. , 1996, Genes & development.

[10]  L. Saxén Organogenesis of the kidney , 1987 .

[11]  Ming-Jer Tang,et al.  The RET–Glial Cell-derived Neurotrophic Factor (GDNF) Pathway Stimulates Migration and Chemoattraction of Epithelial Cells , 1998, The Journal of cell biology.

[12]  G. Raisman,et al.  Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. , 1999, Development.

[13]  A. Palotie,et al.  Cloning, mRNA Distribution and Chromosomal Localisation of the Gene for Glial Cell Line-Derived Neurotrophic Factor Receptor β, a Homologue to GDNFR-α , 1997 .

[14]  D. Newgreen,et al.  GDNF is a chemoattractant for enteric neural cells. , 2001, Developmental biology.

[15]  C. Worby,et al.  Glial cell line-derived neurotrophic factor activates the receptor tyrosine kinase RET and promotes kidney morphogenesis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[16]  V. D’Agati,et al.  Renal agenesis and hypodysplasia in ret-k- mutant mice result from defects in ureteric bud development. , 1996, Development.

[17]  Jamie A Davies,et al.  Pattern and regulation of cell proliferation during murine ureteric bud development , 2004, Journal of anatomy.

[18]  M. Ichihara,et al.  A Targeting Mutation of Tyrosine 1062 in Ret Causes a Marked Decrease of Enteric Neurons and Renal Hypoplasia , 2004, Molecular and Cellular Biology.

[19]  M. Borrello,et al.  RET tyrosine kinase signaling in development and cancer. , 2005, Cytokine & growth factor reviews.

[20]  F. Costantini,et al.  The role of GDNF/Ret signaling in ureteric bud cell fate and branching morphogenesis. , 2005, Developmental cell.

[21]  N. Asai,et al.  Characterization of the ret proto-oncogene products expressed in mouse L cells. , 1993, Oncogene.

[22]  Mart Saarma,et al.  Defects in enteric innervation and kidney development in mice lacking GDNF , 1996, Nature.

[23]  A. McMahon,et al.  GDNF induces branching and increased cell proliferation in the ureter of the mouse. , 1997, Developmental biology.

[24]  H. Hellmich,et al.  Embryonic expression of glial cell-line derived neurotrophic factor (GDNF) suggests multiple developmental roles in neural differentiation and epithelial-mesenchymal interactions , 1996, Mechanisms of Development.

[25]  Se-Jin Lee,et al.  Regulation of metanephric kidney development by growth/differentiation factor 11. , 2003, Developmental biology.

[26]  F. Costantini,et al.  Expression of the c-ret proto-oncogene during mouse embryogenesis. , 1993, Development.

[27]  B. Hogan,et al.  Bone morphogenetic protein 4 regulates the budding site and elongation of the mouse ureter. , 2000, The Journal of clinical investigation.

[28]  R. O. Stuart,et al.  Spatiotemporal regulation of morphogenetic molecules during in vitro branching of the isolated ureteric bud: toward a model of branching through budding in the developing kidney. , 2004, Developmental biology.

[29]  D. Bar-Sagi,et al.  Modulation of signalling by Sprouty: a developing story , 2004, Nature Reviews Molecular Cell Biology.

[30]  J. Bertram,et al.  The Where, What and Why of the Developing Renal Stroma , 2005, Nephron Experimental Nephrology.

[31]  A. McMahon,et al.  Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. , 1996, Development.

[32]  M. Saarma,et al.  Glial-cell-line-derived neurotrophic factor is required for bud initiation from ureteric epithelium. , 1997, Development.

[33]  G. Dressler,et al.  Regulation of ureteric bud outgrowth by Pax2-dependent activation of the glial derived neurotrophic factor gene. , 2001, Development.

[34]  Jonas Frisén,et al.  Renal agenesis and the absence of enteric neurons in mice lacking GDNF , 1996, Nature.

[35]  J. Milbrandt,et al.  GFRα1 Expression in Cells Lacking RET Is Dispensable for Organogenesis and Nerve Regeneration , 2004, Neuron.

[36]  D. Warburton,et al.  Molecular Mechanisms of Early Lung Specification and Branching Morphogenesis , 2005, Pediatric Research.

[37]  Seppo Vainio,et al.  Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development , 2003, Development.

[38]  E. Bottinger,et al.  Novel regulators of kidney development from the tips of the ureteric bud. , 2005, Journal of the American Society of Nephrology : JASN.

[39]  S. Nigam,et al.  Toward an etiological classification of developmental disorders of the kidney and upper urinary tract. , 2002, Kidney international.

[40]  J. Davies,et al.  Erk MAP kinase regulates branching morphogenesis in the developing mouse kidney. , 2001, Development.

[41]  V. D’Agati,et al.  Expression of green fluorescent protein in the ureteric bud of transgenic mice: a new tool for the analysis of ureteric bud morphogenesis. , 1999, Developmental genetics.

[42]  C. Grobstein Inductive epitheliomesenchymal interaction in cultured organ rudiments of the mouse. , 1953, Science.

[43]  J. Milbrandt,et al.  Neurturin: an autocrine regulator of renal collecting duct development. , 1999, Developmental genetics.

[44]  G. Dressler,et al.  The molecular basis of embryonic kidney development , 1997, Mechanisms of Development.

[45]  C. Cebrián,et al.  Morphometric index of the developing murine kidney , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[46]  M. Sanicola,et al.  Perturbation of RET signaling in the embryonic kidney. , 1999, Developmental genetics.

[47]  M. Saarma,et al.  GDNF promotes tubulogenesis of GFRα1-expressing MDCK cells by Src-mediated phosphorylation of Met receptor tyrosine kinase , 2003, The Journal of cell biology.

[48]  Jamie A Davies,et al.  Do different branching epithelia use a conserved developmental mechanism? , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[49]  B. Hogan,et al.  Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. , 1997, Development.

[50]  R. Zeller,et al.  Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis , 2004, Development.

[51]  M. Barnett,et al.  Signalling by glial cell line-derived neurotrophic factor (GDNF) requires heparan sulphate glycosaminoglycan , 2002, Journal of Cell Science.

[52]  J. Milbrandt,et al.  GFRα1-Deficient Mice Have Deficits in the Enteric Nervous System and Kidneys , 1998, Neuron.

[53]  S. Vainio,et al.  Organogenesis: Coordinating early kidney development: lessons from gene targeting , 2002, Nature Reviews Genetics.

[54]  J. Scott,et al.  Antenatal diagnosis of congenital abnormalities in the urinary tract. Results from the Northern Region Fetal Abnormality Survey. , 1988, British journal of urology.

[55]  E. Fuchs,et al.  FGF-7 modulates ureteric bud growth and nephron number in the developing kidney. , 1999, Development.

[56]  Frank Costantini,et al.  Real-time analysis of ureteric bud branching morphogenesis in vitro. , 2004, Developmental biology.

[57]  B. Hogan,et al.  Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. , 2000, Development.

[58]  R. Schneider,et al.  The human protooncogene ret: a communicative cadherin? , 1992, Trends in biochemical sciences.

[59]  I. Fariñas,et al.  Renal and neuronal abnormalities in mice lacking GDNF , 1996, Nature.

[60]  Gerald C. Chu,et al.  TGFβ superfamily signals are required for morphogenesis of the kidney mesenchyme progenitor population , 2004, Development.

[61]  J. Scott Fetal, perinatal, and infant death with congenital renal anomaly , 2002, Archives of disease in childhood.

[62]  Mart Saarma,et al.  Novel functions and signalling pathways for GDNF , 2003, Journal of Cell Science.

[63]  J. Milbrandt,et al.  TrnR2, a Novel Receptor That Mediates Neurturin and GDNF Signaling through Ret , 1997, Neuron.

[64]  A. Woolf,et al.  Glial Cell Line-Derived Neurotrophic Factor Stimulates Ureteric Bud Outgrowth and Enhances Survival of Ureteric Bud Cells in vitro , 1998, Nephron Experimental Nephrology.

[65]  V. D’Agati,et al.  The role of GDNF in patterning the excretory system. , 2005, Developmental biology.

[66]  S. Nigam,et al.  Branching morphogenesis independent of mesenchymal-epithelial contact in the developing kidney. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[67]  W. Cardoso,et al.  FGF-10 is a chemotactic factor for distal epithelial buds during lung development. , 1998, Developmental biology.

[68]  C. M. Meighan,et al.  GDNF and GFRα-1 Are Components of the Axolotl Pronephric Duct Guidance System , 2000 .

[69]  A. McMahon,et al.  Sprouty1 is a critical regulator of GDNF/RET-mediated kidney induction. , 2005, Developmental cell.

[70]  S. Whittemore,et al.  Ret-dependent and -independent Mechanisms of Glial Cell Line-derived Neurotrophic Factor Signaling in Neuronal Cells* , 1999, The Journal of Biological Chemistry.

[71]  M. Tessier-Lavigne,et al.  SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. , 2004, Developmental cell.

[72]  A. McMahon,et al.  Overview: The Molecular Basis of Kidney Development , 2003 .

[73]  Yang-Kao Wang,et al.  Ureteric bud outgrowth in response to RET activation is mediated by phosphatidylinositol 3-kinase. , 2002, Developmental biology.

[74]  Frank Costantini,et al.  Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret , 1994, Nature.

[75]  J. Thomas-Crusells,et al.  GDNF triggers a novel Ret‐independent Src kinase family‐coupled signaling via a GPI‐linked GDNF receptor α1 , 1999, FEBS letters.

[76]  I. Ichikawa,et al.  Paradigm shift from classic anatomic theories to contemporary cell biological views of CAKUT. , 2002, Kidney international.

[77]  E. Batourina,et al.  Vitamin A controls epithelial/mesenchymal interactions through Ret expression , 2001, Nature Genetics.

[78]  V. Pachnis,et al.  Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. , 2002, Development.

[79]  N. Asai,et al.  cDNA cloning of mouse ret proto-oncogene and its sequence similarity to the cadherin superfamily. , 1993, Oncogene.

[80]  M. Bouchard Transcriptional control of kidney development. , 2004, Differentiation; research in biological diversity.

[81]  M. Takahashi,et al.  The GDNF/RET signaling pathway and human diseases. , 2001, Cytokine & growth factor reviews.

[82]  B. Hogan,et al.  Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. , 2000, Development.

[83]  R. Sampogna,et al.  Branching morphogenesis and kidney disease , 2004, Development.

[84]  C. Grobstein Inductive interaction in the development of the mouse metanephros , 1955 .

[85]  M Rehn,et al.  Induced repatterning of type XVIII collagen expression in ureter bud from kidney to lung type: association with sonic hedgehog and ectopic surfactant protein C. , 2001, Development.

[86]  H. Sariola,et al.  The tip-top branching ureter. , 1997, Current opinion in cell biology.

[87]  C. Mendelsohn,et al.  Stromal progenitors are important for patterning epithelial and mesenchymal cell types in the embryonic kidney. , 2003, Seminars in cell & developmental biology.

[88]  V. D’Agati,et al.  Differential activities of the RET tyrosine kinase receptor isoforms during mammalian embryogenesis. , 2001, Genes & development.

[89]  M. Sharpe,et al.  Scatter factor/hepatocyte growth factor is essential for liver development , 1995, Nature.

[90]  C. Grobstein Inductive tissue interaction in development. , 1956, Advances in cancer research.