Integrated β-catenin, BMP, PTEN, and Notch signalling patterns the nephron

Elife. 2015 Feb 3:3:e04000. doi: 10.7554/eLife.04000.

Abstract

The different segments of the nephron and glomerulus in the kidney balance the processes of water homeostasis, solute recovery, blood filtration, and metabolite excretion. When segment function is disrupted, a range of pathological features are presented. Little is known about nephron patterning during embryogenesis. In this study, we demonstrate that the early nephron is patterned by a gradient in β-catenin activity along the axis of the nephron tubule. By modifying β-catenin activity, we force cells within nephrons to differentiate according to the imposed β-catenin activity level, thereby causing spatial shifts in nephron segments. The β-catenin signalling gradient interacts with the BMP pathway which, through PTEN/PI3K/AKT signalling, antagonises β-catenin activity and promotes segment identities associated with low β-catenin activity. β-catenin activity and PI3K signalling also integrate with Notch signalling to control segmentation: modulating β-catenin activity or PI3K rescues segment identities normally lost by inhibition of Notch. Our data therefore identifies a molecular network for nephron patterning.

Keywords: BMP; Notch; PI3K; beta-catenin; developmental biology; kidney development; mouse; patterning; stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics*
  • Bone Morphogenetic Proteins / genetics
  • Bone Morphogenetic Proteins / metabolism*
  • Cell Differentiation
  • Diffusion Chambers, Culture
  • Embryo, Mammalian
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism
  • Gene Expression Regulation, Developmental
  • Mice
  • Mice, Transgenic
  • Nephrons / cytology
  • Nephrons / growth & development
  • Nephrons / metabolism*
  • Organ Culture Techniques
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism*
  • Phosphatidylinositol 3-Kinases / genetics
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Receptors, Notch / antagonists & inhibitors
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism*
  • Signal Transduction
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • Bone Morphogenetic Proteins
  • CTNNB1 protein, mouse
  • RNA, Small Interfering
  • Receptors, Notch
  • beta Catenin
  • Phosphatidylinositol 3-Kinases
  • Proto-Oncogene Proteins c-akt
  • PTEN Phosphohydrolase
  • Pten protein, mouse