Renal Interstitial Platelet-Derived Growth Factor Receptor- β Cells Support Proximal Tubular Regeneration

J Am Soc Nephrol. 2018 May;29(5):1383-1396. doi: 10.1681/ASN.2017101069. Epub 2018 Feb 23.

Abstract

Background: The kidney is considered to be a structurally stable organ with limited baseline cellular turnover. Nevertheless, single cells must be constantly replaced to conserve the functional integrity of the organ. PDGF chain B (PDGF-BB) signaling through fibroblast PDGF receptor-β (PDGFRβ) contributes to interstitial-epithelial cell communication and facilitates regenerative functions in several organs. However, the potential role of interstitial cells in renal tubular regeneration has not been examined.

Methods: In mice with fluorescent protein expression in renal tubular cells and PDGFRβ-positive interstitial cells, we ablated single tubular cells by high laser exposure. We then used serial intravital multiphoton microscopy with subsequent three-dimensional reconstruction and ex vivo histology to evaluate the cellular and molecular processes involved in tubular regeneration.

Results: Single-tubular cell ablation caused the migration and division of dedifferentiated tubular epithelial cells that preceded tubular regeneration. Moreover, tubular cell ablation caused immediate calcium responses in adjacent PDGFRβ-positive interstitial cells and the rapid migration thereof toward the injury. These PDGFRβ-positive cells enclosed the injured epithelium before the onset of tubular cell dedifferentiation, and the later withdrawal of these PDGFRβ-positive cells correlated with signs of tubular cell redifferentiation. Intraperitoneal administration of trapidil to block PDGFRβ impeded PDGFRβ-positive cell migration to the tubular injury site and compromised the recovery of tubular function.

Conclusions: Ablated tubular cells are exclusively replaced by resident tubular cell proliferation in a process dependent on PDGFRβ-mediated communication between the renal interstitium and the tubular system.

Keywords: proliferation; renal proximal tubule cell; renal stem cell; tubular-interstitial crosstalk.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism
  • Cell Communication
  • Cell Dedifferentiation*
  • Cell Movement / drug effects
  • Epithelial Cells / physiology*
  • Female
  • Intravital Microscopy
  • Kidney / cytology
  • Kidney Tubules, Proximal / cytology
  • Kidney Tubules, Proximal / injuries
  • Kidney Tubules, Proximal / physiology*
  • Lymphokines / metabolism
  • Male
  • Mice
  • Phosphodiesterase Inhibitors / pharmacology
  • Platelet-Derived Growth Factor / metabolism
  • Receptor, Platelet-Derived Growth Factor beta / metabolism*
  • Recovery of Function
  • Regeneration*
  • Trapidil / pharmacology
  • Urothelium / injuries
  • Urothelium / physiology*

Substances

  • Lymphokines
  • Pdgfd protein, mouse
  • Phosphodiesterase Inhibitors
  • Platelet-Derived Growth Factor
  • Receptor, Platelet-Derived Growth Factor beta
  • Trapidil
  • Calcium