In vivo two-photon microscopy reveals the contribution of Sox9+ cell to kidney regeneration in a mouse model with extracellular vesicle treatment

J Biol Chem. 2020 Aug 21;295(34):12203-12213. doi: 10.1074/jbc.RA120.012732. Epub 2020 Jul 8.

Abstract

Mesenchymal stem cell (MSC)-derived extracellular vesicles (EVs) have been shown to stimulate regeneration in the treatment of kidney injury. Renal regeneration is also thought to be stimulated by the activation of Sox9+ cells. However, whether and how the activation mechanisms underlying EV treatment and Sox9+ cell-dependent regeneration intersect is unclear. We reasoned that a high-resolution imaging platform in living animals could help to untangle this system. To test this idea, we first applied EVs derived from human placenta-derived MSCs (hP-MSCs) to a Sox9-CreERT2; R26mTmG transgenic mouse model of acute kidney injury (AKI). Then, we developed an abdominal imaging window in the mouse and tracked the Sox9+ cells in the inducible Sox9-Cre transgenic mice via in vivo lineage tracing with two-photon intravital microscopy. Our results demonstrated that EVs can travel to the injured kidneys post intravenous injection as visualized by Gaussia luciferase imaging and markedly increase the activation of Sox9+ cells. Moreover, the two-photon living imaging of lineage-labeled Sox9+ cells showed that the EVs promoted the expansion of Sox9+ cells in kidneys post AKI. Histological staining results confirmed that the descendants of Sox9+ cells contributed to nephric tubule regeneration which significantly ameliorated the renal function after AKI. In summary, intravital lineage tracing with two-photon microscopy through an embedded abdominal imaging window provides a practical strategy to investigate the beneficial functions and to clarify the mechanisms of regenerative therapies in AKI.

Keywords: Sox9; acute kidney injury; extracellular vesicles; intravital microscopy; kidney; lineage tracing; mesenchymal stem cells (MSCs); microscopic imaging; regenerative medicine; two-photon microscopy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Kidney Injury* / genetics
  • Acute Kidney Injury* / metabolism
  • Acute Kidney Injury* / pathology
  • Acute Kidney Injury* / therapy
  • Animals
  • Extracellular Vesicles / metabolism
  • Extracellular Vesicles / transplantation*
  • Humans
  • Intravital Microscopy
  • Kidney / injuries
  • Kidney / physiology*
  • Mesenchymal Stem Cells / metabolism*
  • Mesenchymal Stem Cells / pathology
  • Mice
  • Mice, Transgenic
  • Microscopy, Fluorescence, Multiphoton
  • Regeneration*
  • SOX9 Transcription Factor / genetics
  • SOX9 Transcription Factor / metabolism*

Substances

  • SOX9 Transcription Factor
  • Sox9 protein, mouse