Myeloid PTEN deficiency aggravates renal inflammation and fibrosis in angiotensin II-induced hypertension

J Cell Physiol. 2022 Jan;237(1):983-991. doi: 10.1002/jcp.30574. Epub 2021 Sep 13.

Abstract

Hypertension is a major cause of chronic kidney disease. However, the pathogenesis of hypertensive kidney disease is not fully understood. Recently, we have shown that CXCL16/phosphoinositide-3 kinase γ (PI3Kγ) plays an important role in the development of renal inflammation and fibrosis in angiotensin II (AngII) induced hypertensive nephropathy. In the present study, we examined the role of phosphatase and tensin homolog (PTEN), a major regulator of PI3K signaling, in the pathogenesis of renal inflammation and fibrosis in an experimental model of hypertension induced by AngII. We generated myeloid PTEN conditional knockout mice by crossing PTENflox/flox mice with LysM-driven Cre mice. Littermate LysM-Cre-/- PTENflox/flox mice were used as a control. Both myeloid PTEN knockout mice and their littermate control mice exhibited similar blood pressure at baseline. AngII treatment resulted in an increase in blood pressure that was comparable between myeloid PTEN knockout mice and littermate control mice. Compared with littermate control mice, myeloid PTEN knockout mice developed more severe kidney dysfunction, proteinuria, and fibrosis following AngII treatment. Furthermore, myeloid PTEN deficiency exacerbated total collagen deposition and extracellular matrix protein production and enhanced myeloid fibroblast accumulation and myofibroblast formation in the kidney following AngII treatment. Finally, myeloid PTEN deficiency markedly augmented infiltration of F4/80+ macrophages and CD3+ T cells into the kidneys of AngII-treated mice. Taken together, these results indicate that PTEN plays a crucial role in the pathogenesis of renal inflammation and fibrosis through the regulation of infiltration of myeloid fibroblasts, macrophages, and T lymphocytes into the kidney.

Keywords: PTEN; fibroblast; inflammation; macrophages; renal fibrosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Angiotensin II* / metabolism
  • Animals
  • Female
  • Fibrosis
  • Humans
  • Hypertension* / chemically induced
  • Hypertension* / genetics
  • Hypertension* / pathology
  • Hypertension, Renal
  • Inflammation / pathology
  • Kidney / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nephritis
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism

Substances

  • Angiotensin II
  • PTEN Phosphohydrolase
  • PTEN protein, human
  • Pten protein, mouse

Supplementary concepts

  • Hypertensive Nephropathy