Organelle communication maintains mitochondrial and endosomal homeostasis during podocyte lipotoxicity

JCI Insight. 2024 Aug 8;9(18):e182534. doi: 10.1172/jci.insight.182534.

Abstract

Organelle stress exacerbates podocyte injury, contributing to perturbed lipid metabolism. Simultaneous organelle stresses can occur in the kidney in the diseased state; therefore, a thorough analysis of organelle communication is crucial for understanding the progression of kidney diseases. Although organelles closely interact with one another at membrane contact sites, limited studies have explored their involvement in kidney homeostasis. The endoplasmic reticulum (ER) protein, PDZ domain-containing 8 (PDZD8), is implicated in multiple-organelle-tethering processes and cellular lipid homeostasis. In this study, we aimed to elucidate the role of organelle communication in podocyte injury using podocyte-specific Pdzd8-knockout mice. Our findings demonstrated that Pdzd8 deletion exacerbated podocyte injury in an accelerated obesity-related kidney disease model. Proteomic analysis of isolated glomeruli revealed that Pdzd8 deletion exacerbated mitochondrial and endosomal dysfunction during podocyte lipotoxicity. Additionally, electron microscopy revealed the accumulation of abnormal, fatty endosomes in Pdzd8-deficient podocytes during obesity-related kidney diseases. Lipidomic analysis indicated that glucosylceramide accumulated in Pdzd8-deficient podocytes, owing to accelerated production and decelerated degradation. Thus, the organelle-tethering factor, PDZD8, plays a crucial role in maintaining mitochondrial and endosomal homeostasis during podocyte lipotoxicity. Collectively, our findings highlight the importance of organelle communication at the 3-way junction among the ER, mitochondria, and endosomes in preserving podocyte homeostasis.

Keywords: Chronic kidney disease; Mitochondria; Nephrology; Obesity.

MeSH terms

  • Animals
  • Endoplasmic Reticulum / metabolism
  • Endosomes* / metabolism
  • Homeostasis*
  • Kidney Diseases / genetics
  • Kidney Diseases / metabolism
  • Kidney Diseases / pathology
  • Lipid Metabolism
  • Male
  • Mice
  • Mice, Knockout*
  • Mitochondria* / metabolism
  • Mitochondria* / pathology
  • Obesity / metabolism
  • Obesity / pathology
  • Podocytes* / metabolism
  • Podocytes* / pathology

Grants and funding

This work was supported by the Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Early-Career Scientists (21K16159 to SH), the JSPS Grant-in-Aid for Scientific Research B (21H02824 to RI and 23H02924 to MN), Kyowa Kirin (to RI), Grants from MSD Life Science Foundation (to SH), The Cell Science Research Foundation (to SH), Takeda Science Foundation (to SH), The Ichiro Kanehara Foundation for the Promotion of Medical Sciences and Medical Care (to SH), Ono Medical Research Foundation (to SH), Ishibashi-Yukiko Kinen-Kikin (to SH), Japan Arteriosclerosis Prevention Fund (to SH), Mochida Memorial Foundation for Medical and Pharmaceutical Research (to SH), The Japan Kidney Foundation (JKFB22-1 to SH), and Kowa Life Science Foundation (to SH). The electron microscopic observations were supported by Research Support Project for Life Science and Drug Discovery (Basis for Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from Japan Agency for Medical Research and Development (AMED) under Grant Number JP23ama121002.