Article

CCDC92 promotes podocyte injury by regulating PA28α/ABCA1/cholesterol efflux axis in type 2 diabetic mice

Fu-wen Zuo1, Zhi-yong Liu1, Ming-wei Wang1, Jun-yao Du1, Peng-zhong Ding1, Hao-ran Zhang1, Wei Tang2, Yu Sun1, Xiao-jie Wang1, Yan Zhang1, Yu-sheng Xie1, Ji-chao Wu1, Min Liu1, Zi-ying Wang1, Fan Yi1,3
1 Department of Pharmacology, School of Basic Medical Sciences, Shandong University, Jinan 250012, China
2 Department of Pathogenic Biology, School of Basic Medical Sciences, Shandong University, Jinan 250012, China
3 National Key Laboratory for Innovation and Transformation of Luobing Theory, Key Laboratory of Cardiovascular Remodeling and Function Research, Chinese Ministry of Education and Chinese Ministry of Health, Qilu Hospital, Shandong University, Jinan 250012, China
Correspondence to: Min Liu: liuweimin@sdu.edu.cn, Zi-ying Wang: wangziying@sdu.edu.cn, Fan Yi: fanyi@sdu.edu.cn,
DOI: 10.1038/s41401-023-01213-4
Received: 21 August 2023
Accepted: 7 December 2023
Advance online: 16 January 2024

Abstract

Podocyte lipotoxicity mediated by impaired cellular cholesterol efflux plays a crucial role in the development of diabetic kidney disease (DKD), and the identification of potential therapeutic targets that regulate podocyte cholesterol homeostasis has clinical significance. Coiled-coil domain containing 92 (CCDC92) is a novel molecule related to metabolic disorders and insulin resistance. However, whether the expression level of CCDC92 is changed in kidney parenchymal cells and the role of CCDC92 in podocytes remain unclear. In this study, we found that Ccdc92 was significantly induced in glomeruli from type 2 diabetic mice, especially in podocytes. Importantly, upregulation of Ccdc92 in glomeruli was positively correlated with an increased urine albumin-to-creatinine ratio (UACR) and podocyte loss. Functionally, podocyte-specific deletion of Ccdc92 attenuated proteinuria, glomerular expansion and podocyte injury in mice with DKD. We further demonstrated that Ccdc92 contributed to lipid accumulation by inhibiting cholesterol efflux, finally promoting podocyte injury. Mechanistically, Ccdc92 promoted the degradation of ABCA1 by regulating PA28α-mediated proteasome activity and then reduced cholesterol efflux. Thus, our studies indicate that Ccdc92 contributes to podocyte injury by regulating the PA28α/ABCA1/cholesterol efflux axis in DKD.
Keywords: CCDC92; proteasome activity; podocytes; cholesterol efflux; diabetic kidney disease

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