FIH-1-modulated HIF-1α C-TAD promotes acute kidney injury to chronic kidney disease progression via regulating KLF5 signaling

Acta Pharmacol Sin. 2021 Dec;42(12):2106-2119. doi: 10.1038/s41401-021-00617-4. Epub 2021 Mar 3.

Abstract

Incomplete recovery from episodes of acute kidney injury (AKI) can predispose patients to develop chronic kidney disease (CKD). Although hypoxia-inducible factor-1α (HIF-1α) is a master regulator of the response to hypoxia/ischemia, the role of HIF-1α in CKD progression following incomplete recovery from AKI is poorly understood. Here, we investigated this issue using moderate and severe ischemia/reperfusion injury (I/RI) mouse models. We found that the outcomes of AKI were highly associated with the time course of tubular HIF-1α expression. Sustained activation of HIF-1α, accompanied by the development of renal fibrotic lesions, was found in kidneys with severe AKI. The AKI to CKD progression was markedly ameliorated when PX-478 (a specific HIF-1α inhibitor, 5 mg· kg-1·d-1, i.p.) was administered starting on day 5 after severe I/RI for 10 consecutive days. Furthermore, we demonstrated that HIF-1α C-terminal transcriptional activation domain (C-TAD) transcriptionally stimulated KLF5, which promoted progression of CKD following severe AKI. The effect of HIF-1α C-TAD activation on promoting AKI to CKD progression was also confirmed in in vivo and in vitro studies. Moreover, we revealed that activation of HIF-1α C-TAD resulted in the loss of FIH-1, which was the key factor governing HIF-1α-driven AKI to CKD progression. Overexpression of FIH-1 inhibited HIF-1α C-TAD and prevented AKI to CKD progression. Thus, FIH-1-modulated HIF-1α C-TAD activation was the key mechanism of AKI to CKD progression by transcriptionally regulating KLF5 pathway. Our results provide new insights into the role of HIF-1α in AKI to CKD progression and also the potential therapeutic strategy for the prevention of renal diseases progression.

Keywords: FIH-1; HIF-1α C-terminal activation domain; KLF5; PX-478; acute kidney injury; chronic kidney disease; renal fibrosis.

MeSH terms

  • Acute Kidney Injury / metabolism*
  • Acute Kidney Injury / pathology
  • Animals
  • Disease Progression
  • Hypoxia / metabolism
  • Hypoxia-Inducible Factor 1, alpha Subunit / antagonists & inhibitors
  • Hypoxia-Inducible Factor 1, alpha Subunit / chemistry
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Kidney / metabolism
  • Kidney / pathology
  • Kruppel-Like Transcription Factors / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mixed Function Oxygenases / metabolism*
  • Mustard Compounds / therapeutic use
  • Phenylpropionates / therapeutic use
  • Protein Domains
  • Renal Insufficiency, Chronic / etiology*
  • Renal Insufficiency, Chronic / pathology
  • Signal Transduction / drug effects*
  • Up-Regulation / physiology

Substances

  • 2-amino-3-(4'-N,N-bis(2-chloroethyl)amino)phenylpropionic acid N-oxide
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Klf5 protein, mouse
  • Kruppel-Like Transcription Factors
  • Mustard Compounds
  • Phenylpropionates
  • Mixed Function Oxygenases
  • factor inhibiting hypoxia-inducible factor 1, mouse