Redox DAPK1 destabilizes Pellino1 to govern inflammation-coupling tubular damage during septic AKI

Theranostics. 2020 Sep 15;10(25):11479-11496. doi: 10.7150/thno.49870. eCollection 2020.

Abstract

Tubular damage initiated by inflammatory response and ischemic/hypoxic stress is a hallmark of septic acute kidney injury (AKI), albeit the molecular mechanism coupling the two events remains unclear. We investigated the intrinsic nature of tubular damage with respect to inflammatory/hypoxic stress during septic AKI. Methods: The apoptotic response of tubular cells to LPS stimuli was analyzed before and after hypoxia exposure. Cellular ubiquitination, co-immunoprecipitation, GST-pulldown, in vitro protein kinase assay, immunofluorescence and CRISPR technology were adopted to determine the molecular mechanism underlying this process. In vivo characterization was performed in wild-type and DAPK1-/- mice models of cecal ligation and puncture (CLP). Results: We found that the MyD88-dependent inflammatory response couples to tubular damage during LPS stimuli under hypoxia in a Fn14/SCFFbxw7α-dispensable manner via recruitment of caspase-8 with TRIF-RIP1 signalosome mediated by DAPK1, which directly binds to and phosphorylates Pellino1 at Ser39, leading to Pellino1 poly-ubiquitination and turnover. Either pharmacological deactivation or genetic ablation of DAPK1 makes tubular cells refractory to the LPS-induced damage in the context of hypoxia, while kinase activity of DAPK1 is essential for ruin execution. Targeting DAPK1 effectively protects mice against septic AKI and potentiates the efficacy of a MyD88 homodimerization inhibitor, ST2825. Conclusion: Our findings provide a rationale for the mechanism whereby inflammation intersects with hypoxic tubular damage during septic AKI through a previously unappreciated role of DAPK1-inducible Ser39 phosphorylation in Pellino1 turnover and underscore that combined targeting DAPK1 and MyD88 might be a feasible strategy for septic AKI management.

Keywords: DAPK1; Pellino1; Phosphorylation; Septic acute kidney injury; Tubular damage; Turnover.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Kidney Injury / immunology*
  • Acute Kidney Injury / pathology
  • Acute Kidney Injury / prevention & control
  • Animals
  • CRISPR-Cas Systems / genetics
  • Cell Hypoxia / drug effects
  • Cell Hypoxia / immunology
  • Cell Line
  • Death-Associated Protein Kinases / antagonists & inhibitors
  • Death-Associated Protein Kinases / genetics
  • Death-Associated Protein Kinases / metabolism*
  • Disease Models, Animal
  • Epithelial Cells
  • Gene Knockout Techniques
  • Heterocyclic Compounds, 2-Ring / pharmacology
  • Heterocyclic Compounds, 2-Ring / therapeutic use
  • Humans
  • Kidney Tubules / cytology
  • Kidney Tubules / pathology
  • Mice
  • Mice, Knockout
  • Myeloid Differentiation Factor 88 / antagonists & inhibitors
  • Myeloid Differentiation Factor 88 / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Oxidation-Reduction / drug effects
  • Phosphorylation / drug effects
  • Phosphorylation / genetics
  • RAW 264.7 Cells
  • Sepsis / complications*
  • Sepsis / drug therapy
  • Sepsis / immunology
  • Spiro Compounds / pharmacology
  • Spiro Compounds / therapeutic use
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination / drug effects
  • Ubiquitination / genetics

Substances

  • Heterocyclic Compounds, 2-Ring
  • MYD88 protein, human
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Nuclear Proteins
  • ST2825
  • Spiro Compounds
  • PELI1 protein, human
  • Ubiquitin-Protein Ligases
  • DAPK1 protein, human
  • Dapk1 protein, mouse
  • Death-Associated Protein Kinases
  • Peli1 protein, mouse