Evaluation of protein kinase D auto-phosphorylation as biomarker for NLRP3 inflammasome activation

PLoS One. 2021 Nov 12;16(11):e0248668. doi: 10.1371/journal.pone.0248668. eCollection 2021.

Abstract

Background: The NLRP3 inflammasome is a critical component of sterile inflammation, which is involved in many diseases. However, there is currently no known proximal biomarker for measuring NLRP3 activation in pathological conditions. Protein kinase D (PKD) has emerged as an important NLRP3 kinase that catalyzes the release of a phosphorylated NLRP3 species that is competent for inflammasome complex assembly.

Methods: To explore the potential for PKD activation to serve as a selective biomarker of the NLRP3 pathway, we tested various stimulatory conditions in THP-1 and U937 cell lines, probing the inflammasome space beyond NLRP3. We analyzed the correlation between PKD activation (monitored by its auto-phosphorylation) and functional inflammasome readouts.

Results: PKD activation/auto-phosphorylation always preceded cleavage of caspase-1 and gasdermin D, and treatment with the PKD inhibitor CRT0066101 could block NLRP3 inflammasome assembly and interleukin-1β production. Conversely, blocking NLRP3 either genetically or using the MCC950 inhibitor prevented PKD auto-phosphorylation, indicating a bidirectional functional crosstalk between NLRP3 and PKD. Further assessments of the pyrin and NLRC4 pathways, however, revealed that PKD auto-phosphorylation can be triggered by a broad range of stimuli unrelated to NLRP3 inflammasome assembly.

Conclusion: Although PKD and NLRP3 become functionally interconnected during NLRP3 activation, the promiscuous reactivity of PKD challenges its potential use for tracing the NLRP3 inflammasome pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biomarkers / metabolism
  • Caspase 1 / metabolism
  • Cell Line, Tumor
  • Humans
  • Inflammasomes / metabolism*
  • Inflammation / metabolism
  • Intracellular Signaling Peptides and Proteins / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Phosphate-Binding Proteins / metabolism
  • Phosphorylation
  • Protein Kinase C / metabolism*
  • Pyrin / metabolism
  • U937 Cells

Substances

  • Biomarkers
  • GSDMD protein, human
  • Inflammasomes
  • Intracellular Signaling Peptides and Proteins
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Phosphate-Binding Proteins
  • Pyrin
  • protein kinase D
  • Protein Kinase C
  • Caspase 1

Grants and funding

NIBR provided support in the form of salaries to all authors (DH, JR, AU, CM, MK, UB, CJF, BR, FB), but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.