Signal integration at the PI3K-p85-XBP1 hub endows coagulation protease activated protein C with insulin-like function

Blood. 2017 Sep 21;130(12):1445-1455. doi: 10.1182/blood-2017-02-767921. Epub 2017 Jul 7.

Abstract

Coagulation proteases have increasingly recognized functions beyond hemostasis and thrombosis. Disruption of activated protein C (aPC) or insulin signaling impair function of podocytes and ultimately cause dysfunction of the glomerular filtration barrier and diabetic kidney disease (DKD). We here show that insulin and aPC converge on a common spliced-X-box binding protein-1 (sXBP1) signaling pathway to maintain endoplasmic reticulum (ER) homeostasis. Analogous to insulin, physiological levels of aPC maintain ER proteostasis in DKD. Accordingly, genetically impaired protein C activation exacerbates maladaptive ER response, whereas genetic or pharmacological restoration of aPC maintains ER proteostasis in DKD models. Importantly, in mice with podocyte-specific deficiency of insulin receptor (INSR), aPC selectively restores the activity of the cytoprotective ER-transcription factor sXBP1 by temporally targeting INSR downstream signaling intermediates, the regulatory subunits of PI3Kinase, p85α and p85β. Genome-wide mapping of condition-specific XBP1-transcriptional regulatory patterns confirmed that concordant unfolded protein response target genes are involved in maintenance of ER proteostasis by both insulin and aPC. Thus, aPC efficiently employs disengaged insulin signaling components to reconfigure ER signaling and restore proteostasis. These results identify ER reprogramming as a novel hormonelike function of coagulation proteases and demonstrate that targeting insulin signaling intermediates may be a feasible therapeutic approach ameliorating defective insulin signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Coagulation*
  • Class Ia Phosphatidylinositol 3-Kinase / metabolism*
  • Diabetic Nephropathies / metabolism
  • Endoplasmic Reticulum / metabolism
  • Gene Expression Regulation
  • Homeostasis
  • Humans
  • Insulin / metabolism*
  • Mice, Inbred C57BL
  • Models, Biological
  • Peptide Hydrolases / metabolism*
  • Protein C / metabolism*
  • Signal Transduction*
  • Thrombomodulin / metabolism
  • Unfolded Protein Response / genetics
  • X-Box Binding Protein 1 / metabolism*

Substances

  • Insulin
  • Protein C
  • THBD protein, mouse
  • Thrombomodulin
  • X-Box Binding Protein 1
  • Xbp1 protein, mouse
  • Class Ia Phosphatidylinositol 3-Kinase
  • Peptide Hydrolases