Tissue kallikrein mediates pro-inflammatory pathways and activation of protease-activated receptor-4 in proximal tubular epithelial cells

PLoS One. 2014 Feb 21;9(2):e88894. doi: 10.1371/journal.pone.0088894. eCollection 2014.

Abstract

Tissue kallikrein (KLK1) expression is up-regulated in human diabetic kidney tissue and induced by high glucose (HG) in human proximal tubular epithelial cells (PTEC). Since the kallikrein-kinin system (KKS) has been linked to cellular inflammatory process in many diseases, it is likely that KLK1 expression may mediate the inflammatory process during the development of diabetic nephropathy. In this study, we explored the role of KLK1 in tubular pro-inflammatory responses under the diabetic milieu. Recombinant KLK1 stimulated the production of inflammatory cytokines in PTEC via the activation of p42/44 and p38 MAPK signaling pathways. Molecular knockdown of endogenous KLK1 expression by siRNA transfection in PTEC attenuated advanced glycation end-products (AGE)-induced IL-8 and ICAM-1 productions in vitro. Interestingly, exposure of PTEC to KLK1 induced the expression of protease-activated receptors (PARs). There was a 2.9-fold increase in PAR-4, 1.4-fold increase in PAR-1 and 1.2-fold increase in PAR-2 mRNA levels. Activation of PAR-4 by a selective agonist was found to elicit the pro-inflammatory and pro-fibrotic phenotypes in PTEC while blockade of the receptor by specific antagonist attenuated high glucose-induced IL-6, CCL-2, CTGF and collagen IV expression. Calcium mobilization by the PAR-4 agonist in PTEC was desensitized by pretreatment with KLK1. Consistent with these in vitro findings, there was a markedly up-regulation of tubular PAR-4 expression in human diabetic renal cortical tissues. Together, these results suggest that up-regulation of KLK1 in tubular epithelial cells may mediate pro-inflammatory pathway and PAR activation during diabetic nephropathy and provide a new therapeutic target for further investigation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Blotting, Western
  • Calcium / metabolism
  • Cells, Cultured
  • Cytokines / metabolism
  • DNA Primers / genetics
  • Diabetes Mellitus / metabolism*
  • Enzyme-Linked Immunosorbent Assay
  • Epithelial Cells / cytology
  • Epithelial Cells / metabolism*
  • Humans
  • Immunohistochemistry
  • Inflammation / physiopathology*
  • Interleukin-8 / metabolism
  • Kidney Tubules, Proximal / cytology*
  • RNA Interference
  • RNA, Small Interfering / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Proteinase-Activated / metabolism
  • Receptors, Thrombin / metabolism*
  • Signal Transduction / physiology*
  • Tissue Kallikreins / genetics
  • Tissue Kallikreins / metabolism*

Substances

  • Cytokines
  • DNA Primers
  • Interleukin-8
  • RNA, Small Interfering
  • Receptors, Proteinase-Activated
  • Receptors, Thrombin
  • Tissue Kallikreins
  • protease-activated receptor 4
  • Calcium

Grants and funding

This study was supported by a General Research Fund from the Research Grants Council of Hong Kong (Grant number: HKU 779611M), the National Basic Research Program of China 973 program no. 2012CB517600 (no. 2012CB517606) and Small Project Funding (Project code: 201109176044) from the University of Hong Kong. W.H.Y. is partially supported by an Endowment Fund established for the ‘Yu Professorship in Nephrology’ awarded to S.C.W.T., and the Hong Kong Concrete and the Continental Cement and Gypsum Co. Ltd. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Part of the results from this manuscript has been presented in abstract form at the American Society of Nephrology Kidney Week, 8–13 Nov, 2011, Philadelphia, PA, USA.