H(2)S inhibits hyperglycemia-induced intrarenal renin-angiotensin system activation via attenuation of reactive oxygen species generation

PLoS One. 2013 Sep 13;8(9):e74366. doi: 10.1371/journal.pone.0074366. eCollection 2013.

Abstract

Decrease in endogenous hydrogen sulfide (H2S) was reported to participate in the pathogenesis of diabetic nephropathy (DN). This study is aimed at exploring the relationship between the abnormalities in H2S metabolism, hyperglycemia-induced oxidative stress and the activation of intrarenal renin-angiotensin system (RAS). Cultured renal mesangial cells (MCs) and streptozotocin (STZ) induced diabetic rats were used for the studies. The expressions of angiotensinogen (AGT), angiotensin converting enzyme (ACE), angiotensin II (Ang II) type I receptor (AT1), transforming growth factor-β1 (TGF-β1) and collagen IV were measured by real time PCR and Western blot. Reactive oxygen species (ROS) production was assessed by fluorescent probe assays. Cell proliferation was analyzed by 5'-bromo-2'-deoxyuridine incorporation assay. Ang II concentration was measured by an enzyme immunoassay. AGT, ACE and AT1 receptor mRNA levels and Ang II concentration were increased in high glucose (HG) -treated MCs, the cell proliferation rate and the production of TGF-β1 and of collagen IV productions were also increased. The NADPH oxidase inhibitor diphenylenechloride iodonium (DPI) was able to reverse the HG-induced RAS activation and the changes in cell proliferation and collagen synthesis. Supplementation of H2S attenuated HG-induced elevations in ROS and RAS activation. Blockade on H2S biosynthesis from cystathione-γ-lyase (CSE) by DL-propargylglycine (PPG) resulted in effects similar to that of HG treatment. In STZ-induced diabetic rats, the changes in RAS were also reversed by H2S supplementation without affecting blood glucose concentration. These data suggested that the decrease in H2S under hyperglycemic condition leads to an imbalance between oxidative and reductive species. The increased oxidative species results in intrarenal RAS activation, which, in turn, contributes to the pathogenesis of renal dysfunction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetophenones / pharmacology
  • Angiotensin II Type 1 Receptor Blockers / pharmacology
  • Angiotensinogen / genetics
  • Angiotensinogen / metabolism
  • Animals
  • Blood Glucose / metabolism
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Collagen Type IV / metabolism
  • Cystathionine beta-Synthase / genetics
  • Cystathionine beta-Synthase / metabolism
  • Cystathionine gamma-Lyase / genetics
  • Cystathionine gamma-Lyase / metabolism
  • Diabetes Mellitus, Experimental / enzymology
  • Diabetes Mellitus, Experimental / genetics
  • Diabetes Mellitus, Experimental / pathology
  • Glucose / pharmacology
  • Hydrogen Sulfide / pharmacology*
  • Hyperglycemia / enzymology
  • Hyperglycemia / genetics
  • Hyperglycemia / metabolism*
  • Hyperglycemia / pathology
  • Kidney / drug effects
  • Kidney / pathology*
  • Losartan / pharmacology
  • Mesangial Cells / drug effects
  • Mesangial Cells / metabolism
  • Mesangial Cells / pathology
  • NADPH Oxidases / metabolism
  • Onium Compounds / pharmacology
  • Peptidyl-Dipeptidase A / genetics
  • Peptidyl-Dipeptidase A / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Rats
  • Reactive Oxygen Species / metabolism*
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptor, Angiotensin, Type 1 / metabolism
  • Renin-Angiotensin System / drug effects*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • Acetophenones
  • Angiotensin II Type 1 Receptor Blockers
  • Blood Glucose
  • Collagen Type IV
  • Onium Compounds
  • RNA, Messenger
  • Reactive Oxygen Species
  • Receptor, Angiotensin, Type 1
  • Transforming Growth Factor beta1
  • Angiotensinogen
  • diphenyleneiodonium
  • acetovanillone
  • NADPH Oxidases
  • Peptidyl-Dipeptidase A
  • Cystathionine beta-Synthase
  • Cystathionine gamma-Lyase
  • Glucose
  • Losartan
  • Hydrogen Sulfide

Grants and funding

This research was financially supported by the Natural Science Foundation of China (No. 81070577, 81170636) to LL, (No. 81000280) to XH, (No. 81100531) to ZW and an operating grant from Canadian Diabetes Association to RW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.