ORIGINAL ARTICLE
Role of oxidative stress-induced systemic and cavernosal
molecular alterations in the progression of diabetic
erectile dysfunction
Angela CASTELA,
1,2
Pedro GOMES,
1,3
Valentina F. DOMINGUES,
4
Paula PAÍGA,
4
Raquel COSTA,
1
Pedro VENDEIRA
5
and Carla COSTA
1
Departments of
1
Biochemistry (U38/FCT) and
3
Pharmacology and Therapeutics, Center for Medical Research, Faculty of Medicine of the
University of Porto,
2
Institute for Molecular and Cell Biology of the University of Porto (IBMC-UP),
4
Requimte, Instituto Superior de
Engenharia, Instituto Politécnico do Porto, and
5
Clínica Saúde Atlântica, Clínica Urológica Vendeira, Porto, Portugal
Correspondence
Carla Costa, Faculty of Medicine of the
University of Porto, Department of
Biochemistry, Al. Prof Hernâni Monteiro,
4200-319 Porto, Portugal.
Tel: +351 225513654
Fax: +351 225513655
Email: carcosta@med.up.pt
Received 10 February 2014; revised 13
May 2014; accepted 1 June 2014.
doi: 10.1111/1753-0407.12181
Abstract
Background: Erectile dysfunction (ED) is a prevalent complication of dia-
betes, and oxidative stress is an important feature of diabetic ED. Oxidative
stress-induced damage plays a pivotal role in the development of tissue altera-
tions. However, the deleterious effects of oxidative stress in the corpus caver-
nosum with the progression of diabetes remain unclear. The aim of this study
was to evaluate systemic and penile oxidative stress status in the early and late
stages of diabetes.
Methods: Male Wistar streptozotocin-diabetic rats (and age-matched con-
trols) were examined 2 (early) and 8 weeks (late) after the induction of diabe-
tes. Systemic oxidative stress was evaluated by urinary H2O2 and the ratio of
circulating reduced/oxidized glutathione (GSH/GSSG). Penile oxidative
status was assessed by H2O2 production and 3-nitrotyrosine (3-NT) forma-
tion. Cavernosal endothelial nitric oxide synthase (eNOS) was analyzed by
quantitative immunohistochemistry. Dual immunofluorescence was also per-
formed for 3-NT and α-smooth muscle actin (α-SMA) and eNOS–α-SMA.
Results: There was a significant increase in urinary H2O2 levels in both
diabetic groups. The plasma GSH/GSSG ratio was significantly augmented in
late diabetes. In cavernosal tissue, H2O2 production was significantly
increased in late diabetes. Reactivity for 3-NT was located predominantly in
cavernosal smooth muscle (SM) and was significantly reduced in late diabetes.
Quantitative immunohistochemistry revealed a significant decrease in eNOS
levels in cavernosal SM and endothelium in late diabetes.
Conclusions: The findings indicate that the noxious effects of oxidative stress
are more prominent in late diabetes. Increased penile protein oxidative modi-
fications and decreased eNOS expression may be responsible for structural
and/or functional deregulation, contributing to the progression of diabetes-
associated ED.
Keywords: 3-nitrotyrosine, diabetes, endothelial nitric oxide synthase, erectile
dysfunction, oxidative stress.
Significant findings of the study: The noxious effects of oxidative stress are more prominent in advanced diabetes
and include an imbalance in systemic oxidative stress mechanisms, as well as increased penile protein oxidative
modifications and decreased endothelial nitric oxide synthase expression.
What this study adds: Deleterious oxidative events induced by diabetes contribute to erectile dysfunction, which
strengthens the relevance of preventative antioxidant therapy.
Journal of Diabetes 7 (2015) 393–401
393 © 2014 Ruijin Hospital, Shanghai Jiaotong University School of Medicine and Wiley Publishing Asia Pty Ltd