Abstract
Introduction. Heme oxygenase (HO) isoforms, HO-1, and
HO-2, are responsible for heme breakdown to iron and
carbon monoxide (CO). HO may respond to oxidative stress
and may modulate the expression of vasoactive factors like
nitric oxide (NO). Since diabetes induced oxidative stress
may change HO, the present study examined whether dia-
betes is associated with HO alterations, its relationship with
NO, endothelin-1(ET-1) and the functional significance.
Materials & Methods. Male SD rats with Streptozotocin
induced diabetes were investigated after six-weeks. Poorly
controlled diabetic animals were randomized to one of three
treatment groups (n = 6 each group); a) untreated, b) HO-1
inhibitor SnPP-IX (50 mmol/kgIP/day), c) NO donor mol-
sidomine (120mg/L PO/day) and were compared with age
and sex matched non diabetic control animals with or without
SnPP-IX treatment. Color Doppler ultrasound analysis was
used to determine retinal resistivity index (RI). mRNA for
HO-1, HO-2, ET-1, eNOS and iNOS were analyzed with
competitive RT-PCR. HO distribution in the retina was inves-
tigated by immunocytochemistry.
Results. Diabetic animals expressed lower body weight,
higher blood glucose and increased glycated hemoglobin
levels. HO-1 and HO-2 immuno-reactivity were identified in
the retina. Diabetes induced increased RI was associated with
up-regulation of both ET-1 and HO-1 mRNA expression
but not eNOS or iNOS mRNA. Both SnPP-IX and molsido-
mine treatments prevented a diabetes increase of RI, in spite
of increased ET-1 expression and were associated with
increased iNOS mRNA.
Conclusions. The present data suggests that the HO system
is up-regulated in short term diabetes leading to HO and NO
interactions which may modulate vascular function in the
retina.
Keywords: heme oxygenase; retina; diabetes; mRNA; blood
flow
Introduction
Diabetes is recognized as a worldwide problem reaching near
epidemic levels.
1
Associated with both type 1 and 2 diabetes
is the development of secondary diabetic complications,
which are linked to increased morbidity and mortality.
2
Dia-
betic retinopathy predominantly affects the microvasculature
of the retina.
3
The Diabetes Control and Complications Trial
identified hyperglycemia as one of the main initiating factors
of diabetic complications.
4
During the early stages of the
disease, hyperglycemia causes increased vascular permeabil-
ity and blood flow changes.
5
Alterations of several vasoac-
tive molecules and cytokines such as decreased nitric oxide
(NO), increased angiotensin II, endothelin (ET) and vascu-
lar endothelial growth factor (VEGF) have been demon-
strated in the retina in early diabetes.
6,7
Hyperglycemia has also been demonstrated to increase
oxidative stress.
8
Associated with oxidative stress are specific
biochemical changes including protein kinase C (PKC)
activation, the non-enzymatic glycation of proteins and
increased polyol pathway activity.
3,9
Oxidative stress may
further lead to increased expression of heme oxygenase
(HO). HO catalyses the conversion of heme to biliverdin
with the release of carbon monoxide (CO) and free iron.
Biliverdin is subsequently converted to bilirubin by the
enzyme biliverdin reductase.
10
To date, three isoforms (HO-
1, HO-2, and HO-3) have been characterized with the great-
est research completed with HO-1 and HO-2. HO-1 is also
known as heat shock protein 32 (hsp 32). The protein is
extremely sensitive to both oxidative and cellular stresses.
11
HO-2 is expressed constitutively by endothelial cells, neural
Received: April 28, 2003
Accepted: August 1, 2003
Correspondence: Subrata Chakrabarti, MD, PhD, FRCP(C), University of Western Ontario, Department of Pathology, Dental Sciences
Building, London, Ontario, Canada N6A 5C1. Tel: 519-661-2030; Fax: 519-661-2930; E-mail: schakrab@uwo.ca
Heme oxygenase in the retina in diabetes
Mark Cukiernik
1
, Suranjana Mukherjee
1
, Donal Downey
2
and Subrata Chakabarti
1,3
Departments of
1
Pathology,
2
Diagnostic Radiology and
3
Microbiology & Immunology, University of Western Ontario,
London, Ontario, Canada
Current Eye Research 0271-3683/03/2705-301$16.00
2003, Vol. 27, No. 5, pp. 301–308 © Swets & Zeitlinger