Molecular Vision 2006; 12:405-14 <http://www.molvis.org/molvis/v12/a47/>
Received 15 April 2005 | Accepted 10 April 2006 | Published 20 April 2006
Proliferative diabetic retinal disease is a major cause of
blindness in the Western world [1]. Microvascular occlusion
leads to both hypoxia and ischemia due to nonperfusion of the
inner retina [2-4]. The hypoxic retina responds by generating
growth factors, including vascular endothelial growth factor
(VEGF), culminating in excessive proliferation of new blood
vessels within the retina, often extending into the vitreous [5-
8].
The conversion of arachidonic acid to prostaglandin H
2
(PGH
2
) by the cyclooxygenase (COX) enzymes is the rate-
limiting reaction in the synthesis of prostaglandins [9]. The
COX enzymes exist as two distinct isoforms, COX-1 and
COX-2. COX-1 is largely a constitutive isoform, whereas
COX-2 is induced in response to many different stimuli [9],
including ischemia. The products of these enzymes, the pros-
taglandins, influence a wide range of biological processes of
relevance to ischemic proliferative retinopathies. These include
vascular tone, platelet activity, inflammation, and angiogen-
esis [10,11].
Inhibitors of COX suppress angiogenesis in in vitro and
in vivo models of excess neovascularization [12-15]. Both
COX isoforms have been implicated as signals for angiogenic
factors (VEGF, integrin engagement) and as inducers of VEGF
expression [16,17]. COX-2 has also been reported to drive the
angiogenic response in ocular vascular beds. Disruption of
the COX-2 gene inhibits inflammation-induced corneal an-
giogenesis, but not that induced by VEGF [18]. COX-1 is also
reported to regulate the response of endothelial cells to angio-
genic factors [19]. Both COX isoforms are expressed in mouse,
rat, and human retina [20]. Recent studies have shown that
selective and nonselective COX-inhibitors attenuate retinal
neovascularization in a mouse model of oxygen-induced ret-
inopathy [21-23].
The aim of the present study was to examine the contri-
bution of each COX isozyme to retinal ischemia and
neovascularization by using mice with specific disruption of
either the COX-1 or COX-2 isoform in a model of prolifera-
tive retinopathy. This approach allows the evaluation of the
role of each isoform in oxygen-induced retinopathy without
the confounding nonspecific effects of pharmacological COX
inhibitors [24].
METHODS
Murine model of oxygen-induced retinopathy: C57BL/6J x
129/Ola mice with a targeted disruption of either the COX-1
gene (COX-1
-/-
) or the COX-2 gene (COX-2
-/-
) were gener-
ously provided by R. Langenbach (Laboratory of Environ-
mental Carcinogenesis and Mutagenesis, National Institute of
Environmental Health Sciences, National Institute of Health,
Triangle Park, NC) [25,26]. The mice were employed in an
established model of oxygen-induced retinopathy [27]. Wild-
type mice used in these experiments were of the same genetic
background (C57BL/6J x 129/Ola). Litters of 7-day-old mice
©2006 Molecular Vision
COX-2 protects against thrombosis of the retinal vasculature in a
mouse model of proliferative retinopathy
Lorna M. Cryan,
1
Graham P. Pidgeon,
1
Desmond J. Fitzgerald,
2
Colm J. O’Brien
3
1
Department of Clinical Pharmacology, Royal College of Surgeons in Ireland, Dublin, Ireland; Departments of
2
Molecular Medi-
cine and
3
Ophthalmology, Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin, Ireland
Purpose: Cyclooxygenases (COX-1 and COX-2) and prostaglandins regulate angiogenesis in several settings, including
cancer and ischemia. In the eye, both selective inhibitors of COX-2 and nonselective COX inhibitors are reported to
suppress ischemia-related retinal angiogenesis. Such studies however, may be confounded by the nonspecific effects of
inhibitors.
Methods: Mice lacking either the COX-1 (COX-1
-/-
) or COX-2 isoform (COX-2
-/-
) were employed in a model of oxygen-
induced retinopathy. Vascular responses were examined by histology, isolectin B4 staining of the abluminal endothelium,
and retinal fluorescein angiography.
Results: There was an increase in intravitreal endothelial nuclei in hyperoxia-treated mice compared to normoxic controls
irrespective of the genotype. Quantitative analysis of fluorescein-perfused and isolectin B4-stained retinal angiograms at
postnatal day 18 (P18) revealed similar global levels of neovascular tufts in hyperoxia-treated wild-type, COX-1
-/-
, and
COX-2
-/-
mice. However, hyperoxia-treated COX-2
-/-
mice had increased areas of retinal nonperfusion (29.2±1.9 com-
pared to 16.3±2.7; n=6; p<0.001). COX-1 disruption had no effect (15.6±2.6; n=8). Platelet deposition within retinal
vessels was increased in hyperoxia-treated COX-2
-/-
mice (p<0.05).
Conclusions: Genetic disruption of a single COX isoform is not sufficient to prevent oxygen-induced retinopathy. COX-
2 protects retinal vessels from thrombosis, limiting the area of retinal nonperfusion in oxygen-induced retinopathy.
Correspondence to: Colm O’Brien, MD, Institute of Ophthalmol-
ogy, Mater Misericordiae Hospital, 60 Eccles Street, Dublin 7, Ire-
land; Phone: 353-1-8386730; FAX: 353-1-8305693; email:
cobrien@mater.ie
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