Original Article
Vascular Endothelial Growth Factor in Ocular Fluid of Patients with Diabetic Retinopathy and Other Retinal Disorders
N Engl J Med 1994; 331:1480-1487December 1, 1994
- Abstract
Background
Retinal ischemia induces intraocular neovascularization, which often leads to glaucoma, vitreous hemorrhage, and retinal detachment, presumably by stimulating the release of angiogenic molecules. Vascular endothelial growth factor (VEGF) is an endothelial-cell-specific angiogenic factor whose production is increased by hypoxia.
Methods
We measured the concentration of VEGF in 210 specimens of ocular fluid obtained from 164 patients undergoing intraocular surgery, using both radioimmunoassays and radioreceptor assays. Vitreous proliferative potential was measured with in vitro assays of the growth of retinal endothelial cells and with VEGF-neutralizing antibody.
Results
VEGF was detected in 69 of 136 ocular-fluid samples from patients with diabetic retinopathy, 29 of 38 samples from patients with neovascularization of the iris, and 3 of 4 samples from patients with ischemic occlusion of the central retinal vein, as compared with 2 of 31 samples from patients with no neovascular disorders (P<0.001, P<0.001, and P = 0.006, respectively). The mean (±SD) VEGF concentration in 70 samples of ocular fluid from patients with active proliferative diabetic retinopathy (3.6 ±6.3 ng per milliliter) was higher than that in 25 samples from patients with nonproliferative diabetic retinopathy (0.1 ±0.1 ng per milliliter, P = 0.008), 41 samples from patients with quiescent proliferative diabetic retinopathy (0.2 ±0.6 ng per milliliter, P<0.001), or 31 samples from nondiabetic patients (0.1 ±0.2 ng per milliliter, P = 0.003). Concentrations of VEGF in vitreous fluid (8.8 ±9.9 ng per milliliter) were higher than those in aqueous fluid (5.6 ±8.6 ng per milliliter, P = 0.033) in all 10 pairs of samples obtained simultaneously from the same patient; VEGF concentrations in vitreous fluid declined after successful laser photocoagulation. VEGF stimulated the growth of retinal endothelial cells in vitro, as did vitreous fluid containing measurable VEGF. Stimulation was inhibited by VEGF-neutralizing antibodies.
Conclusions
Our data suggest that VEGF plays a major part in mediating active intraocular neovascularization in patients with ischemic retinal diseases, such as diabetic retinopathy and retinal-vein occlusion.
Media in This Article
Figure 1
Classification of Active and Quiescent Intraocular Neovascularization.Figure 2
Concentrations of Immunoreactive VEGF in Ocular Fluids from Patients Undergoing Intraocular Surgery.Article Activity
- Article
Intraocular neovascularization occurs in numerous ischemic retinal disorders, including diabetic retinopathy, ischemic retinal-vein occlusion, and retinopathy of prematurity1,2. This proliferation often results in vitreous hemorrhage, retinal detachment, and neovascular glaucoma, with subsequent visual loss. Although numerous growth factors stimulate angiogenesis in vivo,3-6 these factors are not consistently increased in proliferative retinopathies5,6 or secreted, as would be expected if they caused intraocular neovascularization at sites distant from those of retinal ischemia.
In neovascular retinopathies such as proliferative diabetic retinopathy, there is initially extensive active proliferation of new vessels1,7. Visual loss at this time results from vitreous hemorrhage or fluid exudation from fragile new vessels. With time, or after laser photocoagulation, the proliferating vessels become fibrotic and involute, causing traction on the retina that may lead to complications such as retinal detachment8,9. Eventually the disease becomes inactive and further visual loss ceases10. The timely inhibition of factors that cause active vascular proliferation may prevent visual loss.
To account for the clinical manifestations of neovascular disease induced by ocular ischemia, it has been hypothesized that a causative substance is produced in the retina. The hypothetical substance is induced by retinal ischemia and is angiogenic, diffusible, more concentrated in vitreous than in aqueous humor, increased during active proliferation, reduced during quiescent proliferation, and diminished after successful laser therapy. Vascular endothelial growth factor (VEGF) is a candidate for such a substance. It is an endothelial-cell-specific angiogenic11 and vasopermeable12 factor that binds to high-affinity, membrane-bound receptors with tyrosine kinase activity13,14. Its expression is induced by hypoxia in tumors12,15-17. VEGF is secreted in four homodimeric forms resulting from alternative RNA splicing18. In ocular tissues its production is increased by hypoxia in retinal pigment epithelial cells19 and retinal pericytes,20,21 and by ischemia-induced neovascularization of the iris in primate eyes22. In our study we attempted to ascertain whether intraocular concentrations of VEGF correlated with active neovascularization and to determine whether VEGF fulfilled the other criteria23 hypothesized for an angiogenic factor in ischemic ocular disorders.
Methods
Study Subjects
Undiluted samples of aqueous, vitreous, and subretinal fluid were obtained from patients undergoing intraocular surgery. The protocol for sample collection was approved by the institutional review board at each institution, and all patients gave informed consent. The surgical procedures included cataract extraction, trabeculectomy, anterior-chamber paracentesis, pars plana vitrectomy, scleral buckling, and pneumatic retinopexy. The patients' primary diagnoses included cataract, chronic open-angle glaucoma, traumatic glaucoma, phacolytic glaucoma, proliferative diabetic retinopathy, neovascular glaucoma, stage 5 retinopathy of prematurity, ischemic central-retinal-vein occlusion, vitreous hemorrhage, traction or rhegmatogenous retinal detachment, macular pucker, endophthalmitis, leukemic retinopathy, epiretinal membrane, choroidal neovascular membrane, uveitis, and retinitis.
Clinical data, including determinations of ocular neovascular activity, were obtained from the surgeon at the time of surgery with standardized forms and were confirmed by standardized fundus photography whenever possible. Neovascularization was considered to be active if there were perfused, multibranching iridic or preretinal capillaries (Figure 1AFigure 1
Classification of Active and Quiescent Intraocular Neovascularization.) and to be quiescent if previously documented active proliferation had regressed fully or if only nonperfused, gliotic vessels or fibrosis was present (Figure 1B).The results in patients with retinal neovascularization were compared with those in patients with the same underlying disorders but no retinal neovascularization and with those in patients with no known underlying potentially neovascularizing disorder. We therefore excluded from this group patients with diabetes mellitus, rubeosis iridis, retinal detachment, choroidal neovascular membranes, retinopathy of prematurity, central-retinal-vein occlusion, uveitis, and retinitis. The indications for surgery in the control group included cataract, chronic open-angle glaucoma, angle-recession glaucoma, and idiopathic epiretinal membrane.
Sample Collection
The samples of ocular fluid were collected in sterile tubes (Thomas Scientific, Swedesboro, N.J.), placed immediately on ice, clarified by centrifugation at 16,000 × g for five minutes at 4 °C, and rapidly frozen at -80 °C. The samples were shipped by overnight mail in dry ice with accompanying data on the patient to the Joslin Diabetes Center, where they were catalogued and labeled in an anonymous fashion. The specimens were then shipped without identifying clinical information to Genentech for the VEGF immunologic and receptor-binding assays.
Radioimmunoassay
Concentrations of VEGF in ocular fluid were measured by radioimmunometric assay with two monoclonal antibodies that bound to different epitopes on VEGF165 and longer isoforms24. The assays were performed in 96-well immunoplates (Immunlon-1, Dynatech, Chantilly, Va.); each well was coated with 100 microliters of a solution containing 10 μg of anti-VEGF monoclonal antibody 5F8 (similar to antibody B2.6.224) per milliliter of solution in 50-mM carbonate buffer (pH 9.6) for 16 hours at 4 °C. The plates were washed three times, blocked for one hour at 25 °C with 300 microliters of 0.5 percent bovine serum albumin and 0.03 percent Tween 80 in phosphate-buffered saline (pH 7.4) per well, and washed subsequently with 0.03 percent Tween 80 in phosphate-buffered saline (pH 7.4) before the addition of diluted samples of ocular fluid (in duplicate measurements of three to six serial twofold dilutions) or standard solutions of VEGF165 (range, 20 pg per milliliter to 50 μg per milliliter).
The plates were incubated for two hours at 25 °C with gentle agitation, the supernatants were discarded, and the wells washed. One hundred microliters of a solution containing 2 × 104 cpm of 125I-labeled anti-VEGF165 monoclonal antibody 2E3 (similar to antibody A4.6.124) was added, and the plates were incubated for two hours at 25 °C with gentle agitation. The supernatants were discarded, the plates washed, and the wells counted by gamma scintigraphy (LKB gamma counter, Gaithersburg, Md.). Concentrations of VEGF were quantitated from a standard curve for VEGF with a four-parameter fit (Kaleidagraph, Synergy Software, Reading, Pa.). The sensitivity of the assay was 0.05 ng per milliliter. The intraassay and interassay coefficients of variation were 5 and 6 percent, respectively. Ocular-fluid samples with undetectable VEGF concentrations in this assay or the receptor-binding assay (described below) were assigned values of 0.05 ng per milliliter.
Receptor-Binding Assay
The procedure for the receptor-binding assay was similar to that used in the radioimmunoassay, except that 125I-labeled fms-like tyrosine kinase (Flt-1) receptor-IgG chimeric protein was used instead of 125I-labeled anti-VEGF monoclonal antibody 2E3. The 5F8 monoclonal anti-VEGF antibody used to coat the plates does not interfere with ligand-receptor binding. Flt-1 is a high-affinity VEGF receptor25. Its entire extracellular domain (758 residues) was cloned by the polymerase chain reaction with Pfu polymerase and fused to the coding sequence for amino acids 216 through 443 of an IgGγ1 heavy-chain clone,26 as described by Park et al27. The chimeric receptor has the same affinity for VEGF as does the full-length VEGF receptor. The sensitivity and variability of this assay were similar to those of the radioimmunoassay.
Assay of Retinal Vascular Endothelial-Cell Growth
Bovine endothelial cells from the retinal microvasculature were isolated by homogenization and a series of filtration steps as described elsewhere28. Primary cultures were grown in fibronectin-coated dishes (NYBen Reagents, New York Blood Center, New York) containing Dulbecco's modified Eagle's medium with 5.5 mM glucose, 10 percent horse serum (Wheaton, Pipersville, Pa.), 50 mg of heparin per liter, and 50 units of endothelial-cell growth factor per liter (Boehringer Mannheim, Indianapolis). After the cultures were confluent, the medium was changed to include 5 percent fetal-calf serum (Hyclone, South, Utah). The cells were fed every three days. Endothelial-cell homogeneity was confirmed with anti-factor VIII antibodies. For the assay, the cells were plated sparsely (2500 cells per well) in 24-well dishes (Costar, Cambridge, Mass.) and incubated overnight in Dulbecco's modified Eagle's medium containing 10 percent calf serum (GIBCO, Grand Island, N.Y.). The mediums were changed the next day, and either VEGF or vitreous fluid (final volume, 15 to 25 percent) was added, with either phosphate-buffered saline or a 1- to 10-fold excess of VEGF-neutralizing rabbit polyclonal antibody. After incubation at 37 °C for four days, the cells were lysed in 0.1 percent sodium dodecyl sulfate, and the DNA content was measured with dye (Hoechst 33258, Hoefer Scientific Instruments, San Francisco) and a fluorometer (model TKO-100, Hoefer). A statistically significant growth response could be detected at concentrations of VEGF as low as 0.1 ng per milliliter. The plates were assayed in triplicate, and each experiment was repeated at least three times unless otherwise indicated.
Statistical Analysis
Categorical data were compared by Fisher's exact test. The unpaired Student's t-test was used to compare quantitative data with normal distributions. Log-normal transformed data were analyzed by the paired t-test for comparisons with unequal variance before and after laser treatment. Immunoreactivity and receptor-binding correlations were determined with linear regression analysis (sum of squares), and significance was calculated from the mean-square F ratio. Ocular-gradient results were analyzed with the paired Student's t-test. Values are reported as means ±SD. Two-tailed test results were considered statistically significant at P ≤ 0.05.
Results
We obtained 210 samples of ocular fluid from 171 eyes of 164 patients (88 women and 76 men) undergoing intraocular surgery. Sixty-five percent of the patients were white, 15 percent were black, 5 percent were Hispanic, and 15 percent were of other or undetermined descent. The mean age of the 31 patients with no known neovascular disorders was 64 years (range, 10 to 89), and the mean age of the 113 patients with proliferative diseases was 57 years (range, 5 months to 89 years). These groups did not differ with regard to sex or ethnic background. The mean ages of the patients with nonproliferative and proliferative diabetic retinopathy were 69 and 53 years, respectively, but there was no difference in mean age among the patients with active proliferative diabetic retinopathy, quiescent proliferative diabetic retinopathy, or neovascularization of the iris (51, 55, and 51 years, respectively). The patients with no neovascular disorders and those with nonproliferative diabetic retinopathy were slightly older than those with proliferative diabetic retinopathy or neovascularization of the iris, probably because the first two of these groups primarily undergo surgery for conditions (e.g., cataract) associated with advancing age. Only two patients with neovascularization had not received retinal laser photocoagulation before the collection of ocular fluids. There was no correlation of VEGF concentrations with age, sex, or ethnic background in any subgroup.
Detection of VEGF in Ocular Fluid
The number and percentage of samples of aqueous and vitreous fluid with detectable concentrations of immunoreactive VEGF are shown in Table 1Table 1
Concentrations of Immunoreactive VEGF in Ocular Fluids of Patients with Retinal Disorders.; results for subretinal-fluid samples are presented in a footnote to Table 1. VEGF was detected in 2 of 31 samples from patients with no neovascular disorder, 69 of 136 samples from patients with diabetes mellitus, 29 of 38 samples from patients with neovascularization of the iris, 5 of 9 samples from patients with chronic retinal detachment, and 3 of 4 samples from patients with central-retinal-vein occlusion. Among patients with diabetes mellitus, VEGF was detectable in 58 of 70 samples from patients with active proliferative retinopathy, as compared with 9 of 41 samples from patients with quiescent proliferative retinopathy and 2 of 25 samples from patients with nonproliferative diabetic retinopathy. VEGF was detected in similar proportions in both aqueous and vitreous fluids among the various groups of patients. It was not detected in any sample collected from patients with endophthalmitis, leukemic retinopathy, uveitis, retinitis, epiretinal membrane, or choroidal neovascular membrane. VEGF was detected in 47 percent of 68 patients with retinal detachment, although 39 had concurrent proliferative diabetic retinopathy. When patients with diabetes mellitus were excluded, VEGF was detected in 5 of 9 samples from patients with chronic retinal detachment (i.e., lasting more than three weeks), as compared with 1 of 31 samples from patients without neovascular disorders (P = 0.003). Mean concentrations of VEGF were higher in samples from patients with chronic retinal detachment (2.8 ±4.7 ng per milliliter) than patients with acute retinal detachment (0.1 ±0.1 ng per milliliter, P = 0.024).VEGF Concentrations and Ocular Neovascularization
The VEGF concentrations in samples of aqueous and vitreous humor from patients without neovascular disorders were compared with those in samples from patients with active or quiescent neovascularization (Figure 2Figure 2
Concentrations of Immunoreactive VEGF in Ocular Fluids from Patients Undergoing Intraocular Surgery.). VEGF was detectable in only 13 of 96 samples from patients with no active neovascularization (mean, 0.1 ±0.4 ng per milliliter), and when detectable, the concentrations were low (0.7 ±0.9 ng per milliliter). The mean VEGF concentration in 70 samples from patients with active proliferative diabetic retinopathy (3.6 ±6.3 ng per milliliter) was significantly higher than that in 31 samples from nondiabetic patients with no proliferative disorder (0.1 ±0.2 ng per milliliter, P = 0.003) and that in 41 samples from patients with quiescent proliferative diabetic retinopathy (0.2 ±0.6 ng per milliliter, P<0.001). The concentrations of VEGF were also high in samples from patients with active proliferation from ischemic central-retinal-vein occlusion, retinopathy of prematurity, or rubeosis iridis. The concentrations were similar when samples of aqueous and vitreous humor were considered individually (Table 2Table 2
Concentrations of Immunoreactive VEGF in Aqueous and Vitreous Fluids.).Determination of Intraocular Gradient of VEGF
Simultaneously collected samples of fluid from the anterior segment (aqueous humor) and the posterior segment (either vitreous humor or subretinal fluid) were tested for VEGF in 14 patients, 10 of whom had active ocular neovascularization and detectable VEGF in the posterior segment. In each of these patients, the posterior-segment VEGF concentration exceeded the aqueous concentration. The mean posterior-segment VEGF concentration was almost 60 percent higher (8.8 ±9.9 vs. 5.6 ±8.6 ng per milliliter, P = 0.033).
Response of VEGF after Treatment of Ocular Neovascularization
Collecting ocular fluids before and after treatment for neovascularization is difficult, because patients who undergo surgery rarely require subsequent procedures. We studied six patients with active neovascularization and one patient with quiescent neovascularization, from each of whom two samples of ocular fluid were collected. The subsequent procedures involved were trabeculectomy (one patient), second vitrectomy (five patients), and anterior-chamber paracentesis (one patient). All the patients had also undergone panretinal laser photocoagulation for neovascularization in the interval between the two operations, and the extent of proliferation had decreased. The intraocular concentrations of VEGF were reduced by an average of 75 percent (from 5.6 ±6.5 to 1.4 ±2.0 ng per milliliter, P = 0.008) in all the patients after successful treatment.
Receptor-Binding Capacity of Ocular VEGF
Among the 19 vitreous-fluid samples randomly tested, all 16 samples with detectable immunoreactive VEGF also had receptor-binding activity, as compared with none of the 3 samples without detectable immunoreactive VEGF. The receptor-binding concentration was 45 percent of the immunoreactivity concentration, and the correlation between the two types of activity was statistically significant (R2 = 0.93, P<0.001).
Stimulation of Retinal Vascular Endothelial-Cell Growth by Ocular VEGF
The number of retinal endothelial cells was increased in vitro in a dose-dependent manner after exposure to 5 or 10 ng of VEGF per milliliter. VEGFneutralizing antibodies blocked this stimulatory effect (Figure 3Figure 3
Growth of Retinal Endothelial Cells in Response to VEGF.). The maximally effective VEGF concentration was 25 ng per milliliter, and the half-maximally effective concentration was 1 ng per milliliter (data not shown).To determine whether VEGF in human vitreous was bioactive, the endothelial proliferative activity of pooled samples of vitreous humor from five patients with active proliferative diabetic retinopathy, a single patient with active proliferative diabetic retinopathy, and pooled samples from six patients with quiescent proliferative diabetic retinopathy was measured. The concentrations of VEGF in these samples were 4.0, 3.3, and <0.05 ng per milliliter, respectively. All the samples stimulated retinal endothelial-cell growth (Figure 4Figure 4
Growth of Retinal Endothelial Cells in Response to VEGF in Vitreous Fluid.). The addition of VEGF-neutralizing antibody did not significantly reduce the response to vitreous fluid from patients with quiescent retinopathy, but it inhibited by 65 percent the response to vitreous fluid from patients with active proliferative diabetic retinopathy.Discussion
We found detectable concentrations of VEGF in ocular fluid from patients with active retinal and anterior-segment neovascularization associated with several ocular diseases with underlying retinal ischemia. In the patients with active neovascularization, VEGF concentrations in the aqueous and vitreous fluid were higher than those that have stimulated endothelial-cell proliferation in vitro and in vivo22. In patients with quiescent neovascularization resulting from retinopathy of prematurity, central-retinal-vein occlusion, or diabetes mellitus, concentrations of VEGF were low or undetectable.
The clinical observation that anterior-segment neovascularization commonly arises in conjunction with ischemic retinal disease suggests a gradient-driven diffusion of angiogenic factors from the posterior to the anterior segment of the eye. Among all the samples, concentrations of VEGF were higher in aqueous than in vitreous fluid, but in simultaneously collected samples the concentrations of VEGF in vitreous fluid were always higher. This gradient may result from the rapid clearance of VEGF from the anterior chamber or from its increased use or more rapid degradation in that chamber. Nevertheless, a vitreous-to-aqueous gradient would promote the anterior diffusion of VEGF, potentially accounting for the clinically observed anterior-segment neovascularization associated with retinal ischemia.
Panretinal photocoagulation induces the regression of clinically active ocular neovascularization8,9. We found that concentrations of VEGF declined in all patients who had decreased neovascular activity after laser photocoagulation. Presumably, the reduction in retinal ischemia after laser therapy reduces the production of angiogenic factors, suppressing neovascularization. Indeed, ischemia-induced VEGF production is reversible by the reinstitution of a normal oxygen supply in vitro21,29.
Vitreous fluid from patients without active retinal neovascularization stimulated the growth of retinal endothelial cells, as have retinal extracts from normal eyes30. In samples of vitreous from patients with active proliferative diabetic retinopathy and high concentrations of VEGF, anti-VEGF antibodies reduced in vitro stimulation of growth by more than 65 percent, to values similar to those in samples from patients with quiescent neovascularization and undetectable concentrations of VEGF. The incomplete inhibition of growth-stimulatory activity suggests the simultaneous activity of other proliferative factors. Indeed, vitreous concentrations of basic fibroblast growth factor,31 insulin-like growth factors, and insulin-like growth factor-binding proteins are increased in patients with diabetic retinopathy and rubeosis iridis5.
VEGF is present in the ocular membranes of patients with proliferative diabetic retinopathy,32 hypoxia stimulates the secretion of VEGF in retinal pigment epithelial cells,29 and VEGF production increases with neovascularization of the iris in primates22. We have reported that retinal endothelial cells have large numbers of high-affinity VEGF receptors14 and that hypoxia increases the VEGF content of messenger RNA (mRNA) in retinal pericytes, retinal endothelial cells, and retinal pigment epithelial cells -- an effect reversed by the reinstitution of normal oxygenation21. These observations suggest a plausible scenario for the initiation and control of the ischemic ocular neovascular response. Alterations in retinal perfusion arising from decreased blood flow (e.g., central-retinal-vein occlusion or carotid occlusive disease33-35), retinal-capillary loss (resulting from diabetic retinopathy or radiation retinopathy, for example), peripheral-vasculature agenesis or obliteration (with, e.g., retinopathy of prematurity or sickle cell disease), or separation of the choroidal blood supply from the retinal pigment epithelium (with, e.g., retinal detachment) can all result in relative retinal ischemia. This ischemia stimulates the synthesis and secretion of VEGF in retinal pericytes, endothelial cells, the retinal pigment epithelium, and possibly other cell types. Depending on the particular variant of mRNA splicing,18 secreted VEGF is either bound to cell-surface or basement-membrane proteoglycans containing heparin (VEGF189,286) or is freely diffusible within the vitreous cavity (VEGF121,165)36. Diffusible VEGF follows its concentration gradient from the vitreous to the anterior segment and is ultimately cleared through the trabecular meshwork. Neovascularization induced by the direct action of VEGF on endothelial cells can arise anywhere along this course, especially in areas of high exposure, such as the pupillary border and the trabecular meshwork. The angiogenic potential of VEGF is enhanced by the synergistic activity of fibroblast growth factor liberated by cellular disruption or death4,37,38. Cell death without ischemia would have less vasoproliferative potential, since increased VEGF production would not be possible. Indeed, the risk of ocular neovascularization in anoxic retinal disorders, such as retinal-artery occlusion, is lower than in ischemic diseases, such as retinal-vein occlusion33. The reduction in relative retinal ischemia as a result of reperfusion, laser photocoagulation, or extensive cell death may reduce the production of VEGF and result in neovascular regression and quiescence.
VEGF meets the criteria hypothesized for an ischemia-induced ocular angiogenic factor,23 and we suggest that it has an important role in mediating the neovascular response of diabetic retinopathy and other ischemic retinal disorders. Deciphering the mechanisms underlying the expression of hypoxia-induced VEGF and its biologic effects should increase our understanding of numerous ocular neovascular diseases and provide new therapeutic approaches to preserving vision.
Supported in part by a grant (EY05110) (to Dr. King) and a pilot and feasibility grant (DERC36836-08) (to Dr. L.P. Aiello), both from the National Institutes of Health; a Capps Scholarship in Diabetes (to Dr. L.P. Aiello); a Heed/Knapp Fellowship from the Heed Ophthalmic Foundation (to Dr. L.P. Aiello); and a Diabetes and Endocrinology Research Center Grant (36836) from the National Institutes of Health (to the Joslin Diabetes Center).
We are indebted to Ms. Leslie Balmat, Sven E. Bursell, Ph.D., Peter A. Campochiaro, M.D., Jerry D. Cavallerano, O.D., Ph.D., Leo T. Chylack, M.D., Eugene DeJuan, M.D., Mr. Dennis Fleming, Julia A. Haller, M.D., Jin Kim, Ph.D., Ms. Kimberly Keville, Mr. Ji Lu, Jeffrey Luttrull, M.D., and Pearl Yazbek, R.N., for their assistance in the acquisition of samples, the production of antibody, and the preparation of the manuscript.
Source Information
From the Department of Ophthalmology, Beetham Eye Institute (L.P.A., P.G.A., S.T.S., L.M.A.), and the Division of Research (L.P.A., H.T., G.L.K.), Joslin Diabetes Center; the Departments of Medicine and Ophthalmology, Brigham and Women's Hospital (L.R.P., M.A.I., G.L.K.); and Harvard Medical School (L.P.A., P.G.A., S.T.S., L.R.P., H.T., M.A.I., L.M.A., G.L.K.) -- all in Boston; the Neuroscience Research Institute, University of California, Santa Barbara (R.L.A.); Genentech, Inc., San Francisco (B.A.K., J.E.P., H.V.N., N.F.); and the Department of Ophthalmology, Wilmer Ophthalmological Institute, Johns Hopkins Hospital, Baltimore (H.D.J.).
Address reprint requests to Dr. L.P. Aiello at the Beetham Eye Institute, Joslin Diabetes Center, 1 Joslin Place, Boston, MA 02215.
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