Dual-Acting Antiangiogenic Gene Therapy Reduces Inflammation and Regresses Neovascularization in Diabetic Mouse Retina

Molecular Therapy - Nucleic Acids - Tập 22 - Trang 329-339 - 2020
Rute S. Araújo1,2, Diogo B. Bitoque1,3, Gabriela A. Silva1,3
1CEDOC–Chronic Diseases Research Center, NOVA Medical School, Universidade Nova de Lisboa, Campo Mártires da Pátria 130, 1169-056 Lisbon, Portugal
2Bioengineering-Cell Therapies and Regenerative Medicine PhD Program, Instituto Superior Técnico, Universidade de Lisboa, Av. Rovisco Pais, 1049-001 Lisbon, Portugal
3NOVA Medical School, Universidade Nova de Lisboa, Campo Mártires da Pátria 130, 1169-056 Lisbon, Portugal

Tài liệu tham khảo

2016 Williams, 2004, Epidemiology of diabetic retinopathy and macular oedema: a systematic review, Eye (Lond.), 18, 963, 10.1038/sj.eye.6701476 Abcouwer, 2014, Diabetic retinopathy: loss of neuroretinal adaptation to the diabetic metabolic environment, Ann. N Y Acad. Sci., 1311, 174, 10.1111/nyas.12412 Frank, 2004, Diabetic retinopathy, N. Engl. J. Med., 350, 48, 10.1056/NEJMra021678 Roy, 2003, Downregulation of fibronectin overexpression reduces basement membrane thickening and vascular lesions in retinas of galactose-fed rats, Diabetes, 52, 1229, 10.2337/diabetes.52.5.1229 Moreno, 2013, Diabetic retinopathy, Nutr. Hosp., 28, 53 Kusuhara, 2018, Pathophysiology of Diabetic Retinopathy: The Old and the New, Diabetes Metab. J., 42, 364, 10.4093/dmj.2018.0182 Watkins, 2003, Retinopathy, BMJ, 326, 924, 10.1136/bmj.326.7395.924 Romero-Aroca, 2011, Managing diabetic macular edema: The leading cause of diabetes blindness, World J. Diabetes, 2, 98, 10.4239/wjd.v2.i6.98 Bandello, 2010, Steroids as part of combination treatment: the future for the management of macular edema?, Ophthalmologica, 224, 41, 10.1159/000315161 Dowler, 2003, Laser management of diabetic retinopathy, J. R. Soc. Med., 96, 277, 10.1177/014107680309600605 Kozak, 2015, Modern retinal laser therapy, Saudi J. Ophthalmol., 29, 137, 10.1016/j.sjopt.2014.09.001 Osaadon, 2014, A review of anti-VEGF agents for proliferative diabetic retinopathy, Eye (Lond.), 28, 510, 10.1038/eye.2014.13 Massin, 2010, Safety and efficacy of ranibizumab in diabetic macular edema (RESOLVE Study): a 12-month, randomized, controlled, double-masked, multicenter phase II study, Diabetes Care, 33, 2399, 10.2337/dc10-0493 Nguyen, 2012, Ranibizumab for diabetic macular edema: results from 2 phase III randomized trials: RISE and RIDE, Ophthalmology, 119, 789, 10.1016/j.ophtha.2011.12.039 Mitchell, 2011, The RESTORE study: ranibizumab monotherapy or combined with laser versus laser monotherapy for diabetic macular edema, Ophthalmology, 118, 615, 10.1016/j.ophtha.2011.01.031 Nguyen, 2010, Two-year outcomes of the ranibizumab for edema of the mAcula in diabetes (READ-2) study, Ophthalmology, 117, 2146, 10.1016/j.ophtha.2010.08.016 Arevalo, 2008, Tractional retinal detachment following intravitreal bevacizumab (Avastin) in patients with severe proliferative diabetic retinopathy, Br. J. Ophthalmol., 92, 213, 10.1136/bjo.2007.127142 Falavarjani, 2013, Adverse events and complications associated with intravitreal injection of anti-VEGF agents: a review of literature, Eye (Lond), 27, 787, 10.1038/eye.2013.107 Moradian, 2008, Intravitreal bevacizumab in active progressive proliferative diabetic retinopathy, Graefes Arch. Clin. Exp. Ophthalmol., 246, 1699, 10.1007/s00417-008-0914-4 Van Geest, 2012, A shift in the balance of vascular endothelial growth factor and connective tissue growth factor by bevacizumab causes the angiofibrotic switch in proliferative diabetic retinopathy, Br. J. Ophthalmol., 96, 587, 10.1136/bjophthalmol-2011-301005 Filek, 2019, Two-year analysis of changes in the optic nerve and retina following anti-VEGF treatments in diabetic macular edema patients, Clin. Ophthalmol., 13, 1087, 10.2147/OPTH.S199758 Hombrebueno, 2015, Sustained intraocular VEGF neutralization results in retinal neurodegeneration in the Ins2(Akita) diabetic mouse, Sci. Rep., 5, 18316, 10.1038/srep18316 Park, 2014, Neuronal cell death in the inner retina and the influence of vascular endothelial growth factor inhibition in a diabetic rat model, Am. J. Pathol., 184, 1752, 10.1016/j.ajpath.2014.02.016 Ferrara, 2003, The biology of VEGF and its receptors, Nat. Med., 9, 669, 10.1038/nm0603-669 Nguyen, 2018, Placental growth factor and its potential role in diabetic retinopathy and other ocular neovascular diseases, Acta Ophthalmol., 96, e1, 10.1111/aos.13325 Carmeliet, 2001, Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions, Nat. Med., 7, 575, 10.1038/87904 Huang, 2015, Deletion of placental growth factor prevents diabetic retinopathy and is associated with Akt activation and HIF1α-VEGF pathway inhibition, Diabetes, 64, 200, 10.2337/db14-0016 Jonas, 2012, Cytokine concentration in aqueous humor of eyes with diabetic macular edema, Retina, 32, 2150, 10.1097/IAE.0b013e3182576d07 Khaliq, 1998, Increased expression of placenta growth factor in proliferative diabetic retinopathy, Lab. Invest., 78, 109 Yamashita, 1999, Expression of placenta growth factor (PIGF) in ischaemic retinal diseases, Eye (Lond.), 13, 372, 10.1038/eye.1999.95 Kovacs, 2015, Angiogenic and Inflammatory Vitreous Biomarkers Associated With Increasing Levels of Retinal Ischemia, Invest. Ophthalmol. Vis. Sci., 56, 6523, 10.1167/iovs.15-16793 Ando, 2014, Aqueous humour levels of placental growth factor in diabetic retinopathy, Acta Ophthalmol., 92, e245, 10.1111/aos.12251 Spirin, 1999, Basement membrane and growth factor gene expression in normal and diabetic human retinas, Curr. Eye Res., 18, 490, 10.1076/ceyr.18.6.490.5267 Gao, 2001, Unbalanced expression of VEGF and PEDF in ischemia-induced retinal neovascularization, FEBS Lett., 489, 270, 10.1016/S0014-5793(01)02110-X Ogata, 2002, Unbalanced vitreous levels of pigment epithelium-derived factor and vascular endothelial growth factor in diabetic retinopathy, Am. J. Ophthalmol., 134, 348, 10.1016/S0002-9394(02)01568-4 Dawson, 1999, Pigment epithelium-derived factor: a potent inhibitor of angiogenesis, Science, 285, 245, 10.1126/science.285.5425.245 Yamagishi, 2007, Pigment-epithelium-derived factor suppresses expression of receptor for advanced glycation end products in the eye of diabetic rats, Ophthalmic Res., 39, 92, 10.1159/000099244 Haurigot, 2012, Long-term retinal PEDF overexpression prevents neovascularization in a murine adult model of retinopathy, PLoS ONE, 7, e41511, 10.1371/journal.pone.0041511 Wang, 2017, Gene therapy for diabetic retinopathy: Are we ready to make the leap from bench to bedside?, Pharmacol. Ther., 173, 1, 10.1016/j.pharmthera.2017.01.003 Calado, 2014, Sustained gene expression in the retina by improved episomal vectors, Tissue Eng. Part A, 20, 2692, 10.1089/ten.tea.2013.0672 Calado, 2016, pEPito-driven PEDF expression ameliorates Diabetic Retinopathy hallmarks, Hum. Gene Ther. Methods, 27, 79, 10.1089/hgtb.2015.169 Araújo, 2020, Dysregulation of trophic factors contributes to diabetic retinopathy in the Ins2Akita mouse, Exp. Eye Res., 194, 108027, 10.1016/j.exer.2020.108027 Miller, 1994, Vascular endothelial growth factor/vascular permeability factor is temporally and spatially correlated with ocular angiogenesis in a primate model, Am. J. Pathol., 145, 574 Ting, 2016, Biomarkers of Diabetic Retinopathy, Curr. Diab. Rep., 16, 125, 10.1007/s11892-016-0812-9 Sasongko, 2015, Circulating markers of inflammation and endothelial function, and their relationship to diabetic retinopathy, Diabet. Med., 32, 686, 10.1111/dme.12640 Altmann, 2018, The Role of Microglia in Diabetic Retinopathy: Inflammation, Microvasculature Defects and Neurodegeneration, Int. J. Mol. Sci., 19, 110, 10.3390/ijms19010110 Xu, 2001, Sensitive blood-retinal barrier breakdown quantitation using Evans blue, Invest. Ophthalmol. Vis. Sci., 42, 789 Surgucheva, 2008, Gamma-synuclein as a marker of retinal ganglion cells, Mol. Vis., 14, 1540 Avery, 2006, Intravitreal bevacizumab (Avastin) in the treatment of proliferative diabetic retinopathy, Ophthalmology, 113, 1695.e1, 10.1016/j.ophtha.2006.05.064 Mason, 2006, Intravitreal injection of bevacizumab (Avastin) as adjunctive treatment of proliferative diabetic retinopathy, Am. J. Ophthalmol., 142, 685, 10.1016/j.ajo.2006.04.058 Hattori, 2010, Dose of intravitreal bevacizumab (Avastin) used as preoperative adjunct therapy for proliferative diabetic retinopathy, Retina, 30, 761, 10.1097/IAE.0b013e3181c70168 Storkebaum, 2004, VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection, BioEssays, 26, 943, 10.1002/bies.20092 Carroll, 2019, Intravitreal AAV2.COMP-Ang1 attenuates deep capillary plexus expansion in the aged diabetic mouse retina, Invest. Ophthalmol. Vis. Sci., 60, 2494, 10.1167/iovs.18-26182 Han, 2013, Retinal angiogenesis in the Ins2(Akita) mouse model of diabetic retinopathy, Invest. Ophthalmol. Vis. Sci., 54, 574, 10.1167/iovs.12-10959 He, 2015, PEDF and its roles in physiological and pathological conditions: implication in diabetic and hypoxia-induced angiogenic diseases, Clin. Sci. (Lond.), 128, 805, 10.1042/CS20130463 Zhang, 2006, Pigment epithelium-derived factor downregulates vascular endothelial growth factor (VEGF) expression and inhibits VEGF-VEGF receptor 2 binding in diabetic retinopathy, J. Mol. Endocrinol., 37, 1, 10.1677/jme.1.02008 Mori, 2001, Pigment epithelium-derived factor inhibits retinal and choroidal neovascularization, J. Cell. Physiol., 188, 253, 10.1002/jcp.1114 Van Bergen, 2017, Neutralization of placental growth factor as a novel treatment option in diabetic retinopathy, Exp. Eye Res., 165, 136, 10.1016/j.exer.2017.09.012 Araújo, 2020, PlGF silencing combined with PEDF overexpression: Modeling RPE secretion as potential therapy for retinal neovascularization, Mol. Biol. Rep., 47, 4413, 10.1007/s11033-020-05496-2 Murata, 1996, The relation between expression of vascular endothelial growth factor and breakdown of the blood-retinal barrier in diabetic rat retinas, Lab. Invest., 74, 819 Carmo, 2000, Effect of cyclosporin-A on the blood—retinal barrier permeability in streptozotocin-induced diabetes, Mediators Inflamm., 9, 243, 10.1080/09629350020025764 Miyamoto, 2007, Placental growth factor-1 and epithelial haemato-retinal barrier breakdown: potential implication in the pathogenesis of diabetic retinopathy, Diabetologia, 50, 461, 10.1007/s00125-006-0539-2 Barber, 2005, The Ins2Akita mouse as a model of early retinal complications in diabetes, Invest. Ophthalmol. Vis. Sci., 46, 2210, 10.1167/iovs.04-1340 Wright, 2012, Retinal blood flow abnormalities following six months of hyperglycemia in the Ins2(Akita) mouse, Exp. Eye Res., 98, 9, 10.1016/j.exer.2012.03.003 Rakoczy, 2010, Characterization of a mouse model of hyperglycemia and retinal neovascularization, Am. J. Pathol., 177, 2659, 10.2353/ajpath.2010.090883 Izawa, 2015, Protective Effects of Antiplacental Growth Factor Antibody Against Light-Induced Retinal Damage in Mice, Invest. Ophthalmol. Vis. Sci., 56, 6914, 10.1167/iovs.15-16748 Haase, 2010, pEPito: a significantly improved non-viral episomal expression vector for mammalian cells, BMC Biotechnol., 10, 20, 10.1186/1472-6750-10-20 Wang, 1999, A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse, J. Clin. Invest., 103, 27, 10.1172/JCI4431 Yoshioka, 1997, A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice, Diabetes, 46, 887, 10.2337/diab.46.5.887 Matsuda, 2004, Electroporation and RNA interference in the rodent retina in vivo and in vitro, Proc. Natl. Acad. Sci. USA, 101, 16, 10.1073/pnas.2235688100 Zudaire, 2011, A computational tool for quantitative analysis of vascular networks, PLoS ONE, 6, e27385, 10.1371/journal.pone.0027385