Angiopoietins as Potential Targets in Management of Retinal Disease

References

• Bourne RRA, Stevens GA, White RA, et al. Causes of vision loss worldwide, 1990–2010: a systematic analysis. Lancet Glob Health. 2013;1(6):e339–349. doi:10.1016/S2214-109X(13)70113-X
   PubMed Web of Science ®Google Scholar
• Boyle JP, Honeycutt AA, Narayan KMV, et al. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U.S. Diabetes Care. 2001;24(11):1936–1940. doi:10.2337/diacare.24.11.1936
   PubMed Web of Science ®Google Scholar
• Fong DS, Aiello L, Gardner TW, et al. Retinopathy in diabetes. Diabetes Care. 2004;27(suppl 1):s84–7. doi:10.2337/diacare.27.2007.S84
   PubMed Web of Science ®Google Scholar
• Ferrara N, Gerber H-P, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9(6):669–676. doi:10.1038/nm0603-669
   PubMed Web of Science ®Google Scholar
• Boyer DS, Hopkins JJ, Sorof J, Ehrlich JS. Anti-vascular endothelial growth factor therapy for diabetic macular edema. Ther Adv Endocrinol Metab. 2013;4(6):151–169. doi:10.1177/2042018813512360
   PubMedGoogle Scholar
• Wang W, Lo ACY. Diabetic retinopathy: pathophysiology and treatments. Int J Mol Sci [Internet]. 2018;19(6):1816.
   PubMed Web of Science ®Google Scholar
• akamura Y, Ohkoshi K, Murata T. New Strategies for Treatment of Diabetic Macular Edema. Journal of Ophthalmology. 2018;2018:e4292154.
   Google Scholar
• Weiss M, Sim DA, Herold T, et al. Compliance and adherence of patients with diabetic macular edema to intravitreal anti-vascular endothelial growth factor therapy in daily practice. Retina Phila Pa. 2018;38(12):2293–2300. doi:10.1097/IAE.0000000000001892
   PubMed Web of Science ®Google Scholar
• Boulanger-Scemama E, Querques G, About F, et al. Ranibizumab for exudative age-related macular degeneration: a five year study of adherence to follow-up in a real-life setting. J Fr Ophtalmol. 2015;38(7):620–627. doi:10.1016/j.jfo.2014.11.015
   PubMed Web of Science ®Google Scholar
• Thurston G, Daly C. The complex role of angiopoietin-2 in the angiopoietin–tie signaling pathway. Cold Spring Harb Perspect Med. 2012;2(9):a006650.
   Web of Science ®Google Scholar
• Schnürch H, Risau W. Expression of tie-2, a member of a novel family of receptor tyrosine kinases, in the endothelial cell lineage. Dev Camb Engl. 1993;119(3):957–968.
   Web of Science ®Google Scholar
• Whitehead M, Osborne A, Widdowson PS, Yu-Wai-Man P, Martin KR. Angiopoietins in diabetic retinopathy: current understanding and therapeutic potential. J Diabetes Res. 2019;;2019:1–9. doi:10.1155/2019/5140521
   Web of Science ®Google Scholar
• Joussen AM, Ricci F, Paris LP, Korn C, Quezada-Ruiz C, Zarbin M. Angiopoietin/Tie2 signalling and its role in retinal and choroidal vascular diseases: a review of preclinical data. Eye. 2021;35:1–12.
   Web of Science ®Google Scholar
• Brunckhorst MK, Wang H, Lu R, Yu Q. Angiopoietin-4 promotes glioblastoma progression by enhancing tumor cell viability and angiogenesis. Cancer Res. 2010;70(18):7283–7293. doi:10.1158/0008-5472.CAN-09-4125
   Web of Science ®Google Scholar
• Kim W. The role of angiopoietin-1 in kidney disease. Electrolytes Blood Press E BP. 2008;6(1):22–26. doi:10.5049/EBP.2008.6.1.22
   PubMedGoogle Scholar
• Scholz A, Plate KH, Reiss Y. Angiopoietin-2: a multifaceted cytokine that functions in both angiogenesis and inflammation. Ann N Y Acad Sci. 2015;1347:45–51. doi:10.1111/nyas.12726
   PubMed Web of Science ®Google Scholar
• Korhonen EA, Lampinen A, Giri H, et al. Tie1 controls angiopoietin function in vascular remodeling and inflammation. J Clin Invest. 2016;126(9):3495–3510. doi:10.1172/JCI84923
   PubMed Web of Science ®Google Scholar
• Li Z, Huang H, Boland P, et al. Embryonic stem cell tumor model reveals role of vascular endothelial receptor tyrosine phosphatase in regulating Tie2 pathway in tumor angiogenesis. Proc Natl Acad Sci U S A. 2009;106(52):22399–22404. doi:10.1073/pnas.0911189106
   Web of Science ®Google Scholar
• Winderlich M, Keller L, Cagna G, et al. VE-PTP controls blood vessel development by balancing Tie-2 activity. J Cell Biol. 2009;185(4):657–671. doi:10.1083/jcb.200811159
   Web of Science ®Google Scholar
• Frye M, Dierkes M, Küppers V, et al. Interfering with VE-PTP stabilizes endothelial junctions in vivo via Tie-2 in the absence of VE-cadherin. J Exp Med. 2015;212(13):2267–2287. doi:10.1084/jem.20150718
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang VM, Chan -C-C. The role of anti-inflammatory agents in age-related macular degeneration (AMD) treatment. Eye. 2011;25(2):127–139. doi:10.1038/eye.2010.196
   PubMed Web of Science ®Google Scholar
• Doganay S, Evereklioglu C, Er H, et al. Comparison of serum NO, TNF-α, IL-1β, sIL-2R, IL-6 and IL-8 levels with grades of retinopathy in patients with diabetes mellitus. Eye. 2002;16(2):163–170. doi:10.1038/sj/eye/6700095
   PubMed Web of Science ®Google Scholar
• Deobhakta A, Chang LK. Inflammation in retinal vein occlusion. Int J Inflamm. 2013;2013:438412. doi:10.1155/2013/438412
   PubMedGoogle Scholar
• Hughes DP, Marron MB, Brindle NPJ. The antiinflammatory endothelial tyrosine kinase Tie2 interacts with a novel nuclear factor-kappaB inhibitor ABIN-2. Circ Res. 2003;92(6):630–636. doi:10.1161/01.RES.0000063422.38690.DC
   Web of Science ®Google Scholar
• Papapetropoulos A, Fulton D, Mahboubi K, et al. Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J Biol Chem. 2000;275(13):9102–9105. doi:10.1074/jbc.275.13.9102
   PubMed Web of Science ®Google Scholar
• Kontos CD, Cha EH, York JD, Peters KG. The endothelial receptor tyrosine kinase Tie1 activates phosphatidylinositol 3-kinase and Akt to inhibit apoptosis. Mol Cell Biol. 2002;22(6):1704–1713. doi:10.1128/MCB.22.6.1704-1713.2002
   PubMed Web of Science ®Google Scholar
• Augustin HG, Koh GY, Thurston G, Alitalo K. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol. 2009;10(3):165–177. doi:10.1038/nrm2639
   PubMed Web of Science ®Google Scholar
• Mirando AC, Shen J, Silva RLE, et al. A collagen IV-derived peptide disrupts α5β1 integrin and potentiates Ang2/Tie2 signaling. JCI Insight. 2019;4(4). doi:10.1172/jci.insight.122043.
   Web of Science ®Google Scholar
• Daly C, Wong V, Burova E, et al. Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev. 2004;18(9):1060–1071. doi:10.1101/gad.1189704
   PubMed Web of Science ®Google Scholar
• Dekker N, van Meurs M, van Leeuwen ALI, et al. Vasculotide, an angiopoietin-1 mimetic, reduces pulmonary vascular leakage and preserves microcirculatory perfusion during cardiopulmonary bypass in rats. Br J Anaesth. 2018;121(5):1041–1051. doi:10.1016/j.bja.2018.05.049
   Web of Science ®Google Scholar
• Gurnik S, Devraj K, Macas J, et al. Angiopoietin-2-induced blood-brain barrier compromise and increased stroke size are rescued by VE-PTP-dependent restoration of Tie2 signaling. Acta Neuropathol (Berl). 2016;131(5):753–773. doi:10.1007/s00401-016-1551-3
   PubMed Web of Science ®Google Scholar
• Rübig E, Stypmann J, Van Slyke P, et al. The synthetic tie2 agonist peptide vasculotide protects renal vascular barrier function in experimental acute kidney injury. Sci Rep. 2016;6:22111. doi:10.1038/srep22111
   Web of Science ®Google Scholar
• Peters S, Cree IA, Alexander R, et al. Angiopoietin modulation of vascular endothelial growth factor: effects on retinal endothelial cell permeability. Cytokine. 2007;40(2):144–150. doi:10.1016/j.cyto.2007.09.001
   Web of Science ®Google Scholar
• Watanabe D, Suzuma K, Suzuma I, et al. Vitreous levels of angiopoietin 2 and vascular endothelial growth factor in patients with proliferative diabetic retinopathy. Am J Ophthalmol. 2005;139(3):476–481. doi:10.1016/j.ajo.2004.10.004
   PubMed Web of Science ®Google Scholar
• Loukovaara S, Robciuc A, Holopainen JM, et al. Ang-2 upregulation correlates with increased levels of MMP-9, VEGF, EPO and TGFβ1 in diabetic eyes undergoing vitrectomy. Acta Ophthalmol (Copenh). 2013;91(6):531–539. doi:10.1111/j.1755-3768.2012.02473.x
   PubMed Web of Science ®Google Scholar
• Oh H, Takagi H, Suzuma K, Otani A, Matsumura M, Honda Y. Hypoxia and vascular endothelial growth factor selectively up-regulate angiopoietin-2 in bovine microvascular endothelial cells. J Biol Chem. 1999;274(22):15732–15739.
   PubMed Web of Science ®Google Scholar
• Ohashi H, Takagi H, Koyama S, et al. Alterations in expression of angiopoietins and the Tie-2 receptor in the retina of streptozotocin induced diabetic rats. Mol Vis. 2004;10:608–617.
   PubMed Web of Science ®Google Scholar
• Park SW, Yun J-H, Kim JH, Kim K-W, Cho C-H, Kim JH. Angiopoietin 2 induces pericyte apoptosis via α3β1 integrin signaling in diabetic retinopathy. Diabetes. 2014;63(9):3057–3068. doi:10.2337/db13-1942
   PubMed Web of Science ®Google Scholar
• Lee SG, Lee CG, Yun IH, Hur DY, Yang JW, Kim HW. Effect of lipoic acid on expression of angiogenic factors in diabetic rat retina. Clin Experiment Ophthalmol. 2012;40(1):e47–57. doi:10.1111/j.1442-9071.2011.02695.x
   PubMed Web of Science ®Google Scholar
• Ma L, Brelen ME, Tsujikawa M, et al. Identification of ANGPT2 as a new gene for neovascular age-related macular degeneration and polypoidal choroidal vasculopathy in the Chinese and Japanese populations. Invest Ophthalmol Vis Sci. 2017;58(2):1076–1083. doi:10.1167/iovs.16-20575
   PubMed Web of Science ®Google Scholar
• Ng DS, Yip YW, Bakthavatsalam M, et al. Elevated angiopoietin 2 in aqueous of patients with neovascular age related macular degeneration correlates with disease severity at presentation. Sci Rep. 2017;7:45081. doi:10.1038/srep45081
   PubMed Web of Science ®Google Scholar
• Huber M, Wachtlin J. Vitreous levels of proteins implicated in angiogenesis are modulated in patients with retinal or choroidal neovascularization. Ophthalmol J Int Ophtalmol Int J Ophthalmol Z Augenheilkd. 2012;228(3):188–193.
   Google Scholar
• The TIME-2b study: a study of AKB-9778, a novel tie 2 activator, in patients with non-proliferative diabetic retinopathy (NPDR) - tabular view - clinicalTrials.gov [Internet]. Available from: https://clinicaltrials.gov/ct2/show/record/NCT03197870. Accessed April 24, 2021.
   Google Scholar
• Hussain RM, Neiweem AE, Kansara V, Harris A, Ciulla TA. Tie-2/Angiopoietin pathway modulation as a therapeutic strategy for retinal disease. Expert Opin Investig Drugs. 2019;28(10):861–869. doi:10.1080/13543784.2019.1667333
   PubMed Web of Science ®Google Scholar
• Regeneron Pharmaceuticals. An open-label, dose-escalation study of the safety and tolerability of intravitreal (IVT) REGN910-3 and IVT REGN910 in patients with either neovascular AMD or DME [Internet]. clinicaltrials.gov; 2016. Available from: https://clinicaltrials.gov/ct2/show/NCT01997164. Accessed June 27, 2021.
   Google Scholar
• Regeneron Pharmaceuticals. A randomized, double-masked, active-controlled, phase 2 study of the efficacy, safety, and tolerability of repeated doses of intravitreal REGN910-3 in patients with diabetic macular edema [Internet]. clinicaltrials.gov; 2018. Available from: https://clinicaltrials.gov/ct2/show/NCT02712008. Accessed June 27, 2021.
   Google Scholar
• Regeneron Pharmaceuticals. A randomized, double-masked, active-controlled phase 2 study of the efficacy, safety, and tolerability of repeated doses of intravitreal REGN910-3 in patients with neovascular age-related macular degeneration [Internet]. clinicaltrials.gov; 2019. Available from: https://clinicaltrials.gov/ct2/show/NCT02713204. Accessed June 27, 2021.
   Google Scholar
• Sato TN, Tozawa Y, Deutsch U, et al. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature. 1995;376(6535):70–74. doi:10.1038/376070a0
   PubMed Web of Science ®Google Scholar
• Regula JT, Lundh von Leithner P, Foxton R, et al. Targeting key angiogenic pathways with a bispecific CrossMAb optimized for neovascular eye diseases. EMBO Mol Med. 2017;9(7):985. doi:10.15252/emmm.201707895
   PubMed Web of Science ®Google Scholar
• Gahn GM, Khanani AM. New therapies of neovascular AMD beyond anti-VEGF injections. Vis Basel Switz. 2018;2(1):15.
   Google Scholar
• Chakravarthy U, Bailey C, Brown D, et al. Phase I trial of anti–vascular endothelial growth factor/anti-angiopoietin 2 bispecific antibody RG7716 for neovascular age-related macular degeneration. Ophthalmol Retina. 2017;1(6):474–485. doi:10.1016/j.oret.2017.03.003
   PubMedGoogle Scholar
• Sahni J, Dugel PU, Patel SS, et al. Safety and efficacy of different doses and regimens of faricimab vs ranibizumab in neovascular age-related macular degeneration: the AVENUE phase 2 randomized clinical trial. JAMA Ophthalmol. 2020;138(9):955–963. doi:10.1001/jamaophthalmol.2020.2685
   PubMed Web of Science ®Google Scholar
• Khanani AM, Patel SS, Ferrone PJ, et al. Efficacy of every four monthly and quarterly dosing of faricimab vs ranibizumab in neovascular age-related macular degeneration: the STAIRWAY phase 2 randomized clinical trial. JAMA Ophthalmol. 2020;138(9):964–972. doi:10.1001/jamaophthalmol.2020.2699
   PubMed Web of Science ®Google Scholar
• Sahni J, Patel SS, Dugel PU, et al. Simultaneous inhibition of angiopoietin-2 and vascular endothelial growth factor-A with faricimab in diabetic macular edema: BOULEVARD phase 2 randomized trial. Ophthalmology. 2019;126(8):1155–1170. doi:10.1016/j.ophtha.2019.03.023
   PubMed Web of Science ®Google Scholar
• Vandekerckhove K ROA. Aflibercept versus ranibizumab for treating persistent diabetic macular oedema. Int Ophthalmol. 2015;35(4):603–609. doi:10.1007/s10792-015-0081-7
   Web of Science ®Google Scholar
• Roche H-L. A phase III, multicenter, randomized, double-masked, active comparator-controlled study to evaluate the efficacy and safety of faricimab (RO6867461) in patients with diabetic macular edema (YOSEMITE) [Internet]. clinicaltrials.gov; 2021. Available from: https://clinicaltrials.gov/ct2/show/NCT03622580. Accessed April 22, 2021.
   Google Scholar
• Roche H-L. A Phase III, multicenter, randomized, double-masked, active comparator-controlled study to evaluate the efficacy and safety of faricimab (RO6867461) in patients with diabetic macular edema (RHINE) [Internet]. clinicaltrials.gov; 2021. Available from: https://clinicaltrials.gov/ct2/show/NCT03622593. Accessed April 22, 2021.
   Google Scholar
• Roche H-L. A Phase III, multicenter, randomized, double-masked, active comparator-controlled study to evaluate the efficacy and safety of faricimab in patients with neovascular age-related macular degeneration (LUCERNE) [Internet]. clinicaltrials.gov; 2021. Available from: https://clinicaltrials.gov/ct2/show/NCT03823300. Accessed April 22, 2021.
   Google Scholar
• Roche H-L. A Phase III, multicenter, randomized, double-masked, active comparator-controlled study to evaluate the efficacy and safety of faricimab in patients with neovascular age-related macular degeneration (TENAYA) [Internet]. clinicaltrials.gov; 2021. Available from: https://clinicaltrials.gov/ct2/show/NCT03823287. Accessed April 22, 2021.
   Google Scholar
• Ingelheim B. Safety, tolerability and pharmacodynamics of single rising intravitreal and multiple rising intravitreal doses of BI 836880 in patients with wAMD (open label, non-randomized, uncontrolled). [Internet]. clinicaltrials.gov; 2021. Available from: https://clinicaltrials.gov/ct2/show/NCT03861234. Accessed June 27, 2021.
   Google Scholar