Intravitreal Delivery of VEGF-A₁₆₅-loaded PLGA Microparticles Reduces Retinal Vaso-Obliteration in an In Vivo Mouse Model of Retinopathy of Prematurity

References

• Gilbert C. Retinopathy of prematurity: A global perspective of the epidemics, population of babies at risk and implications for control. Early Hum Dev. 2008;84:77–82. doi:10.1016/j.earlhumdev.2007.11.009.
   PubMed Web of Science ®Google Scholar
• Roth AM. Retinal vascular development in premature infants. Am J Ophthalmol. 1977;84:636–40.
   PubMed Web of Science ®Google Scholar
• Smith LEH. Pathogenesis of retinopathy of prematurity. Semin Neonatal. 2003Dec 1;8:469–73. doi:10.1016/S1084-2756(03)00119-2.
   PubMedGoogle Scholar
• Iqbal S, Lenz HJ. Integration of novel agents in the treatment of colorectal cancer. Cancer Chemother Pharmacol. 2004 Sep;54(Suppl 1):S32–9. doi:10.1007/s00280-004-0884-0.
   PubMed Web of Science ®Google Scholar
• Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, Xu X, Robinson G, Driver S, Bischoff J, Zhang B, et al. Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med. 1999 Dec;5:1390–95. doi:10.1038/70963.
   PubMed Web of Science ®Google Scholar
• Zhao M, Shi X, Liang J, Miao Y, Xie W, Zhang Y, Li X. Expression of pro- and anti-angiogenic isoforms of VEGF in the mouse model of oxygen-induced retinopathy. Exp Eye Res. 2011;93:921–26. doi:10.1016/j.exer.2011.10.013.
   PubMed Web of Science ®Google Scholar
• Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999 Jan 1;13(1):9–22. doi:10.1096/fasebj.13.1.9.
   PubMed Web of Science ®Google Scholar
• Bates DO, Cui TG, Doughty JM, Winkler M, Sugiono M, Shields JD, Peat D, Gillatt D, Harper SJ. VEGF165b, an inhibitory splice variant of vascular endothelial growth factor, is down-regulated in renal cell carcinoma. Cancer Res. 2002 Jul 15;62:4123–31.
   PubMed Web of Science ®Google Scholar
• Xia XB, Xiong SQ, Xu HZ, Jiang J, Li Y. Suppression of retinal neovascularization by shRNA targeting HIF-1alpha. Curr Eye Res. 2008 Oct;33:892–902. doi:10.1080/02713680802416670.
   PubMed Web of Science ®Google Scholar
• Mintz-Hittner HA, Kennedy KA, Chuang AZ. Efficacy of intravitreal bevacizumab for stage 3+ retinopathy of prematurity. New England J Med. 2011;364:603–15. doi:10.1056/NEJMoa1007374.
   PubMed Web of Science ®Google Scholar
• Bracha P, Moore NA, Ciulla TA, WuDunn D, Cantor LB. The acute and chronic effects of intravitreal anti-vascular endothelial growth factor injections on intraocular pressure: A review. Surv Ophthalmol. 2018 May–Jun;63(3):281–295. doi:10.1016/j.survophthal.2017.08.008. Epub 2017 Sep 5.
   PubMed Web of Science ®Google Scholar
• Wang L, Shi P, Xu Z, Li J, Xie Y, Mitton K, Drenser K, Yan Q. Up-regulation of VEGF by retinoic acid during hyperoxia prevents retinal neovascularization and retinopathy. Invest Ophthalmol Vis Sci. 2014 Jul;55:4276–87. doi:10.1167/iovs.14-14170.
   PubMed Web of Science ®Google Scholar
• Sears JE, Hoppe G, Ebrahem Q, Anand-Apte B. Prolyl hydroxylase inhibition during hyperoxia prevents oxygen-induced retinopathy. Proc Natl Acad Sci U S A. 2008 Dec 16;105:19898–903. doi:10.1073/pnas.0805817105.
   PubMed Web of Science ®Google Scholar
• Yasukawa T, Tabata Y, Kimura H, Ogura Y. Recent advances in intraocular drug delivery systems. Recent Pat Drug Deliv Formul. 2011 Jan;5:1–10.
   PubMedGoogle Scholar
• Figueras-Aloy J, Alvarez-Dominguez E, Morales-Ballus M, Salvia-Roiges MD, Moretones-Sunol G. [Early administration of erythropoietin in the extreme premature, a risk factor for retinopathy of prematurity?]. An Pediatr (Barc). 2010 Dec;73:327–33. doi:10.1016/j.anpedi.2010.09.001.
   PubMed Web of Science ®Google Scholar
• Romagnoli C, Tesfagabir MG, Giannantonio C, Papacci P. Erythropoietin and retinopathy of prematurity. Early Hum Dev. 2011 Mar;87(Suppl 1):S39–42. doi:10.1016/j.earlhumdev.2011.01.027.
   PubMed Web of Science ®Google Scholar
• Ayalasomayajula SP, Kompella UB. Subconjunctivally administered celecoxib-PLGA microparticles sustain retinal drug levels and alleviate diabetes-induced oxidative stress in a rat model. Eur J Pharmacol. 2005 Mar 28;511:191–98. doi:10.1016/j.ejphar.2005.02.019.
   PubMed Web of Science ®Google Scholar
• Chen G, Shi X, Wang B, Xie R, Guo LW, Gong S, Kent KC. Unimolecular micelle-based hybrid system for perivascular drug delivery produces long-term efficacy for neointima attenuation in rats. Biomacromolecules. 2017 Jul 10;18:2205–13. doi:10.1021/acs.biomac.7b00617.
   PubMed Web of Science ®Google Scholar
• Amrite AC, Ayalasomayajula SP, Cheruvu NP, Kompella UB. Single periocular injection of celecoxib-PLGA microparticles inhibits diabetes-induced elevations in retinal PGE2, VEGF, and vascular leakage. Invest Ophthalmol Vis Sci. 2006 Mar;47:1149–60. doi:10.1167/iovs.05-0531.
   PubMed Web of Science ®Google Scholar
• Formiga FR, Pelacho B, Garbayo E, Abizanda G, Gavira JJ, Simon-Yarza T, Mazo M, Tamayo E, Jauquicoa C, Ortiz-de-Solorzano C, et al. Sustained release of VEGF through PLGA microparticles improves vasculogenesis and tissue remodeling in an acute myocardial ischemia-reperfusion model. J Control Release. 2010 Oct 1;147:30–37. doi:10.1016/j.jconrel.2010.07.097.
   PubMed Web of Science ®Google Scholar
• Chang E, McClellan AJ, Farley WJ, Li DQ, Pflugfelder SC, de Paiva CS. Biodegradable PLGA-based drug delivery systems for modulating ocular surface disease under experimental murine dry eye. J Clin Exp Ophthalmol. 2011 Nov 1;2. doi:10.4172/2155-9570.1000191.
   PubMedGoogle Scholar
• Shive MS, Anderson JM. Biodegradation and biocompatibility of PLA and PLGA microspheres. Adv Drug Deliv Rev. 1997 Oct 13;28:5–24.
   PubMed Web of Science ®Google Scholar
• Saito Y, Geisen P, Uppal A, Hartnett ME. Inhibition of NAD(P)H oxidase reduces apoptosis and avascular retina in an animal model of retinopathy of prematurity. Mol Vis. 2007;13:840–53.
   PubMed Web of Science ®Google Scholar
• Connor KM, Krah NM, Dennison RJ, Aderman CM, Chen J, Guerin KI, Sapieha P, Stahl A, Willett KL, Smith LE. Quantification of oxygen-induced retinopathy in the mouse: a model of vessel loss, vessel regrowth and pathological angiogenesis. Nat Protoc. 2009;4:1565–73. doi:10.1038/nprot.2009.187.
   PubMed Web of Science ®Google Scholar
• Mezu-Ndubuisi OJ. In vivo angiography quantifies oxygen-induced retinopathy vascular recovery. Optom Vis Sci. 2016;93:1268. doi:10.1097/OPX.0000000000000941.
   PubMed Web of Science ®Google Scholar
• Pierce EA, Avery RL, Foley ED, Aiello LP, Smith LE. Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc Natl Acad Sci U S A. 1995 Jan 31;92:905–09.
   PubMed Web of Science ®Google Scholar
• Usui T, Ishida S, Yamashiro K, Kaji Y, Poulaki V, Moore J, Moore T, Amano S, Horikawa Y, Dartt D, et al. VEGF164(165) as the pathological isoform: differential leukocyte and endothelial responses through VEGFR1 and VEGFR2. Invest Ophthalmol Vis Sci. 2004 Feb;45:368–74.
   PubMed Web of Science ®Google Scholar
• Saint-Geniez M, Maldonado AE, D’Amore PA. VEGF expression and receptor activation in the choroid during development and in the adult. Invest Ophthalmol Vis Sci. 2006 Jul;47:3135–42. doi:10.1167/iovs.05-1229.
   PubMed Web of Science ®Google Scholar
• Woolard J, Wang WY, Bevan HS, Qiu Y, Morbidelli L, Pritchard-Jones RO, Cui TG, Sugiono M, Waine E, Perrin R, et al. VEGF165b, an inhibitory vascular endothelial growth factor splice variant: mechanism of action, in vivo effect on angiogenesis and endogenous protein expression. Cancer Res. 2004 Nov 1;64:7822–35. doi:10.1158/0008-5472.CAN-04-0934.
   PubMed Web of Science ®Google Scholar
• Konopatskaya O, Churchill AJ, Harper SJ, Bates DO, Gardiner TA. VEGF165b, an endogenous C-terminal splice variant of VEGF, inhibits retinal neovascularization in mice. Mol Vis. 2006 May 26;12:626–32.
   PubMed Web of Science ®Google Scholar
• Panyam J, Dali MM, Sahoo SK, Ma W, Chakravarthi SS, Amidon GL, Levy RJ, Labhasetwar V. Polymer degradation and in vitro release of a model protein from poly (D, L-lactide-co-glycolide) nano-and microparticles. J Control Release. 2003;92:173–87.
   PubMed Web of Science ®Google Scholar
• Sandor M, Enscore D, Weston P, Mathiowitz E. Effect of protein molecular weight on release from micron-sized PLGA microspheres. J Control Release. 2001 Oct 19;76:297–311.
   PubMed Web of Science ®Google Scholar
• Mezu-Ndubuisi OJ, Teng PY, Wanek J, Blair NP, Chau FY, Reddy NM, Raj JU, Reddy SP, Shahidi M. In vivo retinal vascular oxygen tension imaging and fluorescein angiography in the mouse model of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 2013;54:6968–72. doi:10.1167/iovs.13-12126.
   PubMed Web of Science ®Google Scholar
• Smith LE, Wesolowski E, McLellan A, Kostyk SK, D’Amato R, Sullivan R, D’Amore PA. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994 Jan;35:101–11.
   PubMed Web of Science ®Google Scholar
• Mezu-Ndubuisi OJ, Taylor LK, Schoephoerster JA. simultaneous fluorescein angiography and spectral domain optical coherence tomography correlate retinal thickness changes to vascular abnormalities in an in vivo mouse model of retinopathy of prematurity. J Ophthalmol. 2017;2017:1–9. doi:10.1155/2017/9620876.
   Web of Science ®Google Scholar
• Stahl A, Connor KM, Sapieha P, Willett KL, Krah NM, Dennison RJ, Chen J, Guerin KI, Smith LEH. Computer-aided quantification of retinal neovascularization. Angiogenesis. 2009;12:297–301. doi:10.1007/s10456-009-9155-3.
   PubMed Web of Science ®Google Scholar
• Zhang JS, Da Wang J, An Y, Xiong Y, Li J, Jonas J, Xu L, Zhang W, Wan XH. Cedilanid inhibits retinal neovascularization in a mouse model of oxygen-induced retinopathy. Mol Vis. 2017;23:346–55.
   PubMed Web of Science ®Google Scholar
• Shen J, Samul R, Silva RL, Akiyama H, Liu H, Saishin Y, Hackett SF, Zinnen S, Kossen K, Fosnaugh K, et al. Suppression of ocular neovascularization with siRNA targeting VEGF receptor 1. Gene Ther. 2006 Feb;13:225–34. doi:10.1038/sj.gt.3302641.
   PubMed Web of Science ®Google Scholar
• Gardiner TA, Gibson DS, de Gooyer TE, de la Cruz VF, McDonald DM, Stitt AW. Inhibition of tumor necrosis factor-alpha improves physiological angiogenesis and reduces pathological neovascularization in ischemic retinopathy. Am J Pathol. 2005 Feb;166:637–44.
   PubMed Web of Science ®Google Scholar
• Medina RJ, O’Neill CL, Devine AB, Gardiner TA, Stitt AW. The pleiotropic effects of simvastatin on retinal microvascular endothelium has important implications for ischaemic retinopathies. PLoS One. 2008 Jul 9;3:e2584. doi:10.1371/journal.pone.0002584.
   PubMed Web of Science ®Google Scholar
• Penn JS, Tolman BL, Bullard LE. Effect of a water-soluble vitamin E analog, trolox C, on retinal vascular development in an animal model of retinopathy of prematurity. Free Radic Biol Med. 1997;22:977–84.
   PubMed Web of Science ®Google Scholar
• Zhang Q, Zhang J, Guan Y, Zhang S, Zhu C, Xu GT, Wang L. Suppression of retinal neovascularization by the iNOS inhibitor aminoguanidine in mice of oxygen-induced retinopathy. Graefes Arch Clin Exp Ophthalmol. 2009 Jul;247:919–27. doi:10.1007/s00417-009-1066-x.
   PubMed Web of Science ®Google Scholar
• Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development. 1998 May;125:1591–98.
   PubMed Web of Science ®Google Scholar
• Shelke NB, Kadam R, Tyagi P, Rao VR, Kompella UB. Intravitreal Poly(L-lactide) microparticles sustain retinal and choroidal delivery of TG-0054, a hydrophilic drug intended for neovascular diseases. Drug Deliv Transl Res. 2011 Feb;1:76–90. doi:10.1007/s13346-010-0009-8.
   PubMed Web of Science ®Google Scholar
• Gaddipati S, Lu Q, Kasetti RB, Miller MC, Lu Q, Trent JO, Kaplan HJ, Li Q. IKK2 inhibition using TPCA-1-loaded PLGA microparticles attenuates laser-induced choroidal neovascularization and macrophage recruitment. PLoS One. 2015;10:e0121185. doi:10.1371/journal.pone.0121185.
   PubMed Web of Science ®Google Scholar
• Sinha VR, Trehan A. Biodegradable microspheres for protein delivery. J Control Release. 2003;90:261–80.
   PubMed Web of Science ®Google Scholar
• Torchilin VP, Lukyanov AN. Peptide and protein drug delivery to and into tumors: challenges and solutions. Drug Discov Today. 2003;8:259–66.
   PubMed Web of Science ®Google Scholar
• White LJ, Kirby GTS, Cox HC, Qodratnama R, Qutachi O, Rose FRAJ, Shakesheff KM. Accelerating protein release from microparticles for regenerative medicine applications. Mater Sci Eng C. 2013;33:2578–83. doi:10.1016/j.msec.2013.02.020.
   PubMed Web of Science ®Google Scholar
• Andrieu-Soler C, Aubert-Pouessel A, Doat M, Picaud S, Halhal M, Simonutti M, Venier-Julienne MC, Benoit JP, Behar-Cohen F. Intravitreous injection of PLGA microspheres encapsulating GDNF promotes the survival of photoreceptors in the rd1/rd1 mouse. Mol Vis. 2005 Nov 17;11:1002–11.
   PubMed Web of Science ®Google Scholar
• Bible E, Qutachi O, Chau DY, Alexander MR, Shakesheff KM, Modo M. Neo-vascularization of the stroke cavity by implantation of human neural stem cells on VEGF-releasing PLGA microparticles. Biomaterials. 2012 Oct;33:7435–46. doi:10.1016/j.biomaterials.2012.06.085.
   PubMed Web of Science ®Google Scholar
• Visconti RP, Richardson CD, Sato TN. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc Natl Acad Sci U S A. 2002 Jun 11;99:8219–24. doi:10.1073/pnas.122109599.
   PubMed Web of Science ®Google Scholar
• Hao X, Silva EA, Mansson-Broberg A, Grinnemo KH, Siddiqui AJ, Dellgren G, Wardell E, Brodin LA, Mooney DJ, Sylven C. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc Res. 2007 Jul 1;75:178–85. doi:10.1016/j.cardiores.2007.03.028.
   PubMed Web of Science ®Google Scholar
• Yang JP, Liu HJ, Wang ZL, Cheng SM, Cheng X, Xu GL, Liu XF. The dose-effectiveness of intranasal VEGF in treatment of experimental stroke. Neurosci Lett. 2009 Sep 25;461:212–16. doi:10.1016/j.neulet.2009.06.060.
   PubMed Web of Science ®Google Scholar
• Beckert S, Farrahi F, Aslam RS, Scheuenstuhl H, Konigsrainer A, Hussain MZ, Hunt TK. Lactate stimulates endothelial cell migration. Wound Repair Regen. 2006 May–Jun;14:321–24. doi:10.1111/j.1743-6109.2006.00127.x.
   PubMed Web of Science ®Google Scholar
• Porporato PE, Payen VL, de Saedeleer CJ, Preat V, Thissen JP, Feron O, Sonveaux P. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis. 2012 Dec;15:581–92. doi:10.1007/s10456-012-9282-0.
   PubMed Web of Science ®Google Scholar
• De Saedeleer CJ, Copetti T, Porporato PE, Verrax J, Feron O, Sonveaux P. Lactate activates HIF-1 in oxidative but not in Warburg-phenotype human tumor cells. PLoS One. 2012;7:e46571. doi:10.1371/journal.pone.0046571.
   PubMed Web of Science ®Google Scholar
• Romijn HJ, Hofman MA, Gramsbergen A. At what age is the developing cerebral cortex of the rat comparable to that of the full-term newborn human baby? Early Hum Dev. 1991 Jul;26:61–67.
   PubMed Web of Science ®Google Scholar