1,320
Views
56
CrossRef citations to date
0
Altmetric
Reviews

Morphology and Composition of the Inner Limiting Membrane: Species-Specific Variations and Relevance toward Drug Delivery Research

, , , & ORCID Icon
Pages 465-475 | Received 19 Oct 2018, Accepted 20 Dec 2018, Published online: 30 Jan 2019

References

  • Henrich PB, Monnier CA, Halfter W, Haritoglou C, Strauss RW, Lim RYH, Loparic M. Nanoscale topographic and biomechanical studies of the human internal limiting membrane. Invest Ophthalmol Vis Sci. 2012;53(6):2561–70. doi:10.1167/iovs.11-8502.
  • Sebag J. Age-related differences in the human vitreoretinal interface. Arch Ophthalmol. 1991;109(7):966–71. doi:10.1001/archopht.1991.01080070078039.
  • Müller H. Zur histologie der netzhaut. Zeitschrift für Wissenschaftlige Zoologie. 1851;3:234–37.
  • Pedler C. The inner limting membrane of the retina. Br J Ophthalmol. 1961;45(6):423–38. doi:10.1136/bjo.45.6.423.
  • Fine SB. Limiting membranes of the sensory pigment epithelium. Arch Ophthalmol. 1961;66:105–18. doi:10.1001/archopht.1961.00960010849012.
  • Foos RY. Vitreoretinal juncture; topographical variations. Invest Ophthalmol. 1972;11:801–08.
  • Masutani-Noda T, Yamada E. The mosaic pattern of the inner surface of vertebrate retina. Arch Histol Jpn. 1983;46(3):393–400. doi:10.1679/aohc.46.393.
  • Rhodes RH. An ultrastructural study of complex carbohydrates in the posterior chamber and vitreous base of the mouse. Histochem J. 1985;17(3):291–312. doi:10.1007/BF01004592.
  • Sebag J. Anatomy and pathology of the vitreo-retinal interface. Eye. 1992;6:541–52. doi:10.1038/eye.1992.119.
  • Halfter W, Sebag J, Emmet TC. Vitreoretinal interface and inner limiting membrane. In: Sebag J, editor. Vitreous: in health and disease. 1st ed. Springer-Verlag, New York; 2014. p. xxi–xxviii.
  • Wollensak G, Spoerl E, Wirbelauer C, Pham DT. Influence of indocyanine green staining on the biomechanical strength of porcine internal limiting membrane. Ophthalmologica. 2004;218(4):278–82. doi:10.1159/000078621.
  • Peynshaert K, Devoldere J, De Smedt SC, Remaut K. In vitro and ex vivo models to study drug delivery barriers in the posterior segment of the eye. Adv Drug Deliv Rev. 2018;126:44–57. doi:10.1016/j.addr.2017.09.007.
  • Balasubramani M, Schreiber EM, Candiello J, Balasubramani GK, Kurtz J, Halfter W. Molecular interactions in the retinal basement membrane system: A proteomic approach. Matrix Biol. 2010;29(6):471–83. doi:10.1016/j.matbio.2010.04.002.
  • Halfter W, Winzen U, Bishop PN, Eller A. Regulation of eye size by the retinal basement membrane and vitreous body. Investig Ophthalmol Vis Sci. 2006;47(8):3586–94. doi:10.1167/iovs.05-1480.
  • Uechi G, Sun Z, Schreiber EM, Halfter W, Balasubramani M. Proteomic view of basement membranes from human retinal blood vessels, inner limiting membranes, and lens capsules. J Proteome Res. 2014;13(8):3693–705. doi:10.1021/pr5002065.
  • Halfter W, Dong S, Balasubramani M, Bier ME. Temporary disruption of the retinal basal lamina and its effect on retinal histogenesis. Dev Biol. 2001;238(1):79–96. doi:10.1006/dbio.2001.0396.
  • Halfter W, Willem M, Mayer U. Basement membrane-dependent survival of retinal ganglion cells. Investig Ophthalmol Vis Sci. 2005;46(3):1000–09. doi:10.1167/iovs.04-1185.
  • Halfter W, Dong S, Schurer B, Ring C, Cole GJ, Eller A. Embryonic synthesis of the inner limiting membrane and vitreous body. Investig Ophthalmol Vis Sci. 2005;46(6):2202–09. doi:10.1167/iovs.04-1419.
  • Halfter W, Dong S, Dong A, Eller AW, Nischt R. Origin and turnover of ECM proteins from the inner limiting membrane and vitreous body. Eye (Lond). 2008;22(10):1207–13. doi:10.1038/sj.eye.6702590.
  • Martin GR, Timpl R, Kühn K. Basement membrane proteins: molecular structure and function. Adv Protein Chem. 1988;39:1–50.
  • Candiello J, Cole GJ, Halfter W. Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane. Matrix Biol. 2010;29(5):402–10. doi:10.1016/j.matbio.2010.03.004.
  • Halfter W, Monnier C, Müller D, Oertle P, Uechi G, Balasubramani M, Safi F, Lim R, Loparic M, Henrich PB, et al. The bi-functional organization of human basement membranes. PLoS One. 2013;8(7):1–14. doi:10.1371/journal.pone.0067660.
  • Halfter W, Oertle P, Monnier CA, Camenzind L, Reyes-Lua M, Hu H, Candiello J, Labilloy A, Balasubramani M, Henrich PB, et al. New concepts in basement membrane biology. FEBS J. 2015;282(23):4466–79. doi:10.1111/febs.13495.
  • Mao M, Alavi MV, Labelle-Dumais C, Gould DB. Type IV collagens and basement membrane diseases: cell biology and pathogenic mechanisms. Vol. 76 Current Topics in Membranes Elsevier Ltd;2015. p. 61–116.
  • Hohenester E, Yurchenco PD. Laminins in basement membrane assembly. Cell Adh Migr. 2013;7(1):56–63. doi:10.4161/cam.21831.
  • Yurchenco PD. Integrating activities of laminins that drive basement membrane assembly and function. Vol. 76 Current Topics in Membranes Elsevier Ltd;2015. p. 1–30 p.
  • Battaglia C, Mayer U, Aumailley M, Timpl R. Basement‐membrane heparan sulfate proteoglycan binds to laminin by its heparan sulfate chains and to nidogen by sites in the protein core. Eur J Biochem. 1992;208(2):359–66. doi:10.1111/ejb.1992.208.issue-2.
  • Aumailley M, Wiedemann H, Mann K, Timpl R. Binding of nidogen and the laminin nidogen complex to basement membrane collagen type IV. Eur J Biochem. 1989;184(1):241–48. doi:10.1111/ejb.1989.184.issue-1.
  • Matsumoto B, Blanks JC, Ryan SJ. Topographic variation in the rabbit and primate internal limiting membrane. Invest Ophthalmol Vis Sci. 1984;25:71–82.
  • Malecaze F, Caratero C, Caratero A, Arne JL, Mathis A, Bee P, Planel H. Some ultrastructural aspects of the vitreoretinal juncture. Ophthalmologica. 1985;191(1):22–28. doi:10.1159/000309534.
  • Ponsioen TL, van Luyn MJA, van der Worp RJ, Pas HH, Hooymans JMM, Los LI. Human retinal Müller cells synthesize collagens of the vitreous and vitreoretinal interface in vitro. Mol Vis. 2008;14:652–60.
  • Bu SC, Kuijer R, Van Der Worp RJ, Li XR, Hooymans JMM, Los LI. The ultrastructural localization of type II, IV, and VI collagens at the vitreoretinal interface. PLoS One. 2015;10(7):1–23. doi:10.1371/journal.pone.0134325.
  • Heegaard S. Structure of the human vitreoretinal border region. Ophthalmologica. 1994;208:82–92. doi:10.1159/000310458.
  • Syrbe S, Kuhrt H, Gärtner U, Habermann G, Wiedemann P, Bringmann A, Reichenbach A. Müller glial cells of the primate foveola: an electron microscopical study. Exp Eye Res. 2018;167:110–17. doi:10.1016/j.exer.2017.12.004.
  • Foos RY. Vitreoretinal juncture over retinal vessels. Albrecht von Graefes Archiv f?r Klinische und Experimentelle Ophthalmologie. 1977;204:223–34. doi:10.1007/BF00415316.
  • Slijkerman RWN, Song F, Astuti GDN, Huynen MA, van Wijk E, Stieger K, Collin RWJ. The pros and cons of vertebrate animal models for functional and therapeutic research on inherited retinal dystrophies. Prog Retin Eye Res. 2015;48:137–59. doi:10.1016/j.preteyeres.2015.04.004.
  • Noulas AV, Skandalis SS, Feretis E, Theocharis DA, Karamanos NK. Variations in content and structure of glycosaminoglycans of the vitreous gel from different mammalian species. Biomed Chromatogr. 2004;18(7):457–61. doi:10.1002/bmc.340.
  • Pang JJ, Lauramore A, Deng WT, Li Q, Doyle TJ, Chiodo V, Li J, Hauswirth WW. Comparative analysis of in vivo and in vitro AAV vector transduction in the neonatal mouse retina: effects of serotype and site of administration. Vision Res. 2008;48(3):377–85. doi:10.1016/j.visres.2008.06.005.
  • Dalkara D, Kolstad KD, Caporale N, Visel M, Klimczak RR, Schaffer DV, Flannery JG. Inner limiting membrane barriers to AAV-mediated retinal transduction from the vitreous. Mol Ther. 2009;17(12):2096–102. doi:10.1038/mt.2009.181.
  • Vacca O, Darche M, Schaffer DV, Flannery JG, Sahel JA, Rendon A, Dalkara D. AAV-mediated gene delivery in Dp71-null mouse model with compromised barriers. Glia. 2014;62(3):468–76. doi:10.1002/glia.v62.3.
  • Kolstad KD, Dalkara D, Guerin K, Visel M, Hoffmann N, Schaffer DV, Flannery JG. Changes in adeno-associated virus-mediated gene delivery in retinal degeneration. Hum Gene Ther. 2010;578(May):571–78. doi:10.1089/hum.2009.194.
  • Park TK, Wu Z, Kjellstrom S, Zeng Y, Bush RA, Sieving PA, Colosi P. Intravitreal delivery of AAV8 retinoschisin results in cell type-specific gene expression and retinal rescue in the Rs1-KO mouse. Gene Ther. 2009;16(7):916–26. doi:10.1038/gt.2009.61.
  • Hellström M, Ruitenberg MJ, Pollett MA, Ehlert EME, Twisk J, Verhaagen J, Harvey AR. Cellular tropism and transduction properties of seven adeno-associated viral vector serotypes in adult retina after intravitreal injection. Gene Ther. 2009;16(4):521–32. doi:10.1038/gt.2008.178.
  • Yin L, Greenberg K, Hunter JJ, Dalkara D, Kolstad KD, Masella BD, Wolfe R, Visel M, Stone D, Libby RT, et al. Intravitreal injection of AAV2 transduces macaque inner retina. Investig Ophthalmol Vis Sci. 2011;52(5):2775–83. doi:10.1167/iovs.10-6250.
  • Mowat FM, Gornik KR, Dinculescu A, Boye SL, Hauswirth WW, Petersen-Jones SM, Bartoe JT. Tyrosine capsid-mutant AAV vectors for gene delivery to the canine retina from a subretinal or intravitreal approach. Gene Ther. 2014;21(1):96–105. doi:10.1038/gt.2013.64.
  • Aartsen WM, van Cleef KWR, Pellissier LP, Hoek RM, Vos RM, Blits B, Ehlert EME, Balaggan KS, Ali RR, Verhaagen J, et al. GFAP-driven GFP expression in activated mouse Müller glial cells aligning retinal blood vessels following intravitreal injection of AAV2/6 vectors. PLoS One. 2010;5(8):1–12. doi:10.1371/journal.pone.0012387.
  • Ivanova E, Hwang GS, Pan ZH, Troilo D. Evaluation of AAV-mediated expression of chop2-GFP in the marmoset retina. Investig Ophthalmol Vis Sci. 2010;51(10):5288–96. doi:10.1167/iovs.10-5389.
  • Teo KYC, Lee SY, Barathi AV, Tun SBB, Tan L, Constable IJ. Surgical removal of internal limiting membrane and layering of AAV vector on the retina under air enhances gene transfection in a nonhuman primate. Investig Ophthalmol Vis Sci. 2018;59(8):3574–83. doi:10.1167/iovs.18-24333.
  • Wu Z, Miller E, Agbandje-McKenna M, Samulski RJ. 2,3 and 2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6. J Virol. 2006;80(18):9093–103. doi:10.1128/JVI.00895-06.
  • Summerford C, Samulski RJ. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol. 1998;72:1438–45.
  • Boye SL, Bennett A, Scalabrino ML, McCullough KT, Van Vliet K, Choudhury S, Ruan Q, Peterson J, Agbandje-McKenna M, Boye SE, et al. Impact of heparan sulfate binding on transduction of retina by recombinant adeno-associated virus vectors. J Virol. 2016;90(8):4215–31. doi:10.1128/JVI.00200-16.
  • Woodard KT, Liang KJ, Bennett WC, Samulski RJ. Heparan sulfate binding promotes accumulation of intravitreally-delivered adeno-associated viral vectors at the retina for enhanced transduction but weakly influences tropism. J Virol. 2016;90(21):9878–88. doi:10.1128/JVI.01568-16.
  • Sullivan JA, Stanek LM, Lukason MJ, Bu J, Osmond SR, Barry EA, O’Riordan CR, Shihabuddin LS, Cheng SH, Scaria A. Rationally designed AAV2 and AAVrh8R capsids provide improved transduction in the retina and brain. Gene Ther. 2018;25(3):205–19. doi:10.1038/s41434-018-0017-8.
  • Akache B, Grimm D, Pandey K, Yant SR, Xu H, Kay MA. The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol. 2006;80(19):9831–36. doi:10.1128/JVI.00878-06.
  • Klimczak RR, Koerber JT, Dalkara D, Flannery JG, Schaffer DV. A novel adeno-associated viral variant for efficient and selective intravitreal transduction of rat Müller cells. PLoS One. 2009;4(10). doi:10.1371/journal.pone.0007467.
  • Dalkara D, Byrne LC, Klimczak RR, Visel M, Yin L, Merigan WH, Flannery JG, Schaffer DV. In vivo-directed evolution of a new adeno-associated virus for therapeutic outer retinal gene delivery from the vitreous. Sci Transl Med. 2013;5(189):189ra76. doi:10.1126/scitranslmed.3005708.
  • Hickey DG, Edwards TL, Barnard AR, Singh MS, De Silva SR, McClements ME, Flannery JG, Hankins MW, MacLaren RE. Tropism of engineered and evolved recombinant AAV serotypes in the rd1 mouse and ex vivo primate retina. Gene Ther. 2017;24(12):787–800. doi:10.1038/gt.2017.85.
  • Khabou H, Desrosiers M, Winckler C, Fouquet S, Auregan G, Bemelmans AP, Sahel JA, Dalkara D. Insight into the mechanisms of enhanced retinal transduction by the engineered AAV2 capsid variant −7m8. Biotechnol Bioeng. 2016;113(12):2712–24. doi:10.1002/bit.25814.
  • Cehajic-Kapetanovic J, Milosavljevic N, Bedford RA, Lucas RJ, Bishop PN. Efficacy and safety of glycosidic enzymes for improved gene delivery to the retina following intravitreal injection in mice. Mol Ther - Methods Clin Dev. 2018;9(June):192–202. doi:10.1016/j.omtm.2017.12.002.
  • Takahashi K, Igarashi T, Miyake K, Kobayashi M, Yaguchi C, Iijima O, Yamazaki Y, Katakai Y, Miyake N, Kameya S, et al. Improved intravitreal AAV-mediated inner retinal gene transduction after surgical internal limiting membrane peeling in cynomolgus monkeys. Mol Ther. 2017;25(1):296–302. doi:10.1016/j.ymthe.2016.10.004.
  • Sakamoto T, Ueno H, Goto Y, Oshima Y, Ishibashi T, Inomata H. A vitrectomy improves the transfection efficiency of adenoviral vector-mediated gene transfer to Müller cells. Gene Ther. 1998;5(8):1088–97. doi:10.1038/sj.gt.3300591.
  • Tshilenge K-T, Ameline B, Weber M, Mendes-Madeira A, Nedellec S, Biget M, Provost N, Libeau L, Blouin V, Deschamps J-Y, et al. Vitrectomy before intravitreal injection of AAV2/2 vector promotes efficient transduction of retinal ganglion cells in dogs and nonhuman primates. Hum Gene Ther Methods. 2016;27(3):122–34. doi:10.1089/hgtb.2016.034.
  • Da Costa R, Röger C, Segelken J, Barben M, Grimm C, Neidhardt J. A novel method combining vitreous aspiration and intravitreal AAV2/8 injection results in retina-wide transduction in adult mice. Investig Ophthalmol Vis Sci. 2016;57(13):5326–34. doi:10.1167/iovs.16-19701.
  • Lee SH, Colosi P, Lee H, Ohn Y-H, Kim S-W, Kwak HW, Park TK. Laser photocoagulation enhances adeno-associated viral vector transduction of mouse retina. Hum Gene Ther Methods. 2014;25(1):83–91. doi:10.1089/hgtb.2013.089.
  • Lee SH, Kim YS, Nah SK, Kim HJ, Park HY, Yang JY, Park K, Park TK. Transduction patterns of adeno-associated viral vectors in a laser-induced choroidal neovascularization mouse model. Mol Ther - Methods Clin Dev. 2018;9(June):90–98. doi:10.1016/j.omtm.2018.01.008.
  • Boye SE, Alexander JJ, Witherspoon CD, Boye SL, Peterson JJ, Clark ME, Sandefer KJ, Girkin CA, Hauswirth WW, Gamlin PD, et al. Highly efficient delivery of AAV vectors to the primate retina. 2016;1(352):1–43.
  • Stewart MW. Pharmacokinetics, pharmacodynamics and pre-clinical characteristics of ophthalmic drugs that bind VEGF. Expert Rev Clin Pharmacol. 2014;7(2):167–80. doi:10.1586/17512433.2014.884458.
  • Mordenti J, Cuthbertson RA, Ferrara N, Thomsen K, Berleau L, Licko V, Allen PC, Valverde CR, Meng YG, Fei DT et al. Comparisons of the intraocular tissue distribution, pharmacokinetics, and safety of 125 I-labeled full-length and fab antibodies following intravitreal administration. Toxicol Pathol. 1999;27(5):536–44. doi:10.1177/019262339902700507.
  • Peyman GA, Spitznas M, Straatsma BR. Peroxidase diffusion in the normal and photocoagulated retina. Invest Ophthalmol Vis Sci. 1971;10:181–89.
  • Takeuchi A, Kricorian G, Yao XY, Kenny JW, Marmor MF. The rate and source of albumin entry into saline-filled experimental retinal detachments. Investig Ophthalmol Vis Sci. 1994;35:3792–98.
  • Kamei M, Misono K, Lewis H. A study of the ability of tissue plasminogen activator to diffuse into the subretinal space after intravitreal injection in rabbits. Am J Ophthalmol. 1999;128(6):739–46. doi:10.1016/S0002-9394(99)00239-1.
  • Lewis GP, Fisher SK, Anderson DH. Fate of biotinylated basic fibroblast growth factor in the retina following intravitreal injection. ExpEye Res. 1996;62:309–24.
  • Gaudreault J, Fei D, Beyer JC, Ryan A, Rangell L, Shiu V, Damico LA. Pharmacokinetics and retinal distribution of ranibizumab, a humanized antibody fragment directed against VEGF-A, following intravitreal administration in rabbits. Retina. 2007;27(9):1260–66. doi:10.1097/IAE.0b013e318134eecd.
  • Gaudreault J, Fei D, Rusit J, Suboc P, Shiu V. Preclinical pharmacokinetics of ranibizumab (rhuFabV2) after a single intravitreal administration. Investig Ophthalmol Vis Sci. 2005;46(2):726–33. doi:10.1167/iovs.04-0601.
  • Shahar J, Avery RL, Heilweil G, Barak A, Zemel E, Lewis GP, Johnson PT, Fisher SK, Perlman I, Loewenstein A. Electrophysiologic and retinal penetration studies following intravitreal injection of bevacizumab (Avastin). Retina. 2006;26(3):262–69. doi:10.1097/00006982-200603000-00002.
  • Pulido JS, Bakri SJ, Valyi-Nagy T, Shukla D. Rituximab penetrates full-thickness retina in contrast to tissue plasminogen activator control. Retina. 2007;27(8):1071–73. doi:10.1097/IAE.0b013e31804ac032.
  • Ekdawi NS, Pulido JS, Itty S, Marler RJ, Herman DC, Hardwig P, Mohney BG, Valyi-Nagy T, Shukla D. Intravitreal alemtuzumab penetrates full-thickness retina in rabbit eyes. Retina. 2009;29(10):1532–34. doi:10.1097/IAE.0b013e3181b901df.
  • Heiduschka P, Fietz H, Hofmeister S, Schultheiss S, Mack AF, Peters S, Ziemssen F, Niggemann B, Julien S, Bartz-Schmidt KU, et al. Penetration of bevacizumab through the retina after intravitreal injection in the monkey. Investig Ophthalmol Vis Sci. 2007;48(6):2814–23. doi:10.1167/iovs.06-1171.
  • Dib E, Maia M, Longo-Maugeri IM, Martins MC, Mussalem JS, Squaiella CC, Penha FM, Magalha~Es O, Rodrigues EB, Farah ME. Subretinal bevacizumab detection after intravitreous injection in rabbits. Investig Ophthalmol Vis Sci. 2008;49(3):1097–100. doi:10.1167/iovs.07-1225.
  • Lassota N, Prause JU, Scherfig E, Kiilgaard JF, La Cour M. Clinical and histological findings after intravitreal injection of bevacizumab (Avastin) in a porcine model of choroidal neovascularization. Acta Ophthalmol. 2010;88(3):300–08. doi:10.1111/j.1755-3768.2008.01439.x.
  • Goldenberg DT, Giblin FJ, Cheng M, Chintala SK, Trese MT, Drenser KA, Ruby AJ. Posterior vitreous detachment with microplasmin alters the retinal penetration of intravitreal bevacizumab (Avastin) in rabbit eyes. Retina. 2011;31(2):393–400. doi:10.1097/IAE.0b013e3181e586b2.
  • Hutton-Smith LA, Gaffney EA, Byrne HM, Maini PK, Gadkar K, Mazer NA. Ocular pharmacokinetics of therapeutic antibodies given by intravitreal injection: estimation of retinal permeabilities using a 3-compartment semi-mechanistic model. Mol Pharm. 2017;14(8):2690–96. doi:10.1021/acs.molpharmaceut.7b00164.
  • Gadkar K, Pastuskovas CV, Le Couter JE, Elliott JM, Zhang J, Lee CV, Sanowar S, Fuh G, Kim HS, Lombana TN, et al. Design and pharmacokinetic characterization of novel antibody formats for ocular therapeutics. Investig Ophthalmol Vis Sci. 2015;56(9):5390–400. doi:10.1167/iovs.15-17108.
  • Li SK, Liddell MR, Wen H. Effective electrophoretic mobilities and charges of anti-VEGF proteins determined by capillary zone electrophoresis. J Pharm Biomed Anal. 2011;55(3):603–07. doi:10.1016/j.jpba.2010.12.027.
  • Pitkänen L, Pelkonen J, Ruponen M, Rönkkö S, Urtti A. Neural retina limits the nonviral gene transfer to retinal pigment epithelium in an in vitro bovine eye model. Aaps J. 2004;6(3):article25. doi:10.1208/aapsj060322.
  • Apaolaza PS, Del Pozo-Rodríguez A, Solinís MA, Rodríguez JM, Friedrich U, Torrecilla J, Weber BHF, Rodríguez-Gascón A. Structural recovery of the retina in a retinoschisin-deficient mouse after gene replacement therapy by solid lipid nanoparticles. Biomaterials. 2016;90:40–49. doi:10.1016/j.biomaterials.2016.03.004.
  • Martens TF, Peynshaert K, Nascimento TL, Fattal E, Karlstetter M, Langmann T, Picaud S, Demeester J, De Smedt SC, Remaut K, et al. Effect of hyaluronic acid-binding to lipoplexes on intravitreal drug delivery for retinal gene therapy. Eur J Pharm Sci. 2017;103:27–35. doi:10.1016/j.ejps.2017.02.027.
  • Huang D, Chen YS, Rupenthal ID. Hyaluronic acid coated albumin nanoparticles for targeted peptide delivery to the retina. Mol Pharm. 2017;14(2):533–45. doi:10.1021/acs.molpharmaceut.6b01029.
  • Kim H, Robinson SB, Csaky KG. Investigating the movement of intravitreal human serum albumin nanoparticles in the vitreous and retina. Pharm Res. 2009;26(2):329–37. doi:10.1007/s11095-008-9767-0.
  • Andrieu-Soler C, Aubert-Pouessel A, Doat M, Picaud S, Halhal M, Simonutti M, Venier-Julienne MC, Benoit JP and Behar-Cohen F et al. Intravitreous injection of PLGA microspheres encapsulating GDNF promotes the survival of photoreceptors in the rd1/rd1 mouse. Mol Vis. 2005;11(February):1002–11.
  • Peters T, Kim S-W, Castro V, Stingl K, Strasser T, Bolz S, Schraermeyer U, Mihov G, Zong M, Andres-Guerrero V, et al. Evaluation of polyesteramide (PEA) and polyester (PLGA) microspheres as intravitreal drug delivery systems in albino rats. Biomaterials. 2017;124:157–68. doi:10.1016/j.biomaterials.2017.02.006.
  • Lee J, Goh U, Lee HJ, Kim J, Jeong M, Park JH. Effective retinal penetration of lipophilic and lipid-conjugated hydrophilic agents delivered by engineered liposomes. Mol Pharm. 2017;14(2):423–30. doi:10.1021/acs.molpharmaceut.6b00864.
  • Koo H, Moon H, Han H, Na JH, Huh MS, Park JH, Woo SJ, Park KH, Chan Kwon I, Kim K, et al. The movement of self-assembled amphiphilic polymeric nanoparticles in the vitreous and retina after intravitreal injection. Biomaterials. 2012;33(12):3485–93. doi:10.1016/j.biomaterials.2012.01.030.
  • Ochoa GP, Sesma JZ, Díez MA, Díaz-Tahoces A, Avilés-Trigeros M, Grijalvo S, Eritja R, Fernández E, Pedraz JL. A novel formulation based on 2,3-di(tetradecyloxy)propan-1-amine cationic lipid combined with polysorbate 80 for efficient gene delivery to the retina. Pharm Res. 2014;31(7):1665–75. doi:10.1007/s11095-013-1271-5.
  • Ojeda E, Puras G, Agirre M, Zarate J, Grijalvo S, Eritja R, Martinez-Navarrete G, Soto-Sánchez C, Diaz-Tahoces A, Aviles-Trigueros M, et al. The influence of the polar head-group of synthetic cationic lipids on the transfection efficiency mediated by niosomes in rat retina and brain. Biomaterials. 2016;77:267–79. doi:10.1016/j.biomaterials.2015.11.017.
  • Mashal M, Attia N, Puras G, Martínez-Navarrete G, Fernández E, Pedraz JL. Retinal gene delivery enhancement by lycopene incorporation into cationic niosomes based on DOTMA and polysorbate 60. J Control Release. 2017;254(January):55–64. doi:10.1016/j.jconrel.2017.03.386.
  • Kim H, Csaky KG. Nanoparticle-integrin antagonist C16Y peptide treatment of choroidal neovascularization in rats. J Control Release. 2010;142(2):286–93. doi:10.1016/j.jconrel.2009.11.006.
  • Nishihara H. Studies on the ultrastructure of the inner limiting membrane of the retina. I. Surface replication study on the inner limiting membrane of the retina. Nihon Ganka Gakkai Zasshi. 1989 Apr;93(4):429–38.
  • Bourges JL, Gautier SE, Delie F, Bejjani RA, Jeanny JC, Gurny R, BenEzra D, Behar-Cohen FF. Ocular drug delivery targeting the retina and retinal pigment epithelium using polylactide nanoparticles. Investig Ophthalmol Vis Sci. 2003;44(8):3562–69. doi:10.1167/iovs.02-1068.
  • Peynshaert K, Devoldere J, Forster V, Picaud S, De Smedt SC, Remaut K. Toward smart design of retinal drug carriers: a novel bovine retinal explant model to study the barrier role of the vitreoretinal interface. Drug Deliv. 2017;24(1):1384–94. doi:10.1080/10717544.2016.1267822.
  • MacLaren RE, Bennett J, Schwartz SD. Gene therapy and stem cell transplantation in retinal disease: the new frontier. Ophthalmology. 2016;123(10):S98–106. doi:10.1016/j.ophtha.2016.06.041.
  • Johnson TV, Bull ND, Martin KR. Identification of barriers to retinal engraftment of transplanted stem cells. Investig Ophthalmol Vis Sci. 2010;51(2):960–70. doi:10.1167/iovs.09-3884.
  • Nishida A, Takahashi M, Tanihara H, Nakano I. Incorporation and differentiation of hippocampus- derived neural stem cells transplanted in injured adult rat retina AND. Invest Ophthalmol Vis Sci. 2000;41:4268–74.
  • Yu S, Tanabe T, Dezawa M, Ishikawa H, Yoshimura N. Effects of bone marrow stromal cell injection in an experimental glaucoma model. Biochem Biophys Res Commun. 2006;344(4):1071–79. doi:10.1016/j.bbrc.2006.04.003.
  • Wang X, Tay SS, Ng YK. An immunohistochemical study of neuronal and glial cell reactions in retinae of rats with experimental glaucoma. Exp Brain Res. 2000;132(4):476–84. doi:10.1007/s002210000360.
  • Kim IB, Kim KY, Joo CK, Lee MY, Oh SJ, Chung JW, Chun MH. Reaction of Müller cells after increased intraocular pressure in the rat retina. Exp Brain Res. 1998;121(4):419–24. doi:10.1007/s002210050476.
  • Del Amo EM, Rimpelä AK, Heikkinen E, Kari OK, Ramsay E, Lajunen T, Schmitt M, Pelkonen L, Bhattacharya M, Richardson D et al. Pharmacokinetic aspects of retinal drug delivery. Prog Retin Eye Res. 2017;57:134–85. doi:10.1016/j.preteyeres.2016.12.002.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.