Drug and gene delivery to the back of the eye: From bench to bedside

Investigative Ophthalmology and Visual Science

Volumn 55, Issue 4, 2014, Pages 2714-2730

  Rowe Rendleman, Cheryl L ^a   Durazo, Shelley A ^b   Kompella, Uday B ^b   Rittenhouse, Kay D ^c   Di Polo, Adriana ^d   Weiner, Alan L ^e   Grossniklaus, Hans E ^f   Naash, Muna I ^g   Lewin, Alfred S ^h   Horsager, Alan ⁱ   Edelhauser, Henry F ^f  

^a Omar Consulting Group LLC   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c PFIZER INC   (United States)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

^e DrugDel Consulting LLC   (United States)

^f EMORY EYE CENTER   (United States)

^g UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^h UNIVERSITY OF FLORIDA   (United States)

ⁱ UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Drug delivery; Gene therapy; Nanoparticle; Retina; Translational medicine

Indexed keywords

BEVACIZUMAB; CARRIER PROTEIN; CYCLODEXTRIN; DENDRIMER; LENTIVIRUS VECTOR; MACROGOL; NANOPARTICLE; PACLITAXEL; PARVOVIRUS VECTOR;

ARTICLE; BIOAVAILABILITY; BLOOD RETINA BARRIER; CHOROID CAPILLARY LAYER; CLINICAL ASSESSMENT TOOL; COST; DIABETIC RETINOPATHY; DIAGNOSTIC IMAGING; DRUG APPROVAL; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MANUFACTURE; DRUG SCREENING; DRUG SOLUBILITY; GENE DELIVERY SYSTEM; HUMAN; HYDROGEL; MEMBRANE TRANSPORT; MICRONEEDLE; NONHUMAN; NONVIRAL GENE THERAPY; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); POSTERIOR EYE CHAMBER; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; VIRAL GENE THERAPY;

DRUG DELIVERY; GENE THERAPY; NANOPARTICLE; RETINA; TRANSLATIONAL MEDICINE;

DRUG DELIVERY SYSTEMS; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; HUMANS; PHARMACEUTICAL PREPARATIONS; RETINAL DISEASES;

EID: 84899673624     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-13707     Document Type: Article

References (74)

1. Edelhauser HF, Rowe-Rendleman CL, Robinson MR, et al. Ophthalmic drug delivery systems for the treatment of retinal diseases: basic research to clinical applications. Invest Ophthalmol Vis Sci. 2010;51:5403-5420.
2. Gordois A, Pezzullo L, Cutler H. The Global Economic Cost of Visual Impairment. Sidney: Access Economics Pty Limited; 2010.
3. Sebag J. Age-related changes in human vitreous structure. Graefes Arch Clin Exp Ophthalmol. 1987;225:89-93.
4. Hughes PM, Olejnik O, Chang-Lin JE, Wilson CG. Topical and systemic drug delivery to the posterior segment. Adv Drug Deliv Rev. 2005;57:2010-2032.
5. Bill A. Movement of albumin and dextran through the sclera. Arch Ophthalmol. 1965;74:248-252.
6. Robinson MR, Lee SS, Kim H, et al. A rabbit model for assessing the ocular barriers to the transscleral delivery of triamcinolone acetonide. Exp Eye Res. 2006;82:479-487.
7. Olsen TW, Edelhauser HF, Lim JI, Geroski DH. Human scleral permeability. Effects of age, cryotherapy, transscleral diode laser, and surgical thinning. Invest Ophthalmol Vis Sci. 1995; 36:1893-1903.
8. Patel SR, Berezovsky DE, McCarey BE, Zarnitsyn V, Edelhauser HF, Prausnitz MR. Targeted administration into the suprachoroidal space using a microneedle for drug delivery to the posterior segment of the eye. Invest Ophthalmol Vis Sci. 2012; 53:4433-4441.
9. Center for Drug Evaluation and Research. Guidance for Industry: Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. Silver Spring, MD: U.S. Department of Health and Human Services, Food and Drug Administration; 2005:1-27.
10. Rittenhouse KD, Peiffer RL Jr, Pollack GM. Microdialysis evaluation of the ocular pharmacokinetics of propranolol in the conscious rabbit. Pharm Res. 1999;16:736-742.
11. Short BG. Safety evaluation of ocular drug delivery formulations: techniques and practical considerations. Toxicol Pathol. 2008;36:49-62.
12. Balazs EA, Denlinger JL. The Vitreous. New York, NY: Academic Press; 1984.
13. Le Goff MM, Bishop PN. Adult vitreous structure and postnatal changes. Eye (Lond). 2008;22:1214-1222.
14. Kadam RS, Cheruvu NP, Edelhauser HF, Kompella UB. Sclerachoroid-RPE transport of eight beta-blockers in human, bovine, porcine, rabbit, and rat models. Invest Ophthalmol Vis Sci. 2011;52:5387-5399.
15. Nomoto H, Shiraga F, Kuno N, et al. Pharmacokinetics of bevacizumab after topical, subconjunctival, and intravitreal administration in rabbits. Invest Ophthalmol Vis Sci. 2009;50: 4807-4813.
16. Krohne TU, Eter N, Holz FG, Meyer CH. Intraocular pharmacokinetics of bevacizumab after a single intravitreal injection in humans. Am J Ophthalmol. 2008;146:508-512.
17. Durairaj C, Kadam RS, Chandler JW, Hutcherson SL, Kompella UB. Nanosized dendritic polyguanidilyated translocators for enhanced solubility, permeability, and delivery of gatifloxacin. Invest Ophthalmol Vis Sci. 2010;51:5804-5816.
18. Holden CA, Tyagi P, Thakur A, et al. Polyamidoamine dendrimer hydrogel for enhanced delivery of antiglaucoma drugs. Nanomedicine. 2012;8:776-783.
19. Yang H, Tyagi P, Kadam RS, Holden CA, Kompella UB. Hybrid dendrimer hydrogel/PLGA nanoparticle platform sustains drug delivery for one week and antiglaucoma effects for four days following one-time topical administration. ACS Nano. 2012;6: 7595-7606.
20. Ghate D, Edelhauser H. Ocular drug delivery. Expert Opin Drug Deliv. 2006;3:275-287.
21. Jager RD, Aiello LP, Patel SC, Cunningham ET. Risks of intravenous injection: a comprehensive review. Retina. 2004;24:676-698.
22. Koo H, Moon H, Han H, et al. The movement of self-assembled amphiphilic polymeric nanoparticles in the vitreous and retina after intravitreal injection. Biomaterials. 2012;33:3485-3493.
23. Kim H, Robinson SB, Csaky KG. Investigating the movement of intravitreal human serum albumin nanoparticles in the vitreous and retina. Pharm Res. 2009;26:329-337.
24. Khalili H, Godwin A, Lever R, Brocchini S. Comparative Disulfide-Bridging PEGylation of Ranibizumab and the Fab Derived from Bevacizumab. Washington, DC: American Association of Pharmaceutical Scientists; 2011.
25. Misra GP, Singh RS, Aleman TS, Jacobson SG, Gardner TW, Lowe TL. Subconjunctivally implantable hydrogels with degradable and thermoresponsive properties for sustained release of insulin to the retina. Biomaterials. 2009;30:6541-6547.
26. Cunha-Vaz J. The blood retina barrier in retinal disease. Eur J Ophthalmol. 2011;21(suppl 6):S3-S9.
27. Singh SR, Grossniklaus HE, Kang SJ, Edelhauser HF, Ambati BK, Kompella UB. Intravenous transferrin, RGD peptide and dualtargeted nanoparticles enhance anti-VEGF intraceptor gene delivery to laser-induced CNV. Gene Ther. 2009;16:645-659.
28. Carpenter JF, Pikal MJ, Chang BS, Randolph TW. Rational design of stable lyophilized protein formulations: some practical advice. Pharm Res. 1997;14:969-975.
29. Chothe P, Singh N, Ganapathy V. Evidence for two different broad-specificity oligopeptide transporters in intestinal cell line Caco-2 and colonic cell line CCD841. Am J Cell Physiol. 2011;300:1260-1269.
30. Chothe PP, Thakkar SV, Gnana-Prakasam JP, et al. Identification of a novel sodium-coupled oligopeptide transporter (SOPT2) in mouse and human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 2010;51:413-420.
31. Chothe PP, Gnana-Prakasam JP, Ananth S, et al. Transport of hepcidin, an iron-regulatory peptide hormone, into retinal pigment epithelial cells via oligopeptide transporters and its relevance to iron homeostasis. Biochem Biophys Res Comm. 2011;405:244-249.
32. Anand B, Nashed Y, Mitra A. Novel dipeptide prodrugs of acyclovir for ocular herpes infections: bioreversion, antiviral activity and transport across rabbit cornea. Curr Eye Res. 2003;26:151-163.
33. Talluri RS, Samanta SK, Gaudana R, Mitra AK. Synthesis, metabolism and cellular permeability of enzymatically stable dipeptide prodrugs of acyclovir. Int J Pharm. 2008;361:118-124.
34. Mitra AK, Samanta SK, Talluri RS, inventors; The Curators of the University of Missouri, assignee. Stereochemically defined dipeptide esters of antiviral agents for enhanced ocular treatment. US patent 7951774 B2. May 31, 2011.
35. Martínez-Sancho C, Herrero-Vanrell R, Negro S. Vitamin A palmitate and acyclovir biodegradable microspheres for intraocular sustained release. Int J Pharm. 2006;326:100-106.
36. Checa-Casalengua P, Jiang C, Bravo-Osuna I, et al. Retinal ganglion cells survival in a glaucoma model by GDNF/Vit E PLGA microspheres prepared according to a novel microencapsulation procedure. J Control Release. 2011;156:92-100.
37. Edelhauser HF, Boatright JH, Nickerson JM. Third ARVO/Pfizer Research Institute Working Group. Drug delivery to posterior intraocular tissues: third annual ARVO/Pfizer Ophthalmics Research Institute Conference. Invest Ophthalmol Vis Sci. 2008;49:4712-4720.
38. Hahn P, Fekrat S. Best practices for treatment of retinal vein occlusion. Curr Opin Ophthalmol. 2012;23:175-181.
39. Yandrapu SK, Upadhyay AK, Petrash JM, Kompella UB. Nanoparticles in porous microparticles prepared by supercritical infusion and pressure quench technology for sustained delivery of bevacizumab. Mol Pharm. 2013;10:4676-4686.
40. Prentice HM, Biswal MR, Dorey CK, Blanks JC. Hypoxiaregulated retinal glial cell-specific promoter for potential gene therapy in disease. Invest Ophthalmol Vis Sci. 2011;52:8562-8570.
41. Stone EM, Fingert JH, Alward WL, et al. Identification of a gene that causes primary open angle glaucoma. Science. 1997;275: 668-670.
42. Farrar GJ, Kenna PF, Humphries P. On the genetics of retinitis pigmentosa and on mutation-independent approaches to therapeutic intervention. EMBO J. 2002;21:857-864.
43. Bennett J. Commentary: an aye for eye gene therapy. Hum Gene Ther. 2006;17:177-179.
44. Farjo R, Skaggs J, Quiambao AB, Cooper MJ, Naash MI. Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PloS One. 2006;1:e38.
45. Han Z, Conley SM, Makkia R, et al. Comparative analysis of DNA nanoparticles and AAVs for ocular gene delivery. PLoS One. 2012;7:e521819.
46. Ding XQ, Quiambao AB, Fitzgerald JB, Cooper MJ, Conley SM, Naash MI. Ocular delivery of compacted DNA-nanoparticles does not elicit toxicity in the mouse retina. PloS One. 2009;4: e7410.
47. Cai X, Conley SM, Nash Z, Fliesler SJ, Cooper MJ, Naash MI. Gene delivery to mitotic and postmitotic photoreceptors via compacted DNA nanoparticles results in improved phenotype in a mouse model of retinitis pigmentosa. FASEB J. 2010;24: 1178-1191.
48. Konstan MW, Davis PB, Wagener JS. Compacted DNA nanoparticles administered to the nasal mucosa of cystic fibrosis subjects are safe and demonstrate partial to complete cystic fibrosis transmembrane regulator reconstitution. Hum Gene Ther. 2004;15:1255-1269.
49. Koirala A, Makkia RS, Cooper MJ, Naash MI. Nanoparticlemediated gene transfer specific to retinal pigment epithelial cells. Biomaterials. 2011;32:9483-9493.
50. Binley K, Widdowson P, Loader J, et al. Transduction of photoreceptors with equine infectious anemia virus lentiviral vectors: safety and biodistribution of StarGen for Stargardt Disease. Invest Ophthalmol Vis Sci. 2013;54:4061-4071.
51. Calame M, Cachafeiro M, Philippe S, et al. Retinal degeneration progression changes lentiviral vector cell targeting in the retina. PLoS One. 2011;6:e23782.
52. Kay CN, Ryals RC, Aslanidi GV, et al. Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS One. 2013;8:e62097.
53. Petrs-Silva H, Dinculescu A, Li Q, et al. High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther. 2009;17:463-471.
54. Testa F, Maguire AM, Rossi S, et al. Three-year follow-up after unilateral subretinal delivery of adeno-associated virus in patients with Leber congenital amaurosis type 2. Ophthalmology. 2013;120:1283-1291.
55. Bainbridge JW, Smith AJ. Parker SS, et al. Effect of gene therapy on visual function in Leber congenital amaurosis. N Engl J Med. 2008;358:2231-2239.
56. Cideciyan AV, Aleman TS, Boye SL, et al. Human gene therapy for RPE65 isomerase deficiency activates the retinoid cycle of vision but with slow rod kinetics. Proc Natl Acad Sci U S A. 2008;105:15112-15117.
57. Hauswirth W, Aleman TS, Kaushal S, et al. Treatment of Leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector: short-term results of a phase I trial. Hum Gene Ther. 2008;19: 979-990.
58. Kaiser J. Gene therapy. Two teams report progress in reversing loss of sight. Science. 2008;320:606-607.
59. Maguire AM, Simonelli F, Pierce EA, et al. Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med. 2008;358:2240-2248.
60. Daiger SP, Bowne SJ, Sullivan LS. Perspective on genes and mutations causing retinitis pigmentosa. Arch Ophthalmol. 2007;125:151-158.
61. Marc RE, Jones BW. Retinal remodeling in inherited photoreceptor degenerations. Mol Neurobiol. 2003;28:139-147.
62. Yanai D, Weiland JD, Mahadevappa M, Greenberg RJ, Fine I, Humayun MS. Visual performance using a retinal prosthesis in three subjects with retinitis pigmentosa. Am J Ophthalmol. 2007;143:820-827.
63. de Balthasar C, Patel S, Roy A, et al. Factors affecting perceptual thresholds in epiretinal prostheses. Invest Ophthalmol Vis Sci. 49:2303-2314.
64. Winter JO, Cogan SF, Rizzo JF 3rd. Retinal prostheses: current challenges and future outlook. J Biomater Sci Polym Ed. 2007; 18:1031-1055.
65. Roska B, Werblin F. Vertical interactions across ten parallel, stacked representations in the mammalian retina. Nature. 2001;410:583-587.
66. Roska B, Molnar A, Werblin FS. Parallel processing in retinal ganglion cells: how integration of space-time patterns of excitation and inhibition form the spiking output. J Neurophysiol. 2006;95:3810-3822.
67. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M, Dizhoor AM, Pan ZH. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron. 2006;50:23-33.
68. Baccus SA. Timing and computation in inner retinal circuitry. Annu Rev Physiol. 2007;69:271-290.
69. Lagali PS, Balya D, Awatramani GB, et al. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci. 2008;11:667-675.
70. Boyden ES, Zhang F, Bamberg E, et al. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005;8:1263-1268.
71. Dorouchi MM, Greenberg KP, Liu J, et al. Virally delivered channelrhodpsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol Ther. 2005;8: 1263-1268.
72. Jacobsen SG, Cideciyan AV, Ratnakaram R, et al. Gene therapy for Leber congenital amaurosis caused by RPE65 mutations: safety and efficacy in 15 children and adults followed up to 3 years. Arch Ophthalmol. 2012;130:9-24.
73. Tanito M, Haro K, Matsuoka Y, et al. Topical dexamethasonecyclodextrin microparticle eye drops for diabetic macular edema. Invest Ophthalmol Vis Sci. 2011;52:7944-7948.
74. Jayagopal A, Russ PK, Haselton FR. Surface engineering of quantum dots for in vivo vascular imaging. Bioconjug Chem. 2007;18:1424-1433.