A microparticle/hydrogel combination drug-delivery system for sustained release of retinoids

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 10, 2012, Pages 6314-6323

  Gao, Song Qi ^a   Maeda, Tadao ^a   Okano, Kiichiro ^a   Palczewski, Krzysztof ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; OPSIN; POLYGLACTIN; RETINOID; VISUAL PIGMENT; 9 CIS RETINAL; 9-CIS-RETINAL; ACYLTRANSFERASE; GLUCURONIC ACID; HEXURONIC ACID; LACTIC ACID; LECITHIN RETINOL ACYLTRANSFERASE; LECITHIN-RETINOL ACYLTRANSFERASE; MICROSPHERE; POLYGLYCOLIC ACID; POLYLACTIC ACID POLYGLYCOLIC ACID COPOLYMER; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; RETINAL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; ELECTRORETINOGRAPHY; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOLOGY; HYDROGEL; LIGHT DARK CYCLE; MALE; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA DISEASE; SCANNING ELECTRON MICROSCOPY; SINGLE DRUG DOSE; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; SUSTAINED DRUG RELEASE; VISION; ANIMAL; BLINDNESS; CHEMISTRY; DELAYED RELEASE FORMULATION; DISEASE MODEL; DRUG COMBINATION; DRUG EFFECT; GENETICS; HUMAN; INTRAVITREAL DRUG ADMINISTRATION; METABOLISM; METHODOLOGY; MOUSE MUTANT; ORAL DRUG ADMINISTRATION; SUBCUTANEOUS DRUG ADMINISTRATION;

ACYLTRANSFERASES; ADMINISTRATION, ORAL; ALGINATES; ANIMALS; BLINDNESS; DELAYED-ACTION PREPARATIONS; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; DRUG THERAPY, COMBINATION; ELECTRORETINOGRAPHY; FEMALE; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; HYDROGEL; INJECTIONS, SUBCUTANEOUS; INTRAVITREAL INJECTIONS; LACTIC ACID; MALE; MICE; MICE, MUTANT STRAINS; MICROSPHERES; POLYGLYCOLIC ACID; RETINALDEHYDE; RETINOIDS;

EID: 84871700573     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-10279     Document Type: Article

References (74)

1. Cideciyan AV. Leber congenital amaurosis due to RPE65 mutations and its treatment with gene therapy. Prog Retin Eye Res. 2010;29:398-427.
2. Gu SM, Thompson DA, Srikumari CR, et al. Mutations in RPE65 cause autosomal recessive childhood-onset severe retinal dystrophy. Nat Genet. 1997;17:194-197.
3. Palczewski K. Blind dogs that can see: pharmacological treatment of Leber congenital amaurosis caused by a defective visual cycle. Arch Ophthalmol. 2010;128:1483-1485.
4. Palczewski K. G protein-coupled receptor rhodopsin. Annu Rev Biochem. 2006;75:743-767.
5. Palczewski K. Retinoids for treatment of retinal diseases. Trends Pharmacol Sci. 2010;31:284-295.
6. Travis GH, Golczak M, Moise AR, Palczewski K. Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu Rev Pharmacol Toxicol. 2007;47:469-512.
7. McBee JK, Palczewski K, Baehr W, Pepperberg DR. Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog Retin Eye Res. 2001;20:469-529.
8. von Lintig J, Kiser PD, Golczak M, Palczewski K. The biochemical and structural basis for trans-to-cis isomerization of retinoids in the chemistry of vision. Trends Biochem Sci. 2010;35:400-410.
9. Kiser PD, Golczak M, Maeda A, Palczewski K. Key enzymes of the retinoid (visual) cycle in vertebrate retina. Biochim Biophys Acta. 2012;1821:137-151.
10. Parker RO, Crouch RK. Retinol dehydrogenases (RDHs) in the visual cycle. Exp Eye Res. 2010;91:788-792.
11. Lamb TD, Pugh EN Jr. Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res. 2004;23:307-380.
12. den Hollander AI, Roepman R, Koenekoop RK, Cremers FP. Leber congenital amaurosis: genes, proteins and disease mechanisms. Prog Retin Eye Res. 2008;27:391-419.
13. Saari JC, Bredberg DL, Farrell DF. Retinol esterification in bovine retinal pigment epithelium: reversibility of lecithin: retinol acyltransferase. Biochem J. 1993;291:697-700.
14. MacDonald PN, Ong DE. Evidence for a lecithin-retinol acyltransferase activity in the rat small intestine. J Biol Chem. 1988;263:12478-12482.
15. Ruiz A, Winston A, Lim YH, Gilbert BA, Rando RR, Bok D. Molecular and biochemical characterization of lecithin retinol acyltransferase. J Biol Chem. 1999;274:3834-3841.
16. Batten ML, Imanishi Y, Maeda T, et al. Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem. 2004;279: 10422-10432.
17. Imanishi Y, Batten ML, Piston DW, Baehr W, Palczewski K. Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J Cell Biol. 2004;164:373-383.
18. Batten ML, Imanishi Y, Tu DC, et al. Pharmacological and rAAV gene therapy rescue of visual functions in a blind mouse model of Leber congenital amaurosis. PLoS Med. 2005;2:e333.
19. Moiseyev G, Chen Y, Takahashi Y, Wu BX, Ma JX. RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci U S A. 2005;102:12413-12418.
20. Redmond TM, Poliakov E, Yu S, Tsai JY, Lu Z, Gentleman S. Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proc Natl Acad Sci U S A. 2005;102:13658-13663.
21. Jin M, Li S, Moghrabi WN, Sun H, Travis GH. Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell. 2005;122:449-459.
22. Thompson DA, Li Y, McHenry CL, et al. Mutations in the gene encoding lecithin retinol acyltransferase are associated with early-onset severe retinal dystrophy. Nat Genet. 2001;28:123-124.
23. Van Hooser JP, Liang Y, Maeda T, et al. Recovery of visual functions in a mouse model of Leber congenital amaurosis. J Biol Chem. 2002;277:19173-19182.
24. Van Hooser JP, Aleman TS, He YG, et al. Rapid restoration of visual pigment and function with oral retinoid in a mouse model of childhood blindness. Proc Natl Acad Sci U S A. 2000; 97:8623-8628.
25. Wald G, Brown PK, Hubbard R, Oroshnik W. Hindered cis isomers of vitamin A and retinene: the structure of the neo-B isomer. Proc Natl Acad Sci U S A. 1955;41:438-451.
26. DeGrip WJ, Liu RS, Ramamurthy V, Asato A. Rhodopsin analogues from highly hindered 7-cis isomers of retinal. Nature. 1976;262:416-418.
27. Maeda T, Maeda A, Casadesus G, Palczewski K, Margaron P. Evaluation of 9-cis-retinyl acetate therapy in Rpe65_/_ mice. Invest Ophthalmol Vis Sci. 2009;50:4368-4378.
28. Maeda T, Perusek L, Amengual J, Babino D, Palczewski K, von Lintig J. Dietary 9-cis-beta, beta-carotene fails to rescue vision in mouse models of leber congenital amaurosis. Mol Pharmacol. 2011;80:943-952.
29. Maeda T, Cideciyan AV, Maeda A, et al. Loss of cone photoreceptors caused by chromophore depletion is partially prevented by the artificial chromophore pro-drug, 9-cis-retinyl acetate. Hum Mol Genet. 2009;18:2277-2287.
30. Babizhayev MA, Kasus-Jacobi A. State of the art clinical efficacy and safety evaluation of N-acetylcarnosine dipeptide ophthalmic prodrug. Principles for the delivery, self-bioactivation, molecular targets and interaction with a highly evolved histidyl-hydrazide structure in the treatment and therapeutic management of a group of sight-threatening eye diseases. Curr Clin Pharmacol. 2009;4:4-37.
31. Davis J, Olsen TW, Stewart M, Sternberg P Jr. How the comparison of age-related macular degeneration treatments trial results will impact clinical care. Am J Ophthalmol. 2011; 152:509-514.
32. Jager RD, Aiello LP, Patel SC, Cunningham ET Jr. Risks of intravitreous injection: a comprehensive review. Retina. 2004; 24:676-698.
33. O'Byrne SM, Kako Y, Deckelbaum RJ, et al. Multiple pathways ensure retinoid delivery to milk: studies in genetically modified mice. Am J Physiol Endocrinol Metab. 2010;298: E862-E870.
34. Wongsiriroj N, Piantedosi R, Palczewski K, et al. The molecular basis of retinoid absorption: a genetic dissection. J Biol Chem. 2008;283:13510-13519.
35. Kim YK, Wassef L, Hamberger L, et al. Retinyl ester formation by lecithin: retinol acyltransferase is a key regulator of retinoid homeostasis in mouse embryogenesis. J Biol Chem. 2008;283: 5611-5621.
36. O'Byrne SM, Wongsiriroj N, Libien J, et al. Retinoid absorption and storage is impaired in mice lacking lecithin: retinol acyltransferase (LRAT). J Biol Chem. 2005;280:35647-35657.
37. Palczewska G, Maeda T, Imanishi Y, et al. Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes. Nat Med. 2010; 16:1444-1449.
38. Mata E, Igartua M, Patarroyo ME, Pedraz JL, Hernandez RM. Enhancing immunogenicity to PLGA microparticulate systems by incorporation of alginate and RGD-modified alginate. Eur J Pharm Sci. 2011;44:32-40.
39. Woodrow KA, Cu Y, Booth CJ, Saucier-Sawyer JK, Wood MJ, Saltzman WM. Intravaginal gene silencing using biodegradable polymer nanoparticles densely loaded with small-interfering RNA. Nature Materials. 2009;8:526-533.
40. Banerjee A, Arha M, Choudhary S, et al. The influence of hydrogel modulus on the proliferation and differentiation of encapsulated neural stem cells. Biomaterials. 2009;30:4695-4699.
41. Lee J, Tan CY, Lee SK, Kim YH, Lee KY. Controlled delivery of heat shock protein using an injectable microsphere/hydrogel combination system for the treatment of myocardial infarction. J Control Release. 2009;137:196-202.
42. Lee J, Bhang SH, Park H, Kim BS, Lee KY. Active blood vessel formation in the ischemic hindlimb mouse model using a microsphere/hydrogel combination system. Pharm Res. 2010; 27:767-774.
43. Lee J, Lee KY. Local and sustained vascular endothelial growth factor delivery for angiogenesis using an injectable system. Pharm Res. 2009;26:1739-1744.
44. Ateh DD, Leinster VH, Lambert SR, et al. The intracellular uptake of CD95 modified paclitaxel-loaded poly(lactic-coglycolic acid) microparticles. Biomaterials. 2011;32:8538-8547.
45. Allison SD. Analysis of initial burst in PLGA microparticles. Expert Opin Drug Deliv. 2008;5:615-628.
46. Krebs MD, Jeon O, Alsberg E. Localized and sustained delivery of silencing RNA from macroscopic biopolymer hydrogels. J Am Chem Soc. 2009;131:9204-9206.
47. Rosca ID, Watari F, Uo M. Microparticle formation and its mechanism in single and double emulsion solvent evaporation. J Control Release. 2004;99:271-280.
48. Shiose S, Chen Y, Okano K, et al. Toll-like receptor 3 is required for development of retinopathy caused by impaired all-trans-retinal clearance in mice. J Biol Chem. 2011;286: 15543-15555.
49. Maeda A, Golczak M, Chen Y, et al. Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat Chem Biol. 2012;8:170-178.
50. Maeda A, Maeda T, Golczak M, et al. Involvement of all-transretinal in acute light-induced retinopathy of mice. J Biol Chem. 2009;284:15173-15183.
51. Maeda A, Maeda T, Golczak M, et al. Effects of potent inhibitors of the retinoid cycle on visual function and photoreceptor protection from light damage in mice. Mol Pharmacol. 2006;70:1220-1229.
52. Maeda A, Maeda T, Golczak M, Palczewski K. Retinopathy in mice induced by disrupted all-trans-retinal clearance. J Biol Chem. 2008;283:26684-26693.
53. Sakami S, Maeda T, Bereta G, et al. Probing mechanisms of photoreceptor degeneration in a new mouse model of the common form of autosomal dominant retinitis pigmentosa due to P23H opsin mutations. J Biol Chem. 2011;286:10551-10567.
54. Golczak M, Imanishi Y, Kuksa V, Maeda T, Kubota R, Palczewski K. Lecithin: retinol acyltransferase is responsible for amidation of retinylamine, a potent inhibitor of the retinoid cycle. J Biol Chem. 2005;280:42263-42273.
55. Imanishi Y, Gerke V, Palczewski K. Retinosomes: new insights into intracellular managing of hydrophobic substances in lipid bodies. J Cell Biol. 2004;166:447-453.
56. Maeda A, Maeda T, Imanishi Y, Golczak M, Moise AR, Palczewski K. Aberrant metabolites in mouse models of congenital blinding diseases: formation and storage of retinyl esters. Biochemistry. 2006;45:4210-4219.
57. Orban T, Palczewska G, Palczewski K. Retinyl ester storage particles (retinosomes) from the retinal pigmented epithelium resemble lipid droplets in other tissues. J Biol Chem. 2011; 286:17248-17258.
58. Redmond TM, Yu S, Lee E, et al. Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat Genet. 1998;20:344-351.
59. Choonara YE, Pillay V, Danckwerts MP, Carmichael TR, du Toit LC. A review of implantable intravitreal drug delivery technologies for the treatment of posterior segment eye diseases. J Pharm Sci. 2010;99:2219-2239.
60. Baranano DE, Kim SJ, Edelhauser HF, Durairaj C, Kompella UB, Handa JT. Efficacy and pharmacokinetics of intravitreal nonsteroidal anti-inflammatory drugs for intraocular inflammation. Br J Ophthalmol. 2009;93:1387-1390.
61. Guidetti B, Azema J, Malet-Martino M, Martino R. Delivery systems for the treatment of proliferative vitreoretinopathy: materials, devices and colloidal carriers. Curr Drug Deliv. 2008;5:7-19.
62. Tang PH, Fan J, Goletz PW, Wheless L, Crouch RK. Effective and sustained delivery of hydrophobic retinoids to photoreceptors. Invest Ophthalmol Vis Sci. 2010;51:5958-5964.
63. Acland GM, Aguirre GD, Bennett J, et al. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol Ther. 2005;12:1072-1082.
64. Acland GM, Aguirre GD, Ray J, et al. Gene therapy restores vision in a canine model of childhood blindness. Nat Genet. 2001;28:92-95.
65. Bainbridge JW, Smith AJ, Barker SS, et al. Effect of gene therapy on visual function in Leber's congenital amaurosis. N Engl J Med. 2008;358:2231-2239.
66. 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.
67. 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.
68. Takezaki M, Kito Y. Circular dichroism of rhodopsin and isorhodopsin. Nature. 1967;215:1197-1199.
69. Wilson CG. Topical drug delivery in the eye. Exp Eye Res. 2004;78:737-743.
70. Amrite AC, Kompella UB. Size-dependent disposition of nanoparticles and microparticles following subconjunctival administration. J Pharm Pharmacol. 2005;57:1555-1563.
71. Gearhart PM, Gearhart C, Thompson DA, Petersen-Jones SM. Improvement of visual performance with intravitreal administration of 9-cis-retinal in Rpe65-mutant dogs. Arch Ophthalmol. 2010;128:1442-1448.
72. Myles ME, Neumann DM, Hill JM. Recent progress in ocular drug delivery for posterior segment disease: emphasis on transscleral iontophoresis. Adv Drug Deliv Rev. 2005;57: 2063-2079.
73. Yasukawa T, Ogura Y, Tabata Y, Kimura H, Wiedemann P, Honda Y. Drug delivery systems for vitreoretinal diseases. Prog Retin Eye Res. 2004;23:253-281.
74. Maeda A, Maeda T, Palczewski K. Improvement in rod and cone function in mouse model of Fundus albipunctatus after pharmacologic treatment with 9-cis-retinal. Invest Ophthalmol Vis Sci. 2006;47:4540-4546.