Identification of a therapeutic dose of continuously delivered erythropoietin in the eye using an inducible promoter system

Current Gene Therapy

Volumn 13, Issue 4, 2013, Pages 275-281

  Hines Beard, Jessica ^a   Desai, Siddharth ^b   Haag, Rachel ^b   Esumi, Noriko ^c   D'Surney, Lauren ^b   Parker, Scott ^b   Richardson, Cody ^b   Rex, Tonia S ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Dose; Erythropoietin; Gene therapy; Inducible promoter; Intraocular; Recombinant adeno associated virus; Retinal degeneration

Indexed keywords

DOXYCYCLINE; ERYTHROPOIETIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG DOSE INCREASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HEMATOCRIT; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROPROTECTION; NONHUMAN; POLYMERASE CHAIN REACTION; RETINA DEGENERATION; RETINA INJURY; RETINAL NERVE FIBER LAYER THICKNESS; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY;

ANIMALS; DRUG DELIVERY SYSTEMS; ERYTHROPOIETIN; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS; MICE; PROMOTER REGIONS, GENETIC; RETINA; RETINAL DEGENERATION;

EID: 84888126198     PISSN: 15665232     EISSN: 18755631     Source Type: Journal    
DOI: 10.2174/15665232113139990024     Document Type: Article

References (43)

1. Bennicelli J, Wright JF, Komaromy A, et al. Reversal of blindness in animal models of leber congenital amaurosis using optimized AAV2-mediated gene transfer. Mol Ther 2008; 16: 458-65.
2. 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: 2231-9.
3. Jacobson 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.
4. RetNet. (1996-2012). http://www.sph.uth.tmc.edu/retnet/.
5. Grimm C, Wenzel A, Groszer M, et al. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med 2002; 8: 718-24.
6. Grimm C, Wenzel A, Stanescu D, et al. Constitutive overexpression of human erythropoietin protects the mouse retina against induced but not inherited retinal degeneration. J Neurosci 2004; 24: 5651-8.
7. Rex TS, Allocca M, Domenici L, et al. Systemic but not intraocular EPO gene transfer protects the retina from light-and geneticinduced degeneration. Mol Ther 2004; 10: 855-61.
8. Rex TS, Wong Y, Kodali K, Merry S. Neuroprotection of photoreceptors by direct delivery of erythropoietin to the retina of the retinal degeneration slow mouse. Exp Eye Res 2009; 89: 735-40.
9. Sullivan T, Rex TS. Systemic gene delivery protects the photoreceptors in the retinal degeneration slow mouse. Neurochem Res 2011; 36: 613-8.
10. Sullivan TA, Geisert EE, Hines-Beard J, Rex TS. Systemic AAV-mediated gene therapy preserves retinal ganglion cells and visual function in DBA/2J glaucomatous mice. J Hum Gene Ther 2011; 22: 1191-200.
11. Sullivan T, Rex TS. Dose-dependent treatment of optic nerve crush by exogenous systemic mutant erythropoietin. Exp Eye Res 2012; 96: 36-41.
12. Weishaupt JH, Rohde G, Polking E, Siren AL, Ehrenreich H, Bahr M. Effect of erythropoietin axotomy-induced apoptosis in rat retinal ganglion cells. Invest Ophthalmol Vis Sci 2004; 45: 1514-22.
13. King CE, Rodger J, Bartlett C, Esmaili T, Dunlop SA, Beazley LD. Erythropoietin is both neuroprotective and neuroregenerative following optic nerve transection. Exp Neurol 2007; 205: 48-55.
14. Junk AK, Mammis A, Savitz SI, et al. Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc Natl Acad Sci USA 2002; 99: 10659-64.
15. Juul SE, McPherson RJ, Farrell FX, Jolliffe L, Ness DJ, Gleason CA. Erythropoeitin concentrations in cerebrospinal fluid on nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol Neonate 2004; 85; 138-44.
16. Xenocostas A, Cheung W, Farrell F, et al. The pharmacokinetics of erythropoietin in the cerebrospinal fluid after intravenous administration of recombinant human erythropoietin. Eur J Pharmacol 2005; 61: 189-95.
17. Brines ML, Ghezzi P, Keenan S, et al. Erythropoietin crosses the blood-brain barrier to protect against experimental brain injury. Proc Natl Acad Sci USA 2000; 97: 10526-31.
18. Leist M, Ghezzi P, Grasso G, et al. Derivatives of erythropoietin that are tissue protective but not erythropoietic. Science 2004; 305: 239-42.
19. Brines M, Grasso G, Fiordaliso F, et al. Erythropoietin mediates tissue protection through an erythropoietin and common betasubunit heteroreceptor. Proc Natl Acad Sci USA 2004; 101:14907-14912.
20. Jubinsky PT, Krijanovski OI, Nathan, DG, Tavernier J, Sieff CA. The beta chain of the interleukin-3 receptor functionally associates with the erythropoietin receptor. Blood 1997; 90: 1867-73.
21. Stellacci E, Di Noia A, Di Baldassarre A, Migliaccio G, Battistini A, Migliaccio AR. Interaction between the glucocorticoid and erythropoietin receptors in human erythroid cells. Exp Hematol 2009; 37: 559-72.
22. Diederich K, Schäbitz W-R, Minnerup J. Seeing old friends from a different angle: Novel properties of hematopoietic growth factors in the healthy and diseased brain. Hippocampus 2012; 22: 1051-7.
23. Gao G, Lebherz C, Weiner DJ, Grant R, Calcedo R, McCullough B, Bagg A, Zhang Y, Wilson JM. Erythropoietin gene therapy leads to autoimmune anemia in macaques. Blood 2004; 103: 3300-2.
24. Tang Y, Cummins J, Huard J, Wang B. AAV-directed muscular dystrophy gene therapy. Exp Opin Biol Ther 2010; 10: 395-408.
25. Stein L, Roy K, Lei L, Kaushal S. Clinical gene therapy for the treatment of RPE65-associated Leber congenital amaurosis. Exp Opin Biol Ther 2011; 11: 429-39.
26. Stieger K, Chauveau C, Rolling F. Preclinical studies on specific gene therapy for recessive retinal degenerative diseases. Curr Gene Ther 2010; 10: 389-403.
27. Dejneka NS, Auricchio A, Maguire AM, et al. Pharmacologically regulated gene expression in the retina following transduction with viral vectors. Gene Ther 2001; 8: 442-6.
28. Stieger K, Le Meur G, Lasne F, et al. Long-term doxycyclineregulated transgene expression in the retina of nonhuman primates following subretinal injection of recombinant AAV vectors. Mol Ther 2006; 13: 967-75.
29. Markusic DM, de Waart DR, Seppen J. Separating lentiviral vector injection and induction of gene expression in time, does not prevent an immune response to rtTA in rats. PLoS One 2010; 5: e9974.
30. Oshima Y, Oshima S, Nambu H, et al. Increased expression of VEGF in retinal pigmented epithelial cells is not sufficient to cause choroidal neovascularization. J Cell Physiol 2004; 201: 393-400.
31. Chang MA, Horner JW, Conklin BR, DePinho RA, Zack DJ. Tetracycline-inducible system for photoreceptor-specific gene expression. Invest Ophthalmol Vis Sci 2000; 41: 4281-7.
32. van Nie R, Iványi D, Démant P. A new H-2-linked mutation, rds, causing retinal degeneration in the mouse. Tissue Antigens 1978; 12: 106-8.
33. Sanyal S, De Ruiter A, Hawkins RK. Development and degeneration of retina in rds mutant mice: light microscopy. J Comp Neurol 1980; 94: 193-207.
34. Hildinger M, Auricchio A, Gao G, Wang L, Chirmule N, Wilson J. Hybrid vectors based on adeno-associated virus serotypes 2 and 5 for muscle-directed gene transfer. J Virol 2001; 75: 6199-203.
35. Remtulla S, Hallett PE. A schematic eye for the mouse, and comparisons with the rat. Vis Res 1985; 25: 21-31.
36. Rex TS, Peet JA, Surace EM, et al. The distribution, concentration, and toxicity of enhanced green fluorescent protein in retinal cells after genomic or somatic (virus-mediated) gene transfer. Mol Vis 2005; 11: 1236-45.
37. Andersson H, Alestig K. The penetration of doxycycline into CSF. Scand J Infect Dis Suppl 1976; 9: 17-9.
38. McGill TJ, Prusky GT, Douglas RM, et al. Intraocular CNTF reduces vision in normal rats in a dose-dependent manner. Invest Ophthalmol Vis Sci 2007; 48: 5756-66.
39. Wang T, Hu Y, Leach MK, et al. Erythropoietin-loaded oligochitosan nanoparticles for treatment of periventricular leukomalacia. Int J Pharm 2012; 422: 462-71.
40. Zhou X-L, He J-T, Du H-J, et al. Pharmacokinetic and pharmacodynamics profiles of recombinant human erythropoietin-loaded poly(lactic-co-glycolic acid) microspheres in rats. Acta Pharmacol Sin 2012; 33: 137-44.
41. Rong X, Yang S, Miao H, et al. Effects of erythropoietin-dextran microparticle-based PLGA/PLA microspheres on RGCs. Invest Ophthalmol Vis Sci 2012; 53: 6025-34.
42. Ranchon Cole I, Bonhomme B, Doly M. Pre-treatment of adult rats with high doses of erythropoietin induces caspase-9 but prevents light-induced retinal injury. Exp Eye Res 2007; 85: 782-9.
43. Tanito M, Li F, Anderson RE. Intravitreal injection of erythropoietin glycosylation analogs does not protect rod photoreceptor cells from light-induced damage. Adv Exp Med Biol 2012; 723: 137-43.