Subretinal delivery of erythropoietin alleviates the N-methyl-N-nitrosourea-induced photoreceptor degeneration and visual functional impairments: an in vivo and ex vivo study

References

• Applebury ML, Antoch MP, Baxter LC, et al. (2000). The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinalspatial patterning. Neuron 27:513–23.
   PubMed Web of Science ®Google Scholar
• Boudard DL, Tanimoto N, Huber G, et al. (2010). Cone loss is delayed relative to rod loss during induced retinal degeneration in the diurnal cone-rich rodent Arvicanthis ansorgei. Neuroscience 169:1815–30.
   PubMed Web of Science ®Google Scholar
• Caprara C, Grimm C. (2012). From oxygen to erythropoietin: relevance of hypoxia for retinal development, health and disease. Prog Retin Eye Res 31:89–119.
   PubMed Web of Science ®Google Scholar
• Ehrenreich H, Weissenborn K, Prange H, EPO Stroke Trial Group, et al. (2009). Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 40:e647–56.
   PubMed Web of Science ®Google Scholar
• Eversole-Cire P, Concepcion FA, Simon MI, et al. (2000). Synergistic effect of Bcl-2 and BAG-1 on the prevention of photoreceptor cell death. Invest Ophthalmol Vis Sci 41:1953–61.
   PubMed Web of Science ®Google Scholar
• Fernández-Sánchez L, Lax P, Noailles A, et al. (2015). Natural compounds from saffron and bear bile prevent vision loss and retinal degeneration. Molecules 20:13875–93.
   PubMed Web of Science ®Google Scholar
• Gao Y, Deng XG, Sun QN, Zhong ZQ. (2010). Ganoderma spore lipid inhibits N-methyl-N-nitrosourea-induced retinal photoreceptor apoptosis in vivo. Exp Eye Res 90:397–404.
   PubMed Web of Science ®Google Scholar
• Gawad AE, Schlichting L, Strauss O, Zeitz O. (2009). Antiapoptotic properties of erythropoietin: novel strategies for protection of retinal pigmentepithelial cells. Eye (Lond) 23:2245–50.
   PubMed Web of Science ®Google Scholar
• Geneva II. (2016). Photobiomodulation for the treatment of retinal diseases: a review. Int J Ophthalmol 9:145–52.
   PubMed Web of Science ®Google Scholar
• Hanus J, Zhang H, Chen DH, et al. (2015). Gossypol acetic acid prevents oxidative stress-induced retinal pigment epithelial necrosisby regulating the FoxO3/sestrin2 pathway. Mol Cell Biol 35:1952–63.
   PubMed Web of Science ®Google Scholar
• Juul SE, Mayock DE, Comstock BA, Heagerty PJ. (2015). Neuroprotective potential of erythropoietin in neonates; design of a randomized trial. Matern Health Neonatol Perinatol 1:27.
   PubMedGoogle Scholar
• Kruk J, Kubasik-Kladna K, Aboul-Enein HY. (2015). The role oxidative stress in the pathogenesis of eye diseases: current status and a dual role of physical activity. MRMC 16:241–57.
   Web of Science ®Google Scholar
• Kuro M, Yoshizawa K, Uehara N, et al. (2011). Calpain inhibition restores basal autophagy and suppresses MNU-induced photoreceptor celldeath in mice. In Vivo 25:617–23.
   PubMed Web of Science ®Google Scholar
• Levy MA, Claxton DF. (2017). Therapeutic inhibition of BCL-2 and related family members. Expert Opin Investig Drugs 26:293–301.
   PubMed Web of Science ®Google Scholar
• Li W, Sinclair SH, Xu GT. (2010). Effects of intravitreal erythropoietin therapy for patients with chronic and progressive diabeticmacular edema. Ophthalmic Surg Lasers Imaging 41:18–25.
   PubMedGoogle Scholar
• Luo W, Hu L, Wang F. (2015). The protective effect of erythropoietin on the retina. Ophthalmic Res 53:74–81.
   PubMed Web of Science ®Google Scholar
• Maiese K, Li F, Chong ZZ. (2004). Erythropoietin in the brain: can the promise to protect be fulfilled? Trends Pharmacol Sci 25:577–83.
   PubMed Web of Science ®Google Scholar
• Maurer E, Tschopp M, Tappeiner C, Sallin P, Jazwinska A, Enzmann V. (2014). Methylnitrosourea (MNU)-induced retinal degeneration and regeneration in the zebrafish: histological and functional characteristics. J Vis Exp 20:e51909.
   Google Scholar
• Moskowitz A, Hansen RM, Fulton AB. (2016). Retinal, visual, and refractive development in retinopathy of prematurity. Eye Brain 8:103–11.
   PubMed Web of Science ®Google Scholar
• Mowat FM, Occelli LM, Bartoe JT, et al. (2017). Gene therapy in a large animal model of PDE6A-retinitis pigmentosa. Front Neurosci 11:342.
   PubMed Web of Science ®Google Scholar
• Myatt SS, Lam EW. (2007). The emerging roles of forkhead box (Fox) proteins in cancer. Nat Rev Cancer 7:847–59.
   PubMed Web of Science ®Google Scholar
• Nir I, Kedzierski W, Chen J, Travis GH. (2000). Expression of Bcl-2 protects against photoreceptor degeneration in retinal degeneration slow (rds) mice. J Neurosci 20:2150–4.
   PubMed Web of Science ®Google Scholar
• Nour M, Quiambao AB, Peterson WM, et al. (2003). P2Y(2) receptor agonist INS37217 enhances functional recovery after detachment caused by subretinal injection in normal and rds mice. Invest Ophthalmol Vis Sci 44:4505–14.
   PubMed Web of Science ®Google Scholar
• Nowak JZ. (2013). Oxidative stress, polyunsaturated fatty acids-derived oxidation products and bisretinoids as potential inducers of CNS diseases: focus on age-related macular degeneration. Pharmacol Rep 65:288–304.
   PubMed Web of Science ®Google Scholar
• Pang JJ, Dai X, Boye SE, et al. (2011). Long-term retinal function and structure rescue using capsid mutant AAV8 vector in the rd10 mouse, a model of recessive retinitis pigmentosa. Mol Ther 19:234–42.
   PubMed Web of Science ®Google Scholar
• Paquet-Durand F, Azadi S, Hauck SM, et al. (2006). Calpain is activated in degenerating photoreceptors in the rd1 mouse. J Neurochem 96:802–14.
   PubMed Web of Science ®Google Scholar
• Paquet-Durand F, Johnson L, Ekstrom P. (2007). Calpain activity in retinal degeneration. J Neurosci Res 85:693–702.
   PubMed Web of Science ®Google Scholar
• Pasantes-Morales H, Quiroz H, Quesada O. (2002). Treatment with taurine, diltiazem, and vitamin E retards the progressive visual field reduction in retinitis pigmentosa: a 3-year follow-up study . Metab Brain Dis 17:183–97.
   PubMed Web of Science ®Google Scholar
• Petit L, Ma S, Cheng SY, et al. (2017). Rod outer segment development influences AAV-mediated photoreceptor transduction after subretinal injection. Hum Gene Ther 28:464–81.
   PubMed Web of Science ®Google Scholar
• Ponugoti B, Dong G, Graves DT. (2012). Role of forkhead transcription factors in diabetes-induced oxidative stress. Exp Diabetes Res 2012:939751.
   PubMedGoogle Scholar
• Punzo C, Kornacker K, Cepko CL. (2009). Stimulation of the insulin/mTOR pathway delays cone death in a mouse model of retinitis pigmentosa. Nat Neurosci 12:44–52.
   PubMed Web of Science ®Google Scholar
• Qi Y, Dai X, Zhang H, et al. (2015). Trans-corneal subretinal injection in mice and its effect on the function and morphology of the retina. PLoS One 28:e0136523.
   Google Scholar
• Reisenhofer M, Pannicke T, Reichenbach A, Enzmann V. (2016). Characteristics of Müller glial cells in MNU-induced retinal degeneration. Vis Neurosci 33:E013.
   PubMed Web of Science ®Google Scholar
• Rivas MA, Vecino E. (2009). Animal models and different therapies for treatment of retinitis pigmentosa. Histol Histopathol 24:1295–322.
   PubMed Web of Science ®Google Scholar
• Rösch S, Werner C, Müller F, Walter P. (2017). Photoreceptor degeneration by intravitreal injection of N-methyl-N-nitrosourea (MNU) in rabbits: a pilot study. Graefes Arch Clin Exp Ophthalmol 255:317–31.
   PubMed Web of Science ®Google Scholar
• Shen J, Wu Y, Xu JY, et al. (2010). ERK- and Akt-dependent neuroprotection by erythropoietin (EPO) against glyoxal-AGEs via modulation of Bcl-xL, Bax, and BAD. Invest Ophthalmol Vis Sci 51:35–46.
   PubMed Web of Science ®Google Scholar
• Shen W, Chung SH, Irhimeh MR, et al. (2014). Systemic administration of erythropoietin inhibits retinopathy in RCS rats. PLoS One 13:e104759.
   Web of Science ®Google Scholar
• Shin HR, Kim H, Kim KI, Baek SH. (2016). Epigenetic and transcriptional regulation of autophagy. Autophagy 12:2248–9.
   PubMed Web of Science ®Google Scholar
• Shintani K, Shechtman DL, Gurwood AS. (2009). Review and update: current treatment trends for patients with retinitis pigmentosa. Optometry 80:384–401.
   PubMedGoogle Scholar
• Szel A, Rulich P, Caffe AR, Veen van T. (1996). Distribution of cone photoreceptors in the mammalian retina. Microsc Res Tech 35:445–62.
   PubMed Web of Science ®Google Scholar
• Szél A, Röhlich P, Caffé AR, et al. (1992). Unique topographic separation of two spectral classes of cones in the mouse retina. J Comp Neurol 325:327–42.
   PubMed Web of Science ®Google Scholar
• Tao Y, Chen T, Liu B, et al. (2016). The transcorneal electrical stimulation as a novel therapeutic strategy against retinal and optic neuropathy: a review of experimental and clinical trials. Int J Ophthalmol 9:914–9.
   PubMed Web of Science ®Google Scholar
• Tao Y, Chen T, Liu B, et al. (2015). The neurotoxic effects of N-methyl-N-nitrosourea on the electrophysiological property and visual signal transmission of rat's retina. Toxicol Appl Pharmacol 1:44–52.
   Web of Science ®Google Scholar
• Tappeiner C, Balmer J, Iglicki M, et al. (2013). Characteristics of rod regeneration in a novel zebrafish retinal degeneration model using N-methyl-N-nitrosourea (MNU). PLoS One 8:e71064.
   PubMed Web of Science ®Google Scholar
• Timmers AM, Zhang H, Squitieri A, Gonzalez-Pola C. (2001). Subretinal injections in rodent eyes: effects on electrophysiology and histology of rat retina. Mol Vis 7:131–7.
   PubMed Web of Science ®Google Scholar
• Tsubura A, Yoshizawa K, Kuwata M, Uehara N. (2010). Animal models for retinitis pigmentosa induced by MNU; disease progression,mechanisms and therapeutic trials. Histol Histopathol 25:933–44.
   PubMed Web of Science ®Google Scholar
• Umino Y, Solessio E, Barlow RB. (2008). Speed, spatial, and temporal tuning of rod and cone vision in mouse. J Neurosci 28:189–98.
   PubMed Web of Science ®Google Scholar
• Yu DY, Cringle SJ. (2005). Retinal degeneration and local oxygen metabolism. Exp Eye Res 80:745–51.
   PubMed Web of Science ®Google Scholar
• Zhang JF, Wu YL, Xu JY, et al. (2008). Pharmacokinetic and toxicity study of intravitreal erythropoietin in rabbits. Acta Pharmacol Sin 29:1383–90.
   PubMed Web of Science ®Google Scholar
• Zhong Y, Li J, Wang JJ, et al. (2012). X-Box binding protein 1 is essential for the anti-oxidant defense and cell survival in the retinal pigment Epithelium. PLoS One 7:e38616.
   PubMed Web of Science ®Google Scholar
• Zhou Z, Doggett TA, Sene A, et al. (2015). Autophagy supports survival and phototransduction protein levels in rod photoreceptors. Cell Death Differ 22:488–98.
   PubMed Web of Science ®Google Scholar