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Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Review Article

Stem Cell-based Treatment Strategies for Degenerative Diseases of the Retina

Author(s): Deepthi S. Rajendran Nair and Biju B. Thomas*

Volume 17, Issue 3, 2022

Published on: 07 January, 2022

Page: [214 - 225] Pages: 12

DOI: 10.2174/1574888X16666210804112104

Price: $65

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Abstract

Background: The main cause of progressive vision impairment in retinal degenerative diseases is the dysfunction of photoreceptors and the underlying retinal pigment epithelial cells. The inadequate regenerative capacity of the neural retina and lack of established therapeutic options demand the development of clinical-grade protocols to halt the degenerative process in the eye or replace the damaged cells by using stem cell-derived products. Recently, stem cell-based regenerative therapies have been at the forefront of clinical investigations for retinal dystrophies.

Objective: This article will review different stem cell-based therapies currently employed for retinal degenerative diseases, recent clinical trials, and major challenges in the translation of these therapies from bench to bedside.

Methodology: A systematic literature review was conducted to identify potentially relevant articles published in MEDLINE/PubMed, Embase, ClinicalTrials.gov, Drugs@FDA, European Medicines Agency, and World Health Organization International Clinical Trials Registry Platform.

Results: Transplantation of healthy cells to replace damaged cells in the outer retina is a clinically relevant concept because the inner retina that communicates with the visual areas of the brain remains functional even after the photoreceptors are completely lost. Various methods have been established for the differentiation of pluripotent stem cells into different retinal cell types that can be used for therapies. Factors released from transplanted somatic stem cells showed trophic support and photoreceptor rescue during the early stages of the disease. Several preclinical and phase I/II clinical studies using terminally differentiated photoreceptor/retinal pigment epithelial cells derived from pluripotent stem cells have shown proof of concept for visual restoration in Age-related Macular Degeneration (AMD), Stargardt disease, and Retinitis Pigmentosa (RP).

Conclusion: Cell replacement therapy has great potential for vision restoration. The results obtained from the initial clinical trials are encouraging and indicate its therapeutic benefits. The current status of the therapies suggests that there is a long way to go before these results can be applied to routine clinical practice. Input from the ongoing multicentre clinical trials will give a more refined idea for the future design of clinical-grade protocols to transplant GMP level HLA matched cells.

Keywords: Retinal degenerative disease, retinitis pigmentosa (RP), age-related macular degeneration (AMD), stem cell therapy, retinal progenitor cells, ESC-RPE, iPSC-RPE.

[1]
Congdon N, O’Colmain B, Klaver CCW, et al. Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol 2004; 122(4): 477-85.
[http://dx.doi.org/10.1001/archopht.122.4.477] [PMID: 15078664]
[2]
Ferrari S, Di Iorio E, Barbaro V, Ponzin D, Sorrentino FS, Parmeggiani F. Retinitis pigmentosa: Genes and disease mechanisms. Curr Genomics 2011; 12(4): 238-49.
[http://dx.doi.org/10.2174/138920211795860107] [PMID: 22131869]
[3]
Khanna S, Komati R, Eichenbaum DA, Hariprasad I, Ciulla TA, Hariprasad SM. Current and upcoming anti-VEGF therapies and dosing strategies for the treatment of neovascular AMD: A comparative review. BMJ Open Ophthalmol 2019; 4(1): e000398.
[http://dx.doi.org/10.1136/bmjophth-2019-000398] [PMID: 31909196]
[4]
Zhang K, Hopkins JJ, Heier JS, et al. Ciliary neurotrophic factor delivered by encapsulated cell intraocular implants for treatment of geographic atrophy in age-related macular degeneration. Proc Natl Acad Sci USA 2011; 108(15): 6241-5.
[http://dx.doi.org/10.1073/pnas.1018987108] [PMID: 21444807]
[5]
Wu J, Sun X. Complement system and age-related macular degeneration: Drugs and challenges. Drug Des Devel Ther 2019; 13: 2413-25.
[http://dx.doi.org/10.2147/DDDT.S206355] [PMID: 31409975]
[6]
Rashid K, Wolf A, Langmann T. Microglia activation and immunomodulatory therapies for retinal degenerations. Front Cell Neurosci 2018; 12: 176.
[http://dx.doi.org/10.3389/fncel.2018.00176] [PMID: 29977192]
[7]
Schoenberger SD, Kim SJ. Nonsteroidal anti-inflammatory drugs for retinal disease. Int J Inflamm 2013; 2013: 281981.
[http://dx.doi.org/10.1155/2013/281981] [PMID: 23365785]
[8]
Jack LS, Sadiq MA, Do DV, Nguyen QD. Emixustat and lampalizumab: Potential therapeutic options for geographic atrophy. Dev Ophthalmol 2016; 55: 302-9.
[http://dx.doi.org/10.1159/000438954] [PMID: 26501510]
[9]
Lin T-C, Seiler MJ, Zhu D, et al. Assessment of safety and functional efficacy of stem cell-based therapeutic approaches using retinal degenerative animal models. Stem Cells Int 2017; 2017: e9428176.
[10]
Sharma R, Khristov V, Rising A, et al. Clinical-grade stem cell-derived retinal pigment epithelium patch rescues retinal degeneration in rodents and pigs. Sci Transl Med 2019; 11(475): eaat5580.
[http://dx.doi.org/10.1126/scitranslmed.aat5580] [PMID: 30651323]
[11]
Wang S, Lu B, Girman S, et al. Non-invasive stem cell therapy in a rat model for retinal degeneration and vascular pathology. PLoS One 2010; 5(2): e9200.
[http://dx.doi.org/10.1371/journal.pone.0009200]
[12]
Algvere PV, Gouras P, Dafgård Kopp E. Long-term outcome of RPE allografts in non-immunosuppressed patients with AMD. Eur J Ophthalmol 1999; 9(3): 217-30.
[http://dx.doi.org/10.1177/112067219900900310] [PMID: 10544978]
[13]
Algvere PV, Berglin L, Gouras P, Sheng Y, Kopp ED. Transplantation of RPE in age-related macular degeneration: observations in disciform lesions and dry RPE atrophy. Graefes Arch Clin Exp Ophthalmol 1997; 235(3): 149-58.
[http://dx.doi.org/10.1007/BF00941722] [PMID: 9085110]
[14]
Kaplan HJ, Tezel TH, Berger AS, Wolf ML, Del Priore LV. Human photoreceptor transplantation in retinitis pigmentosa. A safety study. Arch Ophthalmol 1997; 115(9): 1168-72.
[http://dx.doi.org/10.1001/archopht.1997.01100160338012] [PMID: 9298059]
[15]
Mahabadi N, Al Khalili Y. Neuroanatomy, retina. Treasure Island, FL: StatPearls Publishing 2020. In: Available from: http://www.ncbi.nlm.nih.gov/books/NBK545310/ (Accessed on: 5 January 2021).
[16]
Steinberg RH. Interactions between the retinal pigment epithelium and the neural retina. Doc Ophthalmol 1985; 60(4): 327-46.
[http://dx.doi.org/10.1007/BF00158922] [PMID: 3905312]
[17]
Wong WL, Su X, Li X, et al. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: A systematic review and meta-analysis. Lancet Glob Health 2014; 2(2): e106-16.
[http://dx.doi.org/10.1016/S2214-109X(13)70145-1] [PMID: 25104651]
[18]
Zając-Pytrus HM, Pilecka A, Turno-Kręcicka A, Adamiec-Mroczek J, Misiuk-Hojło M. The dry form of age-related macular degeneration (AMD): The current concepts of pathogenesis and prospects for treatment. Adv Clin Exp Med 2015; 24(6): 1099-104.
[http://dx.doi.org/10.17219/acem/27093] [PMID: 26771984]
[19]
Danis RP, Lavine JA, Domalpally A. Geographic atrophy in patients with advanced dry age-related macular degeneration: Current challenges and future prospects. Clin Ophthalmol 2015; 9: 2159-74.
[http://dx.doi.org/10.2147/OPTH.S92359] [PMID: 26640366]
[20]
Nowak JZ. Age-related macular degeneration (AMD): Pathogenesis and therapy. Pharmacol Rep 2006; 58(3): 353-63.
[PMID: 16845209]
[21]
Hartong DT, Berson EL, Dryja TP. Retinitis pigmentosa. Lancet 2006; 368(9549): 1795-809.
[http://dx.doi.org/10.1016/S0140-6736(06)69740-7] [PMID: 17113430]
[22]
Duker JS. Stargardt disease.Atlas of retinal OCT: Optical coherence tomography. Netherlands: Elsevier 2018; pp. 149-51.
[http://dx.doi.org/10.1016/B978-0-323-46121-4.00068-6]
[23]
Inoue Y, Iriyama A, Ueno S, et al. Subretinal transplantation of bone marrow mesenchymal stem cells delays retinal degeneration in the RCS rat model of retinal degeneration. Exp Eye Res 2007; 85(2): 234-41.
[http://dx.doi.org/10.1016/j.exer.2007.04.007] [PMID: 17570362]
[24]
Lu B, Wang S, Girman S, McGill T, Ragaglia V, Lund R. Human adult bone marrow-derived somatic cells rescue vision in a rodent model of retinal degeneration. Exp Eye Res 2010; 91(3): 449-55.
[http://dx.doi.org/10.1016/j.exer.2010.06.024] [PMID: 20603115]
[25]
Zhang Y, Wang W. Effects of bone marrow mesenchymal stem cell transplantation on light-damaged retina. Invest Ophthalmol Vis Sci 2010; 51(7): 3742-8.
[http://dx.doi.org/10.1167/iovs.08-3314] [PMID: 20207980]
[26]
Özmert E, Arslan U. Management of retinitis pigmentosa by Wharton’s jelly derived mesenchymal stem cells: Preliminary clinical results. Stem Cell Res Ther 2020; 11(1): 25.
[http://dx.doi.org/10.1186/s13287-020-1549-6] [PMID: 31931872]
[27]
Barzelay A, Weisthal Algor S, Niztan A, et al. Adipose-derived mesenchymal stem cells migrate and rescue RPE in the setting of oxidative stress. Stem Cells Int 2018; 2018: e9682856.
[28]
Hu C, La H, Wei X, et al. Transplantation site affects the outcomes of adipose-derived stem cell-based therapy for retinal degeneration. Stem Cells Int 2020; 2020: 9625798.
[29]
Oner A, Gonen ZB, Sinim N, Cetin M, Ozkul Y. Subretinal adipose tissue-derived mesenchymal stem cell implantation in advanced stage retinitis pigmentosa: A phase I clinical safety study. Stem Cell Res Ther 2016; 7(1): 178.
[http://dx.doi.org/10.1186/s13287-016-0432-y] [PMID: 27906070]
[30]
Jones MK, Lu B, Saghizadeh M, Wang S. Gene expression changes in the retina following subretinal injection of human neural progenitor cells into a rodent model for retinal degeneration. Mol Vis 2016; 22: 472-90.
[PMID: 27217715]
[31]
Fan X-L, Zhang Y, Li X, Fu Q-L. Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy. Cell Mol Life Sci 2020; 77(14): 2771-94.
[http://dx.doi.org/10.1007/s00018-020-03454-6] [PMID: 31965214]
[32]
Lin L, Du L. The role of secreted factors in stem cells-mediated immune regulation. Cell Immunol 2018; 326: 24-32.
[http://dx.doi.org/10.1016/j.cellimm.2017.07.010] [PMID: 28778535]
[33]
Weiss ARR, Dahlke MH. Immunomodulation by mesenchymal stem cells (MSCs): Mechanisms of action of living, apoptotic, and dead MSCs. Front Immunol 2019; 10: 1191.
[http://dx.doi.org/10.3389/fimmu.2019.01191] [PMID: 31214172]
[34]
Bassi ÊJ, de Almeida DC, Moraes-Vieira PMM, Câmara NOS. Exploring the role of soluble factors associated with immune regulatory properties of mesenchymal stem cells. Stem Cell Rev Rep 2012; 8(2): 329-42.
[http://dx.doi.org/10.1007/s12015-011-9311-1] [PMID: 21881832]
[35]
Soleymaninejadian E, Pramanik K, Samadian E. Immunomodulatory properties of mesenchymal stem cells: cytokines and factors. Am J Reprod Immunol 2012; 67(1): 1-8.
[http://dx.doi.org/10.1111/j.1600-0897.2011.01069.x] [PMID: 21951555]
[36]
Kolomeyer AM, Zarbin MA. Trophic factors in the pathogenesis and therapy for retinal degenerative diseases. Surv Ophthalmol 2014; 59(2): 134-65.
[http://dx.doi.org/10.1016/j.survophthal.2013.09.004] [PMID: 24417953]
[37]
Talcott KE, Ratnam K, Sundquist SM, et al. Longitudinal study of cone photoreceptors during retinal degeneration and in response to ciliary neurotrophic factor treatment. Invest Ophthalmol Vis Sci 2011; 52(5): 2219-26.
[http://dx.doi.org/10.1167/iovs.10-6479] [PMID: 21087953]
[38]
Klassen HJ, Ng TF, Kurimoto Y, et al. Multipotent retinal progenitors express developmental markers, differentiate into retinal neurons, and preserve light-mediated behavior. Invest Ophthalmol Vis Sci 2004; 45(11): 4167-73.
[http://dx.doi.org/10.1167/iovs.04-0511] [PMID: 15505071]
[39]
Qiu G, Seiler MJ, Thomas BB, Wu K, Radosevich M, Sadda SR. Revisiting nestin expression in retinal progenitor cells in vitro and after transplantation in vivo. Exp Eye Res 2007; 84(6): 1047-59.
[http://dx.doi.org/10.1016/j.exer.2007.01.014] [PMID: 17451684]
[40]
MacLaren RE, Pearson RA, MacNeil A, et al. Retinal repair by transplantation of photoreceptor precursors. Nature 2006; 444(7116): 203-7.
[http://dx.doi.org/10.1038/nature05161] [PMID: 17093405]
[41]
Safety of a single, intravitreal injection of human retinal progenitor cells (jCell) in retinitis pigmentosa. ClinicalTrials.gov. Available from: https://clinicaltrials.gov/ct2/show/NCT02320812 (Accessed on: 7 December 2020).
[42]
Safety and efficacy of intravitreal injection of human retinal progenitor cells in adults with retinitis pigmentosa. ClinicalTrials.gov. Available from: https://clinicaltrials.gov/ct2/show/NCT03073733 (Accessed on: 7 December 2020).
[43]
ReNeuron Limited. First-in-human phase I/IIa, open-label, prospective study of the safety and tolerability of subretinally transplanted human retinal progenitor cells (hRPC) in patients with retinitis pigmentosa (RP). 2020. clinicaltrials.gov. Report No.: NCT02464436 Available from: https://clinicaltrials.gov/ct2/show/NCT02464436 (Accessed on: 6 December 2020).
[44]
Kashani AH, Uang J, Mert M, et al. Surgical method for implantation of a biosynthetic retinal pigment epithelium monolayer for geographic atrophy: Experience from a phase 1/2a study. Ophthalmol Retina 2020; 4(3): 264-73.
[http://dx.doi.org/10.1016/j.oret.2019.09.017] [PMID: 31786135]
[45]
Mandai M, Fujii M, Hashiguchi T, et al. iPSC-derived retina transplants improve vision in rd1 end-stage retinal-degeneration mice. Stem Cell Reports 2017; 8(1): 69-83.
[http://dx.doi.org/10.1016/j.stemcr.2016.12.008] [PMID: 28076757]
[46]
Kawasaki H, Suemori H, Mizuseki K, et al. Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. Proc Natl Acad Sci USA 2002; 99(3): 1580-5.
[http://dx.doi.org/10.1073/pnas.032662199] [PMID: 11818560]
[47]
Haruta M, Sasai Y, Kawasaki H, et al. In vitro and in vivo characterization of pigment epithelial cells differentiated from primate embryonic stem cells. Invest Ophthalmol Vis Sci 2004; 45(3): 1020-5.
[http://dx.doi.org/10.1167/iovs.03-1034] [PMID: 14985325]
[48]
Klimanskaya I, Hipp J, Rezai KA, West M, Atala A, Lanza R. Derivation and comparative assessment of retinal pigment epithelium from human embryonic stem cells using transcriptomics. Cloning Stem Cells 2004; 6(3): 217-45.
[http://dx.doi.org/10.1089/clo.2004.6.217] [PMID: 15671670]
[49]
Petrus-Reurer S, Winblad N, Kumar P, et al. Generation of retinal pigment epithelial cells derived from human embryonic stem cells lacking human leukocyte antigen class I and II. Stem Cell Reports 2020; 14(4): 648-62.
[http://dx.doi.org/10.1016/j.stemcr.2020.02.006] [PMID: 32197113]
[50]
Idelson M, Alper R, Obolensky A, et al. Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell Stem Cell 2009; 5(4): 396-408.
[http://dx.doi.org/10.1016/j.stem.2009.07.002] [PMID: 19796620]
[51]
Plaza Reyes A, Petrus-Reurer S, Antonsson L, et al. Xeno-free and defined human embryonic stem cell-derived retinal pigment epithelial cells functionally integrate in a large-eyed preclinical model. Stem Cell Reports 2015; 6(1): 9-17.
[PMID: 26724907]
[52]
Lund RD, Wang S, Klimanskaya I, et al. Human embryonic stem cell-derived cells rescue visual function in dystrophic RCS rats. Cloning Stem Cells 2006; 8(3): 189-99.
[http://dx.doi.org/10.1089/clo.2006.8.189] [PMID: 17009895]
[53]
Vugler A, Carr A-J, Lawrence J, et al. Elucidating the phenomenon of HESC-derived RPE: Anatomy of cell genesis, expansion and retinal transplantation. Exp Neurol 2008; 214(2): 347-61.
[http://dx.doi.org/10.1016/j.expneurol.2008.09.007] [PMID: 18926821]
[54]
Lu B, Malcuit C, Wang S, et al. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 2009; 27(9): 2126-35.
[http://dx.doi.org/10.1002/stem.149] [PMID: 19521979]
[55]
Carr A-JF, Vugler A, Lawrence J, et al. Molecular characterization and functional analysis of phagocytosis by human embryonic stem cell-derived RPE cells using a novel human retinal assay. Mol Vis 2009; 15: 283-95.
[PMID: 19204785]
[56]
Hirami Y, Osakada F, Takahashi K, et al. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neurosci Lett 2009; 458(3): 126-31.
[http://dx.doi.org/10.1016/j.neulet.2009.04.035] [PMID: 19379795]
[57]
Buchholz DE, Hikita ST, Rowland TJ, et al. Derivation of functional retinal pigmented epithelium from induced pluripotent stem cells. Stem Cells 2009; 27(10): 2427-34.
[http://dx.doi.org/10.1002/stem.189] [PMID: 19658190]
[58]
Carr A-J, Vugler AA, Hikita ST, et al. Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat. PLoS One 2009; 4(12): e8152.
[http://dx.doi.org/10.1371/journal.pone.0008152] [PMID: 19997644]
[59]
Krohne TU, Westenskow PD, Kurihara T, et al. Generation of retinal pigment epithelial cells from small molecules and OCT4 reprogrammed human induced pluripotent stem cells. Stem Cells Transl Med 2012; 1(2): 96-109.
[http://dx.doi.org/10.5966/sctm.2011-0057] [PMID: 22532929]
[60]
Suárez-Alvarez B, Rodriguez RM, Calvanese V, et al. Epigenetic mechanisms regulate MHC and antigen processing molecules in human embryonic and induced pluripotent stem cells. PLoS One 2010; 5(4): e10192.
[http://dx.doi.org/10.1371/journal.pone.0010192] [PMID: 20419139]
[61]
Meyer JS, Howden SE, Wallace KA, et al. Optic vesicle-like structures derived from human pluripotent stem cells facilitate a customized approach to retinal disease treatment. Stem Cells 2011; 29(8): 1206-18.
[http://dx.doi.org/10.1002/stem.674] [PMID: 21678528]
[62]
Nakano T, Ando S, Takata N, et al. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 2012; 10(6): 771-85.
[http://dx.doi.org/10.1016/j.stem.2012.05.009] [PMID: 22704518]
[63]
Iraha S, Tu H-Y, Yamasaki S, et al. Establishment of immunodeficient retinal degeneration model mice and functional maturation of human esc-derived retinal sheets after transplantation. Stem Cell Reports 2018; 10(3): 1059-74.
[http://dx.doi.org/10.1016/j.stemcr.2018.01.032] [PMID: 29503091]
[64]
Seiler MJ, Aramant RB, Jones MK, Ferguson DL, Bryda EC, Keirstead HS. A new immunodeficient pigmented retinal degenerate rat strain to study transplantation of human cells without immunosuppression. Graefes Arch Clin Exp Ophthalmol 2014; 252(7): 1079-92.
[http://dx.doi.org/10.1007/s00417-014-2638-y] [PMID: 24817311]
[65]
Shirai H, Mandai M, Matsushita K, et al. Transplantation of human embryonic stem cell-derived retinal tissue in two primate models of retinal degeneration. Proc Natl Acad Sci USA 2016; 113(1): E81-90.
[http://dx.doi.org/10.1073/pnas.1512590113] [PMID: 26699487]
[66]
Pearson RA, Gonzalez-Cordero A, West EL, et al. Donor and host photoreceptors engage in material transfer following transplantation of post-mitotic photoreceptor precursors. Nat Commun 2016; 7(1): 13029.
[http://dx.doi.org/10.1038/ncomms13029] [PMID: 27701378]
[67]
Santos-Ferreira T, Llonch S, Borsch O, Postel K, Haas J, Ader M. Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange. Nat Commun 2016; 7: 13028.
[http://dx.doi.org/10.1038/ncomms13028] [PMID: 27701381]
[68]
Singh MS, Balmer J, Barnard AR, et al. Transplanted photoreceptor precursors transfer proteins to host photoreceptors by a mechanism of cytoplasmic fusion. Nat Commun 2016; 7: 13537.
[http://dx.doi.org/10.1038/ncomms13537] [PMID: 27901042]
[69]
Lakowski J, Gonzalez-Cordero A, West EL, et al. Transplantation of photoreceptor precursors isolated via a cell surface biomarker panel from embryonic stem cell-derived self-forming retina. Stem Cells 2015; 33(8): 2469-82.
[http://dx.doi.org/10.1002/stem.2051] [PMID: 25982268]
[70]
Eberle D, Schubert S, Postel K, Corbeil D, Ader M. Increased integration of transplanted CD73-positive photoreceptor precursors into adult mouse retina. Invest Ophthalmol Vis Sci 2011; 52(9): 6462-71.
[http://dx.doi.org/10.1167/iovs.11-7399] [PMID: 21743009]
[71]
Lakowski J, Welby E, Budinger D, et al. Isolation of human photoreceptor precursors via a cell surface marker panel from stem cell-derived retinal organoids and fetal retinae. Stem Cells 2018; 36(5): 709-22.
[http://dx.doi.org/10.1002/stem.2775] [PMID: 29327488]
[72]
Schwartz SD, Hubschman J-P, Heilwell G, et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012; 379(9817): 713-20.
[http://dx.doi.org/10.1016/S0140-6736(12)60028-2] [PMID: 22281388]
[73]
Schwartz SD, Regillo CD, Lam BL, et al. Human embryonic stem cell-derived retinal pigment epithelium in patients with age-related macular degeneration and Stargardt’s macular dystrophy: Follow-up of two open-label phase 1/2 studies. Lancet 2015; 385(9967): 509-16.
[http://dx.doi.org/10.1016/S0140-6736(14)61376-3] [PMID: 25458728]
[74]
Schwartz SD, Tan G, Hosseini H, Nagiel A. Subretinal transplantation of embryonic stem cell-derived retinal pigment epithelium for the treatment of macular degeneration: An assessment at 4 years. Invest Ophthalmol Vis Sci 2016; 57(5): ORSFc1-9.
[http://dx.doi.org/10.1167/iovs.15-18681] [PMID: 27116660]
[75]
Song WK, Park K-M, Kim H-J, et al. Treatment of macular degeneration using embryonic stem cell-derived retinal pigment epithelium: preliminary results in Asian patients. Stem Cell Reports 2015; 4(5): 860-72.
[http://dx.doi.org/10.1016/j.stemcr.2015.04.005] [PMID: 25937371]
[76]
Liu Y, Xu HW, Wang L, et al. Human embryonic stem cell-derived retinal pigment epithelium transplants as a potential treatment for wet age-related macular degeneration. Cell Discov 2018; 4(1): 50.
[http://dx.doi.org/10.1038/s41421-018-0053-y] [PMID: 30245845]
[77]
da Cruz L, Fynes K, Georgiadis O, et al. Phase 1 clinical study of an embryonic stem cell-derived retinal pigment epithelium patch in age-related macular degeneration. Nat Biotechnol 2018; 36(4): 328-37.
[http://dx.doi.org/10.1038/nbt.4114] [PMID: 29553577]
[78]
Mandai M, Watanabe A, Kurimoto Y, et al. Autologous induced stem-cell-derived retinal cells for macular degeneration. N Engl J Med 2017; 376(11): 1038-46.
[http://dx.doi.org/10.1056/NEJMoa1608368] [PMID: 28296613]
[79]
Garber K. RIKEN suspends first clinical trial involving induced pluripotent stem cells. Nat Biotechnol 2015; 33(9): 890-1.
[http://dx.doi.org/10.1038/nbt0915-890] [PMID: 26348942]
[80]
Sugita S, Mandai M, Hirami Y, et al. HLA-matched allogeneic iPS cells-derived RPE transplantation for macular degeneration. J Clin Med 2020; 9(7): E2217.
[http://dx.doi.org/10.3390/jcm9072217] [PMID: 32668747]
[81]
Bhatt NS, Newsome DA, Fenech T, et al. Experimental transplantation of human retinal pigment epithelial cells on collagen substrates. Am J Ophthalmol 1994; 117(2): 214-21.
[http://dx.doi.org/10.1016/S0002-9394(14)73079-X] [PMID: 8116750]
[82]
Thumann G, Hueber A, Dinslage S, et al. Characteristics of iris and retinal pigment epithelial cells cultured on collagen type I membranes. Curr Eye Res 2006; 31(3): 241-9.
[http://dx.doi.org/10.1080/02713680600556966] [PMID: 16531281]
[83]
Rahmani S, Tabandeh F, Faghihi S, Amoabediny G, Shakibaie M, Noorani B, et al. Fabrication and characterization of poly(ε-caprolactone)/gelatin nanofibrous scaffolds for retinal tissue engineering. Int J Polym Mater 2018; 67(1): 27-35.
[http://dx.doi.org/10.1080/00914037.2017.1297939]
[84]
Wong FS, Wong CC, Chan BP, Lo AC. Sustained delivery of bioactive GDNF from collagen and alginate-based cell-encapsulating gel promoted photoreceptor survival in an inherited retinal degeneration model. PLoS One 2016; 11(7): e0159342.
[http://dx.doi.org/10.1371/journal.pone.0159342] [PMID: 27441692]
[85]
Thackaberry EA, Farman C, Zhong F, et al. Evaluation of the toxicity of intravitreally injected plga microspheres and rods in monkeys and rabbits: effects of depot size on inflammatory response. Invest Ophthalmol Vis Sci 2017; 58(10): 4274-85.
[http://dx.doi.org/10.1167/iovs.16-21334] [PMID: 28850638]
[86]
Tao S, Young C, Redenti S, et al. Survival, migration and differentiation of retinal progenitor cells transplanted on micro-machined poly(methyl methacrylate) scaffolds to the subretinal space. Lab Chip 2007; 7(6): 695-701.
[http://dx.doi.org/10.1039/b618583e] [PMID: 17538710]
[87]
Haraguchi Y, Shimizu T, Yamato M, Okano T. Scaffold-free tissue engineering using cell sheet technology. RSC Advances 2012; 2(6): 2184-90.
[http://dx.doi.org/10.1039/c2ra00704e]
[88]
Madden PW, Klyubin I, Ahearne MJ. Silk fibroin safety in the eye: A review that highlights a concern. BMJ Open Ophthalmol 2020; 5(1): e000510.
[http://dx.doi.org/10.1136/bmjophth-2020-000510] [PMID: 33024827]
[89]
Dellinger JG, Cesarano J III, Jamison RD. Robotic deposition of model hydroxyapatite scaffolds with multiple architectures and multiscale porosity for bone tissue engineering. J Biomed Mater Res A 2007; 82(2): 383-94.
[http://dx.doi.org/10.1002/jbm.a.31072] [PMID: 17295231]
[90]
Chen H, Fan X, Xia J, et al. Electrospun chitosan-graft-poly (ɛ- caprolactone)/poly (ɛ-caprolactone) nanofibrous scaffolds for retinal tissue engineering. Int J Nanomedicine 2011; 6: 453-61.
[PMID: 21499434]
[91]
Nuzzi R, Caselgrandi P, Vercelli A. Effect of mesenchymal stem cell-derived exosomes on retinal injury: A review of current findings. Stem Cells Int 2020; 2020: 8883616.
[http://dx.doi.org/10.1155/2020/8883616] [PMID: 33082789]
[92]
Yu B, Shao H, Su C, et al. Exosomes derived from MSCs ameliorate retinal laser injury partially by inhibition of MCP-1. Sci Rep 2016; 6(1): 34562.
[http://dx.doi.org/10.1038/srep34562] [PMID: 27686625]
[93]
Di Pierdomenico J, Scholz R, Valiente-Soriano FJ, et al. Neuroprotective effects of FGF2 and minocycline in two animal models of inherited retinal degeneration. Invest Ophthalmol Vis Sci 2018; 59(11): 4392-403.
[http://dx.doi.org/10.1167/iovs.18-24621] [PMID: 30193320]
[94]
Puertas-Neyra K, Usategui-Martín R, Coco RM, Fernandez-Bueno I. Intravitreal stem cell paracrine properties as a potential neuroprotective therapy for retinal photoreceptor neurodegenerative diseases. Neural Regen Res 2020; 15(9): 1631-8.
[http://dx.doi.org/10.4103/1673-5374.276324] [PMID: 32209762]
[95]
Bhuthalingam R, Lim PQ, Irvine SA, et al. A novel 3D printing method for cell alignment and differentiation. Int J Bioprint 2015; 1(1): 57-65.
[http://dx.doi.org/10.18063/IJB.2015.01.008]
[96]
Cehajic-Kapetanovic J, Xue K, Martinez-Fernandez de la Camara C, et al. Initial results from a first-in-human gene therapy trial on X-linked retinitis pigmentosa caused by mutations in RPGR. Nat Med 2020; 26(3): 354-9.
[http://dx.doi.org/10.1038/s41591-020-0763-1] [PMID: 32094925]
[97]
Kamao H, Mandai M, Ohashi W, et al. Evaluation of the surgical device and procedure for extracellular matrix-scaffold-supported human iPSC-derived retinal pigment epithelium cell sheet transplantation. Invest Ophthalmol Vis Sci 2017; 58(1): 211-20.
[http://dx.doi.org/10.1167/iovs.16-19778] [PMID: 28114582]

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