Retinal therapy with induced pluripotent stem cells; leading the way to human clinical trials

References

• Flaxman SR, Bourne RRA, Resnikoff S, et al. Global causes of blindness and distance vision impairment 1990–2020: a systematic review and meta-analysis. Lancet Glob Health. 2017;5(12):1221–1234.
   PubMed Web of Science ®Google Scholar
• Oswald J, Baranov P. Regenerative medicine in the retina: from stem cells to cell replacement therapy. Ther Adv Ophthalmol. 2018;10:1–21.
   Web of Science ®Google Scholar
• Cunha-Vaz J. The blood-retinal barrier in the management of retinal disease: EURETINA award lecture. Ophthalmologica. 2017;237(1):1–10.
   PubMed Web of Science ®Google Scholar
• Huang Y, Enzmann V, Ildstad ST. Stem cell-based therapeutic applications in retinal degenerative diseases. Stem Cell Rev. 2011;7(2):434–445.
   PubMed Web of Science ®Google Scholar
• Lamba DA, Gust J, Reh TA. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell. 2009;4:73–79.
   PubMed Web of Science ®Google Scholar
• Mellough CB, Sernagor E, Moreno-Gimeno I, et al. Efficient stage specific differentiation of human pluripotent stem cells towards retinal photoreceptor cells. Stem Cells. 2012;30:673–686.
   PubMed Web of Science ®Google Scholar
• Jayakody SA, Gonzalez-Cordero A, Ali RR, et al. Cellular strategies for retinal repair by photoreceptor replacement. Prog Retin Eye Res. 2015;46:31–66.
   PubMed Web of Science ®Google Scholar
• Stern JH, Tian Y, Funderburgh J, et al. Regenerating eye tissues to preserve and restore vision. Cell Stem Cell. 2018;23(3):834–859.
   Web of Science ®Google Scholar
• Klassen H, Lund RD. Retinal transplants can drive a pupillary reflex in host rat brains. Proc Natl Acad Sci. 1987;84(19):6958–6960.
   PubMed Web of Science ®Google Scholar
• Radtke ND, Aramant RB, Petry HM, et al. Vision improvement in retinal degeneration patients by implantation of retina together with retinal pigment epithelium. Am J Ophthalmol. 2008;146(2):172–182.
   PubMed Web of Science ®Google Scholar
• Seiler MJ, Aramant RB, Jones MK, et al. A new immunodeficient pigmented retinal degenerate rat strain to study transplantation of human cells without immunosuppression. Graefes Arch Clin Exp Ophthalmol. 2014;252(7):1079–1092.
   PubMed Web of Science ®Google Scholar
• Lin B, McLelland BT, Mathur A, et al. Sheets of human retinal progenitor transplants improve vision in rats with severe retinal degeneration. Exp Eye Res. 2018;174:13–28.
   PubMed Web of Science ®Google Scholar
• Tropepe V, Coles BL, Chiasson BJ, et al. Retinal stem cells in the adult mammalian eye. Science. 2000;287(5460):2032–2036.
   PubMed Web of Science ®Google Scholar
• Fischer AJ, Bosse JL, El-Hodiri HM. The ciliary marginal zone (CMZ) in development and regeneration of the vertebrate eye. Exp Eye Res. 2014;123:115–120.
   PubMed Web of Science ®Google Scholar
• Coles BL, Angénieux B, Inoue T, et al. Facile isolation and the characterization of human retinal stem cells. Proc Natl Acad Sci USA. 2004;101(44):15772–15777.
   PubMed Web of Science ®Google Scholar
• Liu H, Xu S, Wang Y, et al. Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling. Dev Biol. 2007;308(1):54–67.
   PubMed Web of Science ®Google Scholar
• Cicero SA, Johnson D, Reyntjens S, et al. Cells previously identified as retinal stem cells are pigmented ciliary epithelial cells. Proc Natl Acad Sci USA. 2009;106(16):6685–6690.
   PubMed Web of Science ®Google Scholar
• Gualdoni S, Baron M, Lakowski J, et al. Adult ciliary epithelial cells, previously identified as retinal stem cells with potential for retinal repair, fail to differentiate into new rod photoreceptors. Stem Cells. 2010;28(6):1048–1059.
   PubMed Web of Science ®Google Scholar
• Osakada F, Ikeda H, Mandai M, et al. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat Biotechnol. 2008;26:215–224.
   PubMed Web of Science ®Google Scholar
• Meyer JS, Shearer RL, Capowski EE, et al. Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc Natl Acad Sci USA. 2009;106(39):16698–16703.
   PubMed Web of Science ®Google Scholar
• Reh TA, Lamba D, and Gust J. Directing human embryonic stem cells to a retinal fate. Methods Mol Biol. 2010;636:139–153.
   PubMedGoogle Scholar
• Mellough CB, Sernagor E, Moreno-Gimeno I, et al. Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem Cells. 2012;30(4):673–686.
   PubMed Web of Science ®Google Scholar
• Boucherie C, Mukherjee S, Henckaerts E, et al. Brief report: self-organizing neuroepithelium from human pluripotent stem cells facilitates derivation of photoreceptors. Stem Cells. 2013;31(2):408–414.
   PubMed Web of Science ®Google Scholar
• Klimanskaya I, Hipp J, Rezai KA, et al. Derivation and comparative assessment of retinal pigment epithelium from human embryonic stem cells using transcriptomics. Cloning Stem Cells. 2004;6(3):217–245.
   PubMedGoogle Scholar
• Carr AJ, 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;15:283–295.
   PubMed Web of Science ®Google Scholar
• 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;5:396–408.
   PubMed Web of Science ®Google Scholar
• 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;27:2126–2135.
   PubMed Web of Science ®Google Scholar
• Lund RD, Lawrence JM, Villegas-Pérez MP, et al. Retinal degeneration and transplantation in the royal college of surgeons rat. Eye (Lond). 1998;12:597–604.
   PubMed Web of Science ®Google Scholar
• Pang JJ, Chang B, Hawes NL, et al. Retinal degeneration 12 (rd12): a new, spontaneously arising mouse model for human Leber congenital amaurosis (LCA). Mol Vis. 2005;11:152–162.
   PubMed Web of Science ®Google Scholar
• Duncan JL, LaVail MM, Yasumura D, et al. An RCS-like retinal dystrophy phenotype in mer knockout mice. Invest Ophthalmol Vis Sci. 2003;44(2):826–838.
   PubMed Web of Science ®Google Scholar
• Yanai A, Laver CR, Joe AW, et al. Differentiation of human embryonic stem cells using size-controlled embryoid bodies and negative cell selection in the production of photoreceptor precursor cells. Tissue Eng Part C Methods. 2013;19(10):755–764.
   PubMed Web of Science ®Google Scholar
• Reynolds J, Lamba DA. Human embryonic stem cell applications for retinal degenerations. Exp Eye Res. 2014;123:151–160.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–676.
   PubMed Web of Science ®Google Scholar
• Hiler DJ, Barabas ME, Griffiths LM, et al. Reprogramming of mouse retinal neurons and standardized quantification of their differentiation in 3D retinal cultures. Nat Protoc. 2016;11(10):1955–1976.
   PubMed Web of Science ®Google Scholar
• Lamba DA, McUsic A, Hirata RK, et al. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PLoS One. 2010;5(1):e8763.
   PubMed Web of Science ®Google Scholar
• Jin ZB, Okamoto S, Osakada F, et al. Modeling retinal degeneration using patient-specific induced pluripotent stem cells. PLoS One. 2011 Feb 10;6(2):e17084.
   PubMed Web of Science ®Google Scholar
• Tucker BA, Mullins RF, Streb LM, et al. Patient-specific iPSC-derived photoreceptor precursor cells as a means to investigate retinitis pigmentosa. Elife. 2013;2:e00824.
   PubMed Web of Science ®Google Scholar
• Ohlemacher SK, Iglesias CL, Sridhar A, et al. Generation of highly enriched populations of optic vesicle-like retinal cells from human pluripotent stem cells. Curr Protoc Stem Cell Biol. 2015;2(32):1–20.
   Google Scholar
• Gonzalez-Cordero A, Kruczek K, Naeem A, et al. Recapitulation of human retinal development from human pluripotent stem cells generates transplantable populations of cone photoreceptors. Stem Cell Rep. 2017;9(3):820–837.
   PubMed Web of Science ®Google Scholar
• Hallam D, Hilgen G, Dorgau B, et al. Human-induced pluripotent stem cells generate light responsive retinal organoids with variable and nutrient-dependent efficiency. Stem Cells. 2018 Jul 13. DOI:10.1002/stem.2883
   Web of Science ®Google Scholar
• 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):709–722.
   PubMed Web of Science ®Google Scholar
• Gagliardi G, Ben M’Barek K, Chaffiol A, et al. Characterization and transplantation of CD73-positive photoreceptors isolated from human iPSC-derived retinal organoids. Stem Cell Rep. 2018;11(3):665–680.
   PubMed Web of Science ®Google Scholar
• Denning C, Borgdorff V, Crutchley J, et al. Cardiomyocytes from human pluripotent stem cells: from laboratory curiosity to industrial biomedical platform. Biochim Biophys Acta. 2016;1863:1728–1748.
   PubMed Web of Science ®Google Scholar
• Itakura G, Kawabata S, Ando M, et al. Fail-safe system against potential tumorigenicity after transplantation of iPSC derivatives. Stem Cell Rep. 2017;8(3):673–684.
   PubMed Web of Science ®Google Scholar
• Kogut I, McCarthy SM, Pavlova M, et al. High-efficiency RNA-based reprogramming of human primary fibroblasts. Nat Commun. 2018;9(1):745–760.
   PubMedGoogle Scholar
• 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):771–785.
   PubMed Web of Science ®Google Scholar
• Lukovic D, Castro AA, Garcia Delgado AB, et al. Human iPSC derived disease model of MERTK-associated retinitis pigmentosa. Sci Rep. 2015;5:12910–12921.
   PubMed Web of Science ®Google Scholar
• Kaewkhaw R, Swaroop M, Homma K, et al. Treatment paradigms for retinal and macular diseases using 3-D retina cultures derived from human reporter pluripotent stem cell lines. Invest Ophthalmol Vis Sci. 2016;57(5):1–11.
   PubMed Web of Science ®Google Scholar
• Parfitt DA, Lane A, Ramsden CM, et al. Identification and correction of mechanisms underlying inherited blindness in human iPSC-derived optic cups. Cell Stem Cell. 2016;18(6):769–781.
   PubMed Web of Science ®Google Scholar
• Wiley LA, Burnight ER, DeLuca AP, et al. cGMP production of patient-specific iPSCs and photoreceptor precursor cells to treat retinal degenerative blindness. Sci Rep. 2016;6:30742–30758.
   PubMed Web of Science ®Google Scholar
• Reichman S, Slembrouck A, Gagliardi G, et al. Generation of storable retinal organoids and retinal pigmented epithelium from adherent human iPS cells in xeno-free and feeder-free conditions. Stem Cells. 2017;35(5):1176–1188.
   PubMed Web of Science ®Google Scholar
• Wahlin KJ, Maruotti JA, Sripathi SR, et al. Photoreceptor outer segment-like structures in long-term 3D retinas from human pluripotent stem cells. Sci Rep. 2017;7(1):766–781.
   PubMedGoogle Scholar
• Zhou L, Wang W, Liu Y, et al. Differentiation of induced pluripotent stem cells of swine into rod photoreceptors and their integration into the retina. Stem Cells. 2011;29(6):972–980.
   PubMed Web of Science ®Google Scholar
• Giacalone JC, Sharma TP, Burnight ER, et al. CRISPR-Cas9-based genome editing of human induced pluripotent stem cells. Curr Protoc Stem Cell Biol. 2018;44:5B.7.1-5B.7.22.
   PubMedGoogle Scholar
• Burnight ER, Giacalone JC, Cooke JA, et al. CRISPR-Cas9 genome engineering: treating inherited retinal degeneration. Prog Retin Eye Res. 2018;65:28–49.
   PubMed Web of Science ®Google Scholar
• Jones BW, Kondo M, Terasaki H, et al. Retinal remodeling in the Tg P347L rabbit, a large-eye model of retinal degeneration. J Comp Neurol. 2011 Oct 1;519(14):2713–2733.
   PubMed Web of Science ®Google Scholar
• Petrus-Reurer S, Bartuma H, Aronsson M, et al. Integration of subretinal suspension transplants of human embryonic stem cell-derived retinal pigment epithelial cells in a large-eyed model of geographic atrophy. Invest Ophthalmol Vis Sci. 2017;58(2):1314–1322.
   PubMed Web of Science ®Google Scholar
• Kobayashi E, Hishikawa S, Teratani T, et al. The pig as a model for translational research: overview of porcine animal models at Jichi Medical University. Transplant Res. 2012;1(1):8–17.
   PubMedGoogle Scholar
• Ross JW, Fernandez de Castro JP, Zhao J, et al. Generation of an inbred miniature pig model of retinitis pigmentosa. Invest Ophthalmol Vis Sci. 2012;53(1):501–507.
   PubMed Web of Science ®Google Scholar
• Chao JR, Lamba DA, Klesert TR, et al. Transplantation of human embryonic stem cell-derived retinal cells into the subretinal space of a non-human primate. Transl Vis Sci Technol. 2017;6(3):4–17.
   PubMed Web of Science ®Google Scholar
• Sugita S, Makabe K, Fujii S, et al. Detection of retinal pigment epithelium-specific antibody in iPSC-derived retinal pigment epithelium transplantation models. Stem Cell Rep. 2017;9(5):1501–1515.
   PubMed Web of Science ®Google Scholar
• Luo Z, Li K, Xian B, et al. Establishing a surgical procedure for rhesus epiretinal scaffold implantation with HiPSC-derived retinal progenitors. Stem Cells Int. 2018:1-10.
   Web of Science ®Google Scholar
• Mandai M, Fujii M, Hashiguchi T, et al. iPSC-derived retina transplants improve vision in rd1 end-stage retinal-degeneration mice. Stem Cell Rep. 2017;8(4):1112–1113.
   PubMed Web of Science ®Google Scholar
• McLelland BT, Lin B, Mathur A, et al. Transplanted hESC-derived retina organoid sheets differentiate, integrate, and improve visual function in retinal degenerate rats. Invest Ophthalmol Vis Sci. 2018;59(6):2586–2603.
   PubMed Web of Science ®Google Scholar
• Ben M’Barek K, Habeler W, Plancheron A, et al. Human ESC-derived retinal epithelial cell sheets potentiate rescue of photoreceptor cell loss in rats with retinal degeneration. Sci Transl Med. 2017;9(421):1–12.
   Web of Science ®Google Scholar
• McGill TJ, Bohana-Kashtan O, Stoddard JW, et al. Long-term efficacy of GMP grade xeno-free hESC-derived RPE cells following transplantation. Transl Vis Sci Technol. 2017;6(3):17–35.
   PubMed Web of Science ®Google Scholar
• Zhu J, Cifuentes H, Reynolds J, et al. Immunosuppression via loss of IL2rγ enhances long-term functional integration of hESC-derived photoreceptors in the mouse retina. Cell Stem Cell. 2017;20(3):374–384.
   PubMed Web of Science ®Google Scholar
• Kruczek K, Gonzalez-Cordero A, Goh D, et al. Differentiation and transplantation of embryonic stem cell-derived cone photoreceptors into a mouse model of end-stage retinal degeneration. Stem Cell Rep. 2017;8(6):1659–1674.
   PubMed Web of Science ®Google Scholar
• Wu H, Li J, Mao X, et al. Transplantation of rat embryonic stem cell-derived retinal cells restores visual function in the royal college of surgeons rats. Doc Ophthalmol. 2018 Aug 3. DOI:10.1007/s10633-018-9648-8.
   PubMed Web of Science ®Google Scholar
• Qu L, Gao L, Xu H, et al. Combined transplantation of human mesenchymal stem cells and human retinal progenitor cells into the subretinal space of RCS rats. Sci Rep. 2017;7(1):199–213.
   PubMedGoogle Scholar
• Davis RJ, Alam NM, Zhao C, et al. The developmental stage of adult human stem cell-derived retinal pigment epithelium cells influences transplant efficacy for vision rescue. Stem Cell Rep. 2017;9(1):42–49.
   PubMed Web of Science ®Google Scholar
• Diehl R, Ferrara F, Müller C, et al. Immunosuppression for in vivo research: state-of-the-art protocols and experimental approaches. Cell Mol Immunol. 2017;14(2):146–179.
   PubMed Web of Science ®Google Scholar
• Stegall MD, Morris RE, Alloway RR, et al. Developing new immunosuppression for the next generation of transplant recipients: the path forward. Am J Transplant. 2016;16(4):1094–1101.
   PubMed Web of Science ®Google Scholar
• Taylor CJ, Peacock S, Chaudhry AN, et al. Generating an iPSC bank for HLA-matched tissue transplantation based on known donor and recipient HLA types. Cell Stem Cell. 2012;11(2):147–152.
   PubMed Web of Science ®Google Scholar
• Mattapally S, Pawlik KM, Fast VG, et al. Human leukocyte antigen class I and II knockout human induced pluripotent stem cell-derived cells: universal donor for cell therapy. J Am Heart Assoc. 2018;7(23):e01023.
   Web of Science ®Google Scholar
• Eberle D, Schubert S, Postel K, et al. Increased integration of transplanted CD73-positive photoreceptor precursors into adult mouse retina. Invest Ophthalmol Vis Sci. 2011;52(9):6462–6471.
   PubMed Web of Science ®Google Scholar
• Pearson RA, Barber AC, Rizzi M, et al. Restoration of vision after transplantation of photoreceptors. Nature. 2012;485(7396):99–103.
   PubMed Web of Science ®Google Scholar
• Parker J, Mitrousis N, Shoichet MS. Hydrogel for simultaneous tunable growth factor delivery and enhanced viability of encapsulated cells in vitro. Biomacromolecules. 2016;17(2):476–484.
   PubMed Web of Science ®Google Scholar
• Sleep E, Cosgrove BD, McClendon MT, et al. Injectable biomimetic liquid crystalline scaffolds enhance muscle stem cell transplantation. Proc Natl Acad Sci USA. 2017;114(38):7919–7928.
   Web of Science ®Google Scholar
• 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):509–516.
   PubMed Web of Science ®Google Scholar
• Song WK, Park KM, Kim HJ. Treatment of macular degeneration using embryonic stem cell-derived retinal pigment epithelium: preliminary results in Asian patients. Stem Cell Rep. 2015;4(5):860–872.
   PubMed Web of Science ®Google Scholar
• 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):328–337.
   PubMed Web of Science ®Google Scholar
• 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):1038–1046.
   PubMed Web of Science ®Google Scholar