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Stem cell transplantation as a progressing treatment for retinitis pigmentosa

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Abstract

Retinal degenerative diseases such as retinitis pigmentosa (RP) are of the major causes of vision loss in developed countries. Despite the unclear pathophysiology, treatment methods have been investigated vastly in the past decades. This review article mainly discusses the advances in application of stem cell and progenitor transplantation for retinitis pigmentosa. Stem cell sources such as mesenchymal stem cells, embryonic stem cells, induced pluripotent stem cells, neural stem cells, retinal progenitor cells, and olfactory ensheathing cells are discussed separately in addition to a brief description of two approaches for treatment of early-stage RP, including gene therapy and nutritional therapy.

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References

  • Allocca M, Mussolino C, Garcia-Hoyos M, Sanges D, Iodice C, Petrillo M, Vandenberghe LH, Wilson JM, Marigo V, Surace EM (2007) Novel adeno-associated virus serotypes efficiently transduce murine photoreceptors. J Virol 81:11372–11380

    CAS  PubMed  PubMed Central  Google Scholar 

  • Almedawar S, Vafia K, Schreiter S, Neumann K, Khattak S, Kurth T, Ader M, Karl MO, Tsang SH, Tanaka EM (2020) MERTK-dependent ensheathment of photoreceptor outer segments by human pluripotent stem cell-derived retinal pigment epithelium. Stem Cell Reports 14:374–389. https://doi.org/10.1016/j.stemcr.2020.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andrews MR, Stelzner DJ (2007) Evaluation of olfactory ensheathing and schwann cells after implantation into a dorsal injury of adult rat spinal cord. J Neurotrauma 24:1773–1792. https://doi.org/10.1089/neu.2007.0353

    Article  PubMed  Google Scholar 

  • Andrieu-Soler C, Doat M, Halhal M, Keller N, Jonet L, BenEzra D, Behar-Cohen F (2006) Enhanced oligonucleotide delivery to mouse retinal cells using iontophoresis. Mol vis 12:1098–1107

    CAS  PubMed  Google Scholar 

  • Arnhold S, Absenger Y, Klein H, Addicks K, Schraermeyer U (2007) Transplantation of bone marrow-derived mesenchymal stem cells rescue photoreceptor cells in the dystrophic retina of the rhodopsin knockout mouse. Graefe’s Archive for Clinical and Experimental Ophthalmology 245:414–422

    CAS  PubMed  Google Scholar 

  • Artero-Castro A, Long K, Bassett A, Ávila-Fernandez A, Cortón M, Vidal-Puig A, Jendelova P, Rodriguez-Jimenez FJ, Clemente E, Ayuso C, Slaven E (2021) Gene correction recovers phagocytosis in retinal pigment epithelium derived from retinitis pigmentosa-human-induced pluripotent stem cells. Int J Mol Sci 22. https://doi.org/10.3390/ijms22042092

  • Artero Castro A, Long K, Bassett A, Machuca C, León M, Ávila-Fernandez A, Cortón M, Vidal-Puig T, Ayuso C, Lukovic D, Erceg S (2019) Generation of gene-corrected human induced pluripotent stem cell lines derived from retinitis pigmentosa patient with Ser331Cysfs*5 mutation in MERTK. Stem Cell Research 34. https://doi.org/10.1016/j.scr.2018.11.003

  • Barnea-Cramer AO, Wang W, Lu S-J, Singh MS, Luo C, Huo H, McClements ME, Barnard AR, MacLaren RE, Lanza R (2016) Function of human pluripotent stem cell-derived photoreceptor progenitors in blind mice. Scientific Reps 6

  • Bassuk AG, Zheng A, Li Y, Tsang SH, Mahajan VB (2016) Precision medicine: genetic repair of retinitis pigmentosa in patient-derived stem cells. Scientific reps 6

  • Beltran WA, Cideciyan AV, Boye SE, Ye GJ, Iwabe S, Dufour VL, Marinho LF, Swider M, Kosyk MS, Sha J, Boye SL, Peterson JJ, Witherspoon CD, Alexander JJ, Ying GS, Shearman MS, Chulay JD, Hauswirth WW, Gamlin PD, Jacobson SG, Aguirre GD (2017) Optimization of retinal gene therapy for X-linked retinitis pigmentosa due to RPGR mutations. Mol Ther 25:1866–1880. https://doi.org/10.1016/j.ymthe.2017.05.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beltran WA, Cideciyan AV, Lewin AS, Iwabe S, Khanna H, Sumaroka A, Chiodo VA, Fajardo DS, Román AJ, Deng W-T (2012) Gene therapy rescues photoreceptor blindness in dogs and paves the way for treating human X-linked retinitis pigmentosa. Proc Natl Acad Sci 109:2132–2137

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bemelmans A-P, Kostic C, Crippa SV, Hauswirth WW, Lem J, Munier FL, Seeliger MW, Wenzel A, Arsenijevic Y (2006) Lentiviral gene transfer of RPE65 rescues survival and function of cones in a mouse model of Leber congenital amaurosis. PLoS Med 3:e347

  • Ben M’Barek K, Bertin S, Brazhnikova E, Jaillard C, Habeler W, Plancheron A, Fovet CM, Demilly J, Jarraya M, Bejanariu A, Sahel JA, Peschanski M, Goureau O, Monville C (2020) Clinical-grade production and safe delivery of human ESC derived RPE sheets in primates and rodents. Biomaterials 230:119603. https://doi.org/10.1016/j.biomaterials.2019.119603

    Article  CAS  PubMed  Google Scholar 

  • Ben M’Barek K, Habeler W, Plancheron A, Jarraya M, Goureau O, Monville C (2018) Engineering transplantation-suitable retinal pigment epithelium tissue derived from human embryonic stem cells. J vis Exp. https://doi.org/10.3791/58216

    Article  PubMed  PubMed Central  Google Scholar 

  • Bennett J, Zeng Y, Bajwa R, Klatt L, Li Y, Maguire A (1998) Adenovirus-mediated delivery of rhodopsin-promoted bcl-2 results in a delay in photoreceptor cell death in the rd/rd mouse. Gene therap 5

  • Berson EL, Rosner B, Sandberg MA, Weigel-DiFranco C, Willett WC (2012) ω-3 intake and visual acuity in patients with retinitis pigmentosa receiving vitamin A. Arch Ophthalmol 130:707–711

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bian B, Zhao C, He X, Gong Y, Ren C, Ge L, Zeng Y, Li Q, Chen M, Weng C, He J, Fang Y, Xu H, Yin ZQ (2020) Exosomes derived from neural progenitor cells preserve photoreceptors during retinal degeneration by inactivating microglia. J Extracell Vesicles 9:1748931–1748931. https://doi.org/10.1080/20013078.2020.1748931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birch DG, Bennett LD, Duncan JL, Weleber RG, Pennesi ME (2016) Long-term follow-up of patients with retinitis pigmentosa receiving intraocular ciliary neurotrophic factor implants. Am J Ophthalmol 170:10–14. https://doi.org/10.1016/j.ajo.2016.07.013

    Article  PubMed  PubMed Central  Google Scholar 

  • Birch DG, Bernstein PS, Iannacone A, Pennesi ME, Lam BL, Heckenlively J, Csaky K, Hartnett ME, Winthrop KL, Jayasundera T, Hughbanks-Wheaton DK, Warner J, Yang P, Fish GE, Teske MP, Sklaver NL, Erker L, Chegarnov E, Smith T, Wahle A, VanVeldhuisen PC, McCormack J, Lindblad R, Bramer S, Rose S, Zilliox P, Francis PJ, Weleber RG (2018) Effect of oral valproic acid vs placebo for vision loss in patients with autosomal dominant retinitis pigmentosa: a randomized phase 2 multicenter placebo-controlled clinical trial. JAMA Ophthalmology 136:849–856. https://doi.org/10.1001/jamaophthalmol.2018.1171

    Article  PubMed  PubMed Central  Google Scholar 

  • Birch DG, Weleber RG, Duncan JL, Jaffe GJ, Tao W, Ciliary Neurotrophic Factor Retinitis Pigmentosa Study G (2013) Randomized trial of ciliary neurotrophic factor delivered by encapsulated cell intraocular implants for retinitis pigmentosa. Am J Ophthalmol 156:283-292.e281. https://doi.org/10.1016/j.ajo.2013.03.021

    Article  CAS  Google Scholar 

  • Bolinches-Amorós A, León M, Del Buey FV, Marfany G, Gonzàlez-Duarte R, Erceg S, Lukovic D (2019) Generation of an iPSC line from a retinitis pigmentosa patient carrying a homozygous mutation in CERKL and a healthy sibling. Stem Cell Res 38:101455. https://doi.org/10.1016/j.scr.2019.101455

    Article  CAS  PubMed  Google Scholar 

  • Boudreault K, Justus S, Lee W, Mahajan VB, Tsang SH (2016) Complication of autologous stem cell transplantation in retinitis pigmentosa. JAMA Ophthalmology 134:711–712

    PubMed  Google Scholar 

  • Buchholz DE, Hikita ST, Rowland TJ, Friedrich AM, Hinman CR, Johnson LV, Clegg DO (2009) Derivation of Functional Retinal Pigmented Epithelium from Induced Pluripotent Stem Cells Stem Cells 27:2427–2434

    CAS  PubMed  Google Scholar 

  • Cai S, Smith ME, Redenti SM, Wnek GE, Young MJ (2012) Mouse retinal progenitor cell dynamics on electrospun poly(-caprolactone). J Biomater Sci Polym Ed 23:1451–1465. https://doi.org/10.1163/092050611x584388

    Article  CAS  PubMed  Google Scholar 

  • Canola K, Angénieux B, Tekaya M, Quiambao A, Naash MI, Munier FL, Schorderet DF, Arsenijevic Y (2007) Retinal Stem Cells Transplanted into Models of Late Stages of Retinitis Pigmentosa Preferentially Adopt a Glial or a Retinal Ganglion Cell Fate Investigative Ophthalmology & Visual Science 48:446–454

    Google Scholar 

  • Cao J, Murat C, An W, Yao X, Lee J, Santulli-Marotto S, Harris IR, Inana G (2016) Human umbilical tissue-derived cells rescue retinal pigment epithelium dysfunction in retinal degeneration. Stem Cells 34:367–379

    CAS  PubMed  Google Scholar 

  • Cehajic-Kapetanovic J, Xue K, Martinez-Fernandez de la Camara C, Nanda A, Davies A, Wood LJ, Salvetti AP, Fischer MD, Aylward JW, Barnard AR, Jolly JK, Luo E, Lujan BJ, Ong T, Girach A, Black GCM, Gregori NZ, Davis JL, Rosa PR, Lotery AJ, Lam BL, Stanga PE, MacLaren RE (2020) Initial results from a first-in-human gene therapy trial on X-linked retinitis pigmentosa caused by mutations in RPGR. Nat Med 26:354–359. https://doi.org/10.1038/s41591-020-0763-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cehajic Kapetanovic J, McClements ME, Martinez-Fernandez de la Camara C, MacLaren RE (2019) Molecular strategies for RPGR gene therapy. Genes (basel) 10. https://doi.org/10.3390/genes10090674

  • Charbel Issa P, MacLaren RE (2012) Non-viral retinal gene therapy: a review. Clin Experiment Ophthalmol 40:39–47. https://doi.org/10.1111/j.1442-9071.2011.02649.x

    Article  PubMed  Google Scholar 

  • Cideciyan AV, Sudharsan R, Dufour VL, Massengill MT, Iwabe S, Swider M, Lisi B, Sumaroka A, Marinho LF, Appelbaum T, Rossmiller B, Hauswirth WW, Jacobson SG, Lewin AS, Aguirre GD, Beltran WA (2018) Mutation-independent rhodopsin gene therapy by knockdown and replacement with a single AAV vector. Proc Natl Acad Sci U S A 115:E8547-e8556. https://doi.org/10.1073/pnas.1805055115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cramer AO, MacLaren RE (2013) Translating induced pluripotent stem cells from bench to bedside: application to retinal diseases. Curr Gene Ther 13:139–151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Darrow JJ (2019) Luxturna: FDA documents reveal the value of a costly gene therapy. Drug Discov Today 24:949–954. https://doi.org/10.1016/j.drudis.2019.01.019

    Article  PubMed  Google Scholar 

  • Delgado D, del Pozo-Rodríguez A, Solinís MÁ, Avilés-Triqueros M, Weber BH, Fernández E, R. Gascón A, (2012) Dextran and protamine-based solid lipid nanoparticles as potential vectors for the treatment of X-linked juvenile retinoschisis. Hum Gene Ther 23:345–355

    CAS  PubMed  Google Scholar 

  • Deng S, Oka K (2020) Adeno-associated virus as gene delivery vehicle into the retina. Methods in Molecular Biology (clifton, NJ) 2092:77–90. https://doi.org/10.1007/978-1-0716-0175-4_7

    Article  CAS  Google Scholar 

  • Ding SLS, Koh AE, Kumar S, Ali Khan MS, Alzahrani B, Mok PL (2019) Genetically-modified human mesenchymal stem cells to express erythropoietin enhances differentiation into retinal photoreceptors: an in-vitro study. J Photochem Photobiol B 195:33–38. https://doi.org/10.1016/j.jphotobiol.2019.04.008

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Carvalho E, Murphy C, McInerney V, Krawczyk J, O’Brien T, Howard L, Cai L, Shen S (2020) Derivation of familial iPSC lines from three patients with retinitis pigmentosa carrying an autosomal dominant RPE65 mutation (NUIGi027-A, NUIGi028-A, NUIGi029-A) Stem Cell Res 43:101665. https://doi.org/10.1016/j.scr.2019.101665

  • Domingo-Prim J, Riera M, Burés-Jelstrup A, Corcostegui B, Pomares E (2019) Establishment of an induced pluripotent stem cell line (FRIMOi005-A) derived from a retinitis pigmentosa patient carrying a dominant mutation in RHO gene Stem cell research 38. https://doi.org/10.1016/j.scr.2019.101468

  • Dufour VL, Cideciyan AV, Ye GJ, Song C, Timmers A, Habecker PL, Pan W, Weinstein NM, Swider M, Durham AC, Ying GS, Robinson PM, Jacobson SG, Knop DR, Chulay JD, Shearman MS, Aguirre GD, Beltran WA (2020) Toxicity and efficacy evaluation of an adeno-associated virus vector expressing codon-optimized RPGR delivered by subretinal injection in a canine model of X-linked retinitis pigmentosa. Hum Gene Ther 31:253–267. https://doi.org/10.1089/hum.2019.297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farjo R, Skaggs J, Quiambao AB, Cooper MJ, Naash MI (2006) Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PLoS ONE 1:e38. https://doi.org/10.1371/journal.pone.0000038

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferguson LR, Balaiya S, Mynampati BK, Sambhav K, Chalam KV (2015) Deprivation of bFGF promotes spontaneous differentiation of human embryonic stem cells into retinal pigment epithelial cells. J Stem Cells 10:159–170

    PubMed  Google Scholar 

  • Florio M, Huttner WB (2014) Neural progenitors, neurogenesis and the evolution of the neocortex. Development 141:2182–2194

    CAS  PubMed  Google Scholar 

  • Fukuda S, Nagano M, Yamashita T, Kimura K, Tsuboi I, Salazar G, Ueno S, Kondo M, Kunath T, Oshika T (2013) Functional endothelial progenitor cells selectively recruit neurovascular protective monocyte-derived F4/80+/Ly6c+ macrophages in a mouse model of retinal degeneration. Stem Cells 31:2149–2161

    CAS  PubMed  Google Scholar 

  • Gamm DM, Wang S, Lu B, Girman S, Holmes T, Bischoff N, Shearer RL, Sauvé Y, Capowski E, Svendsen CN (2007) Protection of visual functions by human neural progenitors in a rat model of retinal disease. PloS one 2:e338

  • Gearhart PM, Gearhart C, Thompson DA, Petersen-Jones SM (2010) Improvement of visual performance with intravitreal administration of 9-cis-retinal in Rpe65-mutant dogs. Arch Ophthalmol 128:1442–1448. https://doi.org/10.1001/archophthalmol.2010.210

    Article  CAS  PubMed  Google Scholar 

  • Ghazi NG, Abboud EB, Nowilaty SR, Alkuraya H, Alhommadi A, Cai H, Hou R, Deng WT, Boye SL, Almaghamsi A, Al Saikhan F, Al-Dhibi H, Birch D, Chung C, Colak D, LaVail MM, Vollrath D, Erger K, Wang W, Conlon T, Zhang K, Hauswirth W, Alkuraya FS (2016) Treatment of retinitis pigmentosa due to MERTK mutations by ocular subretinal injection of adeno-associated virus gene vector: results of a phase I trial. Hum Genet 135:327–343. https://doi.org/10.1007/s00439-016-1637-y

    Article  CAS  PubMed  Google Scholar 

  • Giacalone JC, Andorf JL, Zhang Q, Burnight ER, Ochoa D, Reutzel AJ, Collins MM, Sheffield VC, Mullins RF, Han IC, Stone EM, Tucker BA (2019) Development of a molecularly stable gene therapy vector for the treatment of RPGR-associated X-linked retinitis pigmentosa. Hum Gene Ther 30:967–974. https://doi.org/10.1089/hum.2018.244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory-Evans K, Chang F, Hodges MD, Gregory-Evans CY (2009) Ex vivo gene therapy using intravitreal injection of GDNF-secreting mouse embryonic stem cells in a rat model of retinal degeneration

  • Gu S, Xing C, Han J, Tso MO, Hong J (2009) Differentiation of rabbit bone marrow mesenchymal stem cells into corneal epithelial cells in vivo and ex vivo

  • Hambright D, Park K-Y, Brooks M, McKay R, Swaroop A, Nasonkin IO (2012) Long-term survival and differentiation of retinal neurons derived from human embryonic stem cell lines in un-immunosuppressed mouse retina

  • Hamel C (2006) Retinitis pigmentosa. Orphanet J Rare Dis 1:1

    Google Scholar 

  • Hartong DT, Berson EL, Dryja TP (2006) Retinitis pigmentosa. The Lancet 368:1795–1809

    CAS  Google Scholar 

  • He XY, Zhao CJ, Xu H, Chen K, Bian BS, Gong Y, Weng CH, Zeng YX, Fu Y, Liu Y, Yin ZQ (2021) Synaptic repair and vision restoration in advanced degenerating eyes by transplantation of retinal progenitor cells. Stem Cell Reports 16:1805–1817. https://doi.org/10.1016/j.stemcr.2021.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Y, Zhang Y, Liu X, Ghazaryan E, Li Y, Xie J, Su G (2014) Recent advances of stem cell therapy for retinitis pigmentosa. Int J Mol Sci 15:14456–14474

    CAS  PubMed  PubMed Central  Google Scholar 

  • Health Quality O (2017) Retinal prosthesis system for advanced retinitis pigmentosa: a health technology assessment update. Ont Health Technol Assess Ser 17:1–62

    Google Scholar 

  • Holan V, Palacka K, Hermankova B (2021) Mesenchymal stem cell-based therapy for retinal degenerative diseases: experimental models and clinical trials. Cells 10. https://doi.org/10.3390/cells10030588

  • Homma K, Okamoto S, Mandai M, Gotoh N, Rajasimha HK, Chang YS, Chen S, Li W, Cogliati T, Swaroop A (2013) Developing rods transplanted into the degenerating retina of Crx-knockout mice exhibit neural activity similar to native photoreceptors. Stem Cells 31:1149–1159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huo SJ, Li Y, Raisman G, Yin ZQ (2011) Transplanted olfactory ensheathing cells reduce the gliotic injury response of Müller cells in a rat model of retinitis pigmentosa. Brain Res 1382:238–244

    CAS  PubMed  Google Scholar 

  • Huo SJ, Li YC, Xie J, Li Y, Raisman G, Zeng YX, He JR, Weng CH, Yin ZQ (2012) Transplanted olfactory ensheathing cells reduce retinal degeneration in royal college of surgeons rats. Curr Eye Res 37:749–758

    CAS  PubMed  Google Scholar 

  • Idelson M, Alper R, Obolensky A, Ben-Shushan E, Hemo I, Yachimovich-Cohen N, Khaner H, Smith Y, Wiser O, Gropp M (2009) Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell Stem Cell 5:396–408

    CAS  PubMed  Google Scholar 

  • Jian Q, Xu H, Xie H, Tian C, Zhao T, Yin Z (2009) Activation of retinal stem cells in the proliferating marginal region of RCS rats during development of retinitis pigmentosa. Neurosci Lett 465:41–44

    CAS  PubMed  Google Scholar 

  • Jin Z-B, Okamoto S, Osakada F, Homma K, Assawachananont J, Hirami Y, Iwata T, Takahashi M (2011) Modeling retinal degeneration using patient-specific induced pluripotent stem cells. PloS one 6:e17084

  • Jin Z-B, Okamoto S, Xiang P, Takahashi M (2012) Integration-free induced pluripotent stem cells derived from retinitis pigmentosa patient for disease modeling. Stem Cells Transl Med 1:503–509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson CJ, Berglin L, Chrenek MA, Redmond TM, Boatright JH, Nickerson JM (2008) Technical brief: subretinal injection and electroporation into adult mouse eyes. Mol vis 14:2211–2226

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kachi S, Oshima Y, Esumi N, Kachi M, Rogers B, Zack DJ, Campochiaro PA (2005) Nonviral ocular gene transfer. Gene Ther 12:843–851. https://doi.org/10.1038/sj.gt.3302475

    Article  CAS  PubMed  Google Scholar 

  • Kahraman NS, Oner A (2020) Umbilical cord derived mesenchymal stem cell implantation in retinitis pigmentosa: a 6-month follow-up results of a phase 3 trial. Int J Ophthalmol 13:1423–1429. https://doi.org/10.18240/ijo.2020.09.14

    Article  PubMed  PubMed Central  Google Scholar 

  • Kawasaki H, Suemori H, Mizuseki K, Watanabe K, Urano F, Ichinose H, Haruta M, Takahashi M, Yoshikawa K, Nishikawa S-I (2002) Generation of dopaminergic neurons and pigmented epithelia from primate ES cells by stromal cell-derived inducing activity. Proc Natl Acad Sci 99:1580–1585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kay CN, Ryals RC, Aslanidi GV, Min SH, Ruan Q, Sun J, Dyka FM, Kasuga D, Ayala AE, Van Vliet K, Agbandje-McKenna M, Hauswirth WW, Boye SL, Boye SE (2013) Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS ONE 8:e62097. https://doi.org/10.1371/journal.pone.0062097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kenna PF, Humphries MM, Kiang AS, Brabet P, Guillou L, Ozaki E, Campbell M, Farrar GJ, Koenekoop R, Humphries P (2020) Advanced late-onset retinitis pigmentosa with dominant-acting D477G RPE65 mutation is responsive to oral synthetic retinoid therapy. BMJ Open Ophthalmology 5:e000462. https://doi.org/10.1136/bmjophth-2020-000462

    Article  PubMed  PubMed Central  Google Scholar 

  • Kicic A, Shen W-Y, Wilson AS, Constable IJ, Robertson T, Rakoczy PE (2003) Differentiation of marrow stromal cells into photoreceptors in the rat eye. J Neurosci 23:7742–7749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Lewallen M, Chen S, Yu W, Zhang N, Xie T (2013) Multipotent stem cells isolated from the adult mouse retina are capable of producing functional photoreceptor cells. Cell Res 23:788–802

    PubMed  PubMed Central  Google Scholar 

  • Li XX, Yuan XJ, Zhai Y, Yu S, Jia RX, Yang LP, Ma ZZ, Zhao YM, Wang YX, Ge LH (2019) Treatment with stem cells from human exfoliated deciduous teeth and their derived conditioned medium improves retinal visual function and delays the degeneration of photoreceptors. Stem Cells Dev 28:1514–1526. https://doi.org/10.1089/scd.2019.0158

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Tsai Y-T, Hsu C-W, Erol D, Yang J, Wu W-H, Davis RJ, Egli D, Tsang SH (2012) Long-term safety and efficacy of human-induced pluripotent stem cell (iPS) grafts in a preclinical model of retinitis pigmentosa. Mol Med 18:1312

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li YP, Deng WL, Jin ZB (2021) Modeling retinitis pigmentosa through patient-derived retinal organoids. STAR Protoc 2:100438. https://doi.org/10.1016/j.xpro.2021.100438

    Article  PubMed  PubMed Central  Google Scholar 

  • Li YP, Liu H, Jin ZB (2020) Generation of three human iPSC lines from a retinitis pigmentosa family with SLC7A14 mutation. Stem Cell Res 49:102075. https://doi.org/10.1016/j.scr.2020.102075

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Zeng Y, Chen X, Li Q, Wu W, Xue L, Xu H, Yin ZQ (2016) Neural stem cells transplanted to the subretinal space of rd1 mice delay retinal degeneration by suppressing microglia activation. Cytotherapy 18:771–784. https://doi.org/10.1016/j.jcyt.2016.03.001

    Article  CAS  PubMed  Google Scholar 

  • Limoli PG, Limoli CSS, Morales MU, Vingolo EM (2020) Mesenchymal stem cell surgery, rescue and regeneration in retinitis pigmentosa: clinical and rehabilitative prognostic aspects. Restor Neurol Neurosci. https://doi.org/10.3233/rnn-190970

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Lillywhite J, Zhu W, Huang Z, Clark AM, Gosstola N, Maguire CT, Dykxhoorn D, Chen ZY, Yang J (2021) Generation and genetic correction of USH2A c.2299delG mutation in patient-derived induced pluripotent stem cells. Genes (Basel) 12. https://doi.org/10.3390/genes12060805

  • Liu Y, Chen SJ, Li SY, Qu LH, Meng XH, Wang Y, Xu HW, Liang ZQ, Yin ZQ (2017) Long-term safety of human retinal progenitor cell transplantation in retinitis pigmentosa patients. Stem Cell Res Ther 8:209. https://doi.org/10.1186/s13287-017-0661-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu B, Wang S, Girman S, McGill T, Ragaglia V, Lund R (2010) Human adult bone marrow-derived somatic cells rescue vision in a rodent model of retinal degeneration. Exp Eye Res 91:449–455

    CAS  PubMed  Google Scholar 

  • Lund RD, Wang S, Lu B, Girman S, Holmes T, Sauve Y, Messina DJ, Harris IR, Kihm AJ, Harmon AM (2007) Cells isolated from umbilical cord tissue rescue photoreceptors and visual functions in a rodent model of retinal disease. Stem Cells 25:602–611

    CAS  PubMed  Google Scholar 

  • Mahmoudian-Sani MR, Forouzanfar F, Asgharzade S, Ghorbani N (2019) Overexpression of MiR-183/96/182 triggers retina-like fate in human bone marrow-derived mesenchymal stem cells (hBMSCs) in culture. J Ophthalmol 2019. https://doi.org/10.1155/2019/2454362

  • Mangunsong C, Putera B, Haifa R, Suwandjaja M, Sharina A, Sasongko MB, Wirohadidjojo YW (2019) Safety issues of peribulbar injection of umbilical cord mesenchymal stem cell (UC-MSC) in patients with retinitis pigmentosa. Cytotherapy 21:S83. https://doi.org/10.1016/j.jcyt.2019.03.500

    Article  Google Scholar 

  • Mannino G, Russo C, Longo A, Anfuso CD, Lupo G, Lo Furno D, Giuffrida R, Giurdanella G (2021) Potential therapeutic applications of mesenchymal stem cells for the treatment of eye diseases. World J Stem Cells 13:632–644. https://doi.org/10.4252/wjsc.v13.i6.632

    Article  PubMed  PubMed Central  Google Scholar 

  • Marshall C, Lu C, Winstead W, Zhang X, Xiao M, Harding G, Klueber K, Roisen FJ (2006) The therapeutic potential of human olfactory-derived stem cells

  • Matoba S, Zhang Y (2018) Somatic cell nuclear transfer reprogramming: mechanisms and applications cell. Stem Cell 23:471–485. https://doi.org/10.1016/j.stem.2018.06.018

    Article  CAS  Google Scholar 

  • McGill TJ, Osborne L, Lu B, Stoddard J, Huhn S, Tsukamoto A, Capela A (2019) Subretinal transplantation of human central nervous system stem cells stimulates controlled proliferation of endogenous retinal pigment epithelium. Translational Vision Sci Technol 8. https://doi.org/10.1167/tvst.8.3.43

  • Meyer JS, Shearer RL, Capowski EE, Wright LS, Wallace KA, McMillan EL, Zhang S-C, Gamm DM (2009) Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc Natl Acad Sci 106:16698–16703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mollick T, Mohlin C, Johansson K (2016) Human neural progenitor cells decrease photoreceptor degeneration, normalize opsin distribution and support synapse structure in cultured porcine retina. Brain Res 1646:522–534. https://doi.org/10.1016/j.brainres.2016.06.039

    Article  CAS  PubMed  Google Scholar 

  • Moon SY, Zhang D, Chen SC, Lamey TM, Thompson JA, McLaren TL, De Roach JN, Chen FK, McLenachan S (2021) Generation of two induced pluripotent stem cell lines from a retinitis pigmentosa patient with compound heterozygous mutations in CRB1. Stem Cell Res 54:102403. https://doi.org/10.1016/j.scr.2021.102403

    Article  CAS  PubMed  Google Scholar 

  • Musarella MA, Macdonald IM (2011) Current concepts in the treatment of retinitis pigmentosa. J Ophthalmol 2011:753547–753547. https://doi.org/10.1155/2011/753547

    Article  PubMed  Google Scholar 

  • Nadri S, Kazemi B, Eeslaminejad MB, Yazdani S, Soleimani M (2013a) High yield of cells committed to the photoreceptor-like cells from conjunctiva mesenchymal stem cells on nanofibrous scaffolds. Mol Biol Rep 40:3883–3890

    CAS  PubMed  Google Scholar 

  • Nadri S, Yazdani S, Arefian E, Gohari Z, Eslaminejad MB, Kazemi B, Soleimani M (2013b) Mesenchymal stem cells from trabecular meshwork become photoreceptor-like cells on amniotic membrane. Neurosci Lett 541:43–48

    CAS  PubMed  Google Scholar 

  • Ng TK, Fortino VR, Pelaez D, Cheung HS (2014) Progress of mesenchymal stem cell therapy for neural and retinal diseases. World J Stem Cells 6:111–119

    PubMed  PubMed Central  Google Scholar 

  • Öner A (2018) Stem cell treatment in retinal diseases: recent developments. Turkish Journal of Ophthalmology 48:33–38. https://doi.org/10.4274/tjo.89972

    Article  PubMed  PubMed Central  Google Scholar 

  • Özmert E, Arslan U (2020) Management of retinitis pigmentosa by Wharton’s jelly-derived mesenchymal stem cells: prospective analysis of 1-year results. Stem Cell Res Ther 11:353. https://doi.org/10.1186/s13287-020-01870-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patrizi C, Llado M, Benati D, Iodice C, Marrocco E, Guarascio R, Surace EM, Cheetham ME, Auricchio A, Recchia A (2021) Allele-specific editing ameliorates dominant retinitis pigmentosa in a transgenic mouse model. Am J Hum Genet 108:295–308. https://doi.org/10.1016/j.ajhg.2021.01.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Y, Zhang Y, Huang B, Luo Y, Zhang M, Li K, Li W, Wen W, Tang S (2014) Survival and migration of pre-induced adult human peripheral blood mononuclear cells in retinal degeneration slow (rds) mice three months after subretinal transplantation. Curr Stem Cell Res Ther 9:124–133

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petrs-Silva H, Linden R (2014) Advances in gene therapy technologies to treat retinitis pigmentosa. Clin Ophthalmol 8:e136

  • Prado DA, Acosta-Acero M, Maldonado RS (2020) Gene therapy beyond luxturna: a new horizon of the treatment for inherited retinal disease. Curr Opin Ophthalmol 31:147–154. https://doi.org/10.1097/icu.0000000000000660

    Article  PubMed  Google Scholar 

  • Qiang S, Alsaeedi HA, Yuhong C, Yang H, Tong L, Kumar S, Higuchi A, Alarfaj AA, Munisvaradass R, Ling MP, Cheng P (2018) Morphological and genetical changes of endothelial progenitor cells after in-vitro conversion into photoreceptors. J Photochem Photobiol B 183:127–132. https://doi.org/10.1016/j.jphotobiol.2018.04.003

    Article  CAS  PubMed  Google Scholar 

  • Qiu G, Seiler MJ, Mui C, Arai S, Aramant RB, de Juan E, Sadda S (2005) Photoreceptor differentiation and integration of retinal progenitor cells transplanted into transgenic rats. Exp Eye Res 80:515–525

    CAS  PubMed  Google Scholar 

  • Qu L, Gao L, Xu H, Duan P, Zeng Y, Liu Y, Yin ZQ (2017) Combined transplantation of human mesenchymal stem cells and human retinal progenitor cells into the subretinal space of RCS rats. Sci Rep 7. https://doi.org/10.1038/s41598-017-00241-5

  • Radtke ND, Aramant RB, Petry HM, Green PT, Pidwell DJ, Seiler MJ (2008) Vision improvement in retinal degeneration patients by implantation of retina together with retinal pigment epithelium. American journal of ophthalmology 146:172–182. e171

  • Ramlogan-Steel CA, Murali A, Andrzejewski S, Dhungel B, Steel JC, Layton CJ (2019) Gene therapy and the adeno-associated virus in the treatment of genetic and acquired ophthalmic diseases in humans: trials, future directions and safety considerations. Clin Exp Ophthalmol 47:521–536. https://doi.org/10.1111/ceo.13416

    Article  PubMed  Google Scholar 

  • Ramsden CM, Powner MB, Carr A-JF, Smart MJ, da Cruz L, Coffey PJ (2013) Stem cells in retinal regeneration: past, present and future. Development 140:2576–2585

    CAS  PubMed  PubMed Central  Google Scholar 

  • Riera M, Patel A, Corcostegui B, Chang S, Corneo B, Sparrow JR, Pomares E (2019a) Generation of an induced pluripotent stem cell line (FRIMOi002-A) from a retinitis pigmentosa patient carrying compound heterozygous mutations in USH2A gene. Stem Cell Res 35:101386. https://doi.org/10.1016/j.scr.2019.101386

    Article  CAS  PubMed  Google Scholar 

  • Riera M, Patel A, Corcostegui B, Chang S, Sparrow JR, Pomares E, Corneo B (2019b) Establishment and characterization of an iPSC line (FRIMOi001-A) derived from a retinitis pigmentosa patient carrying PDE6A mutations. Stem Cell Res 35:101385. https://doi.org/10.1016/j.scr.2019.101385

    Article  CAS  PubMed  Google Scholar 

  • Rowland TJ, Buchholz DE, Clegg DO (2012) Pluripotent human stem cells for the treatment of retinal disease. J Cell Physiol 227:457–466

    CAS  PubMed  Google Scholar 

  • Russell S, Bennett J, Wellman JA, Chung DC, Yu ZF, Tillman A, Wittes J, Pappas J, Elci O, McCague S, Cross D, Marshall KA, Walshire J, Kehoe TL, Reichert H, Davis M, Raffini L, George LA, Hudson FP, Dingfield L, Zhu X, Haller JA, Sohn EH, Mahajan VB, Pfeifer W, Weckmann M, Johnson C, Gewaily D, Drack A, Stone E, Wachtel K, Simonelli F, Leroy BP, Wright JF, High KA, Maguire AM (2017) Efficacy and safety of voretigene neparvovec (AAV2-hRPE65v2) in patients with RPE65-mediated inherited retinal dystrophy: a randomised, controlled, open-label, phase 3 trial. Lancet 390:849–860. https://doi.org/10.1016/s0140-6736(17)31868-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanjurjo-Soriano C, Erkilic N, Manes G, Dubois G, Hamel CP, Meunier I, Kalatzis V (2018) Generation of an iPSC line, INMi001-A, carrying the two most common USH2A mutations from a compound heterozygote with non-syndromic retinitis pigmentosa. Stem Cell Res 33:228–232. https://doi.org/10.1016/j.scr.2018.11.004

    Article  CAS  PubMed  Google Scholar 

  • Sarkar H, Méjécase C, Harding P, Eintracht J, Toualbi L, Cunha DL, Moosajee M (2021) Generation of two human iPSC lines from patients with autosomal dominant retinitis pigmentosa (UCLi014-A) and autosomal recessive Leber congenital amaurosis (UCLi015-A), associated with RDH12 variants. Stem Cell Res 54:102449. https://doi.org/10.1016/j.scr.2021.102449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satarian L, Nourinia R, Safi S, Kanavi MR, Jarughi N, Daftarian N, Arab L, Aghdami N, Ahmadieh H, Baharvand H (2017) Intravitreal injection of bone marrow mesenchymal stem cells in patients with advanced retinitis pigmentosa; a safety study. J Ophthalmic vis Res 12:58–64. https://doi.org/10.4103/2008-322X.200164

    Article  PubMed  PubMed Central  Google Scholar 

  • Schallenberg M, Charalambous P, Thanos S (2012) GM-CSF protects rat photoreceptors from death by activating the SRC-dependent signalling and elevating anti-apoptotic factors and neurotrophins. Graefes Arch Clin Exp Ophthalmol 250:699–712. https://doi.org/10.1007/s00417-012-1932-9

    Article  CAS  PubMed  Google Scholar 

  • Schatz A, Pach J, Gosheva M, Naycheva L, Willmann G, Wilhelm B, Peters T, Bartz-Schmidt KU, Zrenner E, Messias A, Gekeler F (2017) Transcorneal electrical stimulation for patients with retinitis pigmentosa: a prospective, randomized, sham-controlled follow-up study over 1 year. Invest Ophthalmol vis Sci 58:257–269. https://doi.org/10.1167/iovs.16-19906

    Article  PubMed  Google Scholar 

  • Seiler MJ, Aramant RB (2012) Cell replacement and visual restoration by retinal sheet transplants. Prog Retin Eye Res 31:661–687

    PubMed  PubMed Central  Google Scholar 

  • Semba R, Dagnelie G (2003) Are lutein and zeaxanthin conditionally essential nutrients for eye health? Med Hypotheses 61:465–472. https://doi.org/10.1016/S0306-9877(03)00198-1

    Article  CAS  PubMed  Google Scholar 

  • Shirai H, Mandai M, Matsushita K, Kuwahara A, Yonemura S, Nakano T, Assawachananont J, Kimura T, Saito K, Terasaki H (2016) Transplantation of human embryonic stem cell-derived retinal tissue in two primate models of retinal degeneration. Proc Natl Acad Sci 113:E81–E90

    CAS  PubMed  Google Scholar 

  • Sieving PA, Caruso RC, Tao W, Coleman HR, Thompson DJ, Fullmer KR, Bush RA (2006) Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants. Proc Natl Acad Sci U S A 103:3896–3901. https://doi.org/10.1073/pnas.0600236103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh MS, Issa PC, Butler R, Martin C, Lipinski DM, Sekaran S, Barnard AR, MacLaren RE (2013) Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. Proc Natl Acad Sci 110:1101–1106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Singh RK, Winkler PA, Binette F, Petersen-Jones SM, Nasonkin IO (2021) Comparison of developmental dynamics in human fetal retina and human pluripotent stem cell-derived retinal tissue. Stem Cells Dev 30:399–417. https://doi.org/10.1089/scd.2020.0085

    Article  CAS  PubMed  Google Scholar 

  • Siqueira RC, Messias A, Voltarelli JC, Scott IU, Jorge R (2011) Intravitreal injection of autologous bone marrow–derived mononuclear cells for hereditary retinal dystrophy: a phase I trial. Retina 31:1207–1214

    PubMed  Google Scholar 

  • Smith LE (2004) Bone marrow–derived stem cells preserve cone vision in retinitis pigmentosa. J Clin Investig 114:755–757

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soleimannejad M, Ebrahimi-Barough S, Nadri S, Riazi-Esfahani M, Soleimani M, Tavangar SM, Ai J (2017) Retina tissue engineering by conjunctiva mesenchymal stem cells encapsulated in fibrin gel: hypotheses on novel approach to retinal diseases treatment. Med Hypotheses 101:75–77. https://doi.org/10.1016/j.mehy.2017.02.019

    Article  CAS  PubMed  Google Scholar 

  • Song C, Conlon TJ, Deng WT, Coleman KE, Zhu P, Plummer C, Mandapati S, Van Hoosear M, Green KB, Sonnentag P, Sharma AK, Timmers A, Robinson PM, Knop DR, Hauswirth WW, Chulay JD, Shearman MS, Ye GJ (2018) Toxicology and pharmacology of an AAV vector expressing codon-optimized RPGR in RPGR-deficient Rd9 mice. Hum Gene Ther Clin Dev 29:188–197. https://doi.org/10.1089/humc.2018.168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Souied EH, Reid SN, Piri NI, Lerner LE, Nusinowitz S, Farber DB (2008) Non-invasive gene transfer by iontophoresis for therapy of an inherited retinal degeneration. Exp Eye Res 87:168–175. https://doi.org/10.1016/j.exer.2008.04.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stingl K, Bartz-Schmidt KU, Besch D, Chee CK, Cottriall CL, Gekeler F, Groppe M, Jackson TL, MacLaren RE, Koitschev A, Kusnyerik A, Neffendorf J, Nemeth J, Naeem MAN, Peters T, Ramsden JD, Sachs H, Simpson A, Singh MS, Wilhelm B, Wong D, Zrenner E (2015) Subretinal visual implant alpha IMS – clinical trial interim report. Vision Res 111:149–160. https://doi.org/10.1016/j.visres.2015.03.001

    Article  PubMed  Google Scholar 

  • Svendsen CN, Caldwell MA, Shen J, ter Borg MG, Rosser AE, Tyers P, Karmiol S, Dunnett SB (1997) Long-term survival of human central nervous system progenitor cells transplanted into a rat model of Parkinson’s disease. Exp Neurol 148:135–146

    CAS  PubMed  Google Scholar 

  • Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676. https://doi.org/10.1016/j.cell.2006.07.024

    Article  CAS  PubMed  Google Scholar 

  • Takahashi VKL, Takiuti JT, Jauregui R, Tsang SH (2018) Gene therapy in inherited retinal degenerative diseases, a review. Ophthalmic Genet 39:560–568. https://doi.org/10.1080/13816810.2018.1495745

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Chen Z, Tan X, Luo L, Liu X, Gong L, Li DW, Liu Y (2020a) Generation of a homozygous CRISPR/Cas9-mediated knockout H9 hESC subline for the CRB1 locus. Stem Cell Res 49:102057. https://doi.org/10.1016/j.scr.2020.102057

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Liu X, Chen Z, Luo L, Liu X, Deng J, Li DWC, Liu Y (2020b) Using inducible lentiviral vectors to generate induced pluripotent stem cell line ZOCi001-A from peripheral blood cells of a patient with CRB1−/− retinitis pigmentosa. Stem Cell Res 45. https://doi.org/10.1016/j.scr.2020.101817

  • Tang Z, Zhang Y, Wang Y, Zhang D, Shen B, Luo M, Gu P (2017) Progress of stem/progenitor cell-based therapy for retinal degeneration. J Transl Med 15. https://doi.org/10.1186/s12967-017-1183-y

  • Tao W, Wen R, Goddard MB, Sherman SD, O’Rourke PJ, Stabila PF, Bell WJ, Dean BJ, Kauper KA, Budz VA (2002) Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinitis pigmentosa. Invest Ophthalmol vis Sci 43:3292–3298

    PubMed  Google Scholar 

  • Telias M, Denlinger B, Helft Z, Thornton C, Beckwith-Cohen B, Kramer RH (2019) Retinoic acid induces hyperactivity, and blocking its receptor unmasks light responses and augments vision in retinal degeneration. Neuron 102:574-586.e575. https://doi.org/10.1016/j.neuron.2019.02.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrell D, Comander J (2019) Current stem-cell approaches for the treatment of inherited retinal degenerations. Semin Ophthalmol 34:287–292. https://doi.org/10.1080/08820538.2019.1620808

    Article  PubMed  Google Scholar 

  • Tu HY, Watanabe T, Shirai H, Yamasaki S, Kinoshita M, Matsushita K, Hashiguchi T, Onoe H, Matsuyama T, Kuwahara A, Kishino A, Kimura T, Eiraku M, Suzuma K, Kitaoka T, Takahashi M, Mandai M (2019) Medium- to long-term survival and functional examination of human iPSC-derived retinas in rat and primate models of retinal degeneration. EBioMedicine 39:562–574. https://doi.org/10.1016/j.ebiom.2018.11.028

    Article  PubMed  Google Scholar 

  • Tucker BA, Mullins RF, Streb LM, Anfinson K, Eyestone ME, Kaalberg E, Riker MJ, Drack AV, Braun TA, Stone EM (2013) Patient-specific iPSC-derived photoreceptor precursor cells as a means to investigate retinitis pigmentosa. Elife 2:e00824

  • Tuekprakhon A, Sangkitporn S, Trinavarat A, Pawestri AR, Vamvanij V, Ruangchainikom M, Luksanapruksa P, Pongpaksupasin P, Khorchai A, Dambua A, Boonchu P, Yodtup C, Uiprasertkul M, Sangkitporn S, Atchaneeyasakul LO (2021) Intravitreal autologous mesenchymal stem cell transplantation: a non-randomized phase I clinical trial in patients with retinitis pigmentosa. Stem Cell Res Ther 12:52. https://doi.org/10.1186/s13287-020-02122-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzameret A, Sher I, Belkin M, Treves AJ, Meir A, Nagler A, Levkovitch-Verbin H, Barshack I, Rosner M, Rotenstreich Y (2014) Transplantation of human bone marrow mesenchymal stem cells as a thin subretinal layer ameliorates retinal degeneration in a rat model of retinal dystrophy. Exp Eye Res 118:135–144

    CAS  PubMed  Google Scholar 

  • Uy H, Chan PS, Cruz FM (2013) Stem cell therapy: a novel approach for vision restoration in retinitis pigmentosa. Medical Hypothesis, Discovery & Innovation Ophthalmology Journal 2:52

    Google Scholar 

  • Vandenberghe L, Auricchio A (2012) Novel adeno-associated viral vectors for retinal gene therapy. Gene Ther 19:162–168

    CAS  PubMed  Google Scholar 

  • Wang N-K, Tosi J, Kasanuki JM, Chou CL, Kong J, Parmalee N, Wert KJ, Allikmets R, Lai C-C, Chien C-L (2010a) Transplantation of reprogrammed embryonic stem cells improves visual function in a mouse model for retinitis pigmentosa. Transplantation 89:911

    PubMed  PubMed Central  Google Scholar 

  • Wang S, Girman S, Lu B, Bischoff N, Holmes T, Shearer R, Wright LS, Svendsen CN, Gamm DM, Lund RD (2008) Long-term vision rescue by human neural progenitors in a rat model of photoreceptor degeneration. Invest Ophthalmol vis Sci 49:3201–3206

    PubMed  Google Scholar 

  • Wang S, Lu B, Girman S, Duan J, McFarland T, Zhang Q-s, Grompe M, Adamus G, Appukuttan B, Lund R (2010b) Non-invasive stem cell therapy in a rat model for retinal degeneration and vascular pathology. PloS one 5:e9200

  • Warfvinge K, Kiilgaard JF, Lavik EB, Scherfig E, Langer R, Klassen HJ, Young MJ (2005) Retinal progenitor cell xenografts to the pig retina: morphologic integration and cytochemical differentiation. Arch Ophthalmol 123:1385–1393

    PubMed  Google Scholar 

  • Weiss JN, Levy S (2018) Stem cell ophthalmology treatment study: bone marrow derived stem cells in the treatment of retinitis pigmentosa. Stem Cell Invest 5. https://doi.org/10.21037/sci.2018.04.02

  • Weiss JN, Levy S (2019) Stem cell Ophthalmology Treatment Study (SCOTS): bone marrow derived stem cells in the treatment of Usher syndrome. Stem Cell Invest 6. https://doi.org/10.21037/sci.2019.08.07

  • Wheaton DH, Hoffman DR, Locke KG, Watkins RB, Birch DG (2003) Biological safety assessment of docosahexaenoic acid supplementation in a randomized clinical trial for X-linked retinitis pigmentosa. Arch Ophthalmol 121:1269–1278

    CAS  PubMed  Google Scholar 

  • Xie J, Huo S, Li Y, Dai J, Xu H, Yin ZQ (2017) Olfactory ensheathing cells inhibit gliosis in retinal degeneration by downregulation of the müller cell notch signaling pathway. Cell Transplant 26:967–982. https://doi.org/10.3727/096368917X694994

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie J, Li Y, Dai J, He Y, Sun D, Dai C, Xu H, Yin ZQ (2019) Olfactory ensheathing cells grafted into the retina of RCS rats suppress inflammation by down-regulating the JAK/STAT pathway. Front Cell Neurosci 13:341. https://doi.org/10.3389/fncel.2019.00341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue L, Zeng Y, Li Q, Li Y, Li Z, Xu H, Yin Z (2017) Transplanted Olfactory Ensheathing Cells Restore Retinal Function in a Rat Model of Light-Induced Retinal Damage by Inhibiting Oxidative Stress Oncotarget 8:93087–93102. https://doi.org/10.18632/oncotarget.21857

    Article  Google Scholar 

  • Yamasaki S, Sugita S, Horiuchi M, Masuda T, Fujii S, Makabe K, Kawasaki A, Hayashi T, Kuwahara A, Kishino A, Kimura T, Takahashi M, Mandai M (2021) Low immunogenicity and immunosuppressive properties of human ESC- and iPSC-derived retinas. Stem Cell Reports 16:851–867. https://doi.org/10.1016/j.stemcr.2021.02.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yanai A, Laver C, Joe AW, Gregory-Evans K (2016) Efficient production of photoreceptor precursor cells from human embryonic stem cells. Human Embryonic Stem Cell Protocols 357–369

  • Yang J, Xie M, Zheng W, Hu J, Qu Q (2016) Therapeutical effect of growth-associated protein 43 (GAP43) gene-modified bone marrow mesenchymal stem cell transplantation on rat retinal degenerative diseases. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi 32:1041–1044

    PubMed  Google Scholar 

  • Yoshida T, Ozawa Y, Suzuki K, Yuki K, Ohyama M, Akamatsu W, Matsuzaki Y, Shimmura S, Mitani K, Tsubota K (2014) The use of induced pluripotent stem cells to reveal pathogenic gene mutations and explore treatments for retinitis pigmentosa. Mol Brain 7:1

    Google Scholar 

  • Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917–1920

    CAS  PubMed  Google Scholar 

  • Zerti D, Dorgau B, Felemban M, Ghareeb AE, Yu M, Ding Y, Krasnogor N, Lako M (2020) Developing a simple method to enhance the generation of cone and rod photoreceptors in pluripotent stem cell-derived retinal organoids. Stem Cells (dayton, Ohio) 38:45–51. https://doi.org/10.1002/stem.3082

    Article  CAS  Google Scholar 

  • Zhai W, Gao L, Qu L, Li Y, Zeng Y, Li Q, Xu H, Yin ZQ (2020) Combined transplantation of olfactory ensheathing cells with rat neural stem cells enhanced the therapeutic effect in the retina of RCS rats. Front Cell Neurosci 14:52. https://doi.org/10.3389/fncel.2020.00052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao T, Liang Q, Meng X, Duan P, Wang F, Li S, Liu Y, Yin ZQ (2020) Intravenous infusion of umbilical cord mesenchymal stem cells maintains and partially improves visual function in patients with advanced retinitis pigmentosa. Stem Cells Dev 29:1029–1037. https://doi.org/10.1089/scd.2020.0037

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Das AV, Bhattacharya S, Thoreson WB, Sierra JR, Mallya KB, Ahmad I (2008) Derivation of neurons with functional properties from adult limbal epithelium: implications in autologous cell therapy for photoreceptor degeneration. Stem Cells 26:939–949

    CAS  PubMed  Google Scholar 

  • Zhao Y, Feng K, Liu R, Pan J, Zhang L, Lu X (2019) Vitamins and mineral supplements for retinitis pigmentosa. Journal of Ophthalmology 2019:8524607. https://doi.org/10.1155/2019/8524607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Y, Ding C, Xia S, Jing Y, Mao S, Liu J, Chen J, Chan HF, Tang S, Chen J (2020) Establishment of induced pluripotent stem cell line CSUASOi003- a from an autosomal recessive retinitis pigmentosa patient carrying compound heterozygous mutations in CRB1 gene. Stem Cell Res 44:101742. https://doi.org/10.1016/j.scr.2020.101742

  • Zhu D, Xie M, Gademann F, Cao J, Wang P, Guo Y, Zhang L, Su T, Zhang J, Chen J (2020) Protective effects of human iPS-derived retinal pigmented epithelial cells on retinal degenerative disease. Stem Cell Res Ther 11:98. https://doi.org/10.1186/s13287-020-01608-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Cifuentes H, Reynolds J, Lamba DA (2017) Immunosuppression via loss of IL2rγ enhances long-term functional integration of hESC-derived photoreceptors in the mouse retina cell. Stem Cell 20:374-384.e375. https://doi.org/10.1016/j.stem.2016.11.019

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to appreciate Dr. Shamoei Wang and Dr. Robert MacLaren for their kind cooperation as the expert reviewer.

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Hosseini Shabanan, S., Seyedmirzaei, H., Barnea, A. et al. Stem cell transplantation as a progressing treatment for retinitis pigmentosa. Cell Tissue Res 387, 177–205 (2022). https://doi.org/10.1007/s00441-021-03551-3

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