Advances of stem cell transplantation in the treatment of retinal degeneration_Chinese Journal of Ocular Fundus Diseases

Authors：

Sun Na , Gu Ping ,  Ji Jing

Department of Ophthalmology, Ninth People’s Hospital, Shanghai Jiaotong University School of Medicine 200011, China;

Corresponding author：

Ji Jing, Email: flowerrainday@sina.com

Keywords：

Retinal diseases/therapy; Embryonic stem cells; Adult stem cells; Review

DOI：

10.3760/cma.j.issn.1005-1015.2018.06.021

Video：

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Abstract Full text Figures/Tables Video References Cited by

Retinal degeneration mainly include age-related macular degeneration, retinitispigmentosa and Stargardt’s disease. Although its expression is slightly different, its pathogenesis is photoreceptor cells and/or retinal pigment epithelial (RPE) cel1 damage or degeneration. Because of the 1ack of self-repairing and renewal of retinal photoreceptor cells and RPE cells, cell replacement therapy is one of the most effective methods for treating such diseases.The stem cells currently used for the treatment of retinal degeneration include embryonicstem cells (ESC) and various adult stem cells, such as retinal stem cells (RSC), induced pluripotent stem cells (iPSC). and mesenchyma1 stem cells (MSC). Understanding the currentbasic and clinical application progress of ESC, iPSC, RSC, MSC can provide a new idea for the treatment of retinal degeneration.

Citation： Sun Na, Gu Ping, Ji Jing. Advances of stem cell transplantation in the treatment of retinal degeneration. Chinese Journal of Ocular Fundus Diseases, 2018, 34(6): 613-617. doi: 10.3760/cma.j.issn.1005-1015.2018.06.021 Copy

1.	Wiley LA, Burnight ER, Songstad AE, et al. Patient-specific induced pluripotent stem cells (iPSCs) for the study and treatment of retinal degenerative diseases[J]. Prog Retin Eye Res, 2015, 44: 15-35. DOI: 10.1016/j.preteyeres.2014.10.002.
2.	Tropepe V, Coles BLK, Chiasson BJ, et al. Retinal stem cells in the adult mammalian eye[J]. Science, 2000, 287(5460): 2032-2036.
3.	Coles BL, Angenieux B, Inoue T, et al. Facile isolation and the characterization of human retinal stem cells[J]. Proc Natl Acad Sci USA, 2004, 101(44): 15772-15777. DOI: 10.1073/pnas.0401596101.
4.	Klassen H, Kiilgaard JF, Zahir T, et al. Progenitor cells from the porcine neural retina express photoreceptor markers after transplantation to the subretinal space of allorecipients[J]. Stem Cells, 2007, 25(5): 1222-1230. DOI: 10.1634/stemcells.2006-0541.
5.	Seiler MJ, Aramant RB, Seeliger MW, et al. Functional and structural assessment of retinal sheet allograft transplantation in feline hereditary retinal degeneration[J]. Vet Ophthalmol, 2009, 12(3): 158-169. DOI: 10.1111/j.1463-5224.2009.00693.x.
6.	Li T, Lewallen M, Chen S, et al. Multipotent stem cells isolated from the adult mouse retina are capable of producing functional photoreceptor cells[J]. Cell Res, 2013, 23(6): 788-802. DOI: 10.1038/cr.2013.48.
7.	Radtke ND, Aramant RB, Seiler M, et al. Preliminary report: indications of improved visual function after retinal sheet transplantation in retinitis pigmentosa patients[J]. Am J Ophthalmol, 1999, 128(3): 384-387.
8.	Tang Z, Zhang Y, Wang Y, et al. Progress of stem/progenitor cell-based therapy for retinal degeneration[J]. J Transl Med, 2017, 15(1): 99. DOI: 10.1186/s12967-017-1183-y.
9.	Ikeda H, Osakada F, Watanabe K, et al. Generation of Rx+/Pax6+neural retinal precursors from embryonic stem cells[J]. Proc Natl Acad Sci USA, 2005, 102(32): 11331-11336. DOI: 10.1073/pnas.0500010102.
10.	Lamba DA, Karl MO, Ware CB, et al. Efficient generation of retinal progenitor cells from human embryonic stem cells[J].Proc Natl Acad Sci USA, 2006, 103(34): 12769-12774. DOI: 10.1073/pnas.0601990103.
11.	Osakada F, Ikeda H, Mandai M, et al. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells[J]. Nat Biotechnol, 2008, 26(2): 215-224. DOI: 10.1038/nbt1384.
12.	Amirpour N, Karamali F, Rabiee F, et al. Differentiation of human embryonic stem cell-derived retinal progenitors into retinal cells by Sonic hedgehog and/or retinal pigmented epithelium and transplantation into the subretinal space of sodium iodate-injected rabbits[J]. Stem Cells Dev, 2012, 21(1): 42-53. DOI: 10.1089/scd.2011.0073.
13.	Garcia JM, Mendonca L, Brant R, et al. Stem cell therapy for retinal diseases[J]. World J Stem Cells, 2015, 7(1): 160-164. DOI: 10.4252/wjsc.v7.i1.160.
14.	Schwartz SD, Hubschman JP, Heilwell G, et al. Embryonic stem cell trials for macular degeneration: a preliminary report[J]. Lancet, 2012, 379(9817): 713-720. DOI: 10.1016/s0140-6736(12)60028-2.
15.	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[J]. Lancet, 2015, 385(9967): 509-516. DOI: 10.1016/s0140-6736(14)61376-3.
16.	Song Won K, Park KM, Kim HJ, et al. Treatment of macular degeneration using embryonic stem cell-derived retinal pigment epithelium: preliminary results in asian patients[J]. Stem Cell Reports, 2015, 4(5): 860-872. DOI: https://doi.org/10.1016/j.stemcr.2015.04.005.
17.	Yin ZQ, Liu Y, Li S, et al. Clincal trial: subretinal transplantation of CTS hESC derived RPE in the treatment of wet age-related macular degeneration (wAMD)[J]. Invest Ophthalmol Vis Sci, 2016, 57(12): 3742.
18.	Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors[J]. Cell, 2006, 126(4): 663-676. DOI: 10.1016/j.cell.2006.07.024.
19.	Lamba DA, McUsic A, Hirata RK, et al. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells[J/OL]. PLoS One, 2010, 5(1): 8763[2010-01-20]. https://doi.org/10.1371/journal.pone.0008763. DOI: 10.1371/journal.pone.0008763.
20.	Chakradhar S. An eye to the future: researchers debate best path for stem cell-derived therapies[J]. Nat Med, 2016, 22(2): 116-119. DOI: 10.1038/nm0216-116.
21.	Mandai M, Watanabe A, Kurimoto Y, et al. Autologous induced stem-cell-derived retinal cells for macular degeneration[J]. N Engl J Med, 2017, 376(11): 1038-1046. DOI: 10.1056/NEJMoa1608368.
22.	Sugita S, Iwasaki Y, Makabe K, et al. Successful transplantation of retinal pigment epithelial cells from mhc homozygote iPSCs in MHC-matched models[J]. Stem Cell Reports, 2016, 7(4): 635-648. DOI: 10.1016/j.stemcr.2016.08.010.
23.	Chung J, Park T, Ohn Y, et al. Modulation of retinal wound healing by systemically administered bone marrow-derived mesenchymal stem cells[J]. Korean J Ophthalmol, 2011, 25(4): 268-274. DOI: 10.3341/kjo.2011.25.4.268.
24.	Tomita M, Mori T, Maruyama K, et al. A comparison of neural differentiation and retinal transplantation with bone marrow-derived cells and retinal progenitor cells[J]. Stem Cells, 2006, 24(10): 2270-2278. DOI: 10.1634/stemcells.2005-0507.
25.	Mead B, Logan A, Berry M, et al. Concise review: dental pulp stem cells: a novel cell therapy for retinal and central nervous system repair[J]. Stem Cells, 2017, 35(1): 61-67. DOI: 10.1002/stem.2398.
26.	Mead B, Logan A, Berry M, et al. Intravitreally transplanted dental pulp stem cells promote neuroprotection and axon regeneration of retinal ganglion cells after optic nerve injury[J]. Invest Ophthalmol Vis Sci, 2013, 54(12): 7544-7556. DOI: 10.1167/iovs.13-13045.
27.	Bray AF, Cevallos RR, Gazarian K, et al. Human dental pulp stem cells respond to cues from the rat retina and differentiate to express the retinal neuronal marker rhodopsin[J]. Neuroscience, 2014, 280: 142-155. DOI: 10.1016/j.neuroscience.2014.09.023.
28.	Rahimzadeh A, Mirakabad FS, Movassaghpour A, et al. Biotechnological and biomedical applications of mesenchymal stem cells as a therapeutic system[J]. Artif Cells Nanomed Biotechnol, 2016, 44(2): 559-570. DOI: 10.3109/21691401.2014.968823.
29.	Amirpour N, Amirizade S, Hashemibeni B, et al. Differentiation of eye field neuroectoderm from human adipose-derived stem cells by using small-molecules and hADSC-conditioned medium[J]. Ann Anat, 2018, 221: 17-26. DOI: 10.1016/j.aanat.2018.08.002.
30.	Kuriyan AE, Albini TA, Townsend JH, et al. Vision loss after intravitreal injection of autologous "stem cells" for AMD[J]. N Engl J Med, 2017, 376(11): 1047-1053. DOI: 10.1056/NEJMoa1609583.
31.	Higuchi A, Kumar SS, Benelli G, et al. Stem cell therapies for reversing vision loss[J]. Trends Biotechnol, 2017, 35(11): 1102-1117. DOI: 10.1016/j.tibtech.2017.06.016.
32.	Fukuda S, Nagano M, Yamashita T, et al. Functional endothelial progenitor cells selectively recruit neurovascular protective monocyte-derived F4/80(+)/Ly6c(+) macrophages in a mouse model of retinal degeneration[J]. Stem Cells, 2013, 31(10): 2149-2161. DOI: 10.1002/stem.1469.
33.	Park S, Bauer G, Abedi M, et al. Intravitreal autologous bone marrow CD34+cell therapy for ischemic and degenerative retinal disorders: preliminary phase 1 clinical trial findings[J]. Invest Ophthalmol Vis Sci, 2014, 56(1): 81-89. DOI: 10.1167/iovs.14-15415.
34.	Otteson DC. Talkin’about my (re)generation: The who of intrinsic retinal stem cells[J]. Neuroscience, 2017, 346: 447-449. DOI: https://doi.org/10.1016/j.neuroscience.2017.01.022.
35.	Weinberger L, Ayyash M, Novershtern N, et al. Dynamic stem cell states: naive to primed pluripotency in rodents and humans[J]. Nat Rev Mol Cell Biol, 2016, 17(3): 155-169. DOI: 10.1038/nrm.2015.28.
36.	Santos-Ferreira T, Llonch S, Borsch O, et al. Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange[J]. Nat Commun, 2016, 7: 13028. DOI: 10.1038/ncomms13028.
37.	Lillien L. Changes in retinal cell fate induced by overexpression of EGF receptor[J]. Nature, 1995, 377(6545): 158-162. DOI: 10.1038/377158a0.
38.	Kim J, Wu HH, Lander AD, et al. GDF11 controls the timing of progenitor cell competence in developing retina[J]. Science, 2005, 308(5730): 1927-1930. DOI: 10.1126/science.1110175.
39.	Rosenthal R, Wohlleben H, Malek G, et al. Insulin-like growth factor-1 contributes to neovascularization in age-related macular degeneration[J]. Biochem Biophys Res Commun, 2004, 323(4): 1203-1208. DOI: 10.1016/j.bbrc.2004.08.219.
40.	Xu Y, Balasubramaniam B, Copland DA, et al. Activated adult microglia influence retinal progenitor cell proliferation and differentiation toward recoverin-expressing neuron-like cells in a co-culture model[J]. Graefe’s Arch Clin Exp Ophthalmol, 2015, 253(7): 1085-1096. DOI: 10.1007/s00417-015-2961-y.
41.	Quadrato G, Nguyen T, Macosko EZ, et al. Cell diversity and network dynamics in photosensitive human brain organoids[J]. Nature, 2017, 545(7652): 48-53. DOI: 10.1038/nature22047.
42.	Park SS, Moisseiev E, Bauer G, et al. Advances in bone marrow stem cell therapy for retinal dysfunction[J]. Prog Retin Eye Res, 2017, 56: 148-165. DOI: 10.1016/j.preteyeres.2016.10.002.
43.	Hu Y, Luo M, Ni N, et al. Reciprocal actions of microRNA-9 and TLX in the proliferation and differentiation of retinal progenitor cells[J]. Stem Cells Dev, 2014, 23(22): 2771-2781. DOI: 10.1089/scd.2014.0021.
44.	Ni N, Zhang D, Xie Q, et al. Effects of let-7b and TLX on the proliferation and differentiation of retinal progenitor cells in vitro[J]. Sci Rep, 2014, 4: 6671. DOI: 10.1038/srep06671.
45.	Zhang Y, Yue K, Aleman J, et al. 3D Bioprinting for Tissue and Organ Fabrication[J]. Ann Biomed Eng, 2017, 45(1): 148-163.
46.	Melton C, Judson RL, Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells[J]. Nature, 2010, 463(7281): 621-626. DOI: 10.1038/nature08725.
47.	Banin E, Obolensky A, Idelson M, et al. Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells[J]. Stem Cells, 2006, 24(2): 246-257. DOI: 10.1634/stemcells.2005-0009.
48.	Singh D, Wang SB, Xia T, et al. A biodegradable scaffold enhances differentiation of embryonic stem cells into a thick sheet of retinal cells[J]. Biomaterials, 2018, 154: 158-168. DOI: 10.1016/j.biomaterials.2017.10.052.
49.	Worthington KS, Wiley LA, Kaalberg EE, et al. Two-photon polymerization for production of human iPSC-derived retinal cell grafts[J]. Acta Biomater, 2017, 55: 385-395. DOI: 10.1016/j.actbio.2017.03.039.
50.	Li K, Zhong X, Yang S, et al. HiPSC-derived retinal ganglion cells grow dendritic arbors and functional axons on a tissue-engineered scaffold[J]. Acta Biomater, 2017, 54: 117-127. DOI: 10.1016/j.actbio.2017.02.032.

1. Wiley LA, Burnight ER, Songstad AE, et al. Patient-specific induced pluripotent stem cells (iPSCs) for the study and treatment of retinal degenerative diseases[J]. Prog Retin Eye Res, 2015, 44: 15-35. DOI: 10.1016/j.preteyeres.2014.10.002.
2. Tropepe V, Coles BLK, Chiasson BJ, et al. Retinal stem cells in the adult mammalian eye[J]. Science, 2000, 287(5460): 2032-2036.
3. Coles BL, Angenieux B, Inoue T, et al. Facile isolation and the characterization of human retinal stem cells[J]. Proc Natl Acad Sci USA, 2004, 101(44): 15772-15777. DOI: 10.1073/pnas.0401596101.
4. Klassen H, Kiilgaard JF, Zahir T, et al. Progenitor cells from the porcine neural retina express photoreceptor markers after transplantation to the subretinal space of allorecipients[J]. Stem Cells, 2007, 25(5): 1222-1230. DOI: 10.1634/stemcells.2006-0541.
5. Seiler MJ, Aramant RB, Seeliger MW, et al. Functional and structural assessment of retinal sheet allograft transplantation in feline hereditary retinal degeneration[J]. Vet Ophthalmol, 2009, 12(3): 158-169. DOI: 10.1111/j.1463-5224.2009.00693.x.
6. Li T, Lewallen M, Chen S, et al. Multipotent stem cells isolated from the adult mouse retina are capable of producing functional photoreceptor cells[J]. Cell Res, 2013, 23(6): 788-802. DOI: 10.1038/cr.2013.48.
7. Radtke ND, Aramant RB, Seiler M, et al. Preliminary report: indications of improved visual function after retinal sheet transplantation in retinitis pigmentosa patients[J]. Am J Ophthalmol, 1999, 128(3): 384-387.
8. Tang Z, Zhang Y, Wang Y, et al. Progress of stem/progenitor cell-based therapy for retinal degeneration[J]. J Transl Med, 2017, 15(1): 99. DOI: 10.1186/s12967-017-1183-y.
9. Ikeda H, Osakada F, Watanabe K, et al. Generation of Rx+/Pax6+neural retinal precursors from embryonic stem cells[J]. Proc Natl Acad Sci USA, 2005, 102(32): 11331-11336. DOI: 10.1073/pnas.0500010102.
10. Lamba DA, Karl MO, Ware CB, et al. Efficient generation of retinal progenitor cells from human embryonic stem cells[J].Proc Natl Acad Sci USA, 2006, 103(34): 12769-12774. DOI: 10.1073/pnas.0601990103.
11. Osakada F, Ikeda H, Mandai M, et al. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells[J]. Nat Biotechnol, 2008, 26(2): 215-224. DOI: 10.1038/nbt1384.
12. Amirpour N, Karamali F, Rabiee F, et al. Differentiation of human embryonic stem cell-derived retinal progenitors into retinal cells by Sonic hedgehog and/or retinal pigmented epithelium and transplantation into the subretinal space of sodium iodate-injected rabbits[J]. Stem Cells Dev, 2012, 21(1): 42-53. DOI: 10.1089/scd.2011.0073.
13. Garcia JM, Mendonca L, Brant R, et al. Stem cell therapy for retinal diseases[J]. World J Stem Cells, 2015, 7(1): 160-164. DOI: 10.4252/wjsc.v7.i1.160.
14. Schwartz SD, Hubschman JP, Heilwell G, et al. Embryonic stem cell trials for macular degeneration: a preliminary report[J]. Lancet, 2012, 379(9817): 713-720. DOI: 10.1016/s0140-6736(12)60028-2.
15. 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[J]. Lancet, 2015, 385(9967): 509-516. DOI: 10.1016/s0140-6736(14)61376-3.
16. Song Won K, Park KM, Kim HJ, et al. Treatment of macular degeneration using embryonic stem cell-derived retinal pigment epithelium: preliminary results in asian patients[J]. Stem Cell Reports, 2015, 4(5): 860-872. DOI: https://doi.org/10.1016/j.stemcr.2015.04.005.
17. Yin ZQ, Liu Y, Li S, et al. Clincal trial: subretinal transplantation of CTS hESC derived RPE in the treatment of wet age-related macular degeneration (wAMD)[J]. Invest Ophthalmol Vis Sci, 2016, 57(12): 3742.
18. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors[J]. Cell, 2006, 126(4): 663-676. DOI: 10.1016/j.cell.2006.07.024.
19. Lamba DA, McUsic A, Hirata RK, et al. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells[J/OL]. PLoS One, 2010, 5(1): 8763[2010-01-20]. https://doi.org/10.1371/journal.pone.0008763. DOI: 10.1371/journal.pone.0008763.
20. Chakradhar S. An eye to the future: researchers debate best path for stem cell-derived therapies[J]. Nat Med, 2016, 22(2): 116-119. DOI: 10.1038/nm0216-116.
21. Mandai M, Watanabe A, Kurimoto Y, et al. Autologous induced stem-cell-derived retinal cells for macular degeneration[J]. N Engl J Med, 2017, 376(11): 1038-1046. DOI: 10.1056/NEJMoa1608368.
22. Sugita S, Iwasaki Y, Makabe K, et al. Successful transplantation of retinal pigment epithelial cells from mhc homozygote iPSCs in MHC-matched models[J]. Stem Cell Reports, 2016, 7(4): 635-648. DOI: 10.1016/j.stemcr.2016.08.010.
23. Chung J, Park T, Ohn Y, et al. Modulation of retinal wound healing by systemically administered bone marrow-derived mesenchymal stem cells[J]. Korean J Ophthalmol, 2011, 25(4): 268-274. DOI: 10.3341/kjo.2011.25.4.268.
24. Tomita M, Mori T, Maruyama K, et al. A comparison of neural differentiation and retinal transplantation with bone marrow-derived cells and retinal progenitor cells[J]. Stem Cells, 2006, 24(10): 2270-2278. DOI: 10.1634/stemcells.2005-0507.
25. Mead B, Logan A, Berry M, et al. Concise review: dental pulp stem cells: a novel cell therapy for retinal and central nervous system repair[J]. Stem Cells, 2017, 35(1): 61-67. DOI: 10.1002/stem.2398.
26. Mead B, Logan A, Berry M, et al. Intravitreally transplanted dental pulp stem cells promote neuroprotection and axon regeneration of retinal ganglion cells after optic nerve injury[J]. Invest Ophthalmol Vis Sci, 2013, 54(12): 7544-7556. DOI: 10.1167/iovs.13-13045.
27. Bray AF, Cevallos RR, Gazarian K, et al. Human dental pulp stem cells respond to cues from the rat retina and differentiate to express the retinal neuronal marker rhodopsin[J]. Neuroscience, 2014, 280: 142-155. DOI: 10.1016/j.neuroscience.2014.09.023.
28. Rahimzadeh A, Mirakabad FS, Movassaghpour A, et al. Biotechnological and biomedical applications of mesenchymal stem cells as a therapeutic system[J]. Artif Cells Nanomed Biotechnol, 2016, 44(2): 559-570. DOI: 10.3109/21691401.2014.968823.
29. Amirpour N, Amirizade S, Hashemibeni B, et al. Differentiation of eye field neuroectoderm from human adipose-derived stem cells by using small-molecules and hADSC-conditioned medium[J]. Ann Anat, 2018, 221: 17-26. DOI: 10.1016/j.aanat.2018.08.002.
30. Kuriyan AE, Albini TA, Townsend JH, et al. Vision loss after intravitreal injection of autologous "stem cells" for AMD[J]. N Engl J Med, 2017, 376(11): 1047-1053. DOI: 10.1056/NEJMoa1609583.
31. Higuchi A, Kumar SS, Benelli G, et al. Stem cell therapies for reversing vision loss[J]. Trends Biotechnol, 2017, 35(11): 1102-1117. DOI: 10.1016/j.tibtech.2017.06.016.
32. Fukuda S, Nagano M, Yamashita T, et al. Functional endothelial progenitor cells selectively recruit neurovascular protective monocyte-derived F4/80(+)/Ly6c(+) macrophages in a mouse model of retinal degeneration[J]. Stem Cells, 2013, 31(10): 2149-2161. DOI: 10.1002/stem.1469.
33. Park S, Bauer G, Abedi M, et al. Intravitreal autologous bone marrow CD34+cell therapy for ischemic and degenerative retinal disorders: preliminary phase 1 clinical trial findings[J]. Invest Ophthalmol Vis Sci, 2014, 56(1): 81-89. DOI: 10.1167/iovs.14-15415.
34. Otteson DC. Talkin’about my (re)generation: The who of intrinsic retinal stem cells[J]. Neuroscience, 2017, 346: 447-449. DOI: https://doi.org/10.1016/j.neuroscience.2017.01.022.
35. Weinberger L, Ayyash M, Novershtern N, et al. Dynamic stem cell states: naive to primed pluripotency in rodents and humans[J]. Nat Rev Mol Cell Biol, 2016, 17(3): 155-169. DOI: 10.1038/nrm.2015.28.
36. Santos-Ferreira T, Llonch S, Borsch O, et al. Retinal transplantation of photoreceptors results in donor-host cytoplasmic exchange[J]. Nat Commun, 2016, 7: 13028. DOI: 10.1038/ncomms13028.
37. Lillien L. Changes in retinal cell fate induced by overexpression of EGF receptor[J]. Nature, 1995, 377(6545): 158-162. DOI: 10.1038/377158a0.
38. Kim J, Wu HH, Lander AD, et al. GDF11 controls the timing of progenitor cell competence in developing retina[J]. Science, 2005, 308(5730): 1927-1930. DOI: 10.1126/science.1110175.
39. Rosenthal R, Wohlleben H, Malek G, et al. Insulin-like growth factor-1 contributes to neovascularization in age-related macular degeneration[J]. Biochem Biophys Res Commun, 2004, 323(4): 1203-1208. DOI: 10.1016/j.bbrc.2004.08.219.
40. Xu Y, Balasubramaniam B, Copland DA, et al. Activated adult microglia influence retinal progenitor cell proliferation and differentiation toward recoverin-expressing neuron-like cells in a co-culture model[J]. Graefe’s Arch Clin Exp Ophthalmol, 2015, 253(7): 1085-1096. DOI: 10.1007/s00417-015-2961-y.
41. Quadrato G, Nguyen T, Macosko EZ, et al. Cell diversity and network dynamics in photosensitive human brain organoids[J]. Nature, 2017, 545(7652): 48-53. DOI: 10.1038/nature22047.
42. Park SS, Moisseiev E, Bauer G, et al. Advances in bone marrow stem cell therapy for retinal dysfunction[J]. Prog Retin Eye Res, 2017, 56: 148-165. DOI: 10.1016/j.preteyeres.2016.10.002.
43. Hu Y, Luo M, Ni N, et al. Reciprocal actions of microRNA-9 and TLX in the proliferation and differentiation of retinal progenitor cells[J]. Stem Cells Dev, 2014, 23(22): 2771-2781. DOI: 10.1089/scd.2014.0021.
44. Ni N, Zhang D, Xie Q, et al. Effects of let-7b and TLX on the proliferation and differentiation of retinal progenitor cells in vitro[J]. Sci Rep, 2014, 4: 6671. DOI: 10.1038/srep06671.
45. Zhang Y, Yue K, Aleman J, et al. 3D Bioprinting for Tissue and Organ Fabrication[J]. Ann Biomed Eng, 2017, 45(1): 148-163.
46. Melton C, Judson RL, Blelloch R. Opposing microRNA families regulate self-renewal in mouse embryonic stem cells[J]. Nature, 2010, 463(7281): 621-626. DOI: 10.1038/nature08725.
47. Banin E, Obolensky A, Idelson M, et al. Retinal incorporation and differentiation of neural precursors derived from human embryonic stem cells[J]. Stem Cells, 2006, 24(2): 246-257. DOI: 10.1634/stemcells.2005-0009.
48. Singh D, Wang SB, Xia T, et al. A biodegradable scaffold enhances differentiation of embryonic stem cells into a thick sheet of retinal cells[J]. Biomaterials, 2018, 154: 158-168. DOI: 10.1016/j.biomaterials.2017.10.052.
49. Worthington KS, Wiley LA, Kaalberg EE, et al. Two-photon polymerization for production of human iPSC-derived retinal cell grafts[J]. Acta Biomater, 2017, 55: 385-395. DOI: 10.1016/j.actbio.2017.03.039.
50. Li K, Zhong X, Yang S, et al. HiPSC-derived retinal ganglion cells grow dendritic arbors and functional axons on a tissue-engineered scaffold[J]. Acta Biomater, 2017, 54: 117-127. DOI: 10.1016/j.actbio.2017.02.032.

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