Function of human pluripotent stem cell-derived photoreceptor progenitors in blind mice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Barnea Cramer, Alona O ^a   Wang, Wei ^b   Lu, Shi Jiang ^b   Singh, Mandeep S ^a,c   Luo, Chenmei ^b   Huo, Hongguang ^b   McClements, Michelle E ^a   Barnard, Alun R ^a   MacLaren, Robert E ^a,c,d   Lanza, Robert ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Astellas Institute for Regenerative Medicine   (United States)

^c MOORFIELDS EYE HOSPITAL   (United Kingdom)

^d OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; BLINDNESS; CELL DIFFERENTIATION; HUMAN; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; METABOLISM; MOUSE; PATHOLOGY; RETINITIS PIGMENTOSA; TRANSPLANTATION; VERTEBRATE PHOTORECEPTOR CELL; XENOGRAFT;

ANIMALS; BLINDNESS; CELL DIFFERENTIATION; HETEROGRAFTS; HUMAN EMBRYONIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; PHOTORECEPTOR CELLS, VERTEBRATE; RETINITIS PIGMENTOSA;

EID: 84978924130     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29784     Document Type: Article

References (64)

1. Hartong, D. T., Berson, E. L. & Dryja, T. P. Retinitis pigmentosa. Lancet 368, 1795-1809, doi: 10.1016/s0140-6736(06)69740-7 (2006).
2. Barber, A. C. et al. Repair of the degenerate retina by photoreceptor transplantation. Proceedings of the National Academy of Sciences of the United States of America 110, 354-359, doi: 10.1073/pnas.1212677110 (2013).
3. Luo, J. et al. Human retinal progenitor cell transplantation preserves vision. The Journal of biological chemistry 289, 6362-6371, doi: 10.1074/jbc.M113.513713 (2014).
4. Singh, M. S. et al. Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. Proceedings of the National Academy of Sciences of the United States of America 110, 1101-1106, doi: 10.1073/pnas.1119416110 (2013).
5. Pearson, R. A. et al. Restoration of vision after transplantation of photoreceptors. Nature 485, 99-103, doi: 10.1038/nature10997 (2012).
6. Lamba, D. A., Gust, J. & Reh, T. A. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell stem cell 4, 73-79, doi: 10.1016/j.stem.2008.10.015 (2009).
7. Schmitt, S. et al. Molecular characterization of human retinal progenitor cells. Investigative ophthalmology & visual science 50, 5901-5908, doi: 10.1167/iovs.08-3067 (2009).
8. Schwartz, S. D. et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379, 713-720, doi: 10.1016/s0140-6736(12)60028-2 (2012).
9. Schwartz, S. D. 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 385, 509-516, doi: 10.1016/s0140-6736(14)61376-3 (2015).
10. Song, W. K. et al. Treatment of Macular Degeneration Using Embryonic Stem Cell-Derived Retinal Pigment Epithelium: Preliminary Results in Asian Patients. Stem cell reports, doi: 10.1016/j.stemcr.2015.04.005 (2015).
11. Lamba, D. A., Karl, M. O., Ware, C. B. & Reh, T. A. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 103, 12769-12774, doi: 10.1073/pnas.0601990103 (2006).
12. Osakada, F., Ikeda, H., Sasai, Y. & Takahashi, M. Stepwise differentiation of pluripotent stem cells into retinal cells. Nature protocols 4, 811-824, doi: 10.1038/nprot.2009.51 (2009).
13. Hirami, Y. et al. Generation of retinal cells from mouse and human induced pluripotent stem cells. Neuroscience letters 458, 126-131, doi: 10.1016/j.neulet.2009.04.035 (2009).
14. Lamba, D. A. et al. Generation, purification and transplantation of photoreceptors derived from human induced pluripotent stem cells. PloS one 5, e8763, doi: 10.1371/journal.pone.0008763 (2010).
15. Zhou, L. et al. Differentiation of induced pluripotent stem cells of swine into rod photoreceptors and their integration into the retina. Stem cells (Dayton, Ohio) 29, 972-980, doi: 10.1002/stem.637 (2011).
16. La Torre, A., Lamba, D. A., Jayabalu, A. & Reh, T. A. Production and transplantation of retinal cells from human and mouse embryonic stem cells. Methods Mol Biol 884, 229-246, doi: 10.1007/978-1-61779-848-1-16 (2012).
17. Eiraku, M. & Sasai, Y. Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues. Nature protocols 7, 69-79, doi: 10.1038/nprot.2011.429 (2012).
18. Jin, Z. B., Okamoto, S., Xiang, P. & Takahashi, M. Integration-free induced pluripotent stem cells derived from retinitis pigmentosa patient for disease modeling. Stem cells translational medicine 1, 503-509, doi: 10.5966/sctm.2012-0005 (2012).
19. Osakada, F. et al. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nature biotechnology 26, 215-224, doi: 10.1038/nbt1384 (2008).
20. Takahashi, K. et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872, doi: 10.1016/j.cell.2007.11.019 (2007).
21. Meyer, J. S. et al. Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proceedings of the National Academy of Sciences of the United States of America 106, 16698-16703, doi: 10.1073/pnas.0905245106 (2009).
22. Mellough, C. B., Sernagor, E., Moreno-Gimeno, I., Steel, D. H. & Lako, M. Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem cells (Dayton, Ohio) 30, 673-686, doi: 10.1002/stem.1037 (2012).
23. Nakano, T. et al. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell stem cell 10, 771-785, doi: 10.1016/j.stem.2012.05.009 (2012).
24. Decembrini, S., Koch, U., Radtke, F., Moulin, A. & Arsenijevic, Y. Derivation of Traceable and Transplantable Photoreceptors from Mouse Embryonic Stem Cells. Stem cell reports 2, 853-865, doi: 10.1016/j.stemcr.2014.04.010.
25. Reichman, S. et al. From confluent human iPS cells to self-forming neural retina and retinal pigmented epithelium. Proceedings of the National Academy of Sciences 111, 8518-8523, doi: 10.1073/pnas.1324212111 (2014).
26. Zhong, X. et al. Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nature communications 5, 4047, doi: 10.1038/ncomms5047 (2014).
27. Kaewkhaw, R. et al. Transcriptome dynamics of developing photoreceptors in three-dimensional retina cultures recapitulates temporal sequence of human cone and rod differentiation revealing cell surface markers and gene networks. Stem cells (Dayton, Ohio), doi: 10.1002/stem.2122 (2015).
28. Zhou, S. et al. Differentiation of human embryonic stem cells into cone photoreceptors through simultaneous inhibition of BMP, TGFbeta and Wnt signaling. Development (Cambridge, England) 142, 3294-3306, doi: 10.1242/dev.125385 (2015).
29. Gouras, P., Du, J., Kjeldbye, H., Yamamoto, S. & Zack, D. J. Reconstruction of degenerate rd mouse retina by transplantation of transgenic photoreceptors. Investigative ophthalmology & visual science 33, 2579-2586 (1992).
30. Kwan, A. S., Wang, S. & Lund, R. D. Photoreceptor layer reconstruction in a rodent model of retinal degeneration. Experimental neurology 159, 21-33, doi: 10.1006/exnr.1999.7157 (1999).
31. Tucker, B. A. et al. Transplantation of adult mouse iPS cell-derived photoreceptor precursors restores retinal structure and function in degenerative mice. PloS one 6, e18992, doi: 10.1371/journal.pone.0018992 (2011).
32. Gonzalez-Cordero, A. et al. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nature biotechnology 31, 741-747, doi: 10.1038/nbt.2643 (2013).
33. Eberle, D., Schubert, S., Postel, K., Corbeil, D. & Ader, M. Increased integration of transplanted CD73-positive photoreceptor precursors into adult mouse retina. Investigative ophthalmology & visual science 52, 6462-6471, doi: 10.1167/iovs.11-7399 (2011).
34. Koso, H. et al. CD73, a novel cell surface antigen that characterizes retinal photoreceptor precursor cells. Investigative ophthalmology & visual science 50, 5411-5418, doi: 10.1167/iovs.08-3246 (2009).
35. Lakowski, J. et al. Effective transplantation of photoreceptor precursor cells selected via cell surface antigen expression. Stem cells (Dayton, Ohio) 29, 1391-1404, doi: 10.1002/stem.694 (2011).
36. Eberle, D., Santos-Ferreira, T., Grahl, S. & Ader, M. Subretinal transplantation of MACS purified photoreceptor precursor cells into the adult mouse retina. Journal of visualized experiments: JoVE. e50932, doi: 10.3791/50932 (2014).
37. Lakowski, J. et al. Transplantation of Photoreceptor Precursors Isolated via a Cell Surface Biomarker Panel From Embryonic Stem Cell-Derived Self-Forming Retina. Stem cells (Dayton, Ohio) 33, 2469-2482, doi: 10.1002/stem.2051 (2015).
38. Warren, L., Ni, Y., Wang, J. & Guo, X. Feeder-free derivation of human induced pluripotent stem cells with messenger RNA. Scientific reports 2, 657, doi: 10.1038/srep00657 (2012).
39. Bowes, C. et al. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature 347, 677-680, doi: 10.1038/347677a0 (1990).
40. Farber, D. B. From mice to men: the cyclic GMP phosphodiesterase gene in vision and disease. The Proctor Lecture. Investigative ophthalmology & visual science 36, 263-275 (1995).
41. Lolley, R. N., Rong, H. & Craft, C. M. Linkage of photoreceptor degeneration by apoptosis with inherited defect in phototransduction. Investigative ophthalmology & visual science 35, 358-362 (1994).
42. Chang, B. et al. Two mouse retinal degenerations caused by missense mutations in the beta-subunit of rod cGMP phosphodiesterase gene. Vision research 47, 624-633, doi: 10.1016/j.visres.2006.11.020 (2007).
43. Assawachananont, J. et al. Transplantation of embryonic and induced pluripotent stem cell-derived 3D retinal sheets into retinal degenerative mice. Stem cell reports 2, 662-674, doi: 10.1016/j.stemcr.2014.03.011 (2014).
44. Cehajic-Kapetanovic, J. et al. Restoration of Vision with Ectopic Expression of Human Rod Opsin. Current Biology 25, 2111-2122, doi: http://dx.doi.org/10.1016/j.cub.2015.07.029 (2015).
45. West, E. L. et al. Long-term survival of photoreceptors transplanted into the adult murine neural retina requires immune modulation. Stem cells (Dayton, Ohio) 28, 1997-2007, doi: 10.1002/stem.520 (2010).
46. Lakowski, J. et al. Cone and rod photoreceptor transplantation in models of the childhood retinopathy Leber congenital amaurosis using flow-sorted Crx-positive donor cells. Human molecular genetics 19, 4545-4559, doi: 10.1093/hmg/ddq378 (2010).
47. MacLaren, R. E. et al. Retinal repair by transplantation of photoreceptor precursors. Nature 444, 203-207, doi: 10.1038/nature05161 (2006).
48. Yao, J. et al. XIAP therapy increases survival of transplanted rod precursors in a degenerating host retina. Investigative ophthalmology & visual science 52, 1567-1572, doi: 10.1167/iovs.10-5998 (2011).
49. Eng, L. F. & Ghirnikar, R. S. GFAP and Astrogliosis. Brain Pathology 4, 229-237, doi: 10.1111/j.1750-3639.1994.tb00838.x (1994).
50. Dahl, D. The radial glia of Müller in the rat retina and their response to injury. An immunofluorescence study with antibodies to the glial fibrillary acidic (GFA) protein. Experimental eye research 28, 63-69, doi: http://dx.doi.org/10.1016/0014-4835(79)90106-4 (1979).
51. Zhang, Y., Arner, K., Ehinger, B. & Perez, M. T. Limitation of anatomical integration between subretinal transplants and the host retina. Investigative ophthalmology & visual science 44, 324-331 (2003).
52. Lipinski, D. et al. CNTF gene therapy confers lifelong neuroprotection in a mouse model of human retinitis pigmentosa. Mol Therapy, in press (2015).
53. Harvey, R. J., De'Sperati, C. & Strata, P. The early phase of horizontal optokinetic responses in the pigmented rat and the effects of lesions of the visual cortex. Vision research 37, 1615-1625 (1997).
54. Misslin, R., Belzung, C. & Vogel, E. Behavioural validation of a light/dark choice procedure for testing anti-anxiety agents. Behavioural processes 18, 119-132, doi: 10.1016/s0376-6357(89)80010-5 (1989).
55. Busskamp, V. et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science (New York, N.Y.) 329, 413-417, doi: 10.1126/science.1190897 (2010).
56. Dowling, J. E. The Retina: An Approachable Part of the Brain. (Belknap Press of Harvard University Press, 2012).
57. Swaroop, A., Kim, D. & Forrest, D. Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina. Nature reviews. Neuroscience 11, 563-576, doi: 10.1038/nrn2880 (2010).
58. Haider, N. B. et al. Mutation of a nuclear receptor gene, NR2E3, causes enhanced S cone syndrome, a disorder of retinal cell fate. Nature genetics 24, 127-131, doi: 10.1038/72777 (2000).
59. Stingl, K. et al. Artificial vision with wirelessly powered subretinal electronic implant alpha-IMS. Proceedings. Biological sciences/The Royal Society 280, 20130077, doi: 10.1098/rspb.2013.0077 (2013).
60. Zrenner, E. et al. Subretinal electronic chips allow blind patients to read letters and combine them to words. Proceedings of the Royal Society B: Biological Sciences 278, 1489-1497, doi: 10.1098/rspb.2010.1747 (2011).
61. Cramer, A. O. & MacLaren, R. E. Translating induced pluripotent stem cells from bench to bedside: application to retinal diseases. Current gene therapy 13, 139-151 (2013).
62. Thompson, S. et al. Photoreceptor cells with profound structural deficits can support useful vision in mice. Investigative ophthalmology & visual science 55, 1859-1866, doi: 10.1167/iovs.13-13661 (2014).
63. Sun, J. et al. Protective effects of human iPS-derived retinal pigmented epithelial cells in comparison with human mesenchymal stromal cells and human neural stem cells on the degenerating retina in rd1 mice. Stem cells (Dayton, Ohio), n/a-n/a, doi: 10.1002/stem.1960 (2015).
64. Punzo, C. & Cepko, C. Cellular responses to photoreceptor death in the rd1 mouse model of retinal degeneration. Investigative ophthalmology & visual science 48, 849-857, doi: 10.1167/iovs.05-1555 (2007).