Differentiation and Transplantation of Embryonic Stem Cell-Derived Cone Photoreceptors into a Mouse Model of End-Stage Retinal Degeneration

Stem Cell Reports

Volumn 8, Issue 6, 2017, Pages 1659-1674

  Kruczek, Kamil ^a   Gonzalez Cordero, Anai ^a   Goh, Debbie ^a   Naeem, Arifa ^a   Jonikas, Mindaugas ^a   Blackford, Samuel J I ^a   Kloc, Magdalena ^a   Duran, Yanai ^a   Georgiadis, Anastasios ^a   Sampson, Robert D ^a   Maswood, Ryea N ^a   Smith, Alexander J ^a   Decembrini, Sarah ^b   Arsenijevic, Yvan ^b   Sowden, Jane C ^c   Pearson, Rachael A ^a   West, Emma L ^a   Ali, Robin R ^a,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d MOORFIELDS EYE HOSPITAL   (United Kingdom)

Author keywords

blindness; cell and tissue based therapy; mouse embryonic stem cells; retina; retinal cone photoreceptor cells; retinal degeneration

Indexed keywords

CONE OPSIN; NOTCH1 RECEPTOR; NOTCH2 RECEPTOR; NOTCH2E3 RECEPTOR; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; ONECUT1 PROTEIN; RETINOIC ACID; THYROID HORMONE RECEPTOR BETA; THYROID HORMONE RECEPTOR BETA 2; TRANSCRIPTION FACTOR OTX2; UNCLASSIFIED DRUG; VISUAL PROTEINS AND PIGMENTS; AIPL1 PROTEIN, MOUSE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; EYE PROTEIN; HEPATOCYTE NUCLEAR FACTOR 6; LEUKEMIA INHIBITORY FACTOR; NOTCH RECEPTOR; NR2E3 PROTEIN, MOUSE; NRL PROTEIN, MOUSE; OLIG2 PROTEIN, MOUSE; ONECUT1 PROTEIN, MOUSE; OPSIN; ORPHAN NUCLEAR RECEPTOR; OTX2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR OTX;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL MATURATION; CELL SURVIVAL; CELL SUSPENSION; EMBRYO DEVELOPMENT; END STAGE RETINAL GEGENERATION; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; MOUSE EMBRYONIC STEM CELL; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; POSTNATAL DEVELOPMENT; PRECURSOR; PRIORITY JOURNAL; RETINA CONE; RETINA DEGENERATION; RETINA NERVE CELL; SIGNAL TRANSDUCTION; STEM CELL TRANSPLANTATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CYTOLOGY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; RNA INTERFERENCE; TRANSPLANTATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; EYE PROTEINS; HEPATOCYTE NUCLEAR FACTOR 6; LEUKEMIA INHIBITORY FACTOR; MICE; MICE, KNOCKOUT; MOUSE EMBRYONIC STEM CELLS; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; OPSINS; ORPHAN NUCLEAR RECEPTORS; OTX TRANSCRIPTION FACTORS; RECEPTORS, NOTCH; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL DEGENERATION; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 85019850345     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2017.04.030     Document Type: Article

References (47)

1. Alfano, G., Conte, I., Caramico, T., Avellino, R., Arno, B., Pizzo, M.T., Tanimoto, N., Beck, S.C., Huber, G., Dolle, P., et al. Vax2 regulates retinoic acid distribution and cone opsin expression in the vertebrate eye. Development 138 (2011), 261–271.
2. Applebury, M.L., Antoch, M.P., Baxter, L.C., Chun, L.L.Y., Falk, J.D., Farhangfar, F., Kage, K., Krzystolik, M.G., Lyass, L.A., Robbins, J.T., The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27 (2000), 513–523.
3. Assawachananont, J., Mandai, M., Okamoto, S., Yamada, C., Eiraku, M., Yonemura, S., Sasai, Y., Takahashi, M., Transplantation of embryonic and induced pluripotent stem cell-derived 3D retinal sheets into retinal degenerative mice. Stem Cell Rep. 2 (2014), 662–674.
4. Barnea-Cramer, A.O., Wang, W., Lu, S.-J., Singh, M.S., Luo, C., Huo, H., McClements, M.E., Barnard, A.R., MacLaren, R.E., Lanza, R., Function of human pluripotent stem cell-derived photoreceptor progenitors in blind mice. Sci. Rep., 6, 2016, 29784.
5. Carter-Dawson, L.D., LaVail, M.M., Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritiated thymidine. J. Comp. Neurol. 188 (1979), 263–272.
6. Decembrini, S., Koch, U., Radtke, F., Moulin, A., Arsenijevic, Y., Derivation of traceable and transplantable photoreceptors from mouse embryonic stem cells. Stem Cell Rep. 2 (2014), 853–865.
7. Decembrini, S., Martin, C., Sennlaub, F., Chemtob, S., Biel, M., Samardzija, M., Moulin, A., Behar-Cohen, F., Arsenijevic, Y., Cone genesis tracing by the Chrnb4-EGFP mouse line: evidences of cellular material fusion after cone precursor transplantation. Mol. Ther. J. 25 (2017), 634–653.
8. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., Sasai, Y., Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472 (2011), 51–56.
9. Emerson, M.M., Surzenko, N., Goetz, J.J., Trimarchi, J., Cepko, C.L., Otx2 and Onecut1 promote the fates of cone photoreceptors and horizontal cells and repress rod photoreceptors. Dev. Cell 26 (2013), 59–72.
10. Gonzalez-Cordero, A., West, E.L., Pearson, R.A., Duran, Y., Carvalho, L.S., Chu, C.J., Naeem, A., Blackford, S.J.I., Georgiadis, A., Lakowski, J., et al. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol. 31 (2013), 741–747.
11. Hafler, B.P., Surzenko, N., Beier, K.T., Punzo, C., Trimarchi, J.M., Kong, J.H., Cepko, C.L., Transcription factor Olig2 defines subpopulations of retinal progenitor cells biased toward specific cell fates. Proc. Natl. Acad. Sci. USA 109 (2012), 7882–7887.
12. Hyatt, G.A., Schmitt, E.A., Fadool, J.M., Dowling, J.E., Retinoic acid alters photoreceptor development in vivo. Proc. Natl. Acad. Sci. USA 93 (1996), 13298–13303.
13. Jadhav, A.P., Notch 1 inhibits photoreceptor production in the developing mammalian retina. Development 133 (2006), 913–923.
14. Jayakody, S.A., Gonzalez-Cordero, A., Ali, R.R., Pearson, R.A., Cellular strategies for retinal repair by photoreceptor replacement. Prog. Retin. Eye Res. 46 (2015), 31–66.
15. Jeon, C.J., Strettoi, E., Masland, R.H., The major cell populations of the mouse retina. J. Neurosci. 18 (1998), 8936–8946.
16. Kim, J., Wu, H.-H., Lander, A.D., Lyons, K.M., Matzuk, M.M., Calof, A.L., GDF11 controls the timing of progenitor cell competence in developing retina. Science 308 (2005), 1927–1930.
17. Kim, J.-W., Yang, H.-J., Oel, A.P., Brooks, M.J., Jia, L., Plachetzki, D.C., Li, W., Allison, W.T., Swaroop, A., Recruitment of rod photoreceptors from short-wavelength-sensitive cones during the evolution of nocturnal vision in mammals. Dev. Cell 37 (2016), 520–532.
18. Lakowski, J., Baron, M., Bainbridge, J., Barber, A.C., Pearson, R.A., Ali, R.R., Sowden, J.C., Cone and rod photoreceptor transplantation in models of the childhood retinopathy Leber congenital amaurosis using flow-sorted Crx-positive donor cells. Hum. Mol. Genet. 19 (2010), 4545–4559.
19. Lu, A., Ng, L., Ma, M., Kefas, B., Davies, T.F., Hernandez, A., Chan, C.-C., Forrest, D., Retarded developmental expression and patterning of retinal cone opsins in hypothyroid mice. Endocrinology 150 (2009), 1536–1544.
20. MacLaren, R.E., Pearson, R.A., MacNeil, A., Douglas, R.H., Salt, T.E., Akimoto, M., Swaroop, A., Sowden, J.C., Ali, R.R., Retinal repair by transplantation of photoreceptor precursors. Nature 444 (2006), 203–207.
21. McCaffrery, P., Posch, K.C., Napoli, J.L., Gudas, L., Dräger, U.C., Changing patterns of the retinoic acid system in the developing retina. Dev. Biol. 158 (1993), 390–399.
22. Mears, A.J., Kondo, M., Swain, P.K., Takada, Y., Bush, R.A., Saunders, T.L., Sieving, P.A., Swaroop, A., Nrl is required for rod photoreceptor development. Nat. Genet. 29 (2001), 447–452.
23. Meyer, J.S., Shearer, R.L., Capowski, E.E., Wright, L.S., Wallace, K.A., McMillan, E.L., Zhang, S.-C., Gamm, D.M., Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 106 (2009), 16698–16703.
24. Mizeracka, K., DeMaso, C.R., Cepko, C.L., Notch1 is required in newly postmitotic cells to inhibit the rod photoreceptor fate. Development 140 (2013), 3188–3197.
25. Muranishi, Y., Sato, S., Inoue, T., Ueno, S., Koyasu, T., Kondo, M., Furukawa, T., Gene expression analysis of embryonic photoreceptor precursor cells using BAC-Crx-EGFP transgenic mouse. Biochem. Biophys. Res. Commun. 392 (2010), 317–322.
26. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M., Sasai, Y., Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10 (2012), 771–785.
27. Nelson, B.R., Hartman, B.H., Georgi, S.A., Lan, M.S., Reh, T.A., Transient inactivation of Notch signaling synchronizes differentiation of neural progenitor cells. Dev. Biol. 304 (2007), 479–498.
28. Ng, L., Hurley, J.B., Dierks, B., Srinivas, M., Saltó, C., Vennström, B., Reh, T.A., Forrest, D., A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat. Genet. 27 (2001), 94–98.
29. Ng, L., Ma, M., Curran, T., Forrest, D., Developmental expression of thyroid hormone receptor β2 protein in cone photoreceptors in the mouse. Neuroreport 20 (2009), 627–631.
30. Nishida, A., Furukawa, A., Koike, C., Tano, Y., Aizawa, S., Matsuo, I., Furukawa, T., Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat. Neurosci. 6 (2003), 1255–1263.
31. Ortin-Martinez, A., Tsai, E.L.S., Nickerson, P.E., Bergeret, M., Lu, Y., Smiley, S., Comanita, L., Wallace, V.A., A reinterpretation of cell transplantation: GFP transfer from donor to host photoreceptors. Stem Cells 35 (2016), 932–939.
32. Pearson, R.A., Barber, A.C., Rizzi, M., Hippert, C., Xue, T., West, E.L., Duran, Y., Smith, A.J., Chuang, J.Z., Azam, S.A., et al. Restoration of vision after transplantation of photoreceptors. Nature 485 (2012), 99–103.
33. Pearson, R.A., Hippert, C., Graca, A.B., Barber, A.C., Photoreceptor replacement therapy: challenges presented by the diseased recipient retinal environment. Vis. Neurosci. 31 (2014), 333–344.
34. Pearson, R.A., Gonzalez-Cordero, A., West, E.L., Ribeiro, J.R., Aghaizu, N., Goh, D., Sampson, R.D., Georgiadis, A., Waldron, P.V., Duran, Y., et al. Donor and host photoreceptors engage in material transfer following transplantation of post-mitotic photoreceptor precursors. Nat. Commun., 7, 2016, 13029.
35. Ramamurthy, V., Niemi, G.A., Reh, T.A., Hurley, J.B., Leber congenital amaurosis linked to AIPL1: a mouse model reveals destabilization of cGMP phosphodiesterase. Proc. Natl. Acad. Sci. USA 101 (2004), 13897–13902.
36. Reh, T.A., Photoreceptor transplantation in late stage retinal degeneration. Invest. Ophthalmol. Vis. Sci. 57 (2016), ORSFg1–7.
37. Roberts, M.R., Hendrickson, A., McGuire, C.R., Reh, T.A., Retinoid X receptor (gamma) is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest. Ophthalmol. Vis. Sci. 46 (2005), 2897–2904.
38. Santos-Ferreira, T., Postel, K., Stutzki, H., Kurth, T., Zeck, G., Ader, M., Daylight vision repair by cell transplantation: daylight vision repair by cell transplantation. Stem Cells 33 (2015), 79–90.
39. Seiler, M.J., Aramant, R.B., Cell replacement and visual restoration by retinal sheet transplants. Prog. Retin. Eye Res. 31 (2012), 661–687.
40. Shirai, H., Mandai, M., Matsushita, K., Kuwahara, A., Yonemura, S., Nakano, T., Assawachananont, J., Kimura, T., Saito, K., Terasaki, H., et al. Transplantation of human embryonic stem cell-derived retinal tissue in two primate models of retinal degeneration. Proc. Natl. Acad. Sci. USA 113 (2016), E81–E90.
41. Singh, M.S., Charbel Issa, P., Butler, R., Martin, C., Lipinski, D.M., Sekaran, S., Barnard, A.R., MacLaren, R.E., Reversal of end-stage retinal degeneration and restoration of visual function by photoreceptor transplantation. Proc. Natl. Acad. Sci. USA 110 (2013), 1101–1106.
42. Smiley, S., Nickerson, P.E., Comanita, L., Daftarian, N., El-Sehemy, A., Tsai, E.L.S., Matan-Lithwick, S., Yan, K., Thurig, S., Touahri, Y., et al. Establishment of a cone photoreceptor transplantation platform based on a novel cone-GFP reporter mouse line. Sci. Rep., 6, 2016, 22867.
43. Söderpalm, A., Szél, A., Caffé, A.R., van Veen, T., Selective development of one cone photoreceptor type in retinal organ culture. Invest. Ophthalmol. Vis. Sci. 35 (1994), 3910–3921.
44. Swaroop, A., Kim, D., Forrest, D., Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina. Nat. Rev. Neurosci. 11 (2010), 563–576.
45. Wang, Y., Macke, J.P., Merbs, S.L., Zack, D.J., Klaunberg, B., Bennett, J., Gearhart, J., Nathans, J., A locus control region adjacent to the human red and green visual pigment genes. Neuron 9 (1992), 429–440.
46. Yaron, O., Notch1 functions to suppress cone-photoreceptor fate specification in the developing mouse retina. Development 133 (2006), 1367–1378.
47. Zhong, X., Gutierrez, C., Xue, T., Hampton, C., Vergara, M.N., Cao, L.-H., Peters, A., Park, T.S., Zambidis, E.T., Meyer, J.S., et al. Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat. Commun., 5, 2014, 4047.