Quantification of Retinogenesis in 3D Cultures Reveals Epigenetic Memory and Higher Efficiency in iPSCs Derived from Rod Photoreceptors

Cell Stem Cell

Volumn 17, Issue 1, 2015, Pages 101-115

  Hiler, Daniel ^a   Chen, Xiang ^b   Hazen, Jennifer ^a   Kupriyanov, Sergey ^c   Carroll, Patrick A ^d   Qu, Chunxu ^b   Xu, Beisi ^b   Johnson, Dianna ^e   Griffiths, Lyra ^a   Frase, Sharon ^b   Rodriguez, Alberto R ^c   Martin, Greg ^c   Zhang, Jiakun ^a   Jeon, Jongrye ^a   Fan, Yiping ^b   Finkelstein, David ^b   Eisenman, Robert N ^d   Baldwin, Kristin ^a   Dyer, Michael A ^a,e,f  

^a Department of Developmental Neurobiology ^*  (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d Fred Hutchinson Cancer Research Center   (United States)

^e UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CTCF;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL NUCLEUS; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; EMBRYONIC STEM CELL; EPIGENETICS; FEMALE; FIBROBLAST; GENETIC ANALYSIS; MALE; MOUSE; NONHUMAN; ORGAN CULTURE; ORGANOGENESIS; PHOTORECEPTOR; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; RETINA AMACRINE CELL; RETINA DEGENERATION; RETINA NERVE CELL; RETINA ROD; STEM CELL CULTURE; ANIMAL; CELL CULTURE TECHNIQUE; CELL LINE; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NUCLEAR REPROGRAMMING; PATHOLOGY; PROCEDURES; RETINA; RETINAL DEGENERATION; TRANSGENIC MOUSE;

MURINAE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELLULAR REPROGRAMMING; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, TRANSGENIC; RETINA; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS;

EID: 84936989258     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.05.015     Document Type: Article

References (41)

1. Alunni, A., Menuet, A., Candal, E., Pénigault, J.B., Jeffery, W.R., and Rétaux, S. (2007). Developmental mechanisms for retinal degeneration in the blind cave-fish Astyanax mexicanus. J. Comp. Neurol. 505, 221-233.
2. Assawachananont, J., Mandai, M., Okamoto, S., Yamada, C., Eiraku, M., Yonemura, S., Sasai, Y., and Takahashi, M. (2014). Transplantation of embryonic and induced pluripotent stem cell-derived 3D retinal sheets into retinal degenerative mice. Stem Cell Reports 2, 662-674.
3. Balasubramanian, R., Bui, A., Ding, Q., and Gan, L. (2014). Expression of LIM-homeodomain transcription factors in the developing and mature mouse retina. Gene Expr. Patterns 14, 1-8.
4. Belliveau, M.J., and Cepko, C.L. (1999). Extrinsic and intrinsic factors control the genesis of amacrine and cone cells in the rat retina. Development 126, 555-566.
5. Belliveau, M.J., Young, T.L., and Cepko, C.L. (2000). Late retinal progenitor cells show intrinsic limitations in the production of cell types and the kinetics of opsin synthesis. J. Neurosci. 20, 2247-2254.
6. Birk, O.S., Casiano, D.E., Wassif, C.A., Cogliati, T., Zhao, L., Zhao, Y., Grinberg, A., Huang, S., Kreidberg, J.A., Parker, K.L., et al. (2000). The LIM homeobox gene Lhx9 is essential for mouse gonad formation. Nature 403, 909-913.
7. Buchholz, D.E., Hikita, S.T., Rowland, T.J., Friedrich, A.M., Hinman, C.R., Johnson, L.V., and Clegg, D.O. (2009). Derivation of functional retinal pigmented epithelium from induced pluripotent stem cells. Stem Cells 27, 2427-2434.
8. Buganim, Y., Faddah, D.A., and Jaenisch, R. (2013). Mechanisms and models of somatic cell reprogramming. Nat. Rev. Genet. 14, 427-439.
9. Carey, B.W., Markoulaki, S., Hanna, J.H., Faddah, D.A., Buganim, Y., Kim, J., Ganz, K., Steine, E.J., Cassady, J.P., Creyghton, M.P., et al. (2011). Reprogramming factor stoichiometry influences the epigenetic state and biological properties of induced pluripotent stem cells. Cell Stem Cell 9, 588-598.
10. Cherry, T.J., Trimarchi, J.M., Stadler, M.B., and Cepko, C.L. (2009). Development and diversification of retinal amacrine interneurons at single cell resolution. Proc. Natl. Acad. Sci. USA 106, 9495-9500.
11. Cramer, A.O., and MacLaren, R.E. (2013). Translating induced pluripotent stem cells from bench to bedside: application to retinal diseases. Curr. Gene Ther. 13, 139-151.
12. Dowen, J.M., Fan, Z.P., Hnisz, D., Ren, G., Abraham, B.J., Zhang, L.N., Weintraub, A.S., Schuijers, J., Lee, T.I., Zhao, K., and Young, R.A. (2014). Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159, 374-387.
13. Eiraku, M., and Sasai, Y. (2012a). Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues. Nat. Protoc. 7, 69-79.
14. Eiraku, M., and Sasai, Y. (2012b). Self-formation of layered neural structures in three-dimensional culture of ES cells. Curr. Opin. Neurobiol. 22, 768-777.
15. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., and Sasai, Y. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56.
16. Gonzalez-Cordero, A., West, E.L., Pearson, R.A., Duran, Y., Carvalho, L.S., Chu, C.J., Naeem, A., Blackford, S.J., Georgiadis, A., Lakowski, J., et al. (2013). Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat. Biotechnol. 31, 741-747.
17. Hanna, J.H., Saha, K., and Jaenisch, R. (2010). Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell 143, 508-525.
18. Hargus, G., Ehrlich, M., Araúzo-Bravo, M.J., Hemmer, K., Hallmann, A.L., Reinhardt, P., Kim, K.P., Adachi, K., Santourlidis, S., Ghanjati, F., et al. (2014). Origin-dependent neural cell identities in differentiated human iPSCs in vitro and after transplantation into the mouse brain. Cell Rep. 8, 1697-1703.
19. Hou, C., Dale, R., and Dean, A. (2010). Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc. Natl. Acad. Sci. USA 107, 3651-3656.
20. Hu, Q., Friedrich, A.M., Johnson, L.V., and Clegg, D.O. (2010). Memory in induced pluripotent stem cells: reprogrammed human retinal-pigmented epithelial cells show tendency for spontaneous redifferentiation. Stem Cells 28, 1981-1991.
21. Hyatt, G.A., Schmitt, E.A., Fadool, J.M., and Dowling, J.E. (1996). Retinoic acid alters photoreceptor development in vivo. Proc. Natl. Acad. Sci. USA 93, 13298-13303.
22. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M.J., Ji, H., Ehrlich, L.I., et al. (2010). Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290.
23. Kim, J., Lengner, C.J., Kirak, O., Hanna, J., Cassady, J.P., Lodato, M.A., Wu, S., Faddah, D.A., Steine, E.J., Gao, Q., et al. (2011). Reprogramming of postnatal neurons into induced pluripotent stem cells by defined factors. Stem Cells 29, 992-1000.
24. MacLaren, R.E., Pearson, R.A., MacNeil, A., Douglas, R.H., Salt, T.E., Akimoto, M., Swaroop, A., Sowden, J.C., and Ali, R.R. (2006). Retinal repair by transplantation of photoreceptor precursors. Nature 444, 203-207.
25. Mears, A.J., Kondo, M., Swain, P.K., Takada, Y., Bush, R.A., Saunders, T.L., Sieving, P.A., and Swaroop, A. (2001). Nrl is required for rod photoreceptor development. Nat. Genet. 29, 447-452.
26. Meyer, J.S., Shearer, R.L., Capowski, E.E., Wright, L.S., Wallace, K.A., McMillan, E.L., Zhang, S.C., and Gamm, D.M. (2009). Modeling early retinal development with human embryonic and induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 106, 16698-16703.
27. Meyer, J.S., Howden, S.E., Wallace, K.A., Verhoeven, A.D., Wright, L.S., Capowski, E.E., Pinilla, I., Martin, J.M., Tian, S., Stewart, R., et al. (2011). Optic vesicle-like structures derived from human pluripotent stem cells facilitate a customized approach to retinal disease treatment. Stem Cells 29, 1206-1218.
28. Morrow, E.M., Belliveau, M.J., and Cepko, C.L. (1998). Two phases of rod photoreceptor differentiation during rat retinal development. J. Neurosci. 18, 3738-3748.
29. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M., and Sasai, Y. (2012). Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10, 771-785.
30. Narendra, V., Rocha, P.P., An, D., Raviram, R., Skok, J.A., Mazzoni, E.O., and Reinberg, D. (2015). Transcription. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 347, 1017-1021.
31. 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. (2012). Restoration of vision after transplantation of photoreceptors. Nature 485, 99-103.
32. Phillips, J.E., and Corces, V.G. (2009). CTCF: master weaver of the genome. Cell 137, 1194-1211.
33. Phillips, M.J., Wallace, K.A., Dickerson, S.J., Miller, M.J., Verhoeven, A.D., Martin, J.M., Wright, L.S., Shen, W., Capowski, E.E., Percin, E.F., et al. (2012). Blood-derived human iPS cells generate optic vesicle-like structures with the capacity to form retinal laminae and develop synapses. Invest. Ophthalmol. Vis. Sci. 53, 2007-2019.
34. Pottin, K., Hinaux, H., and Rétaux, S. (2011). Restoring eye size in Astyanax mexicanus blind cavefish embryos through modulation of the Shh and Fgf8 forebrain organising centres. Development 138, 2467-2476.
35. Prickett, A.R., Barkas, N., McCole, R.B., Hughes, S., Amante, S.M., Schulz, R., and Oakey, R.J. (2013). Genome-wide and parental allele-specific analysis of CTCF and cohesin DNA binding in mouse brain reveals a tissue-specific binding pattern and an association with imprinted differentially methylated regions. Genome Res. 23, 1624-1635.
36. Ramsden, C.M., Powner, M.B., Carr, A.J., Smart, M.J., daCruz, L., and Coffey, P.J. (2013). Stem cells in retinal regeneration: past, present and future. Development 140, 2576-2585.
37. Stadtfeld, M., Maherali, N., Borkent, M., and Hochedlinger, K. (2010). A reprogrammable mouse strain from gene-targeted embryonic stem cells. Nat. Methods 7, 53-55.
38. Trimarchi, J.M., Stadler, M.B., Roska, B., Billings, N., Sun, B., Bartch, B., and Cepko, C.L. (2007). Molecular heterogeneity ofdeveloping retinal ganglion and amacrine cells revealed through single cell gene expression profiling. J. Comp. Neurol. 502, 1047-1065.
39. Trimarchi, J.M., Stadler, M.B., and Cepko, C.L. (2008). Individual retinal progenitor cells display extensive heterogeneity of gene expression. PLoS One 3, e1588.
40. Wang, H., Maurano, M.T., Qu, H., Varley, K.E., Gertz, J., Pauli, F., Lee, K., Canfield, T., Weaver, M., Sandstrom, R., et al. (2012). Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22, 1680-1688.
41. 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. (2014). Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat. Commun. 5, 4047.