Differentiation of human embryonic stem cells using size-controlled embryoid bodies and negative cell selection in the production of photoreceptor precursor cells

Tissue Engineering - Part C: Methods

Volumn 19, Issue 10, 2013, Pages 755-764

  Yanai, Anat ^a   Laver, Christopher R J ^a   Joe, Aaron W ^a   Viringipurampeer, Ishaq A ^a   Wang, Xia ^a   Gregory Evans, Cheryl Y ^a   Gregory Evans, Kevin ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELLS; OPHTHALMOLOGY; VISION;

CELL HANDLING; CELL SELECTION; CLINICAL TRIAL; CULTURE MEDIUM; HUMAN EMBRYONIC STEM CELLS; PRECLINICAL STUDIES; PRECURSOR CELLS; RETINAL CELLS;

CYTOLOGY;

FETAL ANTIGEN; LIOTHYRONINE; STAGE SPECIFIC EMBRYO ANTIGEN 4;

ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL SELECTION; CELL SUSPENSION; CHROMOSOME ANALYSIS; CONTROLLED STUDY; EMBRYOID BODY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; KARYOTYPING; PHOTORECEPTOR CELL; PHOTORECEPTOR PRECURSOR CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CELL SIZE; CHROMOSOME BANDING; CULTURE MEDIA; EMBRYOID BODIES; GENE EXPRESSION PROFILING; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOMAGNETIC SEPARATION; KARYOTYPING; PHOTORECEPTOR CELLS, VERTEBRATE; TRANS-ACTIVATORS;

EID: 84882973063     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2012.0524     Document Type: Article

References (38)

1. Gehrs, K.M., Anderson, D.H., Johnson, L.V., and Hageman, G.S. Age-related macular degeneration-emerging pathogenetic and therapeutic concepts. Ann Med 38, 450, 2006.
2. 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. Retinal repair by transplantation of photoreceptor precursors. Nature 444, 203, 2006.
3. La Torre, A., Lamba, D.A., Jayabalu, A., and Reh, T.A. Production and transplantation of retinal cells from human and mouse embryonic stem cells. Methods Mol Biol 884, 229, 2012.
4. Wohl, S.G., Schmeer, C.W., and Isenmann, S. Neurogenic potential of stem/progenitor-like cells in the adult mammalian eye. Prog Retin Eye Res 31, 213, 2012.
5. Inoue, T., Coles, B.L., Dorval, K., Bremner, R., Bessho, Y., Kageyama, R., Hino, S., Matsuoka, M., Craft, C.M., McInnes, R.R., Tremblay, F., Prusky, G.T., and van der Kooy, D. Maximizing functional photoreceptor differentiation from adult human retinal stem cells. Stem Cells 28, 489, 2010.
6. 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., Perez, E.T., Zhong, X., Canto- Soler, M.V., and Gamm, D.M. 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, 2012.
7. Mellough, C.B., Sernagor, E., Moreno-Gimeno, I., Steel, D.H., and Lako, M. Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem Cells 30, 673, 2012.
8. Idelson, M., Alper, R., Obolensky, A., Ben-Shushan, E., Hemo, I., Yachimovich-Cohen, N., Khaner, H., Smith, Y., Wiser, O., Gropp, M., Cohen, M.A., Even-Ram, S., Berman- Zaken, Y., Matzrafi, L., Rechavi, G., Banin, E., and Reubinoff, B. Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell Stem Cell 5, 396, 2009.
9. Lu, B., Malcuit, C., Wang, S., Girman, S., Francis, P., Lemieux, L., Lanza, R., and Lund, R. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells 27, 2126, 2009.
10. Lamba, D.A., Karl, M.O., Ware, C.B., and Reh, T.A. Efficient generation of retinal progenitor cells from human embryonic stem cells. Proc Natl Acad Sci U S A 103, 12769, 2006.
11. Osakada, F., Ikeda, H., Mandai, M., Wataya, T., Watanabe, K., Yoshimura, N., Akaike, A., Sasai, Y., and Takahashi M. Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat Biotechnol 26, 215, 2008.
12. Bauwens, C.L., Peerani, R., Niebruegge, S., Woodhouse, K.A., Kumacheva, E., Husain, M., and Zandstra, P.W. Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells 26, 2300, 2008.
13. Bratt-Leal, A.M., Carpenedo, R.L., and McDevitt, T.C. Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation. Biotechnol Prog 25, 43, 2009.
14. Watanabe, K., Ueno, M., Kamiya, D., Nishiyama, A., Matsumura, M., Wataya, T., Takahashi, J.B., Nishikawa, S., Nishikawa, S., Muguruma, K., and Sasai, Y. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 25, 681, 2007.
15. Levine, E.M., Fuhrmann, S., and Reh, T.A. Soluble factors and the development of rod photoreceptors. Cell Mol Life Sci 57, 224, 2000.
16. Kelley, M.W., Turner, J.K., and Reh, T.A. Regulation of proliferation and photoreceptor differentiation in fetal human retinal cell cultures. Invest Ophthalmol Vis Sci 36, 1280, 1995.
17. Nistor, G., Seiler, M.J., Yan, F., Ferguson, D., and Keirstead, H.S. Three-dimensional early retinal progenitor 3D tissue constructs derived from human embryonic stem cells. J Neurosci Methods 190, 63, 2010.
18. Tibbetts, M.D., Samuel, M.A., Chang, T.S., and Ho, A.C. Stem cell therapy for retinal disease. Curr Opin Ophthalmol 23, 226, 2012.
19. Freund, C.L., Gregory-Evans, C.Y., Furukawa, T., Papaioannou, M., Looser, J., Ploder, L., Bellingham, J., Ng, D., Herbrick, J.A., Duncan, A., Scherer, S.W., Tsui, L.C., Loutradis-Anagnostou, A., Jacobson, S.G., Cepko, C.L., Bhattacharya, S.S., and McInnes, R.R. Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell 91, 543, 1997.
20. Furukawa, T., Morrow, E.M., and Cepko, C.L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 531, 1997.
21. Chen, S., Wang, Q.L., Nie, Z., Sun, H., Lennon, G., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., and Zack, D.J. Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19, 1017, 1997.
22. West, E.L., Gonzalez-Cordero, A., Hippert, C., Osakada, F., Martinez-Barbera, J.P., Pearson, R.A., Sowden, J.C., Takahashi, M., and Ali, R.R. Defining the integration capacity of embryonic stem cell-derived photoreceptor precursors. Stem Cells 30, 1424, 2012.
23. Peters, C.E., Woodside, S.M., and Eaves, A.C. Isolation of subsets of immune cells. Methods Mol Biol 302, 95, 2005.
24. Kannagi, R., Cochran, N.A., Ishigami, F., Hakomori, S., Andrews, P.W., Knowles, B.B., and Solter, D. Stage-specific embryonic antigens (SSEA-3 and - 4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J 2, 2355, 1983.
25. Bibb, L.C., Holt, J.K., Tarttelin, E.E., Hodges, M.D., Gregory- Evans, K., Rutherford, A., Lucas, R.J., Sowden, J.C., and Gregory-Evans, C.Y. Temporal and spatial expression patterns of the CRX transcription factor and its downstream targets. Critical differences during human and mouse eye development. Hum Mol Genet 10, 1571, 2001.
26. D'Amour, K.A., Bang, A.G., Eliazer, S., Kelly, O.K., Agulnick, A.D., Smart, N.G., Moorman, M.A., Kroon, E., Carpenter, M.K., and Baetge, E.E. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 24, 1392, 2006.
27. Kroon, E., Martinson, L.A, Kadoya, K., Bang, A.G., Kelly, O.G., Eliazer, S., Young, H., Richardson, M., Smart, N.G., Cunningham, J., Agulnick, A.D., D'Amour, K.A., Carpenter, M.K., and Baetge, E.E. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 26, 443, 2008.
28. Scott, C.T., McCormick, J.B., and Owen-Smith, J. And then there were two: use of hESC lines. Nat Biotechnol 27, 696, 2009.
29. Rezania, A., Bruin, J.E., Riedel, M.J., Mojibian, M., Asadi, A., Xu, J., Gauvin, R., Narayan, K., Karanu, F., O'Neil, J.J., Ao, Z., Warnock, G.L., and Kieffer, T.J. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes 61, 2016, 2012.
30. Burridge, P.W., Thompson, S., Millrod, M.A., Weinberg, S., Yuan, X., Peters, A., Mahairaki, V., Koliatsos, V.E., Tung, L., and Zambidis, E.T. A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability. PLoS One 6, e18293, 2011.
31. Kehat, I., Kenyagin-Karsenti, D., Snir, M., Segev, H., Amit, M., Gepstein, A., Livne, E., Binah, O., Itskovitz-Eldor, J., and Gepstein, L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 108, 407, 2001.
32. 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., Pattnaik, B., Thomson, J.A., and Gamm, D.M. Optic vesicle-like structures derived from human pluripotent stem cells facilitate a customized approach to retinal disease treatment. Stem Cells 29, 1206, 2011.
33. Lamba, D.A., Gust, J., and Reh, T.A. Transplantation of human embryonic stem cell-derived photoreceptors restores some visual function in Crx-deficient mice. Cell Stem Cell 4, 73, 2009.
34. Swaroop, A., Kim, D., and Forrest, D. Transcriptional regulation of photoreceptor development and homeostasis in mammalian retina. Nat Rev Neurosci 11, 563, 2010.
35. Mucci, I., Legitimo, A., Compagnino, M., Consolini, R., Migliaccio, P., Metelli, M.R., and Scatena, F. The methodological approach for the generation of human dendritic cells from monocytes affects the maturation state of the resultant dendritic cells. Biologicals 37, 288, 2009.
36. Shin, S.Y., Jang, S., Park, C.J., Chi, H.S., Lee, J.H., Lee, J.H., Lee, K.H., Suh, C., Lim, S.E., and Seo, E.J. Application of an immune-magnetic cell sorting method for CD138-positive plasma cells in FISH analysis of multiple myeloma. Int J Lab Hematol 34, 541, 2012.
37. Alon, R., Bayer, E.A., and Wilchek, M. Affinity cleavage of cell surface antibodies using the avidin-biotin system. J Immunol Methods 165, 127, 1993.
38. Zucchelli, M., Ström, S., Holm, F., Malmgren, H., Sahle?n, S., Religa, P., Hovatta, O., Kere, J., and Inzunza, J. In vivo differentiated human embryonic stem cells can acquire chromosomal aberrations more frequently than in vitro during the same period. Stem Cells Dev 21, 3363, 2012.