Using Zinc Finger Nuclease Technology to Generate CRX-Reporter Human Embryonic Stem Cells as a Tool to Identify and Study the Emergence of Photoreceptors Precursors during Pluripotent Stem Cell Differentiation

Stem Cells

Volumn 34, Issue 2, 2016, Pages 311-321

  Collin, Joseph ^a   Mellough, Carla B ^a   Dorgau, Birthe ^a   Przyborski, Stefan ^b   Moreno Gimeno, Inmaculada ^c   Lako, Majlinda ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

^c CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

Author keywords

Cone rod homeobox; Human embryonic stem cells; Photoreceptor precursors; Zinc finger nucleases

Indexed keywords

CONE ROD HOMEOBOX; GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; PUROMYCIN; RECOVERIN; RETINA S ANTIGEN; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; 3' UNTRANSLATED REGION; CONE ROD HOMEOBOX PROTEIN; RIBONUCLEASE; TRANSACTIVATOR PROTEIN; ZINC FINGER PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CLONE; EMBRYOID BODY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENOMIC INSTABILITY; HOMOZYGOTE; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; IMMUNOCYTOCHEMISTRY; NERVE CELL; PHOTORECEPTOR; PIGMENT EPITHELIUM; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; REPORTER GENE; RETINA; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BIOSYNTHESIS; CELL LINE; GENETICS; METABOLISM; PHOTORECEPTOR CELL;

3' UNTRANSLATED REGIONS; CELL DIFFERENTIATION; CELL LINE; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; HUMAN EMBRYONIC STEM CELLS; HUMANS; PHOTORECEPTOR CELLS; RIBONUCLEASES; TRANS-ACTIVATORS; ZINC FINGERS;

EID: 84958244267     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2240     Document Type: Article

References (34)

1. Collin J, Lako M,. Concise review: Putting a finger on stem cell biology: Zinc finger nuclease-driven targeted genetic editing in human pluripotent stem cells. Stem Cells 2011; 29: 1021-1033
2. Zwaka TP, Thomson JA,. Homologous recombination in human embryonic stem cells. Nat Biotechnol 2003; 21: 319-321.
3. Hockemeyer D, Soldner F, Beard C, et al., Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 2009; 27: 851-857.
4. Zou J, Maeder ML, Mali P, et al., Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 2009; 5: 97-110.
5. Stewart R, Yang C, Anyfantis G, et al., Silencing of the expression of pluripotent driven-reporter genes stably transfected into human pluripotent cells. Regen Med 2008; 3: 505-522.
6. Mellough CB, Collin, J, Sernagor E, et al., Lab generated retina: Realizing the dream. Vis Neurosci 2014; 31: 317-332.
7. MacLaren RE, Pearson RA, MacNeil A, et al., Retinal repair by transplantation of photoreceptor precursors. Nature 2006; 444: 203-207.
8. Lakowski J, Baron M, Bainbridge J, et al., Cone and rod photoreceptor transplantation in models of the childhood retinopathy Leber congenital amaurosis using flow-sorted Crx-positive donor cells. Hum Mol Genet 2010; 19: 4545-4559.
9. Eiraku M, Takata N, Ishibashi H, et al., Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 2011; 472: 51-56.
10. Nakano T, Ando S, Takata N, et al., Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 2012; 10: 771-785.
11. Zhong X, Gutierrez C, Xue T, et al., Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat Commun 2014; 5: 4047.
12. Mellough CB, Collin J, Khazim M, et al., IGF-1 signalling plays an important role in the formation of three dimensional laminated neural retina and other ocular structures from human embryonic stem cells. Stem Cells 2015; 33: 2416-2430.
13. Furukawa T, Morrow EM, Cepko CL,. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 1997; 91: 531-541.
14. Freund CL, Gregory-Evans CY, Furukawa T, et al., Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell 1997; 91: 543-553.
15. Samson M, Emerson MM, Cepko CL,. Robust marking of photoreceptor cells and pinealocytes with several reporters under control of the Crx gene. Dev Dyn 2009; 238: 3218-3225.
16. Mellough CB, Sernagor E, Moreno-Gimeno I,. Efficient stage-specific differentiation of human pluripotent stem cells toward retinal photoreceptor cells. Stem Cells 2012; 30: 673-686.
17. Fine EJ, Cradick TJ, Zhao CL, et al., An online bioinformatics tool predicts zinc finger and TALE nuclease off-target activity. Nucleic Acids Research 2014; 42: e42.
18. Stojkovic M, Lako M, Stojkovic P, et al., Derivation of human embryonic stem cells from day-8 blastocysts recovered after three-step in vitro culture. Stem Cells 2004; 22: 790-797
19. Kaewkhaw R, Kaya KD, Brooks M, 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 10.1002/stem.2122.
20. Tanaka T, Yokoi T, Tamalu T, et al., Generation of retinal ganglion cells with functional axons from human induced pluripotent stem cells. Sci Rep 2015; 5: 8344.
21. Lamba DA, McUsic A, Hirata RK, et al., Generation,purification and transplantation of photoreceptors derived from humaninduced pluripotent stem cells. PLoS One 2010; 5: e8763.
22. Barrett LW, Fletcher S, Wilton SD,. Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci 2012; 69: 3613-3634.
23. Porteous MH, Caroll D,. Gene targeting using zinc finger nucleases. Nat Biotechnol 2005; 23: 967-973.
24. Zhang C, Xiao B, Jiang Y, et al., Efficient editing of malaria parasite genome using the CRISPR/Cas9 system. MBio 2014; 5: e01414-14.
25. Furukawa A, Koike C, Lippincott P, et al., The mouse Crx 5′-upstream transgene sequence directs cell-specific and developmentally regulated expression in retinal photoreceptor cells. J Neurosci 2002; 22: 1640-1647.
26. Bibb LC, Holt JK, Tarttelin EE, et al., 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 2001; 10: 1571-1579.
27. Chen S, Wang QL, Nie Z, et al., Crx, a Novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 1997; 19: 1017-1030.
28. Sakuma H, Murakami A, Fujimaki T, et al., Isolation and characterization of the human X-arrestin gene. Gene 1998; 224: 87-95
29. Furukawa T, Morrow EM, Li T, et al., Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat Genet 1999; 23: 466-470.
30. Kimura A, Singh D, Wawrousek EF, et al., Both PCE-1/RX and OTX/CRX interactions are necessary for photoreceptor-specific gene expression. J Biol Chem 2000; 275: 1152-1160.
31. Zhu X, Ma B, Babu S, et al., Mouse cone arrestin gene characterization: Promoter targets expression to cone photoreceptors. FEBS Lett 2002; 524: 116-122.
32. Pickrell SW, Zhu X, Wang X, et al., Deciphering the contribution of known cis-elements in the mouse cone arrestin gene to its cone-specific expression. Invest Ophthalmol Vis Sci 2004; 45: 3877-3884.
33. Fujimaki T, Huang ZY, Kitagawa H, et al., Truncation and mutagenesis analysis of the human X-arrestin gene promoter. Gene 2004; 339: 139-147.
34. Rapaport DH, Stone J,. The area centralis of the retina in the cat and other mammals: Focal point for function and development of the visual system. Neuroscience 1984; 11: 289-301.