GAPTrap: A Simple Expression System for Pluripotent Stem Cells and Their Derivatives

Stem Cell Reports

Volumn 7, Issue 3, 2016, Pages 518-526

  Kao, Tim ^a,b   Labonne, Tanya ^a   Niclis, Jonathan C ^b   Chaurasia, Ritu ^b   Lokmic, Zerina ^a   Qian, Elizabeth ^a,b   Bruveris, Freya F ^a,c   Howden, Sara E ^a,b   Motazedian, Ali ^a,b   Schiesser, Jacqueline V ^c,g   Costa, Magdaline ^c   Sourris, Koula ^a   Ng, Elizabeth ^a   Anderson, David ^a   Giudice, Antonietta ^c   Farlie, Peter ^a,b   Cheung, Michael ^a,b,f   Lamande, Shireen R ^a,b   Penington, Anthony J ^a,b   Parish, Clare L ^b   Thomson, Lachlan H ^b   Rafii, Arash ^d,e   Elliott, David A ^a,b   Elefanty, Andrew G ^a,b,c   Stanley, Edouard G ^a,b,c   more..

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d WEILL CORNELL MEDICAL COLLEGE   (Qatar)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f ROYAL CHILDREN'S HOSPITAL   (Australia)

^g CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

differentiation; expression system; GAPDH; human pluripotent stem cells; lineage tracing; reporter genes

Indexed keywords

ANTIBIOTIC G 418; BETA GALACTOSIDASE; EPITHELIAL CELL ADHESION MOLECULE; FIREFLY LUCIFERASE; GAUSSIA LUCIFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GREEN FLUORESCENT PROTEIN; HYGROMYCIN; PROTEIN; PUROMYCIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DOPAMINERGIC NERVE CELL; ENDODERM; GENE EXPRESSION; GENE EXPRESSION SYSTEM; GENE FUNCTION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; MESODERM; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REPORTER GENE; VENTRAL MESENCEPHALON; CELL DIFFERENTIATION; CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRISPR CAS SYSTEM; CYTOLOGY; GENE VECTOR; GENETICS; METABOLISM; TRANSGENE;

CELL DIFFERENTIATION; CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CRISPR-CAS SYSTEMS; GENE EXPRESSION; GENES, REPORTER; GENETIC VECTORS; HUMANS; PLURIPOTENT STEM CELLS; TRANSCRIPTION ACTIVATOR-LIKE EFFECTOR NUCLEASES; TRANSGENES;

EID: 84990068751     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2016.07.015     Document Type: Article

References (43)

1. Barber, R.D., Harmer, D.W., Coleman, R.A., Clark, B.J., GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol. Genomics 21 (2005), 389–395.
2. Cormack, B.P., Valdivia, R.H., Falkow, S., FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173 (1996), 33–38.
3. Costa, M., Dottori, M., Ng, E., Hawes, S.M., Sourris, K., Jamshidi, P., Pera, M.F., Elefanty, A.G., Stanley, E.G., The hESC line Envy expresses high levels of GFP in all differentiated progeny. Nat. Methods 2 (2005), 259–260.
4. Costa, M., Dottori, M., Sourris, K., Jamshidi, P., Hatzistavrou, T., Davis, R., Azzola, L., Jackson, S., Lim, S.M., Pera, M., et al. A method for genetic modification of human embryonic stem cells using electroporation. Nat. Protoc. 2 (2007), 792–796.
5. Costa, M., Sourris, K., Hatzistavrou, T., Elefanty, A.G., Stanley, E.G., Expansion of human embryonic stem cells in vitro. Curr. Protoc. Stem Cell Biol., Chapter 1, 2008 Unit 1C.1.1–1C.1.7.
6. Davis, R.P., Costa, M., Grandela, C., Holland, A.M., Hatzistavrou, T., Micallef, S.J., Li, X., Goulburn, A.L., Azzola, L., Elefanty, A.G., et al. A protocol for removal of antibiotic resistance cassettes from human embryonic stem cells genetically modified by homologous recombination or transgenesis. Nat. Protoc. 3 (2008), 1550–1558.
7. Elliott, D.A., Braam, S.R., Koutsis, K., Ng, E.S., Jenny, R., Lagerqvist, E.L., Biben, C., Hatzistavrou, T., Hirst, C.E., Yu, Q.C., et al. NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes. Nat. Methods 8 (2011), 1037–1040.
8. Gropp, M., Shilo, V., Vainer, G., Gov, M., Gil, Y., Khaner, H., Matzrafi, L., Idelson, M., Kopolovic, J., Zak, N.B., et al. Standardization of the teratoma assay for analysis of pluripotency of human ES cells and biosafety of their differentiated progeny. PLoS One, 7, 2012, e45532.
9. GTex Consortium, Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science 348 (2015), 648–660.
10. Hockemeyer, D., Soldner, F., Beard, C., Gao, Q., Mitalipova, M., DeKelver, R.C., Katibah, G.E., Amora, R., Boydston, E.A., Zeitler, B., et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 27 (2009), 851–857.
11. Hockemeyer, D., Wang, H., Kiani, S., Lai, C.S., Gao, Q., Cassady, J.P., Cost, G.J., Zhang, L., Santiago, Y., Miller, J.C., et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 29 (2011), 731–734.
12. Howden, S.E., Maufort, J.P., Duffin, B.M., Elefanty, A.G., Stanley, E.G., Thomson, J.A., Simultaneous reprogramming and gene correction of patient fibroblasts. Stem Cell Rep. 5 (2015), 1109–1118.
13. Irion, S., Luche, H., Gadue, P., Fehling, H.J., Kennedy, M., Keller, G., Identification and targeting of the ROSA26 locus in human embryonic stem cells. Nat. Biotechnol. 25 (2007), 1477–1482.
14. Ismail, S.A., Park, H.W., Structural analysis of human liver glyceraldehyde-3-phosphate dehydrogenase. Acta Crystallogr. D Biol. Crystallogr. 61 (2005), 1508–1513.
15. Jang, S.K., Pestova, T.V., Hellen, C.U., Witherell, G.W., Wimmer, E., Cap-independent translation of picornavirus RNAs: structure and function of the internal ribosomal entry site. Enzyme 44 (1990), 292–309.
16. Kriks, S., Shim, J.W., Piao, J., Ganat, Y.M., Wakeman, D.R., Xie, Z., Carrillo-Reid, L., Auyeung, G., Antonacci, C., Buch, A., et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480 (2011), 547–551.
17. Lam, A.J., St-Pierre, F., Gong, Y., Marshall, J.D., Cranfill, P.J., Baird, M.A., McKeown, M.R., Wiedenmann, J., Davidson, M.W., Schnitzer, M.J., et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 9 (2012), 1005–1012.
18. Lian, X., Hsiao, C., Wilson, G., Zhu, K., Hazeltine, L.B., Azarin, S.M., Raval, K.K., Zhang, J., Kamp, T.J., Palecek, S.P., Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. USA 109 (2012), E1848–E1857.
19. Loh, K.M., Ang, L.T., Zhang, J., Kumar, V., Ang, J., Auyeong, J.Q., Lee, K.L., Choo, S.H., Lim, C.Y.Y., Nichane, M., et al. Efficient endoderm induction from human pluripotent stem cells by logically directing signals controlling lineage bifurcations. Cell Stem Cell 14 (2014), 237–252.
20. Luo, Y., Liu, C., Cerbini, T., San, H., Lin, Y., Chen, G., Rao, M.S., Zou, J., Stable enhanced green fluorescent protein expression after differentiation and transplantation of reporter human induced pluripotent stem cells generated by AAVS1 transcription activator-like effector nucleases. Stem Cell Trans. Med. 3 (2014), 821–835.
21. Merzlyak, E.M., Goedhart, J., Shcherbo, D., Bulina, M.E., Shcheglov, A.S., Fradkov, A.F., Gaintzeva, A., Lukyanov, K.A., Lukyanov, S., Gadella, T.W.J., et al. Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 4 (2007), 555–557.
22. Mossman, A.K., Sourris, K., Ng, E., Stanley, E.G., Elefanty, A.G., Mixl1 and oct4 proteins are transiently co-expressed in differentiating mouse and human embryonic stem cells. Stem Cells Dev. 14 (2005), 656–663.
23. Murphy, C.L., Polak, J.M., Differentiating embryonic stem cells: GAPDH, but neither HPRT nor beta-tubulin is suitable as an internal standard for measuring RNA levels. Tissue Eng. 8 (2002), 551–559.
24. Ng, E.S., Davis, R., Stanley, E.G., Elefanty, A.G., A protocol describing the use of a recombinant protein-based, animal product-free medium (APEL) for human embryonic stem cell differentiation as spin embryoid bodies. Nat. Protoc. 3 (2008), 768–776.
25. Niclis, J.C., Pinar, A., Haynes, J.M., Alsanie, W., Jenny, R., Dottori, M., Cram, D.S., Characterization of forebrain neurons derived from late-onset Huntington's disease human embryonic stem cell lines. Front Cell Neurosci., 7, 2013, 37.
26. Ordovas, L., Boon, R., Pistoni, M., Chen, Y., Wolfs, E., Guo, W., Sambathkumar, R., Bobis-Wozowicz, S., Helsen, N., Vanhove, J., et al. Efficient recombinase-mediated cassette exchange in hPSCs to study the hepatocyte lineage reveals AAVS1 locus-mediated transgene inhibition. Stem Cell Rep. 5 (2015), 918–931.
27. Qian, K., Huang, C.-L., Chen, H., Blackbourn, L.W., Chen, Y., Cao, J., Yao, L., Sauvey, C., Du, Z., Zhang, S.-C., A simple and efficient system for regulating gene expression in human pluripotent stem cells and derivatives. Stem Cells 32 (2014), 1230–1238.
28. Santos, E.B., Yeh, R., Lee, J., Nikhamin, Y., Punzalan, B., Punzalan, B., La Perle, K., Larson, S.M., Sadelain, M., Brentjens, R.J., Sensitive in vivo imaging of T cells using a membrane-bound Gaussia princeps luciferase. Nat. Med. 15 (2009), 338–344.
29. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N.G., Palmer, A.E., Tsien, R.Y., Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 22 (2004), 1567–1572.
30. Shultz, L.D., Lyons, B.L., Burzenski, L.M., Gott, B., Chen, X., Chaleff, S., Kotb, M., Gillies, S.D., King, M., Mangada, J., et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174 (2005), 6477–6489.
31. Sim, X., Cardenas-Diaz, F.L., French, D.L., Gadue, P., A doxycycline-inducible system for genetic correction of iPSC disease models. Methods Mol. Biol. 1353 (2015), 13–23.
32. Skelton, R.J.P., Costa, M., Anderson, D.J., Bruveris, F., Finnin, B.W., Koutsis, K., Arasaratnam, D., White, A.J., Rafii, A., Ng, E.S., et al. SIRPA, VCAM1 and CD34 identify discrete lineages during early human cardiovascular development. Stem Cell Res. 13 (2014), 172–179.
33. Smith, J.R., Maguire, S., Davis, L.A., Alexander, M., Yang, F., Chandran, S., ffrench-Constant, C., Pedersen, R.A., Robust, persistent transgene expression in human embryonic stem cells is achieved with AAVS1-targeted integration. Stem Cells 26 (2008), 496–504.
34. Somers, A., Jean, J.-C., Sommer, C.A., Omari, A., Ford, C.C., Mills, J.A., Ying, L., Sommer, A.G., Jean, J.M., Smith, B.W., et al. Generation of transgene-free lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells 28 (2010), 1728–1740.
35. Soriano, P., Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999), 70–71.
36. Stanley, E.G., Biben, C., Allison, J., Hartley, L., Wicks, I.P., Campbell, I.K., McKinley, M., Barnett, L., Koentgen, F., Robb, L., et al. Targeted insertion of a lacZ reporter gene into the mouse Cer1 locus reveals complex and dynamic expression during embryogenesis. Genesis 26 (2000), 259–264.
37. Subach, O.M., Cranfill, P.J., Davidson, M.W., Verkhusha, V.V., An enhanced monomeric blue fluorescent protein with the high chemical stability of the chromophore. PLoS One, 6, 2011, e28674.
38. Szymczak, A.L., Vignali, D.A.A., Development of 2A peptide-based strategies in the design of multicistronic vectors. Expert Opin. Biol. Ther. 5 (2005), 627–638.
39. Szymczak, A.L., Workman, C.J., Wang, Y., Vignali, K.M., Dilioglou, S., Vanin, E.F., Vignali, D.A.A., Correction of multi-gene deficiency in vivo using a single ‘self-cleaving’ 2A peptide-based retroviral vector. Nat. Biotechnol. 22 (2004), 589–594.
40. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., Jones, J.M., Embryonic stem cell lines derived from human blastocysts. Science 282 (1998), 1145–1147.
41. Wood, A.J., Lo, T.-W., Zeitler, B., Pickle, C.S., Ralston, E.J., Lee, A.H., Amora, R., Miller, J.C., Leung, E., Meng, X., et al. Targeted genome editing across species using ZFNs and TALENs. Science, 333, 2011, 307.
42. Wu, H., Liu, X., Jaenisch, R., Double replacement: strategy for efficient introduction of subtle mutations into the murine Col1a-1 gene by homologous recombination in embryonic stem cells. Proc. Natl. Acad. Sci. USA 91 (1994), 2819–2823.
43. Zambrowicz, B.P., Imamoto, A., Fiering, S., Herzenberg, L.A., Kerr, W.G., Soriano, P., Disruption of overlapping transcripts in the ROSA beta geo 26 gene trap strain leads to widespread expression of beta-galactosidase in mouse embryos and hematopoietic cells. Proc. Natl. Acad. Sci. USA 94 (1997), 3789–3794.