Non-integrating episomal plasmid-based reprogramming of human amniotic fluid stem cells into induced pluripotent stem cells in chemically defined conditions

Cell Cycle

Volumn 15, Issue 2, 2016, Pages 234-249

  Slamecka, Jaroslav ^a,b,c   Salimova, Lilia ^a,d   McClellan, Steven ^b   van Kelle, Mathieu ^a,e   Kehl, Debora ^a   Laurini, Javier ^f   Cinelli, Paolo ^a,g   Owen, Laurie ^b   Hoerstrup, Simon P ^a   Weber, Benedikt ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF SOUTH ALABAMA   (United States)

^c RESEARCH INSTITUTE OF ANIMAL PRODUCTION   (Slovakia)

^d EPFL   (Switzerland)

^e EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^f UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

amniotic fluid stem cells; E8; episomal reprogramming; induced pluripotent stem cells; PluriTest; vitronectin; xeno free culture

Indexed keywords

EPSTEIN BARR VIRUS ANTIGEN 1; OCTAMER TRANSCRIPTION FACTOR 4; ORIP EBNA 1; PLASMID VECTOR; RECOMBINANT PROTEIN; RECOMBINANT VITRONECTIN; STAGE SPECIFIC EMBRYO ANTIGEN 1; STAGE SPECIFIC EMBRYO ANTIGEN 4; TRA 1 60; TRA 1 81; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; VITRONECTIN; BIOLOGICAL MARKER; CD15 ANTIGEN; CULTURE MEDIUM; HOMEODOMAIN PROTEIN; MEMBRANE ANTIGEN; NANOG PROTEIN, HUMAN; POU5F1 PROTEIN, HUMAN; PROTEOGLYCAN; SOX2 PROTEIN, HUMAN; STAGE SPECIFIC EMBRYO ANTIGEN; STAGE-SPECIFIC EMBRYONIC ANTIGEN-4; TRA-1-60 ANTIGEN, HUMAN; TRA-1-81 ANTIGEN, HUMAN; TRANSCRIPTION FACTOR SOX;

AMNIOTIC FLUID STEM CELL; ARTICLE; CELL PROLIFERATION; CELLS BY BODY ANATOMY; COMPUTER MODEL; CONTROLLED STUDY; CULTURE MEDIUM; EPISOME; EPITHELIOID CELL; GENE DELIVERY SYSTEM; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROARRAY ANALYSIS; NUCLEAR REPROGRAMMING; PLASMID; PLURIPOTENT STEM CELL; PLURITEST SCORE; SCORING SYSTEM; SOMATIC CELL; STEM CELL CULTURE; TERATOMA; TRANSGENE; AMNION FLUID; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; INDUCED PLURIPOTENT STEM CELL; METABOLISM; PHARMACOLOGY; PROCEDURES; PROTEIN MICROARRAY;

AMNIOTIC FLUID; ANTIGENS, CD15; ANTIGENS, SURFACE; BIOMARKERS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR REPROGRAMMING; CULTURE MEDIA; GENE EXPRESSION; HOMEODOMAIN PROTEINS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NANOG HOMEOBOX PROTEIN; OCTAMER TRANSCRIPTION FACTOR-3; PLASMIDS; PROTEIN ARRAY ANALYSIS; PROTEOGLYCANS; SOXB1 TRANSCRIPTION FACTORS; STAGE-SPECIFIC EMBRYONIC ANTIGENS; TRANSFECTION;

EID: 84962853117     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.1080/15384101.2015.1121332     Document Type: Article

References (49)

1. Y.-H.Loh, S.Agarwal, I.-H.Park, A.Urbach, H.Huo, G.C.Heffner, K.Kim, J.D.Miller, K.Ng, G.Q.Daley. Generation of induced pluripotent stem cells from human blood. Blood 2009; 113:5476-9; PMID:19299331; http://dx.doi.org/10.1182/blood-2009-02-204800
2. P.De Coppi, G.BartschJr, M.M.Siddiqui, T.Xu, C.C.Santos, L.Perin, G.Mostoslavsky, A.C.Serre, E.Y.Snyder, J.J.Yoo, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol 2007; 25:100-6; PMID:17206138; http://dx.doi.org/10.1038/nbt1274
3. D.Schmidt, J.Achermann, B.Odermatt, C.Breymann, A.Mol, M.Genoni, G.Zund, S.P.Hoerstrup. Prenatally fabricated autologous human living heart valves based on amniotic fluid derived progenitor cells as single cell source. Circulation 2007; 116:I64-70; PMID:17846327; http://dx.doi.org/10.1161/CIRCULATIONAHA.107.184051
4. D.Schmidt, J.Achermann, B.Odermatt, M.Genoni, G.Zund, S.P.Hoerstrup. Cryopreserved amniotic fluid-derived cells: a lifelong autologous fetal stem cell source for heart valve tissue engineering. J Heart Valve Dis 2008; 17:446-55; PMID:18751475
5. B.Weber, M.Y.Emmert, L.Behr, R.Schoenauer, C.Brokopp, C.Drögemüller, P.Modregger, M.Stampanoni, D.Vats, M.Rudin, et al. Prenatally engineered autologous amniotic fluid stem cell-based heart valves in the fetal circulation. Biomaterials 2012; 33:4031-43; PMID:22421386; http://dx.doi.org/10.1016/j.biomaterials.2011.11.087
6. M.Zaim, S.Karaman, G.Cetin, S.Isik. Donor age and long-term culture affect differentiation and proliferation of human bone marrow mesenchymal stem cells. Ann Hematol 2012; 91:1175-86; PMID:22395436; http://dx.doi.org/10.1007/s00277-012-1438-x
7. S.Bork, S.Pfister, H.Witt, P.Horn, B.Korn, A.D.Ho, W.Wagner. DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell 2010; 9:54-63; PMID:19895632; http://dx.doi.org/10.1111/j.1474-9726.2009.00535.x
8. T.Phermthai, S.Suksompong, N.Tirawanchai, S.Issaragrisil, S.Julavijitphong, S.Wichitwiengrat, D.Silpsorn, P.Pokathikorn. Epigenetic Analysis and Suitability of Amniotic Fluid Stem Cells for Research and Therapeutic Purposes. Stem Cells Dev 2013; 22:1319-28; PMID:23249260; http://dx.doi.org/10.1089/scd.2012.0371
9. P.Jelinic, P.Shaw. Loss of imprinting and cancer. J Pathol 2007; 211:261-68; PMID:17177177; http://dx.doi.org/10.1002/path.2116
10. K.Kim, A.Doi, B.Wen, K.Ng, R.Zhao, P.Cahan, J.Kim, M.J.Aryee, H.Ji, L.I.Ehrlich, A.Yabuuchi, et al. Epigenetic memory in induced pluripotent stem cells. Nature 2010; 467:285-90; PMID:20644535; http://dx.doi.org/10.1038/nature09342
11. D.Moschidou, S.Mukherjee, M.P.Blundell, K.Drews, G.N.Jones, H.Abdulrazzak, B.Nowakowska, A.Phoolchund, K.Lay, T.S.Ramasamy, et. al. Valproic acid confers functional pluripotency to human amniotic fluid stem cells in a transgene-free approach. Mol Ther 2012; 20:1953-67; PMID:22760542; http://dx.doi.org/10.1038/mt.2012.117
12. S.Eminli, A.Foudi, M.Stadtfeld, N.Maherali, T.Ahfeldt, G.Mostoslavsky, H.Hock, K.Hochedlinger. Differentiation stage determines potential of hematopoietic cells for reprogramming into induced pluripotent stem cells. Nat Genet 2009 ; 41:968-76; PMID:19668214; http://dx.doi.org/10.1038/ng.428
13. R.Zweigerdt, R.Olmer, H.Singh, A.Haverich, U.Martin. Scalable expansion of human pluripotent stem cells in suspension culture. Nat Prot 2011; 6:689-700; http://dx.doi.org/10.1038/nprot.2011.318
14. G.Chen, D.R.Gulbrason, Z.Hou, J.Bolin, V.Ruotti, M.D.Probasco, K.Smuga-Otto, S.E.Howden, N.R.Diol, N.E.Propson, et al. Chemically defined conditions for human iPSC derivation and culture. Nat Methods 2011; 8:424-29; PMID:21478862; http://dx.doi.org/10.1038/nmeth.1593
15. C.Li, J.Zhou, G.Shi, Y.Ma, Y.Yang, J.Gu, H.Yu, S.Jin, Z.Wei, F.Chen, Y.Jin. Pluripotency can be rapidly and efficiently induced in human amniotic fluid-derived cells. Hum Mol Genet 2009; 18:4340-49; PMID:19679563; http://dx.doi.org/10.1093/hmg/ddp386
16. E.Galende, I.Karakikes, L.Edelmann, R.J.Desnick, T.Kerenyi, G.Khoueiry, J.Lafferty, J.T.McGinn, M.Brodman, V.Fuster, et al. Amniotic fluid cells are more efficiently reprogrammed to pluripotency than adult cells. Cell Reprogramm 2010; 12:117-25; http://dx.doi.org/10.1089/cell.2009.0077
17. K.Wolfrum, Y.Wang, A.Prigione, K.Sperling, H.Lehrach, J.Adjaye. The LARGE principle of cellular reprogramming: lost, acquired and retained gene expression in foreskin and amniotic fluid-derived human iPS cells. PLoS One 2010; 5:e13703; PMID:21060825; http://dx.doi.org/10.1371/journal.pone.0013703
18. H.E.Lu, Y.C.Yang, S.M.Chen, H.L.Su, P.C.Huang, M.S.Tsai, T.H.Wang, C.P.Tseng, S.W.Hwang. Modeling neurogenesis impairment in Down syndrome with induced pluripotent stem cells from Trisomy 21 amniotic fluid cells. Exp Cell Res 2013; 319:498-505; PMID:23041301; http://dx.doi.org/10.1016/j.yexcr.2012.09.017
19. Y.Fan, Y.Luo, X.Chen, Q.Li, X.Sun. Generation of human β-thalassemia induced pluripotent stem cells from amniotic fluid cells using a single excisable lentiviral stem cell cassette. J Reprod Dev 2012; 58:404-9; PMID:22498813; http://dx.doi.org/10.1262/jrd.2011-046
20. J.Yu, K.Hu, K.Smuga-Otto, S.Tian, R.Stewart, I.I.Slukvin, J.A.Thomson. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009; 324:797-801; PMID:19325077; http://dx.doi.org/10.1126/science.1172482
21. L.Cheng, N.F.Hansen, L.Zhao, Y.Du, C.Zou, F.X.Donovan, B.K.Chou, G.Zhou, S.Li, S.N.Dowey, et al. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 2012; 10:337-44; PMID:22385660; http://dx.doi.org/10.1016/j.stem.2012.01.005
22. J.Beers, D.R.Gulbranson, N.George, L.I.Siniscalchi, J.Jones, J.A.Thomson, G.Chen. Passaging and colony expansion of human pluripotent stem cells by enzyme-free dissociation in chemically defined culture conditions. Nat Protoc 2012; 7:2029-40; PMID:23099485; http://dx.doi.org/10.1038/nprot.2012.130
23. K.Hu, J.Yu, K.Suknuntha, S.Tian, K.Montgomery, K.D.Choi, R.Stewart, J.A.Thomson, I.I.Slukvin. Efficient generation of transgene-free induced pluripotent stem cells from normal and neoplastic bone marrow and cord blood mononuclear cells. Blood 2011; 117:e109-19; PMID:21296996; http://dx.doi.org/10.1182/blood-2010-07-298331
24. E.M.Chan, E.M.Chan, S.Ratanasirintrawoot, I.-H.Park, P.D.Manos, Y.-H.Loh, H.Huo, J.D.Miller, O.Hartung, J.Rho, et al. Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells. Nat Biotechnol 2009; 27:1033-37; PMID:19826408; http://dx.doi.org/10.1038/nbt.1580
25. A.Nanbo, A.Sugden, B.Sugden. The coupling of synthesis and partitioning of EBV's plasmid replicon is revealed in live cells. EMBO J 2007; 26:4252-62; PMID:17853891; http://dx.doi.org/10.1038/sj.emboj.7601853
26. G.Liang, Y.Zhang. Embryonic stem cell and induced pluripotent stem cell: an epigenetic perspective. Cell Res 2013; 23:49-69; PMID:23247625; http://dx.doi.org/10.1038/cr.2012.175
27. G.Liang, J.He, Y.Zhang. Kdm2b promotes induced pluripotent stem cell generation by facilitating gene activation early in reprogramming. Nat Cell Biol 2012; 14:457-66; PMID:22522173; http://dx.doi.org/10.1038/ncb2483
28. T.T.Onder, N.Kara, A.Cherry, A.U.Sinha, N.Zhu, K.M.Bernt, P.Cahan, B.O.Marcarci, J.Unternaehrer, P.B.Gupta, et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 2012; 483:598-602; PMID:22388813; http://dx.doi.org/10.1038/nature10953
29. R.Li, J.Liang, S.Ni, T.Zhou, X.Qing, H.Li, W.He, J.Chen, F.Li, Q.Zhuang, et al. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010; 7:51-63; PMID:20621050; http://dx.doi.org/10.1016/j.stem.2010.04.014
30. P.Samavarchi-Tehrani, A.Golipour, L.David, H.K.Sung, T.A.Beyer, A.Datti, K.Woltjen, A.Nagy, J.L.Wrana. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010; 7:64-77; PMID:20621051; http://dx.doi.org/10.1016/j.stem.2010.04.015
31. T.S.Mikkelsen, J.Hanna, X.Zhang, M.Ku, M.Wernig, P.Schorderet, B.E.Bernstein, R.Jaenisch, E.S.Lander, A.Meissner. Dissecting direct reprogramming through integrative genomic analysis. Nature 2008; 454:49-55; PMID:18509334; http://dx.doi.org/10.1038/nature07056
32. G.Liang, O.Taranova, K.Xia, Y.Zhang. Butyrate promotes induced pluripotent stem cell generation. J Biol Chem 2010; 285:25516-21; PMID:20554530; http://dx.doi.org/10.1074/jbc.M110.142059
33. Y.Buganim, D.A.Faddah, A.W.Cheng, E.Itskovich, S.Markoulaki, K.Ganz, S.L.Klemm, A.van Oudenaarden, R.Jaenisch. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 2012; 150:1209-22; PMID:22980981; http://dx.doi.org/10.1016/j.cell.2012.08.023
34. T.W.Theunissen, R.Jaenisch. Molecular control of induced pluripotency. Cell Stem Cell 2014; 14:720-34; PMID:24905163; http://dx.doi.org/10.1016/j.stem.2014.05.002
35. K.Ohnishi, K.Semi, T.Yamamoto, M.Shimizu, A.Tanaka, K.Mitsunaga, K.Okita, K.Osafune, Y.Arioka, T.Maeda, et al. Premature termination of reprogramming in vivo leads to cancer development through altered epigenetic regulation. Cell 2014; 156:663-77; PMID:24529372; http://dx.doi.org/10.1016/j.cell.2014.01.005
36. C.R.Goding, D.Pei, X.Lu. Cancer: pathological nuclear reprogramming. Nature Reviews Cancer 2014; 14:568-73; PMID:25030952; http://dx.doi.org/10.1038/nrc3781
37. S.Efroni, R.Duttagupta, J.Cheng, H.Dehghani, D.J.Hoeppner, C.Dash, D.P.Bazett-Jones, S.Le Grice, R.D.McKay, K.H.Buetow, et al. Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2008; 2:437-47; PMID:18462694; http://dx.doi.org/10.1016/j.stem.2008.03.021
38. J.Krejci, R.Uhlirova, G.Galiova, S.Kozubek, J.Smigova, E.Bartova. Genome-wide reduction in H3K9 acetylation during human embryonic stem cell differentiation. J Cell Physiol 2009; 219:677-87; PMID:19202556; http://dx.doi.org/10.1002/jcp.21714
39. X.Li, L.Li, R.Pandey, J.S.Byun, K.Gardner, Z.Qin, Y.Dou. The histone acetyltransferase MOF is a key regulator of the embryonic stem cell core transcriptional network. Cell Stem Cell 2012; 11:163-78; PMID:22862943; http://dx.doi.org/10.1016/j.stem.2012.04.023
40. P.Mali, B.K.Chou, J.Yen, Z.Ye, J.Zou, S.Dowey, R.A.Brodsky, J.E.Ohm, W.Yu, S.B.Baylin, et al. Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes. Stem Cells 2010; 28:713-20; PMID:20201064; http://dx.doi.org/10.1002/stem.402
41. D.,.R.Huangfu R.Maehr, W.Guo, A.Eijkelenboom, M.Snitow, A.E.Chen, D.A.Melton. Induction of pluripotent stem cells by defined factors is greatly improved by small molecule compounds. Nat Biotechnol 2008; 26:795-97; PMID:18568017; http://dx.doi.org/10.1038/nbt1418
42. M.Martí, L.Mulero, C.Pardo, C.Morera, M.Carrió, L.Laricchia-Robbio, C.R.Esteban, J.C.I.Belmonte. Characterization of pluripotent stem cells. Nat Prot 2013; 8:223-53; PMID:Can't; http://dx.doi.org/10.1038/nprot.2012.154
43. Y.Takashima, G.Guo, R.Loos, J.Nichols, G.Ficz, F.Krueger, D.Oxley, F.Santos, J.Clarke, W.Mansfield, et al. Resetting transcription factor control circuitry toward ground-state pluripotency in human. Cell 2014; 158:1254-69; PMID:25215486; http://dx.doi.org/10.1016/j.cell.2014.08.029
44. F.J.Müller, J.Goldmann, P.Löser, J.F.Loring. A call to standardize teratoma assays used to define human pluripotent cell lines. Cell Stem Cell 2010; 6:412-14; PMID:20452314; http://dx.doi.org/10.1016/j.stem.2010.04.009
45. F.J.Müller, B.M.Schuldt, R.Williams, D.Mason, G.Altun, E.P.Papapetrou, S.Danner, J.E.Goldmann, A.Herbst, N.O.Schmidt, et al. A bioinformatic assay for pluripotency in human cells. Nat Methods 2013; 8:315-17; http://dx.doi.org/10.1038/nmeth.1580
46. K.I.Lee, H.T.Kim, D.Y.Hwang. Footprint- and xeno-free human iPSCs derived from urine cells using extracellular matrix-based culture conditions. Biomaterials 2014; 35:8330-38; PMID:24994040; http://dx.doi.org/10.1016/j.biomaterials.2014.05.059
47. O.Parolini, M.Soncini, M.Evangelista, D.Schmidt. Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? Regen Med 2009; 4:275-91; PMID:19317646; http://dx.doi.org/10.2217/17460751.4.2.275
48. G.Jiang, J.Di Bernardo, M.M.Maiden, L.G.Villa-Diaz, O.S.Mabrouk, P.H.Krebsbach, K.S.O'Shea, S.M.Kunisaki. Human transgene-free amniotic fluid-derived induced pluripotent stem cells for autologous cell therapy. Stem Cells Dev 2014; 23:2613-25; PMID:25014361; http://dx.doi.org/10.1089/scd.2014.0110
49. A.M.Drozd, M.P.Walczak, S.Piaskowski, E.Stoczynska-Fidelus, P.Rieske, D.P.Grzela. Generation of human iPSCs from cells of fibroblastic and epithelial origin by means of the oriP/EBNA-1 episomal reprogramming system. Stem Cell Res Ther 2015; 6:122; PMID:26088261; http://dx.doi.org/10.1186/s13287-015-0112-3