Induced pluripotent mesenchymal stromal cell clones retain donor-derived differences in DNA methylation profiles

Molecular Therapy

Volumn 21, Issue 1, 2013, Pages 240-250

  Shao, Kaifeng ^a   Koch, Carmen ^b   Gupta, Manoj K ^a   Lin, Qiong ^c   Lenz, Michael ^b   Laufs, Stephanie ^d   Denecke, Bernd ^c   Schmidt, Manfred ^d   Linke, Matthias ^e   Hennies, Hans C ^a,f,g   Hescheler, Jürgen ^a   Zenke, Martin ^b,c   Zechner, Ulrich ^e   Šarić, Tomo ^a   Wagner, Wolfgang ^b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

^f UNIVERSITY OF COLOGNE   (Germany)

^g INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; REX PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BONE MARROW CELL; CELL ASSAY; CELL CLONE; CELL DIFFERENTIATION; CELL ISOLATION; CLONAL VARIATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; HUMAN; HUMAN CELL; MESENCHYMAL STROMA CELL; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

EID: 84871927954     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.207     Document Type: Article

References (50)

1. Zhu, H, Lensch, MW, Cahan, P and Daley, GQ (2011). Investigating monogenic andcomplex diseases with pluripotent stem cells. Nat Rev Genet 12: 266-275.
2. Zhao, XY, Li, W, Lv, Z, Liu, L, Tong, M, Hai, T et al. (2009). iPS cells produce viablemice through tetraploid complementation. Nature 461: 86-90.
3. Patel, M and Yang, S (2010). Advances in reprogramming somatic cells to inducedpluripotent stem cells. Stem Cell Rev 6: 367-380.
4. Carette, JE, Pruszak, J, Varadarajan, M, Blomen, VA, Gokhale, S, Camargo, FDet al. (2010). Generation of iPSCs from cultured human malignant cells. Blood115: 4039-4042.
5. Sun, N, Panetta, NJ, Gupta, DM, Wilson, KD, Lee, A, Jia, F et al. (2009). Feeder-freederivation of induced pluripotent stem cells from adult human adipose stem cells. ProcNatl Acad Sci USA 106: 15720-15725.
6. Sugii, S, Kida, Y, Kawamura, T, Suzuki, J, Vassena, R, Yin, YQ et al. (2010). Human andmouse adipose-derived cells support feeder-independent induction of pluripotentstem cells. Proc Natl Acad Sci USA 107: 3558-3563.
7. Lister, R, Pelizzola, M, Kida, YS, Hawkins, RD, Nery, JR, Hon, G et al. (2011). Hotspotsof aberrant epigenomic reprogramming in human induced pluripotent stem cells.Nature 471: 68-73.
8. Yan, X, Qin, H, Qu, C, Tuan, RS, Shi, S and Huang, GT (2010). iPS cells reprogrammedfrom human mesenchymal-like stem/progenitor cells of dental tissue origin. Stem CellsDev 19: 469-480.
9. Oda, Y, Yoshimura, Y, Ohnishi, H, Tadokoro, M, Katsube, Y, Sasao, M et al. (2010).Induction of pluripotent stem cells from human third molar mesenchymal stromalcells. J Biol Chem 285: 29270-29278.
10. Kim, MJ, Son, MJ, Son, MY, Seol, B, Kim, J, Park, J et al. (2011). Generation of humaninduced pluripotent stem cells from osteoarthritis patient-derived synovial cells.Arthritis Rheum 63: 3010-3021.
11. Park, IH, Arora, N, Huo, H, Maherali, N, Ahfeldt, T, Shimamura, A et al. (2008).Disease-specific induced pluripotent stem cells. Cell 134: 877-886.
12. Ohnishi, H, Oda, Y, Aoki, T, Tadokoro, M, Katsube, Y, Ohgushi, H et al. (2012). Acomparative study of induced pluripotent stem cells generated from frozen, stockedbone marrow-and adipose tissue-derived mesenchymal stem cells. J Tissue Eng RegenMed 6: 261-271.
13. Doi, A, Park, IH, Wen, B, Murakami, P, Aryee, MJ, Irizarry, R et al. (2009). Differentialmethylation of tissue-and cancer-specific CpG island shores distinguishes humaninduced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat Genet41: 1350-1353.
14. Deng, J, Shoemaker, R, Xie, B, Gore, A, LeProust, EM, Antosiewicz-Bourget, J et al.(2009). Targeted bisulfite sequencing reveals changes in DNA methylation associatedwith nuclear reprogramming. Nat Biotechnol 27: 353-360.
15. Kim, K, Doi, A, Wen, B, Ng, K, Zhao, R, Cahan, P et al. (2010). Epigenetic memory ininduced pluripotent stem cells. Nature 467: 285-290.
16. Ohi, Y, Qin, H, Hong, C, Blouin, L, Polo, JM, Guo, T et al. (2011). Incomplete DNAmethylation underlies a transcriptional memory of somatic cells in human iPS cells.Nat Cell Biol 13: 541-549.
17. Bock, C, Kiskinis, E, Verstappen, G, Gu, H, Boulting, G, Smith, ZD et al. (2011).Reference Maps of human ES and iPS cell variation enable high-throughputcharacterization of pluripotent cell lines. Cell 144: 439-452.
18. Nishino, K, Toyoda, M, Yamazaki-Inoue, M, Fukawatase, Y, Chikazawa, E, Sakaguchi, Het al. (2011). DNA methylation dynamics in human induced pluripotent stem cellsover time. PLoS Genet 7: e1002085.
19. Polo, JM, Liu, S, Figueroa, ME, Kulalert, W, Eminli, S, Tan, KY et al. (2010). Celltype of origin influences the molecular and functional properties of mouse inducedpluripotent stem cells. Nat Biotechnol 28: 848-855.
20. Kim, K, Zhao, R, Doi, A, Ng, K, Unternaehrer, J, Cahan, P et al. (2011). Donor celltype can influence the epigenome and differentiation potential of human inducedpluripotent stem cells. Nat Biotechnol 29: 1117-1119.
21. Bibikova, M, Barnes, B, Tsan, C, Ho, V, Klotzle, B, Le, JM et al. (2011). Highdensity DNA methylation array with single CpG site resolution. Genomics 98:288-295.
22. Sandoval, J, Heyn, H, Moran, S, Serra-Musach, J, Pujana, MA, Bibikova, M et al.(2011). Validation of a DNA methylation microarray for 450,000 CpG sites in thehuman genome. Epigenetics 6: 692-702.
23. Dominici, M, Le Blanc, K, Mueller, I, Slaper-Cortenbach, I, Marini, F, Krause, D et al.(2006). Minimal criteria for defining multipotent mesenchymal stromal cells. TheInternational Society for Cellular Therapy position statement. Cytotherapy 8: 315-317. (Pubitemid 44269669)
24. Mler, FJ, Schuldt, BM, Williams, R, Mason, D, Altun, G, Papapetrou, EP et al. (2011).A bioinformatic assay for pluripotency in human cells. Nat Methods 8: 315-317.
25. Gabriel, R, Eckenberg, R, Paruzynski, A, Bartholomae, CC, Nowrouzi, A, Arens, A et al.(2009). Comprehensive genomic access to vector integration in clinical gene therapy.Nat Med 15: 1431-1436.
26. Lister, R, Pelizzola, M, Dowen, RH, Hawkins, RD, Hon, G, Tonti-Filippini, J et al.(2009). Human DNA methylomes at base resolution show widespread epigenomicdifferences. Nature 462: 315-322.
27. Boulting, GL, Kiskinis, E, Croft, GF, Amoroso, MW, Oakley, DH, Wainger, BJ et al.(2011). A functionally characterized test set of human induced pluripotent stem cells.Nat Biotechnol 29: 279-286.
28. Kaminsky, ZA, Tang, T, Wang, SC, Ptak, C, Oh, GH, Wong, AH et al. (2009). DNAmethylation profiles in monozygotic and dizygotic twins. Nat Genet 41: 240-245.
29. Tan, KY, Eminli, S, Hettmer, S, Hochedlinger, K and Wagers, AJ (2011). Efficientgeneration of iPS cells from skeletal muscle stem cells. PLoS ONE 6: e26406.
30. Schallmoser, K, Bartmann, C, Rohde, E, Reinisch, A, Kashofer, K, Stadelmeyer, Eet al. (2007). Human platelet lysate can replace fetal bovine serum for clinical-scaleexpansion of functional mesenchymal stromal cells. Transfusion 47: 1436-1446. (Pubitemid 47101060)
31. Cholewa, D, Stiehl, T, Schellenberg, A, Bokermann, G, Joussen, S, Koch, C et al.(2011). Expansion of adipose mesenchymal stromal cells is affected by human plateletlysate and plating density. Cell Transplant 20: 1409-1422.
32. Sato, S, Yagi, S, Arai, Y, Hirabayashi, K, Hattori, N, Iwatani, M et al. (2010).Genome-wide DNA methylation profile of tissue-dependent and differentiallymethylated regions (T-DMRs) residing in mouse pluripotent stem cells. Genes Cells15: 607-618.
33. Meissner, A, Mikkelsen, TS, Gu, H, Wernig, M, Hanna, J, Sivachenko, A et al. (2008).Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature454: 766-770.
34. Rakyan, VK, Down, TA, Thorne, NP, Flicek, P, Kulesha, E, Gre, S et al. (2008).An integrated resource for genome-wide identification and analysis of humantissue-specific differentially methylated regions (tDMRs). Genome Res 18:1518-1529.
35. Nagae, G, Isagawa, T, Shiraki, N, Fujita, T, Yamamoto, S, Tsutsumi, S et al. (2011).Tissue-specific demethylation in CpG-poor promoters during cellular differentiation.Hum Mol Genet 20: 2710-2721.
36. Mayshar, Y, Ben-David, U, Lavon, N, Biancotti, JC, Yakir, B, Clark, AT et al. (2010).Identification and classification of chromosomal aberrations in human inducedpluripotent stem cells. Cell Stem Cell 7: 521-531.
37. Ushijima, T, Watanabe, N, Okochi, E, Kaneda, A, Sugimura, T and Miyamoto, K(2003). Fidelity of the methylation pattern and its variation in the genome. GenomeRes 13: 868-874. (Pubitemid 36621747)
38. Shukla, S, Kavak, E, Gregory, M, Imashimizu, M, Shutinoski, B, Kashlev, M et al.(2011). CTCF-promoted RNA polymerase II pausing links DNA methylation tosplicing. Nature 479: 74-79.
39. Fouse, SD, Shen, Y, Pellegrini, M, Cole, S, Meissner, A, Van Neste, L et al. (2008).Promoter CpG methylation contributes to ES cell gene regulation in parallel withOct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell2: 160-169. (Pubitemid 351168712)
40. Colter, DC, Sekiya, I and Prockop, DJ (2001). Identification of a subpopulation ofrapidly self-renewing and multipotential adult stem cells in colonies of human marrowstromal cells. Proc Natl Acad Sci USA 98: 7841-7845. (Pubitemid 32642648)
41. Schellenberg, A, Stiehl, T, Horn, P, Joussen, S, Pallua, N, Ho, AD et al. (2012).Population dynamics of mesenchymal stromal cells during culture expansion.Cytotherapy 14: 401-411.
42. Russell, KC, Phinney, DG, Lacey, MR, Barrilleaux, BL, Meyertholen, KE andO'Connor, KC (2010). In vitro high-capacity assay to quantify the clonal heterogeneityin trilineage potential of mesenchymal stem cells reveals a complex hierarchy oflineage commitment. Stem Cells 28: 788-798.
43. Koch, CM, Suschek, CV, Lin, Q, Bork, S, Goergens, M, Joussen, S et al. (2011). Specificage-associated DNA methylation changes in human dermal fibroblasts. PLoS ONE6: e16679.
44. Wagner, W, Horn, P, Castoldi, M, Diehlmann, A, Bork, S, Saffrich, R et al. (2008).Replicative senescence of mesenchymal stem cells: a continuous and organizedprocess. PLoS ONE 3: e2213.
45. Takahashi, K, Tanabe, K, Ohnuki, M, Narita, M, Ichisaka, T, Tomoda, K et al. (2007).Induction of pluripotent stem cells from adult human fibroblasts by defined factors.Cell 131: 861-872. (Pubitemid 350138099)
46. Durinck, S, Moreau, Y, Kasprzyk, A, Davis, S, De Moor, B, Brazma, A et al. (2005).BioMart and Bioconductor: a powerful link between biological databases andmicroarray data analysis. Bioinformatics 21: 3439-3440. (Pubitemid 41222455)
47. Schmidt, M, Schwarzwaelder, K, Bartholomae, CC, Glimm, H and von Kalle, C(2009). Detection of retroviral integration sites by linear amplification-mediated PCRand tracking of individual integration clones in different samples. Methods Mol Biol506: 363-372.
48. Cartier, N, Hacein-Bey-Abina, S, Bartholomae, CC, Veres, G, Schmidt, M, Kutschera, Iet al. (2009). Hematopoietic stem cell gene therapy with a lentiviral vector in X-linkedadrenoleukodystrophy. Science 326: 818-823.
49. Arens, A, Appelt, JU, Bartholomae, CC, Gabriel, R, Paruzynski, A, Gustafson, D et al.(2012). Bioinformatic clonality analysis of next-generation sequencing-derived viralvector integration sites. Hum Gene Ther Methods 23: 111-118.
50. Lujambio, A, Portela, A, Liz, J, Melo, SA, Rossi, S, Spizzo, R et al. (2010). CpGisland hypermethylation-associated silencing of non-coding RNAs transcribed fromultraconserved regions in human cancer. Oncogene 29: 6390-6401.