Substantial variation in the cardiac differentiation of human embryonic stem cell lines derived and propagated under the same conditions—a comparison of multiple cell lines

References

• Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998; 282: 1145–7
   PubMed Web of Science ®Google Scholar
• Skottman H, Narkilahti S, Hovatta O. Challenges and approaches to the culture of pluripotent human embryonic stem cells. Regen Med. 2007; 2: 265–73
   Google Scholar
• Hoffman LM, Carpenter MK. Characterization and culture of human embryonic stem cells. Nat Biotechnol. 2005; 23: 699–708
   PubMed Web of Science ®Google Scholar
• Cowan CA, Klimanskaya I, McMahon J, Atienza J, Witmyer J, Zucker JP, et al. Derivation of embryonic stem-cell lines from human blastocysts. N Engl J Med. 2004; 350: 1353–6
   PubMed Web of Science ®Google Scholar
• Hoffman LM, Carpenter MK. Human embryonic stem cell stability. Stem Cell Rev. 2005; 1: 139–44
   Google Scholar
• Lee JB, Kim JM, Kim SJ, Park JH, Hong SH, Roh SI, et al. Comparative characteristics of three human embryonic stem cell lines. Mol Cells. 2005; 19: 31–8
   PubMedGoogle Scholar
• Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G, et al. Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol. 2007; 25: 803–16
   PubMed Web of Science ®Google Scholar
• Skottman H, Mikkola M, Lundin K, Olsson C, Strömberg A-M, Tuuri T, et al. Gene expression signatures of seven individual human embryonic stem cell lines. Stem Cells. 2005; 23: 1343–56
   PubMed Web of Science ®Google Scholar
• Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, et al. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest. 2001; 108: 407–14
   PubMed Web of Science ®Google Scholar
• Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, et al. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation. 2003; 107: 2733–40
   PubMed Web of Science ®Google Scholar
• Allegrucci C, Young LE. Differences between human embryonic stem cell lines. Hum Reprod Update. 2007; 13: 103–20
   PubMed Web of Science ®Google Scholar
• Burridge PW, Anderson D, Priddle H, Barbadillo Munoz MD, Chamberlain S, Allegrucci C, et al. Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells. 2007; 25: 929–38
   PubMed Web of Science ®Google Scholar
• Hovatta O, Mikkola M, Gertow K, Stromberg AM, Inzunza J, Hreinsson J, et al. A culture system using human foreskin fibroblasts as feeder cells allows production of human embryonic stem cells. Hum Reprod. 2003; 18: 1404–9
   PubMed Web of Science ®Google Scholar
• Inzunza J, Gertow K, Stromberg MA, Matilainen E, Blennow E, Skottman H, et al. Derivation of human embryonic stem cell lines in serum replacement medium using postnatal human fibroblasts as feeder cells. Stem Cells. 2005; 23: 544–9
   PubMed Web of Science ®Google Scholar
• Mummery CL, van Achterberg TA, van den Eijnden-van Raaij AJ, van Haaster L, Willemse A, de Laat SW, et al. Visceral-endoderm-like cell lines induce differentiation of murine P19 embryonal carcinoma cells. Differentiation. 1991; 46: 51–60
   Google Scholar
• Passier R, Oostwaard DW, Snapper J, Kloots J, Hassink RJ, Kuijk E, et al. Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells. 2005; 23: 772–80
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402–8
   PubMed Web of Science ®Google Scholar
• Rajala K, Hakala H, Panula S, Aivio S, Pihlajamaki H, Suuronen R, et al. Testing of nine different xeno-free culture media for human embryonic stem cell cultures. Hum Reprod. 2007; 22: 1231–8
   PubMed Web of Science ®Google Scholar
• Kim SE, Kim BK, Gil JE, Kim SK, Kim JH. Comparative analysis of the developmental competence of three human embryonic stem cell lines in vitro. Mol Cells. 2007; 23: 49–56
   Google Scholar
• Mikkola M, Olsson C, Palgi J, Ustinov J, Palomaki T, Horelli-Kuitunen N, et al. Distinct differentiation characteristics of individual human embryonic stem cell lines. BMC Dev Biol. 2006; 6: 40
   PubMed Web of Science ®Google Scholar
• Mummery C. Cardiomyocytes from human embryonic stem cells: more than heart repair alone. Bioessays. 2007; 29: 572–9
   Google Scholar
• Devine SM, Bartholomew AM, Mahmud N, Nelson M, Patil S, Hardy W, et al. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. Exp Hematol. 2001; 29: 244–55
   PubMed Web of Science ®Google Scholar
• Xu C, Police S, Rao N, Carpenter MK. Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ Res. 2002; 91: 501–8
   PubMed Web of Science ®Google Scholar
• He J-Q, Ma Y, Lee Y, Thomson JA, Kamp TJ. Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization. Circ Res. 2003; 93: 32–9
   PubMed Web of Science ®Google Scholar
• Pal R, Khanna A. Similar pattern in cardiac differentiation of human embryonic stem cell lines, BG01V and ReliCellhES1, under low serum concentration supplemented with bone morphogenetic protein-2. Differentiation. 2007; 75: 112–22
   PubMedGoogle Scholar
• Osafune K, Caron L, Borowiak M, Martinez RJ, Fitz-Gerald CS, Sato Y, et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol. 2008; 26: 313–5
   PubMed Web of Science ®Google Scholar
• Lauss M, Stary M, Tischler J, Egger G, Puz S, Bader-Allmer A, et al. Single inner cell masses yield embryonic stem cell lines differing in lifr expression and their developmental potential. Biochem Biophys Res Commun. 2005; 331: 1577–86
   Google Scholar
• Tomescot A, Leschik J, Bellamy V, Dubois G, Messas E, Bruneval P, et al. Differentiation in vivo of cardiac committed human embryonic stem cells in postmyocardial infarcted rats. Stem Cells. 2007; 25: 2200–5
   PubMed Web of Science ®Google Scholar
• Beqqali, A, Kloots, J, Ward-van Oostwaard, D, Mummery, C, Passier, R. Genome-wide transcriptional profiling of human embryonic stem cells differentiating to cardiomyocytes. Stem Cells. 2006:1956–67.
   Google Scholar
• Graichen R, Xu X, Braam SR, Balakrishnan T, Norfiza S, Sieh S, et al. Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation. 2008; 76: 357–70
   PubMed Web of Science ®Google Scholar
• Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, et al. Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell. 2003; 5: 877–89
   PubMed Web of Science ®Google Scholar
• Filipczyk AA, Passier R, Rochat A, Mummery CL. Regulation of cardiomyocyte differentiation of embryonic stem cells by extracellular signalling. Cell Mol Life Sci. 2007; 64: 704–18
   Google Scholar
• Hosseinkhani M, Hosseinkhani H, Khademhosseini A, Bolland F, Kobayashi H, Gonzalez SP. Bone morphogenetic protein-4 enhances cardiomyocyte differentiation of cynomolgus monkey ESCs in knockout serum replacement medium. Stem Cells. 2007; 25: 571–80
   Google Scholar
• Pevny LH, Sockanathan S, Placzek M, Lovell-Badge R. A role for SOX1 in neural determination. Development. 1998; 125: 1967–78
   PubMedGoogle Scholar
• Kan L, Israsena N, Zhang Z, Hu M, Zhao LR, Jalali A, et al. Sox1 acts through multiple independent pathways to promote neurogenesis. Dev Biol. 2004; 269: 580–94
   PubMed Web of Science ®Google Scholar
• Snir M, Kehat I, Gepstein A, Coleman R, Itskovitz-Eldor J, Livne E, et al. Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes. Am J Physiol Heart Circ Physiol. 2003; 285: H2355–63
   PubMed Web of Science ®Google Scholar
• Norstrom A, Akesson K, Hardarson T, Hamberger L, Bjorquist P, Sartipy P. Molecular and pharmacological properties of human embryonic stem cell-derived cardiomyocytes. Exp Biol Med (Maywood) 2006; 231: 1753–62
   PubMed Web of Science ®Google Scholar
• Denning C, Allegrucci C, Priddle H, Barbadillo-Munoz MD, Anderson D, Self T, et al. Common culture conditions for maintenance and cardiomyocyte differentiation of the human embryonic stem cell lines, BG01 and HUES-7. Int J Dev Biol. 2006; 50: 27–37
   PubMed Web of Science ®Google Scholar