Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2012 (2012), Article ID 379569, 9 pages
http://dx.doi.org/10.1155/2012/379569
Review Article

Drug Discovery Models and Toxicity Testing Using Embryonic and Induced Pluripotent Stem-Cell-Derived Cardiac and Neuronal Cells

1BioTalentum Ltd., 2100 Gödöllö, Hungary
2Molecular Animal Biotechnology Laboratory, Szent Istvan University, 2100 Gödöllö, Hungary
3Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University 3584 CL Utrecht, The Netherlands

Received 25 October 2011; Revised 7 February 2012; Accepted 16 February 2012

Academic Editor: Mohan C. Vemuri

Copyright © 2012 Rahul S. Deshmukh et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Briggs and T. J. King, “Transplantation of living nuclei from blastula cells into enucleated frogs' eggs,” Proceedings of the National Academy of Sciences of the United States of America, vol. 38, pp. 455–463, 1952. View at Google Scholar
  2. J. B. Gurdon, “The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles,” Journal of Embryology and Experimental Morphology, vol. 10, pp. 622–640, 1962. View at Google Scholar · View at Scopus
  3. J. B. Gurdon, R. A. Laskey, and O. R. Reeves, “The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs,” Journal of Embryology and Experimental Morphology, vol. 34, no. 1, pp. 93–112, 1975. View at Google Scholar · View at Scopus
  4. I. Wilmut, A. E. Schnieke, J. McWhir, A. J. Kind, and K. H. S. Campbell, “Viable offspring derived from fetal and adult mammalian cells,” Nature, vol. 385, no. 6619, pp. 810–813, 1997. View at Publisher · View at Google Scholar · View at Scopus
  5. O. Østrup, I. Petrovicova, F. Strejcek et al., “Nuclear and nucleolar reprogramming during the first cell cycle in bovine nuclear transfer embryos,” Cloning and Stem Cells, vol. 11, no. 3, pp. 367–375, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. O. Østrup, P. Hyttel, D. A. Klærke, and P. Collas, “Remodeling of ribosomal genes in somatic cells by Xenopus egg extract,” Biochemical and Biophysical Research Communications, vol. 412, no. 3, pp. 487–493, 2011. View at Publisher · View at Google Scholar
  7. B. W. Finch and B. Ephrussi, “Retention of multiple developmental potentialities by cells of a mouse testicular teratocarcinoma during prolonged culture in vitro and their extinction upon hybridization with cells of permanent lines,” Proceedings of the National Academy of Sciences of the United States of America, vol. 57, pp. 615–621, 1967. View at Google Scholar
  8. L. C. Stevens and C. C. Little, “Spontaneous testicular teratomas in an inbred strain of mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 40, pp. 1080–1087, 1954. View at Google Scholar
  9. R. A. Miller and F. H. Ruddle, “Pluripotent teratocarcinoma thymus somatic cell hybrids,” Cell, vol. 9, no. 1, pp. 45–55, 1976. View at Google Scholar · View at Scopus
  10. M. J. Evans and M. H. Kaufman, “Establishment in culture of pluripotential cells from mouse embryos,” Nature, vol. 292, no. 5819, pp. 154–156, 1981. View at Google Scholar · View at Scopus
  11. J. A. Thomson, “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998. View at Google Scholar
  12. K. Gertow, S. Przyborski, J. F. Loring et al., “Isolation of human embryonic stem cell-derived teratomas for the assessment of pluripotency,” Current Protocols in Stem Cell Biology, 2007. View at Google Scholar
  13. K. Takahashi and S. Yamanaka, “Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors,” Cell, vol. 126, no. 4, pp. 663–676, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Takahashi, K. Tanabe, M. Ohnuki et al., “Induction of pluripotent stem cells from adult human fibroblasts by defined factors,” Cell, vol. 131, no. 5, pp. 861–872, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Ezashi, B. P. V. L. Telugu, A. P. Alexenko, S. Sachdev, S. Sinha, and R. M. Roberts, “Derivation of induced pluripotent stem cells from pig somatic cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 27, pp. 10993–10998, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Hamanaka, T. Yamaguchi, T. Kobayashi et al., “Generation of Germline-Competent rat induced pluripotent stem cells,” PLoS One, vol. 6, no. 7, Article ID e22008, 2011. View at Publisher · View at Google Scholar
  17. X. Han, J. Han, F. Ding et al., “Generation of induced pluripotent stem cells from bovine embryonic fibroblast cells,” Cell Research, vol. 21, no. 10, pp. 1509–1512, 2011. View at Publisher · View at Google Scholar
  18. J. Liu, D. Balehosur, B. Murray, J. M. Kelly, H. Sumer, and P. J. Verma, “Generation and characterization of reprogrammed sheep induced pluripotent stem cells,” Theriogenology, vol. 77, no. 2, pp. 338–346.e1, 2012. View at Publisher · View at Google Scholar
  19. H. Sumer, J. Liu, L. F. Malaver-Ortega, M. L. Lim, K. Khodadadi, and P. J. Verma, “NANOG is a key factor for induction of pluripotency in bovine adult fibroblasts,” Journal of Animal Science, vol. 89, no. 9, pp. 2708–2716, 2011. View at Publisher · View at Google Scholar
  20. P. A. Tat, H. Sumer, K. L. Jones, K. Upton, and P. J. Verma, “The efficient generation of induced pluripotent stem (iPS) cells from adult mouse adipose tissue-derived and neural stem cells,” Cell Transplantation, vol. 19, no. 5, pp. 525–536, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Pelengaris, M. Khan, and G. Evan, “c-MYC: more than just a matter of life and death,” Nature Reviews Cancer, vol. 2, no. 10, pp. 764–776, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Blelloch, M. Venere, J. Yen, and M. Ramalho-Santos, “Generation of induced pluripotent stem cells in the absence of drug selection,” Cell Stem Cell, vol. 1, no. 3, pp. 245–247, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Nakagawa, M. Koyanagi, K. Tanabe et al., “Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts,” Nature Biotechnology, vol. 26, no. 1, pp. 101–106, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Yu, M. A. Vodyanik, K. Smuga-Otto et al., “Induced pluripotent stem cell lines derived from human somatic cells,” Science, vol. 318, no. 5858, pp. 1917–1920, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. H.-Y. Li, Y. Chien, Y.-J. Chen et al., “Reprogramming induced pluripotent stem cells in the absence of c-Myc for differentiation into hepatocyte-like cells,” Biomaterials, vol. 32, no. 26, pp. 5994–6005, 2011. View at Publisher · View at Google Scholar
  26. C. W. Chang, Y. S. Lai, K. M. Pawlik et al., “Polycistronic lentiviral vector for “hit and run” reprogramming of adult skin fibroblasts to induced pluripotent stem cells,” Stem Cells, vol. 27, no. 5, pp. 1042–1049, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. E. P. Papapetrou and M. Sadelain, “Generation of transgene-free human induced pluripotent stem cells with an excisable single polycistronic vector,” Nature Protocols, vol. 6, no. 9, pp. 1251–1273, 2011. View at Publisher · View at Google Scholar
  28. C. Sarkis, S. Philippe, J. Mallet, and C. Serguera, “Non-integrating lentiviral vectors,” Current Gene Therapy, vol. 8, no. 6, pp. 430–437, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. K. Kaji, K. Norrby, A. Paca, M. Mileikovsky, P. Mohseni, and K. Woltjen, “Virus-free induction of pluripotency and subsequent excision of reprogramming factors,” Nature, vol. 458, no. 7239, pp. 771–775, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Soldner, D. Hockemeyer, C. Beard et al., “Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors,” Cell, vol. 136, no. 5, pp. 964–977, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Woltjen, I. P. Michael, P. Mohseni et al., “PiggyBac transposition reprograms fibroblasts to induced pluripotent stem cells,” Nature, vol. 458, no. 7239, pp. 766–770, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. H. Zhou, S. Wu, J. Y. Joo et al., “Generation of induced pluripotent stem cells using recombinant proteins,” Cell Stem Cell, vol. 4, no. 5, pp. 381–384, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. H. J. Cho, C. S. Lee, Y. W. Kwon et al., “Induction of pluripotent stem cells from adult somatic cells by protein-based reprogramming without genetic manipulation,” Blood, vol. 116, no. 3, pp. 386–395, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Kim, C. H. Kim, J. I. Moon et al., “Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins,” Cell Stem Cell, vol. 4, no. 6, pp. 472–476, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. L. Warren, P. D. Manos, T. Ahfeldt et al., “Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA,” Cell Stem Cell, vol. 7, no. 5, pp. 618–630, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Ambasudhan, M. Talantova, R. Coleman et al., “Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions,” Cell Stem Cell, vol. 9, no. 2, pp. 113–118, 2011. View at Publisher · View at Google Scholar
  37. F. Anokye-Danso, C. M. Trivedi, D. Juhr et al., “Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency,” Cell Stem Cell, vol. 8, no. 4, pp. 376–388, 2011. View at Publisher · View at Google Scholar
  38. Q. Lian, Y. Chow, M. A. Esteban, D. Pei, and H. F. Tse, “Future perspective of induced pluripotent stem cells for diagnosis, drug screening and treatment of human diseases,” Thrombosis and Haemostasis, vol. 104, no. 1, pp. 39–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Menendez, C. Bueno, and L. Wang, “Human embryonic stem cells: a journey beyond cell replacement therapies,” Cytotherapy, vol. 8, no. 6, pp. 530–541, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. C. W. Pouton and J. M. Haynes, “Embryonic stem cells as a source of models for drug discovery,” Nature Reviews Drug Discovery, vol. 6, no. 8, pp. 605–616, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. S. R. Braam, L. Tertoolen, A. van de Stolpe, T. Meyer, R. Passier, and C. L. Mummery, “Prediction of drug-induced cardiotoxicity using human embryonic stem cell-derived cardiomyocytes,” Stem Cell Research, vol. 4, no. 2, pp. 107–116, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Dick, D. Rajamohan, J. Ronksley, and C. Denning, “Evaluating the utility of cardiomyocytes from human pluripotent stem cells for drug screening,” Biochemical Society Transactions, vol. 38, no. 4, pp. 1037–1045, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. H. T. Hogberg, A. Kinsner-Ovaskainen, S. Coecke, T. Hartung, and A. K. Bal-Price, “mRNA expression is a relevant tool to identify developmental neurotoxicants using an in vitro approach,” Toxicological Sciences, vol. 113, no. 1, pp. 95–115, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. A. D. Ebert, J. Yu, F. F. Rose et al., “Induced pluripotent stem cells from a spinal muscular atrophy patient,” Nature, vol. 457, no. 7227, pp. 277–280, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. K. J. Brennand, A. Simone, J. Jou et al., “Modelling schizophrenia using human induced pluripotent stem cells,” Nature, vol. 473, no. 7346, pp. 221–225, 2011. View at Publisher · View at Google Scholar
  46. G. Lee, E. P. Papapetrou, H. Kim et al., “Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs,” Nature, vol. 461, no. 7262, pp. 402–406, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Liu, P. J. Verma, M. V. Evans-Galea et al., “Generation of induced pluripotent stem cell lines from Friedreich ataxia patients,” Stem Cell Reviews and Reports, vol. 7, no. 3, pp. 703–713, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. F. P. Di Giorgio, M. A. Carrasco, M. C. Siao, T. Maniatis, and K. Eggan, “Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model,” Nature Neuroscience, vol. 10, no. 5, pp. 608–614, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. F. P. Di Giorgio, G. L. Boulting, S. Bobrowicz, and K. C. Eggan, “Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation,” Cell Stem Cell, vol. 3, no. 6, pp. 637–648, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Nagai, D. B. Re, T. Nagata et al., “Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons,” Nature Neuroscience, vol. 10, no. 5, pp. 615–622, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. M. C. N. Marchetto, A. R. Muotri, Y. Mu, A. M. Smith, G. G. Cezar, and F. H. Gage, “Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells,” Cell Stem Cell, vol. 3, no. 6, pp. 649–657, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. M. C. N. Marchetto, C. Carromeu, A. Acab et al., “A model for neural development and treatment of rett syndrome using human induced pluripotent stem cells,” Cell, vol. 143, no. 4, pp. 527–539, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. H. N. Nguyen, B. Byers, B. Cord et al., “LRRK2 mutant iPSC-derived da neurons demonstrate increased susceptibility to oxidative stress,” Cell Stem Cell, vol. 8, no. 3, pp. 267–280, 2011. View at Publisher · View at Google Scholar
  54. M. J. Devine, M. Ryten, P. Vodicka et al., “Parkinson's disease induced pluripotent stem cells with triplication of the α-synuclein locus,” Nature Communications, vol. 2, no. 1, article 440, 2011. View at Publisher · View at Google Scholar
  55. Y. Yoshida and S. Yamanaka, “Recent stem cell advances: induced pluripotent stem cells for disease modeling and stem cell-based regeneration,” Circulation, vol. 122, no. 1, pp. 80–87, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. S. R. Braam, R. Passier, and C. L. Mummery, “Cardiomyocytes from human pluripotent stem cells in regenerative medicine and drug discovery,” Trends in Pharmacological Sciences, vol. 30, no. 10, pp. 536–545, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. S. J. Kattman, C. H. Koonce, B. J. Swanson, and B. D. Anson, “Stem cells and their derivatives: a renaissance in cardiovascular translational research,” Journal of Cardiovascular Translational Research, vol. 4, no. 1, pp. 66–72, 2011. View at Publisher · View at Google Scholar
  58. N. Yokoo, S. Baba, S. Kaichi et al., “The effects of cardioactive drugs on cardiomyocytes derived from human induced pluripotent stem cells,” Biochemical and Biophysical Research Communications, vol. 387, no. 3, pp. 482–488, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Gherghiceanu, L. Barad, A. Novak et al., “Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure,” Journal of Cellular and Molecular Medicine, vol. 15, no. 11, pp. 2539–2551, 2011. View at Publisher · View at Google Scholar
  60. E. N. Olson, “A decade of discoveries in cardiac biology,” Nature Medicine, vol. 10, no. 5, pp. 467–474, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Snir, I. Kehat, A. Gepstein et al., “Assessment of the ultrastructural and proliferative properties of human embryonic stem cell-derived cardiomyocytes,” American Journal of Physiology, vol. 285, no. 6, pp. H2355–H2363, 2003. View at Google Scholar · View at Scopus
  62. P. W. Burridge, S. Thompson, M. A. Millrod et al., “A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability,” PLoS One, vol. 6, no. 4, Article ID e18293, 2011. View at Publisher · View at Google Scholar
  63. P. Igelmund, B. K. Fleischmann, I. R. Fischer et al., “Action potential propagation failures in long-term recordings from embryonic stem cell-derived cardiomyocytes in tissue culture,” Pflugers Archiv European Journal of Physiology, vol. 437, no. 5, pp. 669–679, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. M. M. L. Dingemans, H. J. Heusinkveld, A. De Groot, A. Bergman, M. Van den Berg, and R. H. S. Westerink, “Hexabromocyclododecane inhibits depolarization-induced increase in intracellular calcium levels and neurotransmitter release in PC12 cells,” Toxicological Sciences, vol. 107, no. 2, pp. 490–497, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Nakatsu, Y. Kotake, K. Komasaka et al., “Glutamate excitotoxicity is involved in cell death caused by tributyltin in cultured rat cortical neurons,” Toxicological Sciences, vol. 89, no. 1, pp. 235–242, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. R. Barhoumi, Y. Mouneimne, I. Awooda, S. H. Safe, K. C. Donnelly, and R. C. Burghardt, “Characterization of calcium oscillations in normal and benzo[a]pyrene-treated clone 9 cells,” Toxicological Sciences, vol. 68, no. 2, pp. 444–450, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. M. L. Dubois-Dauphin, N. Toni, S. D. Julien, I. Charvet, L. E. Sundstrom, and L. Stoppini, “The long-term survival of in vitro engineered nervous tissue derived from the specific neural differentiation of mouse embryonic stem cells,” Biomaterials, vol. 31, no. 27, pp. 7032–7042, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. O. Preynat-Seauve, D. M. Suter, D. Tirefort et al., “Development of human nervous tissue upon differentiation of embryonic stem cells in three-dimensional culture,” Stem Cells, vol. 27, no. 3, pp. 509–520, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. K. M. Crofton, W. R. Mundy, P. J. Lein et al., “Developmental neurotoxicity testing: recommendations for developing alternative methods for the screening and prioritization of chemicals,” Altex, vol. 28, no. 1, pp. 9–15, 2011. View at Google Scholar
  70. L. Buzanska, J. Sypecka, S. Nerini-Molteni et al., “A human stem cell-based model for identifying adverse effects of organic and inorganic chemicals on the developing nervous system,” Stem Cells, vol. 27, no. 10, pp. 2591–2601, 2009. View at Publisher · View at Google Scholar · View at Scopus
  71. I. Kola and J. Landis, “Can the pharmaceutical industry reduce attrition rates?” Nature Reviews Drug Discovery, vol. 3, no. 8, pp. 711–715, 2004. View at Google Scholar · View at Scopus
  72. K. E. Lasser, P. D. Allen, S. J. Woolhandler, D. U. Himmelstein, S. M. Wolfe, and D. H. Bor, “Timing of new black box warnings and withdrawals for prescription medications,” Journal of the American Medical Association, vol. 287, no. 17, pp. 2215–2220, 2002. View at Google Scholar · View at Scopus
  73. P. D. Kessler and B. J. Byrne, “Myoblast cell grafting into heart muscle: cellular biology and potential applications,” Annual Review of Physiology, vol. 61, pp. 219–242, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. T. Meyer, C. Leisgen, B. Gonser, and E. Günther, “QT-screen: High-throughput cardiac safety pharmacology by extracellular electrophysiology on primary cardiac myocytes,” Assay and Drug Development Technologies, vol. 2, no. 5, pp. 507–514, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. Y. M. Li, Y. P. Guo, and Y. Liu, “Cancer chemotherapy induces cardiotoxicity by targeting cardiac stem cells,” Journal of Cellular and Molecular Medicine, vol. 14, no. 11, pp. 2630–2632, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. E. Raschi and F. De Ponti, “Cardiovascular toxicity of anticancer-targeted therapy: emerging issues in the era of cardio-oncology,” Internal and Emergency Medicine, vol. 7, no. 2, pp. 113–131, 2012. View at Publisher · View at Google Scholar
  77. C. W. Kong, F. G. Akar, and R. A. Li, “Translational potential of human embryonic and induced pluripotent stem cells for myocardial repair: insights from experimental models,” Thrombosis and Haemostasis, vol. 104, no. 1, pp. 30–38, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Moretti, M. Bellin, A. Welling et al., “Patient-specific induced pluripotent stem-cell models for long-QT syndrome,” New England Journal of Medicine, vol. 363, no. 15, pp. 1397–1409, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Peng, A. E. Lacerda, G. E. Kirsch, A. M. Brown, and A. Bruening-Wright, “The action potential and comparative pharmacology of stem cell-derived human cardiomyocytes,” Journal of Pharmacological and Toxicological Methods, vol. 61, no. 3, pp. 277–286, 2010. View at Publisher · View at Google Scholar · View at Scopus
  80. M. K. B. Jonsson, G. Duker, C. Tropp et al., “Quantified proarrhythmic potential of selected human embryonic stem cell-derived cardiomyocytes,” Stem Cell Research, vol. 4, no. 3, pp. 189–200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. H. Andersson, D. Steel, J. Asp et al., “Assaying cardiac biomarkers for toxicity testing using biosensing and cardiomyocytes derived from human embryonic stem cells,” Journal of Biotechnology, vol. 150, no. 1, pp. 175–181, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. H. Andersson, B. Kågedal, and C. F. Mandenius, “Monitoring of troponin release from cardiomyocytes during exposure to toxic substances using surface plasmon resonance biosensing,” Analytical and Bioanalytical Chemistry, vol. 398, no. 3, pp. 1395–1402, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. A. M. Fernandes, T. G. Fernandes, M. M. Diogo, C. L. da Silva, D. Henrique, and J. M. S. Cabral, “Mouse embryonic stem cell expansion in a microcarrier-based stirred culture system,” Journal of Biotechnology, vol. 132, no. 2, pp. 227–236, 2007. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Terstegge, I. Laufenberg, J. Pochert et al., “Automated maintenance of embryonic stem cell cultures,” Biotechnology and Bioengineering, vol. 96, no. 1, pp. 195–201, 2007. View at Publisher · View at Google Scholar
  85. J. Kim, C. J. Lengner, O. Kirak et al., “Reprogramming of postnatal neurons into induced pluripotent stem cells by defined factors,” Stem Cells, vol. 29, no. 6, pp. 992–1000, 2011. View at Publisher · View at Google Scholar
  86. H. Liu, Z. Ye, Y. Kim, S. Sharkis, and Y. Y. Jang, “Generation of endoderm-derived human induced pluripotent stem cells from primary hepatocytes,” Hepatology, vol. 51, no. 5, pp. 1810–1819, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. N. Sun, N. J. Panetta, D. M. Gupta et al., “Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 37, pp. 15720–15725, 2009. View at Publisher · View at Google Scholar · View at Scopus