Small molecule screening in human induced pluripotent stem cell-derived terminal cell types

Journal of Biological Chemistry

Volumn 289, Issue 8, 2014, Pages 4562-4570

  Engle, Sandra J ^a   Vincent, Fabien ^a  

^a PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DIAGNOSIS; MOLECULES; PHYSIOLOGY; STEM CELLS;

CLINICAL OUTCOME; DRUG DISCOVERY; DRUG DISCOVERY PROCESS; HIGH THROUGHPUT SCREENING; HUMAN-INDUCED PLURIPOTENT STEM CELLS; PATIENT SPECIFIC; SMALL MOLECULES; THERAPEUTIC COMPOUNDS;

DRUG PRODUCTS;

AMYOTROPHIC LATERAL SCLEROSIS; BIOSENSOR; CELL DIFFERENTIATION; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; EPIGENETICS; GENOTYPE PHENOTYPE CORRELATION; HEART MUSCLE CELL; HIGH THROUGHPUT SCREENING; HUMAN; IMMUNOFLUORESCENCE; LIVER CELL; MOLECULAR DYNAMICS; MOTONEURON; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PHYSICAL CHEMISTRY; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROCESS TECHNOLOGY; QUANTITATIVE ANALYSIS; REVIEW; SOMATIC CELL;

DRUG ACTION; DRUG DEVELOPMENT; DRUG DISCOVERY; DRUG SCREENING; STEM CELLS;

HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; SMALL MOLECULE LIBRARIES;

EID: 84894418057     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R113.529156     Document Type: Review

References (98)

1. Nolan, G. P. (2007) What's wrong with drug screening today. Nat. Chem. Biol. 3, 187-191
2. Sams-Dodd, F. (2013) Is poor research the cause of the declining productivity of the pharmaceutical industry? An industry in need of a paradigm shift. Drug Discov. Today 18, 211-217
3. Scannell, J. W., Blanckley, A., Boldon, H., and Warrington, B. (2012) Diagnosing the decline in pharmaceutical R&D efficiency. Nat. Rev. Drug Discov. 11, 191-200
4. Arrowsmith, J. (2011) Trial watch: phase II failures: 2008-2010. Nat. Rev. Drug Discov. 10, 328-329
5. Takenaka, T. (2001) Classical vs reverse pharmacology in drug discovery. BJU Int. 88, Suppl. s2, 7-10
6. Eggert, U. S. (2013) The why and how of phenotypic small-molecule screens. Nat. Chem. Biol. 9, 206-209
7. Zheng, W., Thorne, N., and McKew, J. C. (2013) Phenotypic screens as a renewed approach for drug discovery. Drug Discov. Today 18, 1067-1073
8. Macarron, R., Banks, M. N., Bojanic, D., Burns, D. J., Cirovic, D. A., Garyantes, T., Green, D. V., Hertzberg, R. P., Janzen, W. P., Paslay, J. W., Schopfer, U., and Sittampalam, G. S. (2011) Impact of high-throughput screening in biomedical research. Nat. Rev. Drug Discov. 10, 188-195
9. Plenge, R. M., Scolnick, E. M., and Altshuler, D. (2013) Validating therapeutic targets through human genetics. Nat. Rev. Drug Discov. 12, 581-594
10. Swinney, D. C., and Anthony, J. (2011) How were new medicines discovered? Nat. Rev. Drug Discov. 10, 507-519
11. Goldbard, S. (2006) Bringing primary cells to mainstream drug development and drug testing. Curr. Opin. Drug Discov. Devel. 9, 110-116
12. An, W. F., and Tolliday, N. (2010) Cell-based assays for high-throughput screening. Mol. Biotechnol. 45, 180-186
13. Eglen, R., and Reisine, T. (2011) Primary cells and stem cells in drug discovery: emerging tools for high-throughput screening. Assay Drug Dev. Technol. 9, 108-124
14. van der Worp, H. B., Howells, D. W., Sena, E. S., Porritt, M. J., Rewell, S., O'Collins, V., and Macleod, M. R. (2010) Can animal models of disease reliably inform human studies? PLoS Med. 7, e1000245
15. Seok, J., Warren, H. S., Cuenca, A. G., Mindrinos, M. N., Baker, H. V., Xu, W., Richards, D. R., McDonald-Smith, G. P., Gao, H., Hennessy, L., Finnerty, C. C., López, C. M., Honari, S., Moore, E. E., Minei, J. P., Cuschieri, J., Bankey, P. E., Johnson, J. L., Sperry, J., Nathens, A. B., Billiar, T. R., West, M. A., Jeschke, M. G., Klein, M. B., Gamelli, R. L., Gibran, N. S., Brownstein, B. H., Miller-Graziano, C., Calvano, S. E., Mason, P. H., Cobb, J. P., Rahme, L. G., Lowry, S. F., Maier, R. V., Moldawer, L. L., Herndon, D. N., Davis, R. W., Xiao, W., and Tompkins, R. G. (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. U.S.A. 110, 3507-3512
16. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872
17. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., Slukvin, I. I, and Thomson, J. A. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920
18. Xu, Y., Zhu, X., Hahm, H. S., Wei, W., Hao, E., Hayek, A., and Ding, S. (2010) Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc. Natl. Acad. Sci. U.S.A. 107, 8129-8134
19. Desbordes, S. C., and Studer, L. (2013) Adapting human pluripotent stem cells to high-throughput and high-content screening. Nat. Protoc. 8, 111-130
20. Barbaric, I., Gokhale, P. J., Jones, M., Glen, A., Baker, D., and Andrews, P. W. (2010) Novel regulators of stem cell fates identified by a multivariate phenotype screen of small compounds on human embryonic stem cell colonies. Stem Cell Res. 5, 104-119
21. Sherman, S. P., Alva, J. A., Thakore-Shah, K., and Pyle, A. D. (2011) Human pluripotent stem cells: the development of high-content screening strategies. Methods Mol. Biol. 767, 283-295
22. Andrews, P. D., Becroft, M., Aspegren, A., Gilmour, J., James, M. J., McRae, S., Kime, R., Allcock, R. W., Abraham, A., Jiang, Z., Strehl, R., Mountford, J. C., Milligan, G., Houslay, M. D., Adams, D. R., and Frearson, J. A. (2010) High-content screening of feeder-free human embryonic stem cells to identify pro-survival small molecules. Biochem. J. 432, 21-33
23. Makhortova, N. R., Hayhurst, M., Cerqueira, A., Sinor-Anderson, A. D., Zhao, W. N., Heiser, P. W., Arvanites, A. C., Davidow, L. S., Waldon, Z. O., Steen, J. A., Lam, K., Ngo, H. D., and Rubin, L. L. (2011)Ascreen for regulators of survival of motor neuron protein levels. Nat. Chem. Biol. 7, 544-552
24. Ben-David, U., Gan, Q. F., Golan-Lev, T., Arora, P., Yanuka, O., Oren, Y. S., Leikin-Frenkel, A., Graf, M., Garippa, R., Boehringer, M., Gromo, G., and Benvenisty, N. (2013) Selective elimination of human pluripotent stem cells by an oleate synthesis inhibitor discovered in a high-throughput screen. Cell Stem Cell 12, 167-179
25. Chen, T., Yuan, D., Wei, B., Jiang, J., Kang, J., Ling, K., Gu, Y., Li, J., Xiao, L., and Pei, G. (2010) E-cadherin-mediated cell-cell contact is critical for induced pluripotent stem cell generation. Stem Cells 28, 1315-1325
26. Li, Z., and Rana, T. M. (2012) A kinase inhibitor screen identifies smallmolecule enhancers of reprogramming and iPS cell generation. Nat. Commun. 3, 1085
27. Yang, C. S., Lopez, C. G., and Rana, T. M. (2011) Discovery of nonsteroidal anti-inflammatory drug and anticancer drug enhancing reprogramming and induced pluripotent stem cell generation. Stem Cells 29, 1528-1536
28. Kunisada, Y., Tsubooka-Yamazoe, N., Shoji, M., and Hosoya, M. (2012) Small molecules induce efficient differentiation into insulin-producing cells from human induced pluripotent stem cells. Stem Cell Res. 8, 274-284
29. Zhao, W. N., Cheng, C., Theriault, K. M., Sheridan, S. D., Tsai, L. H., and Haggarty, S. J. (2012) A high-throughput screen for Wnt/catenin signaling pathway modulators in human iPSC-derived neural progenitors. J. Biomol. Screen. 17, 1252-1263
30. Oh, S. W., Lee, J. B., Kim, B., Jeon, S., Kim, M. K., Nam, K. H., Ha, J. R., Bhatia, M., Oh, G. T., and Kim, D. Y. (2012) Peptidomimetic smallmolecule compounds promoting cardiogenesis of stem cells. Arch. Pharm. Res. 35, 1979-1988
31. Shan, J., Schwartz, R. E., Ross, N. T., Logan, D. J., Thomas, D., Duncan, S. A., North, T. E., Goessling, W., Carpenter, A. E., and Bhatia, S. N. (2013) Identification of small molecules for human hepatocyte expansion and iPS differentiation. Nat. Chem. Biol. 9, 514-520
32. Minami, I., Yamada, K., Otsuji, T. G., Yamamoto, T., Shen, Y., Otsuka, S., Kadota, S., Morone, N., Barve, M., Asai, Y., Tenkova-Heuser, T., Heuser, J. E., Uesugi, M., Aiba, K., and Nakatsuji, N. (2012) A small molecule that promotes cardiac differentiation of human pluripotent stem cells under defined, cytokine-and xeno-free conditions. Cell Rep. 2, 1448-1460
33. Liang, P., Lan, F., Lee, A. S., Gong, T., Sanchez-Freire, V., Wang, Y., Diecke, S., Sallam, K., Knowles, J. W., Wang, P. J., Nguyen, P. K., Bers, D. M., Robbins, R. C., and Wu, J. C. (2013) Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity. Circulation 127, 1677-1691
34. Sirenko, O., Crittenden, C., Callamaras, N., Hesley, J., Chen, Y. W., Funes, C., Rusyn, I., Anson, B., and Cromwell, E. F. (2013) Multiparameter in vitro assessment of compound effects on cardiomyocyte physiology using iPSC cells. J. Biomol. Screen. 18, 39-53
35. Guo, L., Abrams, R. M., Babiarz, J. E., Cohen, J. D., Kameoka, S., Sanders, M. J., Chiao, E., and Kolaja, K. L. (2011) Estimating the risk of druginduced proarrhythmia using human induced pluripotent stem cell-derived cardiomyocytes. Toxicol. Sci. 123, 281-289
36. Kang, S. J., Jeong, S. H., Kim, E. J., Cho, J. H., Park, Y. I., Park, S. W., Shin, H. S., Son, S. W., and Kang, H. G. (2013) Evaluation of hepatotoxicity of chemicals using hepatic progenitor and hepatocyte-like cells derived from mouse embryonic stem cells: effect of chemicals on ESC-derived hepatocyte differentiation. Cell Biol. Toxicol. 29, 1-11
37. Panzica-Kelly, J. M., Brannen, K. C., Ma, Y., Zhang, C. X., Flint, O. P., Lehman-McKeeman, L. D., and Augustine-Rauch, K. A. (2013) Establishment of a molecular embryonic stem cell developmental toxicity assay. Toxicol. Sci. 131, 447-457
38. McNeish, J., Roach, M., Hambor, J., Mather, R. J., Weibley, L., Lazzaro, J., Gazard, J., Schwarz, J., Volkmann, R., Machacek, D., Stice, S., Zawadzke, L., O'Donnell, C., and Hurst, R. (2010) High-throughput screening in embryonic stem cell-derived neurons identifies potentiators ofamino-3-hydroxyl-5-methyl-4- isoxazolepropionate-type glutamate receptors. J. Biol. Chem. 285, 17209-17217
39. Yang, Y. M., Gupta, S. K., Kim, K. J., Powers, B. E., Cerqueira, A., Wainger, B. J., Ngo, H. D., Rosowski, K. A., Schein, P. A., Ackeifi, C. A., Arvanites, A. C., Davidow, L. S., Woolf, C. J., and Rubin, L. L. (2013) A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS. Cell Stem Cell 12, 713-726
40. Brennand, K. J., Simone, A., Jou, J., Gelboin-Burkhart, C., Tran, N., Sangar, S., Li, Y., Mu, Y., Chen, G., Yu, D., McCarthy, S., Sebat, J., and Gage, F. H. (2011) Modelling schizophrenia using human induced pluripotent stem cells. Nature 473, 221-225
41. Yahata, N., Asai, M., Kitaoka, S., Takahashi, K., Asaka, I., Hioki, H., Kaneko, T., Maruyama, K., Saido, T. C., Nakahata, T., Asada, T., Yamanaka, S., Iwata, N., and Inoue, H. (2011) Anti-A drug screening platform using human iPS cell-derived neurons for the treatment of Alzheimer's disease. PLoS ONE 6, e25788
42. Almeida, S., Zhang, Z., Coppola, G., Mao, W., Futai, K., Karydas, A., Geschwind, M. D., Tartaglia, M. C., Gao, F., Gianni, D., Sena-Esteves, M., Geschwind, D. H., Miller, B. L., Farese, R. V., Jr., and Gao, F. B. (2012) Induced pluripotent stem cell models of progranulin-deficient frontotemporal dementia uncover specific reversible neuronal defects. Cell Rep. 2, 789-798
43. Ebert, A. D., Yu, J., Rose, F. F., Jr., Mattis, V. B., Lorson, C. L., Thomson, J. A., and Svendsen, C. N. (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457, 277-280
44. Lee, G., Papapetrou, E. P., Kim, H., Chambers, S. M., Tomishima, M. J., Fasano, C. A., Ganat, Y. M., Menon, J., Shimizu, F., Viale, A., Tabar, V., Sadelain, M., and Studer, L. (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461, 402-406
45. Yagi, T., Ito, D., Okada, Y., Akamatsu, W., Nihei, Y., Yoshizaki, T., Yamanaka, S., Okano, H., and Suzuki, N. (2011) Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum. Mol. Genet. 20, 4530-4539
46. Peng, J., Liu, Q., Rao, M. S., and Zeng, X. (2013) Using human pluripotent stem cell-derived dopaminergic neurons to evaluate candidate Parkinson's disease therapeutic agents in MPP and rotenone models. J. Biomol. Screen. 18, 522-533
47. Reinhardt, P., Glatza, M., Hemmer, K., Tsytsyura, Y., Thiel, C. S., Höing, S., Moritz, S., Parga, J. A., Wagner, L., Bruder, J. M., Wu, G., Schmid, B., Röpke, A., Klingauf, J., Schwamborn, J. C., Gasser, T., Schöler, H. R., and Sterneckert, J. (2013) Derivation and expansion using only small molecules of human neural progenitors for neurodegenerative disease modeling. PLoS ONE 8, e59252
48. Chambers, S. M., Qi, Y., Mica, Y., Lee, G., Zhang, X. J., Niu, L., Bilsland, J., Cao, L., Stevens, E., Whiting, P., Shi, S. H., and Studer, L. (2012) Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat. Biotechnol. 30, 715-720
49. Maroof, A. M., Keros, S., Tyson, J. A., Ying, S. W., Ganat, Y. M., Merkle, F. T., Liu, B., Goulburn, A., Stanley, E. G., Elefanty, A. G., Widmer, H. R., Eggan, K., Goldstein, P. A., Anderson, S. A., and Studer, L. (2013) Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12, 559-572
50. Crompton, L. A., Byrne, M. L., Taylor, H., Kerrigan, T. L., Bru-Mercier, G., Badger, J. L., Barbuti, P. A., Jo, J., Tyler, S. J., Allen, S. J., Kunath, T., Cho, K., and Caldwell, M. A. (2013) Stepwise, non-adherent differentiation of human pluripotent stem cells to generate basal forebrain cholinergic neurons via hedgehog signaling. Stem Cell Res. 11, 1206-1221
51. Amoroso, M. W., Croft, G. F., Williams, D. J., O'Keeffe, S., Carrasco, M. A., Davis, A. R., Roybon, L., Oakley, D. H., Maniatis, T., Henderson, C. E., and Wichterle, H. (2013) Accelerated high-yield generation of limb-innervating motor neurons from human stem cells. J. Neurosci. 33, 574-586
52. Choi, S. M., Kim, Y., Shim, J. S., Park, J. T., Wang, R. H., Leach, S. D., Liu, J. O., Deng, C., Ye, Z., and Jang, Y. Y. (2013) Efficient drug screening and gene correction for treating liver disease using patient-specific stem cells. Hepatology 57, 2458-2468
53. Xu, X., Lei, Y., Luo, J., Wang, J., Zhang, S., Yang, X. J., Sun, M., Nuwaysir, E., Fan, G., Zhao, J., Lei, L., and Zhong, Z. (2013) Prevention ofamyloid induced toxicity in human iPS cell-derived neurons by inhibition of cyclin-dependent kinases and associated cell cycle events. Stem Cell Res. 10, 213-227
54. Lee, G., Ramirez, C. N., Kim, H., Zeltner, N., Liu, B., Radu, C., Bhinder, B., Kim, Y. J., Choi, I. Y., Mukherjee-Clavin, B., Djaballah, H., and Studer, L. (2012) Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat. Biotechnol. 30, 1244-1248
55. Charbord, J., Poydenot, P., Bonnefond, C., Feyeux, M., Casagrande, F., Brinon, B., Francelle, L., Aurégan, G., Guillermier, M., Cailleret, M., Viegas, P., Nicoleau, C., Martinat, C., Brouillet, E., Cattaneo, E., Peschanski, M., Lechuga, M., and Perrier, A. L. (2013) High throughput screening for inhibitors of REST in neural derivatives of human embryonic stem cells reveals a chemical compound that promotes expression of neuronal genes. Stem Cells 31, 1816-1828
56. Burkhardt, M. F., Martinez, F. J., Wright, S., Ramos, C., Volfson, D., Mason, M., Garnes, J., Dang, V., Lievers, J., Shoukat-Mumtaz, U., Martinez, R., Gai, H., Blake, R., Vaisberg, E., Grskovic, M., Johnson, C., Irion, S., Bright, J., Cooper, B., Nguyen, L., Griswold-Prenner, I., and Javaherian, A. (2013) A cellular model for sporadic ALS using patient-derived induced pluripotent stem cells. Mol. Cell. Neurosci. 56, 355-364
57. Ghosh, Z., Wilson, K. D., Wu, Y., Hu, S., Quertermous, T., and Wu, J. C. (2010) Persistent donor cell gene expression among human induced pluripotent stem cells contributes to differences with human embryonic stem cells. PLoS ONE 5, e8975
58. Abyzov, A., Mariani, J., Palejev, D., Zhang, Y., Haney, M. S., Tomasini, L., Ferrandino, A. F., Rosenberg Belmaker, L. A., Szekely, A., Wilson, M., Kocabas, A., Calixto, N. E., Grigorenko, E. L., Huttner, A., Chawarska, K., Weissman, S., Urban, A. E., Gerstein, M., and Vaccarino, F. M. (2012) Somatic copy number mosaicism in human skin revealed by induced pluripotent stem cells. Nature 492, 438-442
59. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M. J., Ji, H., Ehrlich, L. I., Yabuuchi, A., Takeuchi, A., Cunniff, K. C., Hongguang, H., McKinney-Freeman, S., Naveiras, O., Yoon, T. J., Irizarry, R. A., Jung, N., Seita, J., Hanna, J., Murakami, P., Jaenisch, R., Weissleder, R., Orkin, S. H., Weissman, I. L., Feinberg, A. P., and Daley, G. Q. (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290
60. Ohi, Y., Qin, H., Hong, C., Blouin, L., Polo, J. M., Guo, T., Qi, Z., Downey, S. L., Manos, P. D., Rossi, D. J., Yu, J., Hebrok, M., Hochedlinger, K., Costello, J. F., Song, J. S., and Ramalho-Santos, M. (2011) Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat. Cell Biol. 13, 541-549
61. Cheng, L., Hansen, N. F., Zhao, L., Du, Y., Zou, C., Donovan, F. X., Chou, B. K., Zhou, G., Li, S., Dowey, S. N., Ye, Z., NISC Comparative Sequencing Program, Chandrasekharappa, S. C., Yang, H., Mullikin, J. C., and Liu, P. P. (2012) Low incidence ofDNAsequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 10, 337-344
62. Ban, H., Nishishita, N., Fusaki, N., Tabata, T., Saeki, K., Shikamura, M., Takada, N., Inoue, M., Hasegawa, M., Kawamata, S., and Nishikawa, S. (2011) Efficient generation of transgene-free human induced pluripotent stem cells (iPSCS) by temperature-sensitive Sendai virus vectors. Proc. Natl. Acad. Sci. U.S.A. 108, 14234-14239
63. Warren, L., Manos, P. D., Ahfeldt, T., Loh, Y. H., Li, H., Lau, F., Ebina, W., Mandal, P. K., Smith, Z. D., Meissner, A., Daley, G. Q., Brack, A. S., Collins, J. J., Cowan, C., Schlaeger, T. M., and Rossi, D. J. (2010) Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7, 618-630
64. Hou, P., Li, Y., Zhang, X., Liu, C., Guan, J., Li, H., Zhao, T., Ye, J., Yang, W., Liu, K., Ge, J., Xu, J., Zhang, Q., Zhao, Y., and Deng, H. (2013) Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341, 651-654
65. Nemes, C., Varga, E., Polgar, Z., Klincumhom, N., Pirity, M. K., and Dinnyes, A. (2013) Generation of mouse induced pluripotent stem cells by protein transduction. Tissue Eng. Part. C Methods 10.1089/ ten.tec.2013.0026
66. Okita, K., Yamakawa, T., Matsumura, Y., Sato, Y., Amano, N., Watanabe, A., Goshima, N., and Yamanaka, S. (2013) An efficient nonviral method to generate integration-free human-induced pluripotent stem cells from cord blood and peripheral blood cells. Stem Cells 31, 458-466
67. Seki, T., Yuasa, S., and Fukuda, K. (2012) Generation of induced pluripotent stem cells from a small amount of human peripheral blood using a combination of activated T cells and Sendai virus. Nat. Protoc. 7, 718-728
68. Brown, M. E., Rondon, E., Rajesh, D., Mack, A., Lewis, R., Feng, X., Zitur, L. J., Learish, R. D., and Nuwaysir, E. F. (2010) Derivation of induced pluripotent stem cells from human peripheral blood T lymphocytes. PLoS ONE 5, e11373
69. Maherali, N., and Hochedlinger, K. (2008) Guidelines and techniques for the generation of induced pluripotent stem cells. Cell Stem Cell 3, 595-605
70. Ellis, J., Bruneau, B. G., Keller, G., Lemischka, I. R., Nagy, A., Rossant, J., Srivastava, D., Zandstra, P. W., and Stanford, W. L. (2009) Alternative induced pluripotent stem cell characterization criteria for in vitro applications. Cell Stem Cell 4, 198-199; author reply 202
71. Daley, G. Q., Lensch, M. W., Jaenisch, R., Meissner, A., Plath, K., and Yamanaka, S. (2009) Broader implications of defining standards for the pluripotency of iPSCS. Cell Stem Cell 4, 200-201; author reply 202
72. Burridge, P. W., and Zambidis, E. T. (2013) Highly efficient directed differentiation of human induced pluripotent stem cells into cardiomyocytes. Methods Mol. Biol. 997, 149-161
73. Ma, X., Duan, Y., Tschudy-Seney, B., Roll, G., Behbahan, I. S., Ahuja, T. P., Tolstikov, V., Wang, C., McGee, J., Khoobyari, S., Nolta, J. A., Willenbring, H., and Zern, M. A. (2013) Highly efficient differentiation of functional hepatocytes from human induced pluripotent stem cells. Stem Cells Transl. Med. 2, 409-419
74. Samuel, R., Daheron, L., Liao, S., Vardam, T., Kamoun, W. S., Batista, A., Buecker, C., Schäfer, R., Han, X., Au, P., Scadden, D. T., Duda, D. G., Fukumura, D., and Jain, R. K. (2013) Generation of functionally competent and durable engineered blood vessels from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. U.S.A. 110, 12774-12779
75. Park, T. S., Zimmerlin, L., and Zambidis, E. T. (2013) Efficient and simultaneous generation of hematopoietic and vascular progenitors from human induced pluripotent stem cells. Cytometry A 83, 114-126
76. Kepp, O., Galluzzi, L., Lipinski, M., Yuan, J., and Kroemer, G. (2011) Cell death assays for drug discovery. Nat. Rev. Drug Discov. 10, 221-237
77. Xu, T., Zhang, M., Laurent, T., Xie, M., and Ding, S. (2013) Concise review: chemical approaches for modulating lineage-specific stem cells and progenitors. Stem Cells Transl. Med. 2, 355-361
78. Wang, Y., Chou, B. K., Dowey, S., He, C., Gerecht, S., and Cheng, L. (2013) Scalable expansion of human induced pluripotent stem cells in the defined xeno-free E8 medium under adherent and suspension culture conditions. Stem Cell Res. 11, 1103-1116
79. Cao, N., Liang, H., Huang, J., Wang, J., Chen, Y., Chen, Z., and Yang, H. T. (2013) Highly efficient induction and long-term maintenance of multipotent cardiovascular progenitors from human pluripotent stem cells under defined conditions. Cell Res. 23, 1119-1132
80. Blancas, A. A., Shih, A. J., Lauer, N. E., and McCloskey, K. E. (2011) Endothelial cells from embryonic stem cells in a chemically defined medium. Stem Cells Dev. 20, 2153-2161
81. Prescott, C. (2011) The business of exploiting induced pluripotent stem cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 2323-2328
82. Bock, C., Kiskinis, E., Verstappen, G., Gu, H., Boulting, G., Smith, Z. D., Ziller, M., Croft, G. F., Amoroso, M. W., Oakley, D. H., Gnirke, A., Eggan, K., and Meissner, A. (2011) Reference maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 144, 439-452
83. Zweigerdt, R., Olmer, R., Singh, H., Haverich, A., and Martin, U. (2011) Scalable expansion of human pluripotent stem cells in suspension culture. Nat. Protoc. 6, 689-700
84. Pakzad, M., Totonchi, M., Taei, A., Seifinejad, A., Hassani, S. N., and Baharvand, H. (2010) Presence of a ROCK inhibitor in extracellular matrix supports more undifferentiated growth of feeder-free human embryonic and induced pluripotent stem cells upon passaging. Stem Cell Rev. 6, 96-107
85. Haupt, S., Grützner, J., Thier, M. C., Kallweit, T., Rath, B. H., Laufenberg, I., Forgber, M., Eberhardt, J., Edenhofer, F., and Brüstle, O. (2012) Automated selection and harvesting of pluripotent stem cell colonies. Biotechnol. Appl. Biochem. 59, 77-87
86. Yoo, C. H., Na, H. J., Lee, D. S., Heo, S. C., An, Y., Cha, J., Choi, C., Kim, J. H., Park, J. C., and Cho, Y. S. (2013) Endothelial progenitor cells from human dental pulp-derived iPS cells as a therapeutic target for ischemic vascular diseases. Biomaterials 34, 8149-8160
87. Puttonen, K. A., Ruponen, M., Kauppinen, R., Wojciechowski, S., Hovatta, O., and Koistinaho, J. (2013) Improved method of producing human neural progenitor cells of high purity and in large quantities from pluripotent stem cells for transplantation studies. Cell Transplant. 22, 1753-1766
88. Merkle, F. T., and Eggan, K. (2013) From association to function using human pluripotent stem cells. Cell Stem Cell 12, 656-668
89. Sánchez-Danés, A., Richaud-Patin, Y., Carballo-Carbajal, I., Jiménez-Delgado, S., Caig, C., Mora, S., Di Guglielmo, C., Ezquerra, M., Patel, B., Giralt, A., Canals, J. M., Memo, M., Alberch, J., López-Barneo, J., Vila, M., Cuervo, A. M., Tolosa, E., Consiglio, A., and Raya, A. (2012) Diseasespecific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol. Med. 4, 380-395
90. Yung, S. K., Tilgner, K., Ledran, M. H., Habibollah, S., Neganova, I., Singhapol, C., Saretzki, G., Stojkovic, M., Armstrong, L., Przyborski, S., and Lako, M. (2013) Brief report: human pluripotent stem cell models of Fanconi anemia deficiency reveal an important role for Fanconi anemia proteins in cellular reprogramming and survival of hematopoietic progenitors. Stem Cells 31, 1022-1029
91. Müller, L. U., Milsom, M. D., Harris, C. E., Vyas, R., Brumme, K. M., Parmar, K., Moreau, L. A., Schambach, A., Park, I. H., London, W. B., Strait, K., Schlaeger, T., Devine, A. L., Grassman, E., D'Andrea, A., Daley, G. Q., and Williams, D. A. (2012) Overcoming reprogramming resistance of fanconi anemia cells. Blood 119, 5449-5457
92. Urbach, A., Bar-Nur, O., Daley, G. Q., and Benvenisty, N. (2010) Differential modeling of fragile X syndrome by human embryonic stem cells and induced pluripotent stem cells. Cell Stem Cell 6, 407-411
93. Sheridan, S. D., Theriault, K. M., Reis, S. A., Zhou, F., Madison, J. M., Daheron, L., Loring, J. F., and Haggarty, S. J. (2011) Epigenetic characterization of the Fmr1 gene and aberrant neurodevelopment in human induced pluripotent stem cell models of fragile X syndrome. PLoS ONE 6, e26203
94. Marchetto, M. C., Carromeu, C., Acab, A., Yu, D., Yeo, G. W., Mu, Y., Chen, G., Gage, F. H., and Muotri, A. R. (2010) A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143, 527-539
95. Cheung, A. Y., Horvath, L. M., Grafodatskaya, D., Pasceri, P., Weksberg, R., Hotta, A., Carrel, L., and Ellis, J. (2011) Isolation of MECP2-null Rett syndrome patient hiPS cells and isogenic controls through X-chromosome inactivation. Hum. Mol. Genet. 20, 2103-2115
96. Sherman, S. P., and Pyle, A. D. (2013) Small molecule screening with laser cytometry can be used to identify pro-survival molecules in human embryonic stem cells. PLoS ONE 8, e54948
97. Zhang, J. H., Chung, T. D., and Oldenburg, K. R. (1999) A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4, 67-73
98. Inglese, J., Auld, D. S., Jadhav, A., Johnson, R. L., Simeonov, A., Yasgar, A., Zheng, W., and Austin, C. P. (2006) Quantitative high-throughput screening: a titration-based approach that efficiently identifies biological activities in large chemical libraries. Proc. Natl. Acad. Sci. U.S.A. 103, 11473-11478