Ensuring the quality of stem cell-derived in vitro models for toxicity testing

Advances in Experimental Medicine and Biology

Volumn 856, Issue , 2016, Pages 259-297

  Stacey, Glyn N ^a,b   Coecke, Sandra ^b,c   Price, Anna Bal ^b,c   Healy, Lyn ^b,d   Jennings, Paul ^b,e   Wilmes, Anja ^b,e   Pinset, Christian ^b,f   Ingelman Sundberg, Magnus ^b,g   Louisse, Jochem ^h   Haupt, Simone ^h   Kidd, Darren ^h   Robitski, Andrea ^h   Jahnke, Heinz Georg ^h   Lemaitre, Gilles ^b,f   Myatt, Glenn ^h  

^a MEDICINES AND HEALTHCARE PRODUCTS REGULATORY AGENCY   (United Kingdom)

^b SEURAT 1 Stem Cell Group   (France)

^c JOINT RESEARCH CENTRE   (Italy)

^d THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^e INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^f I Stem   (France)

^g KAROLINSKA INSTITUTE   (Sweden)

^h NONE

Author keywords

Quality control; Stem cell characterisation; Stem cell differentiation; Toxicology

Indexed keywords

BIOLOGICAL MARKER;

CELL DIFFERENTIATION; CELL GROWTH; CELL SELECTION; CELL VIABILITY; CYTOTOXICITY; GLIA CELL; HUMAN; IN VITRO STUDY; INFORMED CONSENT; KERATINOCYTE; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; NERVE CELL; PLURIPOTENT STEM CELL; PLURIPOTENT STEM CELL LINE; PRIORITY JOURNAL; QUALITY CONTROL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHORT TANDEM REPEAT; TOXICITY ASSAY; TOXICOLOGY; CELL PROLIFERATION; CYTOLOGY; PROCEDURES; STANDARDS; TOXICITY TESTING;

CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; IN VITRO TECHNIQUES; PLURIPOTENT STEM CELLS; QUALITY CONTROL; TOXICITY TESTS;

EID: 84988983526     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-3-319-33826-2_11     Document Type: Chapter

References (138)

1. Anonymous (1988) A standard nomenclature for structures of the kidney. The Renal Commission of the International Union of Physiological Sciences (IUPS). Pfl ugers Arch 411(1):113-120
2. Acimovic I, Vilotic A, Pesl M, Lacampagne A, Dvorak P, Rotrekl V, Meli AC (2014) Human pluripotent stem cell-derived cardiomyocytes as research and therapeutic tools. Biomed Res Int 2014:512831
3. Adewumi O, Afl atoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G, Bello PA, Benvenisty N, Berry LS, Bevan S, Blum B, Brooking J, Chen KG, Choo AB, Churchill GA, Corbel M, Damjanov I, Draper JS, Dvorak P, Emanuelsson K, Fleck RA, Ford A, Gertow K, Gertsenstein M, Gokhale PJ, Hamilton RS, Hampl A, Healy LE, Hovatta O, Hyllner J, Imreh MP, Itskovitz-Eldor J, Jackson J, Johnson JL, Jones M, Kee K, King BL, Knowles BB, Lako M, Lebrin F, Mallon BS, Manning D, Mayshar Y, McKay RD, Michalska AE, Mikkola M, Mileikovsky M, Minger SL, Moore HD, Mummery CL, Nagy A, Nakatsuji N, O’Brien CM, Oh SK, Olsson C, Otonkoski T, Park KY, Passier R, Patel H, Patel M, Pedersen R, Pera MF, Piekarczyk MS, Pera RA, Reubinoff BE, Robins AJ, Rossant J, Rugg-Gunn P, Schulz TC, Semb H, Sherrer ES, Siemen H, Stacey GN, Stojkovic M, Suemori H, Szatkiewicz J, Turetsky T, Tuuri T, van den Brink S, Vintersten K, Vuoristo S, Ward D, Weaver TA, Young LA, Zhang W, ISCI, International Stem Cell Initiative (2007) Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25:803-816
4. Araoka T, Mae S, Kurose Y, Uesugi M, Ohta A, Yamanaka S, Osafune K (2014) Effi cient and rapid induction of human iPSCs/ESCs into nephrogenic intermediate mesoderm using small molecule-based differentiation methods. PLoS One 9(1), e84881. doi: 10.1371/journal.pone.0084881
5. Augello A, Kurth T, De Bari C (2010) Mesenchymal stem cells: a perspective from in vitro cultures to in vivo migration and niches. Eur Cell Mater 20:121-133
6. Baharvand H, Mehrjardi NZ, Hatami M, Kiani S, Rao M, Haghighi MM (2007) Neural differentiation from human embryonic stem cells in a defi ned adherent culture condition. Int J Dev Biol 51(5):371-378
7. Barallon R, Steven R, Bauer SR, Butler J, Capes-Davis A, Dirks WG, Elmore E, Furtado M, Kline MC, Kohara A, Los GV, MacLeod RAF, Masters JRW, Nardone M, Nardone RM, Nims RW, Price PJ, Reid YA, Shewale J, Sykes G, Steuer AF, Storts DR, Thomson J, Taraporewala Z, Alston-Roberts C, Kerrigan L (2010a) Recommendation of short tandem repeat profi ling for authenticating human cell lines, stem cells, and tissues. In Vitro Cell Dev Biol Anim 46:727-732
8. Barallon R, Steven R, Bauer SR, Butler J, Capes-Davis A, Dirks WG, Elmore E, Furtado M, Kline MC, Kohara A, Los GV, MacLeod RAF, Masters JRW, Nardone M, Nardone RM, Nims RW, Price PJ, Reid YA, Shewale J, Sykes G, Steuer AF, Storts DR, Thomson J, Taraporewala Z, Alston-Roberts C, Kerrigan L (2010b) on behalf of ATCC® SDO Workgroup ASN-0002. Cell line misidentifi cation: the beginning of the end. Nature Rev. Cancer 10:441-448
9. Blin G, Nury D, Stefanovic S, Neri T, Guillevic O, Brinon B, Bellamy V, Rücker-Martin C, Barbry P, Bel A, Bruneval P, Cowan C, Pouly J, Mitalipov S, Gouadon E, Binder P, Hagège A, Desnos M, Renaud JF, Menasché P, Pucéat M (2010) A purifi ed population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates. J Clin Invest 120(4):1125-1139
10. Boute N, Gribouval O, Roselli S, Benessy F, Lee H, Fuchshuber A, Dahan K, Gubler MC, Niaudet P, Antignac C (2000) NPHS2, encoding the glomerular protein podocin, is mutated in autosomal recessive steroid-resistant nephrotic syndrome. Nat Genet 24(4):349-354
11. Boyle S, Shioda T, Perantoni AO, de Caestecker M (2007) Cited1 and Cited2 are differentially expressed in the developing kidney but are not required for nephrogenesis. Dev Dyn 236(8):2321-2330
12. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, Chen J, Evans S (2003) Isl1 identifi es a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5(6):877-889
13. Capes-Davis A, Reid YA, Kline MC, Storts DR, Strauss E, Dirks WG, Drexler HG, MacLeod RAF, Sykes G, Kohara A, Nakamura Y, Elmore E, Nims RW, Alston-Roberts C, Barallon R, Los GV, Nardone RM, Price PJ, Steuer A, Thomson J, Masters JRW, Kerrigan L (2013) Match criteria for human cell line authentication: where do we draw the line? Intl J Cancer 132:2510-2519
14. Carpenter MK, Inokuma MS, Denham J, Mujtaba T, Chiu CP, Rao MS (2001) Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 172(2):383-397
15. Chen Y, Pelekanos R, Ellis R, Horne R, Wolvetang E, Fisk N (2012) Small molecule mesengenic induction of human induced pluripotent stem cells to generate mesenchymal stem/stromal cells. Stem Cells Transl Med 1(2):83-95
16. Chen KT, Pernelle K, Tsai YH, Wu YH, Hsieh JY, Liao KH, Guguen-Guillouzo C, Wang HW (2014) Liver X receptor α (LXRα/NR1H3) regulates differentiation of hepatocyte-like cells via reciprocal regulation of HNF4α. J Hepatol 61(6):1276-1286
17. Coecke S, Balls M, Bowe G, Davis J, Gstraunthaler G, Hartung T, Hay R, Merten OW, Price A, Schechtman L, Stacey G, Stokes W (2005) Guidance on good cell culture practice. Altern Lab Anim 33:261-287
18. Coecke S, Bowe G, Millcamps A, Bernasconi C, Bostroem AC, Bories G, Fortaner S, Gineste JM, Gouliarmou V, Langezaal I, Liska R, Mendoza E, Morath S, Reina V, Wilk-Zasadna I, Whelan M (2014) Considerations in the development of in vitro toxicity testing methods intended for regulatory use. In: Paul J, Anna P (eds) In vitro toxicology systems, Methods in pharmacology and toxicology. Springer, New York, pp 551-569
19. Davies JA (2002) Morphogenesis of the metanephric kidney. Scientifi cWorldJournal 2:1937-1950. doi: 10.1100/tsw.2002.854
20. Dinella J, Koster M, Koch P (2014) Use of induced pluripotent stem cells in dermatological research. J Invest Dermatol 134, e23. doi: 10.1038/jid.2014.238
21. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D et al (2006) Minimal criteria for defi ning multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315-317
22. Dressler GR (2006) The cellular basis of kidney development. Annu Rev Cell Dev Biol 22:509-529. doi: 10.1146/annurev.cellbio.22.010305.104340
23. Dressler GR (2009) Advances in early kidney specifi cation, development and patterning. Development 136(23):3863-3874. doi: 10.1242/dev.034876
24. Efthymiou A, Chen G, Rao M, Chen G, Boehm M (2014) Self-renewal and cell lineage differentiation strategies in human embryonic stem cells and induced pluripotent stem cells. Expert Opin Biol Ther 14(9):1333-1344
25. Faul C, Asanuma K, Yanagida-Asanuma E, Kim K, Mundel P (2007) Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton. Trends Cell Biol 17(9):428-437
26. Freund C, Davis RP, Gkatzis K, Ward-van Oostwaard D, Mummery CL (2010) The fi rst reported generation of human induced pluripotent stem cells (iPS cells) and iPS cell-derived cardiomyocytes in the Netherlands. Neth Heart J 18(1):51-54
27. Genschow E, Spielmann H, Scholz G, Pohl I, Seiler A, Clemann N, Bremer S, Becker K (2004) Validation of the embryonic stem cell test in the international ECVAM validation study on three in vitro embryotoxicity tests. Altern Lab Anim 32:209-244
28. Gieseck IRL, Hannan NR, Bort R, Hanley NA, Drake RA, Cameron GW, Wynn TA, Vallier L (2014) Maturation of induced pluripotent stem cell derived hepatocytes by 3D-culture. PLoS One 9(1), e86372
29. Glenn J, Whartenby K (2014) Mesenchymal stem cells: Emerging mechanisms of immunomodulation and therapy. World J Stem Cells 6(5):526-539
30. Glenner GG, Folk JE (1961) Glutamyl peptidases in rat and guinea pig kidney slices. Nature 192:338-340
31. Graichen R, Xu X, Braam SR, Balakrishnan T, Norfi za S, Sieh S, Soo SY, Tham SC, Mummery C, Colman A, Zweigerdt R, Davidson BP (2008) Enhanced cardiomyogenesis of human embryonic stem cells by a small molecular inhibitor of p38 MAPK. Differentiation 76(4):357-370
32. Green H, Easley K, Iuchi S (2003) Marker succession during the development of keratinocytes from cultured human embryonic stem cells. Proc Natl Acad Sci U S A 100:15625-15630
33. Guenou H, Nissan X, Larcher F, Feteira J, Lemaitre G, Saidani M, Del Rio M, Barrault CC, Bernard FX, Peschanski M et al (2009) Human embryonic stem-cell derivatives for full reconstruction of the pluristratifi ed epidermis, a preclinical study. Lancet 374:1745-1753
34. Guo Z, Higgins C, Gillette B, Itoh M, Umegaki N, Gledhill K, Sia S, Christiano A (2013) Building a microphysiological skin model from induced pluripotent stem cells. Stem Cell Res Ther 4(Suppl 1):S2. doi: 10.1186/scrt363
35. Gupta K, Rispin A, Stitzel K, Coecke S, Harbell J (2005) Ensuring quality of in vitro alternative test methods: issues and answers. Regul Toxicol Pharmacol 43:219-224
36. Han Y, Miller A, Mangada J, Liu Y, Swistowski A, Zhan M, Rao MS, Zeng X (2009) Identifi cation by automated screening of a small molecule that selectively eliminates neural stem cells derived from hESCs but not dopamine neurons. PLoS One 4(9), e7155. doi: 10.1371/journal.pone.0007155
37. Haniffa M, Collin M, Buckley C, Dazzi F (2009) Mesenchymal stem cells: the fi broblasts’ new clothes? Haematologica 94(2):258-263
38. Harrill JA, Freudenrich TM, Machacek DW, Stice SL, Mundy WR (2010) Quantitative assessment of neurite outgrowth in human embryonic stem cell-derived hN2 cells using automated highcontent image analysis. Neurotoxicology 31(3):277-290
39. Hartung T, Gstraunthaler G, Balls M (2000) Bologna statement on good cell culture practice (GCCP). ALTEX 17:38-39
40. Hay DC, Fletcher J, Payne C, Terrace JD, Gallagher RC, Snoeys J, Black JR, Wojtacha D, Samuel K, Hannoun Z, Pryde A, Filippi C, Currie IS, Forbes SJ, Ross JA, Newsome PN, Iredale JP (2008) Highly effi cient differentiation of hESCs to functional hepatic endoderm requires Activin A and Wnt3a signaling. Proc Natl Acad Sci U S A 105(34):12301-12306
41. Hematti P (2011) Human embryonic stem cell-derived mesenchymal progenitors: an overview. Methods Mol Biol 690:163-174
42. Hematti P (2012) Mesenchymal stromal cells and fi broblasts: a case of mistaken identity? Cytotherapy 14(5):516-521
43. Hogberg HT, Sobanski T, Novellino A, Whelan M, Weiss DG, Bal-Price AK (2011) Application of micro-electrode arrays (MEAs) as an emerging technology for developmental neurotoxicity: evaluation of domoic acid-induced effects in primary cultures of rat cortical neurons. Neurotoxicology 32(1):158-168
44. Holthofer H, Ahola H, Solin ML, Wang S, Palmen T, Luimula P, Miettinen A, Kerjaschki D (1999) Nephrin localizes at the podocyte fi ltration slit area and is characteristically spliced in the human kidney. Am J Pathol 155(5):1681-1687
45. Holzman LB, St John PL, Kovari IA, Verma R, Holthofer H, Abrahamson DR (1999) Nephrin localizes to the slit pore of the glomerular epithelial cell. Kidney Int 56(4):1481-1491
46. Horvat R, Hovorka A, Dekan G, Poczewski H, Kerjaschki D (1986) Endothelial cell membranes contain podocalyxin—the major sialoprotein of visceral glomerular epithelial cells. J Cell Biol 102(2):484-491
47. International Stem Cell Banking Initiative, Andrews PW, Arias-Diaz J, Auerbach J et al (2009) Consensus guidance for banking and supply of human embryonic stem cell lines for research purposes. Stem Cell Rev 5:301-314
48. Isasi R, Andrews PW, Baltz JM, Bredenoord AL, Burton P, Chiu IM, Hull SC, Jung JW, Kurtz A, Lomax G, Ludwig T, McDonald M, Morris C, Ng HH, Rooke H, Sharma A, Stacey GN, Williams C, Zeng F, Knoppers BM (2014) Identifi ability and privacy in pluripotent stem cell research. Cell Stem Cell 14(4):427-430
49. Islam M, Stemig M, Takahashi Y, Hui S (2015) Radiation response of mesenchymal stem cells derived from bone marrow and human pluripotent stem cells. J Radiat Res 56(2):269-277
50. Itoh M, Kiuru M, Cairo MS, Christiano AM (2011) Generation of keratinocytes from normal and recessive dystrophic epidermolysis bullosa-induced pluripotent stem cells. Proc Natl Acad Sci U S A 108:8797-8802
51. Ivashchenko CY, Pipes GC, Lozinskaya IM, Lin Z, Xiaoping X, Needle S, Grygielko ET, Hu E, Toomey JR, Lepore JJ, Willette RN (2013) Human-induced pluripotent stem cell-derived cardiomyocytes exhibit temporal changes in phenotype. Am J Physiol Heart Circ Physiol 305(6):H913-H922
52. Jennings P, Koppelstaetter C, Helbert MJ, Pfaller W (2003) Renal culture models: Contribution to the understanding of nephrotoxic mechanisms. Clinical Nephrotoxins: Renal Injury from drugs and chemicals, 2nd edn, pp. 115-147
53. Jennings P, Koppelstaetter C, Lechner J, Pfaller W (2008) Renal culture models: contribution to the understanding of nephrotoxic mechanisms. In: Broe ME, Porter GA (eds) Clinical nephrotoxins: renal injury from drugs and chemicals, 3rd edn. Springer, New York, pp 223-250
54. Jennings P, Aschauer L, Wilmes A, Gstraunthaler G (2014) Renal cell culture. In: Jennings P, Bal-Price A (eds) In vitro toxicology systems. Methods in pharmacology and toxicology. Springer, New York, pp 79-101. doi: 10.1007/978-1-4939-0521-8_4
55. Kerjaschki D, Sharkey DJ, Farquhar MG (1984) Identifi cation and characterization of podocalyxin— the major sialoprotein of the renal glomerular epithelial cell. J Cell Biol 98(4):1591-1596
56. Kerrigan L, Nims RW (2011) Authentication of human cell-based products: the role of a new consensus standard. Regen Med 6:255-260, http://standards.atcc.org/kwspub/home/the_international_cell_line_authentication_committee-iclac_/ )
57. Kestila M, Lenkkeri U, Mannikko M, Lamerdin J, McCready P, Putaala H, Ruotsalainen V, Morita T, Nissinen M, Herva R, Kashtan CE, Peltonen L, Holmberg C, Olsen A, Tryggvason K (1998) Positionally cloned gene for a novel glomerular protein—nephrin—is mutated in congenital nephrotic syndrome. Mol Cell 1(4):575-582
58. Knoppers BM, Isasi R, Benvenisty N, Kim OJ, Lomax G, Morris C, Murray TH, Lee EH, Perry M, Richardson G, Sipp D, Tanner K, Wahlström J, de Wert G, Zeng F (2011) Publishing SNP genotypes of human embryonic stem cell lines: policy statement of the International Stem Cell Forum Ethics Working Party. Stem Cell Rev 7(3):482-484
59. Kriz W, Kaissling B (2000) Structural organization of the mammalian kidney, vol 1, 3rd edn, The kidney, physiology and pathophysiology. Lippincott Williams & Wilkins, Philadelphia
60. Lam AQ, Freedman BS, Morizane R, Lerou PH, Valerius MT, Bonventre JV (2014) Rapid and effi cient differentiation of human pluripotent stem cells into intermediate mesoderm that forms tubules expressing kidney proximal tubular markers. J Am Soc Nephrol 25(6):1211-1225
61. Lappalainen RS, Salomäki M, Ylä-Outinen L, Heikkilä TJ, Hyttinen JA, Pihlajamäki H, Suuronen R, Skottman H, Narkilahti S (2010) Similarly derived and cultured hESC lines show variation in their developmental potential towards neuronal cells in long-term culture. Regen Med 5(5):749-762
62. Laustriat D, Gide J, Peschanski M (2010) Human pluripotent stem cells in drug discovery and predictive toxicology. Biochem Soc Trans 38:1051-1057
63. Lee YK, Ng KM, Lai WH, Chan YC, Lau YM, Lian Q, Tse HF, Siu CW (2011) Calcium homeostasis in human induced pluripotent stem cell-derived cardiomyocytes. Stem Cell Rev 7(4):976-986
64. Li C, Ruotsalainen V, Tryggvason K, Shaw AS, Miner JH (2000) CD2AP is expressed with nephrin in developing podocytes and is found widely in mature kidney and elsewhere. Am J Physiol Renal Physiol 279(4):F785-F792
65. Li O, Tormin A, Sundberg B, Hyllner J, Le Blanc K, Scheding S (2013) Human embryonic stem cell-derived mesenchymal stroma cells (hES-MSCs) engraft in vivo and support hematopoiesis without suppressing immune function: implications for off-the shelf ES-MSC therapies. PLoS One 8(1), e55319. doi: 10.1371/journal.pone.0055319
66. Lian X, Hsiao C, Wilson G, Zhu K, Hazeltine LB, Azarin SM, Raval KK, Zhang J, Kamp TJ, Palecek SP (2012) Robust cardiomyocyte differentiation from human pluripotent stem cells viatemporal modulation of canonical Wnt signaling. Proc Natl Acad Sci U S A 109(27):E1848-E1857
67. Lim SY, Sivakumaran P, Crombie DE, Dusting GJ, Pébay A, Dilley RJ (2013) Trichostatin A enhances differentiation of human induced pluripotent stem cells to cardiogenic cells for cardiac tissue engineering. Stem Cells Transl Med 2(9):715-725
68. Lundy SD, Zhu WZ, Regnier M, Lafl amme MA (2013) Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev 22(14):1991-2002
69. Luong MX, Auerbach J, Crook JM, Daheron L, Hei D, Lomax G, Loring JF, Ludwig T, Schlaeger TM, Smith KP, Stacey G, Xu RH, Zeng F (2011) A call for standardized naming and reporting of human ESC and iPSC lines. Cell Stem Cell 8(4):357-359
70. Luong MXL, Smith KP, Crook JM, Stacey GN (2012) Biobanks for pluripotent stem cells (Chapter 8). In: Loring JF, Petersen SE (eds) Human stem cell manual, 2nd edn. Elsevier, London, pp 105-125
71. MacLeod RAF, Dirks WG, Matsuo Y, Kaufman M, Milch H, Drexler HG (1999) Widespread intraspecies cross-contamination of human tumour cell lines arising at source. Int J Cancer 83:555-563
72. Mordwinkin NM, Burridge PW, Wu JC (2013) A review of human pluripotent stem cell-derived cardiomyocytes for high-throughput drug discovery, cardiotoxicity screening, and publication standards. J Cardiovasc Transl Res 6(1):22-30
73. Motohashi H, Nakao Y, Masuda S, Katsura T, Kamba T, Ogawa O, Inui K (2013) Precise comparison of protein localization among OCT, OAT, and MATE in human kidney. J Pharm Sci 102(9):3302-3308
74. Mummery C, Ward-van Oostwaard D, Doevendans P, Spijker R, van den Brink S, Hassink R, van der Heyden M, Opthof T, Pera M, de la Riviere AB, Passier R, Tertoolen L (2003) Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endodermlike cells. Circulation 107(21):2733-2740
75. Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, Furuse K, Sasaki H, Fujimura A, Imai M, Kusano E, Tsukita S, Furuse M (2010) Claudin-2-defi cient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc Natl Acad Sci U S A 107(17):8011-8016
76. Narayanan K, Schumacher KM, Tasnim F, Kandasamy K, Schumacher A, Ni M, Gao S, Gopalan B, Zink D, Ying JY (2013) Human embryonic stem cells differentiate into functional renal proximal tubular-like cells. Kidney Int 83(4):593-603
77. Nat R, Nilbratt M, Narkilahti S, Winblad B, Hovatta O, Nordberg A (2007) Neurogenic neuroepithelial and radial glial cells generated from six human embryonic stem cell lines in serum-free suspension and adherent cultures. Glia 55(4):385-399
78. Nielsen S, Frokiaer J, Marples D, Kwon TH, Agre P, Knepper MA (2002) Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82(1):205-244
79. Nims RW, Sykes G, Cottrill K, Ikonomi P, Elmore E (2010) Short tandem repeat profi ling: part of an overall strategy for reducing the frequency of cell misidentifi cation. In Vitro Cell Dev Biol Anim 46:811-819
80. Novellino A, Scelfo B, Palosaari T, Price A, Sobanski T, Shafer TJ, Johnstone AF, Gross GW, Gramowski A, Schroeder O, Jügelt K, Chiappalone M, Benfenati F, Martinoia S, Tedesco MT, Defranchi E, D’Angelo P, Whelan M (2011) Development of micro-electrode array based tests for neurotoxicity: assessment of interlaboratory reproducibility with neuroactive chemicals. Front Neuroeng 4:4. doi: 10.3389/fneng.2011.00004
81. Nunes SS, Miklas JW, Liu J, Aschar-Sobbi R, Xiao Y, Zhang B, Jiang J, Massé S, Gagliardi M, Hsieh A, Thavandiran N, Lafl amme MA, Nanthakumar K, Gross GJ, Backx PH, Keller G, Radisic M (2013) Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat Methods 10(8):781-787
82. OECD (2005) OECD series on testing and assessment. Number 34. Guidance document on the validation and international acceptance of new or updated test methods for hazard assessment. ENV/JM/MONO(2005)14
83. Paige SL, Osugi T, Afanasiev OK, Pabon L, Reinecke H, Murry CE (2010) Endogenous Wnt/betacatenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 5(6), e11134
84. Pan GJ, Chang ZY, Scholer HR, Pei D (2002) Stem cell pluripotency and transcription factor Oct4. Cell Res 12(5-6):321-329
85. Passier R, Oostwaard DW, Snapper J, Kloots J, Hassink RJ, Kuijk E, Roelen B, de la Riviere AB, Mummery C (2005) Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 23(6):772-780
86. Petrova A, Celli A, Jacquet L, Dafou D, Crumrine D, Hupe M, Arno M, Hobbs C, Cvoro A, Karagiannis P, Devito L, Sun R, Adame L, Vaughan R, McGrath J, Mauro T, Ilic D (2014) 3D in vitro model of a functional epidermal permeability barrier from human embryonic stem cells and induced pluripotent stem cells. Stem Cell Reports 2 (5):675-689
87. Pistollato F, Bremer-Hoffmann S, Healy L, Young L, Stacey G (2012) Standardization of pluripotent stem cell cultures for toxicity testing. Expert Opin Drug Metab Toxicol 8:239-257
88. Ren Y, Lee MY, Schliffke S, Paavola J, Amos PJ, Ge X, Ye M, Zhu S, Senyei G, Lum L, Ehrlich BE, Qyang Y (2011) Small molecule Wnt inhibitors enhance the effi ciency of BMP-4-directed cardiac differentiation of human pluripotent stem cells. J Mol Cell Cardiol 51(3):280-287
89. Richert L, Liguori MJ, Abadie C, Heyd B, Mantion G, Halkic N, Waring JF (2006) Gene expression in human hepatocytes in suspension after isolation is similar to the liver of origin, is not affected by hepatocyte cold storage and cryopreservation, but is strongly changed after hepatocyte plating. Drug Metab Dispos 34(5):870-879
90. Rispin A, Harbell JW, Klausner M, Jordan FT, Coecke S, Gupta K, Stitzek K (2004) Quality assurance for in vitro alternative test methods: quality control issues in test kit production. Altern Lab Anim 1(Suppl):725-729
91. Roselli S, Gribouval O, Boute N, Sich M, Benessy F, Attie T, Gubler MC, Antignac C (2002) Podocin localizes in the kidney to the slit diaphragm area. Am J Pathol 160(1):131-139
92. Ruotsalainen V, Ljungberg P, Wartiovaara J, Lenkkeri U, Kestila M, Jalanko H, Holmberg C, Tryggvason K (1999) Nephrin is specifi cally located at the slit diaphragm of glomerular podocytes. Proc Natl Acad Sci U S A 96(14):7962-7967
93. Sariola H (2002) Nephron induction. Nephrol Dial Transplant 17(Suppl 9):88-90
94. Scanu M, Mancuso L, Cao G (2011) Evaluation of the use of human Mesenchymal Stem Cells for acute toxicity tests. Toxicol In Vitro 25(8):1989-1995
95. Schulz TC, Noggle SA, Palmarini GM, Weiler DA, Lyons IG, Pensa KA, Meedeniya AC, Davidson BP, Lambert NA, Condie BG (2004) Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells 22(7):1218-1238
96. Schwartz RE, Fleming HE, Khetani SR, Bhatia SN (2014) Pluripotent stem cell-derived hepatocyte-like cells. Biotechnol Adv 32(2):504-513
97. Schwarz K, Simons M, Reiser J, Saleem MA, Faul C, Kriz W, Shaw AS, Holzman LB, Mundel P (2001) Podocin, a raft-associated component of the glomerular slit diaphragm, interacts with CD2AP and nephrin. J Clin Invest 108(11):1621-1629
98. Scott CW, Peters MF, Dragan YP (2013) Human induced pluripotent stem cells and their use in drug discovery for toxicity testing. Toxicol Lett 219(1):49-58
99. Shan J, Schwartz RE, Ross NT, Logan DJ, Thomas D, Duncan SA, North TE, Goessling W, Carpenter AE, Bhatia SN (2013) Identifi cation of small molecules for human hepatocyte expansion and iPS differentiation. Nat Chem Biol 9(8):514-520
100. Shih NY, Li J, Cotran R, Mundel P, Miner JH, Shaw AS (2001) CD2AP localizes to the slit diaphragm and binds to nephrin via a novel C-terminal domain. Am J Pathol 159(6):2303-2308. doi: 10.1016/S0002-9440(10)63080-5
101. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O, Wray J, Yamanaka S, Chambers I, Smith A (2009) Nanog is the gateway to the pluripotent ground state. Cell 138(4):722-737
102. Sirenko O, Hesley J, Rusyn I, Cromwell EF (2014) High-content assays for hepatotoxicity using induced pluripotent stem cell-derived cells. Assay Drug Dev Technol 12(1):43-54
103. Sivertsson L, Synnergren J, Jensen J, Björquist P, Ingelman-Sundberg M (2013) Hepatic differentiation and maturation of human embryonic stem cells cultured in a perfused three-dimensional bioreactor. Stem Cells Dev 22(4):581-594
104. Soleimani M (2015) The multiple roles of pendrin in the kidney. Nephrol Dial Transplant 30(8):1257-1266. doi: 10.1093/ndt/gfu307
105. Song B, Smink AM, Jones CV, Callaghan JM, Firth SD, Bernard CA, Laslett AL, Kerr PG, Ricardo SD (2012) The directed differentiation of human iPS cells into kidney podocytes. PLoS One 7(9), e46453. doi: 10.1371/journal.pone.0046453
106. Stacey G, Day JG (2007) Long-term ex situ conservation of biological resources and the role of biological resource centers. In: Day DG, Stacey GN (eds) Cryopreservation and freezedrying methods. Humana Press, Totowa
107. Stacey GN, Masters JR (2008) Cryopreservation and banking of mammalian cell lines. Nat Protoc 3:1981-1989
108. Stacey G, Masters JRW, Hay RJ, Drexler HG, MacLeod RAF, Freshney IR (2000) Cell contamination leads to inaccurate data: we must take action now. Nature 403:356
109. Stacey G, Pistollato F, Healy L, Bremer S, Young L, Strehl R, Hyllner J, Emmanuelsson K and Peschanski M on behalf of the Scr&Tox and ToxBank consortia (2012) General Quality and Regulatory Criteria for Establishment and Dissemination of human Pluripotent Stem Cell Lines (hPSCs). Poster presented at Surat-1 scientifi c meeting Lisbon, 2012 and published on the ToxBank data warehouse at http://www.toxbank.net/bio-wikiorhttp://wiki.toxbank.net/w/images/0/08/ToxBank_poster5-CellStandards-120130.pdf
110. Stacey G, Healy L, Kidane L (2012) Points to consider in gaining access to human tissue and cell lines. ToxBank Deliverable 4.6. http://wiki.toxbank.net/w/images/1/18/ToxBank_D4_6_fi nal_10_04_13.pdf
111. Stacey G, Kidane L, Healy L, Myatt G on behalf of ToxBank consortium (2014) Deliverable D4.7. Inventory and map of European suppliers: materials, resources, facilities and standards.http://wiki.toxbank.net/w/images/c/c2/ToxBank_D4_7_Final_11.06.13.pdf
112. Stacey G, Kidane L, Healy L, Myatt G, Hardy B, Bremer S (2014) Coordination of data systems in SEURAT-1 and alternative testing regulatory frameworks to provide smooth and effi cient translation of research developments to qualifi ed toxicity assays. Poster presented at SEURAT-1 scientifi c meeting Lisbon, 2014 and published on the ToxBank data warehouse at http://www.toxbank.net/bio-wiki;http://wiki.toxbank.net/w/images/3/35/ToxBank_ToxBank_JRC_Coord_Poster_Stacey_et_al.pdf
113. Stanley EG, Biben C, Elefanty A, Barnett L, Koentgen F, Robb L, Harvey RP (2002) Effi cient Cre-mediated deletion in cardiac progenitor cells conferred by a 3′UTR-ires-Cre allele of the homeobox gene Nkx2-5. Int J Dev Biol 46(4):431-439
114. Subramanian K, Owens DJ, Raju R, Firpo M, O’Brien TD, Verfaillie CM, Hu WS (2014) Spheroid culture for enhanced differentiation of human embryonic stem cells to hepatocyte-like cells. Stem Cells Dev 23(2):124-131
115. Sutton M, Bonfi eld T (2014) Stem cells: innovations in clinical applications. Stem Cells Int 2014:516278. doi: 10.1155/2014/516278
116. Szkolnicka D, Farnworth SL, Lucendo-Villarin B, Storck C, Zhou W, Iredale JP, Flint O, Hay DC (2014) Accurate prediction of drug-induced liver injury using stem cell-derived populations. Stem Cells Transl Med 3(2):141-148
117. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fi broblasts by defi ned factors. Cell 131:861-872
118. Takasato M, Er PX, Becroft M, Vanslambrouck JM, Stanley EG, Elefanty AG, Little MH (2014) Directing human embryonic stem cell differentiation towards a renal lineage generates a selforganizing kidney. Nat Cell Biol 16(1):118-126
119. Takebe T, Sekine K, Enomura M, Koike H, Kimura M, Ogaeri T, Zhang RR, Ueno Y, Zheng YW, Koike N, Aoyama S, Adachi Y, Taniguchi H (2013) Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499(7459):481-484
120. Takebe T, Zhang RR, Koike H, Kimura M, Yoshizawa E, Enomura M, Koike N, Sekine K, Taniguchi H (2014) Generation of a vascularized and functional human liver from an iPSCderived organ bud transplant. Nat Protoc 9(2):396-409
121. Tang M, Chen W, Liu J, Weir M, Cheng L, Xu H (2014) Human induced pluripotent stem cellderived mesenchymal stem cell seeding on calcium phosphate scaffold for bone regeneration. Tissue Eng Part A 20(7-8):1295-1305
122. Tarunina M, Hernandez D, Johnson CJ, Ramathas V, Jeyakumar M, Watson T et al (2014) Directed differentiation of embryonic stem cells using a bead-based combinatorial screening method. PLoS ONE 9(9), e104301. doi: 10.1371/journal.pone.0104301
123. TheinHan W, Liu J, Tang M, Chen W, Cheng L, Xu H (2013) Induced pluripotent stem cell-derived mesenchymal stem cell seeding on biofunctionalized calcium phosphate cements. Bone Res 4:371-384
124. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM (1998) Embryonic stem cell lines derived from human blastocysts. Science 282(5391): 1145-1147
125. Ulvestad M, Nordell P, Asplund A, Rehnström M, Jacobsson S, Holmgren G, Davidson L, Brolén G, Edsbagge J, Björquist P, Küppers-Munther B, Andersson TB (2013) Drug metabolizing enzyme and transporter protein profi les of hepatocytes derived from human embryonic and induced pluripotent stem cells. Biochem Pharmacol 86(5):691-702
126. United States Pharmacoipoiea (2013) General Chapter. Cryopreservation of Cells, U.S. Pharmacopeia and the National Formulary (USP-NF). http://www.usp.org/councilexperts-expert-committees-overview/expert-committees/general-chapters-biological-analysis
127. Uosaki H, Fukushima H, Takeuchi A, Matsuoka S, Nakatsuji N, Yamanaka S, Yamashita JK (2011) Effi cient and scalable purifi cation of cardiomyocytes from human embryonic and induced pluripotent stem cells by VCAM1 surface expression. PLoS One 6(8), e23657
128. Van Itallie CM, Rogan S, Yu A, Vidal LS, Holmes J, Anderson JM (2006) Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am J Physiol Renal Physiol 291(6):F1288-F1299
129. Vinoth K, Manikandan J, Sethu S, Balakrishnan L, Heng A, Lu K, Hande M, Cao T (2014) Evaluation of human embryonic stem cells and their differentiated fi broblastic progenies as cellular models for in vitro genotoxicity screening. J Biotechnol 184:154-168
130. Wilmes A, Jennings P (2014) The use of renal cell culture for nephrotoxicity investigations. In: Predictive toxicology. Wiley-VCH Verlag GmbH & Co, KGaA, Weinheim, pp 195-216. doi: 10.1002/9783527674183.ch10
131. Wilmes A, Aschauer L, Limonciel A, Pfaller W, Jennings P (2014) Evidence for a role of claudin 2 as a proximal tubular stress responsive paracellular water channel. Toxicol Appl Pharmacol 279(2):163-172
132. Xia Y, Nivet E, Sancho-Martinez I, Gallegos T, Suzuki K, Okamura D, Wu MZ, Dubova I, Esteban CR, Montserrat N, Campistol JM, Izpisua Belmonte JC (2013) Directed differentiation of human pluripotent cells to ureteric bud kidney progenitor-like cells. Nat Cell Biol 15(12):1507-1515. doi: 10.1038/ncb2872
133. Yuan SH, Martin J, Elia J, Flippin J, Paramban RI, Hefferan MP, Vidal JG, Mu Y, Killian RL, Israel MA, Emre N, Marsala S, Marsala M, Gage FH, Goldstein LS, Carson CT (2011) Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS One 6(3), e17540. doi: 10.1371/journal.pone.0017540
134. Zeng X, Chen J, Deng X, Liu Y, Rao MS, Cadet JL, Freed WJ (2006) An in vitro model of human dopaminergic neurons derived from embryonic stem cells: MPP+ toxicity and GDNF neuroprotection. Neuropsychopharmacology 31(12):2708-2715
135. Zeng H, Guo M, Martins-Taylor K, Wang X, Zhang Z, Park JW, Zhan S, Kronenberg MS, Lichtler A, Liu HX, Chen FP, Yue L, Li XJ, Xu RH (2010) Specifi cation of region-specifi c neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS One 5(7), e11853. doi: 10.1371/journal.pone.0011853
136. Zhang SC, Wernig M, Duncan ID, Brüstle O, Thomson JA (2001) In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19(12):1129-1133
137. Zhang P, Li J, Tan Z, Wang C, Liu T, Chen L, Yong J, Jiang W, Sun X, Du L, Ding M, Deng H (2008) Short-term BMP-4 treatment initiates mesoderm induction in human embryonic stem cells. Blood 111(4):1933-1941
138. Zhou J, Su P, Li D, Tsang S, Duan E, Wang F (2010) High-effi ciency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor beta superfamily receptors. Stem Cells 28(10):1741-1750