Human induced pluripotent stem cells and their use in drug discovery for toxicity testing

Toxicology Letters

Volumn 219, Issue 1, 2013, Pages 49-58

  Scott, Clay W ^a   Peters, Matthew F ^a   Dragan, Yvonne P ^a  

^a ASTRAZENECA   (United Kingdom)

Author keywords

Cardiomyocytes; Drug induced liver injury; Induced pluripotent stem cells; Microelectrode array; Toxicity

Indexed keywords

TRANSCRIPTION FACTOR;

ACTION POTENTIAL; CALCIUM TRANSPORT; CARDIOTOXICITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CLINICAL EFFECTIVENESS; COMPUTER MODEL; CYTOTOXICITY; DRUG DEVELOPMENT; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; EPIGENETICS; EX VIVO STUDY; FIBROBLAST; FOLLOW UP; GENE MUTATION; GLIA CELL; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART REPOLARIZATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER TOXICITY; NERVE CELL; NERVE FIBER GROWTH; NEUROTOXICITY; NONHUMAN; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QT PROLONGATION; REGENERATIVE MEDICINE; REVIEW; RISK ASSESSMENT; SAFETY; SEIZURE; STEM CELL TRANSPLANTATION; SYNAPTIC TRANSMISSION; TERATOGENICITY; TOXICITY TESTING; WOUND HEALING; XENOBIOTIC METABOLISM;

CELL CULTURE TECHNIQUES; CENTRAL NERVOUS SYSTEM; DRUG DISCOVERY; DRUG EVALUATION, PRECLINICAL; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LIVER; MYOCYTES, CARDIAC; REGENERATIVE MEDICINE; TOXICITY TESTS;

EID: 84875506766     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.02.020     Document Type: Review

References (79)

1. Asai Y., Tada M., Otsuji T.G., Nakatsuji N. Combination of functional cardiomyocytes derived from human stem cells and a highly-efficient microelectrode array system: an ideal hybrid model assay for drug development. Current Stem Cell Research & Therapy 2010, 5:227-232.
2. Bailey J., Knight A., Balcombe J. The future of teratology research is in vitro. Biogenic Amines 2005, 19:97-145.
3. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
4. Blazeski A., Zhu R., Hunter D.W., Weinberg S.H., Boheler K.R., Zambidis E.T., Tung L. Electrophysiological and contractile function of cardiomyocytes derived from human embryonic stem cells. Progress in Biophysics and Molecular Biology 2012, 110:178-195.
5. Budnitz D.S., Pollock D.A., Weidenbach K.N., Mendelsohn A.B., Schroeder T.J., Annest J.L. National surveillance of emergency department visits for outpatient adverse drug events. JAMA: The Journal of the American Medical Association 2006, 296:1858-1866.
6. Cerignoli F., Charlot D., Whittaker R., Ingermanson R., Gehalot P., Savchenko A., Gallacher D.J., Towart R., Price J.H., McDonough P.M., Mercola M. High throughput measurement of Ca(2+) dynamics for drug risk assessment in human stem cell-derived cardiomyocytes by kinetic image cytometry. Journal of Pharmacological and Toxicological Methods 2012, 66:246-256.
7. Defranchi E., Novellino A., Whelan M., Vogel S., Ramirez T., van Ravenzwaay B., Landsiedel R. Feasibility assessment of micro-electrode chip assay as a method of detecting neurotoxicity in vitro. Frontiers in Neuroengineering 2011, 4:1-12.
8. Easter A., Bell M.E., Damewood J.R., Redfern W.S., Valentin J.P., Winter M.J., Fonck C., Bialecki R.A. Approaches to seizure risk assessment in preclinical drug discovery. Drug Discovery Today 2009, 14:876-884.
9. Ebert A.D., Yu J., Rose F.F., Mattis V.B., Lorson C.L., Thomson J.A., Svendsen C.N. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009, 457:277-280.
10. Feinberg A.W., Alford P.W., Jin H., Ripplinger C.M., Werdich A.A., Sheehy S.P., Grosberg A., Parker K.K. Controlling the contractile strength of engineered cardiac muscle by hierarchal tissue architecture. Biomaterials 2012, 33:5732-5741.
11. Germanguz I., Sedan O., Zeevi-Levin N., Shtrichman R., Barak E., Ziskind A., Eliyahu S., Meiry G., Amit M., Itskovitz-Eldor J., Binah O. Molecular characterization and functional properties of cardiomyocytes derived from human inducible pluripotent stem cells. Journal of Cellular and Molecular Medicine 2011, 15:38-51.
12. Ghodsizadeh A., Taei A., Totonchi M., Seifinejad A., Gourabi H., Pournasr B., Aghdami N., Malekzadeh R., Almadani N., Salekdeh G.H., Baharvand H. Generation of liver disease-specific induced pluripotent stem cells along with efficient differentiation to functional hepatocyte-like cells. Stem Cell Reviews 2010, 6:622-632.
13. Gomez-Lechon M.J., Castel J., Donato M. Hepatocytes - the choice to investigate drug metabolism and toxicity in man: in vitro variability as a reflection of in vivo. Chemico-Biological Interactions 2006, 168:30-50.
14. Gramowski A., Jugelt K., Stuwe S., Schulze R., McGregor G.P., Wartenberg-Demand A., Loock J., Schroder O., Weiss D.G. Functional screening of traditional antidepressants with primary cortical neuronal networks grown on multielectrode neurochips. European Journal of Neuroscience 2006, 24:455-465.
15. Gramowski A., Jugelt K., Weiss D.G., Gross G.W. Substance identification by quantitative characterization of oscillatory activity in murine spinal cord networks on microelectrode arrays. European Journal of Neuroscience 2004, 19:2815-2825.
16. Guengerich F.P. Mechanisms of drug toxicity and relevance to pharmaceutical development. Drug Metabolism and Pharmacokinetics 2011, 26:3-14.
17. Guo L., Abrams R.M., Babiarz J.E., Cohen J.D., Kameoka S., Sanders M.J., Chiao E., Kolaja K.L. Estimating the risk of drug-induced proarrhythmia using human induced pluripotent stem cell-derived cardiomyocytes. Toxicological Sciences 2011, 123:281-289.
18. Hansen D.V., Rubenstein J.L., Kriegstein A.R. Deriving excitatory neurons of the neocortex from pluripotent stem cells. Neuron 2011, 70:645-660.
19. Harmer A.R., Abi-Gerges N., Morton M.J., Pullen G.F., Valentin J.P., Pollard C.E. Validation of an in vitro contractility assay using canine ventricular myocytes. Toxicology and Applied Pharmacology 2012, 260:162-172.
20. Harrill J.A., Robinette B.L., Mundy W.R. Use of high content image analysis to detect chemical-induced changes in synaptogenesis in vitro. Toxicology In Vitro 2011, 25:368-387.
21. Haythornthwaite A., Stoelzle S., Hasler A., Kiss A., Mosbacher J., George M., Bruggemann A., Fertig N. Characterizing human ion channels in induced pluripotent stem cell-derived neurons. Journal of Biomolecular Screening 2012, 17:1264-1272.
22. Hazeltine L.B., Simmons C.S., Salick M.R., Lian X., Badur M.G., Han W., Delgado S.M., Wakatsuki T., Crone W.C., Pruitt B.L., Palecek S.P. Effects of substrate mechanics on contractility of cardiomyocytes generated from human pluripotent stem cells. International Journal of Cell Biology 2012, 10.1155/2012/508294.
23. Heikkila T.J., Yla-Outinen L., Tanskanen J.M., Lappalainen R.S., Skottman H., Suuronen R., Mikkonen J.E., Hyttinen J.A., Narkilahti S. Human embryonic stem cell-derived neuronal cells form spontaneously active neuronal networks in vitro. Experimental Neurology 2009, 218:109-116.
24. Hu B.Y., Weick J.P., Yu J., Ma L.X., Zhang X.Q., Thomson J.A., Zhang S.C. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:4335-4340.
25. Illes S., Fleischer W., Siebler M., Hartung H.P., Dihne M. Development and pharmacological modulation of embryonic stem cell-derived neuronal network activity. Experimental Neurology 2007, 207:171-176.
26. Israel M.A., Yuan S.H., Bardy C., Reyna S.M., Mu Y., Herrera C., Hefferan M.P., Van Gorp S., Nazor K.L., Boscolo F.S., Carson C.T., Laurent L.C., Marsala M., Gage F.H., Remes A.M., Koo E.H., Goldstein L.S. Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 2012, 482:216-220.
27. Johnstone A.F., Gross G.W., Weiss D.G., Schroeder O.H., Gramowski A., Shafer T.J. Microelectrode arrays: a physiologically based neurotoxicity testing platform for the 21st century. Neurotoxicology 2010, 31:331-350.
28. Jozefczuk J., Prigione A., Chavez L., Adjaye J. Comparative analysis of human embryonic stem cell and induced pluripotent stem cell-derived hepatocyte-like cells reveals current drawbacks and possible strategies for improved differentiation. Stem Cells and Development 2011, 20:1259-1275.
29. Kang S.J., Jeong S.H., Kim E.J., Cho J.H., Park Y.I., Park S.W., Shin H.S., Son S.W., Kang H.G. 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 Biology and Toxicology 2013, 29:1-11.
30. Kaplowitz N. Biochemical and cellular mechanisms of toxic liver injury Semin. Liver Disease 2002, 22:137-144.
31. Kenakin T. Differences between natural and recombinant G protein-coupled receptor systems with varying receptor/G protein stoichiometry. Trends in Pharmacological Sciences 1997, 18:456-464.
32. Khanna I. Drug discovery in pharmaceutical industry: productivity challenges and trends. Drug Discovery Today 2012, 17:1088-1102.
33. Khetani S.R., Bhatia S.N. Microscale culture of human liver cells for drug development. Nature Biotechnology 2008, 26:120-126.
34. Kia, R., Sison, R.L., Heslop, J., Kitteringham, N.R., Hanley, N., Mills, J.S., Park, B.K., Goldring, C.E. Stem cell-derived hepatocytes as a predictive model for drug-induced liver injury: are we there yet? British Journal of Clinical Pharmacology, in press.
35. Kola I., Landis J. Can the pharmaceutical industry reduce attrition rates?. Nature Reviews Drug Discovery 2004, 3:711-715.
36. Kulkarni J.S., Khanna A. Functional hepatocyte-like cells derived from mouse embryonic stem cells: a novel in vitro hepatotoxicity model for drug screening. Toxicology In Vitro 2006, 20:1014-1022.
37. Kumar K.K., Aboud A.A., Bowman A.B. The potential of induced pluripotent stem cells as a translational model for neurotoxicological risk. Neurotoxicology 2012, 33:518-529.
38. Larsen J.W., Greendale K. ACOG technical bulletin number 84 - February 1985: teratology. Teratology 1985, 32:493-496.
39. Laverty H., Benson C., Cartwright E., Cross M., Garland C., Hammond T., Holloway C., McMahon N., Milligan J., Park B., Pirmohamed M., Pollard C., Radford J., Roome N., Sager P., Singh S., Suter T., Suter W., Trafford A., Volders P., Wallis R., Weaver R., York M., Valentin J. How can we improve our understanding of cardiovascular safety liabilities to develop safer medicines?. British Journal de Pharmacologie 2011, 163:675-693.
40. LeCluyse E.L., Witek R.P., Andersen M.E., Powers M.J. Organotypic liver culture models: meeting current challenges in toxicity testing. Critical Reviews in Toxicology 2012, 42:501-548.
41. Lee W.M., Senior J.R. Recognizing drug-induced liver injury: current problems, possible solutions. Toxciology and Pathology 2005, 33:155-164.
42. Lee W.M. Drug-induced hepatotoxicity. The New England Journal of Medicine 2003, 349:474-485.
43. Lieu D.K., Liu J., Siu C.W., McNerney G.P., Tse H.F., Abu-Khalil A., Huser T., Li R.A. Absence of transverse tubules contributes to non-uniform Ca(2+) wavefronts in mouse and human embryonic stem cell-derived cardiomyocytes. Stem Cells Development 2009, 18:1493-1500.
44. Lin Z., Will Y. Evaluation of drugs with specific organ toxicities in organ-specific cell lines. Toxicological Sciences 2012, 126:114-127.
45. Lunn J.S., Sakowski S.A., Hur J., Feldman E.L. Stem cell technology for neurodegenerative diseases. Annals of Neurology 2011, 70:353-361.
46. Ma J., Guo L., Fiene S.J., Anson B.D., Thomson J.A., Kamp T.J., Kolaja K.L., Swanson B.J., January C.T. High purity human-induced pluripotent stem cell-derived cardiomyocytes: electrophysiological properteis of action potentials and ionic currents. American Journal of Physiology. Heart and Circulatory Physiology 2011, 301:H2006-H2017.
47. Magalhaes A.C., Dunn H., Ferguson S.S. Regulation of GPCR activity trafficking and localization by GPCR-interacting proteins. British Journal of Pharmacology 2012, 165:1717-1736.
48. McConnell E.R., McClain M.A., Ross J., Lefew W.R., Shafer T.J. Evaluation of multi-well microelectrode arrays for neurotoxicity screening using a chemical training set. Neurotoxicology 2012, 33:1048-1057.
49. 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 A.B., Passier R., Tertoolen L. Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 2003, 107:2733-2740.
50. Nagamoto Y., Tashiro K., Takayama K., Ohashi K., Kawabata K., Sakurai F., Tachibana M., Hayakawa T., Furue M.K., Mizuguchi H. The promotion of hepatic maturation of human pluripotent stem cells in 3D co-culture using type I collagen and Swiss 3T3 cell sheets. Biomaterials 2012, 33:4526-4534.
51. Nau H. Teratogenicity of isotretinoin revisited: species variation and the role of all-trans-retinoic acid. Journal of the American Academy of Dermatology 2001, 45:S183-S187.
52. Novellino A., Scelfo B., Palosaari T., Price A., Sobanski T., Shafer T.J., Johnstone A.F., Gross G.W., Gramowski A., Schroeder O., Jugelt K., Chiappalone M., Benfenati F., Martinoia S., Tedesco M.T., Defranchi E., D'Angelo P., Whelan M. Development of micro-electrode array based tests for neurotoxicity: assessment of interlaboratory reproducibility with neuroactive chemicals. Frontiers in Neuroengineering 2011, 4:1-14.
53. O'Brien P.J., Irwin W., Diaz D., Howard-Cofield E., Krejsa C.M., Slaughter M.R., Gao B., Kaludercic N., Angeline A., Bernardi P., Brain P., Hougham C. High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Archives of Toxicology 2006, 80:580-604.
54. Olson H., Betton G., Robinson D., Thomas K., Monro A., Kolaja G., Lilly P., Sanders J., Sipes G., Bracken W., Dorato M., Van Deun K., Smith P., Berger B., Heller A. Concordance of the toxicity of pharmaceuticals in humans and in animals. Regulatory Toxicology and Pharmacology 2000, 32:56-67.
55. Peters M.F., Scott C.W., Ochalski R., Dragan Y.P. Evaluation of cellular impedance measures of cardiomyocyte cultures for drug screening applications. Assay and Drug Development Technologies 2012, 10:525-532.
56. Pointon A., Abi-Gerges N., Cross M.J., Sidaway J.E. Phenotypic profiling of structural cardiotoxins in vitro reveals dependency on multiple mechanisms of toxicity. Toxicological Sciences 2013, 10.1093/toxsci/kft005.
57. Prot J.M., Leclerc E. The current status of alternatives to animal testing and predictive toxicology methods using liver microfluidic biochips. Annals of Biomedical Engineering 2012, 40:1228-1243.
58. Qiang L., Fujita R., Yamashita T., Angulo S., Rhinn H., Rhee D., Doege C., Chau L., Aubry L., Vanti W.B., Moreno H., Abeliovich A. Directed conversion of Alzheimer's disease patient skin fibroblasts into functional neurons. Cell 2011, 146:359-371.
59. Radio N.M., Freudenrich T.M., Robinette B.L., Crofton K.M., Mundy W.R. Comparison of PC12 and cerebellar granule cell cultures for evaluating neurite outgrowth using high content analysis. Neurotoxicology and Teratology 2010, 32:25-35.
60. Rana P., Anson B., Engle S., Will Y. Characterization of human-induced pluripotent stem cell-derived cardiomyocytes: bioenergetics and utilization in safety screening. Toxicological Sciences 2012, 130:117-131.
61. Rashid S.T., Corbineau S., Hannan N., Marciniak S.J., Miranda E., Alexander G., Huang-Doran I., Griffin J., Ahrlund-Richter L., Skepper J., Semple R., Weber A., Lomas D.A., Vallier L. Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. Journal of Clinical Investigation 2010, 120:3127-3136.
62. Schuster D., Laggner C., Langer T. Why drugs fail - a study on side effects in new chemical entities. Current Pharmaceutical Design 2005, 11:3545-3559.
63. Scott C.W., Peters M.F. Label-free whole-cell assays: expanding the scope of GPCR screening. Drug Discovery Today 2010, 15:704-716.
64. Shah R.R. Can pharmacogenetics help rescue drugs withdrawn from the market?. Pharmacogenomics 2006, 7:889-908.
65. Sibille M., Deigat N., Janin A., Kirkesseli S., Durand D.V. Adverse events in phase-I studies: a report in 1015 healthy volunteers. European Journal of Clinical Pharmacology 1998, 54:13-20.
66. Sirenko O., Crittenden C., Callamaras N., Hesley J., Chen Y.W., Funes C., Rusyn I., Anson B., Cromwell E.F. Multiparameter in vitro assessment of compound effects on cardiomyocyte physiology using iPSC Cells. Journal of Biomolecular Screening 2012, 18:39-53.
67. Son E.Y., Ichida J.K., Wainger B.J., Toma J.S., Rafuse V.F., Woolf C.J., Eggan K. Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 2011, 9:205-218.
68. Spielmann H., Pohl I., Doring B., Liebsch M., Moldenhauer F. The embryonic stem cell test (EST) an in vitro embryotoxicity test using two permanent mouse cell lines: 3T3 fibroblasts and embryonic stem cells. In Vitro & Molecular Toxicology - A Journal of Basic and Applied Research 1997, 10:119-127.
69. Stiegler N.V., Krug A.K., Matt F., Leist M. Assessment of chemical-induced impairment of human neurite outgrowth by multiparametric live cell imaging in high-density cultures. Toxicological Sciences 2011, 121:73-87.
70. Stoelzle S., Obergrussberger A., Bruggemann A., Haarmann C., George M., Kettenhofen R., Fertig N. State-of-the-art automated patch clamp devices heat activation, action potentials, and high throughput in ion channel screening front. Pharmacology 2011, 17:1965-1975.
71. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
72. Takayama K., Kawabata K., Nagamoto Y., Kishimoto K., Tashiro K., Sakurai F., Tachibana M., Kanda K., Hayakawa T., Furue M.K., Mizuguchi H. 3D spheroid culture of hESC/hiPSC-derived hepatocyte-like cells for drug toxicity testing. Biomaterials 2013, 34:1781-1789.
73. Theunissen P.T., Piersma A.H. Innovative approaches in the embryonic stem cell test (EST). Frontiers in Bioscience: A Journal and Virtual Library 2012, 17:1965-1975.
74. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., Jones J.M. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
75. Tulloch N.L., Muskheli V., Razumova M.V., Korte F.S., Regnier M., Hauch K.D., Pabon L., Reinecke H., Murry C.E. Growth of engineered human myocardium with mechanical loading and vascular coculture. Circulation Research 2011, 109:47-59.
76. Vojnits K., Bremer S. Challenges of using pluripotent stem cells for safety assessments of substances. Toxicology 2010, 270:10-17.
77. Wensing G., Ighrayeb I.A., Boix O., Bottcher M. The safety of healthy volunteers in First-in-Man trials - an analysis of studies conducted at the Bayer in-house ward from 2000 to 2005. International Journal of Clinical Pharmacology and Therapeutics 2010, 48:563-570.
78. Xu J.J., Henstock P.V., Dunn M.C., Smith A.R., Chabot J.R., de Graaf D. Cellular imaging predictions of clinical drug-induced liver injury. Toxicological Sciences 2008, 105:97-105.
79. 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., Thomson J.A. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.