Embryonic stem cell-based screen for small molecules: Cluster analysis reveals four response patterns in developing neural cells

Current Medicinal Chemistry

Volumn 20, Issue 5, 2013, Pages 710-723

  Kern, I ^a   Xu, R ^b,c   Julien, S ^c   Suter, D M ^d   Preynat Seauve, O ^a   Baquie M ^e   Poncet, A ^f   Combescure, C ^f   Stoppini, L ^g   Thriel, C V ^h   Krause, Karl Heinz ^a,c  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b Enkam Pharmaceuticals AS   (Denmark)

^c UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^d HARVARD UNIVERSITY   (United States)

^e NEURIX SA   (Switzerland)

^f UNIVERSITY OF GENEVA   (Switzerland)

^g UNIVERSITY OF APPLIED SCIENCES WESTERN SWITZERLAND   (Switzerland)

^h LEIBNIZ RESEARCH CENTRE FOR WORKING ENVIRONMENT AND HUMAN FACTORS   (Germany)

Author keywords

Developmental toxicity; Embryonic stem cells; ESC; In vitro screening; Neural differentiation; Neurotoxicology

Indexed keywords

ACIVICIN; ACLARUBICIN; ACRIFLAVINE; ACRISORCIN; ALBENDAZOLE; ALEXIDINE; ALPHA TUBULIN; AMFEBUTAMONE; AMINOACRIDINE; AMIODARONE; ANCITABINE; ANISOMYCIN; ASTEMIZOLE; BENFLUOREX; BENZALKONIUM; BENZETHONIUM CHLORIDE; BEPRIDIL; BERBERINE; CAMPTOTHECIN; CYTOSTATIC AGENT; ELONGATION FACTOR 1ALPHA; ELONGATION FACTOR 1ALPHA 1; ENDOCRINE DISRUPTOR; FIREFLY LUCIFERASE; METHYLMERCURY; NEUROTOXIN; PSYCHOTROPIC AGENT; SULFONAMIDE; TUBULIN ALPHA 1A; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CLUSTER ANALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DRUG DETERMINATION; DRUG SCREENING; EMBRYONIC STEM CELL; ENZYME ACTIVITY; FIBROBLAST; GENE EXPRESSION; IC 50; IN VITRO STUDY; MOLECULE; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; REPORTER GENE; UBIQUITINATION;

EID: 84877941136     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986713804999330     Document Type: Article

References (59)

1. Miller, G., Is pharma running out of brainy ideas? Science, 2010, 329(5991), 502-504.
2. Drexler, B.; Hentschke, H.; Antkowiak, B.; Grasshoff, C., Organotypic cultures as tools for testing neuroactive drugs -link between in-vitro and invivo experiments. Curr. Med. Chem., 2010, 17(36), 4538-4550.
3. Grandjean, P.; Landrigan, P.J., Developmental neurotoxicity of industrial chemicals. Lancet, 2006, 368(9553), 2167-2178.
4. Ornoy, A., Neuroteratogens in man: an overview with special emphasis on the teratogenicity of antiepileptic drugs in pregnancy. Reprod. Toxicol., 2006, 22(2), 214-226.
5. OECD, Test guideline 426. OECD guideline for the testing of chemicals: Developmental Neurotoxicity Study. 2007.
6. United States Environmental Protection Agency. Health Effects Test Guidelines OPPTS 870.6300 Developmental Neurotoxicity Study. 1998
7. Bal-Price, A.K.; Sunol, C.; Weiss, D.G.; van Vliet, E.; Westerink, R.H.; Costa, L.G., Application of in vitro neurotoxicity testing for regulatory purposes: Symposium III summary and research needs. Neurotoxicology, 2008, 29(3), 520-531.
8. Coecke, S.; Goldberg, A.M.; Allen, S.; Buzanska, L.; Calamandrei, G.; Crofton, K.; Hareng, L.; Hartung, T.; Knaut, H.; Honegger, P.; Jacobs, M.; Lein, P.; Li, A.; Mundy, W.; Owen, D.; Schneider, S.; Silbergeld, E.; Reum, T.; Trnovec, T.; Monnet-Tschudi, F.; Bal-Price, A., Workgroup report: incorporating in vitro alternative methods for developmental neurotoxicity into international hazard and risk assessment strategies. Environ. Health. Perspect., 2007, 115(6), 924-931.
9. Pistollato, F.; Bremer-Hoffmann, S.; Healy, L.; Young, L.; Stacey, G., Standardization of pluripotent stem cell cultures for toxicity testing. Expert Opin. Drug Metab. Toxicol., 2012, 8(2), 239-257.
10. Kuegler, P.B.; Zimmer, B.; Waldmann, T.; Baudis, B.; Ilmjarv, S.; Hescheler, J.; Gaughwin, P.; Brundin, P.; Mundy, W.; Bal-Price, A.K.; Schrattenholz, A.; Krause, K.H.; van Thriel, C.; Rao, M.S.; Kadereit, S.; Leist, M., Markers of murine embryonic and neural stem cells, neurons and astrocytes: reference points for developmental neurotoxicity testing. Altex, 2011, 27(1), 17-42.
11. Breier, J.M.; Gassmann, K.; Kayser, R.; Stegeman, H.; De Groot, D.; Fritsche, E.; Shafer, T.J., Neural progenitor cells as models for highthroughput screens of developmental neurotoxicity: state of the science. Neurotoxicol. Teratol., 2010, 32(1), 4-15.
12. Hogberg, H.T.; Kinsner-Ovaskainen, A.; Coecke, S.; Hartung, T.; Bal-Price, A.K., mRNA expression is a relevant tool to identify developmental neurotoxicants using an in vitro approach. Toxicol. Sci., 2010, 113(1), 95-115.
13. Bal-Price, A.K.; Hogberg, H.T.; Buzanska, L.; Lenas, P.; van Vliet, E.; Hartung, T., In vitro developmental neurotoxicity (DNT) testing: relevant models and endpoints. Neurotoxicology, 2010, 31(5), 545-554.
14. Buzanska, L.; Sypecka, J.; Nerini-Molteni, S.; Compagnoni, A.; Hogberg, H.T.; del Torchio, R.; Domanska-Janik, K.; Zimmer, J.; Coecke, S., A human stem cell-based model for identifying adverse effects of organic and inorganic chemicals on the developing nervous system. Stem cells, 2009, 27(10), 2591-2601.
15. Tamm, C.; Duckworth, J.; Hermanson, O.; Ceccatelli, S., High susceptibility of neural stem cells to methylmercury toxicity: effects on cell survival and neuronal differentiation. J. Neurochem., 2006, 97(1), 69-78.
16. Clothier, R.; Dierickx, P.; Lakhanisky, T.; Fabre, M.; Betanzos, M.; Curren, R.; Sjostrom, M.; Raabe, H.; Bourne, N.; Hernandez, V.; Mainez, J.; Owen, M.; Watts, S.; Anthonissen, R., A database of IC50 values and principal component analysis of results from six basal cytotoxicity assays, for use in the modelling of the in vivo and in vitro data of the EU ACuteTox project. Altern. Lab. Anim., 2008, 36(5), 503-519.
17. Zimmer, B.; Kuegler, P.B.; Baudis, B.; Genewsky, A.; Tanavde, V.; Koh, W.; Tan, B.; Waldmann, T.; Kadereit, S.; Leist, M., Coordinated waves of gene expression during neuronal differentiation of embryonic stem cells as basis for novel approaches to developmental neurotoxicity testing. Cell Death Differ., 2011, 18(3), 383-395.
18. Theunissen, P.T.; Pennings, J.L.; Robinson, J.F.; Claessen, S.M.; Kleinjans, J.C.; Piersma, A.H., Time-response evaluation by transcriptomics of methylmercury effects on neural differentiation of murine embryonic stem cells. Toxicol. Sci., 2011, 122(2), 437-447.
19. Harrill, J.A.; Freudenrich, T.M.; Machacek, D.W.; Stice, S.L.; Mundy, W.R., Quantitative assessment of neurite outgrowth in human embryonic stem cellderived hN2 cells using automated high-content image analysis. Neurotoxicology, 2010, 31(3), 277-290.
20. Forsby, A.; Bal-Price, A.K.; Camins, A.; Coecke, S.; Fabre, N.; Gustafsson, H.; Honegger, P.; Kinsner-Ovaskainen, A.; Pallas, M.; Rimbau, V.; Rodriguez-Farre, E.; Sunol, C.; Vericat, J.A.; Zurich, M.G., Neuronal in vitro models for the estimation of acute systemic toxicity. Toxicol. In Vitro, 2009, 23(8), 1564-1569.
21. Sunol, C.; Babot, Z.; Fonfria, E.; Galofre, M.; Garcia, D.; Herrera, N.; Iraola, S.; Vendrell, I., Studies with neuronal cells: From basic studies of mechanisms of neurotoxicity to the prediction of chemical toxicity. Toxicol. In Vitro, 2008, 22(5), 1350-1355.
22. Zimmer, B.; Lee, G.; Balmer, N.V.; Meganathan, K.; Sachinidis, A.; Studer, L.; Leist, M., Evaluation of developmental toxicants and signaling pathways in a functional test based on the migration of human neural crest cells. Environ. Health Perspect., 2012, 120(8), 1116-1122.
23. Dubois-Dauphin, M.L.; Toni, N.; Julien, S.D.; Charvet, I.; Sundstrom, L.E.; Stoppini, L., The long-term survival of in vitro engineered nervous tissue derived from the specific neural differentiation of mouse embryonic stem cells. Biomaterials, 2010, 31(27), 7032-7042.
24. Suter, D.M.; Preynat-Seauve, O.; Tirefort, D.; Feki, A.; Krause, K.H., Phenazopyridine induces and synchronizes neuronal differentiation of embryonic stem cells. J. Cell. Mol. Med., 2009, 13(2), 1-11.
25. Newland, M.C.; Donlin, W.D.; Paletz, E.M.; Banna, K.M. In Animal Models of Cognitive Impairment. Levin ED, B.J., Ed.; CRC Press: Boca Raton (FL), 2006; chapter 7.
26. Robinson, J.F.; Theunissen, P.T.; van Dartel, D.A.; Pennings, J.L.; Faustman, E.M.; Piersma, A.H., Comparison of MeHg-induced toxicogenomic responses across in vivo and in vitro models used in developmental toxicology. Reprod. Toxicol., 2011, 32(2), 180-188.
27. Suter, D.M.; Cartier, L.; Bettiol, E.; Tirefort, D.; Jaconi, M.E.; Dubois-Dauphin, M.; Krause, K.H., Rapid generation of stable transgenic embryonic stem cell lines using modular lentivectors. Stem cells, 2006, 24(3), 615-623.
28. Barberi, T.; Klivenyi, P.; Calingasan, N.Y.; Lee, H.; Kawamata, H.; Loonam, K.; Perrier, A.L.; Bruses, J.; Rubio, M.E.; Topf, N.; Tabar, V.; Harrison, N.L.; Beal, M.F.; Moore, M.A.; Studer, L., Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol., 2003, 21(10), 1200-1207.
29. Sebaugh, J.L., Guidelines for accurate EC50/IC50 estimation. Pharm. Stat., 2011, 10(2), 128-134.
30. Mundy, W.; Padilla, S.; Shafer, T.J.; Gilbert, M.; Breier, J.M.; Cowden, J.; Crofton, K.; Herr, D.; Jensen, K.; Raffaele, K.; Radio, N.M.; Schumacher, K. Presented at Society of Toxicology, 48th Annual Meeting: Baltimore, 2009; available from: http://www.epa.gov/comptox/toxcast/files/summit/ 48P% 20 Mundy%20TDAS.pdf
31. Kompoliti, K.; Horn, S.S. In Textbook of clinical neurology, 3 ed. Goetz, C.G., Ed.; Saunders: Philadelphia, 2007; chapter 55.
32. Perrier, A.L.; Tabar, V.; Barberi, T.; Rubio, M.E.; Bruses, J.; Topf, N.; Harrison, N.L.; Studer, L., Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. U S A, 2004, 101(34), 12543-12548.
33. Haeckel, R.; Wosniok, W.; Kratochvila, J.; Carobene, A., A pragmatic proposal for permissible limits in external quality assessment schemes with a compromise between biological variation and the state of the art. Clinical chemistry and laboratory medicine : CCLM / FESCC, 2012, 50(5), 833-839.
34. Schulz, H.; Kolde, R.; Adler, P.; Aksoy, I.; Anastassiadis, K.; Bader, M.; Billon, N.; Boeuf, H.; Bourillot, P.Y.; Buchholz, F.; Dani, C.; Doss, M.X.; Forrester, L.; Gitton, M.; Henrique, D.; Hescheler, J.; Himmelbauer, H.; Hubner, N.; Karantzali, E.; Kretsovali, A.; Lubitz, S.; Pradier, L.; Rai, M.; Reimand, J.; Rolletschek, A.; Sachinidis, A.; Savatier, P.; Stewart, F.; Storm, M.P.; Trouillas, M.; Vilo, J.; Welham, M.J.; Winkler, J.; Wobus, A.M.; Hatzopoulos, A.K., The FunGenES database: a genomics resource for mouse embryonic stem cell differentiation. PLoS One, 2009, 4(9), e6804.
35. Ejiri, S., Moonlighting functions of polypeptide elongation factor 1: from actin bundling to zinc finger protein R1-Associated nuclear localization. Biosci. Biotechnol. Biochem., 2002, 66(1), 1-21.
36. Abbott, C.M.; Newbery, H.J.; Squires, C.E.; Brownstein, D.; Griffiths, L.A.; Soares, D.C., eEF1A2 and neuronal degeneration. Biochem. Soc. Trans., 2009, 37(Pt 6), 1293-1297.
37. Newbery, H.J.; Stancheva, I.; Zimmerman, L.B.; Abbott, C.M., Evolutionary importance of translation elongation factor eEF1A variant switching: eEF1A1 down-regulation in muscle is conserved in Xenopus but is controlled at a post-transcriptional level. Biochem. Biophys. Res. Commun., 2011, 411(1), 19-24.
38. Stummann, T.C.; Hareng, L.; Bremer, S., Embryotoxicity hazard assessment of methylmercury and chromium using embryonic stem cells. Toxicology, 2007, 242(1-3), 130-143.
39. Genschow, E.; Spielmann, H.; Scholz, G.; Pohl, I.; Seiler, A.; Clemann, N.; Bremer, S.; Becker, K., Validation of the embryonic stem cell test in the international ECVAM validation study on three in vitro embryotoxicity tests. Altern. Lab. Anim., 2004, 32(3), 209-244.
40. Baek, D.H.; Kim, T.G.; Lim, H.K.; Kang, J.W.; Seong, S.K.; Choi, S.E.; Lim, S.Y.; Park, S.H.; Nam, B.H.; Kim, E.H.; Kim, M.S.; Park, K.L., Embryotoxicity assessment of developmental neurotoxicants using a neuronal endpoint in the embryonic stem cell test. J. Appl. Toxicol., 2011.
41. He, X.; Imanishi, S.; Sone, H.; Nagano, R.; Qin, X.Y.; Yoshinaga, J.; Akanuma, H.; Yamane, J.; Fujibuchi, W.; Ohsako, S., Effects of methylmercury exposure on neuronal differentiation of mouse and human embryonic stem cells. Toxicol. Lett., 2012, 212(1), 1-10.
42. Chen, Z.; Pradhan, S.; Liu, C.; Le, L.Q., Skin-derived Precursors as a Source of Progenitors for Cutaneous Nerve Regeneration. Stem cells, 2012, 30(10), 2261-2270.
43. Masuo, Y.; Ishido, M., Neurotoxicity of endocrine disruptors: possible involvement in brain development and neurodegeneration. J. Toxicol. Environ. Health B. Crit. Rev., 2011, 14(5-7), 346-369.
44. Ara, C.; Asmatullah, Teratogenic and Embryotoxic Effects of Clomiphene Citrate in Developing Mice. Asian-Ast. J. Anim. Sci., 2011, 24(8), 1053-1059.
45. Filosto, M.; Tentorio, M.; Broglio, L.; Buzio, S.; Lazzarini, C.; Pasolini, M.P.; Cotelli, M.S.; Scarpelli, M.; Mancuso, M.; Choub, A.; Padovani, A., Disulfiram neuropathy: two cases of distal axonopathy. Clin. Toxicol., 2008, 46(4), 314-316.
46. Wachter, T.; Rohrich, S.; Frank, A.; Molina-Luna, K.; Pekanovic, A.; Hertler, B.; Schubring-Giese, M.; Luft, A.R., Motor skill learning depends on protein synthesis in the dorsal striatum after training. Exp. Brain Res., 2010, 200(3-4), 319-323.
47. Nzila, A.; Ward, S.A.; Marsh, K.; Sims, P.F.; Hyde, J.E., Comparative folate metabolism in humans and malaria parasites (part I): pointers for malaria treatment from cancer chemotherapy. Trends Parasitol., 2005, 21(6), 292-298.
48. Goncalves, J.; Malta-Vacas, J.; Louis, M.; Brault, L.; Bagrel, D.; Monteiro, C.; Brito, M., Modulation of translation factor's gene expression by histone deacetylase inhibitors in breast cancer cells. Clin. Chem. Lab. Med., 2005, 43(2), 151-156.
49. Rada-Iglesias, A.; Enroth, S.; Ameur, A.; Koch, C.M.; Clelland, G.K.; Respuela-Alonso, P.; Wilcox, S.; Dovey, O.M.; Ellis, P.D.; Langford, C.F.; Dunham, I.; Komorowski, J.; Wadelius, C., Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res., 2007, 17(6), 708-719.
50. Sahay, A.; Hen, R., Adult hippocampal neurogenesis in depression. Nat. Neurosci., 2007, 10(9), 1110-1115.
51. Fajolu, I.B.; Lesi, F.E.A., Drug-induced acute dystonia in a 7 year old child following the use of artesunate-Amodiquine: A case report. Int. J. Risk Saf. Med., 2010, 22(111-114.
52. Wittes, R., Neuromyopathy associated with amodiaquine hydrochloride. C.M.A.J., 1987, 137(7), 635-636.
53. Tagbor, H.K.; Chandramohan, D.; Greenwood, B., The safety of amodiaquine use in pregnant women. Expert Opin. Drug Saf., 2007, 6(6), 631-635.
54. Chakraborty, S.; Shukla, D.; Mishra, B.; Singh, S., Clinical updates on carvedilol: a first choice beta-blocker in the treatment of cardiovascular diseases. Expert Opin. Drug Metab. Toxicol., 2010, 6(2), 237-250.
55. Kumar, A.; Dogra, S., Neuro protective effect of carvedilol, an adrenergic antagonist against colchicine induced cognitive impairment and oxidative damage in rat. Pharmacol. Biochem. Behav., 2009, 92(1), 25-31.
56. Krause, R.M.; Buisson, B.; Bertrand, S.; Corringer, P.J.; Galzi, J.L.; Changeux, J.P.; Bertrand, D., Ivermectin: a positive allosteric effector of the alpha7 neuronal nicotinic acetylcholine receptor. Mol. Pharmacol., 1998, 53(2), 283-294.
57. Hopper, K.; Aldrich, J.; Haskins, S.C., Ivermectin toxicity in 17 collies. J. Vet. Intern. Med., 2002, 16(1), 89-94.
58. Macdonald, N.; Gledhill, A., Potential impact of ABCB1 (p-glycoprotein) polymorphisms on avermectin toxicity in humans. Arch. Toxicol., 2007, 81(8), 553-563.
59. Kadereit, S.; Zimmer, B.; van Thriel, C.; Hengstler, J.G.; Leist, M., Compound selection for in vitro modeling of developmental neurotoxicity. Front. Biosci., 2012, 17(2442-2460.