Sensitivity of neuroprogenitor cells to chemical-induced apoptosis using a multiplexed assay suitable for high-throughput screening

Toxicology

Volumn 333, Issue , 2015, Pages 14-24

  Druwe, Ingrid ^a,b,c   Freudenrich, Theresa M ^b   Wallace, Kathleen ^b   Shafer, Timothy J ^b   Mundy, William R ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Apoptosis; Developmental neurotoxicity; High throughput screening; In vitro models; Neuroprogenitor cells

Indexed keywords

AMOXICILLIN; ARSENIC TRIOXIDE; CASPASE 3; CASPASE 7; CHEMICAL AGENT; CHLORPYRIFOS; DEXAMETHASONE; GLYPHOSATE; KETAMINE; LAMININ; MANGANESE; METHYLMERCURY; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; PARACETAMOL; POLYORNITHINE; STAUROSPORINE; TRIBUTYLTIN; TRIMETHYLTIN; CASP3 PROTEIN, HUMAN; CASP3 PROTEIN, MOUSE; CASP7 PROTEIN, HUMAN; CASP7 PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; EMBRYO; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROTOXICITY; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL CULTURE; ANIMAL; C57BL MOUSE; CELL LINE; CELL SURVIVAL; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PROCEDURES; RISK ASSESSMENT; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TOXICITY TESTING;

RODENTIA;

ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 7; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; RISK ASSESSMENT; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TOXICITY TESTS;

EID: 84927722477     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2015.03.011     Document Type: Article

References (46)

1. Akhtar R.S., Ness J.M., Roth K.A. Bcl-2 family regulation of neuronal development and neurodegeneration. Biochim. Biophys. Acta 2004, 1644:189-203.
2. Akhtar R.S., Geng Y., Klocke B.J., Roth K.A. Neural precursor cells possess multiple p53-dependent apoptotic pathways. Cell Death Differ. 2006, 13:1727-1739.
3. Alenzi F.Q.B. Links between apoptosis, proliferation and the cell cycle. Br. J. Biomed. Sci. 2004, 61:1-4.
4. Bai X., Yan Y., Canfield S., Muravyeva M.Y., Kikuchi C., Zaja I., Corbett J.A., Bosnjak Z.J. Ketamine enhances human neural stem cell proliferation and induces neuronal apoptosis via reactive oxygen species-mediated mitochondrial pathway. Anesth. Analg. 2013, 116:869-880.
5. Bal-Price A.K., Coecke S., Costa L., et al. Advancing the science of developmental neurotoxicity (DNT): testing for better safety evaluation. ALTEX 2012, 29:202-215.
6. Ceccatelli S., Tamm C., Sleeper E., Orrenius S. Neural stem cells and cell death. Toxicol. Lett. 2004, 149:59-66.
7. Coecke S., Goldberg A.M., Allen S., et al. Workgroup report: incorporating in vitro alternative methods for developmental neurotoxicity into international hazard and risk assessment strategies. Environ. Health Perspect. 2007, 115:924-931.
8. Conti L., Cattaneo E. Neural stem cell systems: physiological players or in vitro entities?. Nat. Rev. 2010, 11:176-187.
9. Crofton K.M., Mundy W.R., Lein P.J., Bal-Price A., et al. Developmental neurotoxicity testing: recommendations for developing alternative methods for the screening and prioritization of chemicals. ALTEX 2011, 28:9-15.
10. Crouch A., Kozlowski R., Slater K., et al. The use of ATP bioluminescence as a measure of proliferation and cytotoxicity. J. Immunol. Methods 1993, 160:81-88.
11. Culbreth M.E., Harrill J.A., Freudenrich T.M., Mundy W.R., Shafer T.J. Comparison of chemical-induced changes in proliferation and apoptosis in human and mouse neuroprogenitor cells. Neurotoxicology 2012, 33:1499-1510.
12. Dash A., Blackman B.R., Wamhoff B.R. Organotypic systems in drug metabolism and toxicity: challenges and opportunities. Expert Opin. Drug Metab. Toxicol. 2012, 8:999-1014.
13. De Groot M.W., Westerink R.H., Dingemans M.M. Do not judge a neuron only by its cover: neuronal function in in vitro developmental neurotoxicity testing. Toxicol. Sci. 2013, 132:1-7.
14. De Zio D., Giunta L., Covaro M., Ferraro E., Cecconi F. Expanding roles of programmed cell death in mammalian neurodevelopment. Semin. Cell Dev. Biol. 2005, 16:281-294.
15. Earnshaw W.C., Martins L.M., Kaufmann S.H. Mammalian caspases: structure activation substrates, and functions during apoptosis. Annu. Rev. Biochem. 1999, 68:383-424.
16. Gassmann K., Abel J., Bothe H., Haarmann-Stemmann T., Merk H.F., Quasthoff K.N., Rockel T.D., Schreiber T., Fritsche E. Species-specific differential AhR expression protects human neural progenitor cells against developmental neurotoxicity of PAHs. Environ. Health Perspect. 2010, 118:1571-1577.
17. Geng Y., Walls K.C., Ghosh A.P., Akhtar R.S., Klocke B.J., Roth K.A. Cytoplasmic p53 and activated bax regulate p53-dependent, transcription-independent neural precursor cell apoptosis. J. Histochem. Cytochem. 2010, 58:265-275.
18. Grandjean P., Landrigan P.J. Neurobehavioural effects of developmental neurotoxicity. Lancet Neurol. 2014, 13:330-338.
19. Harrill J.A., Robinette B.L., Mundy W.R. Use of high content image analysis to detect chemical-induced changes in synaptogenesis. Toxicol. In Vitro 2011, 25:368-387.
20. Judson R., Richard A., Dix D.J., Houck K., Kavlock R., Dellarco V., Holderman T., Sayre P., Carpenter T., Smith E. The toxicity data landscape for environmental chemicals. Environ. Health Perspect. 2009, 117:685-695.
21. Kavlock R., Chandler K., Houck K., Hunter S., Judson R., Kleinstreuer N., Knudsen T., Martin M., Padilla S., Reif D., Richard A., Rotroff D., Sipes N., Dix D. Update on EPA's ToxCast program: providing high throughput decision support tools for chemical risk management. Chem. Res. Toxicol. 2012, 25:1287-1302.
22. Köhler C., Orrenius S., Zhivotovsky B. Evaluation of caspase activity in apoptotic cells. J. Immunol. Methods 2002, 265:97-110.
23. Lein P., Locke P., Goldberg A. Meeting report: alternatives for developmental neurotoxicity testing. Environ. Health Perspect. 2007, 115:764-768.
24. Malo N., Hanley J.A., Cerquozzi S., Pelletier J., Nadon R. Statistical practice in high-throughput screening data analysis. Nat. Biotechnol. 2006, 24:167-175.
25. Matsumura I., Tanaka H., Kanakura Y. E2F1 and c-Myc in cell growth and death. Cell Cycle 2003, 2:333-338.
26. Meletis K., Wirta V., Hede S.M., Nistr M., Lundeberg J., Frisen J. p53 suppresses the self-renewal of adult neural stem cells. Development 2006, 133:363-369.
27. NRC Toxicity Testing in the 21st Century: a Vision and a Strategy 2007, National Academies Press, Washington, D.C.
28. Prochazkova J., Kylarova D., Vranka P., Lichnovsky V. Comparative study of apoptosis-detecting techniques: TUNEL, apostain, and lamin B. BioTechniques 2003, 35:528-534.
29. Radio N.M., Mundy W.R. Developmental neurotoxicity testing in vitro: models for assessing chemical effects on neurite outgrowth. Neurotoxicology 2008, 29:361-376.
30. Rice D., Barone S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 2000, 108(Suppl 3):511-533.
31. Schwartz P.H., Nethercott H., Kirov I.I., Ziaeian B., Young M.J., Klassen H. Expression of neurodevelopmental markers by cultured porcine neural precursor cells. Stem Cells 2005, 23:1286-1294.
32. Siegal S., Castellan N.J. Nonparametric Statistics for the Behavioral Sciences 1988, McGraw Hill, New York. 2nd ed.
33. Sidhu J.S., Ponce R.A., Vredevoogd M.A., Yu X., Gribble E., Hong S.-W., Schneider E., Faustman E.M. Cell cycle inhibition by sodium arsenite in primary embryonic rat midbrin neuroepithelial cells. Toxicol. Sci. 2006, 89:475-484.
34. Suzuki J.S., Ishido M. Transcriptome of tributyltin-induced apoptosis of the cultured rat mesencephalic neural stem cells. Toxicology 2011, 287:61-68.
35. 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, 97:69-78.
36. Tamm C., Sabri F., Ceccatelli S. Mitochondrial-mediated apoptosis in neural stem cells exposed to manganese. Toxicol. Sci. 2008, 101:310-320.
37. Thomaidou D., Mione M.C., Cavanagh J.F.R., Parnavelas J.G. Apoptosis and its relation to the cell cycle in the developing cerebral cortex. J. Neurosci. 1997, 17:1075-1085.
38. Thompson E.B. The many roles of c-Myc in apoptosis. Annu. Rev. Physiol. 1998, 60:575-600.
39. Vousdan K.H., Lu X. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2002, 2:594-604.
40. Walter J., Dihné M. Species-dependent differences of embryonic stem cell-derived neural stem cells after interferon gamma treatment. Front. Cell. Neurosci. 2012, 6:52.
41. Wang L., Ohishi T., Shiraki A., Morita R., Akane H., Ikarashi Y., Mitsumori K., Shibutani M. Developmental exposure to manganese chloride induces sustained aberration of neurogenesis in the hippocampal dentate gyrus of mice. Toxicol. Sci. 2012, 127:508-521.
42. Weil M., Jacobson M.D., Coles H.S.R., Davies T.J., Gardner R.L., Raff K.D., Raff M.C. Constitutive expression of the machinery for programmed cell death. J. Cell Biol. 1996, 133:1053-1059.
43. Woodruff T.J., Zota A.R., Schwartz J.M. Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ. Health Perspect. 2011, 119:878-885.
44. Xu X., Lei Y., Luo J., Wang J., Zhang S., Yang X.J., Sun M., Nuwaysir E., Fan G., Zhao J., Lei L., Zhong Z. Prevention of β-amyloid induced toxicity in human iPS cell-derived neurons by inhibition of cyclin-dependent kinases and associated cell cycle events. Stem Cell Res. 2013, 10:213-227.
45. Yoneyama M., Seko K., Kawada K., Sugiyama C., Ogita K. High susceptibility of cortical neural progenitor cells to trimethyltin toxicity: involvement of both caspases and calpain in cell death. Neurochem. Int. 2009, 55:257-264.
46. Yu S., Patchev A.V., Wu Y., Lu J., Holsboer F., Zhang J.Z., Sousa N., Almeida O.F.X. Depletion of the neural precursor cell poos by glucocorticoids. Ann. Neurol. 2010, 67:21-30.