High-Throughput Toxicity and Phenotypic Screening of 3D Human Neural Progenitor Cell Cultures on a Microarray Chip Platform

Stem Cell Reports

Volumn 7, Issue 5, 2016, Pages 970-982

  Nierode, Gregory J ^a   Perea, Brian C ^b   McFarland, Sean K ^c   Pascoal, Jorge F ^d   Clark, Douglas S ^b   Schaffer, David V ^b,c   Dordick, Jonathan S ^a  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of California   (United States)

^d Instituto de Biotecnologia e Bioengenharia Lisboa   (Portugal)

Author keywords

high content screening; high throughput microarray; human neural stem cells; neurotoxicity; screening; three dimensional cell culture

Indexed keywords

CADMIUM CHLORIDE; CYTARABINE; DIPHENHYDRAMINE; DOXORUBICIN; FLUOROURACIL; PARACETAMOL; PARAQUAT; PITAVASTATIN; RETINOIC ACID;

ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; IC50; MICROARRAY ANALYSIS; NEURAL STEM CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL CULTURE; CELL CULTURE TECHNIQUE; CELL SURVIVAL; CYTOLOGY; DNA MICROARRAY; DOSE RESPONSE; DRUG DEVELOPMENT; DRUG EFFECTS; GENETICS; METABOLISM; TOXICITY TESTING;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DISCOVERY; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; NEURAL STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; TOXICITY TESTS, ACUTE;

EID: 84994552896     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2016.10.001     Document Type: Article

References (52)

1. Akashi, T., Minami, J., Ishige, Y., Eishi, Y., Takizawa, T., Koike, M., Yanagishita, M., Basement membrane matrix modifies cytokine interactions between lung cancer cells and fibroblasts. Pathobiology 72 (2005), 250–259.
2. Bani-Yaghoub, M., Tremblay, R.G., Lei, J.X., Zhang, D., Zurakowski, B., Sandhu, J.K., Smith, B., Ribecco-Lutkiewicz, M., Kennedy, J., Walker, P.R., et al. Role of Sox2 in the development of the mouse neocortex. Dev. Biol. 295 (2006), 52–66.
3. Barcellos-Hoff, M.H., Aggeler, J., Ram, T.G., Bissell, M.J., Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105 (1989), 223–235.
4. Bhatia, S.N., Ingber, D.E., Microfluidic organs-on-chips. Nat. Biotechnol. 32 (2014), 760–772.
5. Bignami, A., Eng, L.F., Dahl, D., Uyeda, C.T., Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 43 (1972), 429–435.
6. Breier, J.M., Radio, N.M., Mundy, W.R., Shafer, T.J., Development of a high-throughput screening assay for chemical effects on proliferation and viability of immortalized human neural progenitor cells. Toxicol. Sci. 105 (2008), 119–133.
7. Brent, R.L., Christian, M.S., Diener, R.M., Evaluation of the reproductive and developmental risks of caffeine. Birth Defects Res. B Dev. Reprod. Toxicol. 92 (2011), 152–187.
8. Chan, K.K.W., Oza, A.M., Siu, L.L., The statins as anticancer agents. Clin. Cancer Res. 9 (2003), 10–19.
9. Choi, S.H., Kim, Y.H., Hebisch, M., Sliwinski, C., Lee, S., D'Avanzo, C., Chen, H., Hooli, B., Asselin, C., Muffat, J., et al. A three-dimensional human neural cell culture model of Alzheimer's disease. Nature 515 (2014), 274–278.
10. Clemedson, C., Kolman, A., Forsby, A., The integrated acute systemic toxicity project (ACuteTox) for the optimisation and validation of alternative in vitro tests. Altern. Lab. Anim. 35 (2007), 33–38.
11. Couillard-Despres, S., Winner, B., Karl, C., Lindemann, G., Schmid, P., Aigner, R., Laemke, J., Bogdahn, U., Winkler, J., Bischofberger, J., et al. Targeted transgene expression in neuronal precursors: watching young neurons in the old brain. Eur. J. Neurosci. 24 (2006), 1535–1545.
12. Diasio, R.B., Harris, B.E., Clinical pharmacology of 5-fluorouracil. Clin. Pharmacokinet. 16 (1989), 215–237.
13. DiMasi, J.A., Hansen, R.W., Grabowski, H.G., The price of innovation: new estimates of drug development costs. J. Health Econ. 22 (2003), 151–185.
14. Donato, R., Miljan, E.A., Hines, S.J., Aouabdi, S., Pollock, K., Patel, S., Edwards, F.A., Sinden, J.D., Differential development of neuronal physiological responsiveness in two human neural stem cell lines. BMC Neurosci., 8, 2007, 36.
15. El-Ali, J., Sorger, P.K., Jensen, K.F., Cells on chips. Nature 442 (2006), 403–411.
16. Gewirtz, D.A., A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 57 (1999), 727–741.
17. Goldman, S., Glia as neural progenitor cells. Trends Neurosci. 26 (2003), 590–596.
18. Graham, V., Khudyakov, J., Ellis, P., Pevny, L., SOX2 functions to maintain neural progenitor identity. Neuron 39 (2003), 749–765.
19. Hay, M., Thomas, D.W., Craighead, J.L., Economides, C., Rosenthal, J., Clinical development success rates for investigational drugs. Nat. Biotechnol. 32 (2014), 40–51.
20. Hoffrogge, R., Mikkat, S., Scharf, C., Beyer, S., Christoph, H., Pahnke, J., Mix, E., Berth, M., Uhrmacher, A., Zubrzycki, I.Z., et al. 2-DE proteome analysis of a proliferating and differentiating human neuronal stem cell line (ReNcell VM). Proteomics 6 (2006), 1833–1847.
21. Kohen, N.T., Little, L.E., Healy, K.E., Characterization of Matrigel interfaces during defined human embryonic stem cell culture. Biointerphases 4 (2009), 69–79.
22. Komitova, M., Eriksson, P.S., Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci. Lett. 369 (2004), 24–27.
23. Kwon, S.J., Lee, D.W., Shah, D.A., Ku, B., Jeon, S.Y., Solanki, K., Ryan, J.D., Clark, D.S., Dordick, J.S., Lee, M.-Y., High-throughput and combinatorial gene expression on a chip for metabolism-induced toxicology screening. Nat. Commun., 5, 2014, 3739.
24. Lammer, E.J., Chen, D.T., Hoar, R.M., Agnish, N.D., Benke, P.J., Braun, J.T., Curry, C.J., Fernhoff, P.M., Grix, A.W., Lott, I.T., Retinoic acid embryopathy. N. Engl. J. Med. 313 (1985), 837–841.
25. Lancaster, M.A., Renner, M., Martin, C., Wenzel, D., Bicknell, L.S., Hurles, M.E., Homfray, T., Penninger, J.M., Jackson, A.P., Knoblich, J.A., et al. Cerebral organoids model human brain development and microcephaly. Nature 501 (2013), 373–379.
26. Lange, C., Mix, E., Frahm, J., Glass, Ä., Müller, J., Schmitt, O., Schmöle, A.C., Klemm, K., Ortinau, S., Hübner, R., et al. Small molecule GSK-3 inhibitors increase neurogenesis of human neural progenitor cells. Neurosci. Lett. 488 (2011), 36–40.
27. Ledford, H., Ways to fix the clinical trial. Nature 477 (2011), 7–9.
28. Li, X., Zhang, X., Zhao, S., Wang, J., Liu, G., Du, Y., Micro-scaffold array chip for upgrading cell-based high-throughput drug testing to 3D using benchtop equipment. Lab Chip 14 (2014), 471–481.
29. Li, L., Zhou, Q., Voss, T.C., Quick, K.L., LaBarbera, D.V., High-throughput imaging: focusing in on drug discovery in 3D. Methods 96 (2015), 97–102.
30. Lutolf, M.P., Gilbert, P.M., Blau, H.M., Designing materials to direct stem-cell fate. Nature 462 (2009), 433–441.
31. Markiewicz, I., Lukomska, B., The role of astrocytes in the physiology and pathology of the central nervous system. Acta Neurobiol. Exp. (Wars) 66 (2006), 343–358.
32. McCaffery, P.J., Adams, J., Maden, M., Rosa-Molinar, E., Too much of a good thing: retinoic acid as an endogenous regulator of neural differentiation and exogenous teratogen. Eur. J. Neurosci. 18 (2003), 457–472.
33. Meli, L., Jordan, E.T., Clark, D.S., Linhardt, R.J., Dordick, J.S., Influence of a three-dimensional, microarray environment on human Cell culture in drug screening systems. Biomaterials 33 (2012), 9087–9096.
34. Meli, L., Barbosa, H.S.C., Hickey, A.M., Gasimli, L., Nierode, G., Diogo, M.M., Linhardt, R.J., Cabral, J.M.S., Dordick, J.S., Three dimensional cellular microarray platform for human neural stem cell differentiation and toxicology. Stem Cell Res. 13 (2014), 36–47.
35. Momparler, R.L., Biochemical pharmacology of cytosine arabinoside. Med. Pediatr. Oncol. 10:Suppl 1 (1982), 45–48.
36. Neal, A.P., Guilarte, T.R., Mechanisms of lead and manganese neurotoxicity. Toxicol. Res. (Camb.) 2 (2013), 99–114.
37. Park, D., Xiang, A.P., Mao, F.F., Zhang, L., Di, C.G., Liu, X.M., Shao, Y., Ma, B.F., Lee, J.H., Ha, K.S., et al. Nestin is required for the proper self-renewal of neural stem cells. Stem Cells 28 (2010), 2162–2171.
38. Pino-Barrio, M.J., García-García, E., Menéndez, P., Martínez-Serrano, A., V-Myc immortalizes human neural stem cells in the absence of pluripotency- associated traits. PLoS One, 10, 2015, e0118499.
39. Radovanovic, D., Meier, P.J., Guirguis, M., Lorent, J.P., Kupferschmidt, H., Dose-dependent toxicity of diphenhydramine overdose. Hum. Exp. Toxicol. 19 (2000), 489–495.
40. Ranga, A., Gobaa, S., Okawa, Y., Mosiewicz, K., Negro, A., Lutolf, M.P., 3D niche microarrays for systems-level analyses of cell fate. Nat. Commun., 5, 2014, 4324.
41. Raponi, E., Agenes, F., Delphin, C., Assard, N., Baudier, J., Legraverend, C., Deloulme, J.C., S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55 (2007), 165–177.
42. Roskams, A.J.I., Cai, X., Ronnett, G.V., Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience 83 (1998), 191–200.
43. Shi, Y., Kirwan, P., Livesey, F.J., Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat. Protoc. 7 (2012), 1836–1846.
44. Soen, Y., Soen, Y., Mori, A., Mori, A., Palmer, T.D., Palmer, T.D., Brown, P.O., Brown, P.O., Exploring the regulation of human neural precursor cell differentiation using arrays of signaling microenvironments. Mol. Syst. Biol., 2, 2006, 37.
45. Spence, J.R., Mayhew, C.N., Rankin, S.A., Kuhar, M.F., Vallance, J.E., Tolle, K., Hoskins, E.E., Kalinichenko, V.V., Wells, S.I., Zorn, A.M., et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470 (2011), 105–109.
46. Sprinkle, T.J., 2′,3′-Cyclic nucleotide 3′-phosphodiesterase, an oligodendrocyte-Schwann cell and myelin-associated enzyme of the nervous system. Crit. Rev. Neurobiol. 4 (1989), 235–301.
47. Sun, Y., Pollard, S., Conti, L., Toselli, M., Biella, G., Parkin, G., Willatt, L., Falk, A., Cattaneo, E., Smith, A., Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol. Cell. Neurosci. 38 (2008), 245–258.
48. Takebe, T., Sekine, K., Enomura, M., Koike, H., Kimura, M., Ogaeri, T., Zhang, R.-R., Ueno, Y., Zheng, Y.-W., Koike, N., et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499 (2013), 481–484.
49. Wetsel, R.A., Wang, D., Calame, D.G., Therapeutic potential of lung epithelial progenitor cells derived from embryonic and induced pluripotent stem cells. Annu. Rev. Med. 62 (2011), 95–105.
50. Yarmush, M.L., King, K.R., Living-cell microarrays. Annu. Rev. Biomed. Eng. 11 (2009), 235–257.
51. Zaman, M.H., Trapani, L.M., Sieminski, A.L., Mackellar, D., Gong, H., Kamm, R.D., Wells, A., Lauffenburger, D.A., Matsudaira, P., Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. USA 103 (2006), 10889–10894.
52. Zhang, S.C., Wernig, M., Duncan, I.D., Brüstle, O., Thomson, J.A., In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19 (2001), 1129–1133.