Molecular Profiling of Human Induced Pluripotent Stem Cell-Derived Cells and their Application for Drug Safety Study

Author(s): Toshikatsu Matsui, Norimasa Miyamoto, Fumiyo Saito, Tadahiro Shinozawa*

Journal Name: Current Pharmaceutical Biotechnology

Volume 21 , Issue 9 , 2020


Become EABM
Become Reviewer
Call for Editor

Graphical Abstract:


Abstract:

Drug-induced toxicity remains one of the leading causes of discontinuation of the drug candidate and post-marketing withdrawal. Thus, early identification of the drug candidates with the potential for toxicity is crucial in the drug development process. With the recent discovery of human- Induced Pluripotent Stem Cells (iPSC) and the establishment of the differentiation protocol of human iPSC into the cell types of interest, the differentiated cells from human iPSC have garnered much attention because of their potential applicability in toxicity evaluation as well as drug screening, disease modeling and cell therapy. In this review, we expanded on current information regarding the feasibility of human iPSC-derived cells for the evaluation of drug-induced toxicity with a focus on human iPSCderived hepatocyte (iPSC-Hep), cardiomyocyte (iPSC-CMs) and neurons (iPSC-Neurons). Further, we CSAHi, Consortium for Safety Assessment using Human iPS Cells, reported our gene expression profiling data with DNA microarray using commercially available human iPSC-derived cells (iPSC-Hep, iPSC-CMs, iPSC-Neurons), their relevant human tissues and primary cultured human cells to discuss the future direction of the three types of human iPSC-derived cells.

Keywords: iPSC-derived hepatocyte, iPSC-derived cardiomyocyte, iPSC-derived neurons, drug safety research, microarray, predictive toxicity assay.

[1]
Chan, R.; Benet, L.Z. Evaluation of DILI predictive hypotheses in early drug development. Chem. Res. Toxicol., 2017, 30(4), 1017-1029.
[http://dx.doi.org/10.1021/acs.chemrestox.7b00025] [PMID: 28257576]
[2]
Kuna, L.; Bozic, I.; Kizivat, T.; Bojanic, K.; Mrso, M.; Kralj, E.; Smolic, R.; Wu, G.Y.; Smolic, M. Models of drug induced liver injury (DILI) - Current issues and future perspectives. Curr. Drug Metab., 2018, 19(10), 830-838.
[http://dx.doi.org/10.2174/1389200219666180523095355] [PMID: 29788883]
[3]
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. Regul. Toxicol. Pharmacol., 2000, 32(1), 56-67.
[http://dx.doi.org/10.1006/rtph.2000.1399] [PMID: 11029269]
[4]
Claude, N. [Are non-clinical studies predictive of adverse events in humans?] Ann. Pharm. Fr., 2007, 65(5), 292-297.
[http://dx.doi.org/10.1016/S0003-4509(07)92590-0] [PMID: 17982375]
[5]
Tomida, T.; Okamura, H.; Satsukawa, M.; Yokoi, T.; Konno, Y. Multiparametric assay using HepaRG cells for predicting drug-induced liver injury. Toxicol. Lett., 2015, 236(1), 16-24.
[http://dx.doi.org/10.1016/j.toxlet.2015.04.014] [PMID: 25934330]
[6]
Saito, J.; Okamura, A.; Takeuchi, K.; Hanioka, K.; Okada, A.; Ohata, T. High content analysis assay for prediction of human hepatotoxicity in HepaRG and HepG2 cells. Toxicol. In Vitro, 2016, 33, 63-70.
[http://dx.doi.org/10.1016/j.tiv.2016.02.019] [PMID: 26921665]
[7]
Xu, J.; Oda, S.; Yokoi, T. Cell-based assay using glutathione-depleted HepaRG and HepG2 human liver cells for predicting drug-induced liver injury. Toxicol. In Vitro, 2018, 48, 286-301.
[http://dx.doi.org/10.1016/j.tiv.2018.01.019] [PMID: 29407385]
[8]
Bell, C.C.; Lauschke, V.M.; Vorrink, S.U.; Palmgren, H.; Duffin, R.; Andersson, T.B.; Ingelman-Sundberg, M. Transcriptional, functional, and mechanistic comparisons of stem cell-derived hepatocytes, HepaRG cells, and three-dimensional human hepatocyte spheroids as predictive in vitro systems for drug-induced liver injury. Drug Metab. Dispos., 2017, 45(4), 419-429.
[http://dx.doi.org/10.1124/dmd.116.074369] [PMID: 28137721]
[9]
Choudhury, Y.; Toh, Y.C.; Xing, J.; Qu, Y.; Poh, J.; Li, H.; Tan, H.S.; Kanesvaran, R.; Yu, H.; Tan, M.H. Patient-specific hepatocyte-like cells derived from induced pluripotent stem cells model pazopanib-mediated hepatotoxicity. Sci. Rep., 2017, 7, 41238.
[http://dx.doi.org/10.1038/srep41238] [PMID: 28120901]
[10]
Bénichou, C. Criteria of drug-induced liver disorders. Report of an international consensus meeting. J. Hepatol., 1990, 11(2), 272-276.
[http://dx.doi.org/10.1016/0168-8278(90)90124-A] [PMID: 2254635]
[11]
Oorts, M.; Baze, A.; Bachellier, P.; Heyd, B.; Zacharias, T.; Annaert, P.; Richert, L. Drug-induced cholestasis risk assessment in sandwich-cultured human hepatocytes. Toxicol. In Vitro, 2016, 34, 179-186.
[http://dx.doi.org/10.1016/j.tiv.2016.03.008] [PMID: 27046439]
[12]
Chatterjee, S.; Richert, L.; Augustijns, P.; Annaert, P. Hepatocyte based in vitro model for assessment of drug-induced cholestasis. Toxicol. Appl. Pharmacol., 2014, 274(1), 124-136.
[http://dx.doi.org/10.1016/j.taap.2013.10.032] [PMID: 24211272]
[13]
Dawson, S.; Stahl, S.; Paul, N.; Barber, J.; Kenna, J.G. In vitro inhibition of the bile salt export pump correlates with risk of cholestatic drug-induced liver injury in humans. Drug Metab. Dispos., 2012, 40(1), 130-138.
[http://dx.doi.org/10.1124/dmd.111.040758] [PMID: 21965623]
[14]
Vinken, M.; Knapen, D.; Vergauwen, L.; Hengstler, J.G.; Angrish, M.; Whelan, M. Adverse outcome pathways: A concise introduction for toxicologists. Arch. Toxicol., 2017, 91(11), 3697-3707.
[http://dx.doi.org/10.1007/s00204-017-2020-z] [PMID: 28660287]
[15]
Vinken, M. Adverse outcome pathways as tools to assess drug-induced toxicity. Methods Mol. Biol., 2016, 1425, 325-337.
[http://dx.doi.org/10.1007/978-1-4939-3609-0_14] [PMID: 27311472]
[16]
Ulvestad, M.; Nordell, P.; Asplund, A.; Rehnström, M.; Jacobsson, S.; Holmgren, G.; Davidson, L.; Brolén, G.; Edsbagge, J.; Björquist, P.; Küppers-Munther, B.; Andersson, T.B. Drug metabolizing enzyme and transporter protein profiles of hepatocytes derived from human embryonic and induced pluripotent stem cells. Biochem. Pharmacol., 2013, 86(5), 691-702.
[http://dx.doi.org/10.1016/j.bcp.2013.06.029] [PMID: 23856292]
[17]
Imagawa, K.; Takayama, K.; Isoyama, S.; Tanikawa, K.; Shinkai, M.; Harada, K.; Tachibana, M.; Sakurai, F.; Noguchi, E.; Hirata, K.; Kage, M.; Kawabata, K.; Sumazaki, R.; Mizuguchi, H. Generation of a bile salt export pump deficiency model using patient specific induced pluripotent stem cell-derived hepatocyte-like cells. Sci. Rep., 2017, 7, 41806.
[http://dx.doi.org/10.1038/srep41806] [PMID: 28150711]
[18]
Guo, L.; Dial, S.; Shi, L.; Branham, W.; Liu, J.; Fang, J.L.; Green, B.; Deng, H.; Kaput, J.; Ning, B. Similarities and differences in the expression of drug-metabolizing enzymes between human hepatic cell lines and primary human hepatocytes. Drug Metab. Dispos., 2011, 39(3), 528-538.
[http://dx.doi.org/10.1124/dmd.110.035873] [PMID: 21149542]
[19]
Xuan, J.; Chen, S.; Ning, B.; Tolleson, W.H.; Guo, L. Development of HepG2-derived cells expressing cytochrome P450s for assessing metabolism-associated drug-induced liver toxicity. Chem. Biol. Interact., 2016, 255, 63-73.
[http://dx.doi.org/10.1016/j.cbi.2015.10.009] [PMID: 26477383]
[20]
Tolosa, L.; Gómez-Lechón, M.J.; Pérez-Cataldo, G.; Castell, J.V.; Donato, M.T. HepG2 cells simultaneously expressing five P450 enzymes for the screening of hepatotoxicity: Identification of bioactivable drugs and the potential mechanism of toxicity involved. Arch. Toxicol., 2013, 87(6), 1115-1127.
[http://dx.doi.org/10.1007/s00204-013-1012-x] [PMID: 23397584]
[21]
Takayama, K.; Inamura, M.; Kawabata, K.; Sugawara, M.; Kikuchi, K.; Higuchi, M.; Nagamoto, Y.; Watanabe, H.; Tashiro, K.; Sakurai, F.; Hayakawa, T.; Furue, M.K.; Mizuguchi, H. Generation of metabolically functioning hepatocytes from human pluripotent stem cells by FOXA2 and HNF1α transduction. J. Hepatol., 2012, 57(3), 628-636.
[http://dx.doi.org/10.1016/j.jhep.2012.04.038] [PMID: 22659344]
[22]
Murayama, N.; Yamazaki, H. Cytochrome P450-dependent drug oxidation activities in commercially available hepatocytes derived from human induced pluripotent stem cells cultured for 3 weeks. J. Toxicol. Sci., 2018, 43(4), 241-245.
[http://dx.doi.org/10.2131/jts.43.241] [PMID: 29618712]
[23]
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/hiPSCderived hepatocyte-like cells for drug toxicity testing. Biomaterials, 2013, 34(7), 1781-1789.
[http://dx.doi.org/10.1016/j.biomaterials.2012.11.029] [PMID: 23228427]
[24]
Takayama, K.; Morisaki, Y.; Kuno, S.; Nagamoto, Y.; Harada, K.; Furukawa, N.; Ohtaka, M.; Nishimura, K.; Imagawa, K.; Sakurai, F.; Tachibana, M.; Sumazaki, R.; Noguchi, E.; Nakanishi, M.; Hirata, K.; Kawabata, K.; Mizuguchi, H. Prediction of interindividual differences in hepatic functions and drug sensitivity by using human iPS-derived hepatocytes. Proc. Natl. Acad. Sci. USA, 2014, 111(47), 16772-16777.
[http://dx.doi.org/10.1073/pnas.1413481111] [PMID: 25385620]
[25]
Han, D.; Dara, L.; Win, S.; Than, T.A.; Yuan, L.; Abbasi, S.Q.; Liu, Z.X.; Kaplowitz, N. Regulation of drug-induced liver injury by signal transduction pathways: critical role of mitochondria. Trends Pharmacol. Sci., 2013, 34(4), 243-253.
[http://dx.doi.org/10.1016/j.tips.2013.01.009] [PMID: 23453390]
[26]
Goda, K.; Takahashi, T.; Kobayashi, A.; Shoda, T.; Kuno, H.; Sugai, S. Usefulness of in vitro combination assays of mitochondrial dysfunction and apoptosis for the estimation of potential risk of idiosyncratic drug induced liver injury. J. Toxicol. Sci., 2016, 41(5), 605-615.
[http://dx.doi.org/10.2131/jts.41.605] [PMID: 27665770]
[27]
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. Arch. Toxicol., 2006, 80(9), 580-604.
[http://dx.doi.org/10.1007/s00204-006-0091-3] [PMID: 16598496]
[28]
Boelsterli, U.A.; Lim, P.L. Mitochondrial abnormalities--a link to idiosyncratic drug hepatotoxicity? Toxicol. Appl. Pharmacol., 2007, 220(1), 92-107.
[http://dx.doi.org/10.1016/j.taap.2006.12.013] [PMID: 17275868]
[29]
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. Toxicol. Sci., 2008, 105(1), 97-105.
[http://dx.doi.org/10.1093/toxsci/kfn109] [PMID: 18524759]
[30]
Marroquin, L.D.; Hynes, J.; Dykens, J.A.; Jamieson, J.D.; Will, Y. Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants. Toxicol. Sci., 2007, 97(2), 539-547.
[http://dx.doi.org/10.1093/toxsci/kfm052] [PMID: 17361016]
[31]
Brand, M.D.; Nicholls, D.G. Assessing mitochondrial dysfunction in cells. Biochem. J., 2011, 435(2), 297-312.
[http://dx.doi.org/10.1042/BJ20110162] [PMID: 21726199]
[32]
Eakins, J.; Bauch, C.; Woodhouse, H.; Park, B.; Bevan, S.; Dilworth, C.; Walker, P. A combined in vitro approach to improve the prediction of mitochondrial toxicants. Toxicol. In Vitro, 2016, 34, 161-170.
[http://dx.doi.org/10.1016/j.tiv.2016.03.016] [PMID: 27083147]
[33]
Yu, Y.; Liu, H.; Ikeda, Y.; Amiot, B.P.; Rinaldo, P.; Duncan, S.A.; Nyberg, S.L. Hepatocyte-like cells differentiated from human induced pluripotent stem cells: relevance to cellular therapies. Stem Cell Res. (Amst.), 2012, 9(3), 196-207.
[http://dx.doi.org/10.1016/j.scr.2012.06.004] [PMID: 22885101]
[34]
Sirenko, O.; Hesley, J.; Rusyn, I.; Cromwell, E.F. High-content assays for hepatotoxicity using induced pluripotent stem cell-derived cells. Assay Drug Dev. Technol., 2014, 12(1), 43-54.
[http://dx.doi.org/10.1089/adt.2013.520] [PMID: 24229356]
[35]
Sirenko, O.; Hancock, M.K.; Hesley, J.; Hong, D.; Cohen, A.; Gentry, J.; Carlson, C.B.; Mann, D.A. Phenotypic characterization of toxic compound effects on liver spheroids derived from iPSC using confocal imaging and three-dimensional image analysis. Assay Drug Dev. Technol., 2016, 14(7), 381-394.
[http://dx.doi.org/10.1089/adt.2016.729] [PMID: 27494736]
[36]
Im, I.; Jang, M.J.; Park, S.J.; Lee, S.H.; Choi, J.H.; Yoo, H.W.; Kim, S.; Han, Y.M. Mitochondrial respiratory defect causes dysfunctional lactate turnover via AMP-activated protein kinase activation in human-induced pluripotent stem cell-derived hepatocytes. J. Biol. Chem., 2015, 290(49), 29493-29505.
[http://dx.doi.org/10.1074/jbc.M115.670364] [PMID: 26491018]
[37]
Yokoyama, Y.; Sasaki, Y.; Terasaki, N.; Kawataki, T.; Takekawa, K.; Iwase, Y.; Shimizu, T.; Sanoh, S.; Ohta, S. Comparison of drug metabolism and is related hepatotoxic effects in HepaRG, cryopreserved human hepatocytes, and HepG2 cell cultures. Biol. Pharm. Bull., 2018, 41(5), 722-732.
[http://dx.doi.org/10.1248/bpb.b17-00913] [PMID: 29445054]
[38]
Tolosa, L.; Jiménez, N.; Pelechá, M.; Castell, J.V.; Gómez-Lechón, M.J.; Donato, M.T. Long-term and mechanistic evaluation of drug-induced liver injury in Upcyte human hepatocytes. Arch. Toxicol., 2019, 93(2), 519-532.
[http://dx.doi.org/10.1007/s00204-018-2349-y] [PMID: 30426164]
[39]
Tolosa, L.; Gómez-Lechón, M.J.; López, S.; Guzmán, C.; Castell, J.V.; Donato, M.T.; Jover, R. Human upcyte hepatocytes: characterization of the hepatic phenotype and evaluation for acute and long-term hepatotoxicity routine testing. Toxicol. Sci., 2016, 152(1), 214-229.
[http://dx.doi.org/10.1093/toxsci/kfw078] [PMID: 27208088]
[40]
Takebe, T.; Sekine, K.; Enomura, M.; Koike, H.; Kimura, M.; Ogaeri, T.; Zhang, R.R.; Ueno, Y.; Zheng, Y.W.; Koike, N.; Aoyama, S.; Adachi, Y.; Taniguchi, H. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459), 481-484.
[http://dx.doi.org/10.1038/nature12271] [PMID: 23823721]
[41]
Shinozawa, T.; Yoshikawa, H.Y.; Takebe, T. Reverse engineering liver buds through self-driven condensation and organization towards medical application. Dev. Biol., 2016, 420(2), 221-229.
[http://dx.doi.org/10.1016/j.ydbio.2016.06.036] [PMID: 27364470]
[42]
Takebe, T.; Sekine, K.; Kimura, M.; Yoshizawa, E.; Ayano, S.; Koido, M.; Funayama, S.; Nakanishi, N.; Hisai, T.; Kobayashi, T.; Kasai, T.; Kitada, R.; Mori, A.; Ayabe, H.; Ejiri, Y.; Amimoto, N.; Yamazaki, Y.; Ogawa, S.; Ishikawa, M.; Kiyota, Y.; Sato, Y.; Nozawa, K.; Okamoto, S.; Ueno, Y.; Taniguchi, H. Massive and reproducible production of liver buds entirely from human pluripotent stem cells. Cell Rep., 2017, 21(10), 2661-2670.
[http://dx.doi.org/10.1016/j.celrep.2017.11.005] [PMID: 29212014]
[43]
Yamazaki, D.; Kitaguchi, T.; Ishimura, M.; Taniguchi, T.; Yamanishi, A.; Saji, D.; Takahashi, E.; Oguchi, M.; Moriyama, Y.; Maeda, S.; Miyamoto, K.; Morimura, K.; Ohnaka, H.; Tashibu, H.; Sekino, Y.; Miyamoto, N.; Kanda, Y. Proarrhythmia risk prediction using human induced pluripotent stem cell-derived cardiomyocytes. J. Pharmacol. Sci., 2018, 136(4), 249-256.
[http://dx.doi.org/10.1016/j.jphs.2018.02.005] [PMID: 29555184]
[44]
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. Toxicol. Sci., 2013, 132(2), 317-326.
[http://dx.doi.org/10.1093/toxsci/kft005] [PMID: 23315586]
[45]
Scott, C.W.; Zhang, X.; Abi-Gerges, N.; Lamore, S.D.; Abassi, Y.A.; Peters, M.F. An impedance-based cellular assay using human iPSC-derived cardiomyocytes to quantify modulators of cardiac contractility. Toxicol. Sci., 2014, 142(2), 331-338.
[http://dx.doi.org/10.1093/toxsci/kfu186] [PMID: 25237062]
[46]
Jacobson, E.F.; Tzanakakis, E.S. Who will win: induced pluripotent stem cells versus embryonic stem cells for beta cell replacement and diabetes disease modeling? Curr. Diab. Rep., 2018, 18(12), 133.
[http://dx.doi.org/10.1007/s11892-018-1109-y] [PMID: 30343423]
[47]
Cadet, J.S.; Kamp, T.J. A Recipe for T-tubules in human iPS cellderived cardiomyocytes. Circ. Res., 2017, 121(12), 1294-1295.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.312177] [PMID: 29217703]
[48]
Goineau, S.; Castagné, V. Electrophysiological characteristics and pharmacological sensitivity of two lines of human induced pluripotent stem cell derived cardiomyocytes coming from two different suppliers. J. Pharmacol. Toxicol. Methods, 2018, 90, 58-66.
[http://dx.doi.org/10.1016/j.vascn.2017.12.003] [PMID: 29274391]
[49]
Ji, J.; Kang, J.; Rampe, D. L-type Ca2+ channel responses to bay k 8644 in stem cell-derived cardiomyocytes are unusually dependent on holding potential and charge carrier. Assay Drug Dev. Technol., 2014, 12(6), 352-360.
[http://dx.doi.org/10.1089/adt.2014.596] [PMID: 25147907]
[50]
Huo, J.; Kamalakar, A.; Yang, X.; Word, B.; Stockbridge, N.; Lyn-Cook, B.; Pang, L. Evaluation of batch variations in induced pluripotent stem cell-derived human cardiomyocytes from 2 major suppliers. Toxicol. Sci., 2017, 156(1), 25-38.
[PMID: 28031415]
[51]
Bot, C.T.; Juhasz, K.; Haeusermann, F.; Polonchuk, L.; Traebert, M.; Stoelzle-Feix, S. Cross - site comparison of excitation contraction coupling using impedance and field potential recordings in hiPSC cardiomyocytes. J. Pharmacol. Toxicol. Methods, 2018, 93, 46-58.
[http://dx.doi.org/10.1016/j.vascn.2018.06.006] [PMID: 29940218]
[52]
Kolanowski, T.J.; Antos, C.L.; Guan, K. Making human cardiomyocytes up to date: Derivation, maturation state and perspectives. Int. J. Cardiol., 2017, 241, 379-386.
[http://dx.doi.org/10.1016/j.ijcard.2017.03.099] [PMID: 28377185]
[53]
Lundy, S.D.; Zhu, W.Z.; Regnier, M.; Laflamme, M.A. Structural and functional maturation of cardiomyocytes derived from human pluripotent stem cells. Stem Cells Dev., 2013, 22(14), 1991-2002.
[http://dx.doi.org/10.1089/scd.2012.0490] [PMID: 23461462]
[54]
Kitaguchi, T.; Moriyama, Y.; Taniguchi, T.; Ojima, A.; Ando, H.; Uda, T.; Otabe, K.; Oguchi, M.; Shimizu, S.; Saito, H.; Morita, M.; Toratani, A.; Asayama, M.; Yamamoto, W.; Matsumoto, E.; Saji, D.; Ohnaka, H.; Tanaka, K.; Washio, I.; Miyamoto, N. CSAHi study: Evaluation of multi-electrode array in combination with human iPS cell-derived cardiomyocytes to predict drug-induced QT prolongation and arrhythmia--effects of 7 reference compounds at 10 facilities. J. Pharmacol. Toxicol. Methods, 2016, 78, 93-102.
[http://dx.doi.org/10.1016/j.vascn.2015.12.002] [PMID: 26657830]
[55]
Liang, P.; Lan, F.; Lee, A.S.; Gong, T.; Sanchez-Freire, V.; Wang, Y.; Diecke, S.; Sallam, K.; Knowles, J.W.; Wang, P.J.; Nguyen, P.K.; Bers, D.M.; Robbins, R.C.; Wu, J.C. Drug screening using a library of human induced pluripotent stem cell-derived cardiomyocytes reveals disease-specific patterns of cardiotoxicity. Circulation, 2013, 127(16), 1677-1691.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.113.001883] [PMID: 23519760]
[56]
Lu, H.R.; Whittaker, R.; Price, J.H.; Vega, R.; Pfeiffer, E.R.; Cerignoli, F.; Towart, R.; Gallacher, D.J. High throughput measurement of ca++ dynamics in human stem cell-derived cardiomyocytes by kinetic image cytometery: A cardiac risk assessment characterization using a large panel of cardioactive and inactive compounds. Toxicol. Sci., 2015, 148(2), 503-516.
[http://dx.doi.org/10.1093/toxsci/kfv201] [PMID: 26358003]
[57]
Koci, B.; Luerman, G.; Duenbostell, A.; Kettenhofen, R.; Bohlen, H.; Coyle, L.; Knight, B.; Ku, W.; Volberg, W.; Woska, J.R., Jr; Brown, M.P. An impedance-based approach using human iPSC derived cardiomyocytes significantly improves in vitro prediction of in vivo cardiotox liabilities. Toxicol. Appl. Pharmacol., 2017, 329, 121-127.
[http://dx.doi.org/10.1016/j.taap.2017.05.023] [PMID: 28546047]
[58]
Shinozawa, T.; Nakamura, K.; Shoji, M.; Morita, M.; Kimura, M.; Furukawa, H.; Ueda, H.; Shiramoto, M.; Matsuguma, K.; Kaji, Y.; Ikushima, I.; Yono, M.; Liou, S.Y.; Nagai, H.; Nakanishi, A.; Yamamoto, K.; Izumo, S. Recapitulation of clinical individual susceptibility to drug-induced qt prolongation in healthy subjects using ipsc-derived cardiomyocytes. Stem Cell Reports, 2017, 8(2), 226-234.
[http://dx.doi.org/10.1016/j.stemcr.2016.12.014] [PMID: 28111276]
[59]
Fonck, C.; Easter, A.; Pietras, M.R.; Bialecki, R.A. CNS adverse effects: from functional observation battery/irwin tests to electrophysiology. Handb. Exp. Pharmacol., 2015, 229, 83-113.
[http://dx.doi.org/10.1007/978-3-662-46943-9_4] [PMID: 26091637]
[60]
Cambiaghi, M.; Magri, L.; Cursi, M. Importance of EEG in validating the chronic effects of drugs: Suggestions from animal models of epilepsy treated with rapamycin. Seizure, 2015, 27, 30-39.
[http://dx.doi.org/10.1016/j.seizure.2015.02.015] [PMID: 25891924]
[61]
Cho, S.; Wood, A.; Bowlby, M.R. Brain slices as models for neurodegenerative disease and screening platforms to identify novel therapeutics. Curr. Neuropharmacol., 2007, 5(1), 19-33.
[http://dx.doi.org/10.2174/157015907780077105] [PMID: 18615151]
[62]
McNeish, J.; Roach, M.; Hambor, J.; Mather, R.J.; Weibley, L.; Lazzaro, J.; Gazard, J.; Schwarz, J.; Volkmann, R.; Machacek, D.; Stice, S.; Zawadzke, L.; O’Donnell, C.; Hurst, R. High-throughput screening in embryonic stem cell-derived neurons identifies potentiators of alpha-amino-3-hydroxyl-5-methyl-4-isoxazolepropionate-type glutamate receptors. J. Biol. Chem., 2010, 285(22), 17209-17217.
[http://dx.doi.org/10.1074/jbc.M109.098814] [PMID: 20212047]
[63]
Pacico, N.; Mingorance-Le Meur, A. New in vitro phenotypic assay for epilepsy: Fluorescent measurement of synchronized neuronal calcium oscillations. PLoS One, 2014, 9(1) e84755
[http://dx.doi.org/10.1371/journal.pone.0084755] [PMID: 24416277]
[64]
Nierode, G.J.; Perea, B.C.; McFarland, S.K.; Pascoal, J.F.; Clark, D.S.; Schaffer, D.V.; Dordick, J.S. High-throughput toxicity and phenotypic screening of 3D human neural progenitor cell cultures on a microarray chip platform. Stem Cell Reports, 2016, 7(5), 970-982.
[http://dx.doi.org/10.1016/j.stemcr.2016.10.001] [PMID: 28157485]
[65]
Bradley, J.A.; Luithardt, H.H.; Metea, M.R.; Strock, C.J. In vitro screening for seizure liability using microelectrode array technology. Toxicol. Sci., 2018, 163(1), 240-253.
[http://dx.doi.org/10.1093/toxsci/kfy029] [PMID: 29432603]
[66]
Authier, S.; Arezzo, J.; Delatte, M.S.; Kallman, M.J.; Markgraf, C.; Paquette, D.; Pugsley, M.K.; Ratcliffe, S.; Redfern, W.S.; Stevens, J.; Valentin, J.P.; Vargas, H.M.; Curtis, M.J. Safety pharmacology investigations on the nervous system: An industry survey. J. Pharmacol. Toxicol. Methods, 2016, 81, 37-46.
[http://dx.doi.org/10.1016/j.vascn.2016.06.001] [PMID: 27263834]
[67]
Kreir, M.; Van Deuren, B.; Versweyveld, S.; De Bondt, A.; Van den Wyngaert, I.; Van der Linde, H.; Lu, H.R.; Teuns, G.; Gallacher, D.J. Do in vitro assays in rat primary neurons predict drug induced seizure liability in humans? Toxicol. Appl. Pharmacol., 2018, 346, 45-57.
[http://dx.doi.org/10.1016/j.taap.2018.03.028] [PMID: 29596924]
[68]
Smetters, D.; Majewska, A.; Yuste, R. Detecting action potentials in neuronal populations with calcium imaging. Methods, 1999, 18(2), 215-221.
[http://dx.doi.org/10.1006/meth.1999.0774] [PMID: 10356353]
[69]
Dravid, S.M.; Murray, T.F. Spontaneous synchronized calcium oscillations in neocortical neurons in the presence of physiological [Mg(2+)]: Involvement of AMPA/kainate and metabotropic glutamate receptors. Brain Res., 2004, 1006(1), 8-17.
[http://dx.doi.org/10.1016/j.brainres.2004.01.059] [PMID: 15047019]
[70]
Cook, D.; Brown, D.; Alexander, R.; March, R.; Morgan, P.; Satterthwaite, G.; Pangalos, M.N. Lessons learned from the fate of AstraZeneca’s drug pipeline: A five-dimensional framework. Nat. Rev. Drug Discov., 2014, 13(6), 419-431.
[http://dx.doi.org/10.1038/nrd4309] [PMID: 24833294]
[71]
Meneghello, G.; Verheyen, A.; Van Ingen, M.; Kuijlaars, J.; Tuefferd, M.; Van Den Wyngaert, I.; Nuydens, R.; Nuydens, R. Evaluation of established human iPSC-derived neurons to model neurodegenerative diseases. Neuroscience, 2015, 301, 204-212.
[http://dx.doi.org/10.1016/j.neuroscience.2015.05.071] [PMID: 26047731]
[72]
Odawara, A.; Katoh, H.; Matsuda, N.; Suzuki, I. Induction of long term potentiation and depression phenomena in human induced pluripotent stem cell-derived cortical neurons. Biochem. Biophys. Res. Commun., 2016, 469(4), 856-862.
[http://dx.doi.org/10.1016/j.bbrc.2015.12.087] [PMID: 26718408]
[73]
Odawara, A.; Matsuda, N.; Ishibashi, Y.; Yokoi, R.; Suzuki, I. Toxicological evaluation of convulsant and anticonvulsant drugs in human induced pluripotent stem cell-derived cortical neuronal networks using an MEA system. Sci. Rep., 2018, 8(1), 10416.
[http://dx.doi.org/10.1038/s41598-018-28835-7] [PMID: 29991696]
[74]
Clarke, L.E.; Barres, B.A. Emerging roles of astrocytes in neural circuit development. Nat. Rev. Neurosci., 2013, 14(5), 311-321.
[http://dx.doi.org/10.1038/nrn3484] [PMID: 23595014]
[75]
Ishii, M.N.; Yamamoto, K.; Shoji, M.; Asami, A.; Kawamata, Y. Human Induced Pluripotent Stem Cell (hiPSC)-derived neurons respond to convulsant drugs when co-cultured with hiPSC-derived astrocytes. Toxicology, 2017, 389, 130-138.
[http://dx.doi.org/10.1016/j.tox.2017.06.010] [PMID: 28666936]
[76]
Tukker, A.M.; Wijnolts, F.M.J.; de Groot, A.; Westerink, R.H.S. Human iPSC-derived neuronal models for in vitro neurotoxicity assessment. Neurotoxicology, 2018, 67, 215-225.
[http://dx.doi.org/10.1016/j.neuro.2018.06.007] [PMID: 29909083]
[77]
Rushton, D.J.; Mattis, V.B.; Svendsen, C.N.; Allen, N.D.; Kemp, P.J. Stimulation of GABA-induced Ca2+ influx enhances maturation of human induced pluripotent stem cell-derived neurons. PLoS One, 2013, 8(11) e81031
[http://dx.doi.org/10.1371/journal.pone.0081031] [PMID: 24278369]
[78]
Sirenko, O.; Parham, F.; Dea, S.; Sodhi, N.; Biesmans, S.; Mora-Castilla, S.; Ryan, K.; Behl, M.; Chandy, G.; Crittenden, C.; Vargas- Hurlston, S.; Guicherit, O.; Gordon, R.; Zanella, F.; Carromeu, C. Functional and mechanistic neurotoxicity profiling using human ipsc-derived neural 3D cultures. Toxicol. Sci., 2019, 167(1), 58-76.
[http://dx.doi.org/10.1093/toxsci/kfy218] [PMID: 30169818]
[79]
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. Toxicol. Sci., 2011, 121(1), 73-87.
[http://dx.doi.org/10.1093/toxsci/kfr034] [PMID: 21342877]
[80]
Ryan, K.R.; Sirenko, O.; Parham, F.; Hsieh, J.H.; Cromwell, E.F.; Tice, R.R.; Behl, M. Neurite outgrowth in human induced pluripotent stem cell-derived neurons as a high-throughput screen for developmental neurotoxicity or neurotoxicity. Neurotoxicology, 2016, 53, 271-281.
[http://dx.doi.org/10.1016/j.neuro.2016.02.003] [PMID: 26854185]
[81]
Harrill, J.A.; Freudenrich, T.; Wallace, K.; Ball, K.; Shafer, T.J.; Mundy, W.R. Testing for developmental neurotoxicity using a battery of in vitro assays for key cellular events in neurodevelopment. Toxicol. Appl. Pharmacol., 2018, 354, 24-39.
[http://dx.doi.org/10.1016/j.taap.2018.04.001] [PMID: 29626487]
[82]
Cohen, J.; Tanaka, Y. Comparative sensitivity of human-induced pluripotent stem cell-derived neuronal subtypes to chemically induced neurodegeneration. Appl. In Vitro Toxicol., 2018, 4(4)
[http://dx.doi.org/10.1089/aivt.2017.0028]
[83]
Dingledine, R.; Varvel, N.H.; Dudek, F.E. When and how do seizures kill neurons, and is cell death relevant to epileptogenesis? Adv. Exp. Med. Biol., 2014, 813, 109-122.
[http://dx.doi.org/10.1007/978-94-017-8914-1_9] [PMID: 25012371]
[84]
Quasthoff, S.; Hartung, H.P. Chemotherapy-induced peripheral neuropathy. J. Neurol., 2002, 249(1), 9-17.
[http://dx.doi.org/10.1007/PL00007853] [PMID: 11954874]
[85]
Wolf, S.; Barton, D.; Kottschade, L.; Grothey, A.; Loprinzi, C. Chemotherapy-induced peripheral neuropathy: Prevention and treatment strategies. Eur. J. Cancer, 2008, 44(11), 1507-1515.
[http://dx.doi.org/10.1016/j.ejca.2008.04.018] [PMID: 18571399]
[86]
Rana, P.; Luerman, G.; Hess, D.; Rubitski, E.; Adkins, K.; Somps, C. Utilization of iPSC-derived human neurons for high-throughput drug-induced peripheral neuropathy screening. Toxicol. In Vitro, 2017, 45(Pt 1), 111-118.
[http://dx.doi.org/10.1016/j.tiv.2017.08.014] [PMID: 28843493]
[87]
James, S.E.; Burden, H.; Burgess, R.; Xie, Y.; Yang, T.; Massa, S.M.; Longo, F.M.; Lu, Q. Anti-cancer drug induced neurotoxicity and identification of Rho pathway signaling modulators as potential neuroprotectants. Neurotoxicology, 2008, 29(4), 605-612.
[http://dx.doi.org/10.1016/j.neuro.2008.04.008] [PMID: 18539332]
[88]
Chen, H.Y.; Albertson, T.E.; Olson, K.R. Treatment of drug induced seizures. Br. J. Clin. Pharmacol., 2016, 81(3), 412-419.
[http://dx.doi.org/10.1111/bcp.12720] [PMID: 26174744]
[89]
Ohara, R.; Imamura, K.; Morii, F.; Egawa, N.; Tsukita, K.; Enami, T.; Shibukawa, R.; Mizuno, T.; Nakagawa, M.; Inoue, H. Modeling drug-induced neuropathy using human ipscs for predictive toxicology. Clin. Pharmacol. Ther., 2017, 101(6), 754-762.
[http://dx.doi.org/10.1002/cpt.562] [PMID: 27859025]
[90]
Inoue, H.; Nagata, N.; Kurokawa, H.; Yamanaka, S. iPS cells: a game changer for future medicine. EMBO J., 2014, 33(5), 409-417.
[http://dx.doi.org/10.1002/embj.201387098] [PMID: 24500035]
[91]
Kritis, A.A.; Stamoula, E.G.; Paniskaki, K.A.; Vavilis, T.D. Researching glutamate - induced cytotoxicity in different cell lines: a comparative/collective analysis/study. Front. Cell. Neurosci., 2015, 9, 91.
[http://dx.doi.org/10.3389/fncel.2015.00091] [PMID: 25852482]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 21
ISSUE: 9
Year: 2020
Published on: 09 June, 2020
Page: [807 - 828]
Pages: 22
DOI: 10.2174/1389201021666200422090952
Price: $65

Article Metrics

PDF: 67
HTML: 3