Transcriptome Profiling of Patient-Specific Human iPSC-Cardiomyocytes Predicts Individual Drug Safety and Efficacy Responses In Vitro

Cell Stem Cell

Volumn 19, Issue 3, 2016, Pages 311-325

  Matsa, Elena ^a   Burridge, Paul W ^a,b   Yu, Kun Hsing ^a   Ahrens, John H ^a   Termglinchan, Vittavat ^a   Wu, Haodi ^a   Liu, Chun ^a   Shukla, Praveen ^a   Sayed, Nazish ^a   Churko, Jared M ^a   Shao, Ningyi ^a   Woo, Nicole A ^a   Chao, Alexander S ^a   Gold, Joseph D ^a   Karakikes, Ioannis ^a   Snyder, Michael P ^a   Wu, Joseph C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

cardiomyocytes; induced pluripotent stem cells; personalized drug safety and efficacy; precision medicine

Indexed keywords

RNA; ROSIGLITAZONE; TACROLIMUS; TRANSCRIPTOME; 2,4 THIAZOLIDINEDIONE DERIVATIVE;

ARTICLE; CARDIAC MUSCLE CELL; CARDIOTOXICITY; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL SURVIVAL; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRISPR CAS SYSTEM; CRISPR CAS9 SYSTEM; DNA MODIFICATION; DRUG EFFICACY; DRUG SAFETY; FEMALE; GENE EXPRESSION; GENE MUTATION; GENETIC VARIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INDUCED PLURIPOTENT STEM CELL; METABOLISM; NUCLEAR REPROGRAMMING; PREDICTION; PRIORITY JOURNAL; RNA SEQUENCE; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SKIN FIBROBLAST; TOXICITY TESTING; TOXICOGENETICS; TRANSCRIPTOMICS; CELL DEATH; CYTOLOGY; DRUG EFFECTS; GENE EDITING; GENE EXPRESSION PROFILING; GENETICS; HEART VENTRICLE; HUMAN GENOME; INVERTED REPEAT; TREATMENT OUTCOME;

CELL DEATH; CRISPR-CAS SYSTEMS; GENE EDITING; GENE EXPRESSION PROFILING; GENOME, HUMAN; HEART VENTRICLES; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INVERTED REPEAT SEQUENCES; MYOCYTES, CARDIAC; TACROLIMUS; THIAZOLIDINEDIONES; TREATMENT OUTCOME;

EID: 84991108719     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.07.006     Document Type: Article

References (54)

1. Austin, S., St-Pierre, J., PGC1α and mitochondrial metabolism–emerging concepts and relevance in ageing and neurodegenerative disorders. J. Cell Sci. 125 (2012), 4963–4971.
2. Burridge, P.W., Diecke, S., Matsa, E., Sharma, A., Wu, H., Wu, J.C., Modeling cardiovascular diseases with patient-specific human pluripotent stem cell-derived cardiomyocytes. Methods Mol. Biol. 1353 (2016), 119–130.
3. Casademont, J., Miró, O., Electron transport chain defects in heart failure. Heart Fail. Rev. 7 (2002), 131–139.
4. Chen, I.Y., Matsa, E., Wu, J.C., Induced pluripotent stem cells: at the heart of cardiovascular precision medicine. Nat. Rev. Cardiol. 13 (2016), 333–349.
5. Choi, J., Lee, S., Mallard, W., Clement, K., Tagliazucchi, G.M., Lim, H., Choi, I.Y., Ferrari, F., Tsankov, A.M., Pop, R., et al. A comparison of genetically matched cell lines reveals the equivalence of human iPSCs and ESCs. Nat. Biotechnol. 33 (2015), 1173–1181.
6. Collins, F.S., Varmus, H., A new initiative on precision medicine. N. Engl. J. Med. 372 (2015), 793–795.
7. Fillmore, N., Lopaschuk, G.D., Targeting mitochondrial oxidative metabolism as an approach to treat heart failure. Biochim. Biophys. Acta 1833 (2013), 857–865.
8. Finck, B.N., The PPAR regulatory system in cardiac physiology and disease. Cardiovasc. Res. 73 (2007), 269–277.
9. Frazier, A.H., Ramirez-Correa, G.A., Murphy, A.M., Molecular mechanisms of sarcomere dysfunction in dilated and hypertrophic cardiomyopathy. Prog. Pediatr. Cardiol. 31 (2011), 29–33.
10. Gautier, L., Cope, L., Bolstad, B.M., Irizarry, R.A., affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20 (2004), 307–315.
11. Groop, L., Orho-Melander, M., New insights into impaired muscle glycogen synthesis. PLoS Med., 5, 2008, e25.
12. He, M., Guo, H., Yang, X., Zhang, X., Zhou, L., Cheng, L., Zeng, H., Hu, F.B., Tanguay, R.M., Wu, T., Functional SNPs in HSPA1A gene predict risk of coronary heart disease. PLoS ONE, 4, 2009, e4851.
13. He, H., Tao, H., Xiong, H., Duan, S.Z., McGowan, F.X. Jr., Mortensen, R.M., Balschi, J.A., Rosiglitazone causes cardiotoxicity via peroxisome proliferator-activated receptor γ-independent mitochondrial oxidative stress in mouse hearts. Toxicol. Sci. 138 (2014), 468–481.
14. Hoffmann, B.R., El-Mansy, M.F., Sem, D.S., Greene, A.S., Chemical proteomics-based analysis of off-target binding profiles for rosiglitazone and pioglitazone: clues for assessing potential for cardiotoxicity. J. Med. Chem. 55 (2012), 8260–8271.
15. Ingwall, J.S., Weiss, R.G., Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ. Res. 95 (2004), 135–145.
16. Jornayvaz, F.R., Shulman, G.I., Regulation of mitochondrial biogenesis. Essays Biochem. 47 (2010), 69–84.
17. Kaichi, S., Hasegawa, K., Takaya, T., Yokoo, N., Mima, T., Kawamura, T., Morimoto, T., Ono, K., Baba, S., Doi, H., et al. Cell line-dependent differentiation of induced pluripotent stem cells into cardiomyocytes in mice. Cardiovasc. Res. 88 (2010), 314–323.
18. Laustriat, D., Gide, J., Peschanski, M., Human pluripotent stem cells in drug discovery and predictive toxicology. Biochem. Soc. Trans. 38 (2010), 1051–1057.
19. Lehman, J.J., Barger, P.M., Kovacs, A., Saffitz, J.E., Medeiros, D.M., Kelly, D.P., Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106 (2000), 847–856.
20. Leinwand, L.A., Calcineurin inhibition and cardiac hypertrophy: a matter of balance. Proc. Natl. Acad. Sci. U S A 98 (2001), 2947–2949.
21. Levy, R.J., Serotonin transporter mechanisms and cardiac disease. Circulation 113 (2006), 2–4.
22. Liu, T., Korantzopoulos, P., Li, G., Antioxidant therapies for the management of atrial fibrillation. Cardiovasc. Diagn. Ther. 2 (2012), 298–307.
23. Long, Y.C., Glund, S., Garcia-Roves, P.M., Zierath, J.R., Calcineurin regulates skeletal muscle metabolism via coordinated changes in gene expression. J. Biol. Chem. 282 (2007), 1607–1614.
24. Mahaffey, K.W., Hafley, G., Dickerson, S., Burns, S., Tourt-Uhlig, S., White, J., Newby, L.K., Komajda, M., McMurray, J., Bigelow, R., et al. Results of a reevaluation of cardiovascular outcomes in the RECORD trial. Am. Heart J. 166 (2013), 240–249.e1.
25. Marin-Garcia, J., Goldenthal, M.J., Moe, G.W., Mitochondrial pathology in cardiac failure. Cardiovasc. Res. 49 (2001), 17–26.
26. Martins-Taylor, K., Xu, R.H., Concise review: genomic stability of human induced pluripotent stem cells. Stem Cells 30 (2012), 22–27.
27. Matsa, E., Burridge, P.W., Wu, J.C., Human stem cells for modeling heart disease and for drug discovery. Sci. Transl. Med., 6, 2014, 239ps6.
28. Matsa, E., Ahrens, J.H., Wu, J.C., Human induced pluripotent stem cells as a platform for personalized and precision cardiovascular medicine. Physiol. Rev. 96 (2016), 1093–1126.
29. Mishra, P., Singh, S.V., Verma, A.K., Srivastava, P., Sultana, S., Rath, S.K., Rosiglitazone induces cardiotoxicity by accelerated apoptosis. Cardiovasc. Toxicol. 14 (2014), 99–119.
30. Murphy, E., Estrogen signaling and cardiovascular disease. Circ. Res. 109 (2011), 687–696.
31. Musson, R.E., Cobbaert, C.M., Smit, N.P., Molecular diagnostics of calcineurin-related pathologies. Clin. Chem. 58 (2012), 511–522.
32. Nguyen, T., Nioi, P., Pickett, C.B., The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem. 284 (2009), 13291–13295.
33. 1000 Genomes Project Consortium et al., 2012 1000 Genomes Project Consortium, Abecasis, G.R., Auton, A., Brooks, L.D., DePristo, M.A., Durbin, R.M., Handsaker, R.E., Kang, H.M., Marth, G.T., McVean, G.A., An integrated map of genetic variation from 1,092 human genomes. Nature 491 (2012), 56–65.
34. Ozsolak, F., Milos, P.M., RNA sequencing: advances, challenges and opportunities. Nat. Rev. Genet. 12 (2011), 87–98.
35. Paolini, P., Pick, D., Lapira, J., Sannino, G., Pasqualini, L., Ludka, C., Sprague, L.J., Zhang, X., Bartolotta, E.A., Vazquez-Hidalgo, E., et al. Developmental and extracellular matrix-remodeling processes in rosiglitazone-exposed neonatal rat cardiomyocytes. Pharmacogenomics 15 (2014), 759–774.
36. Potenza, M.A., Gagliardi, S., De Benedictis, L., Zigrino, A., Tiravanti, E., Colantuono, G., Federici, A., Lorusso, L., Benagiano, V., Quon, M.J., Montagnani, M., Treatment of spontaneously hypertensive rats with rosiglitazone ameliorates cardiovascular pathophysiology via antioxidant mechanisms in the vasculature. Am. J. Physiol. Endocrinol. Metab. 297 (2009), E685–E694.
37. Rostambeigi, N., Lanza, I.R., Dzeja, P.P., Deeds, M.C., Irving, B.A., Reddi, H.V., Madde, P., Zhang, S., Asmann, Y.W., Anderson, J.M., et al. Unique cellular and mitochondrial defects mediate FK506-induced islet β-cell dysfunction. Transplantation 91 (2011), 615–623.
38. Rouhani, F., Kumasaka, N., de Brito, M.C., Bradley, A., Vallier, L., Gaffney, D., Genetic background drives transcriptional variation in human induced pluripotent stem cells. PLoS Genet., 10, 2014, e1004432.
39. Scannell, J.W., Bosley, J., When quality beats quantity: decision theory, drug discovery, and the reproducibility crisis. PLoS ONE, 11, 2016, e0147215.
40. Sgodda, M., Cantz, T., Small but significant: inter- and intrapatient variations in iPS cell-based disease modeling. Mol. Ther. 21 (2013), 5–7.
41. Shah, R.D., Gonzales, F., Golez, E., Augustin, D., Caudillo, S., Abbott, A., Morello, J., McDonough, P.M., Paolini, P.J., Shubeita, H.E., The antidiabetic agent rosiglitazone upregulates SERCA2 and enhances TNF-alpha- and LPS-induced NF-kappaB-dependent transcription and TNF-alpha-induced IL-6 secretion in ventricular myocytes. Cell. Physiol. Biochem. 15 (2005), 41–50.
42. Simon, N., Morin, C., Urien, S., Tillement, J.P., Bruguerolle, B., Tacrolimus and sirolimus decrease oxidative phosphorylation of isolated rat kidney mitochondria. Br. J. Pharmacol. 138 (2003), 369–376.
43. Storey, J.D., Madeoy, J., Strout, J.L., Wurfel, M., Ronald, J., Akey, J.M., Gene-expression variation within and among human populations. Am. J. Hum. Genet. 80 (2007), 502–509.
44. Sussman, M.A., Lim, H.W., Gude, N., Taigen, T., Olson, E.N., Robbins, J., Colbert, M.C., Gualberto, A., Wieczorek, D.F., Molkentin, J.D., Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science 281 (1998), 1690–1693.
45. 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 131 (2007), 861–872.
46. Tapia, N., Schöler, H.R., Molecular obstacles to clinical translation of iPSCs. Cell Stem Cell, 2016, 10.1016/j.stem.2016.06.017 in press. Published online July 21, 2016.
47. Trachootham, D., Lu, W., Ogasawara, M.A., Nilsa, R.D., Huang, P., Redox regulation of cell survival. Antioxid. Redox Signal. 10 (2008), 1343–1374.
48. Ventura-Clapier, R., Garnier, A., Veksler, V., Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc. Res. 79 (2008), 208–217.
49. Wilson, K.D., Wu, J.C., Induced pluripotent stem cells. JAMA 313 (2015), 1613–1614.
50. Wilson, P.W., D'Agostino, R.B., Levy, D., Belanger, A.M., Silbershatz, H., Kannel, W.B., Prediction of coronary heart disease using risk factor categories. Circulation 97 (1998), 1837–1847.
51. Young, M.D., Wakefield, M.J., Smyth, G.K., Oshlack, A., Gene Ontology analysis for RNA-seq: accounting for selection bias. Genome Biol., 11, 2010, R14.
52. 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., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318 (2007), 1917–1920.
53. Zhang, Y., Yao, L., Yu, X., Ou, J., Hui, N., Liu, S., A poor imitation of a natural process: a call to reconsider the iPSC engineering technique. Cell Cycle 11 (2012), 4536–4544.
54. Zini, R., Simon, N., Morin, C., Thiault, L., Tillement, J.P., Tacrolimus decreases in vitro oxidative phosphorylation of mitochondria from rat forebrain. Life Sci. 63 (1998), 357–368.