Comparing ESC and iPSC—based models for human genetic disorders

Journal of Clinical Medicine

Volumn 3, Issue 4, 2014, Pages 1146-1162

  Halevy, Tomer ^a   Urbach, Achia ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

Disease modeling; Embryonic stem cells (ESCs); Induced pluripotent stem cells (iPSCs)

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; HUNTINGTIN;

CHROMOSOME ABERRATION; DISEASE MODEL; EMBRYONIC STEM CELL; FANCONI ANEMIA; FRAGILE X SYNDROME; GENE; GENE MUTATION; GENE TARGETING; GENETIC DISORDER; GENETIC MANIPULATION; GENOTYPE; HUMAN; HUNTINGTON CHOREA; METHODOLOGY; NONHUMAN; NUCLEAR REPROGRAMMING; PHENOTYPE; PLURIPOTENT STEM CELL; PREIMPLANTATION GENETIC DIAGNOSIS; REVIEW; TURNER SYNDROME;

EID: 84975780905     PISSN: None     EISSN: 20770383     Source Type: Journal    
DOI: None     Document Type: Review

References (70)

1. Robinton, D.A.; Daley, G.Q. The promise of induced pluripotent stem cells in research and therapy. Nature 2012, 481, 295-305.
2. Roberts, R.M.; Loh, K.M.; Amita, M.; Bernardo, A.S.; Adachi, K.; Alexenko, A.P.; Schust, D.J.; Schulz, L.C.; Telugu, B.P.V.L.; Ezashi, T, et al. Differentiation of trophoblast cells from human embryonic stem cells: To be or not to be? Reproduction 2014, 147, doi:10.1530/REP-14-0080.
3. Xu, R.-H.; Chen, X.; Li, D.S.; Li, R.; Addicks, G.C.; Glennon, C.; Zwaka, T.P.; Thomson, J.A. BMP4 Initiates Human Embryonic Stem Cell Differentiation to Trophoblast. Nat. Biotechnol. 2002, 20, 1261-1264.
4. Vandamme, T.F. Use of rodents as models of human diseases. J. Pharm. Bioallied Sci. 2014, 6, 2-9.
5. Urbach, A.; Schuldiner, M.; Benvenisty, N. Modeling for Lesch-Nyhan disease by gene targeting in human embryonic stem cells. Stem Cells 2004, 22, 635-641.
6. Urbach, A.; Benvenisty, N. Studying early lethality of 45,XO (Turner’s syndrome) embryos using human embryonic stem cells. PLoS One 2009, 4, doi:10.1371/journal.pone.0004175.
7. Eiges, R.; Urbach, A.; Malcov, M.; Frumkin, T.; Schwartz, T.; Amit, A.; Yaron, Y.; Eden, A.; Yanuka, O.; Benvenisty, N, et al. Developmental study of fragile X syndrome using human embryonic stem cells derived from preimplantation genetically diagnosed embryos. Cell Stem Cell 2007, 1, 568-577.
8. Maury, Y.; Gauthier, M.; Peschanski, M.; Martinat, C. Human pluripotent stem cells for disease modelling and drug screening. Bioessays 2012, 34, 61-71.
9. Verlinsky, Y.; Strelchenko, N.; Kukharenko, V.; Rechitsky, S.; Verlinsky, O.; Galat, V.; Kuliev, A. Human embryonic stem cell lines with genetic disorders. Reprod. Biomed. Online 2005, 10, 105-110.
10. Mateizel, I.; Spits, C.; de Rycke, M.; Liebaers, I.; Sermon, K. Derivation, culture, and characterization of VUB hESC lines. Vitr. Cell. Dev. Biol. Anim. 2010, 46, 300-308.
11. Park, I.-H.; Arora, N.; Huo, H.; Maherali, N.; Ahfeldt, T.; Shimamura, A.; Lensch, M.W.; Cowan, C.; Hochedlinger, K.; Daley, G.Q. Disease-specific induced pluripotent stem cells. Cell 2008, 134, 877-886.
12. Dimos, J.T.; Rodolfa, K.T.; Niakan, K.K.; Weisenthal, L.M.; Mitsumoto, H.; Chung, W.; Croft, G.F.; Saphier, G.; Leibel, R.; Goland, R, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321, 1218-1221.
13. Kiskinis, E.; Sandoe, J.; Williams, L.; Boulting, G.; Moccia, R.; Wainger, B.; Han, S.; Peng, T.; Thams, S.; Mikkilineni, S. et al. Pathways Disrupted in Human ALS Motor Neurons Identified through Genetic Correction of Mutant SOD1. Cell Stem Cell 2014, 14, 781-795.
14. Puri, M.C.; Nagy, A. Concise review: Embryonic stem cells versus induced pluripotent stem cells: The game is on. Stem Cells 2012, 30, 10-14.
15. Bilic, J.; Izpisua Belmonte, J.C. Concise review: Induced pluripotent stem cells versus embryonic stem cells: Close enough or yet too far apart? Stem Cells 2012, 30, 33-41.
16. Cherry, A.B.C.; Daley, G.Q. Reprogrammed cells for disease modeling and regenerative medicine. Annu. Rev. Med. 2013, 64, 277-290.
17. Kim, H.; Kim, J.-S. A guide to genome engineering with programmable nucleases. Nat. Rev. Genet. 2014, 15, 321-334.
18. Sandoe, J.; Eggan, K. Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat. Neurosci. 2013, 16, 780-789.
19. Robertson, J.A. Human embryonic stem cell research: Ethical and legal issues. Nat. Rev. Genet. 2001, 2, 74-78.
20. De Wert, G.; Mummery, C. Human embryonic stem cells: Research, ethics and policy. Hum. Reprod. 2003, 18, 672-682.
21. Kim, K.; Doi, A.; Wen, B.; Ng, K.; Zhao, R.; Cahan, P.; Kim, J.; Aryee, M.J.; Ji, H.; Ehrlich, L.I, et al. Epigenetic memory in induced pluripotent stem cells. Nature 2010, 467, 285-290.
22. Bar-Nur, O.; Russ, H.A.; Efrat, S.; Benvenisty, N. Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell 2011, 9, 17-23.
23. Ma, H.; Morey, R.; O’Neil, R.C.; He, Y.; Daughtry, B.; Schultz, M.D.; Hariharan, M.; Nery, J.R.; Castanon, R.; Sabatini, K. et al. Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature 2014, 511, 177-183.
24. Gore, A.; Li, Z.; Fung, H.-L.; Young, J.E.; Agarwal, S.; Antosiewicz-Bourget, J.; Canto, I.; Giorgetti, A.; Israel, M.A.; Kiskinis, E. et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011, 471, 63-67.
25. Yung, S.K.; Tilgner, K.; Ledran, M.H.; Habibollah, S.; Neganova, I.; Singhapol, C.; Saretzki, G.; Stojkovic, M.; Armstrong, L.; Przyborski, S. et al. Brief report: Human pluripotent stem cell models of fanconi anemia deficiency reveal an important role for fanconi anemia proteins in cellular reprogramming and survival of hematopoietic progenitors. Stem Cells 2013, 31, 1022-1029.
26. Muller, L.U.W.; Milsom, M.D.; Harris, C.E.; Vyas, R.; Brumme, K.M.; Parmar, K.; Moreau, L.A.; Schambach, A.; Park, I.H.; London, W.B. et al. Overcoming reprogramming resistance of Fanconi anemia cells. Blood 2012, 119, 5449-5457.
27. Wang, Z.-B.; Zhang, X.; Li, X.-J. Recapitulation of spinal motor neuron-specific disease phenotypes in a human cell model of spinal muscular atrophy. Cell Res. 2013, 23, 378-393.
28. Ebert, A.D.; Yu, J.; Rose, F.F.; Mattis, V.B.; Lorson, C.L.; Thomson, J.A.; Svendsen, C.N. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 2009, 457, 277-280.
29. Tulpule, A.; Kelley, J.M.; Lensch, M.W.; McPherson, J.; Park, I.H.; Hartung, O.; Nakamura, T.; Schlaeger, T.M.; Shimamura, A.; Daley, G.Q. Pluripotent stem cell models of shwachman-diamond syndrome reveal a common mechanism for pancreatic and hematopoietic dysfunction. Cell Stem Cell 2013, 12, 727-736.
30. Bellin, M.; Casini, S.; Davis, R.P.; D’Aniello, C.; Haas, J.; Ward-van Oostwaard, D.; Tertoolen, L.G.J.; Jung, C.B.; Elliott, D.A.; Welling, A. et al. Isogenic human pluripotent stem cell pairs reveal the role of a KCNH2 mutation in long-QT syndrome. EMBO J. 2013, 32, 3161-3175.
31. Seriola, A.; Spits, C.; Simard, J.P.; Hilven, P.; Haentjens, P.; Pearson, C.E.; Sermon, K. Huntington’s and myotonic dystrophy hESCs: Down-regulated trinucleotide repeat instability and mismatch repair machinery expression bupon differentiation. Hum. Mol. Genet. 2011, 20, 176-185.
32. Du, J.; Campau, E.; Soragni, E.; Jespersen, C.; Gottesfeld, J.M. Length-dependent CTG.CAG triplet-repeat expansion in myotonic dystrophy patient-derived induced pluripotent stem cells. Hum. Mol. Genet. 2013, 22, 5276-5287.
33. Saenger, P. Turner’s syndrome. N. Engl. J. Med. 1996, 335, 1749-1754.
34. Ranke, M.B.; Saenger, P. Turner’s syndrome. Lancet 2001, 358, 309-314.
35. Li, W.; Wang, X.; Fan, W.; Zhao, P.; Chan, Y.C.; Chen, S.; Zhang, S.; Guo, X.; Zhang, Y.; Li, Y. et al. Modeling abnormal early development with induced pluripotent stem cells from aneuploid syndromes. Hum. Mol. Genet. 2012, 21, 32-45.
36. Urbach, A.; Bar-Nur, O.; Daley, G.Q.; Benvenisty, N. Differential modeling of fragile X syndrome by human embryonic stem cells and induced pluripotent stem cells. Cell Stem Cell 2010, 6, 407-411.
37. Li, Y.; Wang, H.; Muffat, J.; Cheng, A.W.; Orlando, D.A.; Lovén, J.; Kwok, S.M.; Feldman, D.A.; Bateup, H.S.; Gao, Q. et al. Global transcriptional and translational repression in human-embryonic-stem-cell-derived Rett syndrome neurons. Cell Stem Cell 2013, 13, 446-458.
38. Cheung, A.Y.L.; Horvath, L.M.; Grafodatskaya, D.; Pasceri, P.; Weksberg, R.; Hotta, A.; Carrel, L.; Ellis, J. Isolation of MECP2-null Rett Syndrome patient hiPS cells and isogenic controls through X-chromosome inactivation. Hum. Mol. Genet. 2011, 20, 2103-2115.
39. Marchetto, M.C.N.; Carromeu, C.; Acab, A.; Yu, D.; Yeo, G.W.; Mu, Y.; Chen, G.; Gage, F.H.; Muotri, A.R. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 2010, 143, 527-539.
40. Tulpule, A.; William Lensch, M.; Miller, J.D.; Austin, K.; D’Andrea, A.; Schlaeger, T.M.; Shimamura, A.; Daley, G.Q. Knockdown of Fanconi anemia genes in human embryonic stem cells reveals early developmental defects in the hematopoietic lineage. Blood 2010, 115, 3453-3462.
41. Liu, G.-H.; Suzuki, K.; Li, M.; Qu, J.; Montserrat, N.; Tarantino, C.; Gu, Y.; Yi, F.; Xu, X.; Zhang, W. et al. Modelling Fanconi anemia pathogenesis and therapeutics using integration-free patient-derived iPSCs. Nat. Commun. 2014, 5, 4330.
42. Lu, B.; Palacino, J. A novel human embryonic stem cell-derived Huntington’s disease neuronal model exhibits mutant huntingtin (mHTT) aggregates and soluble mHTT-dependent neurodegeneration. FASEB J. 2013, 27, 1820-1829.
43. HD iPSC Consortium. Induced pluripotent stem cells from patients with Huntington’s disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 2012, 11, 264-278.
44. D’Andrea, A.D.; Grompe, M. Molecular biology of Fanconi anemia: Implications for diagnosis and therapy. Blood 1997, 90, 1725-1736.
45. Raya, A.; Rodríguez-Pizà, I.; Guenechea, G.; Vassena, R.; Navarro, S.; Barrero, M.J.; Consiglio, A.; Castellà, M.; Río, P.; Sleep, E. et al. Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 2009, 460, 53-59.
46. Boyle, L.; Kaufmann, W.E. The behavioral phenotype of FMR1 mutations. Am. J. Med. Genet. Part C Semin. Med. Genet. 2010, 154C, 469-476.
47. Penagarikano, O.; Mulle, J.G.; Warren, S.T. The pathophysiology of fragile X syndrome. Annu. Rev. Genomics Hum. Genet. 2007, 8, 109-129.
48. Wang, T.; Bray, S.M.; Warren, S.T. New perspectives on the biology of fragile X yndrome. Curr. Opin. Genet. Dev. 2012, 22, 256-263.
49. Callan, M.A.; Zarnescu, D.C. Heads-up: New roles for the fragile X mental retardation protein in neural stem and progenitor cells. Genesis 2011, 49, 424-440.
50. Santoro, M.R.; Bray, S.M.; Warren, S.T. Molecular mechanisms of fragile X syndrome: A twenty-year perspective. Annu. Rev. Pathol. 2012, 7, 219-245.
51. Devys, D.; Lutz, Y.; Rouyer, N.; Bellocq, J.P.; Mandel, J.L. The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation. Nat. Genet. 1993, 4, 335-340.
52. Turetsky, T.; Aizenman, E.; Gil, Y.; Weinberg, N.; Shufaro, Y.; Revel, A.; Laufer, N.; Simon, A.; Abeliovich, D.; Reubinoff, B.E. Laser-assisted derivation of human embryonic stem cell lines from IVF embryos after preimplantation genetic diagnosis. Hum. Reprod. 2008, 23, 46-53.
53. Telias, M.; Segal, M.; Ben-Yosef, D. Neural differentiation of Fragile X human Embryonic Stem Cells reveals abnormal patterns of development despite successful neurogenesis. Dev. Biol. 2013, 374, 32-45.
54. Hatton, D.D.; Sideris, J.; Skinner, M.; Mankowski, J.; Bailey, D.B.; Roberts, J.; Mirrett, P. Autistic behavior in children with fragile X syndrome: Prevalence, stability, and the impact of FMRP. Am. J. Med. Genet. Part A 2006, 140, 1804-1813.
55. Kaufmann, W.E.; Cortell, R.; Kau, A.S.M.; Bukelis, I.; Tierney, E.; Gray, R.M.; Cox, C.; Capone, G.T.; Stanard, P. Autism spectrum disorder in fragile X syndrome: Communication, social interaction, and specific behaviors. Am. J. Med. Genet. A 2004, 129A, 225-234.
56. Pietrobono, R.; Tabolacci, E.; Zalfa, F.; Zito, I.; Terracciano, A.; Moscato, U.; Bagni, C.; Oostra, B.; Chiurazzi, P.; Neri, G. Molecular dissection of the events leading to inactivation of the FMR1 gene. Hum. Mol. Genet. 2005, 14, 267-277.
57. Smeets, H.J.; Smits, A.P.; Verheij, C.E.; Theelen, J.P.; Willemsen, R.; van de Burgt, I.; Hoogeveen, A.T.; Oosterwijk, J.C.; Oostra, B.A. Normal phenotype in two brothers with a full FMR1 mutation. Hum. Mol. Genet. 1995, 4, 2103-2108.
58. Sheridan, S.D.; Theriault, K.M.; Reis, S.A.; Zhou, F.; Madison, J.M.; Daheron, L.; Loring, J.F.; Haggarty, S.J. Epigenetic characterization of the FMR1 gene and aberrant neurodevelopment in human induced pluripotent stem cell models of fragile X syndrome. PLoS One 2011, 6, e26203.
59. Alisch, R.S.; Wang, T.; Chopra, P.; Visootsak, J.; Conneely, K.N.; Warren, S.T. Genome-wide analysis validates aberrant methylation in fragile X syndrome is specific to the FMR1 locus. BMC Med. Genet. 2013, 14, 18.
60. Bar-Nur, O.; Caspi, I.; Benvenisty, N. Molecular analysis of FMR1 reactivation in fragile-X induced pluripotent stem cells and their neuronal derivatives. J. Mol. Cell Biol. 2012, 4, 180-183.
61. Martin, J.B.; Gusella, J.F. Huntington’s disease. Pathogenesis and management. N. Engl. J. Med. 1986, 315, 1267-1276.
62. Huntington, T.; Macdonald, M.E.; Ambrose, C.M.; Duyao, M.P.; Myers, R.H.; Lin, C.; Srinidhi, L.; Barnes, G.; Taylor, S.A.; James, M.; Groat, N. et al. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. The Huntington’s Disease Collaborative Research Group. Cell 1993, 72, 971-983.
63. Landles, C.; Sathasivam, K.; Weiss, A.; Woodman, B.; Moffitt, H.; Finkbeiner, S.; Sun, B.; Gafni, J.; Ellerby, L.M.; Trottier, Y. et al. Proteolysis of mutant huntingtin produces an exon 1 fragment that accumulates as an aggregated protein in neuronal nuclei in Huntington disease. J. Biol. Chem. 2010, 285, 8808-8823.
64. Zhang, N.; An, M.C.; Montoro, D.; Ellerby, L.M. Characterization of human Huntington’s disease cell model from induced pluripotent stem cells. PLoS Curr. 2010, 2, 1-11.
65. Camnasio, S.; Carri, A.D.; Lombardo, A.; Grad, I.; Mariotti, C.; Castucci, A.; Rozell, B.; Riso, P.L.; Castiglioni, V.; Zuccato, C. et al. The first reported generation of several induced pluripotent stem cell lines from homozygous and heterozygous Huntington’s disease patients demonstrates mutation related enhanced lysosomal activity. Neurobiol. Dis. 2012, 46, 41-51.
66. Bradley, C.K.; Scott, H.A.; Chami, O.; Peura, T.T.; Dumevska, B.; Schmidt, U.; Stojanov, T. Derivation of Huntington’s disease-affected human embryonic stem cell lines. Stem Cells Dev. 2011, 20, 495-502.
67. 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 2007, 131, 861-872.
68. Park, I.-H.; Zhao, R.; West, J.A.; Yabuuchi, A.; Huo, H.; Ince, T.A.; Lerou, P.H.; Lensch, M.W.; Daley, G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008, 451, 141-146.
69. Yu, J.Y.; 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 2007, 318, 1917-1920.
70. Takahashi, K.; Yamanaka, S. Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors. Cell 2006, 126, 663-676.