Modeling human neurological disorders with induced pluripotent stem cells

Journal of Neurochemistry

Volumn 129, Issue 3, 2014, Pages 388-399

  Imaizumi, Yoichi ^a,b   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY   (Japan)

^b EISAI CO LTD   (Japan)

Author keywords

human disease model; induced pluripotent stem cells; neurological disorders; Parkinson's disease

Indexed keywords

HUMAN DISEASE MODEL; INDUCED PLURIPOTENT STEM CELLS; NEUROLOGICAL DISORDERS; PARKINSON'S DISEASE;

HUMANS; INDUCED PLURIPOTENT STEM CELLS; MODELS, NEUROLOGICAL; NERVOUS SYSTEM DISEASES;

EID: 84899463833     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12625     Document Type: Review

References (82)

1. An M. C., Zhang N., Scott G., Montoro D., Wittkop T., Mooney S., Melov S., and, Ellerby L. M,. (2012) Genetic correction of Huntington's disease phenotypes in induced pluripotent stem cells. Cell Stem Cell, 253-263.
2. Ananiev G., Williams E. C., Li H., and, Chang Q., (2011) Isogenic pairs of wild type and mutant induced pluripotent stem cell (iPSC) lines from Rett syndrome patients as in vitro disease model. PLoS ONE 6, e25255.
3. Andrade L. N., Nathanson J. L., Yeo G. W., Menck C. F., and, Muotri A. R., (2012) Evidence for premature aging due to oxidative stress in iPSCs from Cockayne syndrome. Hum. Mol. Genet. 21, 3825-3834.
4. Bassik M. C., Kampmann M., Lebbink R. J., et al,. (2013) A systematic mammalian genetic interaction map reveals pathways underlying ricin susceptibility. Cell 152, 909-922.
5. Bellin M., Marchetto M. C., Gage F. H., and, Mummery C. L., (2012) Induced pluripotent stem cells: the new patient?. Nat. Rev. Mol. Cell Biol. 13, 713-726.
6. Benraiss A., Toner M. J., Xu Q., et al,. (2013) Sustained mobilization of endogenous neural progenitors delays disease progression in a transgenic model of Huntington's disease. Cell Stem Cell 12, 787-799.
7. Bilican B., Serio A., Barmada S. J., et al,. (2012) Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc. Natl Acad. Sci. USA 109, 5803-5808.
8. Brennand K. J., Simone A., Jou J., et al,. (2011) Modelling schizophrenia using human induced pluripotent stem cells. Nature 473, 221-225.
9. Caiazzo M., Dell'anno M. T., Dvoretskova E., et al,. (2011) Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476, 224-227.
10. Camnasio S., Delli Carri A., Lombardo A., et al,. (2012) 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. 46, 41-51.
11. Chambers S. M., Fasano C. A., Papapetrou E. P., Tomishima M., Sadelain M., and, Studer L., (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280.
12. Chang T., Zheng W., Tsark W., Bates S., Huang H., Lin R. J., and, Yee J. K., (2011) Brief report: phenotypic rescue of induced pluripotent stem cell-derived motoneurons of a spinal muscular atrophy patient. Stem Cells 29, 2090-2093.
13. Cheung A. Y., Horvath L. M., Grafodatskaya D., Pasceri P., Weksberg R., Hotta A., Carrel L., and, Ellis J., (2011) Isolation of MECP2-null Rett Syndrome patient hiPS cells and isogenic controls through X-chromosome inactivation. Hum. Mol. Genet. 20, 2103-2115.
14. Chiang C. H., Su Y., Wen Z., Yoritomo N., Ross C. A., Margolis R. L., Song H., and, Ming G. L., (2011) Integration-free induced pluripotent stem cells derived from schizophrenia patients with a DISC1 mutation. Mol. Psychiatry 16, 358-360.
15. Cong L., Ran F. A., Cox D., et al,. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823.
16. Cooper O., Seo H., Andrabi S,. et al. (2012) Pharmacological rescue of mitochondrial deficits in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci. Transl. Med. 4, 141ra190.
17. Crompton L. A., Byrne M. L., Taylor H., et al,. (2013) Stepwise, non-adherent differentiation of human pluripotent stem cells to generate basal forebrain cholinergic neurons via hedgehog signaling. Stem Cell Res. 11, 1206-1221.
18. Devine M. J., Ryten M., Vodicka P., et al,. (2011) Parkinson's disease induced pluripotent stem cells with triplication of the alpha-synuclein locus. Nat. Commun. 2, 440.
19. Dimos J. T., Rodolfa K. T., Niakan K. K., et al,. (2008) Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321, 1218-1221.
20. Ebert A. D., Yu J., Rose F. F., Jr, Mattis V. B., Lorson C. L., Thomson J. A., and, Svendsen C. N., (2009) Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457, 277-280.
21. Egawa N., Kitaoka S., Tsukita K,. et al. (2012) Drug screening for ALS using patient-specific induced pluripotent stem cells. Sci. Transl. Med. 4, 145ra104.
22. Farrer M., Chan P., Chen R., et al,. (2001) Lewy bodies and parkinsonism in families with parkin mutations. Ann. Neurol. 50, 293-300.
23. Fasano C. A., Chambers S. M., Lee G., Tomishima M. J., and, Studer L., (2010) Efficient derivation of functional floor plate tissue from human embryonic stem cells. Cell Stem Cell 6, 336-347.
24. HD iPSC Consortium. (2012) Induced pluripotent stem cells from patients with Huntington's disease show cag-repeat-expansion-associated phenotypes. Cell Stem Cell 11, 264-278.
25. Higurashi N., Uchida T., Christoph L., et al,. (2013) A human Dravet syndrome model from patient induced pluripotent stem cells. Mol. Brain 6, 19.
26. Imaizumi Y., Okada Y., Akamatsu W., et al,. (2012) Mitochondrial dysfunction associated with increased oxidative stress and alpha-synuclein accumulation in PARK2 iPSC-derived neurons and postmortem brain tissue. Mol. Brain 5, 35.
27. Israel M. A., Yuan S. H., Bardy C., et al,. (2012) Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482, 216-220.
28. Jang J., Kang H. C., Kim H. S., et al,. (2011) Induced pluripotent stem cell models from X-linked adrenoleukodystrophy patients. Ann. Neurol. 70, 402-409.
29. Jang M. H., Bonaguidi M. A., Kitabatake Y., et al,. (2013) Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell 12, 215-223.
30. Jeon I., Lee N., Li J. Y., et al,. (2012) Neuronal properties, in vivo effects, and pathology of a Huntington's disease patient-derived induced pluripotent stem cells. Stem Cells 30, 2054-2062.
31. Jiang H., Ren Y., Yuen E. Y., et al,. (2012) Parkin controls dopamine utilization in human midbrain dopaminergic neurons derived from induced pluripotent stem cells. Nat. Commun. 3, 668.
32. Jiao J., Yang Y., Shi Y., et al,. (2013) Modeling Dravet syndrome using induced pluripotent stem cells (iPSCs) and directly converted neurons. Hum. Mol. Genet. 22, 4241-4252.
33. Juopperi T. A., Kim W. R., Chiang C. H., Yu H., Margolis R. L., Ross C. A., Ming G. L., and, Song H., (2012) Astrocytes generated from patient induced pluripotent stem cells recapitulate features of Huntington's disease patient cells. Mol. Brain 5, 17.
34. Kano S., Colantuoni C., Han F., et al,. (2013) Genome-wide profiling of multiple histone methylations in olfactory cells: further implications for cellular susceptibility to oxidative stress in schizophrenia. Mol. Psychiatry 18, 740-742.
35. Kawasaki H., Mizuseki K., Nishikawa S., Kaneko S., Kuwana Y., Nakanishi S., Nishikawa S. I., and, Sasai Y., (2000) Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40.
36. Koch P., Breuer P., Peitz M., et al,. (2011) Excitation-induced ataxin-3 aggregation in neurons from patients with Machado-Joseph disease. Nature 480, 543-546.
37. Kondo T., Asai M., Tsukita K., et al,. (2013) Modeling Alzheimer's disease with iPSCs reveals stress phenotypes associated with intracellular abeta and differential drug responsiveness. Cell Stem Cell 12, 487-496.
38. Kriks S., Shim J. W., Piao J., et al,. (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551.
39. Lee G., Papapetrou E. P., Kim H., et al,. (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461, 402-406.
40. Lee G., Ramirez C. N., Kim H., et al,. (2012) Large-scale screening using familial dysautonomia induced pluripotent stem cells identifies compounds that rescue IKBKAP expression. Nat. Biotechnol. 30, 1244-1248.
41. Li X. J., Du Z. W., Zarnowska E. D., Pankratz M., Hansen L. O., Pearce R. A., and, Zhang S. C., (2005) Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 23, 215-221.
42. Li L. B., Chang K. H., Wang P. R., Hirata R. K., Papayannopoulou T., and, Russell D. W., (2012) Trisomy correction in down syndrome induced pluripotent stem cells. Cell Stem Cell 11, 615-619.
43. Liu G. H., Qu J., Suzuki K., et al,. (2012a) Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 491, 603-607.
44. Liu J., Koscielska K. A., Cao Z., et al,. (2012b) Signaling defects in iPSC-derived fragile X premutation neurons. Hum. Mol. Genet. 21, 3795-3805.
45. Liu Y., Liu H., Sauvey C., Yao L., Zarnowska E. D., and, Zhang S. C., (2013a) Directed differentiation of forebrain GABA interneurons from human pluripotent stem cells. Nat. Protoc. 8, 1670-1679.
46. Liu Y., Lopez-Santiago L. F., Yuan Y., et al,. (2013b) Dravet syndrome patient-derived neurons suggest a novel epilepsy mechanism. Ann. Neurol. 74, 128-139.
47. Mackay-Sim A., (2013) Patient-derived stem cells: pathways to drug discovery for brain diseases. Front. Cell Neurosci. 7, 29.
48. Mali P., Yang L., Esvelt K. M., Aach J., Guell M., DiCarlo J. E., Norville J. E., and, Church G. M., (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826.
49. Marchetto M. C., Carromeu C., Acab A., Yu D., Yeo G. W., Mu Y., Chen G., Gage F. H., and, Muotri A. R., (2010) A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143, 527-539.
50. Matsuda N., Sato S., Shiba K., et al,. (2010) PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J. Cell Biol. 189, 211-221.
51. Merkle F. T., and, Eggan K., (2013) Modeling human disease with pluripotent stem cells: from genome association to function. Cell Stem Cell 12, 656-668.
52. Miller J. C., Tan S., Qiao G., et al,. (2011) A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol. 29, 143-148.
53. Mitne-Neto M., Machado-Costa M., Marchetto M. C., et al,. (2011) Downregulation of VAPB expression in motor neurons derived from induced pluripotent stem cells of ALS8 patients. Hum. Mol. Genet. 20, 3642-3652.
54. Muotri A. R., Marchetto M. C., Coufal N. G., Oefner R., Yeo G., Nakashima K., and, Gage F. H., (2010) L1 retrotransposition in neurons is modulated by MeCP2. Nature 468, 443-446.
55. Narendra D., Tanaka A., Suen D. F., and, Youle R. J., (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183, 795-803.
56. Nguyen H. N., Byers B., Cord B., et al,. (2011) LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 8, 267-280.
57. Nihei Y., Ito D., Okada Y., Akamatsu W., Yagi T., Yoshizaki T., Okano H., and, Suzuki N., (2013) Enhanced aggregation of androgen receptor in induced pluripotent stem cell-derived neurons from spinal and bulbar muscular atrophy. J. Biol. Chem. 288, 8043-8052.
58. Okada Y., Shimazaki T., Sobue G., and, Okano H., (2004) Retinoic-acid-concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev. Biol. 275, 124-142.
59. Park I. H., Arora N., Huo H., et al,. (2008) Disease-specific induced pluripotent stem cells. Cell 134, 877-886.
60. Patani R., Lewis P. A., Trabzuni D., et al,. (2012) Investigating the utility of human embryonic stem cell-derived neurons to model ageing and neurodegenerative disease using whole-genome gene expression and splicing analysis. J. Neurochem. 122, 738-751.
61. Paulsen Bda S., de Moraes Maciel R., Galina A., et al,. (2012) Altered oxygen metabolism associated to neurogenesis of induced pluripotent stem cells derived from a schizophrenic patient. Cell Transplant. 21, 1547-1559.
62. Pedrosa E., Sandler V., Shah A., Carroll R., Chang C., Rockowitz S., Guo X., Zheng D., and, Lachman H. M., (2011) Development of patient-specific neurons in schizophrenia using induced pluripotent stem cells. J. Neurogenet. 25, 88-103.
63. Rakovic A., Shurkewitsch K., Seibler P., Grunewald A., Zanon A., Hagenah J., Krainc D., and, Klein C., (2012) PTEN-induced putative kinase 1 (PINK1)-dependent ubiquitination of endogenous Parkin attenuates mitophagy: study in human primary fibroblasts and induced pluripotent stem (iPS) cell-derived neurons. J. Biol. Chem. 288, 2223-2237.
64. Reinhardt P., Schmid B., Burbulla L. F., et al,. (2013) Genetic correction of a LRRK2 mutation in human iPSCs links Parkinsonian neurodegeneration to ERK-dependent changes in gene expression. Cell Stem Cell 12, 354-367.
65. Ricciardi S., Ungaro F., Hambrock M., et al,. (2012) CDKL5 ensures excitatory synapse stability by reinforcing NGL-1-PSD95 interaction in the postsynaptic compartment and is impaired in patient iPSC-derived neurons. Nat. Cell Biol. 14, 911-923.
66. Robinton D. A., and, Daley G. Q., (2012) The promise of induced pluripotent stem cells in research and therapy. Nature 481, 295-305.
67. Sanchez-Danes A., Richaud-Patin Y., Carballo-Carbajal I., et al,. (2012) Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol. Med. 4, 380-395.
68. Sawa A., and, Cascella N. G., (2009) Peripheral olfactory system for clinical and basic psychiatry: a promising entry point to the mystery of brain mechanism and biomarker identification in schizophrenia. Am. J. Psychiatry 166, 137-139.
69. Seibler P., Graziotto J., Jeong H., Simunovic F., Klein C., and, Krainc D., (2011) Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J. Neurosci. 31, 5970-5976.
70. Shults C. W., (2006) Lewy bodies. Proc. Natl Acad. Sci. USA 103, 1661-1668.
71. Suzuki K., Mitsui K., Aizawa E., et al,. (2008) Highly efficient transient gene expression and gene targeting in primate embryonic stem cells with helper-dependent adenoviral vectors. Proc. Natl Acad. Sci. USA 105, 13781-13786.
72. Takahashi K., and, Yamanaka S., (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
73. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., and, Yamanaka S., (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872.
74. Urbach A., Bar-Nur O., Daley G. Q., and, Benvenisty N., (2010) Differential modeling of fragile X syndrome by human embryonic stem cells and induced pluripotent stem cells. Cell Stem Cell 6, 407-411.
75. Venkateshappa C., Harish G., Mythri R. B., Mahadevan A., Bharath M. M., and, Shankar S. K., (2012) Increased oxidative damage and decreased antioxidant function in aging human substantia nigra compared to striatum: implications for Parkinson's disease. Neurochem. Res. 37, 358-369.
76. Vierbuchen T., Ostermeier A., Pang Z. P., Kokubu Y., Sudhof T. C., and, Wernig M,. (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463, 1035-1041.
77. Weick J. P., Held D. L., Bonadurer G. F. 3rd, et al,. (2013) Deficits in human trisomy 21 iPSCs and neurons. Proc. Natl Acad. Sci. USA 110, 9962-9967.
78. Yagi T., Ito D., Okada Y., Akamatsu W., Nihei Y., Yoshizaki T., Yamanaka S., Okano H., and, Suzuki N., (2011) Modeling familial Alzheimer's disease with induced pluripotent stem cells. Hum. Mol. Genet. 20, 4530-4539.
79. Zhang N., An M. C., Montoro D., and, Ellerby L. M,. (2010) Characterization of human Huntington's disease cell model from induced pluripotent stem cells. PLoS Curr. 2, RRN1193.
80. Zhang J., Lian Q., Zhu G., et al,. (2011) A human iPSC model of Hutchinson Gilford Progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8, 31-45.
81. Zhang Y., Pak C., Han Y., et al,. (2013) Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78, 785-798.
82. Zhou H., Wu S., Joo J. Y., et al,. (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4, 381-384.