1,892
Views
9
CrossRef citations to date
0
Altmetric
Review Article

Using human induced pluripotent stem cells to model cerebellar disease: Hope and hype

, , , , &
Pages 95-102 | Received 27 Feb 2015, Accepted 18 May 2015, Published online: 12 Aug 2015

References

  • Anand, B. K., Malhotra, C. L., Singh, B., & Dua, S. (1959). Cerebellar projections to limbic system. J Neurophysiol, 22, 451–457.
  • Arseni, C., & Ciurea, A. V. (1981). Statistical survey of 276 cases of medulloblastoma (1935–1978). Acta Neurochir, 57, 159–162.
  • Aubry, L., Bugi, A., Lefort, N., Rousseau, F., Peschanski, M., & Perrier, A. L. (2008). Striatal progenitors derived from human ES cells mature into DARPP32 neurons in vitro and in quinolinic acid-lesioned rats. Proc Natl Acad Sci U S A, 105, 16707–16712.
  • Ausubel, L. J., Lopez, P. M., & Couture, L. A. (2011). GMP scale-up and banking of pluripotent stem cells for cellular therapy applications. Methods Mol Biol, 767, 147–159.
  • Azevedo, F. A., Carvalho, L. R., Grinberg, L. T., Farfel, J. M., Ferretti, R. E., Leite, R. E., et al. (2009). Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J Comp Neurol, 513, 532–541.
  • Bellin, M., Marchetto, M. C., Gage, F. H., & Mummery, C. L. (2012). Induced pluripotent stem cells: The new patient? Nat Rev Mol Cell Biol, 13, 713–726.
  • Bird, M. J., Needham, K., Frazier, A. E., van Rooijen, J., Leung, J., Hough, S., et al. (2014). Functional characterization of Friedreich ataxia iPS-derived neuronal progenitors and their integration in the adult brain. PLoS one, 9, e101718.
  • Buffo, A., & Rossi, F. (2013). Origin, lineage and function of cerebellar glia. Prog Neurobiol, 109, 42–63.
  • Cao, L., Tan, L., Jiang, T., Zhu, X. C., & Yu, J. T. (2014). Induced pluripotent stem cells for disease modeling and drug discovery in neurodegenerative diseases. Mol Neurobiol, Epub ahead of print.
  • Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M., & Studer, L. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol, 27, 275–280.
  • Chambers, S. M., Qi, Y., Mica, Y., Lee, G., Zhang, X. J., Niu, L., et al. (2012). Combined small-molecule inhibition accelerates developmental timing and converts human pluripotent stem cells into nociceptors. Nat Biotechnol, 30, 715–720.
  • Cooper, O., Seo, H., Andrabi, S., Guardia-Laguarta, C., Graziotto, J., Sundberg, M., et al. (2012). Pharmacological rescue of mitochondrial deficits in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci Transl Med, 4, 141ra90.
  • Corti, S., Nizzardo, M., Simone, C., Falcone, M., Nardini, M., Ronchi, D., et al. (2012). Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy. Sci Transl Med, 4, 165ra2.
  • Cyranoski, D. (2013). Stem cells cruise to clinic. Nature, 494, 413.
  • De Zeeuw, C. I., & Berrebi, A. S. (1995). Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci, 7, 2322–2333.
  • Delli Carri, A., Onorati, M., Lelos, M. J., Castiglioni, V., Faedo, A., Menon, R., et al. (2013). Developmentally coordinated extrinsic signals drive human pluripotent stem cell differentiation toward authentic DARPP-32 + medium-sized spiny neurons. Development, 140, 301–312.
  • Devlin, A. C., Burr, K., Borooah, S., Foster, J. D., Cleary, E. M., Geti, I., et al. (2015). Human iPSC-derived motoneurons harbouring TARDBP or C9ORF72 ALS mutations are dysfunctional despite maintaining viability. Nat commun, 6, 5999.
  • Dimos, J. T., Rodolfa, K. T., Niakan, K. K., Weisenthal, L. M., Mitsumoto, H., Chung, W., et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science, 321, 1218–1221.
  • Efthymiou, A., Shaltouki, A., Steiner, J. P., Jha, B., Heman-Ackah, S. M., Swistowski, A., et al. (2014). Functional screening assays with neurons generated from pluripotent stem cell-derived neural stem cells. J Biomol Screen, 19, 32–43.
  • Eigentler, A., Boesch, S., Schneider, R., Dechant, G., & Nat, R. (2013). Induced pluripotent stem cells from friedreich ataxia patients fail to upregulate frataxin during in vitro differentiation to peripheral sensory neurons. Stem Cells Dev, 22, 3271–3282.
  • Erceg, S., Lukovic, D., Moreno-Manzano, V., Stojkovic, M., & Bhattacharya, S. S. (2012). Derivation of cerebellar neurons from human pluripotent stem cells. Curr Protoc Stem Cell Biol, Chapter 1, Unit 1H 5.
  • Frantz, S. (2012). Embryonic stem cell pioneer Geron exits field, cuts losses. Nat Biotechnol, 30, 12–13.
  • Glickstein, M., Strata, P., & Voogd, J. (2009). Cerebellum: History. Neuroscience, 162, 549–559.
  • Grskovic, M., Javaherian, A., Strulovici, B., & Daley, G. Q. (2011). Induced pluripotent stem cells–opportunities for disease modelling and drug discovery. Nat Rev Drug Discov, 10, 915–929.
  • Hekman, K. E., & Gomez, C. M. (2015). The autosomal dominant spinocerebellar ataxias: Emerging mechanistic themes suggest pervasive Purkinje cell vulnerability. J Neurol Neurosurg Psychiatry, 86, 554–61.
  • Hibi, M., & Shimizu, T. (2012). Development of the cerebellum and cerebellar neural circuits. Dev Neurobiol, 72, 282–301.
  • Hick, A., Wattenhofer-Donze, M., Chintawar, S., Tropel, P., Simard, J. P., Vaucamps, N., et al. (2013). Neurons and cardiomyocytes derived from induced pluripotent stem cells as a model for mitochondrial defects in Friedreich's ataxia. Dis Model Mech, 6, 608–621.
  • Hockemeyer, D., Soldner, F., Beard, C., Gao, Q., Mitalipova, M., DeKelver, R. C., et al. (2009). Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol, 27, 851–857.
  • Hockemeyer, D., Wang, H., Kiani, S., Lai, C. S., Gao, Q., Cassady, J. P., et al. (2011). Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol, 29, 731–734.
  • Hoshino, M. (2006). Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum, 5, 193–198.
  • Hou, P., Li, Y., Zhang, X., Liu, C., Guan, J., Li, H., et al. (2013). Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science, 341, 651–654.
  • Hu, B. Y., & Zhang, S. C. (2009). Differentiation of spinal motor neurons from pluripotent human stem cells. Nat Protoc, 4, 1295–1304.
  • Hunsberger, J., Efthymiou, A. G., Malik, N., Behl, M., Mead, I. L., Zeng, X., et al. (2015). Induced pluripotent stem cell models to enable in vitro models for screening in the CNS. Stem Cells Dev, Epub ahead of print.
  • Israel, M. A., Yuan, S. H., Bardy, C., Reyna, S. M., Mu, Y., Herrera, C., et al. (2012). Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature, 482, 216–220.
  • Ito, M. (1984). The modifiable neuronal network of the cerebellum. Jpn J Physiol, 34, 781–792.
  • Jeon, I., Lee, N., Li, J. Y., Park, I. H., Park, K. S., Moon, J., 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.
  • Jiang, J., Lv, W., Ye, X., Wang, L., Zhang, M., Yang, H., et al. (2013). Zscan4 promotes genomic stability during reprogramming and dramatically improves the quality of iPS cells as demonstrated by tetraploid complementation. Cell Res, 23, 92–106.
  • Kamao, H., Mandai, M., Okamoto, S., Sakai, N., Suga, A., Sugita, S., et al. (2014). Characterization of human induced pluripotent stem cell-derived retinal pigment epithelium cell sheets aiming for clinical application. Stem Cell Rep, 2, 205–218.
  • Koch, P., Breuer, P., Peitz, M., Jungverdorben, J., Kesavan, J., Poppe, D., et al. (2011). Excitation-induced ataxin-3 aggregation in neurons from patients with Machado-Joseph disease. Nature, 480, 543–546.
  • Koch, P., Opitz, T., Steinbeck, J. A., Ladewig, J., & Brustle, O. (2009). A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration. Proc Natl Acad Sci U S A, 106, 3225–3230.
  • Kordower, J. H., Chu, Y., Hauser, R. A., Freeman, T. B., & Olanow, C. W. (2008). Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat Med, 14, 504–506.
  • Kriks, S., Shim, J. W., Piao, J., Ganat, Y. M., Wakeman, D. R., Xie, Z., et al. (2011). Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature, 480, 547–551.
  • Ku, S., Soragni, E., Campau, E., Thomas, E. A., Altun, G., Laurent, L. C., et al. (2010). Friedreich's ataxia induced pluripotent stem cells model intergenerational GAATTC triplet repeat instability. Cell Stem Cell, 7, 631–637.
  • Ladewig, J., Koch, P., & Brustle, O. (2013). Leveling Waddington: The emergence of direct programming and the loss of cell fate hierarchies. Nat Rev Mol Cell Biol, 14, 225–236.
  • Lancaster, M. A., Renner, M., Martin, C. A., Wenzel, D., Bicknell, L. S., Hurles, M. E., et al. (2013). Cerebral organoids model human brain development and microcephaly. Nature, 501, 373–379.
  • Lee, G., Papapetrou, E. P., Kim, H., Chambers, S. M., Tomishima, M. J., Fasano, C. A., et al. (2009). Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature, 461, 402–406.
  • Lee, K. S., Zhou, W., Scott-McKean, J. J., Emmerling, K. L., Cai, G. Y., Krah, D. L., et al. (2012). Human sensory neurons derived from induced pluripotent stem cells support varicella-zoster virus infection. PLoS one, 7, e53010.
  • Leiner, H. C. (2010). Solving the mystery of the human cerebellum. Neuropsychology Rev, 20, 229–235.
  • Li, X. J., Du, Z. W., Zarnowska, E. D., Pankratz, M., Hansen, L. O., Pearce, R. A., et al. (2005). Specification of motoneurons from human embryonic stem cells. Nat Biotechnol, 23, 215–221.
  • Li, X. J., Hu, B. Y., Jones, S. A., Zhang, Y. S., Lavaute, T., Du, Z. W., et al. (2008). Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells, 26, 886–893.
  • Malik, N., Efthymiou, A. G., Mather, K., Chester, N., Wang, X., Nath, A., et al. (2014). Compounds with species and cell type specific toxicity identified in a 2000 compound drug screen of neural stem cells and rat mixed cortical neurons. Neurotoxicology, 45, 192–200.
  • Manto, M. (2008). The cerebellum, cerebellar disorders, and cerebellar research–two centuries of discoveries. Cerebellum, 7, 505–516.
  • Marchetto, M. C., Carromeu, C., Acab, A., Yu, D., Yeo, G. W., Mu, Y., et al. (2010). A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell, 143, 527–539.
  • Mendonca, L. S., Nobrega, C., Hirai, H., Kaspar, B. K., Pereira de Almeida, L. (2015). Transplantation of cerebellar neural stem cells improves motor coordination and neuropathology in Machado-Joseph disease mice. Brain, 138, 320–335.
  • Moretti, A., Bellin, M., Welling, A., Jung, C. B., Lam, J. T., Bott-Flugel, L., et al. (2010). Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med, 363, 1397–1409.
  • Muguruma, K., Nishiyama, A., Kawakami, H., Hashimoto, K., & Sasai, Y. (2015). Self-organization of polarized cerebellar tissue in 3D culture of human pluripotent stem cells. Cell Rep, 10, 537–50.
  • Muguruma, K., Nishiyama, A., Ono, Y., Miyawaki, H., Mizuhara, E., Hori, S., et al. (2010). Ontogeny-recapitulating generation and tissue integration of ES cell-derived Purkinje cells. Nat Neurosci, 13, 1171–1180.
  • Okita, K., Matsumura, Y., Sato, Y., Okada, A., Morizane, A., Okamoto, S., et al. (2011). A more efficient method to generate integration-free human iPS cells. Nat Methods, 8, 409–412.
  • Patani, R., Hollins, A. J., Wishart, T. M., Puddifoot, C. A., Alvarez, S., de Lera, A. R., et al. (2011). Retinoid-independent motor neurogenesis from human embryonic stem cells reveals a medial columnar ground state. Nature commun, 2, 214.
  • Patani, R., Lewis, P. A., Trabzuni, D., Puddifoot, C. A., Wyllie, D. J., Walker, R., 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.
  • Perrier, A. L., Tabar, V., Barberi, T., Rubio, M. E., Bruses, J., Topf, N., et al. (2004). Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc Natl Acad Sci U S A, 101, 12543–12548.
  • Perrier, A., & Peschanski, M. (2012). How can human pluripotent stem cells help decipher and cure Huntington's disease? Cell Stem Cell, 11, 153–161.
  • Pomp, O., Brokhman, I., Ben-Dor, I., Reubinoff, B., & Goldstein, R. S. (2005). Generation of peripheral sensory and sympathetic neurons and neural crest cells from human embryonic stem cells. Stem Cells, 23, 923–930.
  • Reubinoff, B. E., Itsykson, P., Turetsky, T., Pera, M. F., Reinhartz, E., Itzik, A., et al. (2001). Neural progenitors from human embryonic stem cells. Nat Biotechnol, 19, 1134–1140.
  • Ross, C. A., & Akimov, S. S. (2014). Human-induced pluripotent stem cells: Potential for neurodegenerative diseases. Hum Mol Genet, 23, R17–26.
  • Ruigrok, T. J. (2011). Ins and outs of cerebellar modules. Cerebellum, 10, 464–474.
  • Salero, E., & Hatten, M. E. (2007). Differentiation of ES cells into cerebellar neurons. Proc Natl Acad Sci U S A, 104, 2997–3002.
  • Sanchez-Danes, A., Richaud-Patin, Y., Carballo-Carbajal, I., Jimenez-Delgado, S., Caig, C., Mora, S., 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.
  • Schlaeger, T. M., Daheron, L., Brickler, T. R., Entwisle, S., Chan, K., Cianci, A., et al. (2015). A comparison of non-integrating reprogramming methods. Nat Biotechnol, 33, 58–63.
  • Schmahmann, J. D. (1997). Rediscovery of an early concept. Int Rev Neurobiol, 41, 3–27.
  • Schondorf, D. C., Aureli, M., McAllister, F. E., Hindley, C. J., Mayer, F., Schmid, B., et al. (2014). iPSC-derived neurons from GBA1-associated Parkinson's disease patients show autophagic defects and impaired calcium homeostasis. Nat Commun, 5, 4028.
  • Schorge, S., van de Leemput, J., Singleton, A., Houlden, H., & Hardy, J. (2010). Human ataxias: A genetic dissection of inositol triphosphate receptor (ITPR1)-dependent signaling. Trends Neurosci, 33, 211–219.
  • Schwartz, R. E., Fleming, H. E., Khetani, S. R., & Bhatia, S. N. (2014). Pluripotent stem cell-derived hepatocyte-like cells. Biotechnol Adv, 32, 504–513.
  • Schwartz, S. D., Hubschman, J. P., Heilwell, G., Franco-Cardenas, V., Pan, C. K., Ostrick, R. M., et al. (2012). Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet, 379, 713–720.
  • Shi, Y., Kirwan, P., & Livesey, F. J. (2012). Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc, 7, 1836–1846.
  • Soldner, F., Laganiere, J., Cheng, A. W., Hockemeyer, D., Gao, Q., Alagappan, R., et al. (2011). Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell, 146, 318–331.
  • Strata, P. (2015). The emotional cerebellum. Cerebellum, Epub ahead of print.
  • Strick, P. L., Dum, R. P., & Fiez, J. A. (2009). Cerebellum and nonmotor function. Annu Rev Neurosci, 32, 413–434.
  • Su, H. L., Muguruma, K., Matsuo-Takasaki, M., Kengaku, M., Watanabe, K., & Sasai, Y. (2006). Generation of cerebellar neuron precursors from embryonic stem cells. Dev Biol, 290, 287–296.
  • Tabar, V., & Studer, L. (2014). Pluripotent stem cells in regenerative medicine: Challenges and recent progress. Nat Rev Genet, 15, 82–92.
  • Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861–872.
  • Ten Donkelaar, H. J., & Lammens, M. (2009). Development of the human cerebellum and its disorders. Clin Perinatol, 36, 513–530.
  • Teng, S., Liu, C., Krettek, C., & Jagodzinski, M. (2014). The application of induced pluripotent stem cells for bone regeneration: Current progress and prospects. Tissue Eng Part B Rev, 20, 328–339.
  • Timmann, D. (2012). [Contribution of the cerebellum to cognition]. Fortschr Neurol Psychiatr, 80, 44–52.
  • Valensi-Kurtz, M., Lefler, S., Cohen, M. A., Aharonowiz, M., Cohen-Kupiec, R., Sheinin, A., et al. (2010). Enriched population of PNS neurons derived from human embryonic stem cells as a platform for studying peripheral neuropathies. PLoS One, 5, e9290.
  • Vierbuchen, T., & Wernig, M. (2012). Molecular roadblocks for cellular reprogramming. Mol Cell, 47, 827–838.
  • Voogd, J. (2014). What we do not know about cerebellar systems neuroscience. Front Syst Neurosci, 8, 227.
  • Voogd, J., Gerrits, N. M., & Ruigrok, T. J. (1996). Organization of the vestibulocerebellum. Ann N Y Acad Sci, 781, 553–579.
  • Wang, S., Wang, B., Pan, N., Fu, L., Wang, C., Song, G., et al. (2015). Differentiation of human induced pluripotent stem cells to mature functional Purkinje neurons. Sci Rep, 5, 9232.
  • Warren, L., Manos, P. D., Ahfeldt, T., Loh, Y. H., Li, H., Lau, F., et al. (2010). Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell, 7, 618–630.
  • White, J. J., & Sillitoe, R. V. (2013). Development of the cerebellum: from gene expression patterns to circuit maps. Wiley Interdiscip Rev Dev Biol, 2, 149–164.
  • Woodard, C. M., Campos, B. A., Kuo, S. H., Nirenberg, M. J., Nestor, M. W., Zimmer, M., et al. (2014). iPSC-derived dopamine neurons reveal differences between monozygotic twins discordant for Parkinson's disease. Cell Rep, 9, 1173–1182.
  • Wurst, W., Bally-Cuif, L. (2001). Neural plate patterning: Upstream and downstream of the isthmic organizer. Nat Rev Neurosci, 2, 99–108.
  • Xie, Y. Z., & Zhang, R. X. (2015). Neurodegenerative diseases in a dish: The promise of iPSC technology in disease modeling and therapeutic discovery. Neurol Sci, 36, 21–27.
  • Yamanaka, S., & Blau, H. M. (2010). Nuclear reprogramming to a pluripotent state by three approaches. Nature, 465, 704–712.
  • Yan, Y., Yang, D., Zarnowska, E. D., Du, Z., Werbel, B., Valliere, C., et al. (2005). Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells, 23, 781–790.
  • Yang, Y. M., Gupta, S. K., Kim, K. J., Powers, B. E., Cerqueira, A., Wainger, B. J., et al. (2013). A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS. Cell Stem Cell, 12, 713–726.
  • Yu, J., Hu, K., Smuga-Otto, K., Tian, S., Stewart, R., Slukvin, I. I., Thomson, J. A.. (2009). Human induced pluripotent stem cells free of vector and transgene sequences. Science, 324, 797–801.
  • Zeng, X., Hunsberger, J. G., Simeonov, A., Malik, N., Pei, Y., & Rao, M. (2014). Concise review: modeling central nervous system diseases using induced pluripotent stem cells. Stem Cells Transl Med, 3, 1418–1428.
  • Zhang, S. C., Wernig, M., Duncan, I. D., Brustle, O., & Thomson, J. A. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol, 19, 1129–1133.