Developmentally coordinated extrinsic signals drive human pluripotent stem cell differentiation toward authentic DARPP-32+ medium-sized spiny neurons

Development (Cambridge)

Volumn 140, Issue 2, 2013, Pages 301-312

  Carri, Alessia Delli ^a   Onorati, Marco ^a   Lelos, Mariah J ^b   Castiglioni, Valentina ^a   Faedo, Andrea ^a   Menon, Ramesh ^c   Camnasio, Stefano ^a   Vuono, Romina ^d   Spaiardi, Paolo ^e   Talpo, Francesca ^e   Toselli, Mauro ^e   Martino, Gianvito ^c   Barker, Roger A ^d   Dunnett, Stephen B ^b   Biella, Gerardo ^e   Cattaneo, Elena ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF PAVIA   (Italy)

Author keywords

DARPP 32 (PPP1R1B); Directed differentiation; Human embryonic stem cells; Huntington's disease; Medium spiny neurons; Striatal neuronal differentiation

Indexed keywords

ADENOSINE A2A RECEPTOR; CALBINDIN; DOPAMINE; PHOSPHOPROTEIN DARPP 32; QUINOLINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; FETUS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; HUNTINGTON CHOREA; IMMUNODETECTION; IN VIVO STUDY; NERVE CELL; NEUROMODULATION; NONHUMAN; PLURIPOTENT STEM CELL; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; TELENCEPHALON;

ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL LINEAGE; CELL SURVIVAL; CELL TRANSPLANTATION; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; EMBRYONIC STEM CELLS; FEMALE; FIBROBLASTS; FLOW CYTOMETRY; GABAERGIC NEURONS; HUMANS; HUNTINGTON DISEASE; MICE; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PATCH-CLAMP TECHNIQUES; PLURIPOTENT STEM CELLS; QUINOLINIC ACID; RATS; RNA; STEM CELLS; TIME FACTORS;

RATTUS;

EID: 84871586691     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.084608     Document Type: Article

References (67)

1. Appolloni, I., Calzolari, F., Corte, G., Perris, R. and Malatesta, P. 2008. Six3 controls the neural progenitor status in the murine CNS. Cereb. Cortex 18, 553-562.
2. Arlotta, P., Molyneaux, B. J., Jabaudon, D., Yoshida, Y. and Macklis, J. D. 2008. Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J. Neurosci. 28, 622-632.
3. Aubry, L., Bugi, A., Lefort, N., Rousseau, F., Peschanski, M. and 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. USA 105, 16707-16712.
4. Beaulieu, J. M. and Gainetdinov, R. R. 2011. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol. Rev. 63, 182-217.
5. Camnasio, S., Carri, A. D., Lombardo, A., Grad, I., Mariotti, C., Castucci, A., Rozell, B., Riso, P. L., Castiglioni, V., Zuccato, C. 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.
6. Campbell, K. 2003. Dorsal-ventral patterning in the mammalian telencephalon. Curr. Opin. Neurobiol. 13, 50-56.
7. 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.
8. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. 1996. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
9. Danjo, T., Eiraku, M., Muguruma, K., Watanabe, K., Kawada, M., Yanagawa, Y., Rubenstein, J. L. and Sasai, Y. 2011. Subregional specification of embryonic stem cell-derived ventral telencephalic tissues by timed and combinatory treatment with extrinsic signals. J. Neurosci. 31, 1919-1933.
10. Deacon, T. W., Pakzaban, P. and Isacson, O. 1994. The lateral ganglionic eminence is the origin of cells committed to striatal phenotypes: neural transplantation and developmental evidence. Brain Res. 668, 211-219.
11. Elkabetz, Y., Panagiotakos, G., Al Shamy, G., Socci, N. D., Tabar, V. and Studer, L. 2008. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 22, 152-165.
12. Ericson, J., Muhr, J., Jessell, T. M. and Edlund, T. 1995. Sonic hedgehog: a common signal for ventral patterning along the rostrocaudal axis of the neural tube. Int. J. Dev. Biol. 39, 809-816.
13. Ericsson, J., Silberberg, G., Robertson, B., Wikstrom, M. A. and Grillner, S. 2011. Striatal cellular properties conserved from lampreys to mammals. J. Physiol. 589, 2979-2992.
14. Fuccillo, M., Rallu, M., McMahon, A. P. and Fishell, G. 2004. Temporal requirement for hedgehog signaling in ventral telencephalic patterning. Development 131, 5031-5040.
15. Gaspard, N. and Vanderhaeghen, P. 2010. From stem cells to neural networks: recent advances and perspectives for neurodevelopmental disorders. Dev. Med. Child Neurol. 53, 13-17.
16. Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., Schiffmann, S. N. et al. 2008. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357.
17. Girault, J. A., Walaas, S. I., Hemmings, H. C., Jr and Greengard, P. 1990. ARPP-21, a cAMP-regulated phosphoprotein enriched in dopamine-innervated brain regions: tissue distribution and regulation of phosphorylation in rat brain. Neuroscience 37, 317-325.
18. Hemmati-Brivanlou, A., Kelly, O. G. and Melton, D. A. 1994. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295.
19. Itsykson, P., Ilouz, N., Turetsky, T., Goldstein, R. S., Pera, M. F., Fishbein, I., Segal, M. and Reubinoff, B. E. 2005. Derivation of neural precursors from human embryonic stem cells in the presence of noggin. Mol. Cell. Neurosci. 30, 24-36.
20. Jiang, Z. G. and North, R. A. 1991. Membrane properties and synaptic responses of rat striatal neurones in vitro. J. Physiol. 443, 533-553.
21. Kang, H. J., Kawasawa, Y. I., Cheng, F., Zhu, Y., Xu, X., Li, M., Sousa, A. M., Pletikos, M., Meyer, K. A., Sedmak, G. et al. 2011. Spatio-temporal transcriptome of the human brain. Nature 478, 483-489.
22. Koch, P., Opitz, T., Steinbeck, J. A., Ladewig, J. and 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. USA 106, 3225-3230.
23. Kohtz, J. D., Baker, D. P., Corte, G. and Fishell, G. 1998. Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to sonic hedgehog. Development 125, 5079-5089.
24. Kreitzer, A. C. 2009. Physiology and pharmacology of striatal neurons. Annu. Rev. Neurosci. 32, 127-147.
25. Kriks, S., Shim, J. W., Piao, J., Ganat, Y. M., Wakeman, D. R., Xie, Z., Carrillo-Reid, L., Auyeung, G., Antonacci, C., Buch, A. et al. 2011. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551.
26. Kuzhikandathil, E. V., Yu, W. and Oxford, G. S. 1998. Human dopamine D3 and D2L receptors couple to inward rectifier potassium channels in mammalian cell lines. Mol. Cell. Neurosci. 12, 390-402.
27. Lavine, N., Ethier, N., Oak, J. N., Pei, L., Liu, F., Trieu, P., Rebois, R. V., Bouvier, M., Hebert, T. E. and Van Tol, H. H. 2002. G protein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J. Biol. Chem. 277, 46010-46019.
28. Li, X. J., Zhang, X., Johnson, M. A., Wang, Z. B., Lavaute, T. and Zhang, S. C. 2009. Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 136, 4055-4063.
29. Liu, H. and Zhang, S. C. 2011. Specification of neuronal and glial subtypes from human pluripotent stem cells. Cell. Mol. Life Sci. 68, 3995-4008.
30. Lupo, G., Harris, W. A. and Lewis, K. E. 2006. Mechanisms of ventral patterning in the vertebrate nervous system. Nat. Rev. Neurosci. 7, 103-114.
31. Ma, L., Hu, B., Liu, Y., Vermilyea, S. C., Liu, H., Gao, L., Sun, Y., Zhang, X. and Zhang, S. C. 2012. Human embryonic stem cell-derived GABA neurons correct locomotion deficits in quinolinic acid-lesioned mice. Cell Stem Cell 10, 455-464.
32. Manuel, M., Martynoga, B., Yu, T., West, J. D., Mason, J. O. and Price, D. J. 2010. The transcription factor Foxg1 regulates the competence of telencephalic cells to adopt subpallial fates in mice. Development 137, 487-497.
33. Marullo, M., Zuccato, C., Mariotti, C., Lahiri, N., Tabrizi, S. J., Di Donato, S. and Cattaneo, E. 2010. Expressed Alu repeats as a novel, reliable tool for normalization of real-time quantitative RT-PCR data. Genome Biol. 11, R9.
34. Mauri, M., Lentini, D., Gravati, M., Foudah, D., Biella, G., Costa, B., Toselli, M., Parenti, M. and Coco, S. 2012. Mesenchymal stem cells enhance GABAergic transmission in co-cultured hippocampal neurons. Mol. Cell. Neurosci. 49, 395-405.
35. Nat, R. and Dechant, G. 2011. Milestones of directed differentiation of mouse and human embryonic stem cells into telencephalic neurons based on neural development in vivo. Stem Cells Dev. 20, 947-958.
36. Nieuwkoop, P. D. 1952. Activation and organization of the central nervous system in amphibians. J. Exp. Zool. 120, 33-81.
37. Nisenbaum, E. S., Wilson, C. J., Foehring, R. C. and Surmeier, D. J. 1996. Isolation and characterization of a persistent potassium current in neostriatal neurons. J. Neurophysiol. 76, 1180-1194.
38. Nogales-Cadenas, R., Carmona-Saez, P., Vazquez, M., Vicente, C., Yang, X., Tirado, F., Carazo, J. M. and Pascual-Montano, A. 2009. GeneCodis: interpreting gene lists through enrichment analysis and integration of diverse biological information. Nucleic Acids Res. 37, W317-W322.
39. Olsson, M., Campbell, K., Wictorin, K. and Bjorklund, A. 1995. Projection neurons in fetal striatal transplants are predominantly derived from the lateral ganglionic eminence. Neuroscience 69, 1169-1182.
40. Onorati, M., Binetti, M., Conti, L., Camnasio, S., Calabrese, G., Albieri, I., Di Febo, F., Toselli, M., Biella, G., Martynoga, B. et al. 2011. Preservation of positional identity in fetus-derived neural stem (NS) cells from different mouse central nervous system compartments. Cell. Mol. Life Sci. 68, 1769-1783.
41. Ouimet, C. C., Miller, P. E., Hemmings, H. C., Jr, Walaas, S. I. and Greengard, P. 1984. DARPP-32, a dopamine-and adenosine 3':5'-monophosphateregulated phosphoprotein enriched in dopamine-innervated brain regions. III. Immunocytochemical localization. J. Neurosci. 4, 111-124.
42. Ouimet, C. C., Langley-Gullion, K. C. and Greengard, P. 1998. Quantitative immunocytochemistry of DARPP-32-expressing neurons in the rat caudatoputamen. Brain Res. 808, 8-12.
43. Pankratz, M. T., Li, X. J., Lavaute, T. M., Lyons, E. A., Chen, X. and Zhang, S. C. 2007. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 25, 1511-1520.
44. Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A. and Quackenbush, J. 2006. TM4 microarray software suite. Methods Enzymol. 411, 134-193.
45. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L. K. and De Robertis, E. M. 1994. Xenopus chordin: a novel dorsalizing factor activated by organizerspecific homeobox genes. Cell 79, 779-790.
46. Schuurmans, C. and Guillemot, F. 2002. Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr. Opin. Neurobiol. 12, 26-34.
47. Shen, W., Hernandez-Lopez, S., Tkatch, T., Held, J. E. and Surmeier, D. J. 2004. Kv1.2-containing K+ channels regulate subthreshold excitability of striatal medium spiny neurons. J. Neurophysiol. 91, 1337-1349.
48. Shi, Y., Kirwan, P., Smith, J., Robinson, H. P. and Livesey, F. J. 2012. Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat. Neurosci. 15, 477-486.
49. Shimamura, K. and Rubenstein, J. L. 1997. Inductive interactions direct early regionalization of the mouse forebrain. Development 124, 2709-2718.
50. Smith, W. C. and Harland, R. M. 1992. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840.
51. Smith, Y., Bevan, M. D., Shink, E. and Bolam, J. P. 1998. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86, 353-387.
52. Smyth, G. K. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3.
53. Stern, C. D. 2001. Initial patterning of the central nervous system: how many organizers? Nat. Rev. Neurosci. 2, 92-98.
54. Surmeier, D. J., Bargas, J. and Kitai, S. T. 1989. Two types of A-current differing in voltage-dependence are expressed by neurons of the rat neostriatum. Neurosci. Lett. 103, 331-337.
55. Surmeier, D. J., Stefani, A., Foehring, R. C. and Kitai, S. T. 1991. Developmental regulation of a slowly-inactivating potassium conductance in rat neostriatal neurons. Neurosci. Lett. 122, 41-46.
56. The 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.
57. Torres, E. M., Dowd, E. and Dunnett, S. B. 2008. Recovery of functional deficits following early donor age ventral mesencephalic grafts in a rat model of Parkinson's disease. Neuroscience 154, 631-640.
58. Ungerstedt, U. and Arbuthnott, G. W. 1970. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res. 24, 485-493.
59. Valenzuela, D. M., Economides, A. N., Rojas, E., Lamb, T. M., Nunez, L., Jones, P., Lp, N. Y., Espinosa, R., 3rd, Brannan, C. I., Gilbert, D. J. et al. 1995. Identification of mammalian noggin and its expression in the adult nervous system. J. Neurosci. 15, 6077-6084.
60. Wang, H. F. and Liu, F. C. 2001. Developmental restriction of the LIM homeodomain transcription factor Islet-1 expression to cholinergic neurons in the rat striatum. Neuroscience 103, 999-1016.
61. Watanabe, K., Kamiya, D., Nishiyama, A., Katayama, T., Nozaki, S., Kawasaki, H., Watanabe, Y., Mizuseki, K. and Sasai, Y. 2005. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat. Neurosci. 8, 288-296.
62. Xu, Q., Guo, L., Moore, H., Waclaw, R. R., Campbell, K. and Anderson, S. A. 2010. Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 65, 328-340.
63. Zhang, S. C., Wernig, M., Duncan, I. D., Brustle, O. and Thomson, J. A. 2001. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133.
64. 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.
65. Zhang, X., Huang, C. T., Chen, J., Pankratz, M. T., Xi, J., Li, J., Yang, Y., Lavaute, T. M., Li, X. J., Ayala, M. et al. 2010. Pax6 is a human neuroectoderm cell fate determinant. Cell Stem Cell 7, 90-100.
66. Zhou, J., Su, P., Li, D., Tsang, S., Duan, E. and Wang, F. 2010. High-efficiency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor beta superfamily receptors. Stem Cells 28, 1741-1750.
67. Zuccato, C., Valenza, M. and Cattaneo, E. 2010. Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 90, 905-981.