Efficient generation of mature cerebellar Purkinje cells from mouse embryonic stem cells

Journal of Neuroscience Research

Volumn 88, Issue 2, 2010, Pages 234-247

  Tao, Osamu ^a,b   Shimazaki, Takuya ^a   Okada, Yohei ^a,c,d   Naka, Hayato ^a   Kohda, Kazuhisa ^a   Yuzaki, Michisuke ^a   Mizusawa, Hidehiro ^b   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KEIO UNIVERSITY   (Japan)

Author keywords

Cerebellar Purkinje cells; Coculture; Mouse embryonic stem cells; SFEB

Indexed keywords

BETA TUBULIN; BONE MORPHOGENETIC PROTEIN 4; BRAIN DERIVED NEUROTROPHIC FACTOR; CALBINDIN; CALCIUM; FIBROBLAST GROWTH FACTOR 8; GLUTAMATE DECARBOXYLASE 67; LIOTHYRONINE; NEURON SPECIFIC NUCLEAR PROTEIN; NEUROTROPHIN 3; PARVALBUMIN; SODIUM; SYNAPTOPHYSIN; WNT3A PROTEIN;

ADHERENT CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELL LINE; CELL MATURATION; CELL STRUCTURE; CELL SURVIVAL; CEREBELLUM; COCULTURE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; EMBRYONIC STEM CELL; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NERVE CELL; NONHUMAN; PATCH CLAMP; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PURKINJE CELL; SPIKE; STEM CELL; SYNAPTOGENESIS; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CALCIUM; CELL LINE; CEREBELLUM; COCULTURE TECHNIQUES; CULTURE MEDIA, SERUM-FREE; EMBRYONIC STEM CELLS; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, INBRED ICR; MICE, TRANSGENIC; NEUROGENESIS; NEURONS; PURKINJE CELLS; SODIUM; SYNAPSES;

EID: 74049099790     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22208     Document Type: Article

References (69)

1. Altmann CR, Brivanlou AH 2001. Neural patterning in the vertebrate embryo. Int Rev Cytol 203:447-482.
2. Alvarez-Dolado M, Pardal R, Garcia-Verdugo JM, Fike JR, Lee HO, Pfeffer K, Lois G, Morrison SJ, Alvarez-Buylla A. 2003. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425:968-973.
3. Baptista CA, Hatten ME, Blazeski R, Mason CA. 1994. Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12:243-260.
4. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, Guo Q, Matzuk MM, Zoghbi HY. 1997. Math1 is essential for genesis of cerebellar granule neurons. Nature 390:169-172.
5. Brorson JR, Bleakman D, Gibbons SJ, Miller RJ. 1991. The properties of intracellular calcium stores in cultured rat cerebellar neurons. J Neurosci 11:4024-4043.
6. Cai C, Grabel L. 2007. Directing the differentiation of embryonic stem cells to neural stem cells. Dev Dyn 236:3255-3266.
7. Carletti B, Rossi F. 2005. Selective rather than inductive mechanisms favour specific replacement of Purkinje cells by embryonic cerebellar cells transplanted to the cerebellum of adult Purkinje cell degeneration (pcd) mice. Eur J Neurosci 22:1001-1012.
8. Carletti B, Williams IM, Leto K, Nakajima K, Magrassi L, Rossi F. 2008. Time constraints and positional cues in the developing cerebellum regulate Purkinje cell placement in the cortical architecture. Dev Biol 317:147-160.
9. + channels to rat Purkinje neuron function. J Physiol 548:53-69.
10. Fischer G. 1982. Cultivation of mouse cerebellar cells in serum free, hormonally defined media: survival of neurons. Neurosci Lett 28:325-329.
11. Gählwiler BH, Llano I. 1989. Sodium and potassium conductances in somatic membranes of rat Purkinje cells from organotypic cerebellar cultures. J Physiol 417:105-122.
12. Gallo V, Ciotti MT, Coletti A, Aloisi F, Levi G. 1982. Selective release of glutamate from cerebellar granule cells differentiating in culture. Proc Natl Acad Sci USA 79:7919-7923.
13. Gardette R, Alvarado-Mallart RM, Crepel F, Sotelo C. 1988. Electrophysiological demonstration of a synaptic integration of transplanted Purkinje cells into the cerebellum of the adult Purkinje cell degeneration mutant mouse. Neuroscience 24:777-789.
14. Gardette R, Crepel F, Alvarado-Mallart RM, Sotelo C. 1990. Fate of grafted embryonic Purkinje cells in the cerebellum of the adult "Purkinje cell degeneration" mutant mice. 2. Development of synaptic response: an in vitro study. J Comp Neurol 295:188-196.
15. Grimaldi P, Carletti B, Rossi F. 2005. Neuronal replacement and integration in the rewiring of cerebellar circuits [review]. Brain Res Rev 49:330-342.
16. Gruol DL, Franklin CL. 1987. Morphological and physiological differentiation of Purkinje neurons in cultures of rat cerebellum. J Neurosci 7:1271-1293.
17. Hashimoto M, Mikoshiba K. 2003. Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J Neurosci 23:11342-11351.
18. Herrup K, Kuemerle B. 1997. The compartmentalization of the cerebellum. Annu Rev Neurosci 20:61-90.
19. Hirai H, Launey T. 2000. The regulatory connection between the activity of granule cell NMDA receptors and dendritic differentiation of cerebellar Purkinje cells. J Neurosci 20:5217-5224.
20. Hirano T, Ohmori H. 1986. Voltage-gated and synaptic currents in rat Purkinje cells in dissociated cell cultures. Proc Natl Acad Sci USA 83:1945-1949.
21. Hirano T, Kubo Y, Wu MM. 1986. Cerebellar granule cells in culture: monosynaptic connections with Purkinje cells and ionic currents. Proc Natl Acad Sci USA 83:4957-4961.
22. Hisatsune C, Kuroda Y, Akagi T, Torashima T, Hirai H, Hashikawa T, Inoue T, Mikoshiba K. 2006. Inositol 1,4,5-triphosphate receptor type 1 in granule cells, not in Purkinje cells, regulates the dendritic morphology of Purkinje cells through brain-derived neurotrophic factor production. J Neurosci 26:10916-10924.
23. Hockberger PE, Tseng HY, Connor JA. 1989. Development of rat cerebellar Purkinje cells: electrophysiological properties following acute isolation and in long-term culture. J Neurosci 9:2258-2271.
24. Hoshino M, Nakamura S, Mori K, Kawauchi T, Terao M, Nishimura YV, Fukuda A, Fuse T, Matsuo N, Sone M, Watanabe M, Bito H, Terashima T, Wright CVE, Kawaguchi Y, Nakao K, Nabeshima Y. 2005. Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47:201-213.
25. Jessell TM. 2000. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nature Rev Genet 1:20-29.
26. Kappor R, Jaeger CB, Llinás R. 1988. Electrophysiology of the mammalian cerebellar cortex in organ culture. Neuroscience 26:493-507.
27. Kawamoto S, Niwa H, Tashiro F, Sano S, Kondoh G, Takeda J, Tabayashi K, Miyazaki J. 2000. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett 470:263-268.
28. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, Nishikawa SI, Sasai Y. 2000. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28:31-40.
29. Lärkfos L, Lindsay RM, Alderson RF. 1996. Characterization of the responses of Purkinje cells to neurotrophin treatment. J Neurochem 66:1362-1373.
30. Leto K, Carletti B, Williams IM, Magrassi L, Rossi F. 2006. Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J Neurosci 26:11682-11694.
31. Lindholm D, Castren E, Tsoulfas P, Kolbeck R, Berzaghi MP, Leingärtner CP, Tesarollo L, Parada LF, Thoernen H. 1993. Neurotrophin-3 induced by tri-iodothyronine in cerebral granule cells promotes Purkinje cell differentiation. J Cell Biol 122:443-450.
32. Llinás R, Sugimori M. 1980a. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:171-195.
33. Llinás R, Sugimori M. 1980b. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305:197-213.
34. Machold R, Fishell G. 2005. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24.
35. Marzban H, Hawkes R. 2007. Fibroblast growth factor promotes the development of deep cerebellar nuclear neurons in dissociated mouse cerebellar cultures. Brain Res 1141:25-36.
36. Metzger F, Kapfhammer JP. 2000. Protein kinase C activity modulates dendritic differentiation of rat Purkinje cells in cerebellar slice cultures. Eur J Neurosci 12:1993-2005.
37. Morrison ME, Mason CA. 1998. Granule neuron regulation of Purkinje cell development: striking a balance between neurotrophin and glutamate signaling. J Neurosci 18:3563-3573.
38. Murry CE, Keller G. 2008. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell 132:661-680.
39. Nakamura H, Sato T, Suzuki-Hirano A. 2008. Isthmus organizer for mesencephalon and metencephalon. Dev Growth Differ 50:S113-S118.
40. Oberdick J, Smeyne RJ, Mann JR, Zackson S, Morgan JI. 1990. A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. Science 248:223-226.
41. Okada Y, Shimazaki T, Sobue G, 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.
42. Okada Y, Matsumoto A, Shimazaki T, Enoki R, Koizumi A, Ishii S, Itoyama Y, Sobue G, Okano H. 2008. Spatio-temporal recapitulation of central nervous system development by murine ES cell-derived neural stem/progenitor cells. Stem cells 26:3086-3098.
43. Salero E, Hatten ME. 2007. Differentiation of ES cells into cerebellar neurons. Proc Natl Acad Sci U S A 104:2997-3002.
44. Sarna JR, Hawkes R. 2003. Patterned Purkinje cell death in the cerebellum. Prog Neurobiol 70:473-507.
45. Schilling K, Dickinson MH, Connor JA, Morgan JI. 1991. Electrical activity in cerebellar cultures determines Purkinje cell dendritic growth patterns. Neuron 7:891-902.
46. Schrenk K, Kapfhammer JP, Metzger F. 2002. Altered dendritic development of cerebellar Purkinje cells in slice cultures from protein kinase Cγ-deficient mice. Neuroscience 110:675-689.
47. Sharma RK, O'Leary TE, Fields CM, Johnson DA. 2003. Development of the outer retina in the mouse. Brain Res Dev Brain Res 145:93-105.
48. Shimada A, Mason CA, Morrison ME. 1998. TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J Neurosci 18:8559-8570.
49. Shimazaki T, Shingo T, Weiss S. 2001. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci 21:742-7653.
50. Sotelo C, Alvarado-Mallart RM. 1986. Growth and differentiation of cerebellar suspensions transplanted into the adult cerebellum of mice with heredodegenerative ataxia. Proc Natl Acad Sci U S A 83:1135-1139.
51. Sotelo C, Alvarado-Mallart RM. 1987. Reconstruction of the defective cerebellar circuitry in adult Purkinje cell degeneration mutant mice by Purkinje cell replacement through transplantation of solid embryonic implants. Neuroscience 20:1-22.
52. Sotelo C, Alvarado-Mallart RM, Gardette R, Crepel F. 1990. Fate of grafted embryonic Purkinje cells in the cerebellum of the adult "Purkinje cell degeneration" mutant mice. 1. Development of reciprocal graft-host interactions. J Comp Neurol 295:165-187.
53. Su HL, 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.
54. Suter DM, Krause KH. 2008. Neural commitment of embryonic stem cells: molecules, pathways and potential for cell therapy. J Pathol 15:355-368.
55. Tomomura M, Rice DS, Morgan JI, Yuzaki M. 2001. Purification of Purkinje cells by fluorescence cell sorting from transgenic mice that express green fluorescent protein. Eur J Neurosci 14:57-63.
56. Triarhou LC, Zhang W, Lee WH. 1995. Graft-induced restoration of function in hereditary cerebellar ataxia. Neuroreport 6:1827-1832.
57. Uusisaari M, Obata K, Knöpfel T. 2007. Morphological and eletrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol 97:901-911.
58. Wallace VA. 1999. Purkinje cell-derived sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9:445-448.
59. Wang VY, Rose MF, Zoghbe HY. 2005. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31-43.
60. Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, Kawasaki H, Watanabe Y, Mizuseki K, Sasai Y. 2005. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8:288-296.
61. Weber A, Schachner M. 1984. Maintenance of immunocytologically identi.ed Purkinje cells from mouse cerebellum in monolayer culture. Brain Res 311:119-130.
62. Wechsler-Reya RJ, Scott MP. 1999. Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron 22:103-114.
63. Weimann JM, Johansson CB, Trejo A, Blau HM. 2003. Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant. Nat Cell Biol 5:959-966.
64. Wilson L, Maden M. 2005. The mechanisms of dorsoventral patterning in the vertebrate neural tube. Dev Biol 282:1-13.
65. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blümcke I. 1996. NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44:1167-1171.
66. Ying QL, Stavridis M, Grif.ths D, Li M, Smith A. 2003. Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat Biotechnol 21:183-186.
67. Yuzaki M, Mikoshiba K, Kagawa Y. 1993. Cerebellar astrocytes specifically support the survival of Purkinje cells in culture. Biochem Biophys Res Commun 197:123-129.
68. Yuzaki M, Forrest D, Verselis LM, Sun SC, Curran T, Connor JA. 1996. Functional NMDA receptors are transiently active and support the survival of Purkinje cells in culture. J Neurosci 16:4651-4661.
69. Zhang W, Lee WH, Triarhou LC. 1996. Grafted cerebellar cells in a mouse model of hereditary ataxia express IGF-1 genes and partially restore behavioral function. Nat Med 2:65-71.