Specification of spatial identities of cerebellar neuron progenitors by ptf1a and atoh1 for proper production of GABAergic and glutamatergic neurons

Journal of Neuroscience

Volumn 34, Issue 14, 2014, Pages 4786-4800

  Yamada, Mayumi ^a   Seto, Yusuke ^a,b   Taya, Shinichiro ^a   Owa, Tomoo ^a,c   Inoue, Yukiko U ^a   Inoue, Takayoshi ^a   Kawaguchi, Yoshiya ^d   Nabeshima, Yo Ichi ^e   Hoshino, Mikio ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b WASEDA UNIVERSITY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e FOUNDATION FOR BIOMEDICAL RESEARCH AND INNOVATION   (Japan)

Author keywords

Cerebellum; Development; Identity; Neuron; Spatial; Transcription factor

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; COMPLEMENTARY DNA; GENOMIC DNA; GLUTAMATE RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; ATOH1 GENE; BRAIN DEVELOPMENT; BRDU ASSAY; CELL FUNCTION; CEREBELLUM; CONTROLLED STUDY; ELECTROPORATION; FEMALE; GABAERGIC TRANSMISSION; GENE; GENE EXPRESSION; GENOTYPE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOUSE; NERVE CELL; NEUROEPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PTF1A GENE; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SPATIAL ANALYSIS;

CEREBELLUM; DEVELOPMENT; IDENTITY; NEURON; SPATIAL; TRANSCRIPTION FACTOR;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CEREBELLUM; EMBRYO, MAMMALIAN; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMIC ACID; KI-67 ANTIGEN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NEURAL STEM CELLS; NEURONS; TRANSCRIPTION FACTORS;

EID: 84899421212     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2722-13.2014     Document Type: Article

References (50)

1. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R (1995) A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem 270:8730-8738. CrossRef Medline
2. Altman J, Bayer SA (1985) Embryonic development of the rat cerebellum. II. Translocation and regional distribution of the deep neurons. J Comp Neurol 231:27-41. CrossRef Medline
3. Aruga J, Inoue T, Hoshino J, Mikoshiba K (2002) Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22:218-225. Medline
4. Batini C, Compoint C, Buisseret-Delmas C, Daniel H, Guegan M (1992) Cerebellar nuclei and the nucleocortical projections in the rat: retrograde tracing coupled to GABA and glutamate immunohistochemistry. J Comp Neurol 315:74-84. CrossRef Medline
5. 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. CrossRef Medline
6. Chan-Palay V, Palay SL, Brown JT, Van Itallie C (1977) Sagittal organization of olivocerebellar and reticulocerebellar projections: autoradiographic studies with 35S-methionine. Exp Brain Res 30:561-576. Medline
7. De Zeeuw CI, Berrebi AS (1995) Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci 7:2322-2333. CrossRef Medline
8. Dun XP (2012) Origin of climbing fiber neurons and the definition of rhombic lip. Int J Dev Neurosci 30:391-395. CrossRef Medline
9. Engelkamp D, Rashbass P, Seawright A, van Heyningen V (1999) Role of Pax6 in development of the cerebellar system. Development 126:3585-3596. Medline
10. Englund C, Kowalczyk T, Daza RA, Dagan A, Lau C, Rose MF, Hevner RF (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 26:9184-9195. CrossRef Medline
11. Fink AJ, Englund C, Daza RA, Pham D, Lau C, Nivison M, Kowalczyk T, Hevner RF (2006) Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J Neurosci 26:3066-3076. CrossRef Medline
12. Fleming JT, He W, Hao C, Ketova T, Pan FC, Wright CC, Litingtung Y, Chiang C (2013) The Purkinje neuron acts as a central regulator of spatially and functionally distinct cerebellar precursors. Dev Cell 27:278-292. CrossRef Medline
13. Flora A, Klisch TJ, Schuster G, Zoghbi HY (2009) Deletion of Atoh1 disrupts Sonic Hedgehog signaling in the developing cerebellum and prevents medulloblastoma. Science 326:1424-1427. CrossRef Medline
14. Fujiyama T, Yamada M, Terao M, Terashima T, Hioki H, Inoue YU, Inoue T, Masuyama N, Obata K, Yanagawa Y, Kawaguchi Y, Nabeshima Y, Hoshino M (2009) Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 136:2049-2058. CrossRef Medline
15. Gazit R, Krizhanovsky V, Ben-Arie N (2004) Math1 controls cerebellar granule cell differentiation by regulating multiple components of the Notch signaling pathway. Development 131:903-913. CrossRef Medline
16. Hashimoto M, Mikoshiba K (2003) Mediolateral compartmentalization of the cerebellum is determined on the "birth date" of Purkinje cells. J Neurosci 23:11342-11351. Medline
17. Hatten ME, Heintz N (1995) Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385-408. CrossRef Medline
18. Hatten ME, Alder J, Zimmerman K, Heintz N (1997) Genes involved in cerebellar cell specification and differentiation. Curr Opin Neurobiol 7:40-47. CrossRef Medline
19. Helms AW, Abney AL, Ben-Arie N, Zoghbi HY, Johnson JE (2000) Autoregulation and multiple enhancers control Math1 expression in the developing nervous system. Development 127:1185-1196. Medline
20. Helms AW, Gowan K, Abney A, Savage T, Johnson JE (2001) Overexpression of MATH1 disrupts the coordination of neural differentiation in cerebellum development. Mol Cell Neurosci 17:671-682. CrossRef Medline
21. Hori K, Hoshino M (2012) GABAergic neuron specification in the spinal cord, the cerebellum, and the cochlear nucleus. Neural Plast 2012:921732. Medline
22. Hoshino M (2006) Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum 5:193-198. CrossRef Medline
23. Hoshino M (2012) Neuronal subtype specification in the cerebellum and dorsal hindbrain. Dev Growth Differ 54:317-326. CrossRef Medline
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 CV, Kawaguchi Y, Nakao K, Nabeshima Y (2005) Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47:201-213. CrossRef Medline
25. Hoshino M, Seto Y, Mayumi Y (2013) Specification of cerebellar and precerebellar neurons. In: Handbook of the cerebellum and cerebellar disor-ders (Manto M, Gruol D, Schmahmann J, Koibuchi N, Rossi F, eds), Vol 1, pp 75-87 New York: Springer
26. Inoue T, Krumlauf R (2001) An impulse to the brain-using in vivo electroporation. Nat Neurosci 4:1156-1158. CrossRef Medline
27. Kanki H, Suzuki H, Itohara S (2006) High-efficiency CAG-FLPe deleter mice in C57BL/6J background. Exp Anim 55:137-141. CrossRef Medline
28. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV (2002) The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 32:128-134. CrossRef Medline
29. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M (2003) The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J 22:4190-4201. CrossRef Medline
30. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M (2006) Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol 8:17-26. CrossRef Medline
31. Krapp A, Knöfler M, Ledermann B, Bürki K, Berney C, Zoerkler N, Hagenbüchle O, Wallauer PK (1998) The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes Dev 12:3752-3763. CrossRef Medline
32. Landsberg RL, Awatramani RB, Hunter NL, Farago AF, DiPietrantonio HJ, Rodriguez CI, Dymecki SM (2005) Hindbrain rhombic lip is comprised of discrete progenitor cell populations allocated by Pax6. Neuron 48:933-947. CrossRef Medline
33. 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. CrossRef Medline
34. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24. CrossRef Medline
35. Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281-294. CrossRef Medline
36. Mathis L, Nicolas JF (2003) Progressive restriction of cell fates in relation to neuroepithelial cell mingling in the mouse cerebellum. Dev Biol 258:20-31. CrossRef Medline
37. Mathis L, Bonnerot C, Puelles L, Nicolas JF (1997) Retrospective clonal analysis of the cerebellum using genetic laacZ/lacZ mouse mosaics. Development 124:4089-4104. Medline
38. Minaki Y, Nakatani T, Mizuhara E, Inoue T, Ono Y (2008) Identification of a novel transcriptional corepressor, Corl2, as a cerebellar Purkinje cellselective marker. Gene Expr Patterns 8:418-423. CrossRef Medline
39. Mizuhara E, Minaki Y, Nakatani T, Kumai M, Inoue T, Muguruma K, Sasai Y, Ono Y (2010) Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin. Dev Biol 338:202-214. CrossRef Medline
40. Nishida K, Hoshino M, Kawaguchi Y, Murakami F (2010) Ptf1a directly controls expression of immunoglobulin superfamily molecules Nephrin and Neph3 in the developing central nervous system. J Biol Chem 285: 373-380. CrossRef Medline
41. Pascual M, Abasolo I, Mingorance-Le Meur A, Martínez A, Del Rio JA, Wright CV, Real FX, Soriano E (2007) Cerebellar GABAergic progenitors adopt an external granule cell-like phenotype in the absence of Ptf1a transcription factor expression. Proc Natl Acad Sci U S A 104:5193-5198. CrossRef Medline
42. Saito T, Nakatsuji N (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev Biol 240:237-246. CrossRef Medline
43. Seto Y, Nakatani T, Masuyama N, Taya S, Kumai M, Minaki Y, Hamaguchi A, Inoue YU, Inoue T, Miyashita S, Fujiyama T, Yamada M, Chapman H, Campbell K, Magnuson MA, Wright CV, Kawaguchi Y, Ikenaka K, Takebayashi H, Ishiwata S, Ono Y, Hoshino M (2014) Temporal identity transition from Purkinje cell progenitors to GABAergic interneuron progenitors in the cerebellum. Nat Commun 5:3337. CrossRef Medline
44. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71. CrossRef Medline
45. Sudarov A, Turnbull RK, Kim EJ, Lebel-Potter M, Guillemot F, Joyner AL (2011) Ascl1 genetics reveals insights into cerebellum local circuit assembly. J Neurosci 31:11055-11069. CrossRef Medline
46. Sultan F, Czubayko U, Thier P (2003) Morphological classification of the rat lateral cerebellar nuclear neurons by principal component analysis. J Comp Neurol 455:139-155. CrossRef Medline
47. Wang VY, Zoghbi HY (2001) Genetic regulation of cerebellar development. Nat Rev Neurosci 2:484-491. CrossRef Medline
48. Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48:31-43. CrossRef Medline
49. Wiebe PO, Kormish JD, Roper VT, Fujitani Y, Alston NI, Zaret KS, Wright CV, Stein RW, GannonM (2007) Ptf1a binds to and activates area III, a highly conserved region of the Pdx1 promoter that mediates early pancreas-wide Pdx1 expression. Mol Cell Biol 27:4093-4104. CrossRef Medline
50. Yamada M, Terao M, Terashima T, Fujiyama T, Kawaguchi Y, Nabeshima Y, Hoshino M (2007) Origin of climbing fiber neurons and their developmental dependence on Ptf1a. J Neurosci 27:10924-10934. CrossRef Medline