A novel and multivalent role of pax6 in cerebellar development

Journal of Neuroscience

Volumn 36, Issue 35, 2016, Pages 9057-9069

  Yeung, Joanna ^a   Ha, Thomas J ^a   Swanson, Douglas J ^a   Goldowitz, Dan ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Atoh1; Pax6; Rhombic lips; Tbr1 and cerebellar nuclear neurons; Tbr2 and unipolar brush cells

Indexed keywords

EOMESODERMIN; PEPTIDES AND PROTEINS; TBR1 PROTEIN; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG; ATOH1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BROXURIDINE; CASP3 PROTEIN, MOUSE; CASPASE 3; DNA BINDING PROTEIN; GLUTAMIC ACID; INSM1 PROTEIN, MOUSE; LIM HOMEODOMAIN PROTEIN; LMX1A PROTEIN, MOUSE; PAX6 PROTEIN, MOUSE; PHOTOPROTEIN; TBR1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL DEATH; CELL LOSS; CELL SURVIVAL; CHIMERA; CONTROLLED STUDY; CYTOARCHITECTURE; EMBRYO; FEMALE; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; AGE; ANIMAL; CELL COUNT; CEREBELLUM; CONFOCAL MICROSCOPY; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; MAMMALIAN EMBRYO; METABOLISM; MUTANT MOUSE STRAIN;

AGE FACTORS; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BROMODEOXYURIDINE; CASPASE 3; CELL COUNT; CEREBELLUM; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUTAMIC ACID; LIM-HOMEODOMAIN PROTEINS; LUMINESCENT PROTEINS; MICE; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; PAX6 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS;

EID: 84984940195     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4385-15.2016     Document Type: Article

References (31)

1. Arner E, Daub CO, Vitting-Seerup K, Andersson R, Lilje B, Drabløs F, Lennartsson A, Rönnerblad M, Hrydziuszko O, Vitezic M, Freeman TC, Alhendi AM, Arner P, Axton R, Baillie JK, Beckhouse A, Bodega B, Briggs J, Brombacher F, Davis M et al. (2015) Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science 347:1010-1014. CrossRef Medline
2. Chizhikov VV, Lindgren AG, Currle DS, Rose MF, Monuki ES, Millen KJ (2006) The roof plate regulates cerebellar cell-type specification and proliferation. Development 133:2793-2804. CrossRef Medline
3. DiCicco-Bloom E, Friedman WJ, Black IB (1993) NT-3 stimulates sympathetic neuroblast proliferation by promoting precursor survival. Neuron 11:1101-1111. CrossRef Medline
4. Duggan A, Madathany T, de Castro SC, Gerrelli D, Guddati K, García-Añoveros J (2008) Transient expression of the conserved zinc finger gene INSM1 in progenitors and nascent neurons throughout embryonic and adult neurogenesis. J Comp Neurol 507:1497-1520. CrossRef Medline
5. Engelkamp D, Rashbass P, Seawright A, van Heyningen V (1999) Role of Pax6 in development of the cerebellar system. Development 126:3585-3596. CrossRef Medline
6. 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
7. Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A, van Heyningen V, Jessell TM, Briscoe J (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded shh signaling. Cell 90: 169-180. CrossRef Medline
8. Estivill-Torrus G, Pearson H, van Heyningen V, Price DJ, Rashbass P (2002) Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development 129:455-466. Medline
9. Farhy C, Elgart M, Shapira Z, Oron-Karni V, Yaron O, Menuchin Y, Rechavi G, Ashery-Padan R (2013) Pax6 is required for normal cell-cycle exit and the differentiation kinetics of retinal progenitor cells. PLoS One 8:e76489. CrossRef Medline
10. 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
11. Goldowitz D (1989) The weaver granuloprival phenotype is due to intrinsic action of the mutant locus in granule cells: evidence from homozygous weaver chimeras. Neuron 2:1565-1575. CrossRef Medline
12. Goldowitz D, Mullen RJ (1982) Granule cell as a site of gene action in the weaver mouse cerebellum: evidence from heterozygous mutant chimeras. J Neurosci 2:1474-1485. Medline
13. Ha TJ, Swanson DJ, Kirova R, Yeung J, Choi K, Tong Y, Chesler EJ, Goldowitz D (2012) Genome-wide microarray comparison reveals downstream genes of Pax6 in the developing mouse cerebellum. Eur J Neurosci 36: 2888-2898. CrossRef Medline
14. Ha T, Swanson D, Larouche M, Glenn R, Weeden D, Zhang P, Hamre K, Langston M, Phillips C, Song M, Ouyang Z, Chesler E, Duvvurru S, Yordanova R, Cui Y, Campbell K, Ricker G, Phillips C, Homayouni R, Gold-owitz D (2015) CbGRiTS: cerebellar gene regulation in time and space. Dev Biol 397:18-30. CrossRef Medline
15. Jensen P, Zoghbi HY, Goldowitz D (2002) Dissection of the cellular and molecular events that position cerebellar Purkinje cells: a study of the math1null-mutant mouse. J Neurosci 22:8110-8116. Medline
16. Jensen SA, Calvert AE, Volpert G, Kouri FM, Hurley LA, Luciano JP, Wu Y, Chalastanis A, Futerman AH, Stegh AH (2014) Bc12L13 is a ceramide synthase inhibitor in glioblastoma. Proc Natl Acad Sci U S A 111:5682-5687. CrossRef Medline
17. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48:17-24. CrossRef Medline
18. Maisonpierre PC, Belluscio L, Squinto S, Ip NY, Furth ME, Lindsay RM, Yancopoulos GD (1990) Neurotrophin-3: a neurotrophic factor related to NGF and BDNF. Science 247:1446-1451. CrossRef Medline
19. Millen KJ, Steshina EY, Iskusnykh IY, Chizhikov VV (2014) Transformation of the cerebellum into more ventral brainstem fates causes cerebellar agenesis in the absence of Ptf1a function. Proc Natl Acad Sci U S A 111: E1777-E1786. CrossRef Medline
20. Morales D, Hatten ME (2006) Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J Neurosci 26:12226-12236. CrossRef Medline
21. Nikoletopoulou V, Plachta N, Allen ND, Pinto L, Götz M, Barde YA (2007) Neurotrophin receptor-mediated death of misspecified neurons generated from embryonic stem cells lacking Pax6. Cell Stem Cell 1:529-540. CrossRef Medline
22. Ninkovic J, Pinto L, Petricca S, Lepier A, Sun J, Rieger MA, Schroeder T, Cvekl A, Favor J, Götz M (2010) The transcription factor Pax6 regulates survival of dopaminergic olfactory bulb neurons via crystallin alphaA. Neuron 68:682-694. CrossRef Medline
23. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, Bulfone A, Hevner RF, West JD, Price DJ (2007) Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol 302:50-65. CrossRef Medline
24. Schmahl W, Knoedlseder M, Favor J, Davidson D (1993) Defects of neuronal migration and the pathogenesis of cortical malformations are associated with small eye (sey) in the mouse, a point mutation at the pax-6-locus. Acta Neuropathol 86:126-135. CrossRef Medline
25. Shen W, Zhu L, Lee SR, Chung SH, Gillies MC (2013) Involvement of NT3 and P75NTR in photoreceptor degeneration following selective muller cell ablation. J Neuroinflammation 10:137. CrossRef Medline
26. Swanson DJ, Goldowitz D (2011) Experimental sey mouse chimeras reveal the developmental deficiencies of Pax6-null granule cells in the postnatal cerebellum. Dev Biol 351:1-12. CrossRef Medline
27. Swanson DJ, Tong Y, Goldowitz D (2005) Disruption of cerebellar granule cell development in the Pax6 mutant, sey mouse. Brain Res Dev Brain Res 160:176-193. CrossRef Medline
28. Toresson H, Potter SS, Campbell K (2000) Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127:4361-4371. Medline
29. Walther C, Gruss P (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113:1435-1449. Medline
30. Yamada M, Seto Y, Taya S, Owa T, Inoue YU, Inoue T, Kawaguchi Y, Nabeshima Y, Hoshino M (2014) Specification of spatial identities of cerebellar neuron progenitors by Ptf1a and Atoh1 for proper production of GABAergic and glutamatergic neurons. J Neurosci 34:4786-4800. CrossRef Medline
31. Yeung J, Ha TJ, Swanson DJ, Choi K, Tong Y, Goldowitz D (2014) Wls provides a new compartmental view of the rhombic lip in mouse cerebellar development. J Neurosci 34:12527-12537. CrossRef Medline