Genome-wide microarray comparison reveals downstream genes of Pax6 in the developing mouse cerebellum

European Journal of Neuroscience

Volumn 36, Issue 7, 2012, Pages 2888-2898

  Ha, Thomas J ^a   Swanson, Douglas J ^a   Kirova, Roumyana ^b   Yeung, Joanna ^a   Choi, Kunho ^a   Tong, Yiai ^c   Chesler, Elissa J ^b,d   Goldowitz, Daniel ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d JACKSON LABORATORY   (United States)

Author keywords

Cerebellum; Development; Granule cell; Sey mutant; Transcription factor; Transcriptome profiling

Indexed keywords

TRANSCRIPTION FACTOR PAX6;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CEREBELLUM; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONAL TISSUE; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENETIC ASSOCIATION; GENOME ANALYSIS; GLUTAMATERGIC NERVE CELL; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; NULL ALLELE; PAX6 GENE; PRIORITY JOURNAL; QUANTITATIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME SERIES ANALYSIS; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CEREBELLUM; COMPARATIVE GENOMIC HYBRIDIZATION; EYE PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84866972217     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08221.x     Document Type: Article

References (49)

1. Arlotta, P., Molyneaux, B.J., Chen, J., Inoue, J., Kominami, R. & Macklis, J.D. (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron, 45, 207-221.
2. Baker, E.J., Jay, J.J., Philip, V.M., Zhang, Y., Li, Z., Kirova, R., Langston, M.A. & Chesler, E.J. (2009) Ontological discovery environment: a system for integrating gene-phenotype associations. Genomics, 94, 377-387.
3. Baker, E.J., Jay, J.J., Bubier, J.A., Langston, M.A. & Chesler, E.J. (2012) GeneWeaver: a web-based system for integrative functional genomics. Nucleic Acids Res., 40, D1067-D1076.
4. Banziger, C., Soldini, D., Schutt, C., Zipperlen, P., Hausmann, G. & Basler, K. (2006) Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell, 125, 509-522.
5. Bartscherer, K., Pelte, N., Ingelfinger, D. & Boutros, M. (2006) Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell, 125, 523-533.
6. Ben-Arie, N., Bellen, H.J., Armstrong, D.L., McCall, A.E., Gordadze, P.R., Guo, Q., Matzuk, M.M. & Zoghbi, H.Y. (1997) Math1 is essential for genesis of cerebellar granule neurons. Nature, 390, 169-172.
7. Benjamini, Y. & Hochberg, Y. (1995) Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc., 57, 289-300.
8. Cantor, H., Simpson, E., Sato, V.L., Fathman, C.G. & Herzenberg, L.A. (1975) Characterization of subpopulations of T lymphocytes. I. Separation and functional studies of peripheral T-cells binding different amounts of fluorescent anti-Thy 1.2 (theta) antibody using a fluorescence-activated cell sorter (FACS). Cell. Immunol., 15, 180-196.
9. Chauhan, B.K., Reed, N.A., Yang, Y., Cermak, L., Reneker, L., Duncan, M.K. & Cvekl, A. (2002a) A comparative cDNA microarray analysis reveals a spectrum of genes regulated by Pax6 in mouse lens. Genes Cells, 7, 1267-1283.
10. Chauhan, B.K., Reed, N.A., Zhang, W., Duncan, M.K., Kilimann, M.W. & Cvekl, A. (2002b) Identification of genes downstream of Pax6 in the mouse lens using cDNA microarrays. J. Biol. Chem., 277, 11539-11548.
11. D'Arcangelo, G., Miao, G.G., Chen, S.C., Soares, H.D., Morgan, J.I. & Curran, T. (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature, 374, 719-723.
12. Dennis, G., Jr, Sherman, B.T., Hosack, D.A., Yang, J., Gao, W., Lane, H.C. & Lempicki, R.A. (2003) DAVID: database for annotation, visualization, and integrated discovery. Genome Biol., 4, P3.
13. Engelkamp, D., Rashbass, P., Seawright, A. & van Heyningen, V. (1999) Role of Pax6 in development of the cerebellar system. Development (Cambridge, England), 126, 3585-3596.
14. Englund, C., Kowalczyk, T., Daza, R.A., Dagan, A., Lau, C., Rose, M.F. & Hevner, R.F. (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J. Neurosci., 26, 9184-9195.
15. Estivill-Torrus, G., Pearson, H., van Heyningen, V., Price, D.J. & 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 (Cambridge, England), 129, 455-466.
16. Fink, A.J., Englund, C., Daza, R.A., Pham, D., Lau, C., Nivison, M., Kowalczyk, T. & Hevner, R.F. (2006) Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J. Neurosci., 26, 3066-3076.
17. Gautier, L., Cope, L., Bolstad, B.M. & Irizarry, R.A. (2004) affy--analysis of Affymetrix GeneChip data at the probe level. Bioinformatics (Oxford, England), 20, 307-315.
18. Glassmann, A., Topka, S., Wang-Eckardt, L., Anders, S., Weisheit, G., Endl, E., Zimmer, A. & Schilling, K. (2009) Basic molecular fingerprinting of immature cerebellar cortical inhibitory interneurons and their precursors. Neuroscience, 159, 69-82.
19. Gibson, U.E., Heid, C.A. & Williams, P.M. (1996) A novel method for real time quantitative RT-PCR. Genome Res., 6, 995-1001.
20. Glynn, D., Bortnick, R.A. & Morton, A.J. (2003) Complexin II is essential for normal neurological function in mice. Hum. Mol. Genet., 12, 2431-2448.
21. Goldowitz, D. & Hamre, K. (1998) The cells and molecules that make a cerebellum. Trends Neurosci., 21, 375-382.
22. Grindley, J.C., Hargett, L.K., Hill, R.E., Ross, A. & Hogan, B.L. (1997) Disruption of PAX6 function in mice homozygous for the Pax6Sey-1Neu mutation produces abnormalities in the early development and regionalization of the diencephalon. Mech. Dev., 64, 111-126.
23. Halder, G., Callaerts, P. & Gehring, W.J. (1995) Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science (New York, N.Y), 267, 1788-1792.
24. Hatten, M.E. & Heintz, N. (1995) Mechanisms of neural patterning and specification in the developing cerebellum. Annu. Rev. Neurosci., 18, 385-408.
25. Heins, N., Malatesta, P., Cecconi, F., Nakafuku, M., Tucker, K.L., Hack, M.A., Chapouton, P., Barde, Y.A. & Gotz, M. (2002) Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci., 5, 308-315.
26. Hill, R.E., Favor, J., Hogan, B.L., Ton, C.C., Saunders, G.F., Hanson, I.M., Prosser, J., Jordan, T., Hastie, N.D. & van Heyningen, V. (1991) Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature, 354, 522-525.
27. Hirai, H., Pang, Z., Bao, D., Miyazaki, T., Li, L., Miura, E., Parris, J., Rong, Y., Watanabe, M., Yuzaki, M. & Morgan, J.I. (2005) Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nat. Neurosci., 8, 1534-1541.
28. Ho Sui, S.J., Mortimer, J.R., Arenillas, D.J., Brumm, J., Walsh, C.J., Kennedy, B.P. & Wasserman, W.W. (2005) oPOSSUM: identification of over-represented transcription factor binding sites in co-expressed genes. Nucleic Acids Res., 33, 3154-3164.
29. Holm, P.C., Mader, M.T., Haubst, N., Wizenmann, A., Sigvardsson, M. & Gotz, M. (2007) Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Mol. Cell. Neurosci., 34, 99-119.
30. Hoshino, M., Nakamura, S., Mori, K., Kawauchi, T., Terao, M., Nishimura, Y.V., Fukuda, A., Fuse, T., Matsuo, N., Sone, M., Watanabe, M., Bito, H., Terashima, T., Wright, C.V., Kawaguchi, Y., Nakao, K. & Nabeshima, Y. (2005) Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron, 47, 201-213.
31. Kamme, F., Salunga, R., Yu, J., Tran, D.T., Zhu, J., Luo, L., Bittner, A., Guo, H.Q., Miller, N., Wan, J. & Erlander, M. (2003) Single-cell microarray analysis in hippocampus CA1: demonstration and validation of cellular heterogeneity. J. Neurosci., 23, 3607-3615.
32. Li, H., Wood, C.L., Liu, Y., Getchell, T.V., Getchell, M.L. & Stromberg, A.J. (2006) Identification of gene expression patterns using planned linear contrasts. BMC Bioinformatics, 7, 245.
33. Logan, C.Y. & Nusse, R. (2004) The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol., 20, 781-810.
34. Machold, R. & Fishell, G. (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron, 48, 17-24.
35. Machold, R., Klein, C. & Fishell, G. (2011) Genes expressed in Atoh1 neuronal lineages arising from the r1/isthmus rhombic lip. Gene Expr. Patterns, 11, 349-359.
36. Miyata, T., Maeda, T. & Lee, J.E. (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev., 13, 1647-1652.
37. Quinn, J.C., Molinek, M., Martynoga, B.S., Zaki, P.A., Faedo, A., Bulfone, A., Hevner, R.F., West, J.D. & Price, D.J. (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.
38. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
39. Sansom, S.N., Griffiths, D.S., Faedo, A., Kleinjan, D.J., Ruan, Y., Smith, J., van Heyningen, V., Rubenstein, J.L. & Livesey, F.J. (2009) The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet., 5, e1000511.
40. St-Onge, L., Sosa-Pineda, B., Chowdhury, K., Mansouri, A. & Gruss, P. (1997) Pax6 is required for differentiation of glucagon-producing alpha-cells in mouse pancreas. Nature, 387, 406-409.
41. Stoykova, A., Treichel, D., Hallonet, M. & Gruss, P. (2000) Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci., 20, 8042-8050.
42. Swanson, D.J. & Goldowitz, D. (2010) Experimental Sey mouse chimeras reveal the developmental deficiencies of Pax6-null granule cells in the postnatal cerebellum. Dev. Biol., 351, 1-12.
43. Swanson, D.J., Tong, Y. & Goldowitz, D. (2005) Disruption of cerebellar granule cell development in the Pax6 mutant, Sey mouse. Brain Res., 160, 176-193.
44. Szymkiewicz, I., Destaing, O., Jurdic, P. & Dikic, I. (2004) SH3P2 in complex with Cbl and Src. FEBS Lett., 565, 33-38.
45. Tietjen, I., Rihel, J.M., Cao, Y., Koentges, G., Zakhary, L. & Dulac, C. (2003) Single-cell transcriptional analysis of neuronal progenitors. Neuron, 38, 161-175.
46. Toresson, H., Potter, S.S. & Campbell, K. (2000) Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development (Cambridge, England), 127, 4361-4371.
47. Tusher, V.G., Tibshirani, R. & Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc. Nat. Acad. Sci. USA, 98, 5116-5121.
48. Wang, V.Y., Rose, M.F. & Zoghbi, H.Y. (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron, 48, 31-43.
49. Yun, K., Potter, S. & Rubenstein, J.L. (2001) Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development (Cambridge, England), 128, 193-205.