Neural development is dependent on the function of specificity protein 2 in cell cycle progression

Development (Cambridge)

Volumn 140, Issue 3, 2013, Pages 552-561

  Liang, Huixuan ^a   Xiao, Guanxi ^a   Yin, Haifeng ^a   Hippenmeyer, Simon ^b   Horowitz, Jonathan M ^a   Ghashghaei, H Troy ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

Author keywords

Cell cycle; M phase; Mouse; Neural progenitors; Neural stem cells; Neurogenesis; Sp2

Indexed keywords

DNA; TRANSCRIPTION FACTOR SP2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL FUNCTION; DNA SYNTHESIS; EMBRYO; GENE DELETION; M PHASE CELL CYCLE CHECKPOINT; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; BRAIN; CELL COUNT; CELL CYCLE; CELL PROLIFERATION; CROSSES, GENETIC; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; EYE PROTEINS; FEMALE; GENETIC MARKERS; HOMEODOMAIN PROTEINS; HOMOLOGOUS RECOMBINATION; INTERMEDIATE FILAMENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; SP2 TRANSCRIPTION FACTOR; STEM CELL NICHE; TRANSPLANTATION CHIMERA;

EID: 84872094223     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.085621     Document Type: Article

References (67)

1. Arai, Y., Pulvers, J. N., Haffner, C., Schilling, B., Nüsslein, I., Calegari, F. and Huttner, W. B. (2011). Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat Commun. 2, 154.
2. Baur, F., Nau, K., Sadic, D., Allweiss, L., Elsässer, H. P., Gillemans, N., de Wit, T., Krüger, I., Vollmer, M., Philipsen, S. et al. (2010). Specificity protein 2 (Sp2) is essential for mouse development and autonomous proliferation of mouse embryonic fibroblasts. PLoS ONE 5, e9587.
3. Black, A. R., Black, J. D. and Azizkhan-Clifford, J. (2001). Sp1 and krüppel-like factor family of transcription factors in cell growth regulation and cancer. J. Cell. Physiol. 188, 143-160.
4. Bollen, M., Gerlich, D. W. and Lesage, B. (2009). Mitotic phosphatases: from entry guards to exit guides. Trends Cell Biol. 19, 531-541.
5. Bouwman, P., Göllner, H., Elsässer, H. P., Eckhoff, G., Karis, A., Grosveld, F., Philipsen, S. and Suske, G. (2000). Transcription factor Sp3 is essential for post-natal survival and late tooth development. EMBO J. 19, 655-661.
6. Brill, M. S., Snapyan, M., Wohlfrom, H., Ninkovic, J., Jawerka, M., Mastick, G. S., Ashery-Padan, R., Saghatelyan, A., Berninger, B. and Götz, M. (2008). A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J. Neurosci. 28, 6439-6452.
7. Budirahardja, Y. and Gönczy, P. (2009). Coupling the cell cycle to development. Development 136, 2861-2872.
8. Burdon, T., Smith, A. and Savatier, P. (2002). Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 12, 432-438.
9. Burns, K. A. and Kuan, C. Y. (2005). Low doses of bromo- and iododeoxyuridine produce near-saturation labeling of adult proliferative populations in the dentate gyrus. Eur. J. Neurosci. 21, 803-807.
10. Calegari, F., Haubensak, W., Haffner, C. and Huttner, W. B. (2005). Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 25, 6533-6538.
11. Cameron, H. A. and McKay, R. D. (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J. Comp. Neurol. 435, 406-417.
12. Costa, M. R., Götz, M. and Berninger, B. (2010). What determines neurogenic competence in glia? Brain Res. Rev. 63, 47-59.
13. Doetsch, F., Caillé, I., Lim, D. A., García-Verdugo, J. M. and Alvarez-Buylla, A. (1999a). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
14. Doetsch, F., García-Verdugo, J. M. and Alvarez-Buylla, A. (1999b). Regeneration of a germinal layer in the adult mammalian brain. Proc. Natl. Acad. Sci. USA 96, 11619-11624.
15. Englund, C., Fink, A., Lau, C., Pham, D., Daza, R. A., Bulfone, A., Kowalczyk, T. and Hevner, R. F. (2005). Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247-251.
16. Farkas, L. M. and Huttner, W. B. (2008). The cell biology of neural stem and progenitor cells and its significance for their proliferation versus differentiation during mammalian brain development. Curr. Opin. Cell Biol. 20, 707-715.
17. Feng, Y. and Walsh, C. A. (2004). Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44, 279-293.
18. Fietz, S. A. and Huttner, W. B. (2011). Cortical progenitor expansion, selfrenewal and neurogenesis-a polarized perspective. Curr. Opin. Neurobiol. 21, 23-35.
19. Fung, T. K. and Poon, R. Y. (2005). A roller coaster ride with the mitotic cyclins. Semin. Cell Dev. Biol. 16, 335-342.
20. García-García, E., Pino-Barrio, M. J., López-Medina, L. and Martínez-Serrano, A. (2012). Intermediate progenitors are increased by lengthening of the cell cycle through calcium signaling and p53 expression in human neural progenitors. Mol. Biol. Cell 23, 1167-1180.
21. Göllner, H., Bouwman, P., Mangold, M., Karis, A., Braun, H., Rohner, I., Del Rey, A., Besedovsky, H. O., Meinhardt, A., van den Broek, M. et al. (2001). Complex phenotype of mice homozygous for a null mutation in the Sp4 transcription factor gene. Genes Cells 6, 689-697.
22. Götz, M. and Huttner, W. B. (2005). The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6, 777-788.
23. Gruber, R., Zhou, Z., Sukchev, M., Joerss, T., Frappart, P. O. and Wang, Z. Q. (2011). MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 13, 1325-1334.
24. Guillemot, F. (2007). Cell fate specification in the mammalian telencephalon. Prog. Neurobiol. 83, 37-52.
25. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, J. I., Guerrier, S., Boutt, E., Peters, E., Barnes, A. P., Parras, C. et al. (2005). Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62.
26. Haubensak, W., Attardo, A., Denk, W. and Huttner, W. B. (2004). Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA 101, 3196-3201.
27. Hayes, N. L. and Nowakowski, R. S. (2002). Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res. Dev. Brain Res. 134, 77-85.
28. He, S., Nakada, D. and Morrison, S. J. (2009). Mechanisms of stem cell selfrenewal. Annu. Rev. Cell Dev. Biol. 25, 377-406.
29. Hippenmeyer, S., Youn, Y. H., Moon, H. M., Miyamichi, K., Zong, H., Wynshaw-Boris, A. and Luo, L. (2010). Genetic mosaic dissection of Lis1 and Ndel1 in neuronal migration. Neuron 68, 695-709.
30. Jacquet, B. V., Patel, M., Iyengar, M., Liang, H., Therit, B., Salinas-Mondragon, R., Lai, C., Olsen, J. C., Anton, E. S. and Ghashghaei, H. T. (2009a). Analysis of neuronal proliferation, migration and differentiation in the postnatal brain using equine infectious anemia virus-based lentiviral vectors. Gene Ther. 16, 1021-1033.
31. Jacquet, B. V., Salinas-Mondragon, R., Liang, H., Therit, B., Buie, J. D., Dykstra, M., Campbell, K., Ostrowski, L. E., Brody, S. L. and Ghashghaei, H. T. (2009b). FoxJ1-dependent gene expression is required for differentiation of radial glia into ependymal cells and a subset of astrocytes in the postnatal brain. Development 136, 4021-4031.
32. Jacquet, B. V., Ruckart, P. and Ghashghaei, H. T. (2010). An organotypic slice assay for high-resolution time-lapse imaging of neuronal migration in the postnatal brain. J. Vis. Exp. 11, 2486.
33. Kim, T. H., Chiera, S. L., Linder, K. E., Trempus, C. S., Smart, R. C. and Horowitz, J. M. (2010). Overexpression of transcription factor sp2 inhibits epidermal differentiation and increases susceptibility to wound- and carcinogeninduced tumorigenesis. Cancer Res. 70, 8507-8516.
34. Kriegstein, A. and Alvarez-Buylla, A. (2009). The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184.
35. Krüger, I., Vollmer, M., Simmons, D. G., Elsässer, H. P., Philipsen, S. and Suske, G. (2007). Sp1/Sp3 compound heterozygous mice are not viable: impaired erythropoiesis and severe placental defects. Dev. Dyn. 236, 2235-2244.
36. Lian, G., Lu, J., Hu, J., Zhang, J., Cross, S. H., Ferland, R. J. and Sheen, V. L. (2012). Filamin a regulates neural progenitor proliferation and cortical size through Wee1-dependent Cdk1 phosphorylation. J. Neurosci. 32, 7672-7684.
37. Liang, H., Hippenmeyer, S. and Ghashghaei, H. T. (2012). A Nestincre transgenic mouse is insufficient for recombination in early embryonic neural progenitors. Biol. Open 1, 1200-1203.
38. Lindqvist, A., Rodríguez-Bravo, V. and Medema, R. H. (2009). The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J. Cell Biol. 185, 193-202.
39. Lizarraga, S. B., Margossian, S. P., Harris, M. H., Campagna, D. R., Han, A. P., Blevins, S., Mudbhary, R., Barker, J. E., Walsh, C. A. and Fleming, M. D. (2010). Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137, 1907-1917.
40. Lu, M., Zhang, R. L., Zhang, Z. G., Yang, J. J. and Chopp, M. (2007). Linkage of cell cycle kinetics between embryonic and adult stroke models: an analytical approach. J. Neurosci. Methods 161, 323-330.
41. Manzini, M. C. and Walsh, C. A. (2011). What disorders of cortical development tell us about the cortex: one plus one does not always make two. Curr. Opin. Genet. Dev. 21, 333-339.
42. Marin, M., Karis, A., Visser, P., Grosveld, F. and Philipsen, S. (1997). Transcription factor Sp1 is essential for early embryonic development but dispensable for cell growth and differentiation. Cell 89, 619-628.
43. Martynoga, B., Morrison, H., Price, D. J. and Mason, J. O. (2005). Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev. Biol. 283, 113-127.
44. Miyata, T., Kawaguchi, A., Saito, K., Kawano, M., Muto, T. and Ogawa, M. (2004). Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131, 3133-3145.
45. Moorefield, K. S., Fry, S. J. and Horowitz, J. M. (2004). Sp2 DNA binding activity and trans-activation are negatively regulated in mammalian cells. J. Biol. Chem. 279, 13911-13924.
46. Nguyêñ-Trân, V. T., Kubalak, S. W., Minamisawa, S., Fiset, C., Wollert, K. C., Brown, A. B., Ruiz-Lozano, P., Barrere-Lemaire, S., Kondo, R., Norman, L. W. et al. (2000). A novel genetic pathway for sudden cardiac death via defects in the transition between ventricular and conduction system cell lineages. Cell 102, 671-682.
47. Noctor, S. C., Martínez-Cerdeño, V., Ivic, L. and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144.
48. Okano, H. and Temple, S. (2009). Cell types to order: temporal specification of CNS stem cells. Curr. Opin. Neurobiol. 19, 112-119.
49. Pinto, L. and Götz, M. (2007). Radial glial cell heterogeneity - the source of diverse progeny in the CNS. Prog. Neurobiol. 83, 2-23.
50. Pomerening, J. R., Ubersax, J. A. and Ferrell, J. E., Jr (2008). Rapid cycling and precocious termination of G1 phase in cells expressing CDK1AF. Mol. Biol. Cell 19, 3426-3441.
51. Pontious, A., Kowalczyk, T., Englund, C. and Hevner, R. F. (2008). Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30, 24-32.
52. Reynolds, B. A. and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
53. Sakai, D., Dixon, J., Dixon, M. J. and Trainor, P. A. (2012). Mammalian neurogenesis requires Treacle-Plk1 for precise control of spindle orientation, mitotic progression, and maintenance of neural progenitor cells. PLoS Genet. 8, e1002566.
54. Salomoni, P. and Calegari, F. (2010). Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol. 20, 233-243.
55. Sessa, A., Mao, C. A., Hadjantonakis, A. K., Klein, W. H. and Broccoli, V. (2008). Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60, 56-69.
56. Silver, D. L., Hou, L., Somerville, R., Young, M. E., Apte, S. S. and Pavan, W. J. (2008). The secreted metalloprotease ADAMTS20 is required for melanoblast survival. PLoS Genet. 4, e1000003.
57. Singh, A. M. and Dalton, S. (2009). The cell cycle and Myc intersect with mechanisms that regulate pluripotency and reprogramming. Cell Stem Cell 5, 141-149.
58. Smith, C. M. and Luskin, M. B. (1998). Cell cycle length of olfactory bulb neuronal progenitors in the rostral migratory stream. Dev. Dyn. 213, 220-227.
59. Stead, E., White, J., Faast, R., Conn, S., Goldstone, S., Rathjen, J., Dhingra, U., Rathjen, P., Walker, D. and Dalton, S. (2002). Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21, 8320-8333.
60. Supp, D. M., Witte, D. P., Branford, W. W., Smith, E. P. and Potter, S. S. (1996). Sp4, a member of the Sp1-family of zinc finger transcription factors, is required for normal murine growth, viability, and male fertility. Dev. Biol. 176, 284-299.
61. Takahashi, T., Nowakowski, R. S. and Caviness, V. S., Jr (1996). The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J. Neurosci. 16, 6183-6196.
62. Terrados, G., Finkernagel, F., Stielow, B., Sadic, D., Neubert, J., Herdt, O., Krause, M., Scharfe, M., Jarek, M. and Suske, G. (2012). Genome-wide localization and expression profiling establish Sp2 as a sequence-specific transcription factor regulating vitally important genes. Nucleic Acids Res. 40, 7844-7857.
63. Toresson, H., Potter, S. S. and Campbell, K. (2000). Genetic control of dorsalventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 127, 4361-4371.
64. van Loo, P. F., Bouwman, P., Ling, K. W., Middendorp, S., Suske, G., Grosveld, F., Dzierzak, E., Philipsen, S. and Hendriks, R. W. (2003). Impaired hematopoiesis in mice lacking the transcription factor Sp3. Blood 102, 858-866.
65. White, M. A., Riles, L. and Cohen, B. A. (2009). A systematic screen for transcriptional regulators of the yeast cell cycle. Genetics 181, 435-446.
66. Xie, J., Yin, H., Nichols, T. D., Yoder, J. A. and Horowitz, J. M. (2010). Sp2 is a maternally inherited transcription factor required for embryonic development. J. Biol. Chem. 285, 4153-4164.
67. Yin, H., Nichols, T. D. and Horowitz, J. M. (2010). Transcription of mouse Sp2 yields alternatively spliced and sub-genomic mRNAs in a tissue- and cell-typespecific fashion. Biochim. Biophys. Acta 1799, 520-531.