Cerebellar granule cells are predominantly generated by terminal symmetric divisions of granule cell precursors

Developmental Dynamics

Volumn 244, Issue 6, 2015, Pages 748-758

  Nakashima, Kie ^a   Umeshima, Hiroki ^b   Kengaku, Mineko ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Cell cycle; Live cell imaging; Medulloblastoma; Neural stem cells; Neurogenesis

Indexed keywords

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; ASYMMETRIC CELL DIVISION; BRAIN CELL CULTURE; CELL CYCLE REGULATION; CELL DIVISION; CELL PROLIFERATION; CEREBELLAR GRANULE CELL; CEREBELLUM; CONTROLLED STUDY; DISSOCIATED CELL CULTURE; ELECTROPORATION; GENETIC TRANSFECTION; GRANULE CELL; GRANULE CELL PRECURSOR; IMMUNOFLUORESCENCE; IN VIVO CULTURE; MOLECULAR IMAGING; MOUSE; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRECURSOR; PRIORITY JOURNAL; TERMINAL SYMMETRIC DIVISION; TIME LAPSE IMAGING; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CELL CYCLE; CONDITIONED MEDIUM; CYTOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; INSTITUTE FOR CANCER RESEARCH MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; PHYSIOLOGY; REPORTER GENE; SIGNAL TRANSDUCTION;

MAMMALIA;

BIOLOGICAL MARKER; CDKN1B PROTEIN, MOUSE; CONDITIONED MEDIUM; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DOUBLECORTIN PROTEIN; FLUORESCENT DYE; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; NEUROPEPTIDE; SHH PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN;

ANIMALS; ASYMMETRIC CELL DIVISION; BIOMARKERS; CELL CYCLE; CELL DIVISION; CELLS, CULTURED; CEREBELLUM; CULTURE MEDIA, CONDITIONED; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FLUORESCENT DYES; GENES, REPORTER; HEDGEHOG PROTEINS; HEK293 CELLS; HUMANS; MICE, INBRED ICR; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; NEUROPEPTIDES; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING;

EID: 84929946913     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24276     Document Type: Article

References (51)

1. Altman J, Bayer S. 1997. Development of the cerebellar system in relation to its evolution, structure and function. The generating, movements, and settling of cerebellar granule cells and the formation of parallel fibers. (Ed. P. Petralia and C. L. Unger), pp.334-358. Boca Raton, FL: CRC.
2. Arai Y, Pulvers JN, Haffner C, Schilling B, Nüsslein I, Calegari F, Huttner WB. 2011. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nature Commun 2:154.
3. Chen JK, Taipale J, Young KE, Maiti T, Beachy PA. 2002. Small molecule modulation of Smoothened activity. Proc Natl Acad Sci USA 99:14071-14076.
4. Dahmane N, Ruizi Altaba A. 1999. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100.
5. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nature reviews. Neuroscience 8:438-450.
6. Espinosa J, Luo L. 2008. Timing neurogenesis and differentiation: insights from quantitative clonal analyses of cerebellar granule cells. J Neurosci 28:2301-2312.
7. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J. 1999. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:247-256.
8. Frank-Kamenetsky M, Zhang X. 2002. Small-molecule modulators of Hedgehog signaling: identification and characterization of Smoothened agonists and antagonists. J Biol 1:1-19.
9. Fujita S. 1967. Quantitative and analysis of cell proliferation in the cortex differentiation postnatal of the mouse cerebellum. J Cell Biol 32:277-287.
10. Fujita S, Shimada M, Nakamura T. 1966. H3-Thymidine autoradiographic studies on the cell proliferation and differentiation in the external and the internal granular layers of the mouse cerebellum. J Comp Neurol 128:191-208.
11. Gleeson JG, Peter TL, Flanagan LA, Walsh CA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271.
12. Goodrich LV. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277:1109-1113.
13. Götz M, Huttner WB. 2005. The cell biology of neurogenesis. Nature reviews. Mol Cell Biol 6:777-788.
14. Hatten M. 1985. Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100:384-396.
15. Hatten M, Roussel M. 2011. Development and cancer of the cerebellum. Trends Neurosci 34:134-142.
16. Hatten ME, Heintz N. 1995. Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18:385-408.
17. Haubensak W, Attardo A, Denk W, Huttner WB. 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.
18. Kawaji K, Umeshima H, Eiraku M, Hirano T, Kengaku M. 2004. Dual phases of migration of cerebellar granule cells guided by axonal and dendritic leading processes. Mol Cell Neurosci 25:228-240.
19. Lai K, Kaspar BK, Gage FH, Schaffer DV. 2003. Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nature Neurosci 6:21-27.
20. Lange C, Huttner WB, Calegari F. 2009. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320-31.
21. Lui JH, Hansen DV, Kriegstein AR. 2011. Development and evolution of the human neocortex. Cell 146:18-36.
22. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G. 2003. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39:937-950.
23. Malatesta P, Hartfuss E, Götz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253-5263.
24. Mares V, Lodin Z. 1970. The cellular kinetics of the developing mouse cerebellum. II. The function of the external granular layer in the process of gyrification. Brain Res 23:343-352.
25. Miyata T, Kawaguchi A, Okano H, Ogawa M. 2001. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727-741.
26. Miyata T, Kawaguchi D, Kawaguchi A, Gotoh Y. 2010. Mechanisms that regulate the number of neurons during mouse neocortical development. Curr Opin Neurobiol 20:22-28.
27. Miyazawa K, Himi T, Garcia V, Yamagishi H, Sato S, Ishizaki Y. 2000. A Role for p27 / Kip1 in the control of cerebellar granule cell precursor proliferation. J Neurosci 20:5756-5763.
28. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neurosci 7:136-144.
29. Paridaen JTML, Huttner WB. 2014. Neurogenesis during development of the vertebrate central nervous system. EMBO Reports 15:351-364.
30. Pilaz L-J, Patti D, Marcy G, Ollier E, Pfister S, Douglas RJ, Betizeau M, Gautier E, Cortay V, Doerflinger N, Kennedy H, Dehay C. 2009. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc Natl Acad Sci USA 106:21924-21929.
31. Pons S, Trejo J, Martínez-Morales J, Martí E. 2001. Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128:1481-1491.
32. Ramón y Cajal, S. 1911. Histology of the nervous system of man and vertebrates. Vol. 11, pp 66-86. New York: Oxford University Press.
33. Rios I, Alvarez-Rodríguez R, Martí E, Pons S. 2004. Bmp2 antagonizes sonic hedgehog-mediated proliferation of cerebellar granule neurones through Smad5 signalling. Development 131:3159-3168.
34. Roussel M, Hatten M. 2011. Cerebellum: development and medulloblastoma. Curr Topics Dev Biol 94:235-282.
35. Ryder EF, Cepko CL. 1994. Migration patterns of clonally related granule cells and their progenitors in the developing chick cerebellum. Neuron 12:1011-1029.
36. Saade M, Gutiérrez-Vallejo I. 2013. Sonic hedgehog signaling switches the mode of division in the developing nervous system. Cell Reports 4:492-503.
37. Scholzen T, Gerdes J. 2000. The Ki-67 protein: From the Known and the Unknown. J Cell Physiol 182:311-322.
38. Schüller U, Heine VM, Mao J, Kho AT, Dillon AK, Han YG, Huillard E, Sun T, Ligon AH, Qian Y, Ma Q, Alvarez-Buylla A, McMahon AP, Rowitch DH, Ligon KL. 2008. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14:123-134.
39. Takahashi T, Nowakowski RS, Caviness VS. 1995. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046-6057.
40. Taverna E, Götz M, Huttner WB. 2014. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. Annu Rev Cell Dev Biol 30:465-502.
41. Umeshima H, Kengaku M. 2013. Differential roles of cyclin-dependent kinase 5 in tangential and radial migration of cerebellar granule cells. Mol Cell Neurosci 52:62-72.
42. Umeshima H, Hirano T, Kengaku M. 2007. Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons. Proc Natl Acad Sci U S A 104:16182-16187.
43. Vaillant C, Denis M. 2009. SHH pathway and Cerebellar development. Cerebellum 8:291-301.
44. Vaillant C, Michos O, Orolicki S, Brellier F, Taieb S, Moreno E, Té H, Zeller R, Monard D. 2007. Protease nexin 1 and its receptor LRP modulate SHH signalling during cerebellar development. Development 134:1745-1754.
45. Wallace V. 1999. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 9:445-448.
46. Wang X, Qiu R, Tsark W, Lu Q. 2007. Rapid promoter analysis in developing mouse brain and genetic labeling of young neurons by doublecortin-DsRed-express. J Neurosci Res 85:3567-3573.
47. Wechsler-Reya R. 2001. Caught in the matrix: how vitronectin controls neuronal differentiation. Trends Neurosci 24:680-682.
48. Wechsler-Reya RJ, Scott MP. 1999. Control of neuronal precursor proliferation in the cerebellum by sonic hedgehog. Neuron 22:103-114.
49. Xenaki D, Martin IB, Yoshida L, Ohyama K, Gennarini G, Grumet M, Sakurai T, Furley AJW. 2011. F3/contactin and TAG1 play antagonistic roles in the regulation of sonic hedgehog-induced cerebellar granule neuron progenitor proliferation. Development 138:519-29.
50. Yamasaki T, Kawaji K, Ono K, Bito H, Hirano T, Osumi N. 2001. Pax6 regulates granule cell polarization during parallel fiber formation in the developing cerebellum. Development 128:3133-3144.
51. Yang ZJ, Ellis T, Markant SL, Read TA, Kessler JD, Bourboulas M, Schüller U, Machold R, Fishell G, Rowitch DH, Wainwright BJ, Wechsler-Reya RJ. 2008. Medulloblastoma can be initiated by deletion of patched in lineage-restricted progenitors or stem cells. Cancer Cell. 14:135-145.