The genesis of cerebellar GABAergic neurons: Fate potential and specification mechanisms

Frontiers in Neuroanatomy

Volumn , Issue FEBRUARY 2012, 2012, Pages

  Leto, Ketty ^a   Rolando, Chiara ^a   Rossi, Ferdinando ^a  

^a UNIVERSITY OF TURIN   (Italy)

Author keywords

Ascl 1; Fate specification; GABAergic interneuron; Heterotopic heterochronic transplantation; Pax 2; Prospective white matter; Purkinje cell; Ventricular zone

Indexed keywords

ARTICLE; CELL POPULATION; CELL PROLIFERATION; CEREBELLUM NUCLEUS; GABAERGIC SYSTEM; HETEROTOPIC TRANSPLANTATION; HUMAN; INTERNEURON; MITOSIS; NERVE CELL MEMBRANE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROEPITHELIUM; NONHUMAN; OLIVARY NUCLEUS; POSTNATAL DEVELOPMENT; PURKINJE CELL; SUBVENTRICULAR ZONE; WHITE MATTER;

EID: 84857082960     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2012.00006     Document Type: Article

References (106)

1. Acazawa, C., Ishibashi, M., Shimizu, C., Nakanishi, S., Kageyama, R. (1995). A mammalian helixloop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Bill Chem 270, 8730-8738.
2. Alcántara, S., Ruiz, M., De Castro, F., Soriano, E., Sotelo, C. (2000). Netrin1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development 127, 1359-1372.
3. Alder, J., Cho, N. K., Hatten, M. E. (1996). Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron 17, 389-399.
4. Altman, J. (1972). Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J Comp Neurol 145, 353-398.
5. Altman, J., and Bayer, S. A. (1997). Development of the cerebellar system in relation to its evolution, structures and functions. Boca Raton, FL: CRC.
6. Anthony, T. E., Mason, H. A., Gridley, T., Fishell, G., Heintz, N. (2005). Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19, 1028-1033.
7. Bartos, M., Vida, I., Jonas, P. (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8, 45-56.
8. Bastianelli, E. (2003). Distribution of calciumbinding proteins in the cerebellum. Cerebellum 2, 242-262.
9. Batista-Brito, R., Close, J., Machold, R., Fishell, G. (2008). The distinct temporal origins of olfactory bulb interneuron subtypes. J. Neurosci. 28(15), 3966-3975.
10. Batista-Brito, R. and Fishell, G. (2009). The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol 87, 81-118.
11. 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(6656), 169-172.
12. Bovetti, S., Peretto, P., Fasolo, A., De Marchis, S. (2007). Spatiotemporal specification of olfactory bulb interneurons. J Mol Hist 38, 563-569.
13. Carletti, B., Grimaldi, P., Magrassi, L., Rossi, F. (2002). Specification of cerebellar progenitors following heterotopic/heterochronic transplantation to the embryonic CNS in vivo and in vitro. J. Neurosci 22, 7132-7146.
14. Carletti, B., Grimaldi, P., Magrassi, L., Rossi, F. (2004). Engraftment and differentiation of neocortical progenitor cells transplanted to the embryonic brain in utero. J. Neurocytol 33, 309-319.
15. Carletti, B., Williams, I. M., Leto, K., Nakajima, K., Magrassi, L., Rossi, F. (2008) Time constraints and positional cues in the developing cerebellum regulate Purkinje cell placement in the cortical architecture. Dev Biol 317, 147-160.
16. Caspary, T., Anderson, K. V. (2003). Patterning cell types in the dorsal spinal cord: what the mouse mutants say. Nat Rev Neurosci 4(4), 289-297.
17. Chizhikov, V. V., Lindgren, A. G., Currle, D. S., Rose, M. F., Monuki, E. S., Millen, K. J. (2006). The roof plate regulates cerebellar cell-type specification and proliferation. Development 133(15), 2793-2804.
18. Dalgard, C. L., Zhou, Q., Lundell, T. G., Doughty, M. L. (2011). Altered gene expression in the emerging cerebellar primordium of Neurog1-/-mice. Brain Res 1388, 12-21.
19. Di Cristo, G. (2007). Development of cortical GABAergic circuits and its implications for neurodevelopmental disorders. Clin Genet 72(1), 1-8.
20. Englund, C. M., Kowalczyk, T., Daza, R. A. M., 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.
21. Fink, A. J., Englund, C., Daza, R. A. M., Pham, D., Lau, C., Nivison, M., Kowalczk, 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.
22. Florio, M., Leto, K., Muzio, L., Tinterri, A., Badaloni, A., Croci, L., Zordan, P., Barili, V., Albieri, I., Guillemot, F., Rossi, F., Consalez, G. G. (2011). Neurog2 regulates progenitor cell cycle progression and Purkinje cell dendritogenesis in cerebellar development. Molecular Mechanisms in Neuroscience, Abstr.
23. Fünfschilling, U, Reichardt, L. F. (2002). Cremediated recombination in rhombic lip derivatives. Genesis 33(4), 160-169.
24. Gao, W. Q., Hatten, M. E. (1994). Immortalizing oncogenes subvert the establishement of granule cell identity in developing cerebellum. Development 120, 1059-1070.
25. Geurtz, F. J., Timmermans, J., Shigemoto, R., De Schutter, E. (2001). Morphological and neurochemical differentiation of large granular layer interneurons in the adult rat cerebellum. Neuroscience 104(2), 499-512.
26. Glassmann, A., Topka, S., Wang-Eckardt, L., Anders, S., Weisheit, G., Endl, E., Zimmer, A., Schillig, K. (2009). Basic molecular fingerprinting of immature cerebellar cortical inhibitory interneurons and their precursors. Neuroscience 159(1), 69-82.
27. Grimaldi, P., Carletti, B., Magrassi, L., Rossi, F. (2005). Fate restriction and developmental potential of cerebellar progenitors. Transplantation studies in the developing CNS. Prog Brain Res 148, 57-68.
28. Grimaldi, P., and Rossi, F. (2006). Lack of neurogenesis in the adult rat cerebellum after Purkinje cell degeneration and growth factor infusion. Eur J Neurosci 23, 2656-2668.
29. Grimaldi, P., Parras, C., Guillemot, F., Rossi, F., Wassef, M. (2009). Origins and control of the differentiation of inhibitory interneurons and glia in the cerebellum. Dev. Biol 328, 422-433.
30. Hallonet, M. E., Teillet, M. A., Le Douarin, N. M. (1990). A new approach to the development of the cerebellum provided by the quailchick marker system. Development 108, 19-31.
31. Hallonet, M. E., Le Douarin, N. M. (1993). Tracing neuroepithelial cells of the mesencephalic and metencephalic alar plates during cerebellar ontogeny in quailchick chimaeras. Eur J Neurosci 5, 1145-1155.
32. Hatten, M. E, and Heintz, N. (1995). Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18, 385-408.
33. Helms, A. W., and Johnson, J. E. (2003). Specification of dorsal spinal cord interneurons. Curr Opin Neurobiol 13(1), 42-49.
34. Henke, R. M., Savage, T. K., Meredith, D. M., Glasgow, S. M., Hori, K., Dumas, J., McDonald, R. J., Johnson, J. E. (2009). Neurog2 is a direct downstream target of the Ptf1a-Rbpj transcription complex in dorsal spinal cord. Development 136(17), 2945-2954.
35. Hensch, T. K. (2004). Critical period regulation. Annu Rev Neurosci 27, 549-579.
36. Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6, 877-888.
37. 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. E., Kawaguchi, Y., Nakao, K., Nabeshima, Y. I. (2005). 'Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 47, 201-213.
38. Hoshino, M. (2006). Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum 5(3), 193-198.
39. Huard, J. M., Forster, C. C., Carter, M. L., Sicinski, P., Ross, M. E. (1999). Cerebellar histogenesis in mice lacking cyclin D2. Development 126(9), 1927-1935.
40. Chiang, C. (2010). Transventricular delivery of Sonic hedgehog is essential to cerebellar ventricular zone development. Proc Natl Acad Sci U S A 107(18), 8422-8427.
41. Jankovski, A., Rossi, F., Sotelo, C. (1996). Neuronal precursors in the postnatal mouse cerebellum are fully committed cells: evidence from heterochronic transplantation. Eur J Neurosci 8, 2308-2320.
42. Kim, E. J., Battiste, J., Nakagawa, Y., Johnson, J. E. (2008). Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol Cell Neurosci 38(4), 595-606.
43. Kim, E. J., Hori, K., Wyckoff, A., Dickel, L. K., Koundakjian, E. J., Goodrich, L. V., Johnson, J. E. (2011) Spatiotemporal fate map of neurogenin1 (Neurog1) lineages in the mouse central nervous system. J Comp Neurol 519(7), 1355-1370.
44. Klein, C., Butt, S. J. B., Machold, R. P., Johnson, J. E., Fishell, G. (2005). Cerebellum and forebrain derived stem cells possess intrinsic regional character. Development 132, 4497-4508.
45. Komine, O., Nagaoka, M., Hiraoka, Y., Hoshino, M., Kawaguchi, Y., Pear, W. S., Tanaka, K. (2011). RBP-J promotes the maturation of neuronal progenitors. Dev Biol 354(1), 44-54.
46. Koscheck T., Weyer A., Schilling, R. L., Schilling, K. (2003). Morphological development and neurochemical differentiation of cerebellar inhibitory interneurons in microexplants cultures. Neuroscience 116(4), 973-984.
47. Lainé, J, and Axelrad, H. (2002). Extending the cerebellar Lugaro cell class. Neuroscience 115(2), 363-374.
48. Lee, A., Kessler, J. D., Read, T. A., Kaiser, C., Corbeil, D., Huttner, W. B., Johnson, J. E., Wechsler-Reya, R. J. (2005). Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 6, 723-729.
49. Lee, Y., Katyal, S., Li, Y., El-Khamisy, S. F., Russell, H. R., Caldecott, K. W., McKinnon, P. J. (2009). Genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1. Nat Neurosci 12(8), 973-980.
50. Leto, K., Carletti, B., Williams, I. M., 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.
51. Leto, K., Bartolini, A., Rossi, F. (2008). Development of cerebellar GABAergic interneurons:Origin and shaping of the "minibrain" local connections. Cerebellum 7, 523-529.
52. Leto, K., Bartolini, A., Yanagawa, Y., Obata, K., Magrassi, L., Schilling, K., Rossi, F. (2009). Laminar fate and phenotype specification of cerebellar GABAergic interneurons. J. Neurosci 29(21), 7079-7091.
53. Leto, K., Bartolini, A., Rossi, F. (2010). The prospective white matter: an atipica neurogenic niche in the developing cerebellum. Arch Ital Biol 148, 137-146.
54. Leto, K., Bartolini, A., Di Gregorio, A., Imperiale, D., De Luca, A., Parmigiani, E., Filipkowski, R. K., Kaczmarek, L., Rossi, F. (2011). Modulation of cell-cycle dynamics is required to regulate the numbers of cerebellar GABAergic interneurons and their rhythm of maturation. Development 138(16), 3463-3472.
55. Levitt, P., Eagleson, K. L., Powell, E. M. (2004). Regulation of neocortical interneuron development and the implications for neurodevelopmental disorders. Trends Neurosci 27(7), 400-406.
56. Lin, J. C., Cai, L., Cepko, C. L. (2001). The external granule layer of the developing chick cerebellum generates granule cells and cells of the isthmus and rostral hindbrain. J. Neurosci 21(1), 159-168.
57. Lui, J. H., Hansen, D. V., Kriegstein, A. R. (2011). Development and evolution of the human neocortex. Cell 146(1), 18-36.
58. Lundell, T. G., Zhou, Q., Doughty, M. L. (2009). Neurogenin1 expression in cell lineages of the cerebellar cortex in embryonic and postnatal mice. Dev. Dyn 238, 3310-3325.
59. Machold, R. P., and Fishell, G. (2005). Math1 is expressed in temporally discrete pools of cerebellar rhombiclip neural progenitors. Neuron 48, 17-24.
60. Machold, R. P., Kittell, D. J., Fishell, G. J. (2007). Antagonism between Notch and bone morphogenetic protein receptor signaling regulates neurogenesis in the cerebellar rhombic lip. Neural Develop 2, 5.
61. Manzano, J., Cuadrado, M., Morte, B., Bernal, J. (2007). Influence of thyroid hormone and thyroid hormone receptors in the generation of cerebellar gammaaminobutyric acidergic interneurons from precursor cells. Endocrinology 148(12), 5746-5751.
62. Maricich, S. M. and 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.
63. Mathis, L., Bonnerot C., Puelles L., Nicolas, J. F. (1997). Retrospective clonal analysis of the cerebellum using genetic laacZ/lacZ mouse mosaics. Development 124, 4089-4104.
64. Mathis, L., and Nicolas, J. F. (2003) Progressive restriction of cell fates in relation to neuroepithelial cell mingling in the mouse cerebellum. Dev Biol 258, 20-31.
65. Mecklemburg, N., Garcia-López, R., Puelles, E., Sotelo, C., Martinez, S. (2011). Cerebellar oligodendroglial cells have a mesencephalic origin. Glia doi: 10.1002/glia.21236.
66. Miale, I. R., and Sidman, R. L. (1961). An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4, 277-296.
67. Milosevic, A., Goldman, J. E. (2002). Progenitors in the postnatal cerebellar white matter are antigenically heterogeneous. J Comp Neurol 452, 192-203.
68. Milosevic, A., and Goldman, J. E. (2004). Potential of progenitors from postnatal cerebellar neuroepithelium and white matter: lineage specified vs multipotent fate. Mol. Cell. Neurosci 26, 342-353.
69. Milosevic, A., Noctor, S. C., Martinez-Cerdeno, V., Kriegstein, A. R., Goldman, J. E. (2008). Progenitors from the postnatal forebrain subventricular zone differentiate into cerebellar-like interneurons and cerebellar-specific astrocytes upon transplantation. Mol. Cell. Neurosci 39, 324-334.
70. Mizuhara, E., Minaki, Y., Nakatani, T., Kumai, M., Inoue, T., Muguruma, K., Sasai, Y., Ono, Y. (2009). Purkinje cells originate from cerebellar ventricular zone progenitors positive for Neph3 and E-cadherin. Dev. Biol 338, 202-214.
71. Möhler, H., Fritschy, J. M., Crestani, F., Hensch, T., Rudolph, U. (2004). Specific GABA(A) circuits in brain development and therapy. Biochem Pharmacol 68(8), 1685-1690.
72. Morales, D., Hatten, M. E. (2006). Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. J. Neurosci 26(47), 12226-12236.
73. Nunzi, M. G., Birnstiel, S., Bhattacharyya, B. J., Slater, N. T., Mugnaini, E. (2001). Unipolar brush cells form a glutamatergic projection system within the mouse cerebellar cortex. J Comp Neurol 434(3), 329-341.
74. Nunzi, M. G., Shigemoto, R., Mugnaini, E. (2002). Differential expression of calretinin and metabotropic glutamate receptor mGluR1alpha defines subsets of unipolar brush cells in mouse cerebellum. J Comp Neurol 451(2), 189-199.
75. Owens, D. F., and Kriegstein, A. R. (2002). Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3(9), 715-727.
76. Pascual, M., Abrasolo, I., Mingorance-Le Meur, A., Martinez, A., Del Rio, J. A., Wright, C. V. E., Real, F. X., Soriano, E. (2007). Cerebellar GABAergic progenitors adopt an external granule celllike phenotype in the absence of Ptf1a transcription factor expression. Pnas 104, 5193-5198.
77. Ponti, G., Peretto, P., Bonfanti, L. (2008). Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS One 3(6), e2366.
78. Ponti, G., Crociara, P., Armentano, M., Bonfanti, L. (2010). Adult neurogenesis without germinal layers: the "atypical" cerebellum of rabbit. Arch Ital Biol 148(2), 147-158.
79. Ramóny Cajal, S. (1911). Histologie du système nerveux de l'homme et des vertébrés. Paris: Maloine.
80. Rakic, P. (1972). Extrinsic cytological determinants of basket and stellate cell dendritic pattern in the cerebellar molecular layer. J Comp Neurol 146, 335-354.
81. Rolando, C., Gribaudo, S., Yoshikawa, K., Leto, K., De Marchis, S., Rossi, F. (2010). Extracerebellar progenitors grafted to the neurogenic milieu of the postnatal rat cerebellum adapt to the host environment but fail to acquire cerebellar identities. Eur J Neurosci 31, 1340-1351.
82. Rossi, F., Borsello, T., Strata, P. (1992). Embryonic Purkinje cells grafted on the surface of the cerebellar cortex integrate in the adult unlesioned cerebellum. Eur J Neurosci 4(6), 589-593.
83. Salsano, E., Croci, L., Maderna, E., Lupo, L., Pollo, B., Giordana, M. T., Consalez, G. G., Finocchiaro, G. (2007). Expression of the neurogenic basic helix-loop-helix transcription factor NEUROG1 identifies a subgroup of medulloblastomas not expressing ATOH1. Neuro Oncol 9(3), 298-307.
84. Schilling, K., Oberdick, J., Rossi, F., Baader, S. L. (2008). Besides Purkinje cells and granule neurons: an appraisal of the cell biology of the interneurons of the cerebellar cortex. Histochem Cell Biol 130(4), 601-615.
85. Schilling, K. (2011). Specification and development of GABAergic interneurons. In Manto, M., Koibuchi, N., Schmamann, J., Gruol, D., Rossi, F. (eds) Handbook of The Cerebellum and Cerebellar Disorders. Springer, New York, Berlin.
86. Sekerkovà, G., Ilijic, E., Mugnaini, E. (2004b). Time of origin of unipolar brush cells in the rat cerebellum as observed by prenatal bromodeoxyuridine labeling. Neuroscience 127, 845-858.
87. Silbereis, J., Cheng, E., Ganat, Y. M., Ment, L. R., Vaccarino, F. M. (2009). Precursors with glial fibrillary acidic protein promoter activity transiently generate GABA interneurons in the postnatal cerebellum. Stem Cells 27, 1152-1163.
88. Silbereis, J., Heintz, T., Taylor, M. M., Ganat, Y., Ment, L. R., Bordey, A., Vaccarino, F. M. (2010). Astroglial cells in the external granular layer are precursors of cerebellar granule neurons in neonates. Mol. Cell. Neurosci 44(4), 362-373.
89. Sillitoe, R. V., and Joyner, A. L. (2007). Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23, 549-577.
90. Simat, M., Parpan, F., Fritschy, J. M. (2007). Heterogeneity of glycinergic and gabaergic interneurons in the granule cell layer of mouse cerebellum. J Comp Neurol 500(1):71-83.
91. Singec, I., Knoth, R., Ditter, M., Frotscher, M., Volk, B. (2003). Neurogranin expression by cerebellar neurons in rodents and nonhuman primates. J. Comp. Neurol 459, 278-289.
92. Sotelo, C., and Alvarado-Mallart, R. M., (1991). The reconstruction of cerebellar circuits. Trends Neurosci 14(8), 350-355.
93. Sudarov, A., Turnbull, R. K., Kim, E. J., Lebel-Potter, M., Guillemot, F., Joyner, A. L. (2011). Ascl1 genetics reveals insights into cerebellum local circuit assembly. J. Neurosci 31(30), 11055-11069.
94. Sultan, F., and Bower, J. M. (1998). Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal components analysis. J Comp Neurol 393, 353-373.
95. Sun, Q. Q. (2007). The missing piece in the "Use it or lose it" puzzle: is inhibition regulated by activity or does it acts on its own accord?. Rev Neurosci 18, 295-310.
96. Uussisari, M., and Knöpfel, T. (2010). Functional classification of neurons in the mouse lateral cerebellar nuclei. Cerebellum 30. PMID: 21116763
97. Yamanaka, H., Yanagawa, Y., Obata, K. (2004). Development of stellate and basket cells and their apoptosis in mouse cerebellar cortex. Neurosci Res 50, 13-22.
98. Wang, V. Y., Rose, M. F., Zoghbi, H. (2005). Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48, 31-43.
99. Weisheit, G., Gliem, M., Endl, E., Pfeffer, P. L., Busslinger, M., Schilling, K. (2006). Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24, 466-478.
100. Williams, I. M, Carletti, B., Leto, K., Magrassi, L., Rossi, F. (2008). Cerebellar granule cells transplanted in vivo can follow physiological and unusual migratory routes to integrate into the recipient cortex. Neurobiol Dis 30, 139-149.
101. Wingate, R. J. T. (2001). The rhombic lip and early cerebellar development. Curr Opin Neurobiol 11, 82-88.
102. Wingate, R. J., and Hatten, M. E. (1999). The role of the rhombic lip in avian cerebellum development. Development 126(20), 4395-4404
103. Wonders, C. P., Taylor, L., Welagen, J., Mbata, I. C., Xiang, J. Z., Anderson, S. T. (2008). A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Developmental Biol 314, 127-136.
104. Zhang, L., and Goldman, J. E. (1996a). Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16, 47-54.
105. Zhang, L., and Goldman, J. E. (1996b). Developmental fates and migratory pathways of dividing progenitors in the postnatal rat Cerebellum. J Comp Neurol 370, 536-550.
106. Zordan, P., Croci, L., Hawkes, R., Consalez, G. G. (2008). Comparative analysis of proneural gene expression in the embryonic cerebellum. Dev Dyn 237(6), 1726-1735.