Profound morphological and functional changes of rodent Purkinje cells between the first and the second postnatal weeks: A metamorphosis?

Frontiers in Neuroanatomy

Volumn , Issue APRIL 2012, 2012, Pages

  Dusart, Isabelle ^a,b   Flamant, Frederic ^c  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c Univ Lyon 1   (France)

Author keywords

Development; Purkinje cell

Indexed keywords

4 AMINOBUTYRIC ACID; LIOTHYRONINE; THYROID HORMONE; THYROXINE;

CELL ACTIVITY; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL POPULATION; CELL STRUCTURE; CELL SURVIVAL; GLIA CELL; INNERVATION; INTERNEURON; METAMORPHOSIS; MYELINATION; NERVE FIBER; NERVE FIBER REGENERATION; NONHUMAN; PERINATAL PERIOD; PHASE TRANSITION; PURKINJE CELL; REVIEW; SYNAPSE;

EID: 84864025130     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (149)

1. Ahlgren, S. C., Wallace, H., Bishop, J., Neophytou, C., and Raff, M. C. (1997). Effects of thyroid hormone on embryonic oligodendrocyte precursor cell development in vivo and in vitro. Mol. Cell. Neurosci. 9, 420-432.
2. Ameisen, J. C. (2002). On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9, 367-393.
3. Ango, F., Wu, C., Van Der Want, J. J., Wu, P., Schachner, M., and Huang, Z. J. (2008). Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biol. 6:e103. doi: 10.1371/journal.pbio.0060103
4. Armengol, J. A., and Sotelo, C. (1991). Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in 'in vitro' slices. Brain Res. Dev. Brain Res. 64, 95-114.
5. Baptista, C. A., Hatten, M. E., Blazeski, R., and Mason, C. A. (1994). Cell-cell interactions influence survival and differentiation of purified Purkinje cells in vitro. Neuron 12, 243-260.
6. Bartlett, W. P., Li, X. S., Williams, M., and Benkovic, S. (1991). Localization of insulin-like growth factor-1 mRNA in murine central nervous system during postnatal development. Dev. Biol. 147, 239-250.
7. Ben-Ari, Y., Gaiarsa, J. L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87, 1215-1284.
8. Bernal, J. (2007). Thyroid hormone receptors in brain development and function. Nat. Clin. Pract. Endocrinol. Metab. 3, 249-259.
9. Berry, M., and Bradley, P. (1976). The growth of the dendritic trees of Purkinje cells in the cerebellum of the rat. Brain Res. 112, 1-35.
10. Bertossi, M., Roncali, L., Mancini, L., Ribatti, D., and Nico, B. (1986). Process of differentiation of cerebellar Purkinje neurons in the chick embryo. Anat. Embryol. (Berl.) 175, 25-34.
11. Billon, N., Jolicoeur, C., Tokumoto, Y., Vennstrom, B., and Raff, M. (2002). Normal timing of oligodendrocyte development depends on thyroid hormone receptor alpha 1 (TRalpha1). EMBO J. 21, 6452-6460.
12. Bochukova, E., Schoenmakers, N., Agostini, M., Schoenmakers, E., Rajanayagam, O., Keogh, J. M., Henning, E., Reinemund, J., Gevers, E., Sarri, M., Downes, K., Offiah, A., Albanese, A., Halsall, D., Schwabe, J. W., Bain, M., Lindley, K., Muntoni, F., Khadem, F. V., Dattani, M., Farooqi, I. S., Gurnell, M., and Chatterjee, K. (2012). Amutation in the thyroid hormone receptor alpha gene. N. Engl. J. Med. 366, 243-249.
13. Bondy, C., Werner, H., Roberts, C. T., and Leroith, D. (1992). Cellular pattern of type-I insulin-like growth factor receptor gene expression during maturation of the rat brain: comparison with insulin-like growth factors I and II. Neuroscience 46, 909-923.
14. Boukhtouche, F., Brugg, B., Wehrle, R., Bois-Joyeux, B., Danan, J. L., Dusart, I., and Mariani, J. (2010). Induction of earlyPurkinje cell dendritic differentiation bythyroidhor-mone requires RORalpha. Neural Dev. 5, 18.
15. Boukhtouche, F., Doulazmi, M., Frederic, F., Dusart, I., Brugg, B., and Mariani, J. (2006a). RORalpha, a pivotal nuclear receptor for Purkinje neuron survival and differentiation: from development to ageing. Cerebellum 5, 97-104.
16. Boukhtouche, F., Janmaat, S., Vodjdani, G., Gautheron, V., Mallet, J., Dusart, I., and Mariani, J. (2006b). Retinoid-related orphan receptor alpha controls the early steps of Purkinje cell dendritic differentiation. J. Neurosci. 26, 1531-1538.
17. Bouslama-Oueghlani, L., Wehrle, R., Sotelo, C., and Dusart, I. (2003). The developmental loss of the ability of Purkinje cells to regenerate their axons occurs in the absence of myelin: an in vitro model to prevent myelination. J. Neurosci. 23, 8318-8329.
18. Bovolenta, P., Liem, R. K., and Mason, C. A. (1984). Development of cerebellar astroglia: transitions in form and cytoskeletal content. Dev. Biol. 102, 248-259.
19. Bradley, D. J., Towle, H. C., and Young, W. S. 3rd. (1992). Spatial and temporal expression of alpha-and beta-thyroid hormone receptor mRNAs, including the beta 2-subtype, in the developing mammalian nervous system. J. Neurosci. 12, 2288-2302.
20. Bradley, P., and Berry, M. (1976). The effects of reduced climbing and parallel fibre input on Purkinje cell dendritic growth. Brain Res. 109, 133-151.
21. Burazin, T. C., and Gundlach, A. L. (1999). Localization of GDNF/neurturin receptor (c-ret, GFRalpha-1 and alpha-2) mRNAs in postnatal rat brain: differential regional and temporal expression in hippocampus, cortex and cerebellum. Brain Res. Mol. Brain Res. 73, 151-171.
22. Cajal, R. (1911). Histologie du Système Nerveux de Vhomme etdes Vertébrés. Paris: Maloine.
23. Cajal, R. (1926). Sur les fibres moussues et quelques points douteux de la texture de l'écorce cérébelleuse. Trab. Lab. Invest. Biol. Univ. Madrid 24, 215-251.
24. Carletti, B., and Rossi, F. (2008). Neurogenesis in the cerebellum. Neuroscientist14, 91-100.
25. Chedotal, A., and Sotelo, C. (1992). Early development of olivocerebellar projections in the fetal rat using CGRP immunocyto-chemistry. Eur. J. Neurosci. 4, 1159-1179.
26. Chedotal, A., and Sotelo, C. (1993). The 'creeper stage' in cerebellar climbing fiber synaptogenesis precedes the 'pericellular nest'-ultrastructural evidence with parvalbumin immunocytochem-istry. Brain Res. Dev. Brain Res. 76, 207-220.
27. Chomez, P., Neveu, I., Mansen, A., Kiesler, E., Larsson, L., Vennstrom, B., and Arenas, E. (2000). Increased cell death and delayed development in the cerebellum of mice lacking the rev-erbA(alpha) orphan receptor. Development 127, 1489-1498.
28. Cohen-Cory, S., Dreyfus, C. F., and Black, I. B. (1989). Expression of high-and low-affinity nerve growth factor receptors by Purkinje cells in the developing rat cerebellum. Exp. Neurol. 105, 104-109.
29. Crepel, F., Delhaye-Bouchaud, N., and Dupont, J. L. (1981). Fate of the multiple innervation of cerebellar Purkinje cells by climbing fibers in immature control, x-irradiated and hypothyroid rats. Brain Res. 227, 59-71.
30. Crepel, F., Mariani, J., and Delhaye-Bouchaud, N. (1976). Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J. Neurobiol. 7, 567-578.
31. de Bilbao, F., Guarin, E., Nef, P., Vallet, P., Giannakopoulos, P., and Dubois-Dauphin, M. (1999). Postnatal distribution of cpp32/caspase 3 mRNA in the mouse central nervous system: an in situ hybridization study. J. Comp. Neurol. 409, 339-357.
32. Delpire, E. (2000). Cation-chloride cotransporters in neuronal communication. News Physiol. Sci. 15, 309-312.
33. Durand, B., and Raff, M. (2000). A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 22, 64-71.
34. Dusart, I., Airaksinen, M. S., and Sotelo, C. (1997). Purkinje cell survival and axonal regeneration are age dependent: an in vitro study. J. Neurosci. 17, 3710-3726.
35. Dusart, I., Ghoumari, A., Wehrle, R., Morel, M. P., Bouslama-Oueghlani, L., Camand, E., and Sotelo, C. (2005). Cell death and axon regeneration of Purkinje cells after axotomy: challenges of classical hypotheses of axon regeneration. Brain Res. Brain Res. Rev. 49, 300-316.
36. Dusart, I., Guenet, J. L., and Sotelo, C. (2006). Purkinje cell death: differences between developmental cell death and neurodegenerative death in mutant mice. Cerebellum 5, 163-173.
37. Dusart, I., and Sotelo, C. (1994). Lack of Purkinje cell loss in adult rat cerebellum following protracted axotomy: degenerative changes and regenerative attempts of the severed axons. J. Comp. Neurol. 347, 211-232.
38. 2+ signalling in developing rat cerebellar Purkinje neurones. J. Physiol. 536, 429-437.
39. Eisenman, L. M., Schalekamp, M. P., and Voogd, J. (1991). Development of the cerebellar cortical efferent projection: an in-vitro anterograde tracing study in rat brain slices. Brain Res. Dev. Brain Res. 60, 261-266.
40. Fan, H., Favero, M., and Vogel, M. W. (2001). Elimination of Bax expression in mice increases cerebellar Purkinje cell numbers but not the number of granule cells. J. Comp. Neurol. 436, 82-91.
41. Fauquier, T., Romero, E., Picou, F., Chatonnet, F., Nguyen, X. N., Quignodon, L., and Flamant, F. (2011). Severe impairment of cerebellum development in mice expressing a dominant-negative mutation inactivating thyroid hormone receptor alpha1 isoform. Dev. Biol. 356, 350-358.
42. Fisher, D. A., Polk, D. H., and Wu, S. Y. (1994). Fetal thyroid metabolism: a pluralistic system. Thyroid 4, 367-371.
43. Flamant, F., Poguet, A. L., Plateroti, M., Chassande, O., Gauthier, K., Streichenberger, N., Mansouri, A., and Samarut, J. (2002). Congenital hypothyroid Pax8(-/-) mutant mice can be rescued by inactivating the TRalpha gene. Mol. Endocrinol. 16, 24-32.
44. Foran, D. R., and Peterson, A. C. (1992). Myelin acquisition in the central nervous system of the mouse revealed by an MBP-Lac Z transgene. J. Neurosci. 12, 4890-4897.
45. Gao, W. Q., Zheng, J. L., and Karihaloo, M. (1995). Neurotrophin-4/5 (NT-4/5) and brain-derived neu-rotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J. Neurosci. 15, 2656-2667.
46. Garcia-Segura, L. M., Rodriguez, J. R., and Torres-Aleman, I. (1997). Localization of the insulin-like growth factor I receptor in the cerebellum and hypothalamus of adult rats: an electron microscopic study. J. Neurocytol. 26, 479-490.
47. Gardette, R., Crepel, F., Alvarado-Mallart, R. M., and Sotelo, C. (1990). Fate of grafted embryonic Purkinje cells in the cerebellum of the adult "Purkinje cell degeneration" mutant mouse. II. Development of synaptic responses: an in vitro study. J. Comp. Neurol. 295, 188-196.
48. Gardette, R., Debono, M., Dupont, J. L., and Crepel, F. (1985). Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. I. Postsynaptic potentials. Brain Res. 351, 47-55.
49. Ghoumari, A. M., Dusart, I., El-Etr, M., Tronche, F., Sotelo, C., Schumacher, M., and Baulieu, E. E. (2003). Mifepristone (RU486) protects Purkinje cells from cell death in organotypic slice cultures of postnatal rat and mouse cerebellum. Proc. Natl. Acad. Sci. U.S.A. 100, 7953-7958.
50. Ghoumari, A. M., Piochon, C., Tomkiewicz, C., Eychenne, B., Levenes, C., Dusart, I., Schumacher, M., and Baulieu, E. E. (2006). Neuroprotective effect of mifepristone involves neuron depolarization. FASEB J. 20, 1377-1386.
51. Ghoumari, A. M., Wehrle, R., Bernard, O., Sotelo, C., and Dusart, I. (2000). Implication of Bcl-2 and Caspase-3 in age-related Purkinje cell death in murine organotypic culture: an in vitro model to study apoptosis. Eur. J. Neurosci. 12, 2935-2949.
52. Ghoumari, A. M., Wehrle, R., De Zeeuw, C. I., Sotelo, C., and Dusart, I. (2002). Inhibition of protein kinase C prevents Purkinje cell death but does not affect axonal regeneration. J. Neurosci. 22, 3531-3542.
53. Gianola, S., and Rossi, F. (2001). Evolution of the Purkinje cell response to injury and regenerative potential during postnatal development of the rat cerebellum. J. Comp. Neurol. 430, 101-117.
54. Gianola, S., Savio, T., Schwab, M. E., and Rossi, F. (2003). Cell-autonomous mechanisms and myelin-associated factors contribute to the development of Purkinje axon intracortical plexus in the rat cerebellum. J. Neurosci. 23, 4613-4624.
55. Gold, D. A., Gent, P. M., and Hamilton, B. A. (2007). ROR alpha in genetic control of cerebellum development: 50 staggering years. Brain Res. 1140, 19-25.
56. Goswami, J., Martin, L. A., Goldowitz, D., Beitz, A. J., and Feddersen, R. M. (2005). Enhanced Purkinje cell survival but compromised cerebellar function in targeted anti-apoptotic protein transgenic mice. Mol. Cell. Neurosci. 29, 202-221.
57. Hadj-Sahraoui, N., Seugnet, I., Ghorbel, M. T., and Demeneix, B. (2000). Hypothyroidism prolongs mitotic activity in the post-natal mouse brain. Neurosci. Lett. 280, 79-82.
58. Hamilton, B. A., Frankel, W. N., Kerrebrock, A. W., Hawkins, T. L., Fitzhugh, W., Kusumi, K., Russell, L. B., Mueller, K. L., Van Berkel, V., Birren, B. W., Kruglyak, L., and Lander, E. S. (1996). Disruption of the nuclear hormone receptor RORalpha in staggerer mice. Nature 379, 736-739.
59. Hashimoto, K., Curty, F. H., Borges, P. P., Lee, C. E., Abel, E. D., Elmquist, J. K., Cohen, R. N., and Wondisford, F. E. (2001). An unli-ganded thyroid hormone receptor causes severe neurological dysfunction. Proc. Natl. Acad. Sci. U.S.A. 98, 3998-4003.
60. Hashimoto, K., Ichikawa, R., Kitamura, K., Watanabe, M., and Kano, M. (2009). Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63, 106-118.
61. Hashimoto, K., and Kano, M. (2003). Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38, 785-796.
62. Heuer, H., and Mason, C. A. (2003). Thyroid hormone induces cerebellar Purkinje cell dendritic development via the thyroid hormone receptor alpha1. J. Neurosci. 23, 10604-10612.
63. Heuer, H., and Visser, T. J. (2009). Minireview: pathophysiological importance of thyroid hormone transporters. Endocrinology 150, 1078-1083.
64. Hurtado de Mendoza, T., Perez-Garcia, C. G., Kroll, T. T., Hoong, N. H., O'Leary, D. D., and Verma, I. M. (2011). Antiapoptotic protein Lifeguard is required for survival and maintenance of Purkinje and granular cells. Proc. Natl. Acad. Sci. U.S.A. 108, 17189-17194.
65. Ibarrola, N., and Rodriguez-Pena, A. (1997). Hypothyroidism coordinately and transiently affects myelin protein gene expression in most rat brain regions during postnatal development. Brain Res. 752, 285-293.
66. Ibhazehiebo, K., Iwasaki, T., Shimokawa, N., and Koibuchi, N. (2011). I, 2, 5, 6, 9, 10-alphaHexabromocyclo-dodecane (HBCD) impairs thyroid hormone-induced dendrite arborization of Purkinje cells and suppresses thyroid hormone receptor-mediated transcription. Cerebellum 10, 22-31.
67. Ichikawa, R., Yamasaki, M., Miyazaki, T., Konno, K., Hashimoto, K., Tatsumi, H., Inoue, Y., Kano, M., and Watanabe, M. (2011). Developmental switching of peri-somatic innervation from climbing fibers to basket cell fibers in cerebellar Purkinje cells. J. Neurosci. 31, 16916-16927.
68. Jankowski, J., Miething, A., Schilling, K., and Baader, S. L. (2009). Physiological Purkinje cell death is spatiotemporally organized in the developing mouse cerebellum. Cerebellum 8, 277-290.
69. Kalinovsky, A., Boukhtouche, F., Blazeski, R., Bornmann, C., Suzuki, N., Mason, C. A., and Scheiffele, P. (2011). Development of axon-target specificity of ponto-cerebellar affer-ents. PLoS Biol. 9:e1001013. doi: 10.1371/journal.pbio.1001013
70. Kaneko, M., Yamaguchi, K., Eiraku, M., Sato, M., Takata, N., Kiyohara, Y., Mishina, M., Hirase, H., Hashikawa, T., and Kengaku, M. (2011). Remodeling of mono-planar Purkinje cell dendrites during cerebellar circuit formation. PLoS One 6:e20108. doi: 10.1371/journal.pone.0020108
71. Kano, M., and Hashimoto, K. (2009). Synapse elimination in the central nervous system. Curr. Opin. Neurobiol. 19, 154-161.
72. Kim, B. J., Takamoto, N., Yan, J., Tsai, S. Y., and Tsai, M. J. (2009). Chicken Ovalbumin Upstream Promoter-Transcription Factor II (COUP-TFII) regulates growth and patterning of the postnatal mouse cerebellum. Dev. Biol. 326, 378-391.
73. Kitao, Y., Hashimoto, K., Matsuyama, T., Iso, H., Tamatani, T., Hori, O., Stern, D. M., Kano, M., Ozawa, K., and Ogawa, S. (2004). ORP150/HSP12A regulates Purkinje cell survival: a role for endoplasmic reticulum stress in cerebellar development. J. Neurosci. 24, 1486-1496.
74. Koibuchi, N., and Chin, W. W. (2000). Thyroid hormone action and brain development. Trends Endocrinol. Metab. 11, 123-128.
75. Koibuchi, N., Yamaoka, S., and Chin, W. W. (2001). Effect of altered thyroid status on neurotrophin gene expression during postnatal development of the mouse cerebellum. Thyroid11, 205-210.
76. Kole, A. J., Swahari, V., Hammond, S. M., and Deshmukh, M. (2011). miR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. GenesDev. 25, 125-130.
77. Kress, E., Samarut, J., and Plateroti, M. (2009). Thyroid hormones and the control of cell proliferation or cell differentiation: paradox or duality? Mol. Cell. Endocrinol. 313, 36-49.
78. Kriaucionis, S., and Heintz, N. (2009). The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930.
79. Larramendi, L. M. (1969). "Analysis of synaptogenesis in the cerebellum of the mouse, " in Neurobiology of Cerebellar Evolution and Development, ed R. Llinas (Chicago: American Medical Association), 803-843.
80. Lazarus, K. J., Bradshaw, R. A., West, N. R., and Bunge, P. (1976). Adaptive survival or rat sympathetic neurons cultured without supporting cells or exogenous nerve growth factor. Brain Res. 113, 159-164.
81. Letellier, M., Bailly, Y., Demais, V., Sherrard, R. M., Mariani, J., and Lohof, A. M. (2007). Reinnervation of late postnatal Purkinje cells by climbing fibers: neosynap-togenesis without transient multi-innervation. J. Neurosci. 27, 5373-5383.
82. Letellier, M., Wehrle, R., Mariani, J., and Lohof, A. M. (2009). Synapse elimination in olivo-cerebellar explants occurs during a critical period and leaves an indelible trace in Purkinje cells. Proc. Natl. Acad. Sci. U.S.A. 106, 14102-14107.
83. Levine, J. M., Stincone, F., and Lee, Y. S. (1993). Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7, 307-321.
84. Lindholm, D., Castren, E., Tsoulfas, P., Kolbeck, R., Berzaghi Mda, P., Leingartner, A., Heisenberg, C. P., Tessarollo, L., Parada, L. F., and Thoenen, H. (1993). Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J. Cell Biol. 122, 443-450.
85. Madalosso, S. H., Perez-Villegas, E. M., and Armengol, J. A. (2005). Naturally occurring neuronal death during the postnatal development of Purkinje cells and their pre-cerebellar afferent projections. Brain Res. Brain Res. Rev. 49, 267-279.
86. Manzano, J., Bernal, J., and Morte, B. (2007a). Influence of thyroid hormones on maturation of rat cerebellar astrocytes. Int. J. Dev. Neurosci. 25, 171-179.
87. Manzano, J., Cuadrado, M., Morte, B., and Bernal, J. (2007b). Influence of thyroid hormone and thyroid hormone receptors in the generation of cerebellar gamma-aminobutyric acid-ergic interneurons from precursor cells. Endocrinology 148, 5746-5751.
88. Mariani, J., and Changeux, J. P. (1981). Ontogenesis of olivocerebellar relationships. I. Studies by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J. Neurosci. 1, 696-702.
89. Marin-Teva, J. L., Dusart, I., Colin, C., Gervais, A., Van Rooijen, N., and Mallat, M. (2004). Microglia promote the death of developing Purkinje cells. Neuron 41, 535-547.
90. Marta, C. B., Adamo, A. M., Soto, E. F., and Pasquini, J. M. (1998). Sustained neonatal hyperthyroidism in the rat affects myelination in the central nervous system. J. Neurosci. Res. 53, 251-259.
91. Mason, C. A., Christakos, S., and Catalano, S. M. (1990). Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J. Comp. Neurol. 297, 77-90.
92. Mason, C. A., and Gregory, E. (1984). Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons. J. Neurosci. 4, 1715-1735.
93. McNabb, F. M. (2006). Avian thyroid development and adaptive plasticity. Gen. Comp. Endocrinol. 147, 93-101.
94. Mellstrom, B., Naranjo, J. R., Santos, A., Gonzalez, A. M., and Bernal, J. (1991). Independent expression of the alpha and beta c-erbA genes in developing rat brain. Mol. Endocrinol. 5, 1339-1350.
95. Miale, I. L., and Sidman, R. L. (1961). An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 4, 277-296.
96. Mikawa, S., Wang, C., Shu, F., Wang, T., Fukuda, A., and Sato, K. (2002). Developmental changes in KCC1, KCC2 and NKCC1 mRNAs in the rat cerebellum. Brain Res. Dev. Brain Res. 136, 93-100.
97. Minichiello, L., and Klein, R. (1996). TrkB and TrkC neurotrophin receptors cooperate in promoting survival of hippocampal and cerebellar granule neurons. Genes Dev. 10, 2849-2858.
98. Morara, S., Van Der Want, J. J., De Weerd, H., Provini, L., and Rosina, A. (2001). Ultrastructural analysis of climbing fiber-Purkinje cell synaptogenesis in the rat cerebellum. Neuroscience 108, 655-671.
99. Morel, M. P., Dusart, I., and Sotelo, C. (2002). Sprouting of adult Purkinje cell axons in lesioned mouse cerebellum: "non-permissive" versus "permissive" environment. J. Neurocytol. 31, 633-647.
100. Morte, B., Manzano, J., Scanlan, T., Vennstrom, B., and Bernal, J. (2002). Deletion of the thyroid hormone receptor alpha 1 prevents the structural alterations of the cerebellum induced by hypothyroidism. Proc. Natl. Acad. Sci. U.S.A. 99, 3985-3989.
101. Neveu, I., and Arenas, E. (1996). Neurotrophins promote the survival and development of neurons in the cerebellum of hypothyroid rats in vivo. J. Cell Biol. 133, 631-646.
102. Nicholson, J. L., and Altman, J. (1972). Synaptogenesis in the rat cerebellum: effects of early hypo-and hyperthyroidism. Science 176, 530-532.
103. Nieto-Bona, M. P., Busiguina, S., and Torres-Aleman, I. (1995). Insulinlike growth factor I is an afferent trophic signal that modulates calbindin-28kD in adult Purkinje cells. J. Neurosci. Res. 42, 371-376.
104. Oppenheim, R. W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
105. Oppenheimer, J. H., and Schwartz, H. L. (1997). Molecular basis ofthyroid hormone-dependent brain development. Endocr. Rev. 18, 462-475.
106. Orduz, D., and Llano, I. (2007). Recurrent axon collaterals underlie facilitating synapses between cerebellar Purkinje cells. Proc. Natl. Acad. Sci. U.S.A. 104, 17831-17836.
107. Orike, N., Middleton, G., Borthwick, E., Buchman, V., Cowen, T., and Davies, A. M. (2001). Role of PI 3-kinase, Akt and Bcl-2-related proteins in sustaining the survival of neurotrophic factor-independent adult sympathetic neurons. J. Cell Biol. 154, 995-1005.
108. Picou, T., Fauquier, F., Chatonnet, F., and Flamant, F. (2012). A bimodal influence of thyroid hormone on cerebellum oligodendrocyte differentiation. Mol. Endocrinol. 26, 608-618.
109. Pierce, D. R., Williams, D. K., and Light, K. E. (1999). Purkinje cell vulnerability to developmental ethanol exposure in the rat cerebellum. Alcohol. Clin. Exp. Res. 23, 1650-1659.
110. Portella, A. C., Carvalho, F., Faustino, L., Wondisford, F. E., Ortiga-Carvalho, T. M., and Gomes, F. C. (2010). Thyroid hormone receptor beta mutation causes severe impairment of cerebellar development. Mol. Cell. Neurosci. 44, 68-77.
111. Poulain, F. E., Chauvin, S., Wehrle, R., Desclaux, M., Mallet, J., Vodjdani, G., Dusart, I., and Sobel, A. (2008). SCLIP is crucial for the formation and development of the Purkinje cell dendritic arbor. J. Neurosci. 28, 7387-7398.
112. Putcha, G. V., Deshmukh, M., and Johnson, E. M. Jr. (2000). Inhibition of apoptotic signaling cascades causes loss of trophic factor dependence during neuronal maturation. J. Cell Biol. 149, 1011-1018.
113. Qin, J., Suh, J. M., Kim, B. J., Yu, C. T., Tanaka, T., Kodama, T., Tsai, M. J., and Tsai, S. Y. (2007). The expression pattern of nuclear receptors during cerebellar development. Dev. Dyn. 236, 810-820.
114. Qiu, C. H., Miyazaki, W., Iwasaki, T., Londono, M., Ibhazehiebo, K., Shimokawa, N., and Koibuchi, N. (2009). Retinoic Acid receptor-related orphan receptor alpha-enhanced thyroid hormone receptor-mediated transcrip tion requires its ligand binding domain which is not, by itself, sufficient: possible direct interaction of two receptors. Thyroid 19, 893-898.
115. Quignodon, L., Legrand, C., Allioli, N., Guadano-Ferraz, A., Bernal, J., Samarut, J., and Flamant, F. (2004). Thyroid hormone signaling is highly heterogeneous during pre-and postnatal brain development. J. Mol. Endocrinol. 33, 467-476.
116. Quignodon, L., Vincent, S., Winter, H., Samarut, J., and Flamant, F. (2007). A point mutation in the activation function 2 domain of thyroid hormone receptor alpha1 expressed after CRE-mediated recombination partially recapitulates hypothyroidism. Mol. Endocrinol. 21, 2350-2360.
117. Raff, M. C., Barres, B. A., Burne, J. F., Coles, H. S., Ishizaki, Y., and Jacobson, M. D. (1994). Programmed cell death and the control of cell survival. Philos. Trans. R. Soc. Lond. B Biol. Sci. 345, 265-268.
118. Rakotomamonjy, J., Levenes, C., Baulieu, E. E., Schumacher, M., and Ghoumari, A. M. (2011). Novel protective effect of mifepristone on detrimental GABAA receptor activity to immature Purkinje neurons. FASEB J. 25, 3999-4010.
119. Repici, M., Wehrle, R., Antoniou, X., Borsello, T., and Dusart, I. (2011). c-Jun N-terminal kinase (JNK) and p38 play different roles in age-related Purkinje cell death in murine organotypic culture. Cerebellum 10, 281-290.
120. Rinehart, J., Vazquez, N., Kahle, K. T., Hodson, C. A., Ring, A. M., Gulcicek, E. E., Louvi, A., Bobadilla, N. A., Gamba, G., and Lifton, R. P. (2011). WNK2 kinase is a novel regulator of essential neuronal cation-chloride cotransporters. J. Biol. Chem. 286, 30171-30180.
121. Rocamora, N., Garcia-Ladona, F. J., Palacios, J. M., and Mengod, G. (1993). Differential expression of brain-derived neurotrophic factor, neurotrophin-3, and low-affinity nerve growth factor receptor during the postnatal development of the rat cerebellar system. Brain Res. Mol. Brain Res. 17, 1-8.
122. Sajan, S. A., Waimey, K. E., and Millen, K. J. (2010). Novel approaches to studying the genetic basis of cerebellar development. Cerebellum 9, 272-283.
123. Schwab, M. E., and Bartholdi, D. (1996). Degeneration and regeneration of axons in the lesioned spinal cord. Physiol. Rev. 76, 319-370.
124. Sherrard, R. M., Dixon, K. J., Bakouche, J., Rodger, J., Lemaigre-Dubreuil, Y., and Mariani, J. (2009). Differential expression of TrkB isoforms switches climbing fiber-Purkinje cell synaptogenesis to selective synapse elimination. Dev. Neurobiol. 69, 647-662.
125. Sidman, R. L., Lane, P. W., and Dickie, M. M. (1962). Staggerer, a new mutation in the mouse affecting the cerebellum. Science 137, 610-612.
126. Sofroniew, M. V., Cooper, J. D., Svendsen, C. N., Crossman, P., Lindsay, R. M., Zafra, F., and Lindholm, D. (1993). Atrophy but not death of adult septal cholinergic neurons after ablation of target capacity to produce mRNAs for NGF, BDNF, and NT3. J. Neurosci. 13, 5263-5276.
127. Sofroniew, M. V., Galletly, N. P., Isacson, O., and Svendsen, C. N. (1990). Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science 247, 338-342.
128. Sotelo, C. (2004). Cellular and genetic regulation of the development of the cerebellar system. Prog. Neurobiol. 72, 295-339.
129. Sotelo, C. (2008). Development of "Pinceaux" formations and dendritic translocation of climbing fibers during the acquisition of the balance between glutamater-gic and gamma-aminobutyric acidergic inputs in developing Purkinje cells. J. Comp. Neurol. 506, 240-262.
130. Sotelo, C., and Dusart, I. (2009). Intrinsic versus extrinsic determinants during the development of Purkinje cell dendrites. Neuroscience 162, 589-600.
131. Strait, K. A., Zou, L., and Oppenheimer, J. H. (1992). Beta 1 isoform-specific regulation of a triiodothyronine-induced gene during cerebellar development. Mol. Endocrinol. 6, 1874-1880.
132. Svendsen, C. N., Kew, J. N., Staley, K., and Sofroniew, M. V. (1994). Death of developing septal cholinergic neurons following NGF withdrawal in vitro: protection by protein synthesis inhibition. J. Neurosci. 14, 75-87.
133. Takayama, C., and Inoue, Y. (2007). Developmental localization of potassium chloride co-transporter 2 (KCC2) in the Purkinje cells of embryonic mouse cerebellum. Neurosci. Res. 57, 322-325.
134. Takeda, T., and Maekawa, K. (1989). Transient direct connection of vestibular mossy fibers to the vestibulocerebellar Purkinje cells in early postnatal development of kittens. Neuroscience 32, 99-111.
135. Tata, J. R. (2006). Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol. Cell. Endocrinol. 246, 10-20.
136. Tsutsui, K. (2008). Neurosteroids in the Purkinje cell: biosynthesis, mode of action and functional significance. Mol. Neurobiol. 37, 116-125.
137. van Welie, I., Smith, I. T., and Watt, A. J. (2011). The metamorphosis of the developing cerebellar microcircuit. Curr. Opin. Neurobiol. 21, 245-253.
138. Vaughn, A. E., and Deshmukh, M. (2008). Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10, 1477-1483.
139. Velier, J. J., Ellison, J. A., Fisher, R. S., and Vinters, H. V. (1997). The trkC receptor is transiently localized to Purkinje cell dendrites during outgrowth and maturation in the rat. J. Neurosci. Res. 50, 649-656.
140. Verhoelst, C. H., Roelens, S. A., and Darras, V. M. (2005). Role of spa-tiotemporal expression of iodothy-ronine deiodinase proteins in cerebellar cell organization. Brain Res. Bull. 67, 196-202.
141. Verhoelst, C. H., Vandenborne, K., Severi, T., Bakker, O., Zandieh Doulabi, B., Leonard, J. L., Kuhn, E. R., Van Der Geyten, S., and Darras, V. M. (2002). Specific detection of type III iodothyronine deio-dinase protein in chicken cerebellar purkinje cells. Endocrinology 143, 2700-2707.
142. Wallis, K., Dudazy, S., Van Hogerlinden, M., Nordstrom, K., Mittag, J., and Vennstrom, B. (2010). The Thyroid hormone receptor {alpha}1 protein is expressed in embryonic postmitotic neurons and persists in most adult neurons. Mol. Endocrinol. 24, 1904-1916.
143. Watt, A. J., Cuntz, H., Mori, M., Nusser, Z., Sjostrom, P. J., and Hausser, M. (2009). Traveling waves in developing cerebellar cortex mediated by asymmetrical Purkinje cell connectivity. Nat. Neurosci. 12, 463-473.
144. Weiss, R. E., and Refetoff, S. (2000). Resistance to thyroid hormone. Rev. Endocr. Metab. Disord. 1, 97-108.
145. Winter, H., Ruttiger, L., Muller, M., Kuhn, S., Brandt, N., Zimmermann, U., Hirt, B., Bress, A., Sausbier, M., Conscience, A., Flamant, F., Tian, Y., Zuo, J., Pfister, M., Ruth, R, Lowenheim, H., Samarut, J., Engel, J., and Knipper, M. (2009). Deafness in TRbeta mutants is caused by malformation of the tectorial membrane. J. Neurosci. 29, 2581-2587.
146. Wright, K. M., and Deshmukh, M. (2006). Restricting apoptosis for postmitotic cell survival and its relevance to cancer. Cell Cycle 5, 1616-1620.
147. Wright, K. M., Smith, M. I., Farrag, L., and Deshmukh, M. (2007). Chromatin modification of Apaf-1 restricts the apoptotic pathway in mature neurons. J. Cell Biol. 179, 825-832.
148. Yan, Q., and Johnson, E. M. Jr. (1988). An immunohistochemical study of the nerve growth factor receptor in developing rats. J. Neurosci. 8, 3481-3498.
149. Zanjani, H. S., Vogel, M. W., Delhaye-Bouchaud, N., Martinou, J. C., and Mariani, J. (1996). Increased cerebellar Purkinje cell numbers in mice overexpressing a human bcl-2 transgene. J. Comp. Neurol. 374, 332-341.