Cerebellum: Links between development, developmental disorders and motor learning

Frontiers in Neuroanatomy

Volumn , Issue JANUARY 2012, 2012, Pages

  Manto, Mario U ^a   Jissendi, Patrice ^a  

^a ERASME HOSPITAL   (Belgium)

Author keywords

Cerebellum; Developmental; Genes; Inferior olive; Learning; Purkinje neurons; Transcription factors

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; NEUROTRANSMITTER; PANCREATIC TRANSCRIPTION FACTOR 1A; REELIN; SONIC HEDGEHOG PROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR MATH1; UNCLASSIFIED DRUG;

BRAIN MATURATION; BRAIN SIZE; CEREBELLUM; DEVELOPMENTAL DISORDER; DYSLEXIA; EMBRYO DEVELOPMENT; ENGRAILED 2 GENE; GABAERGIC SYSTEM; GENE; GENE MUTATION; GENETIC IMPROVEMENT; GRANULE CELL; HERC GENE; HUMAN; INTERNEURON; LEARNING; LEARNING DISORDER; MOTOR DEVELOPMENT; MOTOR PERFORMANCE; NERVE CELL DEGENERATION; NONHUMAN; PERINATAL PERIOD; PREMATURITY; PURKINJE CELL; RETINOIC ACID RELATED ORPHAN RECEPTOR ALPHA GENE; REVIEW; SENSORIMOTOR NEUROPATHY; STEROIDOGENESIS;

EID: 84856770080     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2012.00001     Document Type: Review

References (94)

1. Allin, M. P. G., Salaria, S., Nosarti, C., Wyatt, J., Rifkin, L., and Murray, R. M. (2005). Vermis and lateral lobes of the cerebellum in adolescents born very preterm. Neuroreport 16, 1821-1824.
2. Allin, M. P. G., Walshe, M., Fern, A., Nosarti, C., Rushe, T., Cuddy, M., Wyatt, J., Rifkin, L., and Murray, R. (2008). Cognitive maturation in preterm and term born adolescents. J. Neurol. Neurosurg. Psychiatry 79, 381-386.
3. Almli, C. R., Levy, T. J., Han, B. H., Shah, A. R., Gidday, J. M., and Holtzman, D. M. (2000). BDNF protects against spatial memory deficits following neonatal hypoxia-ischemia. Exp. Neurol. 166, 99-114.
4. Apps, R., and Lee, S. (2002). Central regulation of cerebellar climbing fibre input during motor learning. J. Physiol. 541, 301-317.
5. Aruga, J. (2004). The role of Zic genes in neural development. Mol. Cell. Neurosci. 26, 205-221.
6. Awasaki, T., and Ito, K. (2004). Engulfing action of glial cells isrequired for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 14, 668-677.
7. Beffert, U., Weeber, E. J., Morfini, G., Ko, J., Brady, S. T., Tsai, L. H., Sweatt, J. D., and Herz, J. (2004). Reelin and cyclin-dependent kinase 5-dependent signals cooperate in regulating neuronal migration and synaptic transmission. J. Neurosci. 24, 1897-1906.
8. Bermingham, N. A., Hassan, B. A., Wang, V. Y., Fernandez, M., Banfi, S., Bellen, H. J., Fritzsch, B., and Zoghbi, H. Y. (2001). Proprioceptor pathway development is dependent on Math1. Neuron 30, 411-422.
9. Bishop, D. V., and Snowling, M. J. (2004). Developmental dyslexia and specific language impairment: same or different? Psychol. Bull. 130, 858-886.
10. Bolduc, M. E., du Plessis, A. J., Sullivan, N., Guizard, N., Zhang, X., Robertson, R. L., and Limperopoulos, C. (2011). Regional cerebellar volumes predict functional outcome in children with cerebellar malformations. Cerebellum.
11. Boukhtouche, F., Vodjdani, G., Jarvis, C. I., Bakouche, J., Staels, B., Mallet, J., Mariani, J., Lemaigre-Dubreuil, Y., and Brugg, B. (2006). Human retinoic acid receptor-related orphan receptor alpha1 overexpression protects neurones against oxidative stress-induced apoptosis. J. Neurochem. 96, 1778-1789.
12. Byrne, M., Agerbo, E., Bennedsen, B., Eaton, W. W., and Mortensen, P. B. (2007). Obstetric conditions and risk of first admission with schizophrenia: a Danish national register based study. Schizophr. Res. 97, 51-59.
13. Carletti, B., and Rossi, F. (2008). Neurogenesis in the cerebellum. Neuroscientist 14, 91-100.
14. Cendelín, J., Korelusová, I., and Vozeh, F. (2009). The effect of cerebellar transplantation and enforced physical activity on motor skills and spatial learning in adult Lurcher mutant mice. Cerebellum 8, 35-45.
15. Chedotal, A., and Sotelo, C. (1993). The 'creeper stage' in cerebellar climbing fiber synaptogenesis precedes the 'pericellular nest' ultrastructural evidence with parvalbumin immunocytochemistry. Brain Res. Dev. Brain Res. 76, 207-220.
16. Cheh, M. A., Millonig, J. H., Roselli, L. M., Ming, X., Jacobsen, E., Kamdar, S., and Wagner, G. C. (2006). En2 knockout mice display neurobehav- ioral and neurochemical alterations relevant to autism spectrum disorder. Brain Res. 1116, 166-176.
17. Chen, C., Kano, M., Abeliovich, A., Chen, L., Bao, S., Kim, J. J., Hashimoto, K., Thompson, R. F., and Tonegawa, S. (1995). Impaired motor coordination correlates with persistent multiple climbing fiber innervation in PKC gamma mutant mice. Cell 83, 1233-1242.
18. Corrales, J. D., Blaess, S., Mahoney, E. M., and Joyner, A. L. (2006). The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133, 1811-1821.
19. Corrales, J. D., Rocco, G. L., Blaess, S., Guo, Q., and Joyner, A. L. (2004). Spatial pattern of sonic hedgehog signaling through Gli genes during cerebellum development. Development 131, 5581-5590.
20. Crépel, F., Mariani, J., and DelhayeBouchaud, N. (1976). Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J. Neurobiol. 7, 567-578.
21. DeCamp, D. L., Thompson, T. M., de Sauvage, F. J., and Lerner, M. R. (2000). Smoothened activates Galphai-mediated signaling in frog melanophores. J. Biol. Chem. 275, 26322-26327.
22. Dehart, D. B., Lanoue, L., Tint, G. S., and Sulik, K. K. (1997). Pathogenesis of malformations in a rodent model for Smith-Lemli- Opitz syndrome. Am. J. Med. Genet. 68, 328-337.
23. Delerive, P., Monté, D., Dubois, G., Trottein, F., Fruchart-Najib, J., Mariani, J., Fruchart, J. C., and Staels, B. (2001). The orphan nuclear receptor ROR alpha is a negative regulator of the inflammatory response. EMBO Rep. 2, 42-48.
24. Delgado-García, J. M., and Gruart, A. (2002). The role of interpositus nucleus in eyelid conditioned responses. Cerebellum 1, 289-308.
25. Dixon, K. J., Hilber, W., Speare, S. Willson, M. L., Bower, A. J., and Sherrard, R. M. (2005). Post-lesion transcommissural olivocerebellar reinnervation improves motor function following unilateral pedunculotomy in the neonatal rat. Exp. Neurol. 196, 254-265.
26. Drobyshevsky, A., Bregman, J., Storey, P., Meyer, J., Prasad, P. V., Derrick, M., MacKendrick, W., and Tan, S. (2007). Serial diffusion tensor imaging detects white matter changes that correlate with motor outcome in premature infants. Dev. Neurosci. 29, 289-301.
27. Dyet, L. E., Kennea, N., Counsell, S. J., Maalouf, E. F., Ajayi-Obe, M., Duggan, P. J., Harrison, M., Allsop, J. M., Hajnal, J., Herlihy, A. H., Edwards, B., Laroche, S., Cowan, F. M., Rutherford, M. A., and Edwards, A. D. (2006). Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118, 536-548.
28. Eccles, J. C., Llinás, R., and Sasaki, K. (1966). The excitatory synaptic action of climbing fibers on the Purkinje cells of the cerebellum. J. Physiol. 182, 268-296.
29. Ferretti, E., De Smaele, E., Miele, E., Laneve, P., Po, A., Pelloni, M., Paganelli, A., Di Marcotullio, L., Caffarelli, E., Screpanti, I., Bozzoni, I., and Gulino, A. (2008). Concerted microRNA control of Hedgehog signalling in cerebellar neuronal progenitor and tumour cells. EMBO J. 27, 2616-2627.
30. Fogarty, M. P., Emmenegger, B. A., Grasfeder, L. L., Oliver, T. G., and Wechsler-Reya, R. J. (2007). Fibroblast growth factor blocks Sonic hedgehog signaling in neu- ronal precursors and tumor cells. Proc. Natl. Acad. Sci. U.S.A. 104, 2973-2978.
31. Grimaldi, P., Parras, C., Guillemot, F., Rossi, F., and Wassef, M. (2009). Origins and control of the differentiation of inhibitory interneurons and glia in the cerebellum. Dev. Biol. 328, 422-433.
32. Hajós, F., Patel, A. J., and Balázs, R. (1973). Effect of thyroid deficiency on the synaptic organization of the rat cerebellar cortex. Brain Res. 50, 387-401.
33. 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 ROR in staggerer mice. Nature 379, 736-739.
34. Harvey, J. A., Welsh, J. P., Yeo, C. H., and Romano, A. G. (1993). Recoverable and nonrecoverable deficits in conditioned responses after cerebellar cortical lesions. J. Neurosci. 13, 1624-1635.
35. Hashimoto, K., and Kano, M. (2003). Functional differentiation of multiple climbing fiber inputs dur- ing synapse elimination in the developing cerebellum. Neuron 38, 785-796.
36. Huard, J. M., Forster, C. C., Carter, M. L., Sicinski, P., and Ross, M. E. (1999). Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 126, 1927-1935.
37. 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 life- guard is required for survival and maintenance of purkinje and granular cells. Proc. Natl. Acad. Sci. U.S.A. 108, 17189-17194.
38. Ichise, T., Kano, M., Hashimoto, K., Yanagihara, D., Nakao, K., Shigemoto, R., Katsuki, M., and Aiba, A. (2000). mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288, 1832-1835.
39. Ito, M. (2006). Cerebellar circuitry as a neuronal machine. Prog. Neurobiol. 78, 272-303.
40. Jetten, A. M. (2009). Retinoid-related orphan receptors (RORs): critical roles in development, immunity, circadian rhythm, and cellular metabolism. Nucl. Recept. Signal. 7, e003.
41. Joubert, M., Eisenring, J. J., Robb, J. P., and Andermann, F. (1969). Familial agenesis of the cerebellar vermis. A syndrome of episodic hyperpnea, abnormal eye movements, ataxia, and retardation. Neurology 19, 813-825.
42. Journiac, N., Jolly, S., Jarvis, C., Gautheron, V., Rogard, M., Trembleau, A., Blondeau, J. P., Mariani, J., and Vernet-der Garabedian, B. (2009). The nuclear receptor ROR(alpha) exerts a bi-directional regulation of IL-6 in resting and reactive astrocytes. Proc. Natl. Acad. Sci. U.S.A. 106, 21365-21370.
43. Koibuchi, N. (2008). The role of thyroid hormone on cerebellar development. Cerebellum 7, 530-533.
44. Koibuchi, N., Jingu, H., Iwasaki, T., and Chin, W. W. (2003). Current perspectives on the role of thyroid hormone in growth and development of cerebellum. Cerebellum 2, 279-289.
45. Kuemerle, B., Zanjani, H., Joyner, A., and Herrup, K. (1997). Pattern deformities and cell loss in Engrailed-2mutant mice suggest two separate patterning events during cerebellar development. J. Neurosci. 17, 7881-7889.
46. Landis, D. M., and Sidman, R. L. (1978). Electron microscopic analysis of postnatal histogenesis in the cerebellar cortex of staggerer mutant mice. J. Comp. Neurol. 179, 831-863.
47. Landis, S. C., and Mullen, R. J. (1978). The development and degeneration of Purkinje cells in pcd mutant mice. J. Comp. Neurol. 177, 125-143.
48. Lanoue, L., Dehart, D. B., Hinsdale, M. E., Maeda, N., Tint, G. S., and Sulik, K. K. (1997). Limb, genital, CNS, and facial malformations result from gene/environment-induced cholesterol deficiency: further evidence for a link to sonic hedgehog. Am. J. Med. Genet. 73, 24-31.
49. Leto, K., and Rossi, F.(2011). Specification and differentiation of cerebellar GABAergic neurons. Cerebellum.
50. Limperopoulos, C., Bassan, H., Sullivan, N. R., Soul, J. S., Robertson, R. L. Jr., Moore, M., Ringer, S. A., Volpe, J. J., and du Plessis, A. J. (2008). Positive screening for autism in ex-preterm infants: prevalence and risk factors. Pediatrics 121, 758-765.
51. Limperopoulos, C., Soul, J. S., Haidar, H., Huppi, P. S., Bassan, H., Warfield, S. K., Robertson, R. L., Moore, M., Akins, P., Volpe, J. J., and du Plessis, A. J. (2005). Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 116, 844-850.
52. Manto, M. (2010). Cerebellar Disorders. A Practical Approach to Diagnosis and Management. Cambridge, UK: Cambridge University Press.
53. Mariani, J., Benoit, P., Hoang, M. D., Thomson, M. A., and DelhayeBouchaud, N. (1990). Extent of multiple innervation of cerebellar Purkinje cells by climbing fibers in adult X-irradiated rats. Comparison of different schedules of irradia- tion during the first postnatal week. Brain Res. Dev. Brain Res. 57, 63-70.
54. Mashimo, T., Hadjebi, O., AmairPinedo, F., Tsurumi, T., Langa, F., Serikawa, T., Sotelo, C., Guénet, J. L., and Rosa, J. L. (2009). Progressive Purkinje cell degeneration in tambaleante mutant mice is a consequence of a missense muta- tion in HERC1 E3 ubiquitin ligase. PLoS Genet. 5, e1000784. doi: 10.1371/journal.pgen.1000784.
55. 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.
56. Narberhaus, A., Lawrence, E., Allin, M. P. G., Walshe, M., McGuire, P. K., Rifkin, L., Murray, R. M., and Nosarti, C. (2009). Neural substrates of visual paired associates in young adults with a history of very preterm birth: alterations in fronto-parieto-occipital networks and caudate nucleus. Neuroimage 47, 1884-1893.
57. Nicholson, J. L., and Altman, J. (1972). Synaptogenesis in the rat cerebellum: effects of early hypo- and hyperthyroidism. Science 176, 530-532.
58. Nicolson, R. I., and Fawcett, A. J. (1990). Automaticity: a new framework for dyslexia research? Cognition 35, 159-182.
59. Nicolson, R. I., and Fawcett, A. J. (2011). Dyslexia, dysgraphia, procedural learning and the cerebellum. Cortex 47, 117-127.
60. Nicolson, R. I., Fawcett, A. J., and Dean, P. (1995). Time estimation deficits in developmental dyslexia: evidence of cerebellar involvement. Proc. Biol. Sci. 259, 43-47.
61. Nicot, A., Lelievre, V., Tam, J., Waschek, J. A., and DiCicco-Bloom, E. (2002). Pituitary adenylate cyclase- activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J. Neurosci. 22, 9244-9254.
62. Pasquier, L., Marcorelles, P., Loget, P., Pelluard, F., Carles, D., Perez, M. J., Bendavid, C., de La Rochebrochard, C., Ferry, M., David, V., Odent, S., and Laquerrière, A. (2009). Rhombencephalosynapsis and related anomalies: a neuropathological study of 40 fetal cases. Acta. Neuropathol. 117, 185-200.
63. Porras-García,E.,Sánchezcampusano, R., Marti ́nez-Vargas, D., Domínguez-del-Toro, E., Cendelín, J., Vozeh, F., and Delgadogarcía, J. M. (2010). Behavioral characteristics, associative learning capabilities, and dynamic association mapping in an animal model of cerebellar degeneration. J. Neurophysiol. 104, 346-365.
64. Pujadas, L., Gruart, A., Bosch, C., Delgado, L., Teixeira, C. M., Rossi, D., de Lecea, L., Martínez, A., Delgado-García, J. M., and Soriano, E. (2010). Reelin regulates postna- tal neurogenesis and enhances spine hypertrophy and long-term potentiation. J. Neurosci. 30, 4636-4649.
65. Raoul, C., Pettmann, B., and Henderson, C. E. (2000). Active killing of neurons during develop- ment and following stress: a role for p75(NTR) and Fas? Curr. Opin. Neurobiol. 10, 111-117.
66. Rubin, J. B., Choi, Y., and Segal, R. A. (2002). Cerebellar proteoglycans regulate sonic hedgehog responses during development. Development 129, 2223-2232.
67. 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.
68. Sakamoto, H., Ukena, K., and Tsutsui, K. (2001). Effects of progesterone synthesized de novo in the developing Purkinje cell on its dendritic growth and synaptogenesis. J. Neurosci. 21, 6221-6232.
69. Sasahara, K., Shikimi, H., Haraguchi, S., Sakamoto, H., Honda, S., Harada, N., and Tsutsui, K. (2007). Mode of action and functional significance of estrogen-inducing dendritic growth, spinogenesis, and synaptogenesis in the developing Purkinje cell. J. Neurosci. 27, 7408-7417.
70. Scelfo, B., and Strata, P. (2005). Correlationbetween multiple climbing fiber regression and parallel fiber response development in the postnatal mouse cerebellum. Eur. J. Neurosci. 21, 971-978.
71. Schonewille, M., Gao, Z., Boele, H. J., Veloz, M. F., Amerika, W. E., Simek, A. A., De Jeu, M. T., Steinberg, J. P., Takamiya, K., Hoebeek, F. E., Linden, D. J., Huganir, R. L., and De Zeeuw, C. I. (2011). Reevaluating the role of LTD in cere- bellar motor learning. Neuron 70, 43-50.
72. Sellick, G. S., Barker, K. T., StolteDijkstra, I., Fleischmann, C., Coleman, R. J., Garrett, C., Gloyn, A. L., Edghill, E. L., Hattersley, A. T., Wellauer, P. K., Goodwin, G., and Houlston, R. S. (2004). Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat. Genet. 36, 1301-1305.
73. Sillitoe, R. V., Vogel, M. W., and Joyner, A. L. (2010). Engrailed homeobox genes regulate establishment of the cerebellar afferent circuit map. J. Neurosci. 30, 10015-10024.
74. Sotelo, C., and Alvarado-Mallart, R. M. (1986). Growth and differentiation of cerebellar suspensions transplanted into the adult cerebellum of mice with heredodegenerative ataxia. Proc. Natl. Acad. Sci. U.S.A. 83, 1135-1139.
75. Spassky, N., Han, Y. G., Aguilar, A., Strehl, L., Besse, L., Laclef, C., Ros, M. R., Garcia-Verdugo, J. M., and Alvarez-Buylla, A. (2008). Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev. Biol. 317, 246-259.
76. Spreen, O., Risser, A. H., and Edgell, D. (1995). Prematurity and Low BirthWeight.Developmental Neuropsychology.Oxford, UK: Oxford University Press.
77. Sudarov, A., Turnbull, R. K., Kim, E. J., Lebel-Potter, M., Guillemot, F., and Joyner, A. L. (2011). Ascl1 genetics reveals insights into cerebellum local circuit assembly. J. Neurosci. 31, 11055-11069.
78. Sugihara, I. (2005). Microzonal projection and climbing fiber remodeling in single olivocerebellar axons of newborn rats at postnatal days 4-7. J. Comp. Neurol. 487, 93-106.
79. Sugihara, I.(2006). Organization and remodeling of the olivocerebellar climbing fiber projection. Cerebellum 5, 15-22.
80. Sugihara, I., Lohof, A. M., Letellier, M., Mariani, J., and Sherrard, R. M. (2003). Post-lesion transcommissural growth of olivary climbing fibres creates functional synaptic microzones. Eur. J. Neurosci. 18, 3027-3036.
81. Sugihara, I., Wu, H-S., and Shinoda, Y. (1999). Morphology of single olivocerebellar axons labeled with biotinylated dextran amine in the rat. J. Comp. Neurol. 414, 131-148.
82. Sugihara, I., Wu, H-S., and Shinoda, Y. (2001). The entire trajectories of single olivocerebellar axons in the cerebellar cortex and their contribution to cerebellar compartmentalization. J. Neurosci. 21, 7715-7723.
83. Tsutsui, K. (2008). Progesterone biosynthesis and action in the developing neuron (review). Endocrinology 149, 2757-2761.
84. Vaillant, C., Didier-Bazes, M., Hutter, A., Belin, M. F., and Thomasset, N. (1999). Spatiotemporal expression patterns of metalloproteinases and their inhibitors in the post- natal developing rat cerebellum. J. Neurosci. 19, 4994-5004.
85. Vaillant, C., and Monard, D. (2009). SHH pathway and cerebellar development. Cerebellum 8, 291-301.
86. Wang, T., and Morgan, J. I. (2007). The Purkinje cell degeneration (pcd) mouse: an unexpected molecular link between neuronal degeneration and regeneration. Brain Res. 1140, 26-40.
87. Wechsler-Reya, R. J., and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114.
88. Wei, H., Zou, H., Sheikh, A. M., Malik, M., Dobkin, C., Brown, W. T., and Li, X. (2011). IL-6 is increased in the cerebellum of autistic brain and alters neural cell adhesion, migration and synaptic formation. J. Neuroinflammation 8, 52.
89. Weiner, H. L., Bakst, R., Hurlbert, M. S., Ruggiero, J., Ahn, E., Lee, W. S., Stephen, D., Zagzag, D., Joyner, A. L., and Turnbull, D. H. (2002). Induction of medulloblas- tomas in mice by sonic hedgehog, independent of Gli1. Cancer Res. 62, 6385-6389.
90. Wetts, R., and Herrup, K. (1982). Interaction of granule, Purkinje and inferior olivary neurons in lurcher chimeric mice. II. Granule cell death. Brain Res. 250, 358-362.
91. Willson, M. L., Bower, A. J., and Sherrard, R. M.(2007). Developmental neural plasticity and its cognitive benefits: olivocerebellar reinnervation com- pensates for spatial function in the cerebellum. Eur. J. Neurosci. 25, 1475-1483.
92. Yamada, M., Terao, M., Terashima, T., Fujiyama, T., Kawaguchi, Y., Nabeshima, Y., and Hoshino, M. (2007). Origin of climbing fiber neurons and their developmental dependence on Ptf1a. J. Neurosci. 27, 10924-10934.
93. Zou, Y. R., Kottmann, A. H., Kuroda, M., Taniuchi, I., and Littman, D. R. (1998). Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393, 595-599.
94. Zuo, J., De Jager, P. L., Takahashi, K. A., Jiang, W., Linden, D. J., and Heintz, N. (1997). Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature 388, 769-773.