Oligodendrocyte ablation affects the coordinated interaction between granule and Purkinje neurons during cerebellum development

Experimental Cell Research

Volumn 313, Issue 13, 2007, Pages 2946-2957

  Collin, Ludovic ^a   Doretto, Sandrine ^a,b   Malerba, Monica ^a,b   Ruat, Martial ^c   Borrelli, Emiliana ^a,b  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CNRS   (France)

Author keywords

Cerebellum development; Granule neurons; Oligodendrocytes; Purkinje cells; Transgenic mice

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; REELIN; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GLIA CELL; GRANULE CELL; IN VIVO STUDY; MALE; MOLECULAR INTERACTION; MOUSE; MYELIN SHEATH; NERVE FIBER; NONHUMAN; OLIGODENDROGLIA; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PURKINJE CELL; TRANSGENIC MOUSE;

ERINACEIDAE; MUS MUSCULUS; VERTEBRATA;

EID: 34547156089     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.05.003     Document Type: Article

References (79)

1. Sotelo C. Cellular and genetic regulation of the development of the cerebellar system. Prog. Neurobiol. 72 (2004) 295-339
2. Ramón y Cajal S. Sobre las fibras nerviosas de la capa granulosa del cerebelo. Int. Mon.schr. Anat. Physiol. 6 (1889) 158-174
3. Ramón y Cajal S. Studies on Vertebrate Neurogenesis (1960), Thomas, Springfield, IL 423
4. Ramón y Cajal S. Histologie du Système Nerveux de l'Homme et des Vertébrés (1911), A. Maloine, Paris
5. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus rhesus. J. Comp. Neurol. 141 (1971) 283-312
6. Palay S.F., and Chan-Palay V. Cerebellar Cortex, Cytology and Organization (1974), Springer-Verlag, Berlin
7. Miale I.L., and Sidman R.L. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 4 (1961) 277-296
8. Hatten M.E., and Heintz N. Mechanisms of neural patterning and specification in the developing cerebellum. Annu. Rev. Neurosci. 18 (1995) 385-408
9. Goldowitz D., and Hamre K. The cells and molecules that make a cerebellum. Trends Neurosci. 21 (1998) 375-382
10. Tissir F., and Goffinet A.M. Reelin and brain development. Nat. Rev., Neurosci. 4 (2003) 496-505
11. Rice D.S., and Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24 (2001) 1005-1039
12. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., and Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97 (1999) 689-701
13. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., and Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374 (1995) 719-723
14. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., and Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 24 (1999) 471-479
15. Wechsler-Reya R.J., and Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22 (1999) 103-114
16. Wallace V.A. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr. Biol. 9 (1999) 445-448
17. Traiffort E., Charytoniuk D., Watroba L., Faure H., Sales N., and Ruat M. Discrete localizations of hedgehog signalling components in the developing and adult rat nervous system. Eur. J. Neurosci. 11 (1999) 3199-3214
18. Miyazawa K., Himi T., Garcia V., Yamagishi H., Sato S., and Ishizaki Y. A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J. Neurosci. 20 (2000) 5756-5763
19. Lewis P.M., Gritli-Linde A., Smeyne R., Kottmann A., and McMahon A.P. Sonic hedgehog signaling is required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Dev. Biol. 270 (2004) 393-410
20. Huard J.M., Forster C.C., Carter M.L., Sicinski P., and Ross M.E. Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development (Cambridge, England) 126 (1999) 1927-1935
21. Dahmane N., and Ruiz-i-Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development (Cambridge, England) 126 (1999) 3089-3100
22. Shimada A., Mason C.A., and Morrison M.E. TrkB signaling modulates spine density and morphology independent of dendrite structure in cultured neonatal Purkinje cells. J. Neurosci. 18 (1998) 8559-8570
23. Segal R.A., Takahashi H., and McKay R.D. Changes in neurotrophin responsiveness during the development of cerebellar granule neurons. Neuron 9 (1992) 1041-1052
24. Schwartz P.M., Borghesani P.R., Levy R.L., Pomeroy S.L., and Segal R.A. Abnormal cerebellar development and foliation in BDNF-/- mice reveals a role for neurotrophins in CNS patterning. Neuron 19 (1997) 269-281
25. Morrison M.E., and Mason C.A. Granule neuron regulation of Purkinje cell development: striking a balance between neurotrophin and glutamate signaling. J. Neurosci. 18 (1998) 3563-3573
26. Courtney M.J., Akerman K.E., and Coffey E.T. Neurotrophins protect cultured cerebellar granule neurons against the early phase of cell death by a two-component mechanism. J. Neurosci. 17 (1997) 4201-4211
27. Borghesani P.R., Peyrin J.M., Klein R., Rubin J., Carter A.R., Schwartz P.M., Luster A., Corfas G., and Segal R.A. BDNF stimulates migration of cerebellar granule cells. Development (Cambridge, England) 129 (2002) 1435-1442
28. Bates B., Rios M., Trumpp A., Chen C., Fan G., Bishop J.M., and Jaenisch R. Neurotrophin-3 is required for proper cerebellar development. Nat. Neurosci. 2 (1999) 115-117
29. Collin L., Usiello A., Erbs E., Mathis C., and Borrelli E. Motor training compensates for cerebellar dysfunctions caused by oligodendrocyte ablation. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 325-330
30. Delaney C.L., Brenner M., and Messing A. Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. J. Neurosci. 16 (1996) 6908-6918
31. Djatchkova-Podkletnova I., and Alho H. Alterations in the development of rat cerebellum and impaired behavior of juvenile rats after neonatal 6-OHDA treatment. Neurochem. Res. 30 (2005) 1599-1605
32. Mathis C., Collin L., and Borrelli E. Oligodendrocyte ablation impairs cerebellum development. Development (Cambridge, England) 130 (2003) 4709-4718
33. Mathis C., Denisenko-Nehrbass N., Girault J.A., and Borrelli E. Essential role of oligodendrocytes in the formation and maintenance of central nervous system nodal regions. Development (Cambridge, England) 128 (2001) 4881-4890
34. Mathis C., Hindelang C., LeMeur M., and Borrelli E. A transgenic mouse model for inducible and reversible dysmyelination. J. Neurosci. 20 (2000) 7698-7705
35. Podkletnova I., and Alho H. Neonatal noradrenaline depletion prevents the transition of Bergmann glia in the developing cerebellum. J. Chem. Neuroanat. 14 (1998) 167-173
36. Traiffort E., Moya K.L., Faure H., Hassig R., and Ruat M. High expression and anterograde axonal transport of aminoterminal sonic hedgehog in the adult hamster brain. Eur. J. Neurosci. 14 (2001) 839-850
37. Delassalle A., Zalc B., Lachapelle F., Raoul M., Collier P., and Jacque C. Regional distribution of myelin basic protein in the central nervous system of quaking, jimpy, and normal mice during development and aging. J. Neurosci. Res. 6 (1981) 303-313
38. Hatten M.E. Central nervous system neuronal migration. Annu. Rev. Neurosci. 22 (1999) 511-539
39. Weyer A., and Schilling K. Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J. Neurosci. Res. 73 (2003) 400-409
40. Buttiglione M., Revest J.M., Rougon G., and Faivre-Sarrailh C. F3 neuronal adhesion molecule controls outgrowth and fasciculation of cerebellar granule cell neurites: a cell-type-specific effect mediated by the Ig-like domains. Mol. Cell. Neurosci. 8 (1996) 53-69
41. De Benedictis L., Bizzoca A., Corsi P., Albieri I., Consalez G.G., and Gennarini G. Activation profile of the F3/Contactin gene in the developing mouse cerebellum. Mol. Cell. Neurosci. 32 (2006) 403-418
42. Faivre-Sarrailh C., Gennarini G., Goridis C., and Rougon G. F3/F11 cell surface molecule expression in the developing mouse cerebellum is polarized at synaptic sites and within granule cells. J. Neurosci. 12 (1992) 257-267
43. Virgintino D., Ambrosini M., D'Errico P., Bertossi M., Papadaki C., Karagogeos D., and Gennarini G. Regional distribution and cell type-specific expression of the mouse F3 axonal glycoprotein: a developmental study. J. Comp. Neurol. 413 (1999) 357-372
44. Ben-Arie N., Bellen H.J., Armstrong D.L., McCall A.E., Gordadze P.R., Guo Q., Matzuk M.M., and Zoghbi H.Y. Math1 is essential for genesis of cerebellar granule neurons. Nature 390 (1997) 169-172
45. Bizzoca A., Virgintino D., Lorusso L., Buttiglione M., Yoshida L., Polizzi A., Tattoli M., Cagiano R., Rossi F., Kozlov S., Furley A., and Gennarini G. Transgenic mice expressing F3/contactin from the TAG-1 promoter exhibit developmentally regulated changes in the differentiation of cerebellar neurons. Development (Cambridge, England) 130 (2003) 29-43
46. Kuhar S.G., Feng L., Vidan S., Ross M.E., Hatten M.E., and Heintz N. Changing patterns of gene expression define four stages of cerebellar granule neuron differentiation. Development (Cambridge, England) 117 (1993) 97-104
47. Sakurai T., Lustig M., Babiarz J., Furley A.J., Tait S., Brophy P.J., Brown S.A., Brown L.Y., Mason C.A., and Grumet M. Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. J. Cell Biol. 154 (2001) 1259-1273
48. Stottmann R.W., and Rivas R.J. Distribution of TAG-1 and synaptophysin in the developing cerebellar cortex: relationship to Purkinje cell dendritic development. J. Comp. Neurol. 395 (1998) 121-135
49. Herrup K. Role of staggerer gene in determining cell number in cerebellar cortex: I. Granule cell death is an indirect consequence of staggerer gene action. Brain Res. 313 (1983) 267-274
50. Dumesnil-Bousez N., and Sotelo C. Early development of the Lurcher cerebellum: Purkinje cell alterations and impairment of synaptogenesis. J. Neurocytol. 21 (1992) 506-529
51. Jensen P., Zoghbi H.Y., and Goldowitz D. Dissection of the cellular and molecular events that position cerebellar Purkinje cells: a study of the math1 null-mutant mouse. J. Neurosci. 22 (2002) 8110-8116
52. Lin S.C., Huck J.H., Roberts J.D., Macklin W.B., Somogyi P., and Bergles D.E. Climbing fiber innervation of NG2-expressing glia in the mammalian cerebellum. Neuron 46 (2005) 773-785
53. Bouslama-Oueghlani L., Wehrle R., Sotelo C., and Dusart I. Heterogeneity of NG2-expressing cells in the newborn mouse cerebellum. Dev. Biol. 285 (2005) 409-421
54. Lindholm D., Hamner S., and Zirrgiebel U. Neurotrophins and cerebellar development. Perspect. Dev. Neurobiol. 5 (1997) 83-94
55. Huang E.J., and Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24 (2001) 677-736
56. Gorski J.A., Zeiler S.R., Tamowski S., and Jones K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J. Neurosci. 23 (2003) 6856-6865
57. Gao W.Q., Zheng J.L., and Karihaloo M. Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J. Neurosci. 15 (1995) 2656-2667
58. Segal R.A., Pomeroy S.L., and Stiles C.D. Axonal growth and fasciculation linked to differential expression of BDNF and NT3 receptors in developing cerebellar granule cells. J. Neurosci. 15 (1995) 4970-4981
59. Carter A.R., Berry E.M., and Segal R.A. Regional expression of p75NTR contributes to neurotrophin regulation of cerebellar patterning. Mol. Cell. Neurosci. 22 (2003) 1-13
60. Hay J.C., and Scheller R.H. SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 9 (1997) 505-512
61. Mariani J., Crepel F., Mikoshiba K., Changeux J.P., and Sotelo C. Anatomical, physiological and biochemical studies of the cerebellum from Reeler mutant mouse. Philos. Trans. R. Soc. Lond., B Biol. Sci. 281 (1977) 1-28
62. Miyata T., Nakajima K., Mikoshiba K., and Ogawa M. Regulation of Purkinje cell alignment by reelin as revealed with CR-50 antibody. J. Neurosci. 17 (1997) 3599-3609
63. Howell B.W., Herrick T.M., Hildebrand J.D., Zhang Y., and Cooper J.A. Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr. Biol. 10 (2000) 877-885
64. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., and Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24 (1999) 481-489
65. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., and D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41 (2004) 71-84
66. Altman J., and Bayer A.S. Summary: mechanisms in the development of the fine circuitry and the foliation of the cerebellar cortex. Development of the Cerebellar System in Relation to its Evolution, Structure and Functions (1997), CRC Press 684-725
67. Edgar J.M., Anderson T.J., Dickinson P.J., Barrie J.A., McCulloch M.C., Nave K.A., and Griffiths I.R. Survival of, and competition between, oligodendrocytes expressing different alleles of the Plp gene. J. Cell Biol. 158 (2002) 719-729
68. Wilkins A., Majed H., Layfield R., Compston A., and Chandran S. Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J. Neurosci. 23 (2003) 4967-4974
69. Kaplan M.R., Meyer-Franke A., Lambert S., Bennett V., Duncan I.D., Levinson S.R., and Barres B.A. Induction of sodium channel clustering by oligodendrocytes. Nature 386 (1997) 724-728
70. Kaplan M.R., Cho M.H., Ullian E.M., Isom L.L., Levinson S.R., and Barres B.A. Differential control of clustering of the sodium channels Na(v)1.2 and Na(v)1.6 at developing CNS nodes of Ranvier. Neuron 30 (2001) 105-119
71. Du Y., and Dreyfus C.F. Oligodendrocytes as providers of growth factors. J. Neurosci. Res. 68 (2002) 647-654
72. Dai X., Lercher L.D., Clinton P.M., Du Y., Livingston D.L., Vieira C., Yang L., Shen M.M., and Dreyfus C.F. The trophic role of oligodendrocytes in the basal forebrain. J. Neurosci. 23 (2003) 5846-5853
73. Dusart I., Airaksinen M.S., and Sotelo C. Purkinje cell survival and axonal regeneration are age dependent: an in vitro study. J. Neurosci. 17 (1997) 3710-3726
74. Charytoniuk D., Porcel B., Rodriguez Gomez J., Faure H., Ruat M., and Traiffort E. Sonic Hedgehog signalling in the developing and adult brain. J. Physiol. (Paris) 96 (2002) 9-16
75. van Dillen I.J., Mulder N.H., Vaalburg W., de Vries E.F., and Hospers G.A. Influence of the bystander effect on HSV-tk/GCV gene therapy. A review. Curr. Gene Ther. 2 (2002) 307-322
76. Rash J.E., Yasumura T., Dudek F.E., and Changeux J.P. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J. Neurosci. 21 (2001) 1983-2000
77. Goldowitz D., Cushing R.C., Laywell E., D'Arcangelo G., Sheldon M., Sweet H.O., Davisson M., Steindler D., and Curran T. Cerebellar disorganization characteristic of reeler in scrambler mutant mice despite presence of reelin. J. Neurosci. 17 (1997) 8767-8777
78. McCall M.A., Gregg R.G., Behringer R.R., Brenner M., Delaney C.L., Galbreath E.J., Zhang C.L., Pearce R.A., Chiu S.Y., and Messing A. Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiology. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 6361-6366
79. Pan B., Fromholt S.E., Hess E.J., Crawford T.O., Griffin J.W., Sheikh K.A., and Schnaar R.L. Myelin-associated glycoprotein and complementary axonal ligands, gangliosides, mediate axon stability in the CNS and PNS: neuropathology and behavioral deficits in single- and double-null mice. Exp. Neurol. 195 (2005) 208-217