Four distinct phases of basket/stellate cell migration after entering their final destination (the molecular layer) in the developing cerebellum

Developmental Biology

Volumn 332, Issue 2, 2009, Pages 309-324

  Cameron, D Bryant ^a   Kasai, Kazue ^b   Jiang, Yulan ^a   Hu, Taofang ^a   Saeki, Yoshinaga ^b   Komuro, Hitoshi ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Basket cell; Brain slices; Cerebellum; Early postnatal mice; Inhibitory interneurons; Neuronal cell migration; Stellate cell; Time lapse imaging

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL CONTACT; CELL MIGRATION; CEREBELLUM; CHRONOSEQUENCE; CONTROLLED STUDY; DENDRITE; FEMALE; MALE; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; STELLATE CELL; VELOCITY;

MUS;

EID: 67650985955     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.05.575     Document Type: Article

References (75)

1. Adams N.C., Tomoda T., Cooper M., Dietz G., and Hatten M.E. Mice that lack astrotactin have slowed neuronal migration. Development 129 (2002) 965-972
2. Altman J. Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J. Comp. Neurol. 145 (1972) 353-359
3. Altman J. Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J. Comp. Neurol. 145 (1972) 399-463
4. Anderson S.A., Marin O., Horn C., Jennings K., and Rubenstein J.L.R. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128 (2001) 353-363
5. Ang E.S.B.C., Haydar T.F., Gluncic V., and Rakic P. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J. Neurosci. 23 (2003) 5805-5815
6. Bix G.J., and Clark G.D. Platelet-activating factor receptor stimulation disrupts neuronal migration in vitro. J. Neurosci. 18 (1998) 307-318
7. 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 129 (2002) 1435-1442
8. Botia B., Basille M., Allais A., Raoult E., Falluel-Morel A., Galas L., Jolivel V., Wurtz O., Komuro H., Fournier A., Vaudry H., Burel D., Gonzalez B., and Vaudry D. Neurotrophic effects of PACAP in the cerebellar cortex. Peptides 28 (2007) 1746-1752
9. Cameron D.B., Galas L., Jiang Y., Raoult E., Vaudry D., and Komuro H. Cerebellar cortical-layer-specific control of neuronal migration by pituitary adenylate cyclase-activating polypeptide. Neuroscience 146 (2007) 697-712
10. Cameron, D.B., Raoult, E., Galas, L., Jiang, Y., Lee, K., Hu, T., Vaudry, D., Komuro, H., in press. Role of PACAP in controlling granule cell migration. Cerebellum. doi:10.1007/s12311-009-0121-9.
11. Doughty M.L., Lohof A., Campana A., Delhaye-Bouchaud N., and Mariani J. Neurotrophin-3 promotes cerebellar granule cell exit from the EGL. Eur. J. Neurosci. 10 (1998) 3007-3011
12. Fujita S. Quantitative analysis of cell proliferation and differentiation in the cortex of postnatal mouse cerebellum. J. Cell Biol. 32 (1967) 277-287
13. 3-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 (1966) 191-208
14. Ghashghaei H.T., Weber J., Penvy L., Schmid R., Schwab M.H., Lloyd K.C., Eisenstat D.D., Lai C., and Anton E.S. The role of neuregulin-ErbB4 interactions on the proliferation and organization of cells in the subventricular zone. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1930-1935
15. Guerrini R., and Filippi T. Neuronal migration disorders, genetics, and epileptogenesis. J. Child Neurol. 20 (2005) 287-299
16. Guijarro P., Simo S., Pascual M., Abasolo I., Del Rio J.A., and Soriano E. Netrin1 exerts a chemorepulsive effect on migrating cerebellar interneurons in a Dcc-independent way. Mol. Cell. Neurosci. 33 (2006) 389-400
17. Hallonet M.E.R., and Le Dourain N.M. Tracing neuroepithelial cells of the mesencephalic and metencephalic alar plates during cerebellar ontogeny in quail-chick chimeras. Eur. J. Neurosci. 5 (1993) 1145-1155
18. Hekmat A., Kunemund V., Fischer G., and Schachner M. Small inhibitory cerebellar interneurons grow in a perpendicular orientation to granule cell neurites in culture. Neuron 2 (1989) 1113-1122
19. Husmann K., Faissner A., and Schachner M. Tenascin promotes cerebellar granule cell migration and neurite outgrowth by different domains in the fibronectin type III repeats. J. Cell Biol. 116 (1992) 1475-1486
20. Jiang Y., Kumada T., Cameron D.B., and Komuro H. Cerebellar granule cell migration and the effects of alcohol. Dev. Neurosci. 30 (2008) 7-23
21. Kasai K., and Saeki Y. DNA-based methods to prepare helper virus-free herpes amplicon vectors and versatile design of amplicon vector plasmids. Curr. Gene Ther. 6 (2006) 303-314
22. Kerjan G., and Gleeson J.G. Genetic mechanisms underlying abnormal neuronal migration in classical lissencephaly. Trends Genet. 23 (2007) 623-630
23. 2+ transients control CNS neuronal migration. Cell Calcium 37 (2005) 387-393
24. Komuro H., and Rakic P. Selective role of N-type calcium channels in neuronal migration. Science 257 (1992) 806-809
25. Komuro H., and Rakic P. Modulation of neuronal migration by NMDA receptors. Science 260 (1993) 95-97
26. Komuro H., and Rakic P. Dynamics of granule cell migration: a confocal microscopic study in acute cerebellar slice preparations. J. Neurosci. 15 (1995) 1110-1120
27. 2+ fluctuations modulate the rate of neuronal migration. Neuron 17 (1996) 275-285
28. Komuro H., and Rakic P. Distinct modes of neuronal migration in different domains of developing cerebellar cortex. J. Neurosci. 18 (1998) 1478-1490
29. 2+ fluctuations. J. Neurobiol. 37 (1998) 110-130
30. Komuro H., and Rakic P. In vitro analysis of signal mechanisms involved in neuronal migration. In: Haynes L.W. (Ed). The Neuron in Tissue Culture (1999), John Wiley & Sons, New York 57-69
31. Komuro H., and Yacubova E. Recent advances in cerebellar granule cell migration. Cell. Mol. Life Sci. 60 (2003) 1084-1098
32. Komuro H., Yacubova E., Yacubova E., and Rakic P. Mode and tempo of tangential cell migration in the cerebellar external granular layer. J. Neurosci. 21 (2001) 527-540
33. Kriegstein A.R., and Noctor S.C. Pattern of neuronal migration in the embryonic cortex. Trends Neurosci. 27 (2004) 392-399
34. 2+ transients. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 8479-8484
35. Kumada T., Lakshmana M.K., and Komuro H. Reversal of Neuronal migration in a mouse model of fetal alcohol syndrome by controlling second-messenger signalings. J. Neurosci. 26 (2006) 742-756
36. Kumada T., Jiang Y., Cameron D.B., and Komuro H. How does alcohol impair neuronal migration?. J. Neurosci. Res. 85 (2007) 465-470
37. Kumada T., Jiang Y., Kawanami A., Cameron D.B., and Komuro H. Autonomous turning of cerebellar granule cells in vitro by intrinsic programs. Dev. Biol. 326 (2009) 237-259
38. Leto K., Carletti B., Williams I.M., Magrassi L., and Rossi F. Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J. Neurol. 26 (2006) 11682-11694
39. Ma Q., Jones D., Borghesani P.R., Segal R.A., Nagasawa T., Kishimoto T., Bronson R.T., and Springer T.A. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 9448-9453
40. Magyar-Lehmann S., Suter C.S., Stahel W., and Schachner M. Behaviour of small inhibitory interneurons in early postnatal mouse cerebellar microexplant cultures: a video time-lapse analysis. Eur. J. Neurosci. 7 (1995) 1449-1459
41. Maricich S.M., and Herrup K. Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J. Neurobiol. 41 (1999) 281-294
42. Marin O., and Rubenstein J.L.R. A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci. 2 (2001) 780-790
43. Marin O., and Rubenstein J.L.R. Cell migration in the forebrain. Ann. Rev. Neurosci. 26 (2003) 441-483
44. Miale I., and Sidman R.L. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp. Neurol. 4 (1961) 277-296
45. Milosevic A., and Goldman J.E. Progenitors in the postnatal cerebellar white matter are antigenically heterogeneous. J. Comp. Neurol. 452 (2002) 192-203
46. Milosevic A., and Goldman J.E. Potential of progenitors from postnatal cerebellar neuroepithelium and white matter: lineage specified vs. multipotent fate. Mol. Cell. Neurosci. 26 (2004) 342-353
47. Nadarajah B., and Parnavelas J.G. Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 4 (2002) 143-150
48. Napieralski J.A., and Eisenman L.M. Developmental analysis of the external granular layer in the meander tail mutant mouse: do cerebellar microneurons have independent progenitors?. Dev. Dynamics 197 (1993) 244-254
49. Otero R.A., Sotelo C., and Alvarado-Mallart R.-M. Chick/quail chimeras with partial cerebellar grafts: an analysis of the origin and migration of cerebellar cells. J. Comp. Neurol. 333 (1993) 597-615
50. Pang T., Atefy R., and Sheen V. Malformations of cortical development. Neurologist 14 (2008) 181-191
51. Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electron microscopic study in Macacus rhesus. J. Comp. Neurol. 141 (1971) 283-312
52. Rakic P. Kinetics of proliferation and latency between final cell division and onset of differentiation of cerebellar stellate and basket neurons. J. Comp. Neurol. 147 (1973) 523-546
53. Rakic P. Principles of neuronal cell migration. Experientia 46 (1990) 882-891
54. Rakic P. Molecular and cellular mechanisms of neuronal migration: relevance to cortical epilepsies. Adv. Neurol. 84 (2000) 1-14
55. Rakic P., and Komuro H. The role of receptor/channel activity in neuronal cell migration. J. Neurobiol. 26 (1995) 299-315
56. Rakic P., Cameron R.S., and Komuro H. Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr. Opin. Neurobiol. 4 (1994) 63-69
57. Rio C., Rieff H.I., Qi P., Khurana T.S., and Corfas G. Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19 (1997) 39-50
58. Saeki Y., Fraefel C., Ichikawa T., Breakefield X.O., and Chiocca E.A. Improved helper virus-free packaging system for HSV amplicon vectors using an ICP27-deleted, oversized HSV-1 DNA in a bacterial artificial chromosome. Mol. Ther. 3 (2001) 591-601
59. Saeki Y., Breakefield X.O., and Chiocca E.A. Improved HSV-1 amplicon packaging system using ICP27-deleted, oversized HSV-1 BAC DNA. Methods Mol. Med. 76 (2003) 51-60
60. Santiago M.F., Berredo-Pinho M., Costa M.R., Gandra M., Cavalcante L.A., and Mendez-Otero R. Expression and function of ganglioside 9-O-acetyl GD3 in postmitotic granule cell development. Mol. Cell. Neurosci. 17 (2001) 488-499
61. Seeds N.W., Basham M.E., and Haffke S.P. Neuronal migration is retarded in mice lacking the tissue plasminogen activator gene. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 14118-14123
62. Smith I.L., Hardwicke M.A., and Sandri-Goldin R.M. Evidence that the herpes simplex virus immediate early protein ICP27 acts post-transcriptionally during infection to regulate gene expression. Virology 186 (1992) 74-86
63. Tanaka D., Maekawa K., Yanagawa Y., Obata K., and Murakami F. Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development 133 (2006) 2167-2176
64. Tanaka D.H., Yanagida M., Zhu Y., Mikami S., Nagasawa T., Miyazaki J., Yanagawa Y., Obata K., and Murakami F. Random walk behavior of migrating cortical interneurons in the marginal zone: time-lapse analysis in flat-mount cortex. J. Neurol. 29 (2009) 1300-1311
65. Tashiro Y., Yanagawa Y., Obata K., and Murakami F. Development and migration of GABAergic neurons in the mouse myelencephalon. J. Comp. Neurol. 503 (2007) 260-269
66. Ten Donkelaar H.J., Lammens M., Wesseling P., Thijessen H.O., and Renier W.O. Development and developmental disorders of the human cerebellum. J. Neurol. 250 (2003) 1025-1036
67. Weisheit G., Gliem M., Endl E., Pfeffer P.L., Busslinger M., and Schilling K. Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur. J. Neurosci. 24 (2006) 466-478
68. Yacubova E., and Komuro H. Intrinsic program for migration of cerebellar granule cells in vitro. J. Neurosci. 22 (2002) 5966-5981
69. Yacubova E., and Komuro H. Stage-specific control of neuronal migration by somatostatin. Nature 415 (2002) 77-81
70. Yacubova E., and Komuro H. Cellular and molecular mechanisms of cerebellar granule cell migration. Cell Biochem. Biophys. 37 (2003) 213-234
71. Yamanaka H., Yanagawa Y., and Obata K. Development of stellate and basket cells and their apoptosis in mouse cerebellar cortex. Neurosci. Res. 50 (2004) 13-22
72. Yip J., Soghomonian J.-J., and Blatt G.J. Increased GAD67 mRNA expression in cerebellar interneurons in autism: implications for Purkinje cell dysfunction. J. Neurosci. Res. 86 (2008) 525-530
73. Zhang L., and Goldman J.E. Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16 (1996) 47-54
74. Zhang L., and Goldman J.E. Developmental fates and migratory pathways of dividing progenitors in the postnatal rat cerebellum. J. Comp. Neurol. 370 (1996) 536-550
75. Zou Y.R., Kottmann A.H., Kuroda M., Taniuchi I., and Littman D.R. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393 (1998) 595-599