 |
Previous Article | Next Article 
Journal of Neuroscience, Vol 15, 981-989, Copyright © 1995 by Society for Neuroscience
Motility and cytoskeletal organization of migrating cerebellar granule neurons
RJ Rivas and ME Hatten
Rockefeller University, New York, New York 10021-6399.
To characterize CNS neuronal precursor migration along astroglial fibers,
we examined the motility of the migratory leading process and
cytoskeletal-based mechanisms of locomotion of early postnatal mouse
cerebellar granule neurons in vitro. To visualize the surface motility of
the leading process, granule neurons were labeled with the fluorescent
lipophilic dye, PKH-26, and imaged by time lapse fluorescence microscopy.
The motile behavior and cytoskeletal organization of the migrating neuron
had several distinctive features. As the migrating neuron moved along the
glial fiber, the leading process rapidly extended, projecting up to 40
microns, and retracted, withdrawing towards the cell soma. Broad
lamellipodia were common along the entire length of the leading process,
giving it a ruffled appearance. Within the cell soma, a cage-like
distribution of microtubules encircled the nucleus and actin filaments
formed a subcortical rim underneath the plasma membrane. Disruption of
actin filaments with cytochalasin B inhibited migration, suggesting
involvement of actin subunit assembly in neuronal migration. Both
microtubules and actin filaments were heavily concentrated in the leading
process; the leading process did not show the development of a distinct
actin-rich domain at its tip.
This article has been cited by other articles:

|
 |

|
 |
 
J. M. Weimer, Y. Yokota, A. Stanco, D. J. Stumpo, P. J. Blackshear, and E.S. Anton
MARCKS modulates radial progenitor placement, proliferation and organization in the developing cerebral cortex
Development,
September 1, 2009;
136(17):
2965 - 2975.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Razafsky and D. Hodzic
Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections
J. Cell Biol.,
August 24, 2009;
186(4):
461 - 472.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. M. Bilimoria and A. Bonni
Cultures of Cerebellar Granule Neurons
CSH Protocols,
December 1, 2008;
2008(13):
pdb.prot5107 - pdb.prot5107.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
C. Metin, R. B. Vallee, P. Rakic, and P. G. Bhide
Modes and Mishaps of Neuronal Migration in the Mammalian Brain
J. Neurosci.,
November 12, 2008;
28(46):
11746 - 11752.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Calderon de Anda, A. Gartner, L.-H. Tsai, and C. G. Dotti
Pyramidal neuron polarity axis is defined at the bipolar stage
J. Cell Sci.,
January 15, 2008;
121(2):
178 - 185.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Hirota, T. Ohshima, N. Kaneko, M. Ikeda, T. Iwasato, A. B. Kulkarni, K. Mikoshiba, H. Okano, and K. Sawamoto
Cyclin-Dependent Kinase 5 Is Required for Control of Neuroblast Migration in the Postnatal Subventricular Zone
J. Neurosci.,
November 21, 2007;
27(47):
12829 - 12838.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Umeshima, T. Hirano, and M. Kengaku
Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons
PNAS,
October 9, 2007;
104(41):
16182 - 16187.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. C. Bellenchi, C. B. Gurniak, E. Perlas, S. Middei, M. Ammassari-Teule, and W. Witke
N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex
Genes & Dev.,
September 15, 2007;
21(18):
2347 - 2357.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Borrell, B. K. Kaspar, F. H. Gage, and E. M. Callaway
In vivo Evidence for Radial Migration of Neurons by Long-Distance Somal Translocation in the Developing Ferret Visual Cortex
Cereb Cortex,
November 1, 2006;
16(11):
1571 - 1583.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. S. B. C. Ang Jr, V. Gluncic, A. Duque, M. E. Schafer, and P. Rakic
From the Cover: Prenatal exposure to ultrasound waves impacts neuronal migration in mice
PNAS,
August 22, 2006;
103(34):
12903 - 12910.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. M. Morozov, A. E. Ayoub, and P. Rakic
Translocation of Synaptically Connected Interneurons across the Dentate Gyrus of the Early Postnatal Rat Hippocampus.
J. Neurosci.,
May 10, 2006;
26(19):
5017 - 5027.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. P. Farwell, S. A. Dubord-Tomasetti, A. Z. Pietrzykowski, and J. L. Leonard
Dynamic Nongenomic Actions of Thyroid Hormone in the Developing Rat Brain
Endocrinology,
May 1, 2006;
147(5):
2567 - 2574.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. C. Olson, S. Kim, and C. A. Walsh
Impaired Neuronal Positioning and Dendritogenesis in the Neocortex after Cell-Autonomous Dab1 Suppression
J. Neurosci.,
February 8, 2006;
26(6):
1767 - 1775.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Toyo-Oka, S. Sasaki, Y. Yano, D. Mori, T. Kobayashi, Y. Y. Toyoshima, S. M. Tokuoka, S. Ishii, T. Shimizu, M. Muramatsu, et al.
Recruitment of katanin p60 by phosphorylated NDEL1, an LIS1 interacting protein, is essential for mitotic cell division and neuronal migration
Hum. Mol. Genet.,
November 1, 2005;
14(21):
3113 - 3128.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Gonzalez-Billault, J. A. Del Rio, J. M. Urena, E. M. Jimenez-Mateos, M. J. Barallobre, M. Pascual, L. Pujadas, S. Simo, A. L. Torre, R. Gavin, et al.
A role of MAP1B in Reelin-dependent Neuronal Migration
Cereb Cortex,
August 1, 2005;
15(8):
1134 - 1145.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Bellion, J.-P. Baudoin, C. Alvarez, M. Bornens, and C. Metin
Nucleokinesis in Tangentially Migrating Neurons Comprises Two Alternating Phases: Forward Migration of the Golgi/Centrosome Associated with Centrosome Splitting and Myosin Contraction at the Rear
J. Neurosci.,
June 15, 2005;
25(24):
5691 - 5699.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-B. Manent, M. Demarque, I. Jorquera, C. Pellegrino, Y. Ben-Ari, L. Aniksztejn, and A. Represa
A Noncanonical Release of GABA and Glutamate Modulates Neuronal Migration
J. Neurosci.,
May 11, 2005;
25(19):
4755 - 4765.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Yoshizawa, T. Kawauchi, M. Sone, Y. V. Nishimura, M. Terao, K. Chihama, Y.-i. Nabeshima, and M. Hoshino
Involvement of a Rac Activator, P-Rex1, in Neurotrophin-Derived Signaling and Neuronal Migration
J. Neurosci.,
April 27, 2005;
25(17):
4406 - 4419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. F. McManus and J. A. Golden
Topical Review: Neuronal Migration in Developmental Disorders
J Child Neurol,
April 1, 2005;
20(4):
280 - 286.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Tsukada, A. Prokscha, E. Ungewickell, and G. Eichele
Doublecortin Association with Actin Filaments Is Regulated by Neurabin II
J. Biol. Chem.,
March 25, 2005;
280(12):
11361 - 11368.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Bystron, Z. Molnar, V. Otellin, and C. Blakemore
Tangential Networks of Precocious Neurons and Early Axonal Outgrowth in the Embryonic Human Forebrain
J. Neurosci.,
March 16, 2005;
25(11):
2781 - 2792.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. S. Schmid, S. Shelton, A. Stanco, Y. Yokota, J. A. Kreidberg, and E. S. Anton
{alpha}3{beta}1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development
Development,
December 15, 2004;
131(24):
6023 - 6031.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Nagano, S. Morikubo, and M. Sato
Filamin A and FILIP (Filamin A-Interacting Protein) Regulate Cell Polarity and Motility in Neocortical Subventricular and Intermediate Zones during Radial Migration
J. Neurosci.,
October 27, 2004;
24(43):
9648 - 9657.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Tanaka, F. F. Serneo, C. Higgins, M. J. Gambello, A. Wynshaw-Boris, and J. G. Gleeson
Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration
J. Cell Biol.,
June 7, 2004;
165(5):
709 - 721.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Moya and M. Valdeolmillos
Polarized Increase of Calcium and Nucleokinesis in Tangentially Migrating Neurons
Cereb Cortex,
June 1, 2004;
14(6):
610 - 618.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H.-t. Xu, X.-b. Yuan, C.-b. Guan, S. Duan, C.-p. Wu, and L. Feng
Calcium signaling in chemorepellant Slit2-dependent regulation of neuronal migration
PNAS,
March 23, 2004;
101(12):
4296 - 4301.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. F. McManus and J. A. Golden
Topical Review: Neuronal Migration in Developmental Disorders
J Child Neurol,
March 1, 2004;
19(3):
280 - 286.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
S. S. Kholmanskikh, J. S. Dobrin, A. Wynshaw-Boris, P. C. Letourneau, and M. E. Ross
Disregulated RhoGTPases and Actin Cytoskeleton Contribute to the Migration Defect in Lis1-Deficient Neurons
J. Neurosci.,
September 24, 2003;
23(25):
8673 - 8681.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Rakic
Developmental and Evolutionary Adaptations of Cortical Radial Glia
Cereb Cortex,
June 1, 2003;
13(6):
541 - 549.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. C. Adams, T. Tomoda, M. Cooper, G. Dietz, and M. E. Hatten
Mice that lack astrotactin have slowed neuronal migration
Development,
March 4, 2003;
129(4):
965 - 972.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Taoka, T. Ichimura, A. Wakamiya-Tsuruta, Y. Kubota, T. Araki, T. Obinata, and T. Isobe
V-1, a Protein Expressed Transiently during Murine Cerebellar Development, Regulates Actin Polymerization via Interaction with Capping Protein
J. Biol. Chem.,
February 14, 2003;
278(8):
5864 - 5870.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Hatten
New Directions in Neuronal Migration
Science,
September 6, 2002;
297(5587):
1660 - 1663.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Yacubova and H. Komuro
Intrinsic Program for Migration of Cerebellar Granule Cells In Vitro
J. Neurosci.,
July 15, 2002;
22(14):
5966 - 5981.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S.-i. Hirai, A. Kawaguchi, R. Hirasawa, M. Baba, T. Ohnishi, and S. Ohno
MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo
Development,
January 10, 2002;
129(19):
4483 - 4495.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Cau, S. Faure, M. Comps, C. Delsert, and N. Morin
A novel p21-activated kinase binds the actin and microtubule networks and induces microtubule stabilization
J. Cell Biol.,
December 10, 2001;
155(6):
1029 - 1042.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Komuro, E. Yacubova, E. Yacubova, and P. Rakic
Mode and Tempo of Tangential Cell Migration in the Cerebellar External Granular Layer
J. Neurosci.,
January 15, 2001;
21(2):
527 - 540.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. T. Lin, J. G. Gleeson, J. C. Corbo, L. Flanagan, and C. A. Walsh
DCAMKL1 Encodes a Protein Kinase with Homology to Doublecortin that Regulates Microtubule Polymerization
J. Neurosci.,
December 15, 2000;
20(24):
9152 - 9161.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Takei, J. Teng, A. Harada, and N. Hirokawa
Defects in Axonal Elongation and Neuronal Migration in Mice with Disrupted tau and map1b Genes
J. Cell Biol.,
September 4, 2000;
150(5):
989 - 1000.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Shiraishi, A. Mizutani, H. Bito, K. Fujisawa, S. Narumiya, K. Mikoshiba, and T. Furuichi
Cupidin, an Isoform of Homer/Vesl, Interacts with the Actin Cytoskeleton and Activated Rho Family Small GTPases and Is Expressed in Developing Mouse Cerebellar Granule Cells
J. Neurosci.,
October 1, 1999;
19(19):
8389 - 8400.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Horesh, T. Sapir, F. Francis, S. G. Wolf, M. Caspi, M. Elbaum, J. Chelly, and O. Reiner
Doublecortin, a stabilizer of microtubules
Hum. Mol. Genet.,
September 1, 1999;
8(9):
1599 - 1610.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Vaudry, B. J. Gonzalez, M. Basille, A. Fournier, and H. Vaudry
Neurotrophic activity of pituitary adenylate cyclase-activating polypeptide on rat cerebellar cortex during development
PNAS,
August 3, 1999;
96(16):
9415 - 9420.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Maeda and M. Noda
Involvement of Receptor-like Protein Tyrosine Phosphatase {zeta}/RPTP{beta} and Its Ligand Pleiotrophin/Heparin-binding Growth-associated Molecule (HB-GAM) in Neuronal Migration
J. Cell Biol.,
July 13, 1998;
142(1):
203 - 216.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Komuro and P. Rakic
Distinct Modes of Neuronal Migration in Different Domains of Developing Cerebellar Cortex
J. Neurosci.,
February 15, 1998;
18(4):
1478 - 1490.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. J. Bix and G. D. Clark
Platelet-Activating Factor Receptor Stimulation Disrupts Neuronal Migration In Vitro
J. Neurosci.,
January 1, 1998;
18(1):
307 - 318.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. L. Faust and M. E. Hatten
Targeted Deletion of the PEX2 Peroxisome Assembly Gene in Mice Provides a Model for Zellweger Syndrome, a Human Neuronal Migration Disorder
J. Cell Biol.,
December 1, 1997;
139(5):
1293 - 1305.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. L. Shorte
N-Methyl-D-Aspartate Evokes Rapid Net Depolymerization of Filamentous Actin in Cultured Rat Cerebellar Granule Cells
J Neurophysiol,
August 1, 1997;
78(2):
1135 - 1143.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Phelps, R. Barber, and J. Vaughn
Nonradial migration of interneurons can be experimentally altered in spinal cord slice cultures
Development,
January 7, 1996;
122(7):
2013 - 2022.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
J. P. Aumais, J. R. Tunstead, R. S. McNeil, B. T. Schaar, S. K. McConnell, S.-H. Lin, G. D. Clark, and L.-y. Yu-Lee
NudC Associates with Lis1 and the Dynein Motor at the Leading Pole of Neurons
J. Neurosci.,
December 15, 2001;
21(24):
RC187 - RC187.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|