Dynamic features of postnatal subventricular zone cell motility

A two-photon time-lapse study

Chae Nam Sang, Yongsoo Kim, Dilyan Dryanovski, Avery Walker, Gwendolyn Goings, Kevin Woolfrey, Su Kang Seong, Chris Chu, Anjen Chenn, Ferenc Erdelyi, Gabor Szabo, Philip Hockberger, Francis G. Szele

Research output: Contribution to journalArticle

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Abstract

Neuroblasts migrate long distances in the postnatal subventricular zone (SVZ) and rostral migratory stream (RMS) to the olfactory bulbs. Many fundamental features of SVZ migration are still poorly understood, and we addressed several important questions using two-photon time-lapse microscopy of brain slices from postnatal and adult eGFP+ transgenic mice. 1) Longitudinal arrays of neuroblasts, so-called chain migration, have never been dynamically visualized in situ. We found that neuroblasts expressing doublecortin-eGFP (Dcx-eGFP) and glutamic acid decarboxylase-eGFP (Gad-eGFP) remained within arrays, which maintained their shape for many hours, despite the fact that there was a wide variety of movement within arrays. 2) In the dorsal SVZ, neuroblasts migrated rostrocaudally as expected, but migration shifted to dorsoventral orientations throughout ventral regions of the lateral ventricle. 3) Whereas polarized bipolar morphology has been a gold standard for inferring migration in histologic sections, our data indicated that migratory morphology was not predictive of motility. 4) Is there local motility in addition to long distance migration? 5) How fast is SVZ migration? Unexpectedly, one-third of motile neuroblasts moved locally in complex exploratory patterns and at average speeds slower than long distance movement. 6) Finally, we tested, and disproved, the hypothesis that all motile cells in the SVZ express doublecortin, indicating that Dcx is not required for migration of all SVZ cell types. These data show that cell motility in the SVZ and RMS is far more complex then previously thought and involves multiple cell types, behaviors, speeds, and directions.

Original languageEnglish (US)
Pages (from-to)190-208
Number of pages19
JournalJournal of Comparative Neurology
Volume505
Issue number2
DOIs
StatePublished - Nov 10 2007

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Lateral Ventricles
Photons
Cell Movement
Glutamate Decarboxylase
Olfactory Bulb
Emigration and Immigration
Transgenic Mice
Microscopy
Brain

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

Sang, C. N., Kim, Y., Dryanovski, D., Walker, A., Goings, G., Woolfrey, K., ... Szele, F. G. (2007). Dynamic features of postnatal subventricular zone cell motility: A two-photon time-lapse study. Journal of Comparative Neurology, 505(2), 190-208. https://doi.org/10.1002/cne.21473
Sang, Chae Nam ; Kim, Yongsoo ; Dryanovski, Dilyan ; Walker, Avery ; Goings, Gwendolyn ; Woolfrey, Kevin ; Seong, Su Kang ; Chu, Chris ; Chenn, Anjen ; Erdelyi, Ferenc ; Szabo, Gabor ; Hockberger, Philip ; Szele, Francis G. / Dynamic features of postnatal subventricular zone cell motility : A two-photon time-lapse study. In: Journal of Comparative Neurology. 2007 ; Vol. 505, No. 2. pp. 190-208.
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Sang, CN, Kim, Y, Dryanovski, D, Walker, A, Goings, G, Woolfrey, K, Seong, SK, Chu, C, Chenn, A, Erdelyi, F, Szabo, G, Hockberger, P & Szele, FG 2007, 'Dynamic features of postnatal subventricular zone cell motility: A two-photon time-lapse study', Journal of Comparative Neurology, vol. 505, no. 2, pp. 190-208. https://doi.org/10.1002/cne.21473

Dynamic features of postnatal subventricular zone cell motility : A two-photon time-lapse study. / Sang, Chae Nam; Kim, Yongsoo; Dryanovski, Dilyan; Walker, Avery; Goings, Gwendolyn; Woolfrey, Kevin; Seong, Su Kang; Chu, Chris; Chenn, Anjen; Erdelyi, Ferenc; Szabo, Gabor; Hockberger, Philip; Szele, Francis G.

In: Journal of Comparative Neurology, Vol. 505, No. 2, 10.11.2007, p. 190-208.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Dynamic features of postnatal subventricular zone cell motility

T2 - A two-photon time-lapse study

AU - Sang, Chae Nam

AU - Kim, Yongsoo

AU - Dryanovski, Dilyan

AU - Walker, Avery

AU - Goings, Gwendolyn

AU - Woolfrey, Kevin

AU - Seong, Su Kang

AU - Chu, Chris

AU - Chenn, Anjen

AU - Erdelyi, Ferenc

AU - Szabo, Gabor

AU - Hockberger, Philip

AU - Szele, Francis G.

PY - 2007/11/10

Y1 - 2007/11/10

N2 - Neuroblasts migrate long distances in the postnatal subventricular zone (SVZ) and rostral migratory stream (RMS) to the olfactory bulbs. Many fundamental features of SVZ migration are still poorly understood, and we addressed several important questions using two-photon time-lapse microscopy of brain slices from postnatal and adult eGFP+ transgenic mice. 1) Longitudinal arrays of neuroblasts, so-called chain migration, have never been dynamically visualized in situ. We found that neuroblasts expressing doublecortin-eGFP (Dcx-eGFP) and glutamic acid decarboxylase-eGFP (Gad-eGFP) remained within arrays, which maintained their shape for many hours, despite the fact that there was a wide variety of movement within arrays. 2) In the dorsal SVZ, neuroblasts migrated rostrocaudally as expected, but migration shifted to dorsoventral orientations throughout ventral regions of the lateral ventricle. 3) Whereas polarized bipolar morphology has been a gold standard for inferring migration in histologic sections, our data indicated that migratory morphology was not predictive of motility. 4) Is there local motility in addition to long distance migration? 5) How fast is SVZ migration? Unexpectedly, one-third of motile neuroblasts moved locally in complex exploratory patterns and at average speeds slower than long distance movement. 6) Finally, we tested, and disproved, the hypothesis that all motile cells in the SVZ express doublecortin, indicating that Dcx is not required for migration of all SVZ cell types. These data show that cell motility in the SVZ and RMS is far more complex then previously thought and involves multiple cell types, behaviors, speeds, and directions.

AB - Neuroblasts migrate long distances in the postnatal subventricular zone (SVZ) and rostral migratory stream (RMS) to the olfactory bulbs. Many fundamental features of SVZ migration are still poorly understood, and we addressed several important questions using two-photon time-lapse microscopy of brain slices from postnatal and adult eGFP+ transgenic mice. 1) Longitudinal arrays of neuroblasts, so-called chain migration, have never been dynamically visualized in situ. We found that neuroblasts expressing doublecortin-eGFP (Dcx-eGFP) and glutamic acid decarboxylase-eGFP (Gad-eGFP) remained within arrays, which maintained their shape for many hours, despite the fact that there was a wide variety of movement within arrays. 2) In the dorsal SVZ, neuroblasts migrated rostrocaudally as expected, but migration shifted to dorsoventral orientations throughout ventral regions of the lateral ventricle. 3) Whereas polarized bipolar morphology has been a gold standard for inferring migration in histologic sections, our data indicated that migratory morphology was not predictive of motility. 4) Is there local motility in addition to long distance migration? 5) How fast is SVZ migration? Unexpectedly, one-third of motile neuroblasts moved locally in complex exploratory patterns and at average speeds slower than long distance movement. 6) Finally, we tested, and disproved, the hypothesis that all motile cells in the SVZ express doublecortin, indicating that Dcx is not required for migration of all SVZ cell types. These data show that cell motility in the SVZ and RMS is far more complex then previously thought and involves multiple cell types, behaviors, speeds, and directions.

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