Expression of drebrin E in migrating neuroblasts in adult rat brain: Coincidence between drebrin E disappearance from cell body and cessation of migration

doi:10.1016/j.neuroscience.2007.10.068

Neuroscience

Volume 152, Issue 3, 27 March 2008, Pages 670-682

https://doi.org/10.1016/j.neuroscience.2007.10.068 Get rights and content

Abstract

Migrating neuroblasts in the adult brain form the rostral migratory stream (RMS) from the lateral ventricle to the olfactory bulb (OB) and then differentiate in the OB. In this study, we immunohistochemically analyzed drebrin expression in the RMS of the adult rat brain. Although drebrin is concentrated in dendritic spines of mature neurons, drebrin-immunopositive (DIP) cell bodies were observed in the RMS. The polysialated form of a neural cell adhesion molecule (PSA-NCAM) was detected in DIP cells. K_i-67, a marker of proliferating cells, was also detected in a subset of DIP cells; however, neither glial fibrillary acidic protein, nestin nor vimentin was detected in DIP cells. These results indicate that DIP cells in the RMS are migrating neuroblasts. An image subtraction method, based on using anti-pan-drebrin and anti-drebrin A antibodies, demonstrated that DIP migrating neuroblasts are immunopositive for drebrin E but not for drebrin A (E+A−). Furthermore, olfactory bulbectomy increased the number of cells with drebrin E+A− signals in the RMS, indicating that these cells migrate along the RMS. Drebrin E+A− cells were also found in the subgranular layer of the dentate gyrus and in the piriform cortex. Thus, detection of drebrin E+A− signals is useful for identifying migrating neuroblasts in the adult brain. In the OB, drebrin E+A− signals were observed in the cell bodies of migrating neuroblasts in the core region; however, only fibrous and punctate drebrin E+A− signals were observed in postmigratory neuroblasts at the outer layers. These data demonstrate that the disappearance of drebrin E+A− signals from the cell body coincides with the cessation of neuronal migration. The disappearance of drebrin E from the cell body may be a molecular switch for the cessation of migration in newly generated neuroblasts.

Section snippets

Animals

Eight-week-old male Sprague–Dawley (SD) rats (Charles River Laboratories, Yokohama, Japan) were individually housed in a temperature- and humidity-controlled room in a 12-h light/dark cycle with food and water available ad libitum. For cell culture, pregnant Wistar rats (Charles River Laboratories) were used. All animal treatments were performed in accordance with regulations outlined by Japanese law and the NIH guidelines, and were approved by the Animal Care and Experimentation Committee of

Intense drebrin immunostaining in RMS of adult rat brain

Immunohistochemical analysis using the anti-pan-drebrin antibody M2F6 demonstrated an intensely immunostained stream along the route of the SVZ and RMS (arrows in Fig. 2A, C), through which newly generated neuroblasts migrate to the OB. This intensely stained drebrin-immunopositive (DIP) stream spread in the OB (Fig. 2E). In contrast to M2F6, the drebrin A-specific antibody DAS2 did not immunostain the stream (Fig. 2B, D, F); however, both DAS2 and M2F6 similarly stained the neuropil regions of

Discussion

In this study, we demonstrate that migrating neuroblasts in the adult SVZ-RMS-OB system have drebrin E+A− signals in their cell bodies. DCX is also expressed in the cell body in the migrating neuroblasts; however, DCX remains to be expressed through migratory and postmigratory stages in adult neurogenesis. Also note that the disappearance of drebrin E+A− signals from the cell body coincides with the cessation of neuronal migration. These results indicate that drebrin E+A− signal is a good

Conclusion

In conclusion, drebrin E but not drebrin A is detected in the cell body of migrating neuroblasts in the adult brain. The disappearance of drebrin E from the cell body coincides with the cessation of migration. Because drebrin modifies the characteristics of actin filaments, the disappearance of drebrin E from the cell body causes a change in the organization of the actin cytoskeleton, suggesting that the actin cytoskeleton plays a pivotal role in the cessation of adult neuronal migration.

Acknowledgments

This work was supported in part by Grants-in-Aid for Scientific Research on Priority Areas-Elucidation of neural network function in the brain from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT) (17023008). We thank Drs. Kunihiko Obata, Kenichi Uyemura and Hideto Takahashi for helpful comments. We also thank Dr. Pokay Ma for editing this manuscript.

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Cellular neuroscienceExpression of drebrin E in migrating neuroblasts in adult rat brain: Coincidence between drebrin E disappearance from cell body and cessation of migration

Abstract

Section snippets

Animals

Intense drebrin immunostaining in RMS of adult rat brain

Discussion

Conclusion

Acknowledgments

Curr Biol

Neuron

Cell

Neuron

Neuron

Neuron

Trends Neurosci

Neurosci Lett

Dev Brain Res

J Biol Chem

J Neurosci Methods

Mol Brain Res

Mech Dev

Eur J Cell Biol

Exp Cell Res

Brain Res Bull

Brain Res Bull

Neurochem Int

Dev Brain Res

Brain Res

Neurosci Res Suppl

Exp Cell Res

J Biol Chem

Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses

J Comp Neurol

Actin-binding protein, drebrin, accumulates in submembranous regions in parallel with neuronal differentiation

J Neurosci Res

RNAi reveals doublecortin is required for radial migration in rat neocortex

Nat Neurosci

Cellular neuroscience
Expression of drebrin E in migrating neuroblasts in adult rat brain: Coincidence between drebrin E disappearance from cell body and cessation of migration