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Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb - PubMed

  • ️Mon Jan 01 2007

Comparative Study

Blood vessels form a scaffold for neuroblast migration in the adult olfactory bulb

Serena Bovetti et al. J Neurosci. 2007.

Abstract

New cells are continuously added to the rodent olfactory bulb (OB), throughout development and in adults. These cells migrate tangentially from the subventricular zone along the rostral migratory stream to the OB, where they migrate radically from the center to periphery of the OB. Although different modalities of radial migration have been described in other brain regions, the mechanisms governing radial migration in the OB are still mostly unknown. Here, we identify a new modality of migration in which neuronal precursors migrate along blood vessels toward their destination. Our results show that half of the radially migrating cells associate with the vasculature in the granule cell layer of the OB, and in vivo time-lapse imaging demonstrates that they use blood vessels as a scaffold for their migration through an interaction with the extracellular matrix and perivascular astrocyte end feet. The present data provide evidence that a new modality of migration, vasophilic migration, is occurring in the adult brain and reveals a novel role of brain vasculature.

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Figures

Figure 1.
Figure 1.

SVZ-derived migratory cells associated with blood vessels. A–B, Coronal sections of the OB showing CTG-positive cells (green) and blood vessels (A; lumen tetramethylrhodamine isothiocyanate fill; red) counterstained with DAPI (B; blue). C–D, Coronal section of P24 mouse OB showing blood vessels (C; red); neuronal precursors (green) exiting the SEL and entering the GCL associate with blood vessels (D; arrows). E–H, Higher-magnification photographs of coronal OB sections showing CTb-labeled cells associated to blood vessels. I, Frequency distribution graph of the number of CTG-positive cells (abscissa) versus distances from the blood vessels (ordinate). The number of CTG-positive cells closer than 3 μm is significantly different from a random distribution (MANOVA, * p < 0.001). Scale bars: (in B) A, B, 200 μm; (in D) C, D, 200 μm; (in H) F–H, 20 μm. MCL, Mitral cell layer; ONL, olfactory nerve layer.

Figure 2.
Figure 2.

SVZ-derived migratory cells are neuroblasts and associate with perivascular astrocytic end feet. A, GAD65-GFP positive cell (green) with a leading process wrapping around a capillary (red) in the granule cell layer of the young adult olfactory bulb. B, CTG-labeled SVZ-derived progenitor (green) migrating along a bulb blood vessel (lumen tetramethylrhodamine isothiocyanate fill; red) with GFAP immunohistochemical labeling of astrocytes (blue). GFAP-positive processes are rarely seen between the migratory cell and vessel and no CTG-positive cells express GFAP. C, Bright-field photograph showing DAB-stained CTb-labeled SVZ-derived progenitors (arrows). CTb in cell processes is typically punctate because of lissome accumulation of the CTb. D, Electron microscopic image of the same field shown in C showing the perivascular space around the blood vessel (BV). Endothelial cells have been pseudocolored red, perivascular astrocyte processes blue, and the migrating SVZ progenitors green. Punctate DAB reaction product is present in lysosomes and around a migrating cell nucleus (arrows) at identical locations to that present in the bright-field photograph in C. E, Higher magnification photograph showing a thin astrocyte process (a) between the migrating (m) and the endothelial cell (e). A small space containing the ECM is present between the astrocyte and migratory cell. Scale bar: (in E) A, B, 10 μm; C, 3 μm; D, 2 μm; E, 250 nm.

Figure 3.
Figure 3.

Double-label time-lapse confocal microscopy showing neuronal precursors migrating along the blood vessels. A–G, Photographs of a CTG-labeled neuroblast (green) and blood vessel (red) at selected time points from t = 0 min to t = 150 min. H, Schematic drawing of three different cells moving along vessels as a function of time. Scale bar: (in H) A–H, 50 μm. ONL, Olfactory nerve layer.

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