Neuronal migration depends on blood flow in the adult brain

Author:

Ogino Takashi1,Saito Akari1,Sawada Masato12,Takemura Shoko1,Nagase Jiro1,Kawase Honomi1,Inada Hiroyuki3,Herranz-Pérez Vicente45ORCID,Mukouyama Yoh-suke6,Ema Masatsugu7ORCID,García-Verdugo José Manuel4,Nabekura Junichi3ORCID,Sawamoto Kazunobu12ORCID

Affiliation:

1. Department of Developmental and Regenerative Biology, Nagoya City University Graduate School of Medical Sciences

2. Division of Neural Development and Regeneration, National Institute for Physiological Sciences

3. Division of Homeostatic Development, Department of Developmental Physiology, National Institute for Physiological Sciences

4. Laboratory of Comparative Neurobiology, Cavanilles Institute, University of Valencia

5. Department of Cell Biology

6. Laboratory of Stem Cell and Neuro-Vascular Biology, Cell and Development Biology Center

7. Department of Stem Cells and Human Disease Models, Research Center for Animal Life Science, Shiga University of Medical Science

Abstract

In animal tissues, several cell types migrate along blood vessels, raising the possibility that blood flow influences cell migration. Here, we show that blood flow promotes the migration of new olfactory-bulb neurons in the adult brain. Neuronal migration is facilitated by blood flow, leading to accumulation of new neurons near blood vessels with abundant blood flow. Blood flow inhibition attenuates blood vessel-guided neuronal migration, suggesting that blood contains factors beneficial to neuronal migration. We found that ghrelin, which is increased in blood by hunger, directly influences neuronal migration. Ghrelin signaling promotes somal translocation by activating actin cytoskeleton contraction at the rear of the cell soma. New neurons mature in the olfactory bulb and contribute to the olfactory function for sensing odorants from food. Finally, we show that neuronal migration is increased by calorie restriction, and that ghrelin signaling is involved in the process. This study suggests that blood flow promotes neuronal migration through blood-derived ghrelin signaling in the adult brain, which could be one of the mechanisms that improve the olfactory function for food-seeking behavior during starvation.

Publisher

eLife Sciences Publications, Ltd

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