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The Journal of Neuroscience, June 14, 2006, 26(24):6627-6636; doi:10.1523/JNEUROSCI.0149-06.2006

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Neurobiology of Disease
Subventricular Zone-Derived Neuroblasts Migrate and Differentiate into Mature Neurons in the Post-Stroke Adult Striatum

Toru Yamashita,^1,2,4,8 * Mikiko Ninomiya,^1,2,5,8 * Pilar Hernández Acosta,^6,7 Jose Manuel García-Verdugo,⁶ Takehiko Sunabori,^1,2,8 Masanori Sakaguchi,^2,8 Kazuhide Adachi,^1,2,3,8 Takuro Kojima,^1,2,8 Yuki Hirota,^1,2,8 Takeshi Kawase,³ Nobuo Araki,⁵ Koji Abe,⁴ Hideyuki Okano,^2,8 and Kazunobu Sawamoto^1,2,8

¹Bridgestone Laboratory of Developmental and Regenerative Neurobiology and Departments of ²Physiology and ³Neurosurgery, Keio University School of Medicine, Tokyo 160-8582, Japan, ⁴Department of Neurology, Okayama University Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama 700-8558, Japan, ⁵Department of Neurology, Saitama Medical School, Saitama 350-0495, Japan, ⁶University of Valencia, Valencia 46100, Spain, ⁷Centro de Investigacion Principe Felipe, Valencia 46013, Spain, and ⁸Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Saitama 332-0012, Japan

Correspondence should be addressed to Kazunobu Sawamoto, Bridgestone Laboratory of Developmental and Regenerative Neurobiology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, Japan. Email: sawamoto{at}sc.itc.keio.ac.jp

Recent studies have revealed that the adult mammalian brain has the capacity to regenerate some neurons after various insults. However, the precise mechanism of insult-induced neurogenesis has not been demonstrated. In the normal brain, GFAP-expressing cells in the subventricular zone (SVZ) of the lateral ventricles include a neurogenic cell population that gives rise to olfactory bulb neurons only. Herein, we report evidence that, after a stroke, these cells are capable of producing new neurons outside the olfactory bulbs. SVZ GFAP-expressing cells labeled by a cell-type-specific viral infection method were found to generate neuroblasts that migrated toward the injured striatum after middle cerebral artery occlusion. These neuroblasts in the striatum formed elongated chain-like cell aggregates similar to those in the normal SVZ, and these chains were observed to be closely associated with thin astrocytic processes and blood vessels. Finally, long-term tracing of the green fluorescent-labeled cells with a Cre-loxP system revealed that the SVZ-derived neuroblasts differentiated into mature neurons in the striatum, in which they expressed neuronal-specific nuclear protein and formed synapses with neighboring striatal cells. These results highlight the role of the SVZ in neuronal regeneration after a stroke and its potential as an important therapeutic target for various neurological disorders.

Key words: subventricular zone; cerebral ischemia; migration; neurogenesis; regeneration; striatum

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Received Jan. 13, 2006; revised May 9, 2006; accepted May 13, 2006.

Correspondence should be addressed to Kazunobu Sawamoto, Bridgestone Laboratory of Developmental and Regenerative Neurobiology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, Japan. Email: sawamoto{at}sc.itc.keio.ac.jp

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