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The Journal of Neuroscience, August 13, 2008, 28(33):8344-8353; doi:10.1523/JNEUROSCI.1670-08.2008

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Cellular/Molecular
Regulation of Axonal Elongation and Pathfinding from the Entorhinal Cortex to the Dentate Gyrus in the Hippocampus by the Chemokine Stromal Cell-Derived Factor 1

Yoichi Ohshima,^1,2,3 Takekazu Kubo,² Ryuta Koyama,⁴ Masaki Ueno,^1,2 Masanori Nakagawa,³ and Toshihide Yamashita^1,2

¹Department of Molecular Neuroscience, Graduate School of Medicine, Osaka University, Osaka 565-0871, Japan, ²Department of Neurobiology, Graduate School of Medicine, Chiba University, Chiba 260-8670, Japan, ³Molecular Neurology and Gerontology, Kyoto Prefectural University of Medicine, Kyoto 602-8566, Japan, and ⁴Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo 113-0033, Japan

Correspondence should be addressed to either of the following: Toshihide Yamashita or Takekazu Kubo, Department of Molecular Neuroscience, Graduate School of Medicine, Osaka University, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan. Email: yamashita{at}molneu.med.osaka-u.ac.jp or Email: kubo{at}restaff.chiba-u.jp

During the early developmental stage, a neural circuit is established between the entorhinal cortex (EC) and the hippocampal dentate gyrus (DG) via the perforant pathway. However, the manner in which the perforant fibers are navigated has mostly remained a mystery. Here, we analyzed the functional role of a chemokine, namely, stromal cell-derived factor 1 (SDF-1), in the navigation of the perforant fibers. SDF-1 was observed to promote neurite growth, which is dependent on mDia1, in cultured entorhinal cortical neurons obtained from rats at postnatal day 0. We then used entorhino-hippocampal cocultures comprising green fluorescence-labeled EC and DG slices to assess the projection of the perforant fibers from the EC. Although the specific laminar termination of the entorhinal axons was observed with this system, the number of appropriately terminating entorhinal axons decreased significantly when the SDF-1 signaling pathway was blocked by a neutralizing antibody against SDF-1 or by the specific SDF-1 receptor antagonist AMD3100 (1,1'-[1,4-phenylenebis(methylene)]bis-1,4,8,11-tetra-azacyclotetradecane octahydrochloride). Furthermore, inhibition of the SDF-1 signaling pathway resulted in a decrease in the immunoreactivity for PSD-95 (postsynaptic density protein-95) in the DG, possibly because of a reduction in the number of projecting perforant fibers. These results demonstrate that SDF-1 plays a critical role in promoting the growth of perforant fibers from the EC to the DG.

Key words: stromal cell-derived factor-1; CXCR4; hippocampus; dentate gyrus; entorhinal cortex; axonal elongation; slice culture; cell culture

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Received Dec. 23, 2007; revised June 24, 2008; accepted June 30, 2008.

Correspondence should be addressed to either of the following: Toshihide Yamashita or Takekazu Kubo, Department of Molecular Neuroscience, Graduate School of Medicine, Osaka University, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan. Email: yamashita{at}molneu.med.osaka-u.ac.jp or Email: kubo{at}restaff.chiba-u.jp

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