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The Journal of Neuroscience, June 21, 2006, 26(25):6834-6840; doi:10.1523/JNEUROSCI.1728-06.2006

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Development/Plasticity/Repair
Stromal Cell-Derived Factor-1 (Chemokine C-X-C Motif Ligand 12) and Chemokine C-X-C Motif Receptor 4 Are Required for Migration of Gonadotropin-Releasing Hormone Neurons to the Forebrain

Gerald A. Schwarting,^1,2 Timothy R. Henion,^1,2 J. David Nugent,¹ Benjamin Caplan,¹ and Stuart Tobet³

¹Shriver Center, Waltham, Massachusetts 02452, ²Department of Cell Biology, University of Massachusetts Medical Center, Worcester, Massachusetts 01655, and ³College of Veterinary Medicine and Biomedical Science, Colorado State University, Fort Collins, Colorado 80523

Correspondence should be addressed to Gerald A. Schwarting, The Shriver Center/University of Massachusetts Medical Center, 200 Trapelo Road, Waltham, MA 02452. Email: gerald.schwarting{at}umassmed.edu

Gonadotropin-releasing hormone (GnRH) neurons migrate from the vomeronasal organ (VNO) in the nasal compartment to the basal forebrain in mice, beginning on embryonic day 11 (E11). These neurons use vomeronasal axons as guides to migrate through the nasal mesenchyme. Most GnRH neurons then migrate along the caudal branch of the vomeronasal nerve to reach the hypothalamus. We show here that stromal cell-derived factor-1 [SDF-1, also known as chemokine C-X-C motif ligand 12 (CXCL12)] is expressed in the embryonic nasal mesenchyme from as early as E10 in an increasing rostral to caudal gradient that is most intense at the border of the nasal mesenchyme and the telencephalon. Chemokine C-X-C motif receptor 4 (CXCR4), the receptor for SDF-1, is expressed by neurons in the olfactory epithelium and VNO. Cells derived from these sensory epithelia, including migrating GnRH neurons and ensheathing glial precursors of the migrating mass (MM), also express CXCR4, suggesting that they may use SDF-1 as a chemokine. In support of this, most GnRH neurons of CXCR4^–/– mice fail to exit the VNO at E13, and comparatively few GnRH neurons reach the forebrain. There is also a significant decrease in the total number of GnRH neurons in CXCR4^–/– mice and an increase in cell death within the VNO relative to controls. The MM is smaller in CXCR4^–/– mice, suggesting that some MM cells also require SDF-1/CXCR4 function for migration and survival.

Key words: gonadotropin-releasing hormone; luteinizing hormone-releasing hormone; cell migration; migrating mass; chemokine; Kallmann's syndrome

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Received Jan. 5, 2006; accepted May 18, 2006.

Correspondence should be addressed to Gerald A. Schwarting, The Shriver Center/University of Massachusetts Medical Center, 200 Trapelo Road, Waltham, MA 02452. Email: gerald.schwarting{at}umassmed.edu

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