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The Journal of Neuroscience, December 17, 2003, 23(37):11523-11538

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Development/Plasticity/Repair
Interaxonal Eph-Ephrin Signaling May Mediate Sorting of Olfactory Sensory Axons in Manduca sexta

Megumi Kaneko and Alan Nighorn

Program in Neuroscience and Arizona Research Laboratories Division of Neurobiology, The University of Arizona, Tucson, Arizona 85721

We have investigated possible roles of the Eph family receptor tyrosine kinases and their ligand ephrins in the developing primary olfactory nerve pathway in the moth Manduca sexta. The Manduca homologs of the Eph receptor (MsEph) and ephrin ligand (MsEphrin) are most closely related to Drosophila Eph and ephrin, respectively. In situ labeling with Fc-fusion probes, in which IgG Fc was linked to the extracellular domain of MsEph (Eph-Fc) or MsEphrin (ephrin-Fc), reveals that both Eph receptors and ephrins are expressed on axons of olfactory receptor cells (ORCs) during their ingrowth to the primary center, the antennal lobe (AL). Interestingly, Eph receptors and ephrins are differentially distributed among identifiable glomeruli such that glomeruli with high receptor staining show little or no ligand staining, and vice versa, suggesting a complementary Eph-ephrin expression by subsets of ORC axons innervating a particular set of glomeruli. In contrast, neither Eph receptors nor ephrins are detectable in intrinsic components of the AL. In vitro, ephrin-Fc and Eph-Fc, when present homogeneously in the substratum, inhibit neurite outgrowth from olfactory epithelial explants. Moreover, in patterned substratum, neurites growing on the standard substratum turn or stop after encountering the test substratum containing ephrin-Fc. These in vitro observations indicate that MsEphrin can act as an inhibitor/repulsive cue for ORC axons. Based on results from in situ and in vitro experiments, we hypothesize that Eph receptors and ephrins mediate axon sorting and fasciculation through repulsive axon-axon interactions.

Key words: Eph receptor; ephrin; olfactory system; sensory mapping; axon guidance; insect

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Received June 23, 2003; revised September 17, 2003; accepted October 23, 2003.

This article has been cited by other articles:

				T. M. Coate, T. L. Swanson, and P. F. Copenhaver Reverse Signaling by Glycosylphosphatidylinositol-Linked Manduca Ephrin Requires a Src Family Kinase to Restrict Neuronal Migration In Vivo J. Neurosci., March 18, 2009; 29(11): 3404 - 3418. [Abstract] [Full Text] [PDF]

				T. M. Coate, J. A. Wirz, and P. F. Copenhaver Reverse Signaling via a Glycosyl-Phosphatidylinositol-Linked Ephrin Prevents Midline Crossing by Migratory Neurons during Embryonic Development in Manduca J. Neurosci., April 9, 2008; 28(15): 3846 - 3860. [Abstract] [Full Text] [PDF]

				M. A. Wolman, A. M. Regnery, T. Becker, C. G. Becker, and M. C. Halloran Semaphorin3D Regulates Axon Axon Interactions by Modulating Levels of L1 Cell Adhesion Molecule J. Neurosci., September 5, 2007; 27(36): 9653 - 9663. [Abstract] [Full Text] [PDF]

				M. Boyle, A. Nighorn, and J. B. Thomas Drosophila Eph receptor guides specific axon branches of mushroom body neurons Development, May 1, 2006; 133(9): 1845 - 1854. [Abstract] [Full Text] [PDF]

				B. W. Lipscomb and L. P. Tolbert Temporally Staggered Glomerulus Development in the Moth Manduca sexta Chem Senses, March 1, 2006; 31(3): 237 - 247. [Abstract] [Full Text] [PDF]

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