Interaxonal Eph-Ephrin Signaling May Mediate Sorting of Olfactory Sensory Axons in Manduca sexta

Megumi Kaneko, Alan J Nighorn

Research output: Contribution to journalArticle

31 Citations (Scopus)

Abstract

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 glomeruliwith 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.

Original languageEnglish (US)
Pages (from-to)11523-11538
Number of pages16
JournalJournal of Neuroscience
Volume23
Issue number37
StatePublished - Dec 17 2003

Fingerprint

Ephrins
Manduca
Axons
Eph Family Receptors
Olfactory Receptor Neurons
Ligands
EphA1 Receptor
Olfactory Nerve
Staining and Labeling
Olfactory Pathways
Moths
Neurites

Keywords

  • Axon guidance
  • Eph receptor
  • Ephrin
  • Insect
  • Olfactory system
  • Sensory mapping

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Interaxonal Eph-Ephrin Signaling May Mediate Sorting of Olfactory Sensory Axons in Manduca sexta. / Kaneko, Megumi; Nighorn, Alan J.

In: Journal of Neuroscience, Vol. 23, No. 37, 17.12.2003, p. 11523-11538.

Research output: Contribution to journalArticle

@article{554e3ee3adba4e2b9f9dd9894853824c,
title = "Interaxonal Eph-Ephrin Signaling May Mediate Sorting of Olfactory Sensory Axons in Manduca sexta",
abstract = "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 glomeruliwith 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.",
keywords = "Axon guidance, Eph receptor, Ephrin, Insect, Olfactory system, Sensory mapping",
author = "Megumi Kaneko and Nighorn, {Alan J}",
year = "2003",
month = "12",
day = "17",
language = "English (US)",
volume = "23",
pages = "11523--11538",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "37",

}

TY - JOUR

T1 - Interaxonal Eph-Ephrin Signaling May Mediate Sorting of Olfactory Sensory Axons in Manduca sexta

AU - Kaneko, Megumi

AU - Nighorn, Alan J

PY - 2003/12/17

Y1 - 2003/12/17

N2 - 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 glomeruliwith 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.

AB - 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 glomeruliwith 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.

KW - Axon guidance

KW - Eph receptor

KW - Ephrin

KW - Insect

KW - Olfactory system

KW - Sensory mapping

UR - http://www.scopus.com/inward/record.url?scp=0346433984&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0346433984&partnerID=8YFLogxK

M3 - Article

C2 - 14684856

AN - SCOPUS:0346433984

VL - 23

SP - 11523

EP - 11538

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 37

ER -