The expression of cell adhesion molecules on the growth cones of chick cutaneous and muscle sensory neurons

Marcia Honig, Joseph Kueter

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

In the developing chick hindlimb, axons that will project along a given peripheral nerve sort out together, as they traverse the plexus region at the base of the limb, and become segregated from axons that will project along other peripheral nerves. This sorting out may involve, at least in part, the differential expression of various cell adhesion molecules (CAMs). To begin to explore this possibility, we have compared the relative levels of immunofluorescent labeling on the growth cones of two populations of sensory neurons whose axons become segregated from one another: cutaneous and muscle sensory neurons. We took a tissue culture approach, since this allowed us to readily visualize the immunofluorescent labeling of individual growth cones, and identified the two cell types by previous retrograde labeling with DiI. Two dorsal root ganglion explants, one containing DiI-labeled cutaneous neurons and the other containing DiI-labeled muscle sensory neurons, from opposite sides of the same embryo, were plated together in each culture dish. For all the CAMs we studied (NCAM, polysialylated NCAM, G4/L1, axonin-1, SC1/DM-GRASP/BEN, and N-cadherin), the intensity of immunofluorescent labeling typically was fairly uniform on the growth cone, its filopodia, and the portion of the neurite just proximal tothe growth cone. Only one CAM, axonin-1, exhibited labeling that was especially intense at sites of interneuronal contact. Quantification of labeling intensities using image analysis showed that cutaneous and muscle sensory growth cones did not consistently differ from one another in their levels of expression of G4/L1 or of axonin-1. The latter finding stands in contrast to recent reports claiming that axonin-1 is not expressed on muscle sensory neurons. Each of the other CAMs (NCAM, polysialylated NCAM, SC1/DM-GRASP/BEN, and N-cadherin) also showed considerable overlap in the distribution of labeling intensities between the two populations, but overall, expression levels on muscle sensory growth cones were greater than on cutaneous growth cones. How the differential expression of some CAMs could potentially contribute to the way that cutaneous and muscle sensory growth cones become segregated from one another and the implications of these results for sensory neuron specification are discussed.

Original languageEnglish (US)
Pages (from-to)563-583
Number of pages21
JournalDevelopmental Biology
Volume167
Issue number2
DOIs
StatePublished - Jan 1 1995

Fingerprint

Growth Cones
Cell Adhesion Molecules
Sensory Receptor Cells
Contactin 2
Neural Cell Adhesion Molecules
Muscles
Skin
Axons
Cadherins
Peripheral Nerves
Pseudopodia
Spinal Ganglia
Neurites
Hindlimb
Population
Embryonic Structures
Extremities
Neurons

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Developmental Biology
  • Cell Biology

Cite this

The expression of cell adhesion molecules on the growth cones of chick cutaneous and muscle sensory neurons. / Honig, Marcia; Kueter, Joseph.

In: Developmental Biology, Vol. 167, No. 2, 01.01.1995, p. 563-583.

Research output: Contribution to journalArticle

@article{3287d30b5afe4e64bfbc6d13b6778d2f,
title = "The expression of cell adhesion molecules on the growth cones of chick cutaneous and muscle sensory neurons",
abstract = "In the developing chick hindlimb, axons that will project along a given peripheral nerve sort out together, as they traverse the plexus region at the base of the limb, and become segregated from axons that will project along other peripheral nerves. This sorting out may involve, at least in part, the differential expression of various cell adhesion molecules (CAMs). To begin to explore this possibility, we have compared the relative levels of immunofluorescent labeling on the growth cones of two populations of sensory neurons whose axons become segregated from one another: cutaneous and muscle sensory neurons. We took a tissue culture approach, since this allowed us to readily visualize the immunofluorescent labeling of individual growth cones, and identified the two cell types by previous retrograde labeling with DiI. Two dorsal root ganglion explants, one containing DiI-labeled cutaneous neurons and the other containing DiI-labeled muscle sensory neurons, from opposite sides of the same embryo, were plated together in each culture dish. For all the CAMs we studied (NCAM, polysialylated NCAM, G4/L1, axonin-1, SC1/DM-GRASP/BEN, and N-cadherin), the intensity of immunofluorescent labeling typically was fairly uniform on the growth cone, its filopodia, and the portion of the neurite just proximal tothe growth cone. Only one CAM, axonin-1, exhibited labeling that was especially intense at sites of interneuronal contact. Quantification of labeling intensities using image analysis showed that cutaneous and muscle sensory growth cones did not consistently differ from one another in their levels of expression of G4/L1 or of axonin-1. The latter finding stands in contrast to recent reports claiming that axonin-1 is not expressed on muscle sensory neurons. Each of the other CAMs (NCAM, polysialylated NCAM, SC1/DM-GRASP/BEN, and N-cadherin) also showed considerable overlap in the distribution of labeling intensities between the two populations, but overall, expression levels on muscle sensory growth cones were greater than on cutaneous growth cones. How the differential expression of some CAMs could potentially contribute to the way that cutaneous and muscle sensory growth cones become segregated from one another and the implications of these results for sensory neuron specification are discussed.",
author = "Marcia Honig and Joseph Kueter",
year = "1995",
month = "1",
day = "1",
doi = "10.1006/dbio.1995.1049",
language = "English (US)",
volume = "167",
pages = "563--583",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - The expression of cell adhesion molecules on the growth cones of chick cutaneous and muscle sensory neurons

AU - Honig, Marcia

AU - Kueter, Joseph

PY - 1995/1/1

Y1 - 1995/1/1

N2 - In the developing chick hindlimb, axons that will project along a given peripheral nerve sort out together, as they traverse the plexus region at the base of the limb, and become segregated from axons that will project along other peripheral nerves. This sorting out may involve, at least in part, the differential expression of various cell adhesion molecules (CAMs). To begin to explore this possibility, we have compared the relative levels of immunofluorescent labeling on the growth cones of two populations of sensory neurons whose axons become segregated from one another: cutaneous and muscle sensory neurons. We took a tissue culture approach, since this allowed us to readily visualize the immunofluorescent labeling of individual growth cones, and identified the two cell types by previous retrograde labeling with DiI. Two dorsal root ganglion explants, one containing DiI-labeled cutaneous neurons and the other containing DiI-labeled muscle sensory neurons, from opposite sides of the same embryo, were plated together in each culture dish. For all the CAMs we studied (NCAM, polysialylated NCAM, G4/L1, axonin-1, SC1/DM-GRASP/BEN, and N-cadherin), the intensity of immunofluorescent labeling typically was fairly uniform on the growth cone, its filopodia, and the portion of the neurite just proximal tothe growth cone. Only one CAM, axonin-1, exhibited labeling that was especially intense at sites of interneuronal contact. Quantification of labeling intensities using image analysis showed that cutaneous and muscle sensory growth cones did not consistently differ from one another in their levels of expression of G4/L1 or of axonin-1. The latter finding stands in contrast to recent reports claiming that axonin-1 is not expressed on muscle sensory neurons. Each of the other CAMs (NCAM, polysialylated NCAM, SC1/DM-GRASP/BEN, and N-cadherin) also showed considerable overlap in the distribution of labeling intensities between the two populations, but overall, expression levels on muscle sensory growth cones were greater than on cutaneous growth cones. How the differential expression of some CAMs could potentially contribute to the way that cutaneous and muscle sensory growth cones become segregated from one another and the implications of these results for sensory neuron specification are discussed.

AB - In the developing chick hindlimb, axons that will project along a given peripheral nerve sort out together, as they traverse the plexus region at the base of the limb, and become segregated from axons that will project along other peripheral nerves. This sorting out may involve, at least in part, the differential expression of various cell adhesion molecules (CAMs). To begin to explore this possibility, we have compared the relative levels of immunofluorescent labeling on the growth cones of two populations of sensory neurons whose axons become segregated from one another: cutaneous and muscle sensory neurons. We took a tissue culture approach, since this allowed us to readily visualize the immunofluorescent labeling of individual growth cones, and identified the two cell types by previous retrograde labeling with DiI. Two dorsal root ganglion explants, one containing DiI-labeled cutaneous neurons and the other containing DiI-labeled muscle sensory neurons, from opposite sides of the same embryo, were plated together in each culture dish. For all the CAMs we studied (NCAM, polysialylated NCAM, G4/L1, axonin-1, SC1/DM-GRASP/BEN, and N-cadherin), the intensity of immunofluorescent labeling typically was fairly uniform on the growth cone, its filopodia, and the portion of the neurite just proximal tothe growth cone. Only one CAM, axonin-1, exhibited labeling that was especially intense at sites of interneuronal contact. Quantification of labeling intensities using image analysis showed that cutaneous and muscle sensory growth cones did not consistently differ from one another in their levels of expression of G4/L1 or of axonin-1. The latter finding stands in contrast to recent reports claiming that axonin-1 is not expressed on muscle sensory neurons. Each of the other CAMs (NCAM, polysialylated NCAM, SC1/DM-GRASP/BEN, and N-cadherin) also showed considerable overlap in the distribution of labeling intensities between the two populations, but overall, expression levels on muscle sensory growth cones were greater than on cutaneous growth cones. How the differential expression of some CAMs could potentially contribute to the way that cutaneous and muscle sensory growth cones become segregated from one another and the implications of these results for sensory neuron specification are discussed.

UR - http://www.scopus.com/inward/record.url?scp=0028913173&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0028913173&partnerID=8YFLogxK

U2 - 10.1006/dbio.1995.1049

DO - 10.1006/dbio.1995.1049

M3 - Article

VL - 167

SP - 563

EP - 583

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 2

ER -