Peanut agglutinin and chondroitin-6-sulfate are molecular markers for tissues that act as barriers to axon advance in the avian embryo

Abstract

Axon outgrowth between the spinal cord and the hindlimb of the chick embryo is constrained by three tissues that border axon pathways. Growth cones turn to avoid the posterior sclerotome, perinotochordal mesenchyme, and pelvic girdle precursor during normal development and after experimental manipulation. We wanted to know if these functionally similar barriers to axon advance also share a common molecular composition. Since the posterior sclerotome differentially binds peanut agglutinin (PNA) and since PNA binding is also typical of prechondrogenic differentiation, we examined the pattern of expression of PNA binding sites and cartilage proteoglycan epitopes in relation to axon outgrowth. We found that all three barrier tissues preferentially express both PNA binding sites and chondroitin-6-sulfate (C-6-S) immunoreactivity at the time when growth cones avoid these tissues. Moreover, both epitopes are expressed in the roof plate of the spinal cord and in the early limb bud, two additional putative barriers to axon advance. In contrast, neither epitope is detected in peripheral axon pathways. In the somites, this dichotomous pattern of expression clearly preceded the invasion of the anterior sclerotome by either motor growth cones or neural crest cells. However, in the limb, barrier markers disappeared from presumptive axon pathways in concert with the invasion of axons. Since this coordinate pattern suggested that the absence of barrier markers in these axon pathways requires an interaction with growth cones, we analyzed the pattern of barrier marker expression following unilateral neural tube deletions. We found that PNA-negative axon pathways developed normally even in the virtual absence of axon outgrowth. We conclude that the absence of staining with carbohydrate-specific barrier markers is an independent characteristic of the cells that comprise axon pathways. These results identify two molecular markers that characterize known functional barriers to axon advance and suggest that barrier tissues may impose patterns on peripheral nerve outgrowth by virtue of their distinct molecular composition.

Long‐distance cue from emerging dermis stimulates neural crest melanoblast migration

“…cult to distinguish, it is notable that the distribution of a marker for inhibitory function in the proximal path is unchanged by the dermal grafts. Peanut agglutinin lectin, an inhibitory marker (Oakley and Tosney, 1991;Oakley et al, 1994), is retained within the proximal path even in the presence of a large graft ( Fig. 3E; n ϭ 12).…”

Extracellular matrix of the central nervous system: from neglect to challenge

“…The rapid switch from embryonic and early postnatal extracellular matrices to their mature form in the normal adult CNS (Rauch 2004), the fast disappearance of CSPGs from the predestined axonal pathways observed in the developing periphery (Landolt et al 1995;Oakley and Tosney 1991), as well as the reactive changes following nervous system lesions (Galtrey and Fawcett 2007; Zurn and Bandtlow 2006) cannot solely be attributed to adjustments in the ECM expression patterns, but must also depend on highly active proteolytic processes (Agrawal et al 2008;Ethell and Ethell 2007;Flannery 2006;Gottschall et al 2005;Milward et al 2007;Porter et al 2005). The selective turnover of lecticans may in this context be essential for altering the cell migration and axon growth properties of many nervous tissues.…”

The Brain Chondroitin Sulfate Proteoglycan Brevican Associates with Astrocytes Ensheathing Cerebellar Glomeruli and Inhibits Neurite Outgrowth from Granule Neurons

“…Inhibition of axon growth in vivo often occurs at specific sites in the nervous system, referred to as "barriers." Chondroitin sulfates have been implicated as active components of barriers that cause the repulsion of advancing axons in vivo (Snow et al, 1990(Snow et al, , 1991Oakley and Tosney, 1991;Perris et al, 1991;Brittis et al, 1992).…”