B. Wehrlehaller et M. Chiquet, DUAL FUNCTION OF TENASCIN - SIMULTANEOUS PROMOTION OF NEURITE GROWTH AND INHIBITION OF GLIAL MIGRATION, Journal of Cell Science, 106, 1993, pp. 597-610
The extracellular matrix molecule tenascin is expressed within the dev
eloping peripheral nervous system, first by migrating neural crest cel
ls and later by satellite (Schwann precursor) cells at the growing tip
s of peripheral nerves. Here we found that the neurite promoting activ
ity of tenascin for sensory neurons is developmentally regulated: very
young sensory ganglia of stage 23 (4 days old) embryos grew neurites
on tenascin as fast as on laminin and fibronectin. The growth response
of older (day 7 and 9) ganglia on laminin and fibronectin was similar
to that of 4-day-old ganglia, while on tenascin neurite growth occure
d only after a lag phase and at a slower rate. Neurite growth on tenas
cin was inhibited by antibodies to beta1 integrin and by heparin. Whil
e tenascin promotes neurite outgrowth of peripheral neurons, we found
that it does not allow satellite cell migration when it is present on
the substratum, and it inhibits migration of satellite cells on fibron
ectin when added in soluble form. In contrast, soluble tenascin did no
t significantly alter the rate of neurite growth on tenascin, fibronec
tin or laminin substrata, although neurites were straighter and less a
ttached. When isolated satellite cells were added to neurites grown on
tenascin, they preferentially adhered to and elongated along neurite
surfaces. Using patterned substrata of tenascin versus fibronectin or
laminin confirmed that tenascin borders allow neurites to pass but act
as barriers to migrating satellite cells. We postulate that tenascin
or related molecules with dual functions in cell adhesion are importan
t for peripheral nerve morphogenesis. Tenascin allows axonal growth, b
ut may restrict random satellite cell migration into the fibronectin-r
ich mesenchyme, thereby inducing the compaction of nerve fascicles.