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Journal of Neuroscience, Vol 14, 384-398, Copyright © 1994 by Society for Neuroscience
Cytoskeletal movements and substrate interactions during initiation of neurite outgrowth by sympathetic neurons in vitro
CL Smith
Laboratory of Neural Control, NINDS, National Institutes of Health, Bethesda, Maryland 20892.
The initial outgrowth of neurites from chick sympathetic neurons grown in
vitro was investigated by time-lapse microscopy with laser-scanning and
conventional light microscopes. Video-enhanced contrast, differential
interference contrast optics (VECDIC) were used to monitor movements of
neuronal cytoplasm, as well as the movements of small beads attached to the
surface membrane, and interference reflection microscopy (IRM) was used to
determine the concomitant pattern of attachment to the growth substrate
(polyornithine or laminin). Related changes in the distributions of actin
filaments, microtubules, and neurofilaments were determined by fluorescence
labeling methods. Neurite formation on both substrates entailed invasion of
the actin cores of filopodia by cytoplasm containing microtubules and
neurofilaments. Small beads attached to the surface membrane surrounding
the cytoplasm moved outward simultaneously with the cytoplasm. Cytoplasm
invaded filopodia of neurons plated on laminin soon after attachment to the
substrate or, for neurons generated in vitro, within as little as 3 min
after cytokinesis. However, cytoplasm invaded filopodia of neurons grown on
polyornithine only when they contacted a three-dimensional object such as
another cell or a large, polyornithine-coated polystyrene bead. The
observation that adhesion of filopodia to polyornithine-coated beads can
initiate neurite formation is inconsistent with the commonly held view that
neurite formation requires adhesion mediated by specific cell adhesion
molecules. Simultaneous IRM and DIC imaging showed that cytoplasm invaded
filopodia when only their tips were closely apposed to a substrate but not
when they were closely apposed to a substrate along their entire lengths.
These findings help to elucidate the mechanisms by which interactions
between the cytoskeleton and the growth substrate initiate and produce the
neuronal movements that lead to the formation of neurites.
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