Kinetic-structural analysis of neuronal growth cone veil motility.
Neuronal growth cone advance was investigated by correlative light and electron microscopy carried out on chick dorsal root ganglion cells. Advance was analyzed in terms of the two principal organelles responsible for protrusive motility in the growth cone - namely, veils and filopodia. Veils alternated between rapid phases of protrusion and retraction. Electron microscopy revealed characteristic structural differences between the phases. Our results provide a significant advance in three respects: first, protruding veils are comprised of a densely branched network of actin filaments that is lamellipodial in appearance and includes the Arp2/3 complex. On the basis of this structural and biomarker evidence, we infer that the dendritic nucleation and/or array-treadmilling mechanism of protrusive motility is conserved in veil protrusion of growth cones as in the motility of fibroblasts; second, retracting veils lack dendritic organization but contain a sparse network of long filaments; and third, growth cone filopodia have the capacity to nucleate dendritic networks along their length, a property consistent with veil formation seen at the light microscopic level but not previously understood in supramolecular terms. These elements of veil and filopodial organization, when taken together, provide a conceptual framework for understanding the structural basis of growth cone advance.
Mongiu
Anne K
AK
Department of Cell and Molecular Biology, Northwestern University Feinberg School of Medicine, Marine Biological Laboratory, 303 E. Chicago Avenue, Chicago, IL 60611, USA. akmongi@northwestern.edu
Weitzke
Elizabeth L
EL
Chaga
Oleg Y
OY
Borisy
Gary G
GG
D008841:Actin Cytoskeleton / Q000502:physiology*; D051376:Actin-Related Protein 2-3 Complex / Q000502:physiology*; D000818:Animals; D002465:Cell Movement / Q000502:physiology; D002642:Chick Embryo; D005347:Fibroblasts / Q000502:physiology; D005727:Ganglia, Spinal / Q000166:cytology / Q000502:physiology; D020439:Growth Cones / Q000502:physiology* / Q000648:ultrastructure; D007700:Kinetics; D008954:Models, Biological; D009474:Neurons / Q000502:physiology* / Q000648:ultrastructure; D011554:Pseudopodia / Q000502:physiology* / Q000648:ultrastructure
D051376:Actin-Related Protein 2-3 Complex