Tensile regulation of axonal elongation and initiation

Jing Zheng, P. Lamoureux, V. Santiago, T. Dennerll, R. E. Buxbaum, S. R. Heidemann*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

178 Scopus citations

Abstract

Neurites of chick sensory neurons in culture were attached by their growth cones to glass needles of known compliance and were subjected to increasing tensions as steps of constant force; each step lasted 30-60 min and was 25-50 μdyn greater than the previous step. After correcting for elastic stretching, neurite elongation rate increased in proportion to tension magnitude greater than a tension threshold. The value of the tension threshold required for growth varied between 25 and 560 μdyn, with most between 50 and 150 μdyn. The growth sensitivity of neurites to tension was surprisingly high: an increase in tension of 1 μdyn increased the elongation rate an average of about 1.5 μm/hr. The linear relationship between growth rate and tension provides a simple control mechanism for axons to accommodate tissue expansion in growing animals that consistently maintains a moderate rest tension on axons. Styrene microspheres treated with polyethyleneimine were used to label the surface of neurites in order to determine the site and pattern of surface addition during the experimental ''towed growth'' regime. New membrane is added interstitially throughout the neurite, but different regions of neurite vary widely in the amount of new membrane added. This contrasts with membrane addition specifically at the distal end in growth-cone-mediated growth. The different sites for membrane addition in growth mediated by towing and by the growth cone indicate that the membrane addition process is sensitive to the mode of growth. We confirmed the finding of Bray (1984) that neurites can be initiated de novo by application of tension to the cell margin of chick sensory neurons. Initiation required tensions above some threshold and tension magnitudes very similar to those required for neurite elongation. Initiated neurites developed growth cones capable of normal motility and axonal elongation. Such neurites also contained a normal array of microtubules as assessed by immunofluorescence and by electron microscopy.

Original languageEnglish (US)
Pages (from-to)1117-1125
Number of pages9
JournalJournal of Neuroscience
Volume11
Issue number4
DOIs
StatePublished - 1991

ASJC Scopus subject areas

  • Neuroscience(all)

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