Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Nov 1;111(5):1949–1957. doi: 10.1083/jcb.111.5.1949

Growth cone behavior and production of traction force

PMCID: PMC2116337  PMID: 2229183

Abstract

The growth cone must push its substrate rearward via some traction force in order to propel itself forward. To determine which growth cone behaviors produce traction force, we observed chick sensory growth cones under conditions in which force production was accommodated by movement of obstacles in the environment, namely, neurites of other sensory neurons or glass fibers. The movements of these obstacles occurred via three, different, stereotyped growth cone behaviors: (a) filopodial contractions, (b) smooth rearward movement on the dorsal surface of the growth cone, and (c) interactions with ruffling lamellipodia. More than 70% of the obstacle movements were caused by filopodial contractions in which the obstacle attached at the extreme distal end of a filopodium and moved only as the filopodium changed its extension. Filopodial contractions were characterized by frequent changes of obstacle velocity and direction. Contraction of a single filopodium is estimated to exert 50-90 microdyn of force, which can account for the pull exerted by chick sensory growth cones. Importantly, all five cases of growth cones growing over the top of obstacle neurites (i.e., geometry that mimics the usual growth cone/substrate interaction), were of the filopodial contraction type. Some 25% of obstacle movements occurred by a smooth backward movement along the top surface of growth cones. Both the appearance and rate of movements were similar to that reported for retrograde flow of cortical actin near the dorsal growth cone surface. Although these retrograde flow movements also exerted enough force to account for growth cone pulling, we did not observe such movements on ventral growth cone surfaces. Occasionally obstacles were moved by interaction with ruffling lamellipodia. However, we obtained no evidence for attachment of the obstacles to ruffling lamellipodia or for directed obstacle movements by this mechanism. These data suggest that chick sensory growth cones move forward by contractile activity of filopodia, i.e., isometric contraction on a rigid substrate. Our data argue against retrograde flow of actin producing traction force.

Full Text

The Full Text of this article is available as a PDF (3.3 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aletta J. M., Greene L. A. Growth cone configuration and advance: a time-lapse study using video-enhanced differential interference contrast microscopy. J Neurosci. 1988 Apr;8(4):1425–1435. doi: 10.1523/JNEUROSCI.08-04-01425.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Argiro V., Bunge M. B., Johnson M. I. Correlation between growth form and movement and their dependence on neuronal age. J Neurosci. 1984 Dec;4(12):3051–3062. doi: 10.1523/JNEUROSCI.04-12-03051.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baas P. W., White L. A., Heidemann S. R. Microtubule polarity reversal accompanies regrowth of amputated neurites. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5272–5276. doi: 10.1073/pnas.84.15.5272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bovolenta P., Mason C. Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J Neurosci. 1987 May;7(5):1447–1460. doi: 10.1523/JNEUROSCI.07-05-01447.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bray D., Chapman K. Analysis of microspike movements on the neuronal growth cone. J Neurosci. 1985 Dec;5(12):3204–3213. doi: 10.1523/JNEUROSCI.05-12-03204.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bray D., Hollenbeck P. J. Growth cone motility and guidance. Annu Rev Cell Biol. 1988;4:43–61. doi: 10.1146/annurev.cb.04.110188.000355. [DOI] [PubMed] [Google Scholar]
  7. Bray D. Surface movements during the growth of single explanted neurons. Proc Natl Acad Sci U S A. 1970 Apr;65(4):905–910. doi: 10.1073/pnas.65.4.905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bray D., White J. G. Cortical flow in animal cells. Science. 1988 Feb 19;239(4842):883–888. doi: 10.1126/science.3277283. [DOI] [PubMed] [Google Scholar]
  9. Bretscher M. S. Endocytosis: relation to capping and cell locomotion. Science. 1984 May 18;224(4650):681–686. doi: 10.1126/science.6719108. [DOI] [PubMed] [Google Scholar]
  10. Bridgman P. C., Dailey M. E. The organization of myosin and actin in rapid frozen nerve growth cones. J Cell Biol. 1989 Jan;108(1):95–109. doi: 10.1083/jcb.108.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Buxbaum R. E., Heidemann S. R. A thermodynamic model for force integration and microtubule assembly during axonal elongation. J Theor Biol. 1988 Oct 7;134(3):379–390. doi: 10.1016/s0022-5193(88)80068-7. [DOI] [PubMed] [Google Scholar]
  12. Dennerll T. J., Joshi H. C., Steel V. L., Buxbaum R. E., Heidemann S. R. Tension and compression in the cytoskeleton of PC-12 neurites. II: Quantitative measurements. J Cell Biol. 1988 Aug;107(2):665–674. doi: 10.1083/jcb.107.2.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dennerll T. J., Lamoureux P., Buxbaum R. E., Heidemann S. R. The cytomechanics of axonal elongation and retraction. J Cell Biol. 1989 Dec;109(6 Pt 1):3073–3083. doi: 10.1083/jcb.109.6.3073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dunn G. A., Heath J. P. A new hypothesis of contact guidance in tissue cells. Exp Cell Res. 1976 Aug;101(1):1–14. doi: 10.1016/0014-4827(76)90405-5. [DOI] [PubMed] [Google Scholar]
  15. Forscher P., Smith S. J. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol. 1988 Oct;107(4):1505–1516. doi: 10.1083/jcb.107.4.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goldberg D. J., Burmeister D. W. Looking into growth cones. Trends Neurosci. 1989 Dec;12(12):503–506. doi: 10.1016/0166-2236(89)90110-0. [DOI] [PubMed] [Google Scholar]
  17. Goldberg D. J., Burmeister D. W. Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J Cell Biol. 1986 Nov;103(5):1921–1931. doi: 10.1083/jcb.103.5.1921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heath J. P. Behaviour and structure of the leading lamella in moving fibroblasts. I. Occurrence and centripetal movement of arc-shaped microfilament bundles beneath the dorsal cell surface. J Cell Sci. 1983 Mar;60:331–354. doi: 10.1242/jcs.60.1.331. [DOI] [PubMed] [Google Scholar]
  19. Huxley H. E. Muscular contraction and cell motility. Nature. 1973 Jun 22;243(5408):445–449. doi: 10.1038/243445a0. [DOI] [PubMed] [Google Scholar]
  20. Kapfhammer J. P., Raper J. A. Collapse of growth cone structure on contact with specific neurites in culture. J Neurosci. 1987 Jan;7(1):201–212. doi: 10.1523/JNEUROSCI.07-01-00201.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Katz M. J., George E. B., Gilbert L. J. Axonal elongation as a stochastic walk. Cell Motil. 1984;4(5):351–370. doi: 10.1002/cm.970040505. [DOI] [PubMed] [Google Scholar]
  22. Kerst A., Chmielewski C., Livesay C., Buxbaum R. E., Heidemann S. R. Liquid crystal domains and thixotropy of filamentous actin suspensions. Proc Natl Acad Sci U S A. 1990 Jun;87(11):4241–4245. doi: 10.1073/pnas.87.11.4241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lamoureux P., Buxbaum R. E., Heidemann S. R. Direct evidence that growth cones pull. Nature. 1989 Jul 13;340(6229):159–162. doi: 10.1038/340159a0. [DOI] [PubMed] [Google Scholar]
  24. Letourneau P. C. Cell-substratum adhesion of neurite growth cones, and its role in neurite elongation. Exp Cell Res. 1979 Nov;124(1):127–138. doi: 10.1016/0014-4827(79)90263-5. [DOI] [PubMed] [Google Scholar]
  25. Lockerbie R. O. The neuronal growth cone: a review of its locomotory, navigational and target recognition capabilities. Neuroscience. 1987 Mar;20(3):719–729. doi: 10.1016/0306-4522(87)90235-1. [DOI] [PubMed] [Google Scholar]
  26. Mitchison T., Kirschner M. Cytoskeletal dynamics and nerve growth. Neuron. 1988 Nov;1(9):761–772. doi: 10.1016/0896-6273(88)90124-9. [DOI] [PubMed] [Google Scholar]
  27. NAKAI J., KAWASAKI Y. Studies on the mechanism determining the course of nerve fibers in tissue culture. I. The reaction of the growth cone to various obstructions. Z Zellforsch Mikrosk Anat. 1959;51:108–122. doi: 10.1007/BF00345083. [DOI] [PubMed] [Google Scholar]
  28. NAKAI J. Studies on the mechanism determining the course of nerve fibers in tissue culture. II. The mechanism of fasciculation. Z Zellforsch Mikrosk Anat. 1960;52:427–449. doi: 10.1007/BF00339758. [DOI] [PubMed] [Google Scholar]
  29. Sheetz M. P., Turney S., Qian H., Elson E. L. Nanometre-level analysis demonstrates that lipid flow does not drive membrane glycoprotein movements. Nature. 1989 Jul 27;340(6231):284–288. doi: 10.1038/340284a0. [DOI] [PubMed] [Google Scholar]
  30. Smith S. J. Neuronal cytomechanics: the actin-based motility of growth cones. Science. 1988 Nov 4;242(4879):708–715. doi: 10.1126/science.3055292. [DOI] [PubMed] [Google Scholar]
  31. Taylor D. L., Condeelis J. S. Cytoplasmic structure and contractility in amoeboid cells. Int Rev Cytol. 1979;56:57–144. doi: 10.1016/s0074-7696(08)61821-5. [DOI] [PubMed] [Google Scholar]
  32. Trinkaus J. P. Further thoughts on directional cell movement during morphogenesis. J Neurosci Res. 1985;13(1-2):1–19. doi: 10.1002/jnr.490130102. [DOI] [PubMed] [Google Scholar]
  33. Tsui H. C., Lankford K. L., Klein W. L. Differentiation of neuronal growth cones: specialization of filopodial tips for adhesive interactions. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8256–8260. doi: 10.1073/pnas.82.23.8256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wessells N. K., Letourneau P. C., Nuttall R. P., Ludueña-Anderson M., Geiduschek J. M. Responses to cell contacts between growth cones, neurites and ganglionic non-neuronal cells. J Neurocytol. 1980 Oct;9(5):647–664. doi: 10.1007/BF01205031. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES