Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1980 Aug 1;86(2):616–623. doi: 10.1083/jcb.86.2.616

Slow components of axonal transport: two cytoskeletal networks

PMCID: PMC2111498  PMID: 6156946

Abstract

We have identified two slowly moving groups of axonally transported proteins in guinea pig retinal ganglion cell axons (4). The slowest group of proteins, designated slow component a (SCa), has a transport rate of 0.25 mm/d and consists of tubulin and neurofilament protein. The other slowly transported group of proteins, designated slow components b (SCb), has a transport rate of 2-3 mm/d and consists of many polypeptides, one of which is actin (4). Our analyses of the transport kinetics of the individual polypeptides of SCa and SCb indicate that (a) the polypeptides of SCa are transported coherently in the optic axons, (b) the polypeptides of SCb are also transported coherently but completely separately from the SCa polypeptides, and (c) the polypeptides of SCa differ completely from those comprising SCb. We relate these results to our general hypothesis that slow axonal transport represents the movements of structural complexes of proteins. Furthermore, it is proposed that SCa corresponds to the microtubule- neurofilament network, and that SCb represents the transport of the microfilament network together with the proteins complexed with microfilaments.

Full Text

The Full Text of this article is available as a PDF (976.6 KB).

Selected References

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

  1. Bennett G., Di Giamberardino L., Koenig H. L., Droz B. Axonal migration of protein and glycoprotein to nerve endings. II. Radioautographic analysis of the renewal of glycoproteins in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H)fucose and (3H)-glucosamine. Brain Res. 1973 Sep 28;60(1):129–146. doi: 10.1016/0006-8993(73)90853-6. [DOI] [PubMed] [Google Scholar]
  2. Berkowitz S. A., Katagiri J., Binder H. K., Williams R. C., Jr Separation and characterization of microtubule proteins from calf brain. Biochemistry. 1977 Dec 13;16(25):5610–5617. doi: 10.1021/bi00644a035. [DOI] [PubMed] [Google Scholar]
  3. Black M. M., Lasek R. J. Axonal transport of actin: slow component b is the principal source of actin for the axon. Brain Res. 1979 Aug 10;171(3):401–413. doi: 10.1016/0006-8993(79)91045-x. [DOI] [PubMed] [Google Scholar]
  4. Bonner W. M., Laskey R. A. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. doi: 10.1111/j.1432-1033.1974.tb03599.x. [DOI] [PubMed] [Google Scholar]
  5. Buckley I. K. Three dimensional fine structure of cultured cells: possible implications for subcellular motility. Tissue Cell. 1975;7(1):51–72. doi: 10.1016/s0040-8166(75)80007-3. [DOI] [PubMed] [Google Scholar]
  6. Byers H. R., Porter K. R. Transformations in the structure of the cytoplasmic ground substance in erythrophores during pigment aggregation and dispersion. I. A study using whole-cell preparations in stereo high voltage electron microscopy. J Cell Biol. 1977 Nov;75(2 Pt 1):541–558. doi: 10.1083/jcb.75.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang C. M., Goldman R. D. The localization of actin-like fibers in cultured neuroblastoma cells as revealed by heavy meromyosin binding. J Cell Biol. 1973 Jun;57(3):867–874. doi: 10.1083/jcb.57.3.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clarke F. M., Masters C. J. On the association of glycolytic components in skeletal muscle extracts. Biochim Biophys Acta. 1974 Jul 17;358(1):193–207. doi: 10.1016/0005-2744(74)90270-8. [DOI] [PubMed] [Google Scholar]
  9. Cooper P. D., Smith R. S. The movement of optically detectable organelles in myelinated axons of Xenopus laevis. J Physiol. 1974 Oct;242(1):77–97. doi: 10.1113/jphysiol.1974.sp010695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Di Giamberardino L. D., Bennett G., Koenig H. L., Droz B. Axonal migration of protein and glycoprotein to nerve endings. 3. Cell fraction analysis of chicken ciliary ganglion after intracerebral injection of labeled precursors of proteins and glycoproteins. Brain Res. 1973 Sep 28;60(1):147–159. doi: 10.1016/0006-8993(73)90854-8. [DOI] [PubMed] [Google Scholar]
  11. Droz B., Koenig H. L., Biamberardino L. D., Di Giamberardino L. Axonal migration of protein and glycoprotein to nerve endings. I. Radioautographic analysis of the renewal of protein in nerve endings of chicken ciliary ganglion after intracerebral injection of (3H)lysine. Brain Res. 1973 Sep 28;60(1):93–127. doi: 10.1016/0006-8993(73)90852-4. [DOI] [PubMed] [Google Scholar]
  12. Fink B. R., Byers M. R., Middaugh M. E. Dynamics of colchicine effects on rapid axonal transport and axonal morphology. Brain Res. 1973 Jun 29;56:299–311. doi: 10.1016/0006-8993(73)90343-0. [DOI] [PubMed] [Google Scholar]
  13. Forman D. S., McEwen B. S., Grafstein B. Rapid transport of radioactivity in goldfish optic nerve following injections of labeled glucosamine. Brain Res. 1971 Apr 16;28(1):119–130. doi: 10.1016/0006-8993(71)90529-4. [DOI] [PubMed] [Google Scholar]
  14. Fossel E. T., Solomon A. K. Ouabain-sensitive interaction between human red cell membrane and glycolytic enzyme complex in cytosol. Biochim Biophys Acta. 1978 Jun 16;510(1):99–111. doi: 10.1016/0005-2736(78)90133-5. [DOI] [PubMed] [Google Scholar]
  15. Giolli R. A., Creel D. J. The primary optic projections in pigmented and albino guinea pigs: an experimental degeneration study. Brain Res. 1973 May 30;55(1):25–39. doi: 10.1016/0006-8993(73)90486-1. [DOI] [PubMed] [Google Scholar]
  16. Goldman J. E., Kim K. S., Schwartz J. H. Axonal transport of [3H]serotonin in an identified neuron of Aplysia californica. J Cell Biol. 1976 Aug;70(2 Pt 1):304–318. doi: 10.1083/jcb.70.2.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Goldman J. E., Schwartz J. H. Cellular specificity of serotonin storage and axonal transport in identified neurones of Aplysia californica. J Physiol. 1974 Oct;242(1):61–76. doi: 10.1113/jphysiol.1974.sp010694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goldman R. D., Milsted A., Schloss J. A., Starger J., Yerna M. J. Cytoplasmic fibers in mammalian cells: cytoskeletal and contractile elements. Annu Rev Physiol. 1979;41:703–722. doi: 10.1146/annurev.ph.41.030179.003415. [DOI] [PubMed] [Google Scholar]
  19. Goldman R. D. The use of heavy meromyosin binding as an ultrastructural cytochemical method for localizing and determining the possible functions of actin-like microfilaments in nonmuscle cells. J Histochem Cytochem. 1975 Jul;23(7):529–542. doi: 10.1177/23.7.1095652. [DOI] [PubMed] [Google Scholar]
  20. Hoffman P. N., Lasek R. J. The slow component of axonal transport. Identification of major structural polypeptides of the axon and their generality among mammalian neurons. J Cell Biol. 1975 Aug;66(2):351–366. doi: 10.1083/jcb.66.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hynes R. O., Destree A. T. 10 nm filaments in normal and transformed cells. Cell. 1978 Jan;13(1):151–163. doi: 10.1016/0092-8674(78)90146-0. [DOI] [PubMed] [Google Scholar]
  22. Karlsson J. O., Sjöstrand J. Synthesis, migration and turnover of protein in retinal ganglion cells. J Neurochem. 1971 May;18(5):749–767. doi: 10.1111/j.1471-4159.1971.tb12005.x. [DOI] [PubMed] [Google Scholar]
  23. Karlsson J. O., Sjöstrand J. Transport of microtubular protein in axons of retinal ganglion cells. J Neurochem. 1971 Jun;18(6):975–982. doi: 10.1111/j.1471-4159.1971.tb12027.x. [DOI] [PubMed] [Google Scholar]
  24. Keen J. H., Willingham M. C., Pastan I. H. Clathrin-coated vesicles: isolation, dissociation and factor-dependent reassociation of clathrin baskets. Cell. 1979 Feb;16(2):303–312. doi: 10.1016/0092-8674(79)90007-2. [DOI] [PubMed] [Google Scholar]
  25. Komiya Y., Kurokawa M. Asymmetry of protein transport in two branches of bifurcating axons. Brain Res. 1978 Jan 13;139(2):354–358. doi: 10.1016/0006-8993(78)90936-8. [DOI] [PubMed] [Google Scholar]
  26. Kuczmarski E. R., Rosenbaum J. L. Studies on the organization and localization of actin and myosin in neurons. J Cell Biol. 1979 Feb;80(2):356–371. doi: 10.1083/jcb.80.2.356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lasek R. J. Axoplasmic transport of labeled proteins in rat ventral motoneurons. Exp Neurol. 1968 May;21(1):41–51. doi: 10.1016/0014-4886(68)90032-0. [DOI] [PubMed] [Google Scholar]
  28. Lasek R. Axoplasmic transport in cat dorsal root ganglion cells: as studied with [3-H]-L-leucine. Brain Res. 1968 Mar;7(3):360–377. doi: 10.1016/0006-8993(68)90003-6. [DOI] [PubMed] [Google Scholar]
  29. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  30. Le Beux Y. J. An ultrastructural study of the synaptic densities, nematosomes, neurotubules, neurofilaments and of a further three-dimensional filamentous network as disclosed by the E-PTA staining procedure. Z Zellforsch Mikrosk Anat. 1973;143(2):239–272. doi: 10.1007/BF00307481. [DOI] [PubMed] [Google Scholar]
  31. LeBeux Y. J., Willemot J. An ultrastructural study of the microfilaments in rat brain by means of heavy meromyosin labeling. I. The perikaryon, the dendrites and the axon. Cell Tissue Res. 1975 Jun 27;160(1):1–36. doi: 10.1007/BF00219840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Levin B. E. Axonal transport of [3H]proteins in a noradrenergic system of the rat brain. Brain Res. 1978 Jul 7;150(1):55–68. doi: 10.1016/0006-8993(78)90653-4. [DOI] [PubMed] [Google Scholar]
  33. Liem R. K., Yen S. H., Salomon G. D., Shelanski M. L. Intermediate filaments in nervous tissues. J Cell Biol. 1978 Dec;79(3):637–645. doi: 10.1083/jcb.79.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lorenz T., Willard M. Subcellular fractionation of intra-axonally transport polypeptides in the rabbit visual system. Proc Natl Acad Sci U S A. 1978 Jan;75(1):505–509. doi: 10.1073/pnas.75.1.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McEwen B. S., Forman D. S., Grafstein B. Components of fast and slow axonal transport in the goldfish optic nerve. J Neurobiol. 1971;2(4):361–377. doi: 10.1002/neu.480020408. [DOI] [PubMed] [Google Scholar]
  36. Metuzals J. Configuration of a filamentous network in the axoplasm of the squid (Loligo pealii L.) giant nerve fiber. J Cell Biol. 1969 Dec;43(3):480–505. doi: 10.1083/jcb.43.3.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Metuzals J., Mushynski W. E. Electron microscope and experimental investigations of the neurofilamentous network in Deiters' neurons. Relationship with the cell surface and nuclear pores. J Cell Biol. 1974 Jun;61(3):701–722. doi: 10.1083/jcb.61.3.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Metuzals J., Tasaki I. Subaxolemmal filamentous network in the giant nerve fiber of the squid (Loligo pealei L.) and its possible role in excitability. J Cell Biol. 1978 Aug;78(2):597–621. doi: 10.1083/jcb.78.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Mori H., Komiya Y., Kurokawa M. Slowly migrating axonal polypeptides. Inequalities in their rate and amount of transport between two branches of bifurcating axons. J Cell Biol. 1979 Jul;82(1):174–184. doi: 10.1083/jcb.82.1.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Mowbray J., Moses V. The tentative identification in Escherichia coli of a multienzyme complex with glycolytic activity. Eur J Biochem. 1976 Jun 15;66(1):25–36. doi: 10.1111/j.1432-1033.1976.tb10421.x. [DOI] [PubMed] [Google Scholar]
  41. Neville D. M., Jr Molecular weight determination of protein-dodecyl sulfate complexes by gel electrophoresis in a discontinuous buffer system. J Biol Chem. 1971 Oct 25;246(20):6328–6334. [PubMed] [Google Scholar]
  42. Pearse B. M. Coated vesicles from pig brain: purification and biochemical characterization. J Mol Biol. 1975 Sep 5;97(1):93–98. doi: 10.1016/s0022-2836(75)80024-6. [DOI] [PubMed] [Google Scholar]
  43. Pollard T. D., Weihing R. R. Actin and myosin and cell movement. CRC Crit Rev Biochem. 1974 Jan;2(1):1–65. doi: 10.3109/10409237409105443. [DOI] [PubMed] [Google Scholar]
  44. Rodríguez Echandía E. L., Ramirez B. U., Fernandez H. L. Studies on the mechanism of inhibition of axoplasmic transport of neuronal organelles. J Neurocytol. 1973 Jun;2(2):149–156. doi: 10.1007/BF01474717. [DOI] [PubMed] [Google Scholar]
  45. Rubin R. W., Howard J., Leonardi C. A biochemical and ultrastructural comparison of Triton X-100 models of normal and transformed cells. Tissue Cell. 1979;11(3):413–423. doi: 10.1016/0040-8166(79)90053-3. [DOI] [PubMed] [Google Scholar]
  46. Schlaepfer W. W., Freeman L. A. Neurofilament proteins of rat peripheral nerve and spinal cord. J Cell Biol. 1978 Sep;78(3):653–662. doi: 10.1083/jcb.78.3.653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Spooner B. S., Yamada K. M., Wessells N. K. Microfilaments and cell locomotion. J Cell Biol. 1971 Jun;49(3):595–613. doi: 10.1083/jcb.49.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Stone G. C., Wilson D. L., Hall M. E. Two-dimensional gel electrophoresis of proteins in rapid axoplasmic transport. Brain Res. 1978 Apr 14;144(2):287–302. doi: 10.1016/0006-8993(78)90155-5. [DOI] [PubMed] [Google Scholar]
  49. Wang E., Goldman R. D. Functions of cytoplasmic fibers in intracellular movements in BHK-21 cells. J Cell Biol. 1978 Dec;79(3):708–726. doi: 10.1083/jcb.79.3.708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Webster R. E., Henderson D., Osborn M., Weber K. Three-dimensional electron microscopical visualization of the cytoskeleton of animal cells: immunoferritin identification of actin- and tubulin-containing structures. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5511–5515. doi: 10.1073/pnas.75.11.5511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Weiss P. A., Mayr R. Neuronal organelles in neuroplasmic ("axonal") flow. II. Neurotubules. Acta Neuropathol. 1971;5(Suppl):198–120. [PubMed] [Google Scholar]
  52. Willard M. B., Hulebak K. L. The intra-axonal transport of polypeptide H: evidence for a fifth (very slow) group of transported proteins in the retinal ganglion cells of the rabbit. Brain Res. 1977 Nov 11;136(2):289–306. doi: 10.1016/0006-8993(77)90804-6. [DOI] [PubMed] [Google Scholar]
  53. Willard M., Cowan W. M., Vagelos P. R. The polypeptide composition of intra-axonally transported proteins: evidence for four transport velocities. Proc Natl Acad Sci U S A. 1974 Jun;71(6):2183–2187. doi: 10.1073/pnas.71.6.2183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Willard M., Wiseman M., Levine J., Skene P. Axonal transport of actin in rabbit retinal ganglion cells. J Cell Biol. 1979 Jun;81(3):581–591. doi: 10.1083/jcb.81.3.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Wolosewick J. J., Porter K. R. Microtrabecular lattice of the cytoplasmic ground substance. Artifact or reality. J Cell Biol. 1979 Jul;82(1):114–139. doi: 10.1083/jcb.82.1.114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Wolosewick J. J., Porter K. R. Stereo high-voltage electron microscopy of whole cells of the human diploid line, WI-38. Am J Anat. 1976 Nov;147(3):303–323. doi: 10.1002/aja.1001470305. [DOI] [PubMed] [Google Scholar]
  57. Yamada K. M., Spooner B. S., Wessells N. K. Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol. 1971 Jun;49(3):614–635. doi: 10.1083/jcb.49.3.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Zelená J. Bidirectional movements of mitochondria along axons of an isolated nerve segment. Z Zellforsch Mikrosk Anat. 1968;92(2):186–196. doi: 10.1007/BF00335646. [DOI] [PubMed] [Google Scholar]
  59. Zelená J., Lubińska L., Gutmann E. Accumulation of organelles at the ends of interrupted axons. Z Zellforsch Mikrosk Anat. 1968;91(2):200–219. doi: 10.1007/BF00364311. [DOI] [PubMed] [Google Scholar]

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

RESOURCES