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J Cell Biol. 1980 August 1; 86(2): 616–623.
PMCID: PMC2111498

Slow components of axonal transport: two cytoskeletal networks


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.

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Selected References

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  • Bennett G, Di Giamberardino L, Koenig HL, 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. [PubMed]
  • Berkowitz SA, Katagiri J, Binder HK, Williams RC., Jr Separation and characterization of microtubule proteins from calf brain. Biochemistry. 1977 Dec 13;16(25):5610–5617. [PubMed]
  • Black MM, Lasek RJ. 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. [PubMed]
  • Bonner WM, Laskey RA. A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem. 1974 Jul 1;46(1):83–88. [PubMed]
  • Buckley IK. Three dimensional fine structure of cultured cells: possible implications for subcellular motility. Tissue Cell. 1975;7(1):51–72. [PubMed]
  • Byers HR, Porter KR. 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. [PMC free article] [PubMed]
  • Chang CM, Goldman RD. 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. [PMC free article] [PubMed]
  • Clarke FM, Masters CJ. On the association of glycolytic components in skeletal muscle extracts. Biochim Biophys Acta. 1974 Jul 17;358(1):193–207. [PubMed]
  • Cooper PD, Smith RS. The movement of optically detectable organelles in myelinated axons of Xenopus laevis. J Physiol. 1974 Oct;242(1):77–97. [PubMed]
  • Di Giamberardino LD, Bennett G, Koenig HL, 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. [PubMed]
  • Droz B, Koenig HL, Biamberardino LD, 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. [PubMed]
  • Rodríguez Echandía EL, Ramirez BU, Fernandez HL. Studies on the mechanism of inhibition of axoplasmic transport of neuronal organelles. J Neurocytol. 1973 Jun;2(2):149–156. [PubMed]
  • Fink BR, Byers MR, Middaugh ME. Dynamics of colchicine effects on rapid axonal transport and axonal morphology. Brain Res. 1973 Jun 29;56:299–311. [PubMed]
  • Forman DS, McEwen BS, Grafstein B. Rapid transport of radioactivity in goldfish optic nerve following injections of labeled glucosamine. Brain Res. 1971 Apr 16;28(1):119–130. [PubMed]
  • Fossel ET, Solomon AK. Ouabain-sensitive interaction between human red cell membrane and glycolytic enzyme complex in cytosol. Biochim Biophys Acta. 1978 Jun 16;510(1):99–111. [PubMed]
  • Giolli RA, Creel DJ. The primary optic projections in pigmented and albino guinea pigs: an experimental degeneration study. Brain Res. 1973 May 30;55(1):25–39. [PubMed]
  • Goldman JE, Kim KS, Schwartz JH. Axonal transport of [3H]serotonin in an identified neuron of Aplysia californica. J Cell Biol. 1976 Aug;70(2 Pt 1):304–318. [PMC free article] [PubMed]
  • Goldman JE, Schwartz JH. Cellular specificity of serotonin storage and axonal transport in identified neurones of Aplysia californica. J Physiol. 1974 Oct;242(1):61–76. [PubMed]
  • Goldman RD. 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. [PubMed]
  • Goldman RD, Milsted A, Schloss JA, Starger J, Yerna MJ. Cytoplasmic fibers in mammalian cells: cytoskeletal and contractile elements. Annu Rev Physiol. 1979;41:703–722. [PubMed]
  • Hoffman PN, Lasek RJ. 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. [PMC free article] [PubMed]
  • Hynes RO, Destree AT. 10 nm filaments in normal and transformed cells. Cell. 1978 Jan;13(1):151–163. [PubMed]
  • Karlsson JO, Sjöstrand J. Synthesis, migration and turnover of protein in retinal ganglion cells. J Neurochem. 1971 May;18(5):749–767. [PubMed]
  • Karlsson JO, Sjöstrand J. Transport of microtubular protein in axons of retinal ganglion cells. J Neurochem. 1971 Jun;18(6):975–982. [PubMed]
  • Keen JH, Willingham MC, Pastan IH. Clathrin-coated vesicles: isolation, dissociation and factor-dependent reassociation of clathrin baskets. Cell. 1979 Feb;16(2):303–312. [PubMed]
  • Komiya Y, Kurokawa M. Asymmetry of protein transport in two branches of bifurcating axons. Brain Res. 1978 Jan 13;139(2):354–358. [PubMed]
  • Kuczmarski ER, Rosenbaum JL. Studies on the organization and localization of actin and myosin in neurons. J Cell Biol. 1979 Feb;80(2):356–371. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Lasek RJ. Axoplasmic transport of labeled proteins in rat ventral motoneurons. Exp Neurol. 1968 May;21(1):41–51. [PubMed]
  • Laskey RA, Mills AD. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. [PubMed]
  • Le Beux YJ. 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. [PubMed]
  • LeBeux YJ, 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. [PubMed]
  • Levin BE. Axonal transport of [3H]proteins in a noradrenergic system of the rat brain. Brain Res. 1978 Jul 7;150(1):55–68. [PubMed]
  • Liem RK, Yen SH, Salomon GD, Shelanski ML. Intermediate filaments in nervous tissues. J Cell Biol. 1978 Dec;79(3):637–645. [PMC free article] [PubMed]
  • 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. [PubMed]
  • McEwen BS, Forman DS, Grafstein B. Components of fast and slow axonal transport in the goldfish optic nerve. J Neurobiol. 1971;2(4):361–377. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Metuzals J, Mushynski WE. 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. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Neville DM., 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]
  • Pearse BM. Coated vesicles from pig brain: purification and biochemical characterization. J Mol Biol. 1975 Sep 5;97(1):93–98. [PubMed]
  • Pollard TD, Weihing RR. Actin and myosin and cell movement. CRC Crit Rev Biochem. 1974 Jan;2(1):1–65. [PubMed]
  • Rubin RW, 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. [PubMed]
  • Schlaepfer WW, Freeman LA. Neurofilament proteins of rat peripheral nerve and spinal cord. J Cell Biol. 1978 Sep;78(3):653–662. [PMC free article] [PubMed]
  • Spooner BS, Yamada KM, Wessells NK. Microfilaments and cell locomotion. J Cell Biol. 1971 Jun;49(3):595–613. [PMC free article] [PubMed]
  • Stone GC, Wilson DL, Hall ME. Two-dimensional gel electrophoresis of proteins in rapid axoplasmic transport. Brain Res. 1978 Apr 14;144(2):287–302. [PubMed]
  • Wang E, Goldman RD. Functions of cytoplasmic fibers in intracellular movements in BHK-21 cells. J Cell Biol. 1978 Dec;79(3):708–726. [PMC free article] [PubMed]
  • Webster RE, 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. [PubMed]
  • Weiss PA, Mayr R. Neuronal organelles in neuroplasmic ("axonal") flow. II. Neurotubules. Acta Neuropathol. 1971;5(Suppl):198–120. [PubMed]
  • Willard M, Cowan WM, Vagelos PR. 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. [PubMed]
  • Willard MB, Hulebak KL. 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. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Wolosewick JJ, Porter KR. Stereo high-voltage electron microscopy of whole cells of the human diploid line, WI-38. Am J Anat. 1976 Nov;147(3):303–323. [PubMed]
  • Wolosewick JJ, Porter KR. Microtrabecular lattice of the cytoplasmic ground substance. Artifact or reality. J Cell Biol. 1979 Jul;82(1):114–139. [PMC free article] [PubMed]
  • Yamada KM, Spooner BS, Wessells NK. Ultrastructure and function of growth cones and axons of cultured nerve cells. J Cell Biol. 1971 Jun;49(3):614–635. [PMC free article] [PubMed]
  • Zelená J. Bidirectional movements of mitochondria along axons of an isolated nerve segment. Z Zellforsch Mikrosk Anat. 1968;92(2):186–196. [PubMed]
  • Zelená J, Lubińska L, Gutmann E. Accumulation of organelles at the ends of interrupted axons. Z Zellforsch Mikrosk Anat. 1968;91(2):200–219. [PubMed]

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