Abstract
Regenerating axons have been intensively studied with regard to the mechanisms and determinants of elongation, and several lines of evidence suggest that the delivery of cytoskeletal proteins (tubulin and actin, in particular) are correlates of outgrowth and may be rate limiting (see Lasek and Hoffman, 1976; Wujck and Lasek. 1983). In addition lo changes in axonal length, regeneration involves marked changes in axonal caliber and in cytoskeletal composition. The rcgcneraling axon provides the best available system in which to test critically the hypotheses underlying several of our recent studies. These hypotheses are that neurofilament content is the major correlate of axonal caliber and that axonal neurofilament content is, in turn, determined, in large part, by neurofilament delivery via slow axonal transport. This review will first summarize the general problem of the determinants of axonal caliber and then focus on recent data from regenerating nerves. These data can be considered in terms of three regions of the regenerating axon—the proximal stump, the maturing sprouts, and the distal sprouts.
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References
Aitkin, J. T., and Thomas, P. K., 1962, Retrograde changes in fibre size following nerve section, J. Anat. 96: 121–129.
Berthold, C. H., 1978, Morphology of normal peripheral axons, in: Physiology and Pathobiology of Axons (S. G. Waxman, ed.), pp. 3–63, Raven Press, New York.
Black, M. M., and Lasek, R. J., 1979, Slowing of the rate of axonal regeneration during growth and maturation, Exp. Neurol. 63: 108–119.
Bloom, G. S., and Vallée, R. B., 1983, Association of microtubule-associated protein 2 (MAP 2) with microtubules and intermediate filaments in cultured brain cells, J. Cell Biol. 96: 1523–1531.
Chou, S.-M., and Hartmann, H. A., 1965, Electron microscopy of focal neuroaxonal lesions produced by ß, ß′-iminodipropionitrile (IDPN) in rats, Acta Neuropathol. (Bed.) 4: 590–603.
Clark, A. W., Griffin, J. W., and Price, D. L., 1980, The axonal pathology in chronic IDPN intoxication, J. Neuropathol. Exp. Neurol. 39: 42–55.
Cragg, B. G., and Thomas, P. K., 1961, Changes in conduction velocity and fibre size proximal to peripheral nerve lesions, J. Physiol. (Lond.) 157: 315–327.
Duncan, D., 1948, Alterations in the structure of nerves caused by restricting their growth with ligatures, J. Neuropathol. Exp. Neurol. 7: 261–273.
Ellisman, M. H., and Porter, K. R., 1980, Microtrabecular structure of the axoplasmic matrix: Visualization of cross-linking structures and their distribution, J. Cell Biol. 87: 464–479.
Friede, R. L., 1971, Changes in microtubules and neurofilaments in constricted, hypoplastic nerve fibers, Acta Neuropathol. (Berl.) [Suppl.] 5: 216–225.
Friede, R. L., and Samorajski, T., 1970, Axon caliber related to neurofilaments and microtubules in sciatic nerve fibers of rats and mice, Anat. Rec. 167: 379–388.
Greenman, M. J., 1913, Studies on the regeneration of the peroneal nerve of the albino rat: Number and sectional areas of fibers: Area relation of axis to sheath, J. Comp. Neurol. 23: 479–513.
Griffin, J. W., Drachman, D. B., and Price, B. L., 1976, Fast axonal transport in motor nerve regeneration, J. Neurobiol. 7: 355–370.
Griffin, J. W., Hoffman, P. N., Clark, A. W., Carroll, P. T., and Price, D. L., 1978, Slow axonal transport of neurofilament proteins: Impairment by ß, ß′-iminodipropionitrile administration, Science 202: 633–635.
Griffin, J. W., Fahnestock, K. E., Price, D. L., and Hoffman, P. N., 1983, Microtubule-neurofilament segregation produced by ß, ß′-iminodipropionitrile: Evidence for the association of fast axonal transport with microtubules, J. Neurosci. 3: 557–566.
Griffin, J. W., Anthony, D. C., Fahnestock, K., Hoffman, P. N., and Graham, D. G., 1984, 3,4-Dimethyl-2,5-hexanedione impairs axonal transport of neurofilament proteins, J Neurosci. 4: 1516–1526.
Gutmann, E., and Sanders, F. K., 1943, Recovery of fibre numbers and diameters in the regeneration of peripheral nerves, J. Physiol. (Lond.) 101: 489–518.
Gutmann, E., Gutmann, L., Medawar, P. B., and Young, J. Z., 1942, The rate of regeneration of nerve, J. Exp. Biol. 19: 14–44.
Hirokawa, N., 1982, Cross-linker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method, J. Cell Biol. 94: 129–142.
Hirokawa, N., Glicksman, M. A., and Willard, M., 1984, Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton, J. Cell Biol. 98: 1523–1536.
Hoffman, P. N., and Lasek, R. J., 1975, The slow component of axonal transport. Identification of major structural polypeptides of the axon and their generality among mammalian neurons, J. Cell Biol. 66: 351–366.
Hoffman, P. N., and Lasek, R. J., 1980, Axonal transport of the cytoskeleton in regenerating motor neurons: Constancy and change, Brain Res. 202: 317–333.
Hoffman, P. N., Lasek, R. J., Griffin, J. W., and Price, D. L., 1983, Slowing of the axonal transport of neurofilament protein during development, J. Neurosci. 3: 1694–1700.
Hoffman, P. N., Griffin, J. W., and Price, D. L., 1984, Control of axonal caliber by neurofilament transport J. Cell Biol. (in press).
Hursh, J. B., 1939, Conduction velocity and diameter of nerve fibers, Am J. Physiol. 127: 131–139.
Ingebritsen, T. S., and Cohen, P., 1983, Protein phosphatases: Properties and role in cellular regulation, Science 221: 333–338.
Jones, S. M., and Williams, R. C., Jr., 1982, Phosphate content of the polypeptides of mammalian neurofilaments, J. Cell Biol. 95: 227a.
Kreutzberg, G. W., and Schubert, P., 1971a, Volume changes in the axon during regeneration, Acta Neuropathol. (Berl.) 17: 220–226.
Kreutzberg, G. W., and Schubert, P., 1971b, Changes in axonal flow during regeneration of mammalian motor nerves, Acta Neuropathol. (Berl.) [Suppl.] 5: 70–75.
Kuno, M., Miyata, Y., and Munoz-Martinez, E. J., 1974a, Differential reactions of fast and slow α-motoneurones to axotomy, J. Physiol. (Lond.) 240: 725–739.
Kuno, M., Miyata, Y., and Munoz-Martinez, E. J., 1974b, Properties of fast and slow alpha motoneurones following motor reinnervation, J. Physiol. (Lond.) 242: 273–288.
Lasek, R. J., and Black, M. M., 1977, How do axons stop growing? Some clues from the metabolism of the proteins in the slow component of axonal transport, in: Mechanisms, Regulation and Special Functions of Protein Synthesis in the Brain (S. Roberts, A. Lajtha, and W. H. Gispen, eds.), pp. 161–169, Elsevier/North Holland Biomedical Press, Amsterdam.
Lasek, R. J., and Hoffman, P. N., 1976, The neuronal cytoskeleton, axonal transport and axonal growth, Cold Spring Harbor Conf. Cell Prolif. 3: 1021–1049.
Leterrier, J.-F., Liem, R. K. H., and Shelanski, M. L., 1981, Preferential phosphorylation of the 150,000 molecular weight component of neurofilaments by a cyclic AMP-dependent, micro-tubule-associated protein kinase, J. Cell Biol. 90: 755–760.
Liem, R. K. H., Yen, S-H., Salomon, G. D., and Shelanski, M. L., 1978, Intermediate filaments in nervous tissues, J. Cell Biol. 79: 637–645.
Matus, A., Bernhardt, R., and Hugh-Jones, T., 1981, High molecular weight microtubule-asso-ciated proteins are preferentially associated with dendritic microtubules in brain, Proc. Natl. Acad. Sci. U.S.A. 78: 3010–3014.
Morris, J. R., and Lasek, R. J., 1982, Stable polymers of the axonal cytoskeleton: The axoplasmic ghost, J. Cell Biol. 92: 192–198.
Nystrom, B., 1968, Fibre diameter increase in nerves to “slow-red” and “fast-white” cat muscles during postnatal development, Acta Neurol. Scand. 44: 265–294.
Pant, H. C., Shecket, G., Gainer, H., and Lasek, R. J., 1978, Neurofilament protein is phospho-rylated in the squid giant axon, J. Cell Biol. 78: 23–27.
Papasozomenos, S. Ch., Binder, L. I., Bender, P. K., and Payne, M. R., 1983, The axonal cytoskeleton in the ß,ß′-iminodipropionitrile (IDPN) model, J. Neuropathol. Exp. Neurol. 42:310.
Peters, A., and Vaughn, J. E., 1967, Microtubules and filaments in the axons and astrocytes of early postnatal rat optic nerves, J. Cell Biol. 32: 113–119.
Roots, B. I., 1983, Neurofilament accumulation induced in synapses by leupeptin, Science 221: 971–972.
Schlaepfer, W. W., 1978, Observations on the disassembly of isolated mammalian neurofilaments, J. Cell Biol. 76: 50–56.
Schlaepfer, W. W., and Freeman, L. A., 1978, Neurofilament proteins of rat peripheral nerve and spinal cord, J. Cell Biol. 78: 653–662.
Takenaka, T., and Inomata, K., 1981, Axoplasmic transport of microtubule-associated proteins in the rat sciatic nerve, J. Neurobiol. 12: 479–486.
Tsukita, S., Usukura, J., Tsukita, S., and Ishikawa, H., 1982, The cytoskeleton in myelinated axons: A freeze-etch replica study, Neuroscience 7: 2135–2147.
Tytell, M., and Lasek, R. J., 1978, Axonal transport in guinea pig optic neurons: Each component consists of a distinct pattern of proteins, Neurosci. Abstr. 6:37.
Vallée, R. B., DiBartolomeis, M. J., and Theurkauf, W. E., 1981, A protein kinase bound to the projection portion of MAP 2 (microtubule-associated protein 2), J. Cell Biol. 90: 568–576.
Weiss, P. A., and Mayr, R., 1971, Organelles in neuroplasmic (“axonal”) flow: Neurofilaments, Proc. Natl. Acad. Sci. U.S.A. 68: 846–850.
Willard, M., and Simon, C., 1981, Antibody decoration of neurofilaments, J. Cell Biol 89: 198–205.
Wujek, J. R., and Lasek, R. J., 1983, Correlation of axonal regeneration and slow component b in two branches of a single axon, J. Neurosci. 3: 243–251.
Yamada, K. M., Spooner, B. S., and Wessells, N. K., 1971, Ultrastructure and function of growth cones and axons of cultured nerve cells, J. Cell Biol. 49: 614–635.
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© 1984 Plenum Press, New York
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Hoffman, P.N., Griffin, J.W., Price, D.L. (1984). Neurofilament Transport in Axonal Regeneration. In: Elam, J.S., Cancalon, P. (eds) Axonal Transport in Neuronal Growth and Regeneration. Advances in Neurochemistry, vol 22. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-1197-3_14
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DOI: https://doi.org/10.1007/978-1-4684-1197-3_14
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