Loss of axonal microtubules and neurofilaments after stretch-injury to guinea pig optic nerve fibers

Journal of Neurotrauma

Volumn 14, Issue 9, 1997, Pages 603-614

  Maxwell, W L ^a   Graham, D I ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b SOUTHERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Microtubules; Optic nerve; Stretch injury

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; CYTOSKELETON; GUINEA PIG; HEAD INJURY; MICROTUBULE; MORPHOMETRICS; NERVE FIBER MEMBRANE; NERVE FIBER TRANSPORT; NERVE INJURY; NEUROFILAMENT; NONHUMAN; OPTIC NERVE FIBER; RANVIER NODE;

EID: 0030756577     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.1997.14.603     Document Type: Article

References (56)

1. BALLIN, R.H.M., and THOMAS, P.K. (1969). Changes at the nodes of Ranvier during Wallerian degeneration: an electron microscope study. Acta Neuropathol. 14, 237-249.
2. BASS, P.W., and BLACK, M.M. (1990). Individual microtubules in the axon consist of domains that differ in both composition and stability. J. Cell Biol. 111, 495-509.
3. BASS, P.W., SLAUGHTER, T., BROWN, A., and BLACK, M.M. (1991). Microtubule dynamics in axons and dendrites. J. Neurosci. Res. 30, 134-153.
4. BASS, P.W., PIENKOWSKI, T.P., CIMBALNIK, K.A., TOYAMA, K., BAKALIS, S., AHMAD, F.J., and KOSIK, K.S. (1994). Tau confers drug stability but not cold stability to microtubules in living cells. J. Cell Sci. 107, 135-143.
5. BAUR, P.S., and STACEY, T.R. (1977). The use of PIPES buffer in the fixation of mammalian and marine tissues for electron microscopy. J. Microsc. 100, 315-327.
6. BLUMBERGS, P.C., SCOTT, G., MANAVIS, J., WAINWRIGHT, H., SIMPSON, D.A., and MCLEAN, A.J. (1994). Staining of amyloid precursor protein to study axonal damage in mild head injury. The Lancet 344, 1055-1056.
7. BRADY, S.T. (1991). Molecular motors in the nervous system. Neuron 7, 521-533.
8. CHRISTMAN, C.W., GRADY, M.S., WALKER, S.A., HOLLOWAY, K.L., and POVLISHOCK, J.T. (1994). Ultrastructural studies of diffuse axonal injury in humans. J. Neurotrauma 11, 173-186.
9. DE WAEGH, S., LEE, V.M-Y., and BRADY, S.T. (1992). Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 68, 451-463.
10. DONAT, J.R., and WISNIEWSKI, H.M. (1973). The spatiotemporal pattern of Wallerian degeneration in mammalian peripheral nerves. Brain Res. 53, 41-53.
11. FRIEDE, R.L., BARDOSI, A., and WEGENER, G. (1985). Effects of cold adaptation and starvation on sciatic nerve fibers in the frog. Exp. Neurol. 90, 434-443.
12. GASKIN, F., CANTON, C.R., and SHELANSKI, M.L. (1975). Biochemical studies on in vitro assembly and disassembly of microtubules. Ann. N. Y. Acad. Sci. 253, 133-146.
13. GENNARELLI, T.A., THIBAULT, L.E., TIPPERMAN, R., TOMEI, G., SERGOT, R., BROWN, M., MAXWELL, W.L., GRAHAM, D.I., ADAMS, J.H., IRVINE, A., GENNARELLI, L.M., DUHAIME, A.C., BOOCK, R., and GREENBERG, J. (1989). Axonal injury in the optic nerve: A model simulating diffuse axonal injury in the brain. J. Neurosurg. 71, 315-325.
14. GENTLEMAN, S.M., ROBERTS, G.W., GENNARELLI, T.A., MAXWELL, W.L., ADAMS, J.H., KERR, S., and GRAHAM, D.I. (1995). Axonal injury: a universal consequence of fatal closed head injury? Acta Neuropathol. 89, 537-543.
15. GLASS, J.D., and GRIFFIN, J.W. (1991). Neurofilament redistribution in transected nerves: evidence for bidirectional transport of neurofilaments. J. Neurosci. 11, 3146-3154.
16. GLASS, J.D., SCHRYER, B.L., and GRIFFIN, J.W. (1994). Calcium-mediated degeneration of the axonal cytoskeleton in the Ola mouse. J. Neurochem. 62, 2472-2745.
17. GRADY, M.S., MCLAUGHLIN, M.R., CHRISTMAN, C.W., VALADKA, A.B., FLINGER, C.L., and POVLISHOCK, J.T. (1993). The use of antibodies targeted against the neurofilament subunits for the detection of diffuse axonal injury in humans. J. Neuropathol. Exp. Neurol. 52, 143-152.
18. GUY, J., ELLIS, A., KELLEY, K., and HOPE, G.M. (1989). Spectra of G ratio, myelin sheath thickness, and axon and fiber diameter in the guinea pig optic nerve. J. Comp. Neurol. 287, 446-454.
19. HEIDEMANN, S.R., HAMBURG, M.A., THOMAS, S.J., SONG, B., LINDLEY, S., and CHU, D. (1984). Spatial organisation of axonal microtubules. J. Cell Biol. 99, 1289-1295.
20. HUFFMAN, P.N., THOMPSON, G.W., GRIFFIN, J.W., and PRICE, D.L. (1985). Changes in neurofilament transport coincide temporally with alterations in the caliber of axons in regenerating motor fibres. J. Cell Biol. 101, 1332-1340.
21. ISHISE, J., and ROSENBLUTH, J. (1986). Nodal and paranodal structural changes in frog optic nerve during early Wallerian degeneration. J. Neurocytol. 15, 657-670.
22. JAFARI, S.S., MAXWELL, W.L., NIELSON, M., and GRAHAM, D.I. (1997). Axonal cytoskeletal changes after nondisruptive axonal injury. J. Neurocytol. 26, 207-221.
23. JOB, D., FISCHER, E.H., and MARGOLIS, R.L. (1981). Rapid disassembly of cold-stable microtubules by calmodulin. Proc. Natl. Acad. Sci. USA 78, 4679-4682.
24. LANGFORD, G.M. (1978). In vitro assembly of dogfish brain tubulin and induction of coiled ribbon polymers by calcium. Exp. Cell Res. 111, 139-151.
25. MARGOLIS, R.L. (1983). Calcium and microtubules. In Calcium and Cell Function Vol IV W.Y. Cheung (ed.). Academic Press, New York, pp. 313-335.
26. MARGULIES, S.S., THIBAULT, L.E., and GENNARELLI, T.A. (1990). Physical model simulations of brain injury in the primate. J. Biomech. 23, 823-836.
27. MARTINEZ, A.J., and FRIEDE, R.L. (1970). Accumulation of axoplasmic organelles in swollen nerve fibres. Brain Res. 19, 183-198.
28. MATA, M., KUPINA, N., and FINK, D.J. (1992). Phosphorylation-dependent neurofilament epitopes are reduced at the node of Ranvier. J. Neurocytol. 21, 199-210.
29. MATSUMURA, F., and HAYASHI, M. (1976). Polymorphism of tubulin assembly. In vitro formation of sheet, twisted ribbon, and microtubule. Biochim. Biophys. Acta 453, 162-175.
30. MAXWELL, W.L. (1996). Histopathological changes at central nodes of Ranvier after stretch-injury. Microsc. Res. Tech. 34, 522-535.
31. MAXWELL, W.L., IRVINE, A., GRAHAM, D.I., ADAMS, J.H., GENNARELLI, T.A., TIPPERMAN, R., and STURATIS, M. (1991). Focal axonal injury: the early axonal response to stretch. J. Neurocytol. 20, 157-164.
32. MAXWELL, W.L., WATT, C., GRAHAM, D.I., and GENNARELLI, T.A. (1993). Ultrastructural evidence of axonal shearing as a result of lateral acceleration of the head in non-human primates. Acta Neuropathol. 86, 136-144.
33. MAXWELL, W.L., McCREATH, B.J., GRAHAM, D.I., and GENNARELLI, T.A. (1995). Cytochemical evidence for redistribution of membrane pump calcium-ATPase and ecto-Ca-ATPase activity, and calcium influx in myelinated nerve fibres of the optic nerve after stretch injury. J. Neurocytol. 24, 925-942.
34. MAXWELL, W.L., POVLISHOCK, J.T., and GRAHAM, D.I. (1997). A mechanistic analysis of non-disruptive axonal injury. J. Neurotrauma 14(7), 419-440.
35. MINWEGEN, P., and FRIEDE, R.L. (1984). Conduction velocity varies with osmotically induced changes in the area of the axon's profile. Brain Res. 279, 105-113.
36. NAKAZAWA, E., and ISCHIKAWA, H. (1995). Occurrence of fasciculated microtubules at nodes of Ranvier in rat spinal roots. J. Neurocytol. 24, 399-407.
37. NISHIDA, E., and SAKAI, H. (1977). Calcium-sensitivity of the microtubule reassembly system. Difference between crude brain extract and purified microtubular proteins. J. Biochem. (Tokyo) 82, 303-306.
38. OLMSTED, J.B., and BORISY, G.G. (1975). Ionic and nucleotide requirements for microtubule polymerization in vitro. Biochem. 14, 2996-3005.
39. PETTUS, E.H., CHRISTMAN, C.W., GIEBEL, M.L., and POVLISHOCK, J.T. (1994). Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J. Neurotrauma 11, 507-522.
40. PETTUS, E.H., and POVLISHOCK, J.T. (1996). Characterization of a distinct subset of intra-axonal ultrastructural changes associated with traumatically induced alteration in axolemma permeability. Brain Res. 722, 1-11.
41. POVLISHOCK, J.T. (1992). Traumatically induced axonal injury: Pathogenesis and pathobiological implications. Brain Pathol. 2, 1-12.
42. POVLISHOCK, J.T., BECKER, D.P., CHENG, C.L.Y., and VAUGHAN, G.W. (1983). Axonal change in minor head injury. J. Neuropathol. Exp. Neurol. 42, 225-242.
43. POVLISHOCK, J.T., and CHRISTMAN, C.W. (1995). The pathobiology of traumatically induced axonal injury in animals and humans: A review of current thoughts. J. Neurotrauma 12, 555-562.
44. PRICE, R.L., PAGGI, P., LASEK, R.J., and KATZ, M.J. (1988). Neurofilaments are spaced randomly in the radial dimension of axons. J. Neurocytol. 17, 55-62.
45. RELES, A., and FRIEDE, R.L. (1991). Axonal cytoskeleton at the nodes of Ranvier. J. Neurocytol. 20, 450-458.
46. SHEETZ, M.P., STEUER, E.R., and SCHROER, T.A. (1989). The mechanism and regulation of fast axonal transport. TINS 12, 474-478.
47. SMITH, R.S. (1991). Rapid organelle transport in axons. Adv. Struct. Biol. 1, 91-116.
48. SMITH, R.S., and SNYDER, R.E. (1995). Anterograde to retrograde reversal of fast axonal transport within cold blocked and rewarmed intact axons. Brain Res. 672, 205-213.
49. SZARO, B.G., WHITNALL, M.H., and GAINER, H. (1990). Phosphorylation-dependent epitopes on neurofilament proteins and neurofilament densities differ in axons in the corticospinal and primary sensory dorsal column tracts in the rat spinal cord. J. Comp. Neurol. 302, 220-235.
50. 2+-dependent and independent binding of modulator protein to the particulate fraction from brain. J. Cyclic Nucleotide Res. 4, 219-231.
51. WAXMAN, S.G., BLACK, J.A., STYS, P.K., and RANSOM, B.R. (1992). Ultrastructural concomitants of anoxic injury and early post-anoxic recovery in rat optic nerve. Brain Res. 574, 105-119.
52. WAXMAN, S.G., BLACK, J.A., RANSOM, B.R., and STYS, P.K. (1993). Protection of the axonal cytoskeleton in anoxic optic nerve by decreased extracellular calcium. Brain Res. 614, 137-145.
53. WEISENBERG, R. (1972). Microtubule formation in vitro in solutions containing low calcium concentrations. Science 177, 1104-1105.
54. WHITE, L.A., BAAS. P.W., and HEIDEMANN, S.R. (1987). Microtubule stability in severed axons. J. Neurocytol. 16, 775-784.
55. WRIGLEY, N.G. (1968). The lattice spacing of crystalline catalase as an internal standard of length in electron microscopy. J. Ultrastruct. Res. 24, 454-464.
56. YAGHMAI, A., and POVLISHOCK, J.T. (1992). Traumatically induced reactive charge as visualized through the use of monoclonal antibodies targeted to the neurofilament nutrients. J. Neuropathol. Exp. Neurol. 51, 158-176.