A mechanistic analysis of nondisruptive axonal injury: A review

Journal of Neurotrauma

Volumn 14, Issue 7, 1997, Pages 419-440

  Maxwell, William L ^a   Povlishock, John T ^b   Graham, David L ^c  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SOUTHERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Axolemmal perturbation; Cytoskeletal change; Delayed axotomy; Diffuse axonal injury; Experimental animals and human studies; Impaired axoplasmic transport; Traumatic brain injury

Indexed keywords

CALCIUM; CALMODULIN; CALPAIN;

AXOPLASM; BRAIN INJURY; CALCIUM TRANSPORT; CELL ORGANELLE; CYTOSKELETON; DEPHOSPHORYLATION; HUMAN; MICROTUBULE; NERVE CELL LESION; NERVE FIBER DEGENERATION; NERVE FIBER MEMBRANE; NERVE FIBER TRANSECTION; NERVE INJURY; NEUROFILAMENT; NONHUMAN; REVIEW;

EID: 0030752893     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.1997.14.419     Document Type: Review

References (118)

1. ADAMS, J.H. (1992). Head injury, in: Greenfield's Neuropathology, 5th edition. J.H. Adams and L.W. Duchen (eds), Edward Arnold: London, pp. 106-152.
2. ADAMS, J.H., DOYLE, D., FORD, I., GENNARELLI, T.A., GRAHAM, D.I., and McCLELLAN, D. (1989). Diffuse axonal injury in head injury: Definition, diagnosis and grading. Histopathology 15, 49-59.
3. ADAMS, J.H., GRAHAM, D.I., GENNARELLI, T.A., and MAXWELL, W.L. (1991). Editorial: Diffuse axonal injury in non-missile head injury. J Neurol. Neurosurg. Psychiatr. 54, 481-483.
4. BADALAMENTE, M.A., HURST, L.C., and STRACHER, A. (1986). Calcium-induced degeneration of the cytoskeleton in monkey and human peripheral nerves. J. Hand Surg. 11, 337-340.
5. BALLENTINE, J.D. (1988). Spinal cord trauma: In search of the meaning of granular axoplasm and vesicular myelin. J. Neuropathol. Exp. Neurol. 47, 77-92.
6. BASS, P.W. and BLACK, M.M. (1990). Individual microtubules in the axon consist of domains hat differ in both composition and stability. J. Cell Biol. 111, 495-509.
7. BASS, P.W., SLAUGHTER, T., BROWN, A., and BLACK, M.M. (1991). Microtubule dynamics in axon and dendrites. J. Neurosci. Res. 30, 134-153.
8. 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.
9. BENNETT, G.S., and DILULLO, C. (1985). Slow posttranslational modification of a neurofilament protein. J. Cell Biol. 100, 1799-1804.
10. BERTHOLD, C. (1982). Some aspects of the ultrastructural organization of peripheral myelinated axons in the cat, in: Axoplasmic Transport. D. Weiss (ed), Springer-Verlag: New York, pp. 40-54.
11. BLACK, M.M., KEYSER, P., and SOBEL, E. (1986). Interval between the synthesis and assembly of cytoskeletal proteins in cultured neurons. J. Neurosci. 6, 1004-1012.
12. BLAUSTEIN, M.P. (1988). Calcium transport and buffering in neurons. Trends in Neuroscience 11, 438-443.
13. 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. Lancet 344, 1055-1056.
14. BLUMBERGS, P.C., SCOTT, G., MANAVIS, J., WAINWRIGHT, H., SIMPSON, D.A., and MCLEAN, A.J. (1995). Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J. Neurotrauma 12, 565-572.
15. BORGENS, R.B., JAFFE, L.F., and COHEN, M.J. (1980). Large and persistent electrical currents enter transected lamprey spinal cord. Proc. Natl. Acad. Sci. USA 77, 1209-1213.
16. BORGERS, M., DEBRABANDER, M., VAN REEMPTS, J., AWOUTERS, F., and JACOB, W.A. (1977). Intranuclear microtubules in lung mast cells of guinea pig in anaphylactic shock. Laboratory Investigation 37, 1-7.
17. 2+-dependent proteolysis in situ. Biochem. J. 239, 191-197.
18. CAJAL, S., RAMON, Y. (1959). Degeneration and Regeneration of the Nervous System, vol. 2. R.M. May (transl and ed) Hafner, New York.
19. CHENG, C.L.Y., and POVLISHOCK, J.T. (1988). The effect of traumatic brain injury on the visual system: A morphologic characterization of reactive axonal change. J. Neurotrauma 5, 47-60.
20. 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.
21. DE WAEGH, S., and BRADY, S.T. (1990). Altered slow axonal transport and regeneration in a myelin-deficient mutant mouse: The Trembler as an in vivo model for Schwann cell-axon interactions. J. Neurosci. 10, 1855-1865.
22. DE WAEGH, S.M., 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.
23. ERB, D.E., and POVLISHOCK, J.T. (1988). Axonal damage in severe traumatic brain injury: An experimental study in cat. Acta Neuropathol. 76, 347-358.
24. GALBRAITH, J.A., THIBAULT, L.E., and MATTESON, R.A. (1993). Mechanical and electrical responses of the squid giant axon to simple elongation. J. Biomech. Eng. 115, 13-22.
25. GASKIN F., CANTON, C.R., and SHELANSKI, M.L. (1975). Biochemical studies in in vitro assembly and disassembly of microtubules. Ann N.Y. Acad. Sci. 253, 133-146.
26. GENNARELLI, T.A., THIBAULT, L.E., ADAMS, J.H., GRAHAM, D.I., THOMPSON, C.J., and MARCINCIN, R.P. (1982). Diffuse axonal injury and traumatic coma in the primate. Ann. of Neurol. 12, 564-574.
27. GENNARELLI, T.A., THIBAULT, L.E., TIPPERMAN, R., et al. (1989). Axonal injury in the optic nerve: A model simulating diffuse axonal injury in man. J. Neurosurg. 71, 244-253.
28. GENTLEMAN, S.M., NASH, M.J., SWEETING, C.J., GRAHAM, D.I., and ROBERTS, G.W. (1993). β-Amyloid precursor protein (β-APP) as a marker of axonal injury after head injury. Neurosci. Lett. 160, 139-144.
29. GENTLEMAN, S.W., 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 Neuropathologica 89, 537-543.
30. 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, 2472-2475.
31. GOTOW, T., and TANAKA, J. (1994). Phosphorylation of neurofilament H subunit as related to arrangement of neurofilaments. J. Neurosci. Res. 37, 691-713.
32. GRADY, M.S., MCLAUGHLIN, M.R., CHRISTMAN, C.W., VALADAKA, A.B., FLINGER, C.L., and POVLISHOCK, J.T. (1993). The use of antibodies against neurofilament subunits for the detection of diffuse axonal injury in humans. J. Neuropathol. Exp. Neurol. 52, 143-152.
33. A (Glycogen synthase kinase 3). J. Biol. Chem. 226, 8262-8267.
34. GULTEKIN, S.H., and SMITH, T.W. (1994). Diffuse axonal injury in craniocerebral trauma: A comparative histologic and immunohistochemical study. Arch. Pathol. Lab. Med. 118, 168-171.
35. HAGESTEDT, T., LICHTENBERG, B., WILLE, H., MANDELOE, E.-M., and MANDELKOW, E. (1989). Tau protein becomes long and stiff upon phosphorylation: Correlation between paracrystalline structure and degree of phosphorylation. J. Cell Biol. 109, 1643-1651.
36. HALL, G.F., and KOSIK, K.S. (1993). Axotomy-induced neurofilament phosphorylation is inhibited in situ by microinjection of PKA and PKC inhibitors into identified lamprey neurons. Neuron 10, 613-625.
37. HALL, G.F., and LEE, V.M.-L. (1995). Neurofilament sidearm proteolysis is a prominent early effect of axotomy in lamprey giant central neurons. J. Comp. Neurol. 353, 38-49.
38. HELLMICH, M.R., PANT, H.C., WADA, E., and BATTEY, J.F. (1992). Neuronal cdc2-like kinase: A cdc2-related protein kinase with predominantly neuronal expression. Proc. Natl. Acad. Sci. USA 89, 10867-10871.
39. HISANAGA, S., GONADA, Y., INAGAKI, M., IKAI, A., and HIROKAWA, N. (1990). Effects of phosphorylation of the neurofilament L protein on filamentous structures. Cell Reg. 1, 237-248.
40. HISANAGA, S., KUSUBATA, M., OKUMURA, E., and KISHIOMOTO, T. (1991). Phosphorylation of neurofilament H subunit at the tail domain by CDC2 kinase dissociates the association with microtubules. J. Biol. Chem. 266, 21798-21803.
41. HISANAGA, S., ISHIGURO, K., UCHIDA, T., OKUMURA, E., OKANA, T., and HIROKAWA, N. (1993). Tau protein kinase II has a similar characteristic to cdc2 kinase for phosphorylating neurofilament proteins. J. Biol. Chem. 268, 15056-15060.
42. HUFFMAN, P.N., and LASEK, R.J. (1975). The slow component of axonal transport: Identification of the major structural polypeptides of the axon and their generality among mammalian neurons. J. Cell Biol. 66, 351-366.
43. JAFARI, S.S., MAXWELL, W.L., NEILSON, M., and GRAHAM, D.I. (1997). Axonal cytoskeletal changes after non-disruptive axonal injury. J. Neurocytol. 26, 207-221.
44. 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.
45. JOHNSON, G.V.W., GREENWOOD, J.A., COSTELLO, A.C., and TRONSOSO, J.C. (1991). The regulatory role of calmodulin in the proteolysis of individual neurofilament proteins by calpain. Neurochem. Res. 16, 869-873.
46. 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.
47. LEVINE, J., and WILLARD, M. (1980). The composition and organization of axonally transported proteins in the retinal ganglion cells of the guinea pig. Brain Res. 194, 137-154.
48. MCHALE, M.K., HALL, G.F., and COHEN, M.J. (1995). Early cytoskeletal changes following injury of giant spinal axons in the lamprey. J. Comp. Neurol. 353, 25-37.
49. MCKENZIE, K.J., MCLELLAN, D.R., GENTLEMAN, S.M., MAXWELL, W.L., GENNARELLI, T.A., and GRAHAM, D.I. (1996). Is β-APP a marker of axonal damage in short-surviving head injury? Acta Neuropathol. 92, 608-613.
50. MCQUARRIE, I.G., BRADY, S., and LASEK, R.J. (1986). Diversity in the axonal transport of structural proteins: Major differences between optic and spinal axons in the rat. J. Neurosci. 6, 1593-1605.
51. 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.
52. MATA, M., STAPLE, J., and FINK, D.J. (1986). Changes in intra-axonal calcium distribution following nerve crush. J. Neurobiol. 17, 449-467.
53. 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.
54. MAXWELL, W.L. (1995). Microtubular changes in axons after stretch injury. J. Neurotrauma 12, 363.
55. MAXWELL, W.L. (1996). Histopathological changes at central nodes of Ranvier after stretch injury. Micro. Res. Tech. 34, 522-535.
56. MAXWELL, W.L., KANSAGRA, A.M., GRAHAM, D.I., ADAMS, J.H., GENNARELLI, T.A. (1983). Freeze-fracture studies of reactive myelinated nerve fibres after diffuse axonal injury. Acta Neuropathol. 76, 395-406.
57. MAXWELL, W.L., IRVINE, A., STRANG, R.H.C., GRAHAM, D.I., ADAMS, J.H., GENNARELLI, T.A. (1990). Glycogen accumulation in axons after stretch injury. J. Neurocytol. 19, 235-241.
58. MAXWELL, W.L., IRVINE, A., GRAHAM, D.I., ADAMS, J.H., GENNARELLI, T.A. (1991). Focal axonal injury: The early axonal response to stretch. J. Neurocytol. 20, 157-164.
59. 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.
60. MAXWELL, W.L., GALLAGHER, M.E., GRAHAM, D.I., and GENNARELLI, T.A. (1994a). Quantifiable alterations of the axonal cytoskeleton after stretch injury to the adult guinea pig optic nerve. Neuropathol. Appl. Neurobiol. 20, 303.
61. MAXWELL, W.L., GRAHAM, D.I., and GENNARELLI, T.A. (1994b). Observations on the axonal cytoskeleton after focal axonal injury (FAI). Brain Pathol. 4, 488.
62. MAXWELL, W.L., ISLAM, M.N., GRAHAM, D.I., and GENNARELLI, T.A. (1994c). A qualitative and quantitative analysis of the cell soma response to stretch injury in the optic nerve of the adult guinea pig. J. Neurocytol. 23, 379-392.
63. 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.
64. MAXWELL, W.L., and GRAHAM, D.I. (1997). Loss of axonal microtubules and neurofilaments after stretch-injury to guinea-pig optic nerve fibers. J. Neurotrauma (in press).
65. MAXWELL, W.L., KOSANLAVIT, R., and GRAHAM, D.I. (1997). Structural change in the internodal axolemma after stretch-injury to the guinea pig optic nerve. Neuropath. Appl. Neurobiol. 23, 165.
66. MIYASAKA, H., OKABE, S., ISHIGURO, K., UCHIDA, T., and HIROKAWA, N. (1993). Interaction of the tail domain of high molecular weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by τ protein kinase II. J. Biol. Chem. 268, 22695-22702.
67. NAKAMURA, Y., TAKEDA, M., ANGELIDES, K.D., TANAKA, T., TADA, K., and NISHIMURA, T. (1990). Effect of phosphorylation on 68kDa neurofilament subunit protein assembly by the cyclic AMP dependent protein kinase in vitro. Biochem. Biophys. Res. Comm. 169, 744-750.
68. NEWCOMB, J.K., KAMPFL, A., POSMANTUR, R.M., et al. (1997). Immunohistochemical study of calpain-mediated breakdown products to α-spectrin following controlled cortical impact injury in the rat. J. Neurotrauma 14, 369-383.
69. NG, H.K., MAHALIYANA, R.D., and POON, W.S. (1994). The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin stains. Clin. Neurol. Neurosurg. 96, 24-31.
70. NISHIDA, E., and SAKAI, H. (1977). Calcium sensitivity of the microtubule reassembly system: Difference between crude brain extracts and purified microtubule proteins. J. Biochem. (Tokyo) 82, 303-306.
71. NIXON, R. A. (1991). Axonal transport by cytoskeletal proteins, in: The Neuronal Cytoskeleton, B. Burgoyne, (ed), Wiley-Liss, Inc: New York, pp. 283-307.
72. NIXON, R.A. (1993). The regulation of neurofilament protein dynamics of phosphorylation: Clues to neurofibrillary pathobiology. Brain Pathol. 3, 29-38.
73. NIXON, R.A., BROWN, B.A., and MAROTTA, C.A. (1982). Post-translational modification of a neurofilament protein during axoplasmic transport: Implications for regional specialization of CNS axons. J. Cell Biol. 94, 150-158.
74. NIXON, R.A., BROWN, B.A., and MAROTTA, C.A. (1983). Limited proteolytic modifications of a neurofilament protein involves a proteinase activated by endogenous levels of calcium. Brain Res. 275, 384-388.
75. NIXON, R.A., QUACKENBUSH, R., and VITTO, A. (1986). Multiple calcium-activated neutral proteinases (CANP) in mouse retinal ganglion cell neurons: Specificities for endogenous neuronal substrates and comparison to purified brain CANP. J. Neurosci. 6, 1252-1263.
76. NIXON, R.A., PASKEVICH, P.A., SIHAG, R.K., and THAYER, C.Y. (1994). Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J. Cell. Biol. 126, 1031-1046.
77. OCHS, S., and JERSILD, R.A. (1990). Myelin intrusions in beaded nerve fibres. Neurosci. 36, 553-567.
78. OCHS, S., POURMAND, R., and JERSILD, R.A. (1996). Origin of beading constrictions at the axolemma: Presence in unmyelinated axons and after β,β′-iminodpropionitrile degradation of the cytoskeleton. Neurosci. 70, 1081-1096.
79. OLMSTED, J.B., and BORISY, G.G. (1975). Ionic and nucleotide requirements for microtubule polymerization in vitro. Biochemistry 14, 2996-3005.
80. 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.
81. PETTUS, E.H., and POVLISHOCK, J.T. (1994). Evidence of prolonged alterations in axolemma permeability following traumatic brain injury. J. Neurotrauma 12, 475.
82. PETTUS, E.H., and POVLISHOCK, J.T. (1996). Characterization of a distinct set of intra-axonal ultrastructural changes associated with traumatically induced alteration in axolemma permeability. Brain Res. 772, 1-11.
83. PLEASURE, S.J., SELZER, M.E., and LEE, V.M.-Y. (1989). Lamprey neurofilaments combine in one subunit the features of each mammalian neurofilament protein, but are highly phosphorylated only in large axons. J. Neurosci. 9, 698-709.
84. POVLISHOCK, J.T. (1986). Traumatically induced axonal damage without concomitant change in focally related neuronal somata and dendrites. Acta Neuropathol. 70, 53-79.
85. POVLISHOCK, J.T. (1992). Traumatically induced axonal injury: Pathogenesis and pathobiological implications. Brain Pathol. 2, 1-12.
86. POVLISHOCK, J.T., BECKER, D., CHENG, C., and VAUGHN, G. (1983). Axonal change in minor head injury. J. Neuropathol. Exp. Neurol. 42, 225-242.
87. POVLISHOCK, J.T., and KONTOS, H.A. (1985). Continuing axonal and vascular change following experimental brain trauma. Central Nerv. Syst. Trauma 2, 285-298.
88. POVLISHOCK, J.T., and CHRISTMAN, C.W. (1995a). The pathobiology of traumatically induced axonal injury in animals and humans: A review of current thoughts. J. Neurotrauma 12, 555-563.
89. POVLISHOCK, J.T., and CHRISTMAN, C.W. (1995b). Diffuse axonal injury, in: The Axon: Structure, function and pathophysiology. S.G. Waxman, J.D. Kocsis, and P.K. Stys (eds) Oxford University Press: New York, pp 504-529.
90. POVLISHOCK, J.T., GIEBEL, M.L., and PETTUS, E. (1995). Traumatically induced alterations in axolemma permeability are associated with a distinct subset of intra-axonal cytoskeletal changes. J. Neurotrauma 12, 417.
91. POVLISHOCK, J.T., and JENKINS, L.W. (1995). Are the pathobiological changes evoked by traumatic brain injury immediate and irreversible? Brain Pathol. 5, 415-426.
92. POVLISHOCK, J.T., and PETTUS, E.H. (1996). Traumatically induced axonal damage: Evidence for enduring changes in axolemma permeability with associated cytoskeletal change. Acta Neurochir. 66, 81-86.
93. POVLISHOCK, J.T., MARMAROU, A., MCINTOSH, T., TROJANOWSKI, J.Q., and MOROI, J. (1997). Impact acceleration injury in the rat: Evidence for focal axolemma change and related neurofilament sidearm alteration. J. Neuropath. Exp. Neurol. 56, 347-359.
94. 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.
95. RELES, A., and FRIEDE, R.L. (1991). Axonal cytoskeleton at the nodes of Ranvier. J. Neurocytol. 20, 450-458.
96. ROSS, D.T., GRAHAM, D.I., ADAMS, J.H., and GENNARELLI, T.A. (1992). Correlation of neurofilament immunohistochemistry with silver staining of damaged axons following head injury. Soc. Neurosci. Abstr. 18, 1088(457.9).
97. ROSS, D.T., MEANEY, D.F., SABOL, M.K., SMITH, D.H., and GENNARELLI, T.A. (1994). Distribution of forebrain diffuse axonal injury following inertial closed head injury in miniature swine. Exp. Neurol. 126, 291-299.
98. SAATMAN, K.E., BOZYCZKO-COYNE, D., MARCY, V., SIMAN, R., and MCINTOSH, T.K. (1996). Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropathol. Exp. Neurol. 55, 850-860.
99. SCARPA, A. (1976). Kinetic and thermodynamic aspects of mitochondrial calcium transport, in: Mitochondria: Bioenergetics, Biogenesis and Membrane Structure. L. Packer, A. Gomez-Puyou (eds), Academic Press: New York, pp. 31-45.
100. SCHLAEPFER, W.W. (1974). Calcium-induced degeneration of axoplasm in isolated segments of rat peripheral nerve. Brain Res. 69, 203-215.
101. SCHLAEPFER, W.W. (1977). Structural alterations of peripheral nerve induced by the calcium ionophore A23187. Brain Res. 136, 1-9.
102. SCHLAEPFER, W.W., and ZIMMERMAN, U.-J.P. (1985). Mechanisms underlying the neuronal response to ischemic injury. Calcium-activated proteolysis of neurofilaments. Prog. Brain. Res. 63, 185-196.
103. SHERRIFF, F.E., BRIDGES, L.R., GENTLEMAN, S.M., SIVALOGANATHAN, S., and WILSON, S. (1994). Markers of axonal injury in post mortem human brain. Acta Neuropathol. 88, 433-439.
104. SLOAN, K.E., STEVENSON, J.A., and BIGBEE, J.W. (1991). Qualitative and quantitative comparison of the distribution of phosphorylated and nonphosphorylated epitopes within central and peripheral axons of adult hamster. Cell Tissue Res. 263, 265-270.
105. STERNBERGER, L.A., and STERNBERGER, N.H. (1983). Monoclonal antibodies distinguish phosphorylated and non-phosphorylated forms of neurofilament in situ. Proc. Natl. Acad. Sci. USA 80, 6126-6130.
106. STRAUTMAN, A.F., CORK, R.J., and ROBINSON, K.R. (1990). The distribution of free calcium in transected spinal axons and its modulation by applied electric fields. J. Neurosci. 10, 3564-3575.
107. 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 primar sensory dorsal column tract in the rat spinal cord. J. Comp. Neurol. 302, 220-235.
108. TASHIRO, T., and KOMIYA, Y. (1991). Maturation and aging of the axonal cytoskeleton: Biochemical analysis of transported tubulin. J. Neurosci. Res. 30, 192-200.
109. TOMEI, G., SPAGNOLI, D., DUCATI, A., et al. (1990). Morphology and neurophysiology of focal axonal injury experiments induced in the guinea pig optic nerve. Acta Neuropathol. 80, 506-513.
110. WADE, C.R., OHARA, P.T., and LIEBERMAN, A.R. (1980). Calcium localization in normal and degenerating myelinated nerve fibres of the CNS. J. Anat. 130, 641-644.
111. WATSON, D.F., HOFFMAN, P.N., and GRIFFIN, J.W. (1990). The cold stability of microtubules increase during axonal maturation. J. Neurosci. 10, 3344-3352.
112. WATSON, D. (1991). Regional variation in the abundance of axonal cytoskeletal proteins. J. Neurosci. Res. 30, 226-231.
113. 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.
114. WEBSTER, H.DEF., and AMES, A. (1965). Reversible and irreversible changes in the fine structure of nervous tissue during oxygen and glucose deprivation. J. Cell Biol. 26, 885-909.
115. WEISENBERG, R. (1972). Microtubule formation in vitro in solutions containing low calcium concentrations. Science 117, 1104-1105.
116. YAGHMAI, A., and POVLISHOCK, J.T. (1992). Traumatically induced reactive change as visualized through the use of monoclonal antibodies targeted to the neurofilament subunits. J. Neuropathol. Exp. Neurol. 51, 158-176.
117. 666 in neurofilament. J. Neurochem. 64, 1848-1854.
118. YAWO, H., and KUNO, M. (1985). Calcium dependence of membrane sealing at the cut end of the cockroach giant axon. J. Neurosci. 5, 1626-1632.