Axonal pathology in traumatic brain injury

Experimental Neurology

Volumn 246, Issue , 2013, Pages 35-43

  Johnson, Victoria E ^a   Stewart, William ^b   Smith, Douglas H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b SOUTHERN GENERAL HOSPITAL   (United Kingdom)

Author keywords

Axon; Axonal pathology; DAI; Diffuse axonal Injury; Head injury; Microtubule; Neurodegeneration; Rotational acceleration; TBI; Traumatic brain injury

Indexed keywords

BRAIN CONCUSSION; COGNITIVE DEFECT; COMA; CONFUSION; DEGENERATIVE DISEASE; DIFFUSE AXONAL INJURY; DISEASE SEVERITY; HISTOPATHOLOGY; HUMAN; NERVE FIBER DEGENERATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TRAUMATIC BRAIN INJURY; UNCONSCIOUSNESS; WHITE MATTER;

AXON; AXONAL PATHOLOGY; DAI; DIFFUSE AXONAL INJURY; HEAD INJURY; MICROTUBULE; NEURODEGENERATION; ROTATIONAL ACCELERATION; TBI; TRAUMATIC BRAIN INJURY;

ANIMALS; AXONS; BRAIN INJURIES; COMA; DIFFUSE AXONAL INJURY; HUMANS; NERVE DEGENERATION; NERVE FIBERS, MYELINATED;

EID: 84879844434     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.01.013     Document Type: Review

References (149)

1. Adams J.H., Graham D.I., Murray L.S., Scott G. Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann. Neurol. 1982, 12:557-563.
2. Adams J.H., Doyle D., Graham D.I., Lawrence A.E., McLellan D.R. Diffuse axonal injury in head injuries caused by a fall. Lancet 1984, 2:1420-1422.
3. Adams J.H., Doyle D., Ford I., Gennarelli T.A., Graham D.I., McLellan D.R. Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 1989, 15:49-59.
4. Adams J.H., Graham D.I., Gennarelli T.A., Maxwell W.L. Diffuse axonal injury in non-missile head injury. J. Neurol. Neurosurg. Psychiatry 1991, 54:481-483.
5. Baker A.J., Phan N., Moulton R.J., Fehlings M.G., Yucel Y., Zhao M., Liu E., Tian G.F. Attenuation of the electrophysiological function of the corpus callosum after fluid percussion injury in the rat. J. Neurotrauma 2002, 19:587-599.
6. Banik N.L., Hogan E.L., Hsu C.Y. The multimolecular cascade of spinal cord injury. Studies on prostanoids, calcium, and proteinases. Neurochem. Pathol. 1987, 7:57-77.
7. Bazarian J.J., Zhong J., Blyth B., Zhu T., Kavcic V., Peterson D. Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J. Neurotrauma 2007, 24:1447-1459.
8. Bazarian J.J., Zhu T., Blyth B., Borrino A., Zhong J. Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion. Magn. Reson. Imaging 2012, 30:171-180.
9. Benz I., Beck W., Kraas W., Stoll D., Jung G., Kohlhardt M. Two types of modified cardiac Na+ channels after cytosolic interventions at the alpha-subunit capable of removing Na+ inactivation. Eur. Biophys. J. 1997, 25:189-200.
10. Blumbergs P.C., Jones N.R., North J.B. Diffuse axonal injury in head trauma. J. Neurol. Neurosurg. Psychiatry 1989, 52:838-841.
11. Blumbergs P.C., Scott G., Manavis J., Wainwright H., Simpson D.A., McLean A.J. Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J. Neurotrauma 1995, 12:565-572.
12. Bramlett H.M., Dietrich W.D. Quantitative structural changes in white and gray matter 1year following traumatic brain injury in rats. Acta Neuropathol. 2002, 103:607-614.
13. Browne K.D., Chen X.H., Meaney D.F., Smith D.H. Mild traumatic brain injury and diffuse axonal injury in swine. J. Neurotrauma 2011, 28:1747-1755.
14. Buki A., Koizumi H., Povlishock J.T. Moderate posttraumatic hypothermia decreases early calpain-mediated proteolysis and concomitant cytoskeletal compromise in traumatic axonal injury. Exp. Neurol. 1999, 159:319-328.
15. Buki A., Okonkwo D.O., Povlishock J.T. Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J. Neurotrauma 1999, 16:511-521.
16. Buki A., Siman R., Trojanowski J.Q., Povlishock J.T. The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J. Neuropathol. Exp. Neurol. 1999, 58:365-375.
17. Buki A., Farkas O., Doczi T., Povlishock J.T. Preinjury administration of the calpain inhibitor MDL-28170 attenuates traumatically induced axonal injury. J. Neurotrauma 2003, 20:261-268.
18. Cajal S.M. Degeneration and Regeneration in the Nervous System 1928, Oxford University Press, Oxford, UK.
19. Chen X.-H., Meaney D.F., Xu B.-N., Nonaka M., McIntosh T.K., Wolf J.A., Saatman K.E., Smith D.H. Evolution of neurofilament subtype accumulation in axons following diffuse brain injury in the pig. J. Neuropathol. Exp. Neurol. 1999, 58:588-596.
20. Chen X.H., Siman R., Iwata A., Meaney D.F., Trojanowski J.Q., Smith D.H. Long-term accumulation of amyloid-beta, beta-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma. Am. J. Pathol. 2004, 165:357-371.
21. Chen X.H., Johnson V.E., Uryu K., Trojanowski J.Q., Smith D.H. A lack of amyloid beta plaques despite persistent accumulation of amyloid beta in axons of long-term survivors of traumatic brain injury. Brain Pathol. 2009, 19:214-223.
22. Christman C.W., Grady M.S., Walker S.A., Holloway K.L., Povlishock J.T. Ultrastructural studies of diffuse axonal injury in humans. J. Neurotrauma 1994, 11:173-186.
23. Chung R.S., Staal J.A., McCormack G.H., Dickson T.C., Cozens M.A., Chuckowree J.A., Quilty M.C., Vickers J.C. Mild axonal stretch injury in vitro induces a progressive series of neurofilament alterations ultimately leading to delayed axotomy. J. Neurotrauma 2005, 22:1081-1091.
24. Corsellis J.A., Bruton C.J., Freeman-Browne D. The aftermath of boxing. Psychol. Med. 1973, 3:270-303.
25. Dale G.E., Leigh P.N., Luthert P., Anderton B.H., Roberts G.W. Neurofibrillary tangles in dementia pugilistica are ubiquitinated. J. Neurol. Neurosurg. Psychiatry 1991, 54:116-118.
26. DeKosky S.T., Abrahamson E.E., Ciallella J.R., Paljug W.R., Wisniewski S.R., Clark R.S., Ikonomovic M.D. Association of increased cortical soluble abeta42 levels with diffuse plaques after severe brain injury in humans. Arch. Neurol. 2007, 64:541-544.
27. Deng Y., Thompson B.M., Gao X., Hall E.D. Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp. Neurol. 2007, 205:154-165.
28. Deng-Bryant Y., Singh I.N., Carrico K.M., Hall E.D. Neuroprotective effects of tempol, a catalytic scavenger of peroxynitrite-derived free radicals, in a mouse traumatic brain injury model. J. Cereb. Blood Flow Metab. 2008, 28:1114-1126.
29. Faul M., Xu L., Wald M.M., Coronado V.G. Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths 2010, Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, Atlanta (GA).
30. Finkelstein E., Corso P., Miller T. The Incidence and Economic Burden of Injuries in the United States 2006, Oxford University Press, New York (NY).
31. Fleminger S., Oliver D.L., Lovestone S., Rabe-Hesketh S., Giora A. Head injury as a risk factor for Alzheimer's disease: the evidence 10years on; a partial replication. J. Neurol. Neurosurg. Psychiatry 2003, 74:857-862.
32. Forman M.S., Trojanowski J.Q., Lee V.M. Neurodegenerative diseases: a decade of discoveries paves the way for therapeutic breakthroughs. Nat. Med. 2004, 10:1055-1063.
33. Fujita E.P., Povlishock J.T. The combination of either tempol or FK506 with delayed hypothermia: implications for traumatically inducedmicrovascular and axonal protection. J. Neurotrauma 2011, 28:1209-1218.
34. Gale S.D., Johnson S.C., Bigler E.D., Blatter D.D. Nonspecific white matter degeneration following traumatic brain injury. J. Int. Neuropsychol. Soc. 1995, 1:17-28.
35. Geddes J.F., Vowles G.H., Nicoll J.A., Revesz T. Neuronal cytoskeletal changes are an early consequence of repetitive head injury. Acta Neuropathol. 1999, 98:171-178.
36. Gedye A., Beattie B.L., Tuokko H., Horton A., Korsarek E. Severe head injury hastens age of onset of Alzheimer's disease. J. Am. Geriatr. Soc. 1989, 37:970-973.
37. Gennarelli T.A., Thibault L.E., Adams J.H., Graham D.I., Thompson C.J., Marcincin R.P. Diffuse axonal injury and traumatic coma in the primate. Ann. Neurol. 1982, 12:564-574.
38. Gentleman S.M., Nash M.J., Sweeting C.J., Graham D.I., Roberts G.W. Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci. Lett. 1993, 160:139-144.
39. Gentleman S.M., Roberts G.W., Gennarelli T.A., Maxwell W.L., Adams J.H., Kerr S., Graham D.I. Axonal injury: a universal consequence of fatal closed head injury?. Acta Neuropathol. 1995, 89:537-543.
40. Gentleman S.M., Greenberg B.D., Savage M.J., Noori M., Newman S.J., Roberts G.W., Griffin W.S., Graham D.I. A beta 42 is the predominant form of amyloid beta-protein in the brains of short-term survivors of head injury. Neuroreport 1997, 8:1519-1522.
41. Gentleman S.M., Leclercq P.D., Moyes L., Graham D.I., Smith C., Griffin W.S., Nicoll J.A. Long-term intracerebral inflammatory response after traumatic brain injury. Forensic Sci. Int. 2004, 146:97-104.
42. Gitler D., Spira M.E. Real time imaging of calcium-induced localized proteolytic activity after axotomy and its relation to growth cone formation. Neuron 1998, 20:1123-1135.
43. Grady M.S., McLaughlin M.R., Christman C.W., Valadka A.B., Fligner C.L., Povlishock J.T. The use of antibodies targeted against the neurofilament subunits for the detection of diffuse axonal injury in humans. J. Neuropathol. Exp. Neurol. 1993, 52:143-152.
44. Graham D.I., Adams J.H., Gennarelli T.A. Mechanisms of non-penetrating head injury. Prog. Clin. Biol. Res. 1988, 234:159-168.
45. Graham D.I., Smith C., Reichard R., Leclercq P.D., Gentleman S.M. Trials and tribulations of using beta-amyloid precursor protein immunohistochemistry to evaluate traumatic brain injury in adults. Forensic Sci. Int. 2004, 146:89-96.
46. Graves A.B., White E., Koepsell T.D., Reifler B.V., van Belle G., Larson E.B., Raskind M. The association between head trauma and Alzheimer's disease. Am. J. Epidemiol. 1990, 131:491-501.
47. Gultekin S.H., Smith T.W. Diffuse axonal injury in craniocerebral trauma. A comparative histologic and immunohistochemical study. Arch. Pathol. Lab. Med. 1994, 118:168-171.
48. Guo Z., Cupples L.A., Kurz A., Auerbach S.H., Volicer L., Chui H., Green R.C., Sadovnick A.D., Duara R., DeCarli C., Johnson K., Go R.C., Growdon J.H., Haines J.L., Kukull W.A., Farrer L.A. Head injury and the risk of AD in the MIRAGE study. Neurology 2000, 54:1316-1323.
49. Guskiewicz K.M., Marshall S.W., Bailes J., McCrea M., Cantu R.C., Randolph C., Jordan B.D. Association between recurrent concussion and late-life cognitive impairment in retired professional football players. Neurosurgery 2005, 57:719-726. discussion 719-726.
50. Holbourn A.H.S. Mechanics of head injury. Lancet 1943, 242:438-441.
51. Holbourn A.H.S. Mechanics of brain injuries. Br. Med. Bull. 1945, 3:147-149.
52. Huh J.W., Franklin M.A., Widing A.G., Raghupathi R. Regionally distinct patterns of calpain activation and traumatic axonal injury following contusive brain injury in immature rats. Dev. Neurosci. 2006, 28:466-476.
53. Hunter, J.V., Wilde, E.A., Tong, K.A., Holshouser, B.A., in press. Emerging imaging tools for use with traumatic brain injury research. J. Neurotrauma.
54. Ikonomovic M.D., Uryu K., Abrahamson E.E., Ciallella J.R., Trojanowski J.Q., Lee V.M., Clark R.S., Marion D.W., Wisniewski S.R., DeKosky S.T. Alzheimer's pathology in human temporal cortex surgically excised after severe brain injury. Exp. Neurol. 2004, 190:192-203.
55. Iwata A., Stys P.K., Wolf J.A., Chen X.H., Taylor A.G., Meaney D.F., Smith D.H. Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J. Neurosci. 2004, 24:4605-4613.
56. Jafari S.S., Maxwell W.L., Neilson M., Graham D.I. Axonal cytoskeletal changes after non-disruptive axonal injury. J. Neurocytol. 1997, 26:207-221.
57. Jafari S.S., Nielson M., Graham D.I., Maxwell W.L. Axonal cytoskeletal changes after nondisruptive axonal injury. II. Intermediate sized axons. J. Neurotrauma 1998, 15:955-966.
58. Johnson V.E., Stewart W., Stewart J.E., Graham D.I., Praestgaard A.H., Smith D.H. A neprilysin polymorphism and amyloid-beta plaques following traumatic brain injury. J. Neurotrauma 2009, 8:1197-1202.
59. Johnson V.E., Stewart W., Smith D.H. Traumatic brain injury and amyloid-beta pathology: a link to Alzheimer's disease?. Nat. Rev. Neurosci. 2010, 11:361-370.
60. Johnson, V. E., Stewart, W., Smith, D.H., in press. Widespread tau and amyloid-beta pathology many years after a single traumatic brain injury in humans. Brain Pathology.
61. Kamal A., Stokin G.B., Yang Z., Xia C.H., Goldstein L.S. Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 2000, 28:449-459.
62. Kamal A., Almenar-Queralt A., LeBlanc J.F., Roberts E.A., Goldstein L.S. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 2001, 414:643-648.
63. Kampfl A., Posmantur R., Nixon R., Grynspan F., Zhao X., Liu S.J., Newcomb J.K., Clifton G.L., Hayes R.L. mu-calpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J. Neurochem. 1996, 67:1575-1583.
64. Kupina N.C., Nath R., Bernath E.E., Inoue J., Mitsuyoshi A., Yuen P.W., Wang K.K., Hall E.D. The novel calpain inhibitor SJA6017 improves functional outcome after delayed administration in a mouse model of diffuse brain injury. J. Neurotrauma 2001, 18:1229-1240.
65. Lazarov O., Morfini G.A., Lee E.B., Farah M.H., Szodorai A., DeBoer S.R., Koliatsos V.E., Kins S., Lee V.M., Wong P.C., Price D.L., Brady S.T., Sisodia S.S. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J. Neurosci. 2005, 25:2386-2395.
66. Loane D.J., Byrnes K.R. Role of microglia in neurotrauma. Neurotherapeutics 2010, 7:366-377.
67. Margulies S.S., Thibault L.E., Gennarelli T.A. Physical model simulations of brain injury in the primate. J. Biomech. 1990, 23:823-836.
68. Marklund N., Blennow K., Zetterberg H., Ronne-Engstrom E., Enblad P., Hillered L. Monitoring of brain interstitial total tau and beta amyloid proteins by microdialysis in patients with traumatic brain injury. J. Neurosurg. 2009, 110:1227-1237.
69. Marmarou C.R., Povlishock J.T. Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp. Neurol. 2006, 197:353-362.
70. Martland H. Punch drunk. J. Am. Med. Assoc. 1928, 91:1103-1107.
71. Maxwell W.L., Graham D.I. Loss of axonal microtubules and neurofilaments after stretch-injury to guinea pig optic nerve fibers. J. Neurotrauma 1997, 14:603-614.
72. Maxwell W.L., Watt C., Pediani J.D., Graham D.I., Adams J.H., Gennarelli T.A. Localisation of calcium ions and calcium-ATPase activity within myelinated nerve fibres of the adult guinea-pig optic nerve. J. Anat. 1991, 176:71-79.
73. Maxwell W.L., McCreath B.J., Graham D.I., Gennarelli T.A. 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. 1995, 24:925-942.
74. Maxwell W.L., Kosanlavit R., McCreath B.J., Reid O., Graham D.I. Freeze-fracture and cytochemical evidence for structural and functional alteration in the axolemma and myelin sheath of adult guinea pig optic nerve fibers after stretch injury. J. Neurotrauma 1999, 16:273-284.
75. Maxwell W.L., Domleo A., McColl G., Jafari S.S., Graham D.I. Post-acute alterations in the axonal cytoskeleton after traumatic axonal injury. J. Neurotrauma 2003, 20:151-168.
76. Mayer A.R., Ling J., Mannell M.V., Gasparovic C., Phillips J.P., Doezema D., Reichard R., Yeo R.A. A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 2010, 74:643-650.
77. McGinn M.J., Kelley B.J., Akinyi L., Oli M.W., Liu M.C., Hayes R.L., Wang K.K., Povlishock J.T. Biochemical, structural, and biomarker evidence for calpain-mediated cytoskeletal change after diffuse brain injury uncomplicated by contusion. J. Neuropathol. Exp. Neurol. 2009, 68:241-249.
78. McKee A.C., Cantu R.C., Nowinski C.J., Hedley-Whyte E.T., Gavett B.E., Budson A.E., Santini V.E., Lee H.S., Kubilus C.A., Stern R.A. Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury. J. Neuropathol. Exp. Neurol. 2009, 68:709-735.
79. Meaney D.F., Smith D.H., Shreiber D.I., Bain A.C., Miller R.T., Ross D.T., Gennarelli T.A. Biomechanical analysis of experimental diffuse axonal injury. J. Neurotrauma 1995, 12:689-694.
80. Meaney D.F., Smith D.H., Shreiber D.I., Bain A.C., Miller R.T., Ross D.T., Gennarelli T.A. Biomechanical analysis of experimental diffuse axonal injury. Traumatic Brain Injury: Bioscience and Mechanics 1996, 167-180. Mary Ann Liebert, Inc. F.A. Bandak, R.H. Eppinger, A.K. Ommaya (Eds.).
81. Miles L., Grossman R.I., Johnson G., Babb J.S., Diller L., Inglese M. Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj. 2008, 22:115-122.
82. Molgaard C.A., Stanford E.P., Morton D.J., Ryden L.A., Schubert K.R., Golbeck A.L. Epidemiology of head trauma and neurocognitive impairment in a multi-ethnic population. Neuroepidemiology 1990, 9:233-242.
83. Monnerie H., Tang-Schomer M.D., Iwata A., Smith D.H., Kim H.A., Le Roux P.D. Dendritic alterations after dynamic axonal stretch injury in vitro. Exp. Neurol. 2010, 224:415-423.
84. Mortimer J.A., French L.R., Hutton J.T., Schuman L.M. Head injury as a risk factor for Alzheimer's disease. Neurology 1985, 35:264-267.
85. Mortimer J.A., van Duijn C.M., Chandra V., Fratiglioni L., Graves A.B., Heyman A., Jorm A.F., Kokmen E., Kondo K., Rocca W.A., et al. Head trauma as a risk factor for Alzheimer's disease: a collaborative re-analysis of case-control studies. EURODEM Risk Factors Research Group. Int. J. Epidemiol. 1991, 20(Suppl. 2):S28-S35.
86. Mustafa A.G., Singh I.N., Wang J., Carrico K.M., Hall E.D. Mitochondrial protection after traumatic brain injury by scavenging lipid peroxyl radicals. J. Neurochem. 2010, 114:271-280.
87. Mustafa A.G., Wang J.A., Carrico K.M., Hall E.D. Pharmacological inhibition of lipid peroxidation attenuates calpain-mediated cytoskeletal degradation after traumatic brain injury. J. Neurochem. 2011, 117:579-588.
88. Nemetz P.N., Leibson C., Naessens J.M., Beard M., Kokmen E., Annegers J.F., Kurland L.T. Traumatic brain injury and time to onset of Alzheimer's disease: a population-based study. Am. J. Epidemiol. 1999, 149:32-40.
89. Nevin N.C. Neuropathological changes in the white matter following head injury. J. Neuropathol. Exp. Neurol. 1967, 26:77-84.
90. Ng H.K., Mahaliyana R.D., Poon W.S. The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin strains. Clin. Neurol. Neurosurg. 1994, 96:24-31.
91. Nicoll J.A., Roberts G.W., Graham D.I. Apolipoprotein E epsilon 4 allele is associated with deposition of amyloid beta-protein following head injury. Nat. Med. 1995, 1:135-137.
92. Okonkwo D.O., Povlishock J.T. An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J. Cereb. Blood Flow Metab. 1999, 19:443-451.
93. Omalu B.I., DeKosky S.T., Minster R.L., Kamboh M.I., Hamilton R.L., Wecht C.H. Chronic traumatic encephalopathy in a National Football League player. Neurosurgery 2005, 57:128-134. discussion 128-134.
94. Omalu B.I., DeKosky S.T., Hamilton R.L., Minster R.L., Kamboh M.I., Shakir A.M., Wecht C.H. Chronic traumatic encephalopathy in a national football league player: part II. Neurosurgery 2006, 59:1086-1092. discussion 1092-1083.
95. O'Meara E.S., Kukull W.A., Sheppard L., Bowen J.D., McCormick W.C., Teri L., Pfanschmidt M., Thompson J.D., Schellenberg G.D., Larson E.B. Head injury and risk of Alzheimer's disease by apolipoprotein E genotype. Am. J. Epidemiol. 1997, 146:373-384.
96. Ommaya A.K., Hirsch A. Tolerances for cerebral concussion from head impact and whiplash in primates. J. Biomech. 1971, 4:13-21.
97. Oppenheimer D.R. Microscopic lesions in the brain following head injury. J. Neurol. Neurosurg. Psychiatry 1968, 31:299-306.
98. Peerless S.J., Rewcastle N.B. Shear injuries of the brain. Can. Med. Assoc. J. 1967, 96:577-582.
99. Pettus E.H., Povlishock J.T. Characterization of a distinct set of intra-axonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res. 1996, 722:1-11.
100. Plassman B.L., Havlik R.J., Steffens D.C., Helms M.J., Newman T.N., Drosdick D., Phillips C., Gau B.A., Welsh-Bohmer K.A., Burke J.R., Guralnik J.M., Breitner J.C. Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias. Neurology 2000, 55:1158-1166.
101. Povlishock J.T. Traumatically induced axonal injury: pathogenesis and pathobiological implications. Brain Pathol. 1992, 2:1-12.
102. Povlishock J.T., Becker D.P. Fate of reactive axonal swellings induced by head injury. Lab. Invest. 1985, 52:540-552.
103. Povlishock J.T., Katz D.I. Update of neuropathology and neurological recovery after traumatic brain injury. J. Head Trauma Rehabil. 2005, 20:76-94.
104. Povlishock J.T., Pettus E.H. Traumatically induced axonal damage: evidence for enduring changes in axolemmal permeability with associated cytoskeletal change. Acta Neurochir. Suppl. 1996, 66:81-86.
105. Povlishock J.T., Becker D.P., Cheng C.L.Y., Vaughan G.W. Axonal change in minor head injury. J. Neuropathol. Exp. Neurol. 1983, 42:225-242.
106. Povlishock J.T., Buki A., Koiziumi H., Stone J., Okonkwo D.O. Initiating mechanisms involved in the pathobiology of traumatically induced axonal injury and interventions targeted at blunting their progression. Acta Neurochir. (Suppl.) (Wien.) 1999, 73:15-20.
107. Rand C.W., Courville C.B. Histologic changes in the brain in cases of fatal injury to the head; alterations in nerve cells. Arch. Neurol. Psychiatry 1946, 55:79-110.
108. Reeves T.M., Phillips L.L., Povlishock J.T. Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp. Neurol. 2005, 196:126-137.
109. Reeves T.M., Phillips L.L., Lee N.N., Povlishock J.T. Preferential neuroprotective effect of tacrolimus (FK506) on unmyelinated axons following traumatic brain injury. Brain Res. 2007, 1154:225-236.
110. Reichard R.R., Smith C., Graham D.I. The significance of beta-APP immunoreactivity in forensic practice. Neuropathol. Appl. Neurobiol. 2005, 31:304-313.
111. Roberts G.W., Allsop D., Bruton C. The occult aftermath of boxing. J. Neurol. Neurosurg. Psychiatry 1990, 53:373-378.
112. Roberts G.W., Gentleman S.M., Lynch A., Graham D.I. beta A4 amyloid protein deposition in brain after head trauma. Lancet 1991, 338:1422-1423.
113. Roberts G.W., Gentleman S.M., Lynch A., Murray L., Landon M., Graham D.I. Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 1994, 57:419-425.
114. Saatman K.E., Bozyczko-Coyne D., Marcy V., Siman R., McIntosh T.K. Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J. Neuropathol. Exp. Neurol. 1996, 55:850-860.
115. Saatman K.E., Murai H., Bartus R.T., Smith D.H., Hayward N.J., Perri B.R., McIntosh T.K. Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3428-3433.
116. Saatman K.E., Zhang C., Bartus R.T., McIntosh T.K. Behavioral efficacy of posttraumatic calpain inhibition is not accompanied by reduced spectrin proteolysis, cortical lesion, or apoptosis. J. Cereb. Blood Flow Metab. 2000, 20:66-73.
117. Saatman K.E., Abai B., Grosvenor A., Vorwerk C.K., Smith D.H., Meaney D.F. Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J. Cereb. Blood Flow Metab. 2003, 23:34-42.
118. Salib E., Hillier V. Head injury and the risk of Alzheimer's disease: a case control study. Int. J. Geriatr. Psychiatry 1997, 12:363-368.
119. Schofield P.W., Tang M., Marder K., Bell K., Dooneief G., Chun M., Sano M., Stern Y., Mayeux R. Alzheimer's disease after remote head injury: an incidence study. J. Neurol. Neurosurg. Psychiatry 1997, 62:119-124.
120. Shaw K., MacKinnon M.A., Raghupathi R., Saatman K.E., McLntosh T.K., Graham D.I. TUNEL-positive staining in white and grey matter after fatal head injury in man. Clin. Neuropathol. 2001, 20:106-112.
121. Sherriff F.E., Bridges L.R., Sivaloganathan S. Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol. (Berl.) 1994, 87:55-62.
122. Singleton R.H., Stone J.R., Okonkwo D.O., Pellicane A.J., Povlishock J.T. The immunophilin ligand FK506 attenuates axonal injury in an impact-acceleration model of traumatic brain injury. J. Neurotrauma 2001, 18:607-614.
123. Smith D.H., Meaney D.F. Axonal damage in traumatic brain injury. Neuroscientist 2000, 6:483-495.
124. Smith D.H., Meaney D.F., McIntosh T.K. Experimental models of traumatic brain injury. Discoveries in Head Trauma 1996, 5-25. IBC.
125. Smith D.H., Chen X.-H., Xu B.-N., McIntosh T.K., Gennarelli T.A., Meaney D.F. Characterization of diffuse axonal pathology and selective hippocampal damage following inertial brain trauma in the pig. J. Neuropathol. Exp. Neurol. 1997, 56:822-834.
126. Smith D.H., Chen X.H., Nonaka M., Trojanowski J.Q., Lee V.M., Saatman K.E., Leoni M.J., Xu B.N., Wolf J.A., Meaney D.F. Accumulation of amyloid beta and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig. J. Neuropathol. Exp. Neurol. 1999, 58:982-992.
127. Smith D.H., Wolf J.A., Lusardi T.A., Lee V.M., Meaney D.F. High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J. Neurosci. 1999, 19:4263-4269.
128. Smith D.H., Nonaka M., Miller R., Leoni M., Chen X.H., Alsop D., Meaney D.F. Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J. Neurosurg. 2000, 93:315-322.
129. Smith D.H., Chen X.H., Iwata A., Graham D.I. Amyloid beta accumulation in axons after traumatic brain injury in humans. J. Neurosurg. 2003, 98:1072-1077.
130. Smith D.H., Meaney D.F., Shull W.H. Diffuse axonal injury in head trauma. J. Head Trauma Rehabil. 2003, 18:307-316.
131. Smith D.H., Uryu K., Saatman K.E., Trojanowski J.Q., McIntosh T.K. Protein accumulation in traumatic brain injury. Neuromolecular Med. 2003, 4:59-72.
132. Staal J.A., Vickers J.C. Selective vulnerability of non-myelinated axons to stretch injury in an in vitro co-culture system. J. Neurotrauma 2011, 28:841-847.
133. Staal J.A., Dickson T.C., Chung R.S., Vickers J.C. Disruption of the ubiquitin proteasome system following axonal stretch injury accelerates progression to secondary axotomy. J. Neurotrauma 2009, 26:781-788.
134. Staal J.A., Dickson T.C., Gasperini R., Liu Y., Foa L., Vickers J.C. Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J. Neurochem. 2010, 112:1147-1155.
135. Stokin G.B., Lillo C., Falzone T.L., Brusch R.G., Rockenstein E., Mount S.L., Raman R., Davies P., Masliah E., Williams D.S., Goldstein L.S. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005, 307:1282-1288.
136. Stone J.R., Okonkwo D.O., Singleton R.H., Mutlu L.K., Helm G.A., Povlishock J.T. Caspase-3-mediated cleavage of amyloid precursor protein and formation of amyloid Beta peptide in traumatic axonal injury. J. Neurotrauma 2002, 19:601-614.
137. Strich S.J. Diffuse degeneration of the cerebral white matter in severe dementia following head injury. J. Neurol. Neurosurg. Psychiatry 1956, 19:163-185.
138. Strich S.J. Sharing of the nerve fibers as a cause of brain damage due to head injury: a pathological study of 20 cases. Lancet 1961, 278:443-448.
139. Sullivan P., Petitti D., Barbaccia J. Head trauma and age of onset of dementia of the Alzheimer type. JAMA 1987, 257:2289-2290.
140. Tang-Schomer M.D., Patel A.R., Baas P.W., Smith D.H. Mechanical breaking of microtubules in axons during dynamic stretch injury underlies delayed elasticity, microtubule disassembly, and axon degeneration. FASEB J. 2010, 24:1401-1410.
141. Tang-Schomer M.D., Johnson V.E., Baas P.W., Stewart W., Smith D.H. Partial interruption of axonal transport due tomicrotubule breakage accounts for the formation of periodic varicosities after traumatic axonal injury. Exp. Neurol. 2012, 233:364-372.
142. Thibault L.E., Gennarelli T.A., Margulies S.S., Marcus J., Eppinger R. The strain dependent pathophysiological consequences of inertial loading on central nervous system tissue. Proceedings of the International Conference on the Biomechanics of Impact, Lyon, France 1990, 191-202.
143. Tokuda T., Ikeda S., Yanagisawa N., Ihara Y., Glenner G.G. Re-examination of ex-boxers' brains using immunohistochemistry with antibodies to amyloid beta-protein and tau protein. Acta Neuropathol. (Berl.) 1991, 82:280-285.
144. Tran H.T., Laferla F.M., Holtzman D.M., Brody D.L. Controlled cortical impact traumatic brain injury in 3xTg-ADmice causes acute intra-axonal amyloid-{beta} accumulation and independently accelerates the development of tau abnormalities. J. Neurosci. 2011, 31:9513-9525.
145. Uryu K., Chen X.H., Martinez D., Browne K.D., Johnson V.E., Graham D.I., Lee V.M., Trojanowski J.Q., Smith D.H. Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Exp. Neurol. 2007, 208:185-192.
146. von Reyn C.R., Spaethling J.M., Mesfin M.N., Ma M., Neumar R.W., Smith D.H., Siman R., Meaney D.F. Calpain mediates proteolysis of the voltage-gated sodium channel alpha-subunit. J. Neurosci. 2009, 29:10350-10356.
147. Wilde E.A., McCauley S.R., Hunter J.V., Bigler E.D., Chu Z., Wang Z.J., Hanten G.R., Troyanskaya M., Yallampalli R., Li X., Chia J., Levin H.S. Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 2008, 70:948-955.
148. Wolf J.A., Stys P.K., Lusardi T., Meaney D., Smith D.H. Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J. Neurosci. 2001, 21:1923-1930.
149. Yuen T.J., Browne K.D., Iwata A., Smith D.H. Sodium channelopathy induced by mild axonal trauma worsens outcome after a repeat injury. J. Neurosci. Res. 2009, 87:3620-3625.