Repetitive head trauma, chronic traumatic encephalopathy and tau: Challenges in translating from mice to men

Experimental Neurology

Volumn 275, Issue , 2016, Pages 389-404

  Ojo, Joseph O ^a,b,d   Mouzon, Benoit C ^a,b,c,d   Crawford, Fiona ^a,b,c,d  

^a ROSKAMP INSTITUTE   (United States)

^b OPEN UNIVERSITY   (United Kingdom)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d Chronic Effects of Neurotrauma Consortium ^*  (United States)

Author keywords

Animal models; Astroglial tangles; Concussion; CTE; Neurobehaviour; Neurofibrillary tangles; Neuropathology; Repetitive TBI; Tau; Transgenic mice

Indexed keywords

AMYLOID BETA PROTEIN; LITHIUM; MINOCYCLINE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TAU PROTEIN;

CELL ACTIVATION; DIFFUSE AXONAL INJURY; DISEASE DURATION; GENETIC PREDISPOSITION; GLIOSIS; HEAD INJURY; HIPPOCAMPUS; HUMAN; LIFESTYLE MODIFICATION; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; REVIEW; SEX DIFFERENCE; SYSTEMATIC REVIEW; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURY, CHRONIC; COMPLICATION; DISEASE MODEL; METABOLISM; MOUSE; PATHOLOGY; PROCEDURES; TRANSLATIONAL RESEARCH; TRENDS;

ANIMALS; BRAIN INJURY, CHRONIC; CRANIOCEREBRAL TRAUMA; DISEASE MODELS, ANIMAL; HUMANS; MICE; TAU PROTEINS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84949726779     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.06.003     Document Type: Review

References (190)

1. Abisambra J.F., Scheff S. Brain injury in the context of tauopathies. J. Alzheimer's Dis. 2014, 40:495-518.
2. Acker C.M., Forest S.K., Zinkowski R., Davies P., d'Abramo C. Sensitive quantitative assays for tau and phospho-tau in transgenic mouse models. Neurobiol. Aging 2013, 34:338-350.
3. Ahmed Z., Cooper J., Murray T.K., Garn K., McNaughton E., Clarke H., Parhizkar S., Ward M.A., Cavallini A., Jackson S., Bose S., Clavaguera F., Tolnay M., Lavenir I., Goedert M., Hutton M.L., O'Neill M.J. A novel in vivo model of tau propagation with rapid and progressive neurofibrillary tangle pathology: the pattern of spread is determined by connectivity, not proximity. Acta Neuropathol. 2014, 127:667-683.
4. Alonso A., Zaidi T., Novak M., Grundke-Iqbal I., Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6923-6928.
5. Alonso A.D., Zaidi T., Novak M., Barra H.S., Grundke-Iqbal I., Iqbal K. Interaction of tau isoforms with Alzheimer's disease abnormally hyperphosphorylated tau and in vitro phosphorylation into the disease-like protein. J. Biol. Chem. 2001, 276:37967-37973.
6. Andorfer C., Kress Y., Espinoza M., de Silva R., Tucker K.L., Barde Y.A., Duff K., Davies P. Hyperphosphorylation and aggregation of tau in mice expressing normal human tau isoforms. J. Neurochem. 2003, 86:582-590.
7. Arun P., Abu-Taleb R., Oguntayo S., Tanaka M., Wang Y., Valiyaveettil M., Long J.B., Zhang Y., Nambiar M.P. Distinct patterns of expression of traumatic brain injury biomarkers after blast exposure: role of compromised cell membrane integrity. Neurosci. Lett. 2013, 552:87-91.
8. Bailes J.E., Petraglia A.L., Omalu B.I., Nauman E., Talavage T. Role of subconcussion in repetitive mild traumatic brain injury. J. Neurosurg. 2013, 119:1235-1245.
9. Baugh C.M., Robbins C.A., Stern R.A., McKee A.C. Current understanding of chronic traumatic encephalopathy. Curr. Treat. Options Neurol. 2014, 16:306.
10. Bazarian J.J., Zhu T., Zhong J., Janigro D., Rozen E., Roberts A., Javien H., Merchant-Borna K., Abar B., Blackman E.G. Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLoS One 2014, 9:e94734.
11. Bhaskar K., Yen S.H., Lee G. Disease-related modifications in tau affect the interaction between Fyn and Tau. J. Biol. Chem. 2005, 280:35119-35125.
12. Biagas K.V., Grundl P.D., Kochanek P.M., Schiding J.K., Nemoto E.M. Posttraumatic hyperemia in immature, mature, and aged rats: autoradiographic determination of cerebral blood flow. J. Neurotrauma 1996, 13:189-200.
13. Blennow K., Hardy J., Zetterberg H. The neuropathology and neurobiology of traumatic brain injury. Neuron 2012, 76:886-899.
14. Bolton A.N., Saatman K.E. Regional neurodegeneration and gliosis are amplified by mild traumatic brain injury repeated at 24-hour intervals. J. Neuropathol. Exp. Neurol. 2014, 73:933-947.
15. Bowman K.M., Blau A. Psychotic states following head and brain injury in adults and children 1940, 309-359. See Brock.
16. Braak H., Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging 1997, 18:351-357.
17. Braak H., Thal D.R., Ghebremedhin E., Del Tredici K. Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100years. J. Neuropathol. Exp. Neurol. 2011, 70:960-969.
18. Breedlove E.L., Robinson M., Talavage T.M., Morigaki K.E., Yoruk U., O'Keefe K., King J., Leverenz L.J., Gilger J.W., Nauman E.A. Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football. J. Biomech. 2012, 45:1265-1272.
19. Injuries of the Skull, Brain and Spinal Cord. Neuropsychiatric, Surgical, and Medico-Legal Aspects 1940, Williams & Wilkins, Baltimore, MD. S. Brock (Ed.).
20. Broglio S.P., Eckner J.T., Martini D., Sosnoff J.J., Kutcher J.S., Randolph C. Cumulative head impact burden in high school football. J. Neurotrauma 2011, 28:2069-2078.
21. Buee L., Delacourte A. Comparative biochemistry of tau in progressive supranuclear palsy, corticobasal degeneration, FTDP-17 and Pick's disease. Brain Pathol. 1999, 9:681-693.
22. Buzzini S.R., Guskiewicz K.M. Sport-related concussion in the young athlete. Curr. Opin. Pediatr. 2006, 18:376-382.
23. Cantu R.C. Chronic traumatic encephalopathy in the National Football League. Neurosurgery 2007, 61:223-225.
24. Catale C., Marique P., Closset A., Meulemans T. Attentional and executive functioning following mild traumatic brain injury in children using the Test for Attentional Performance (TAP) battery. J. Clin. Exp. Neuropsychol. 2009, 31:331-338.
25. Chen H., Richard M., Sandler D.P., Umbach D.M., Kamel F. Head injury and amyotrophic lateral sclerosis. Am. J. Epidemiol. 2007, 166:810-816.
26. Colodner K.J., Feany M.B. Glial fibrillary tangles and JAK/STAT-mediated glial and neuronal cell death in a Drosophila model of glial tauopathy. J. Neurosci. 2010, 30:16102-16113.
27. Cook R.S., Schweer L., Shebesta K.F., Hartjes K., Falcone R.A. Mild traumatic brain injury in children: just another bump on the head?. J. Trauma Nurs. 2006, 13:58-65.
28. Cook-Craig P.G., Millspaugh P.H., Recktenwald E.A., Kelly N.C., Hegge L.M., Coker A.L., Pletcher T.S. From empower to Green Dot : successful strategies and lessons learned in developing comprehensive sexual violence primary prevention programming. Violence against women 2014, 20:1162-1178.
29. Corsellis J.A., Bruton C.J., Freeman-Browne D. The aftermath of boxing. Psychol. Med. 1973, 3:270-303.
30. Crisco J.J., Fiore R., Beckwith J.G., Chu J.J., Brolinson P.G., Duma S., McAllister T.W., Duhaime A.C., Greenwald R.M. Frequency and location of head impact exposures in individual collegiate football players. J. Athl. Train. 2010, 45:549-559.
31. Critchley M. Medical aspects of boxing, particularly from a neurological standpoint. Br. Med. J. 1957, 1:357-362.
32. 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.
33. Dams-O'Connor K., Gibbons L.E., Bowen J.D., McCurry S.M., Larson E.B., Crane P.K. Risk for late-life re-injury, dementia and death among individuals with traumatic brain injury: a population-based study. J. Neurol. Neurosurg. Psychiatry 2013, 84:177-182.
34. Daneshvar D.H., Goldstein L.E., Kiernan P.T., Stein T.D., McKee A.C. Post-traumatic neurodegeneration and chronic traumatic encephalopathy. Mol. Cell. Neurosci. 2015, 66(Pt B):81-90.
35. Delacourte A., Robitaille Y., Sergeant N., Buee L., Hof P.R., Wattez A., Laroche-Cholette A., Mathieu J., Chagnon P., Gauvreau D. Specific pathological Tau protein variants characterize Pick's disease. J. Neuropathol. Exp. Neurol. 1996, 55:159-168.
36. Delacourte A., Sergeant N., Wattez A., Gauvreau D., Robitaille Y. Vulnerable neuronal subsets in Alzheimer's and Pick's disease are distinguished by their tau isoform distribution and phosphorylation. Ann. Neurol. 1998, 43:193-204.
37. Elobeid A., Soininen H., Alafuzoff I. Hyperphosphorylated tau in young and middle-aged subjects. Acta Neuropathol. 2012, 123:97-104.
38. Faden A.I., Loane D.J. Chronic neurodegeneration after traumatic brain injury: Alzheimer disease, chronic traumatic encephalopathy, or persistent neuroinflammation?. Neurotherapeutics 2015, 12:143-150.
39. Faden A.I., Wu J., Stoica B.A., Loane D.J. Progressive inflammatory-mediated neurodegeneration after traumatic brain or spinal cord injury. Br. J. Pharmacol. 2015, 10.1111/bph.13179.
40. Fay T.B., Yeates K.O., Taylor H.G., Bangert B., Dietrich A., Nuss K.E., Rusin J., Wright M. Cognitive reserve as a moderator of postconcussive symptoms in children with complicated and uncomplicated mild traumatic brain injury. J. Int. Neuropsychol. Soc. 2010, 16:94-105.
41. Field M., Collins M.W., Lovell M.R., Maroon J. Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes. J. Pediatr. 2003, 142:546-553.
42. 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.
43. Forman M.S., Lal D., Zhang B., Dabir D.V., Swanson E., Lee V.M., Trojanowski J.Q. Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration. J. Neurosci. 2005, 25:3539-3550.
44. Gabbita S.P., et al. Cleaved-tau: a biomarker of neuronal damage after traumatic brain injury. J. Neurotrauma 2005, 22(1):83-94.
45. Gama Sosa M.A., et al. Selective vulnerability of the cerebral vasculature to blast injury in a rat model of mild traumatic brain injury. Acta. Neuropathol. Commun. 2014, 2:67.
46. Gandy S., DeKosky S.T. [18F]-T807 tauopathy PET imaging in chronic traumatic encephalopathy. F1000Research 2014, 3:229.
47. Gardner A., Iverson G.L., McCrory P. Chronic traumatic encephalopathy in sport: a systematic review. Br. J. Sports Med. 2014, 48:84-90.
48. Gardner R.C., Burke J.F., Nettiksimmons J., Kaup A., Barnes D.E., Yaffe K. Dementia risk after traumatic brain injury vs nonbrain trauma: the role of age and severity. JAMA Neurol. 2014, 71:1490-1497.
49. Geddes J.F., Vowles G.H., Robinson S.F., Sutcliffe J.C. Neurofibrillary tangles, but not Alzheimer-type pathology, in a young boxer. Neuropathol. Appl. Neurobiol. 1996, 22:12-16.
50. 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.
51. 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.
52. Gelber R.P., Launer L.J., White L.R. The Honolulu-Asia Aging Study: epidemiologic and neuropathologic research on cognitive impairment. Curr. Alzheimer Res. 2012, 9:664-672.
53. Genis L., et al. Tau hyperphosphorylation in apolipoprotein E-deficient and control mice after closed head injury. J. Neurosci. Res. 2000, 60(4):559-564.
54. Gennarelli T.A., Adams J.H., Graham D.I. Acceleration induced head injury in the monkey.I. The model, its mechanical and physiological correlates. Acta Neuropathol. Suppl. 1981, 7:23-25.
55. 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.
56. Giza C.C., Hovda D.A. The neurometabolic cascade of concussion. J. Athl. Train. 2001, 36:228-235.
57. Giza C.C., Griesbach G.S., Hovda D.A. Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain. Behav. Brain Res. 2005, 157:11-22.
58. Goedert M., Jakes R. Expression of separate isoforms of human tau protein: correlation with the tau pattern in brain and effects on tubulin polymerization. EMBO J. 1990, 9:4225-4230.
59. Goedert M., Spillantini M.G., Jakes R., Rutherford D., Crowther R.A. Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 1989, 3:519-526.
60. Goedert M., Spillantini M.G., Cairns N.J., Crowther R.A. Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 1992, 8:159-168.
61. Goldstein L.E., Fisher A.M., Tagge C.A., Zhang X.L., Velisek L., Sullivan J.A., Upreti C., Kracht J.M., Ericsson M., Wojnarowicz M.W., Goletiani C.J., Maglakelidze G.M., Casey N., Moncaster J.A., Minaeva O., Moir R.D., Nowinski C.J., Stern R.A., Cantu R.C., Geiling J., Blusztajn J.K., Wolozin B.L., Ikezu T., Stein T.D., Budson A.E., Kowall N.W., Chargin D., Sharon A., Saman S., Hall G.F., Moss W.C., Cleveland R.O., Tanzi R.E., Stanton P.K., McKee A.C. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 2012, 4:134ra160.
62. Goldstein L.E., McKee A.C., Stanton P.K. Considerations for animal models of blast-related traumatic brain injury and chronic traumatic encephalopathy. Alzheimers Res. Ther. 2014, 6:64.
63. Gotz J., Tolnay M., Barmettler R., Chen F., Probst A., Nitsch R.M. Oligodendroglial tau filament formation in transgenic mice expressing G272V tau. Eur. J. Neurosci. 2001, 13:2131-2140.
64. Graves A.B., White E., Koepsell T.D., Reifler B.V., van Belle G., Larson E.B. The association between aluminum-containing products and Alzheimer's disease. J. Clin. Epidemiol. 1990, 43:35-44.
65. 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.
66. 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.
67. 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).
68. Hanes J., Zilka N., Bartkova M., Caletkova M., Dobrota D., Novak M. Rat tau proteome consists of six tau isoforms: implication for animal models of human tauopathies. J. Neurochem. 2009, 108:1167-1176.
69. Hazrati L.N., Tartaglia M.C., Diamandis P., Davis K.D., Green R.E., Wennberg R., Wong J.C., Ezerins L., Tator C.H. Absence of chronic traumatic encephalopathy in retired football players with multiple concussions and neurological symptomatology. Front. Hum. Neurosci. 2013, 7:222.
70. Hawkins B.E., et al. Rapid accumulation of endogenous tau oligomers in a rat model of traumatic brain injury: possible link between traumatic brain injury and sporadic tauopathies. J. Biol. Chem. 2013, 288(23):17042-17050.
71. Higuchi M., Ishihara T., Zhang B., Hong M., Andreadis A., Trojanowski J., Lee V.M. Transgenic mouse model of tauopathies with glial pathology and nervous system degeneration. Neuron 2002, 35:433-446.
72. Hof P.R., Bouras C., Buee L., Delacourte A., Perl D.P., Morrison J.H. Differential distribution of neurofibrillary tangles in the cerebral cortex of dementia pugilistica and Alzheimer's disease cases. Acta Neuropathol. 1992, 85:23-30.
73. Hoshino S., et al. Emergence of immunoreactivities for phosphorylated tau and amyloid-beta protein in chronic stage of fluid percussion injury in rat brain. Neurol. Rep. 1998, 9(8):1879-1883.
74. Huber B.R., Meabon J.S., Martin T.J., Mourad P.D., Bennett R., Kraemer B.C., Cernak I., Petrie E.C., Emery M.J., Swenson E.R., Mayer C., Mehic E., Peskind E.R., Cook D.G. Blast exposure causes early and persistent aberrant phospho- and cleaved-tau expression in a murine model of mild blast-induced traumatic brain injury. J. Alzheimer's Dis. 2013, 37:309-323.
75. Huh J.W., Widing A.G., Raghupathi R. Basic science; repetitive mild non-contusive brain trauma in immature rats exacerbates traumatic axonal injury and axonal calpain activation: a preliminary report. J. Neurotrauma 2007, 24:15-27.
76. Huh J.W., Widing A.G., Raghupathi R. Midline brain injury in the immature rat induces sustained cognitive deficits, bihemispheric axonal injury and neurodegeneration. Exp. Neurol. 2008, 213:84-92.
77. Hutton M., Lendon C.L., Rizzu P., Baker M., Froelich S., Houlden H., Pickering-Brown S., Chakraverty S., Isaacs A., Grover A., Hackett J., Adamson J., Lincoln S., Dickson D., Davies P., Petersen R.C., Stevens M., de Graaff E., Wauters E., van Baren J., Hillebrand M., Joosse M., Kwon J.M., Nowotny P., Che L.K., Norton J., Morris J.C., Reed L.A., Trojanowski J., Basun H., Lannfelt L., Neystat M., Fahn S., Dark F., Tannenberg T., Dodd P.R., Hayward N., Kwok J.B., Schofield P.R., Andreadis A., Snowden J., Craufurd D., Neary D., Owen F., Oostra B.A., Hardy J., Goate A., van Swieten J., Mann D., Lynch T., Heutink P. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 1998, 393:702-705.
78. Hyman B.T., Trojanowski J.Q. Consensus recommendations for the postmortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. J. Neuropathol. Exp. Neurol. 1997, 56:1095-1097.
79. 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.
80. Iliff J.J., et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J. Neurosci. 2014, 34(49):16180-16193.
81. Iqbal K., Liu F., Gong C.X., Alonso Adel C., Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol. 2009, 118:53-69.
82. Ishihara T., Hong M., Zhang B., Nakagawa Y., Lee M.K., Trojanowski J.Q., Lee V.M. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 1999, 24:751-762.
83. Ishihara T., Zhang B., Higuchi M., Yoshiyama Y., Trojanowski J.Q., Lee V.M. Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am. J. Pathol. 2001, 158:555-562.
84. Jeganathan S., von Bergen M., Brutlach H., Steinhoff H.J., Mandelkow E. Global hairpin folding of tau in solution. Biochemistry 2006, 45:2283-2293.
85. Jeganathan S., Hascher A., Chinnathambi S., Biernat J., Mandelkow E.M., Mandelkow E. Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of Tau and generates a pathological (MC-1) conformation. J. Biol. Chem. 2008, 283:32066-32076.
86. Johnson V.E., Stewart W. Traumatic brain injury: age at injury influences dementia risk after TBI. Nat. Rev. Neurol. 2015, 11(3):128-130.
87. Johnson V.E., Stewart W., Smith D.H. Traumatic brain injury and amyloid-beta pathology: a link to Alzheimer's disease? Nature reviews. Neuroscience 2010, 11:361-370.
88. Jordan B.D. Chronic traumatic brain injury associated with boxing. Semin. Neurol. 2000, 20:179-185.
89. Jordan B.D. The clinical spectrum of sport-related traumatic brain injury. Nat. Rev. Neurol. 2013, 9:222-230.
90. Jordan B.D., Jahre C., Hauser W.A., Zimmerman R.D., Zarrelli M., Lipsitz E.C., Johnson V., Warren R.F., Tsairis P., Folk F.S. CT of 338 active professional boxers. Radiology 1992, 185:509-512.
91. Jordan B.D., Matser E.J., Zimmerman R.D., Zazula T. Sparring and cognitive function in professional boxers. Phys. Sportsmed. 1996, 24:87-98.
92. Kanaan N.M., Morfini G.A., LaPointe N.E., Pigino G.F., Patterson K.R., Song Y., Andreadis A., Fu Y., Brady S.T., Binder L.I. Pathogenic forms of tau inhibit kinesin-dependent axonal transport through a mechanism involving activation of axonal phosphotransferases. J. Neurosci. 2011, 31:9858-9868.
93. Kanaan N.M., Morfini G., Pigino G., LaPointe N.E., Andreadis A., Song Y., Leitman E., Binder L.I., Brady S.T. Phosphorylation in the amino terminus of tau prevents inhibition of anterograde axonal transport. Neurobiol. Aging 2012, 33(826):e815-e830.
94. Kane M.J., Angoa-Perez M., Briggs D.I., Viano D.C., Kreipke C.W., Kuhn D.M. A mouse model of human repetitive mild traumatic brain injury. J. Neurosci. Methods 2012, 203:41-49.
95. Karlin A.M. Concussion in the pediatric and adolescent population: "different population, different concerns". PM R 2011, 3:S369-S379.
96. Kieslich M., Fiedler A., Heller C., Kreuz W., Jacobi G. Minor head injury as cause and co-factor in the aetiology of stroke in childhood: a report of eight cases. J. Neurol. Neurosurg. Psychiatry 2002, 73:13-16.
97. Koerte I.K., Ertl-Wagner B., Reiser M., Zafonte R., Shenton M.E. White matter integrity in the brains of professional soccer players without a symptomatic concussion. JAMA 2012, 308:1859-1861.
98. Kokjohn T.A., Maarouf C.L., Daugs I.D., Hunter J.M., Whiteside C.M., Malek-Ahmadi M., Rodriguez E., Kalback W., Jacobson S.A., Sabbagh M.N., Beach T.G., Roher A.E. Neurochemical profile of dementia pugilistica. J. Neurotrauma 2013, 30:981-997.
99. Kovesdi E., et al. The effect of enriched environment on the outcome of traumatic brain injury; a behavioral, proteomics, and histological study. Front. Neurosci. 2011, 5:42.
100. Kovesdi E., et al. Acute minocycline treatment mitigates the symptoms of mild blast-induced traumatic brain injury. Front. Neurol. 2012, 3:111.
101. Lasagna-Reeves C.A., Castillo-Carranza D.L., Sengupta U., Clos A.L., Jackson G.R., Kayed R. Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice. Mol. Neurodegener. 2011, 6:39.
102. Lehman E.J., Hein M.J., Baron S.L., Gersic C.M. Neurodegenerative causes of death among retired National Football League players. Neurology 2012, 79:1970-1974.
103. Liliang P.C., et al. Relationship between injury severity and serum tau protein levels in traumatic brain injured rats. Resuscitation 2010, 81(9):1205-1208.
104. Lin W.L., Lewis J., Yen S.H., Hutton M., Dickson D.W. Filamentous tau in oligodendrocytes and astrocytes of transgenic mice expressing the human tau isoform with the P301L mutation. Am. J. Pathol. 2003, 162:213-218.
105. Loosemore M., Knowles C.H., Whyte G.P. Amateur boxing and risk of chronic traumatic brain injury: systematic review of observational studies. BMJ 2007, 335:809.
106. LoPresti P., Szuchet S., Papasozomenos S.C., Zinkowski R.P., Binder L.I. Functional implications for the microtubule-associated protein tau: localization in oligodendrocytes. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:10369-10373.
107. Luo J., Nguyen A., Villeda S., Zhang H., Ding Z., Lindsey D., Bieri G., Castellano J.M., Beaupre G.S., Wyss-Coray T. Long-term cognitive impairments and pathological alterations in a mouse model of repetitive mild traumatic brain injury. Front. Neurol. 2014, 5:12.
108. Mannix R., Meehan W.P., Mandeville J., Grant P.E., Gray T., Berglass J., Zhang J., Bryant J., Rezaie S., Chung J.Y., Peters N.V., Lee C., Tien L.W., Kaplan D.L., Feany M., Whalen M. Clinical correlates in an experimental model of repetitive mild brain injury. Ann. Neurol. 2013, 74:65-75.
109. Martland H. Punch drunk. JAMA 1928, 91:1103-1107.
110. Mawdsley C., Ferguson F.R. Neurological disease in boxers. Lancet 1963, 2:795-801.
111. McCrory P., Meeuwisse W.H., Kutcher J.S., Jordan B.D., Gardner A. What is the evidence for chronic concussion-related changes in retired athletes: behavioural, pathological and clinical outcomes?. Br. J. Sports Med. 2013, 47:327-330.
112. 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.
113. McKee A.C., Gavett B.E., Stern R.A., Nowinski C.J., Cantu R.C., Kowall N.W., Perl D.P., Hedley-Whyte E.T., Price B., Sullivan C., Morin P., Lee H.S., Kubilus C.A., Daneshvar D.H., Wulff M., Budson A.E. TDP-43 proteinopathy and motor neuron disease in chronic traumatic encephalopathy. J. Neuropathol. Exp. Neurol. 2010, 69:918-929.
114. McKee A.C., Stern R.A., Nowinski C.J., Stein T.D., Alvarez V.E., Daneshvar D.H., Lee H.S., Wojtowicz S.M., Hall G., Baugh C.M., Riley D.O., Kubilus C.A., Cormier K.A., Jacobs M.A., Martin B.R., Abraham C.R., Ikezu T., Reichard R.R., Wolozin B.L., Budson A.E., Goldstein L.E., Kowall N.W., Cantu R.C. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013, 136:43-64.
115. McKee A.C., Daneshvar D.H., Alvarez V.E., Stein T.D. The neuropathology of sport. Acta Neuropathol. 2014, 127:29-51.
116. McKee A.C., Stein T.D., Kiernan P.T., Alvarez V.E. The neuropathology of chronic traumatic encephalopathy. Brain Pathol. 2015, 25:350-364.
117. McKenzie J.E., Roberts G.W., Royston M.C. Comparative investigation of neurofibrillary damage in the temporal lobe in Alzheimer's disease, Down's syndrome and dementia pugilistica. Neurodegeneration 1996, 5:259-264.
118. McMillan P., Korvatska E., Poorkaj P., Evstafjeva Z., Robinson L., Greenup L., Leverenz J., Schellenberg G.D., D'Souza I. Tau isoform regulation is region- and cell-specific in mouse brain. J. Comp. Neurol. 2008, 511:788-803.
119. Miller H. Mental after-effects of head injury. Proc. R. Soc. Med. 1966, 59:257-261.
120. Millspaugh J.A. Dementia pugilistica. US Naval Med. Bull. 1937, 35:297-303.
121. 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.
122. Montenigro P.H., Baugh C.M., Daneshvar D.H., Mez J., Budson A.E., Au R., Katz D.I., Cantu R.C., Stern R.A. Clinical subtypes of chronic traumatic encephalopathy: literature review and proposed research diagnostic criteria for traumatic encephalopathy syndrome. Alzheimers Res. Ther. 2014, 6:68.
123. Montenigro P.H., Corp D.T., Stein T.D., Cantu R.C., Stern R.A. Chronic traumatic encephalopathy: historical origins and current perspective. Annu. Rev. Clin. Psychol. 2015, 11:309-330.
124. Morris M., Maeda S., Vossel K., Mucke L. The many faces of tau. Neuron 2011, 70:410-426.
125. 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.
126. 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.
127. Mouzon B., Chaytow H., Crynen G., Bachmeier C., Stewart J., Mullan M., Stewart W., Crawford F. Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes. J. Neurotrauma 2012, 29:2761-2773.
128. Mouzon B.C., Bachmeier C., Ferro A., Ojo J.O., Crynen G., Acker C.M., Davies P., Mullan M., Stewart W., Crawford F. Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model. Ann. Neurol. 2014, 75:241-254.
129. Mychasiuk R., Hehar H., van Waes L., Esser M.J. Diet, age, and prior injury status differentially alter behavioral outcomes following concussion in rats. Neurobiol. Dis. 2015, 73:1-11.
130. Namjoshi D.R., Cheng W.H., McInnes K.A., Martens K.M., Carr M., Wilkinson A., Fan J., Robert J., Hayat A., Cripton P.A., Wellington C.L. Merging pathology with biomechanics using CHIMERA (Closed-Head Impact Model of Engineered Rotational Acceleration): a novel, surgery-free model of traumatic brain injury. Mol. Neurodegener. 2014, 9:55.
131. 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.
132. Nordstrom P., Michaelsson K., Gustafson Y., Nordstrom A. Traumatic brain injury and young onset dementia: a nationwide cohort study. Ann. Neurol. 2014, 75:374-381.
133. Ojo J.O., Mouzon B., Greenberg M.B., Bachmeier C., Mullan M., Crawford F. Repetitive mild traumatic brain injury augments tau pathology and glial activation in aged hTau mice. J. Neuropathol. Exp. Neurol. 2013, 72:137-151.
134. 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).
135. 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).
136. Omalu B.I., Fitzsimmons R.P., Hammers J., Bailes J. Chronic traumatic encephalopathy in a professional American wrestler. J. Forensic Nurs. 2010, 6:130-136.
137. Omalu B.I., Hamilton R.L., Kamboh M.I., DeKosky S.T., Bailes J. Chronic traumatic encephalopathy (CTE) in a National Football League Player: case report and emerging medicolegal practice questions. J. Forensic Nurs. 2010, 6:40-46.
138. Omalu B., Bailes J., Hamilton R.L., Kamboh M.I., Hammers J., Case M., Fitzsimmons R. Emerging histomorphologic phenotypes of chronic traumatic encephalopathy in American athletes. Neurosurgery 2011, 69:173-183. (discussion 183).
139. Omalu B., Hammers J.L., Bailes J., Hamilton R.L., Kamboh M.I., Webster G., Fitzsimmons R.P. Chronic traumatic encephalopathy in an Iraqi war veteran with posttraumatic stress disorder who committed suicide. Neurosurg. Focus. 2011, 31:E3.
140. Ommaya A.K., Goldsmith W., Thibault L. Biomechanics and neuropathology of adult and paediatric head injury. Br. J. Neurosurg. 2002, 16:220-242.
141. Osnato M. The role of trauma in various neuropsychiatric conditions. Am. J. Psychiatry 1929, 86:643-660.
142. Osnato M., Giliberti V. Postconcussion neurosis-traumatic encephalitis: a conception of postconcussion phenomena. Arch. Neurol. Psychiatry 1927, 18:181-214.
143. Perez-Polo J.R., et al. A rodent model of mild traumatic brain blast injury. J. Neurosci. Res. 2015, 93(4):549-561.
144. Petraglia A.L., Plog B.A., Dayawansa S., Chen M., Dashnaw M.L., Czerniecka K., Walker C.T., Viterise T., Hyrien O., Iliff J.J., Deane R., Nedergaard M., Huang J.H. The spectrum of neurobehavioral sequelae after repetitive mild traumatic brain injury: a novel mouse model of chronic traumatic encephalopathy. J. Neurotrauma 2014, 31:1211-1224.
145. Petraglia A.L., Plog B.A., Dayawansa S., Dashnaw M.L., Czerniecka K., Walker C.T., Chen M., Hyrien O., Iliff J.J., Deane R., Huang J.H., Nedergaard M. The pathophysiology underlying repetitive mild traumatic brain injury in a novel mouse model of chronic traumatic encephalopathy. Surg. Neurol. Int. 2014, 5:184.
146. 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.
147. Polydoro M., Acker C.M., Duff K., Castillo P.E., Davies P. Age-dependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology. J. Neurosci. 2009, 29:10741-10749.
148. Poorkaj P., Bird T.D., Wijsman E., Nemens E., Garruto R.M., Anderson L., Andreadis A., Wiederholt W.C., Raskind M., Schellenberg G.D. Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann. Neurol. 1998, 43:815-825.
149. Prins M.L., Hales A., Reger M., Giza C.C., Hovda D.A. Repeat traumatic brain injury in the juvenile rat is associated with increased axonal injury and cognitive impairments. Dev. Neurosci. 2010, 32:510-518.
150. Reddy C.C., Collins M.W., Gioia G.A. Adolescent sports concussion. Phys. Med. Rehabil. Clin. N. Am. 2008, 19:247-269. (viii).
151. Roberts A.H. Brain Damage in Boxers 1969, Pitman Publishing.
152. Roberts G.W. Immunocytochemistry of neurofibrillary tangles in dementia pugilistica and Alzheimer's disease: evidence for common genesis. Lancet 1988, 2:1456-1458.
153. Roberts G.W., Allsop D., Bruton C. The occult aftermath of boxing. J. Neurol. Neurosurg. Psychiatry 1990, 53:373-378.
154. 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.
155. 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.
156. Ross D.T., Meaney D.F., Sabol M.K., Smith D.H., Gennarelli T.A. Distribution of forebrain diffuse axonal injury following inertial closed head injury in miniature swine. Exp. Neurol. 1994, 126:291-299.
157. Rovelet-Lecrux A., Lecourtois M., Thomas-Anterion C., Le Ber I., Brice A., Frebourg T., Hannequin D., Campion D. Partial deletion of the MAPT gene: a novel mechanism of FTDP-17. Hum. Mutat. 2009, 30:E591-E602.
158. Saing T., Dick M., Nelson P.T., Kim R.C., Cribbs D.H., Head E. Frontal cortex neuropathology in dementia pugilistica. J. Neurotrauma 2012, 29:1054-1070.
159. 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.
160. Schmidt M.L., Zhukareva V., Newell K.L., Lee V.M., Trojanowski J.Q. Tau isoform profile and phosphorylation state in dementia pugilistica recapitulate Alzheimer's disease. Acta Neuropathol. 2001, 101:518-524.
161. Schmidt S., Kwee L.C., Allen K.D., Oddone E.Z. Association of ALS with head injury, cigarette smoking and APOE genotypes. J. Neurol. Sci. 2010, 291:22-29.
162. 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.
163. Schultz C., Dehghani F., Hubbard G.B., Thal D.R., Struckhoff G., Braak E., Braak H. Filamentous tau pathology in nerve cells, astrocytes, and oligodendrocytes of aged baboons. J. Neuropathol. Exp. Neurol. 2000, 59:39-52.
164. Schultz C., Hubbard G.B., Rub U., Braak E., Braak H. Age-related progression of tau pathology in brains of baboons. Neurobiol. Aging 2000, 21:905-912.
165. Schultz C., Ghebremedhin E., Del Tredici K., Rub U., Braak H. High prevalence of thorn-shaped astrocytes in the aged human medial temporal lobe. Neurobiol. Aging 2004, 25:397-405.
166. Shin R.W., Iwaki T., Kitamoto T., Tateishi J. Hydrated autoclave pretreatment enhances tau immunoreactivity in formalin-fixed normal and Alzheimer's disease brain tissues. Lab. Invest. 1991, 64:693-702.
167. 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.
168. 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.
169. Smith D.H., Johnson V.E., Stewart W. Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nature reviews. Neurology 2013, 9:211-221.
170. Snowdon D.A. Aging and Alzheimer's disease: lessons from the Nun Study. The Gerontologist 1997, 37:150-156.
171. Snowdon D.A., Nun S. Healthy aging and dementia: findings from the Nun Study. Ann. Intern. Med. 2003, 139:450-454.
172. Spillane J.D. Five boxers. Br. Med. J. 1962, 2:1205-1210.
173. Spillantini M.G., Murrell J.R., Goedert M., Farlow M.R., Klug A., Ghetti B. Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7737-7741.
174. Stamm J.M., Bourlas A.P., Baugh C.M., Fritts N.G., Daneshvar D.H., Martin B.M., McClean M.D., Tripodis Y., Stern R.A. Age of first exposure to football and later-life cognitive impairment in former NFL players. Neurology 2015, 84(11):1114-1120.
175. Stein T.D., Montenigro P.H., Alvarez V.E., Xia W., Crary J.F., Tripodis Y., Daneshvar D.H., Mez J., Solomon T., Meng G., Kubilus C.A., Cormier K.A., Meng S., Babcock K., Kiernan P., Murphy L., Nowinski C.J., Martin B., Dixon D., Stern R.A., Cantu R.C., Kowall N.W., McKee A.C. Beta-amyloid deposition in chronic traumatic encephalopathy. Acta Neuropathol. 2015, 10.1007/s00401-015-1435-y.
176. Sullivan P., Petitti D., Barbaccia J. Head trauma and age of onset of dementia of the Alzheimer type. JAMA 1987, 257:2289-2290.
177. Talavage T.M., Nauman E.A., Breedlove E.L., Yoruk U., Dye A.E., Morigaki K.E., Feuer H., Leverenz L.J. Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J. Neurotrauma 2014, 31:327-338.
178. 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. 1991, 82:280-285.
179. Tran H.T., LaFerla F.M., Holtzman D.M., Brody D.L. Controlled cortical impact traumatic brain injury in 3xTg-AD mice causes acute intra-axonal amyloid-beta accumulation and independently accelerates the development of tau abnormalities. J. Neurosci. 2011, 31:9513-9525.
180. Tran H.T., Sanchez L., Esparza T.J., Brody D.L. Distinct temporal and anatomical distributions of amyloid-beta and tau abnormalities following controlled cortical impact in transgenic mice. PLoS One 2011, 6:e25475.
181. Tran H.T., Sanchez L., Brody D.L. Inhibition of JNK by a peptide inhibitor reduces traumatic brain injury-induced tauopathy in transgenic mice. J. Neuropathol. Exp. Neurol. 2012, 71:116-129.
182. Tzekov R., Quezada A., Gautier M., Biggins D., Frances C., Mouzon B., Jamison J., Mullan M., Crawford F. Repetitive mild traumatic brain injury causes optic nerve and retinal damage in a mouse model. J. Neuropathol. Exp. Neurol. 2014, 73:345-361.
183. Victoroff J. Traumatic encephalopathy: review and provisional research diagnostic criteria. NeuroRehabilitation 2013, 32:211-224.
184. Ward S.M., Himmelstein D.S., Lancia J.K., Binder L.I. Tau oligomers and tau toxicity in neurodegenerative disease. Biochem. Soc. Trans. 2012, 40:667-671.
185. Ward S.M., Himmelstein D.S., Lancia J.K., Fu Y., Patterson K.R., Binder L.I. TOC1: characterization of a selective oligomeric tau antibody. J. Alzheimer's Dis. 2013, 37:593-602.
186. White L. Brain lesions at autopsy in older Japanese-American men as related to cognitive impairment and dementia in the final years of life: a summary report from the Honolulu-Asia aging study. J. Alzheimer's Dis. 2009, 18:713-725.
187. Xu L., Nguyen J.V., Lehar M., Menon A., Rha E., Arena J., Ryu J., Marsh-Armstrong N., Marmarou C.R., Koliatsos V.E. Repetitive mild traumatic brain injury with impact acceleration in the mouse: multifocal axonopathy, neuroinflammation, and neurodegeneration in the visual system. Exp. Neurol. 2014, 10.1016/j.expneurol.2014.11.004.
188. Yoshiyama Y., Uryu K., Higuchi M., Longhi L., Hoover R., Fujimoto S., McIntosh T., Lee V.M., Trojanowski J.Q. Enhanced neurofibrillary tangle formation, cerebral atrophy, and cognitive deficits induced by repetitive mild brain injury in a transgenic tauopathy mouse model. J. Neurotrauma 2005, 22:1134-1141.
189. Yu F., et al. Lithium reduces BACE1 overexpression, beta amyloid accumulation, and spatial learning deficits in mice with traumatic brain injury. J. Neurotrauma 2012, 29(13):2342-2351.
190. Zhang J., Teng Z., Song Y., Hu M., Chen C. Inhibition of monoacylglycerol lipase prevents chronic traumatic encephalopathy-like neuropathology in a mouse model of repetitive mild closed head injury. J. Cereb. Blood Flow Metab. 2015, 35:443-453.