SNTF immunostaining reveals previously undetected axonal pathology in traumatic brain injury

Acta Neuropathologica

Volumn 131, Issue 1, 2016, Pages 115-135

  Johnson, Victoria E ^a   Stewart, William ^a,b,c   Weber, Maura T ^a   Cullen, D Kacy ^a   Siman, Robert ^a   Smith, Douglas H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b QUEEN ELIZABETH UNIVERSITY HOSPITAL   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Amyloid precursor protein; Axonal pathology; Concussion; Diffuse axonal injury; Mild TBI; Neurofilaments; SNTF; Spectrin breakdown; TBI; Traumatic brain injury

Indexed keywords

AMYLOID PRECURSOR PROTEIN; NEUROFILAMENT H PROTEIN; NEUROFILAMENT M PROTEIN; NEUROFILAMENT PROTEIN; PROTEIN; SPECTRIN N TERMINAL FRAGMENT; UNCLASSIFIED DRUG; NEUROFILAMENT PROTEIN H;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; BRAIN TISSUE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOSKELETON; DIFFUSE AXONAL INJURY; DISEASE SEVERITY; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MINIPIG; NERVE FIBER; NERVE FIBER TRANSPORT; NEUROPATHOLOGY; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; PORCINE MODEL; PRIORITY JOURNAL; PROGNOSIS; SURVIVAL TIME; TRAUMATIC BRAIN INJURY; ANIMAL; AXON; BRAIN; BRAIN INJURIES; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONAL TRANSPORT; AXONS; BRAIN; BRAIN INJURIES; DIFFUSE AXONAL INJURY; IMMUNOHISTOCHEMISTRY; MALE; NEUROFILAMENT PROTEINS;

EID: 84952981184     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-015-1506-0     Document Type: Article

References (85)

1. Adams JH, Doyle D, Ford I, Gennarelli TA, Graham DI, McLellan DR (1989) Diffuse axonal injury in head injury: definition, diagnosis and grading. Histopathology 15:49–59
2. Adams JH, Graham DI, Gennarelli TA, Maxwell WL (1991) Diffuse axonal injury in non-missile head injury. J Neurol Neurosurg Psychiatry 54:481–483
3. Adams JH, Graham DI, Murray LS, Scott G (1982) Diffuse axonal injury due to nonmissile head injury in humans: an analysis of 45 cases. Ann Neurol 12:557–563
4. Baines AJ (2009) Evolution of spectrin function in cytoskeletal and membrane networks. Biochem Soc Trans 37:796–803
5. Bazarian JJ, Zhong J, Blyth B, Zhu T, Kavcic V, Peterson D (2007) Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study. J Neurotrauma 24:1447–1459
6. Blumbergs PC, Scott G, Manavis J, Wainwright H, Simpson DA, McLean AJ (1994) Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344:1055–1056
7. Blumbergs PC, Scott G, Manavis J, Wainwright H, Simpson DA, McLean AJ (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
8. Browne KD, Chen XH, Meaney DF, Smith DH (2011) Mild traumatic brain injury and diffuse axonal injury in swine. J Neurotrauma 28:1747–1755
9. Buki A, Farkas O, Doczi T, Povlishock JT (2003) Preinjury administration of the calpain inhibitor MDL-28170 attenuates traumatically induced axonal injury. J Neurotrauma 20:261–268
10. Buki A, Koizumi H, Povlishock JT (1999) Moderate posttraumatic hypothermia decreases early calpain-mediated proteolysis and concomitant cytoskeletal compromise in traumatic axonal injury. Exp Neurol 159:319–328
11. Buki A, Okonkwo DO, Povlishock JT (1999) Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J Neurotrauma 16:511–521
12. Buki A, Povlishock JT (2006) All roads lead to disconnection?–Traumatic axonal injury revisited. Acta Neurochir (Wien) 148:181–193 (discussion 193–184)
13. Buki A, Siman R, Trojanowski JQ, Povlishock JT (1999) The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J Neuropathol Exp Neurol 58:365–375
14. Campbell MJ, Morrison JH (1989) Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. J Comp Neurol 282:191–205
15. Christman CW, Salvant JB Jr, Walker SA, Povlishock JT (1997) Characterization of a prolonged regenerative attempt by diffusely injured axons following traumatic brain injury in adult cat: a light and electron microscopic immunocytochemical study. Acta Neuropathol 94:329–337
16. Coronado VG, McGuire LC, Sarmiento K, Bell J, Lionbarger MR, Jones CD, Geller AI, Khoury N, Xu L (2012) Trends in traumatic brain injury in the US and the public health response: 1995–2009. J Saf Res 43:299–307
17. Eierud C, Craddock RC, Fletcher S, Aulakh M, King-Casas B, Kuehl D, LaConte SM (2014) Neuroimaging after mild traumatic brain injury: review and meta-analysis. NeuroImage Clin 4:283–294
18. Faul M, Xu L, Wald MM, Coronado VG (2010) Traumatic brain injury in the United States: emergency department visits, hospitalizations, and deaths. Centers for Disease Control and Prevention, National Center for Injury Prevention and Control, Atlanta
19. Geddes JF, Vowles GH, Beer TW, Ellison DW (1997) The diagnosis of diffuse axonal injury: implications for forensic practice. Neuropathol Appl Neurobiol 23:339–347
20. Geddes JF, Whitwell HL, Graham DI (2000) Traumatic axonal injury: practical issues for diagnosis in medicolegal cases. Neuropathol Appl Neurobiol 26:105–116
21. Gennarelli TA, Thibault LE, Adams JH, Graham DI, Thompson CJ, Marcincin RP (1982) Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 12:564–574
22. Gentleman SM, Nash MJ, Sweeting CJ, Graham DI, Roberts GW (1993) Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. Neurosci Lett 160:139–144
23. Gentleman SM, Roberts GW, Gennarelli TA, Maxwell WL, Adams JH, Kerr S, Graham DI (1995) Axonal injury: a universal consequence of fatal closed head injury? Acta Neuropathol 89:537–543
24. Grady MS, McLaughlin MR, Christman CW, Valadka AB, Fligner CL, Povlishock JT (1993) The use of antibodies targeted against the neurofilament subunits for the detection of diffuse axonal injury in humans. J Neuropathol Exp Neurol 52:143–152
25. Graham DI, Adams JH, Nicoll JA, Maxwell WL, Gennarelli TA (1995) The nature, distribution and causes of traumatic brain injury. Brain Pathol 5:397–406
26. Graham DI, Gentleman SM, Lynch A, Roberts GW (1995) Distribution of beta-amyloid protein in the brain following severe head injury. Neuropathol Appl Neurobiol 21:27–34
27. Graham DI, Smith C, Reichard R, Leclercq PD, Gentleman SM (2004) Trials and tribulations of using beta-amyloid precursor protein immunohistochemistry to evaluate traumatic brain injury in adults. Forensic Sci Int 146:89–96
28. Hanell A, Greer JE, McGinn MJ, Povlishock JT (2015) Traumatic brain injury-induced axonal phenotypes react differently to treatment. Acta Neuropathol 129:317–332
29. Hayashi T, Ago K, Ago M, Ogata M (2009) Two patterns of beta-amyloid precursor protein (APP) immunoreactivity in cases of blunt head injury. Leg Med (Tokyo) 11(Suppl 1):S171–S173
30. Humphreys I, Wood RL, Phillips CJ, Macey S (2013) The costs of traumatic brain injury: a literature review. ClinicoEconomics Outcomes Res: CEOR 5:281–287
31. Hunter JV, Wilde EA, Tong KA, Holshouser BA (2012) Emerging imaging tools for use with traumatic brain injury research. J Neurotrauma 29:654–671
32. Hyder AA, Wunderlich CA, Puvanachandra P, Gururaj G, Kobusingye OC (2007) The impact of traumatic brain injuries: a global perspective. NeuroRehabilitation 22:341–353
33. Iwata A, Stys PK, Wolf JA, Chen XH, Taylor AG, Meaney DF, Smith DH (2004) Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J Neurosci 24:4605–4613
34. Johnson VE, Stewart JE, Begbie FD, Trojanowski JQ, Smith DH, Stewart W (2013) Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain 136:28–42
35. Johnson VE, Stewart W, Smith DH (2013) Axonal pathology in traumatic brain injury. Exp Neurol 246:35–43
36. Kampfl A, Posmantur R, Nixon R, Grynspan F, Zhao X, Liu SJ, Newcomb JK, Clifton GL, Hayes RL (1996) mu-Calpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J Neurochem 67:1575–1583
37. Leclercq PD, McKenzie JE, Graham DI, Gentleman SM (2001) Axonal injury is accentuated in the caudal corpus callosum of head-injured patients. J Neurotrauma 18:1–9
38. Marmarou CR, Walker SA, Davis CL, Povlishock JT (2005) Quantitative analysis of the relationship between intra- axonal neurofilament compaction and impaired axonal transport following diffuse traumatic brain injury. J Neurotrauma 22:1066–1080
39. Maxwell WL, Watt C, Pediani JD, Graham DI, Adams JH, Gennarelli TA (1991) Localisation of calcium ions and calcium-ATPase activity within myelinated nerve fibres of the adult guinea-pig optic nerve. J Anat 176:71–79
40. Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips JP, Doezema D, Reichard R, Yeo RA (2010) A prospective diffusion tensor imaging study in mild traumatic brain injury. Neurology 74:643–650
41. McCracken E, Hunter AJ, Patel S, Graham DI, Dewar D (1999) Calpain activation and cytoskeletal protein breakdown in the corpus callosum of head-injured patients. J Neurotrauma 16:749–761
42. McGinn MJ, Kelley BJ, Akinyi L, Oli MW, Liu MC, Hayes RL, Wang KK, Povlishock JT (2009) Biochemical, structural, and biomarker evidence for calpain-mediated cytoskeletal change after diffuse brain injury uncomplicated by contusion. J Neuropathol Exp Neurol 68:241–249
43. Meaney DF, Smith DH, Shreiber DI, Bain AC, Miller RT, Ross DT, Gennarelli TA (1995) Biomechanical analysis of experimental diffuse axonal injury. J Neurotrauma 12:689–694
44. Miles L, Grossman RI, Johnson G, Babb JS, Diller L, Inglese M (2008) Short-term DTI predictors of cognitive dysfunction in mild traumatic brain injury. Brain Inj 22:115–122
45. Niogi SN, Mukherjee P, Ghajar J, Johnson C, Kolster RA, Sarkar R, Lee H, Meeker M, Zimmerman RD, Manley GT et al (2008) Extent of microstructural white matter injury in postconcussive syndrome correlates with impaired cognitive reaction time: a 3T diffusion tensor imaging study of mild traumatic brain injury. AJNR Am J Neuroradiol 29:967–973
46. Okonkwo DO, Melon DE, Pellicane AJ, Mutlu LK, Rubin DG, Stone JR, Helm GA (2003) Dose-response of cyclosporin A in attenuating traumatic axonal injury in rat. NeuroReport 14:463–466
47. Okonkwo DO, Povlishock JT (1999) An intrathecal bolus of cyclosporin A before injury preserves mitochondrial integrity and attenuates axonal disruption in traumatic brain injury. J Cereb Blood Flow Metab 19:443–451
48. Pettus EH, Christman CW, Giebel ML, Povlishock JT (1994) Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change. J Neurotrauma 11:507–522
49. Pettus EH, Povlishock JT (1996) Characterization of a distinct set of intra-axonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res 722:1–11
50. Povlishock JT, Buki A, Koiziumi H, Stone J, Okonkwo DO (1999) Initiating mechanisms involved in the pathobiology of traumatically induced axonal injury and interventions targeted at blunting their progression. Acta Neurochir Suppl 73:15–20
51. Povlishock JT, Marmarou A, McIntosh T, Trojanowski JQ, Moroi J (1997) Impact acceleration injury in the rat: evidence for focal axolemmal change and related neurofilament sidearm alteration. J Neuropathol Exp Neurol 56:347–359
52. Reeves TM, Phillips LL, Povlishock JT (2005) Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp Neurol 196:126–137
53. Reichard RR, Smith C, Graham DI (2005) The significance of beta-APP immunoreactivity in forensic practice. Neuropathol Appl Neurobiol 31:304–313
54. Roberts-Lewis JM, Savage MJ, Marcy VR, Pinsker LR, Siman R (1994) Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J Neurosci: Off J Soc Neurosci 14:3934–3944
55. Ross DT, Meaney DF, Sabol MK, Smith DH, Gennarelli TA (1994) Distribution of forebrain diffuse axonal injury following inertial closed head injury in miniature swine. Exp Neurol 126:291–299
56. Saatman KE, Abai B, Grosvenor A, Vorwerk CK, Smith DH, Meaney DF (2003) Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J Cereb Blood Flow Metab 23:34–42
57. Saatman KE, Bozyczko-Coyne D, Marcy V, Siman R, McIntosh TK (1996) Prolonged calpain-mediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J Neuropathol Exp Neurol 55:850–860
58. Shahim P, Tegner Y, Wilson DH, Randall J, Skillback T, Pazooki D, Kallberg B, Blennow K, Zetterberg H (2014) Blood biomarkers for brain injury in concussed professional ice hockey players. JAMA neurol 71:684–692
59. Sherriff FE, Bridges LR, Sivaloganathan S (1994) Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol (Berl) 87:55–62
60. Shoji M, Golde TE, Ghiso J, Cheung TT, Estus S, Shaffer LM, Cai XD, McKay DM, Tintner R, Frangione B et al (1992) Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 258:126–129
61. Siman R, Flood DG, Thinakaran G, Neumar RW (2001) Endoplasmic reticulum stress-induced cysteine protease activation in cortical neurons: effect of an Alzheimer’s disease-linked presenilin-1 knock-in mutation. J Biol Chem 276:44736–44743
62. Siman R, Giovannone N, Hanten G, Wilde EA, McCauley SR, Hunter JV, Li X, Levin HS, Smith DH (2013) Evidence that the blood biomarker SNTF predicts brain imaging changes and persistent cognitive dysfunction in mild TBI patients. Frontiers in neurology 4:190
63. Siman R, McIntosh TK, Soltesz KM, Chen Z, Neumar RW, Roberts VL (2004) Proteins released from degenerating neurons are surrogate markers for acute brain damage. Neurobiol Dis 16:311–320
64. Siman R, Noszek JC, Kegerise C (1989) Calpain I activation is specifically related to excitatory amino acid induction of hippocampal damage. J Neurosci 9:1579–1590
65. Siman R, Shahim P, Tegner Y, Blennow K, Zetterberg H, Smith DH (2015) Serum SNTF increases in concussed professional ice hockey players and relates to the severity of postconcussion symptoms. J Neurotrauma (in press)
66. Siman R, Toraskar N, Dang A, McNeil E, McGarvey M, Plaum J, Maloney E, Grady MS (2009) A panel of neuron-enriched proteins as markers for traumatic brain injury in humans. J Neurotrauma 26:1867–1877
67. Siman R, Zhang C, Roberts VL, Pitts-Kiefer A, Neumar RW (2005) Novel surrogate markers for acute brain damage: cerebrospinal fluid levels corrrelate with severity of ischemic neurodegeneration in the rat. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab 25:1433–1444
68. Singleton RH, Stone JR, Okonkwo DO, Pellicane AJ, Povlishock JT (2001) The immunophilin ligand FK506 attenuates axonal injury in an impact-acceleration model of traumatic brain injury. J Neurotrauma 18:607–614
69. Smith DH, Chen XH, Xu BN, McIntosh TK, Gennarelli TA, Meaney DF (1997) Characterization of diffuse axonal pathology and selective hippocampal damage following inertial brain trauma in the pig. J Neuropathol Exp Neurol 56:822–834
70. Smith DH, Hicks R, Povlishock JT (2013) Therapy development for diffuse axonal injury. J Neurotrauma 30:307–323
71. Smith DH, Johnson VE, Stewart W (2013) Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nat Rev Neurol 9:211–221
72. Smith DH, Nonaka M, Miller R, Leoni M, Chen XH, Alsop D, Meaney DF (2000) Immediate coma following inertial brain injury dependent on axonal damage in the brainstem. J Neurosurg 93:315–322
73. Smith DH, Wolf JA, Lusardi TA, Lee VM, Meaney DF (1999) High tolerance and delayed elastic response of cultured axons to dynamic stretch injury. J Neurosci 19:4263–4269
74. Staal JA, Dickson TC, Gasperini R, Liu Y, Foa L, Vickers JC (2010) Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J Neurochem 112:1147–1155
75. Staal JA, Vickers JC (2011) Selective vulnerability of non-myelinated axons to stretch injury in an in vitro co-culture system. J Neurotrauma 28:841–847
76. Sternberger LA, Sternberger NH (1983) Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 80:6126–6130
77. Stone JR, Singleton RH, Povlishock JT (2001) Intra-axonal neurofilament compaction does not evoke local axonal swelling in all traumatically injured axons. Exp Neurol 172:320–331
78. Tang-Schomer MD, Johnson VE, Baas PW, Stewart W, Smith DH (2012) Partial interruption of axonal transport due to microtubule breakage accounts for the formation of periodic varicosities after traumatic axonal injury. Exp Neurol 233:364–372
79. Tang-Schomer MD, Patel AR, Baas PW, Smith DH (2010) Mechanical breaking of microtubules in axons during dynamic stretch injury underlies delayed elasticity, microtubule disassembly, and axon degeneration. FASEB J 24:1401–1410
80. von Reyn CR, Spaethling JM, Mesfin MN, Ma M, Neumar RW, Smith DH, Siman R, Meaney DF (2009) Calpain mediates proteolysis of the voltage-gated sodium channel alpha-subunit. J Neurosci 29:10350–10356
81. Wilde EA, McCauley SR, Hunter JV, Bigler ED, Chu Z, Wang ZJ, Hanten GR, Troyanskaya M, Yallampalli R, Li X et al (2008) Diffusion tensor imaging of acute mild traumatic brain injury in adolescents. Neurology 70:948–955
82. Wolf JA, Stys PK, Lusardi T, Meaney D, Smith DH (2001) Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels. J Neurosci 21:1923–1930
83. Yaghmai A, Povlishock J (1992) Traumatically induced reactive change as visualized through the use of monoclonal antibodies targeted to neurofilament subunits. J Neuropathol Exp Neurol 51:158–176
84. Yallampalli R, Wilde EA, Bigler ED, McCauley SR, Hanten G, Troyanskaya M, Hunter JV, Chu Z, Li X, Levin HS (2013) Acute white matter differences in the fornix following mild traumatic brain injury using diffusion tensor imaging. J Neuroimaging: Off J Am Soc Neuroimaging 23:224–227
85. Yamazaki T, Koo EH, Selkoe DJ (1997) Cell surface amyloid beta-protein precursor colocalizes with beta 1 integrins at substrate contact sites in neural cells. J Neurosci 17:1004–1010