Experimental traumatic brain injury induces rapid aggregation and oligomerization of amyloid-beta in an Alzheimer's disease mouse model

Journal of Neurotrauma

Volumn 31, Issue 1, 2014, Pages 125-134

  Washington, Patricia M ^a   Morffy, Nicholas ^a   Parsadanian, Maia ^a   Zapple, David N ^a   Burns, Mark P ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

adult brain injury; axonal injury; beta amyloid

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; BIOCHEMISTRY; BRAIN CORTEX; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTERNAL CAPSULE; HIPPOCAMPAL FIMBRIA; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IPSILATERAL CORTEX; MALE; MOLECULAR WEIGHT; MOUSE; MOUSE MODEL; NERVE FIBER; NONHUMAN; OLIGOMERIZATION; PROTEIN AGGREGATION; PROTEIN PROCESSING; SHAM PROCEDURE; TISSUE HOMOGENATE; TRANSGENIC MOUSE; TRAUMATIC BRAIN INJURY; WESTERN BLOTTING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; BRAIN INJURIES; DISEASE MODELS, ANIMAL; MICE; MICE, TRANSGENIC;

EID: 84892705258     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2013.3017     Document Type: Article

References (60)

1. 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., Shalat, S.L., Soininen, H., and Hofman, A. (1991). 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. 20, Suppl. 2, S28-S35.
2. 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., and Breitner, J.C. (2000). Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias. Neurology 55, 1158-1166.
3. Schofield, P.W., Tang, M., Marder, K., Bell, K., Dooneief, G., Chun, M., Sano, M., Stern, Y., and Mayeux, R. (1997). Alzheimer's disease after remote head injury: an incidence study. J. Neurol. Neurosurg. Psychiatry 62, 119-124.
4. Chen, X.H., Siman, R., Iwata, A., Meaney, D.F., Trojanowski, J.Q., and Smith, D.H. (2004). Long-term accumulation of amyloid-beta, beta-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma. Am. J. Pathol. 165, 357-371.
5. Smith, D.H., Chen, X.H., Iwata, A., and Graham, D.I. (2003). Amyloid beta accumulation in axons after traumatic brain injury in humans. J. Neurosurg. 98, 1072-1077.
6. Uryu, K., Chen, X.H., Martinez, D., Browne, K.D., Johnson, V.E., Graham, D.I., Lee, V.M., Trojanowski, J.Q., and Smith, D.H. (2007). Multiple proteins implicated in neurodegenerative diseases accumulate in axons after brain trauma in humans. Exp. Neurol. 208, 185-192.
7. Ikonomovic, M.D., Uryu, K., Abrahamson, E.E., Ciallella, J.R., Tro-janowski, J.Q., Lee, V.M., Clark, R.S., Marion, D.W., Wisniewski, S.R., and Dekosky, S.T. (2004). Alzheimer's pathology in human temporal cortex surgically excised after severe brain injury. Exp. Neurol. 190, 192-203.
8. Roberts, G.W., Gentleman, S.M., Lynch, A., and Graham, D.I. (1991). beta A4 amyloid protein deposition in brain after head trauma. Lancet 338, 1422-1423.
9. Roberts, G.W., Gentleman, S.M., Lynch, A., Murray, L., Landon, M., and Graham, D.I. (1994). Beta amyloid protein deposition in the brain after severe head injury: implications for the pathogenesis of Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 57, 419-425.
10. Hardy, J., and Selkoe, D.J. (2002). The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
11. Hardy, J.A., and Higgins, G.A. (1992). Alzheimer's disease: the amyloid cascade hypothesis. Science 256, 184-185.
12. Selkoe, D.J. (1998). The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell. Biol. 8, 447-453.
13. Walsh, D.M., and Selkoe, D.J. (2007). A beta oligomers-a decade of discovery. J. Neurochem. 101, 1172-1184.
14. Benilova, I., Karran, E., and De Strooper, B. (2012). The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nat. Neurosci. 15, 349-357.
15. Selkoe, D.J. (2002). Alzheimer's disease is a synaptic failure. Science 298, 789-791.
16. McLean, C.A., Cherny, R.A., Fraser, F.W., Fuller, S.J., Smith, M.J., Beyreuther, K., Bush, A.I., and Masters, C.L. (1999). Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 46, 860-866.
17. Lue, L.F., Kuo, Y.M., Roher, A.E., Brachova, L., Shen, Y., Sue, L., Beach, T., Kurth, J.H., Rydel, R.E., and Rogers, J. (1999). Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862.
18. Walsh, D.M., Klyubin, I., Fadeeva, J.V., Cullen, W.K., Anwyl, R., Wolfe, M.S., Rowan, M.J., and Selkoe, D.J. (2002). Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
19. Shankar, G.M., Li, S., Mehta, T.H., Garcia-Munoz, A., Shepardson, N.E., Smith, I., Brett, F.M., Farrell, M.A., Rowan, M.J., Lemere, C.A., Regan, C.M., Walsh, D.M., Sabatini, B.L., and Selkoe, D.J. (2008). Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842.
20. Lambert, M.P., Barlow, A.K., Chromy, B.A., Edwards, C., Freed, R., Liosatos, M., Morgan, T.E., Rozovsky, I., Trommer, B., Viola, K.L., Wals, P., Zhang, C., Finch, C.E., Krafft, G.A., and Klein, W.L. (1998). Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95, 6448-6453.
21. Dahlgren, K.N., Manelli, A.M., Stine, W.B., Jr., Baker, L.K., Krafft, G.A., and LaDu, M.J. (2002). Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 277, 32046-32053.
22. Deshpande, A., Mina, E., Glabe, C., and Busciglio, J. (2006). Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J. Neurosci. 26, 6011-6018.
23. Gatson, J.W., Warren, V., Abdelfattah, K., Wolf, S., Hynan, L.S., Moore, C., Diaz-Arrastia, R., Minei, J.P., Madden, C., and Wigginton, J.G. (2013). Detection of beta-amyloid oligomers as a predictor of neurological outcome after brain injury. J. Neurosurg. 118, 1336-1342.
24. Abrahamson, E.E., Ikonomovic, M.D., Ciallella, J.R., Hope, C.E., Paljug, W.R., Isanski, B.A., Flood, D.G., Clark, R.S., and DeKosky, S.T. (2006). Caspase inhibition therapy abolishes brain trauma-induced increases in Abeta peptide: implications for clinical outcome. Exp. Neurol. 197, 437-450.
25. Abrahamson, E.E., Ikonomovic, M.D., Dixon, C.E., and Dekosky, S.T. (2009). Simvastatin therapy prevents brain trauma-induced increases in beta-amyloid peptide levels. Ann. Neurol. 66, 407-414.
26. Laskowitz, D.T., Song, P., Wang, H., Mace, B., Sullivan, P.M., Vitek, M.P., and Dawson, H.N. (2010). Traumatic brain injury exacerbates neurodegenerative pathology: improvement with an apolipoprotein E-based therapeutic. J. Neurotrauma 27, 1983-1995.
27. Loane, D.J., Pocivavsek, A., Moussa, C.E., Thompson, R., Matsuoka, Y., Faden, A.I., Rebeck, G.W., and Burns, M.P. (2009). Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury. Nat. Med. 15, 377-379.
28. Loane, D.J., Washington, P.M., Vardanian, L., Pocivavsek, A., Hoe, H.S., Duff, K.E., Cernak, I., Rebeck, G.W., Faden, A.I., and Burns, M.P. (2011). Modulation of ABCA1 by an LXR agonist reduces beta-amyloid levels and improves outcome after traumatic brain injury. J. Neurotrauma 28, 225-236.
29. Mannix, R.C., Zhang, J., Park, J., Zhang, X., Bilal, K., Walker, K., Tanzi, R.E., Tesco, G., and Whalen, M.J. (2011). Age-dependent effect of apolipoprotein E4 on functional outcome after controlled cortical impact in mice. J. Cereb. Blood Flow Metab. 31, 351-361
30. Uryu, K., Laurer, H., McIntosh, T., Pratico, D., Martinez, D., Leight, S., Lee, V.M., and Trojanowski, J.Q. (2002). Repetitive mild brain trauma accelerates Abeta deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis. J. Neurosci. 22, 446-454.
31. Wang, H., Durham, L., Dawson, H., Song, P., Warner, D.S., Sullivan, P.M., Vitek, M.P., and Laskowitz, D.T. (2007). An apolipoprotein E-based therapeutic improves outcome and reduces Alzheimer's disease pathology following closed head injury: evidence of pharmacoge-nomic interaction. Neuroscience 144, 1324-1333.
32. Fraser, P.E., Nguyen, J.T., Inouye, H., Surewicz, W.K., Selkoe, D.J., Podlisny, M.B., and Kirschner, D.A. (1992). Fibril formation by primate, rodent, and Dutch-hemorrhagic analogues of Alzheimer amyloid beta-protein. Biochemistry 31, 10716-10723.
33. Hartman, R.E., Laurer, H., Longhi, L., Bales, K.R., Paul, S.M., McIn-tosh, T.K., and Holtzman, D.M. (2002). Apolipoprotein E4 influences amyloid deposition but not cell loss after traumatic brain injury in a mouse model of Alzheimer's disease. J. Neurosci. 22, 10083-10087.
34. Tran, H.T., Sanchez, L., Esparza, T.J. and Brody, D.L. (2011). Distinct temporal and anatomical distributions of amyloid-beta and tau abnormalities following controlled cortical impact in transgenic mice. PLoS One 6, e25475.
35. Nakagawa, Y., Nakamura, M., McIntosh, T.K., Rodriguez, A., Berlin, J.A., Smith, D.H., Saatman, K.E., Raghupathi, R., Clemens, J., Saido, T.C., Schmidt, M.L., Lee, V.M., and Trojanowski, J.Q. (1999). Traumatic brain injury in young, amyloid-beta peptide overexpressing transgenic mice induces marked ipsilateral hippocampal atrophy and diminished Abeta deposition during aging. J. Comp. Neurol. 411, 390-398.
36. Nakagawa, Y., Reed, L., Nakamura, M., McIntosh, T.K., Smith, D.H., Saatman, K.E., Raghupathi, R., Clemens, J., Saido, T.C., Lee, V.M., and Trojanowski, J.Q. (2000). Brain trauma in aged transgenic mice induces regression of established abeta deposits. Exp. Neurol. 163, 244-252.
37. Conte, V., Uryu, K., Fujimoto, S., Yao, Y., Rokach, J., Longhi, L., Trojanowski, J.Q., Lee, V.M., McIntosh, T.K., and Pratico, D. (2004). Vitamin E reduces amyloidosis and improves cognitive function in Tg2576 mice following repetitive concussive brain injury. J. Neu-rochem. 90, 758-764.
38. Murai, H., Pierce, J.E., Raghupathi, R., Smith, D.H., Saatman, K.E., Trojanowski, J.Q., Lee, V.M., Loring, J.F., Eckman, C., Younkin, S., and McIntosh, T.K. (1998). Twofold overexpression of human beta-amyloid precursor proteins in transgenic mice does not affect the neuromotor, cognitive, or neurodegenerative sequelae following experimental brain injury. J. Comp. Neurol. 392, 428-438.
39. Smith, D.H., Nakamura, M., McIntosh, T.K., Wang, J., Rodriguez, A., Chen, X.H., Raghupathi, R., Saatman, K.E., Clemens, J., Schmidt, M.L., Lee, V.M., and Trojanowski, J.Q. (1998). Brain trauma induces massive hippocampal neuron death linked to a surge in beta-amyloid levels in mice overexpressing mutant amyloid precursor protein. Am. J. Pathol. 153, 1005-1010.
40. Washington, P.M., Forcelli, P.A., Wilkins, T., Zapple, D., Parsada-nian, M., and Burns, M.P. (2012). The effect of injury severity on behavior: a phenotypic study of cognitive and emotional deficits after mild, moderate and severe controlled cortical impact injury in mice. J. Neurotrauma 29, 2283-2296.
41. Oddo, S., Caccamo, A., Shepherd, J.D., Murphy, M.P., Golde, T.E., Kayed, R., Metherate, R., Mattson, M.P., Akbari, Y., and LaFerla, F.M. (2003). Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39, 409-421.
42. Hirata-Fukae, C., Li, H.F., Hoe, H.S., Gray, A.J., Minami, S.S., Ha-mada, K., Niikura, T., Hua, F., Tsukagoshi-Nagai, H., Horikoshi-Sakuraba, Y., Mughal, M., Rebeck, G.W., LaFerla, F.M., Mattson, M.P., Iwata, N., Saido, T.C., Klein, W.L., Duff, K.E., Aisen, P.S., and Mat-suoka, Y. (2008). Females exhibit more extensive amyloid, but not tau, pathology in an Alzheimer transgenic model. Brain Res. 1216, 92-103.
43. Luo, Y., Bolon, B., Kahn, S., Bennett, B.D., Babu-Khan, S., Denis, P., Fan, W., Kha, H., Zhang, J., Gong, Y., Martin, L., Louis, J.C., Yan, Q., Richards, W.G., Citron, M., and Vassar, R. (2001). Mice deficient in BACE1, the Alzheimer's beta-secretase, have normal phenotype and abolished beta-amyloid generation. Nat. Neurosci. 4, 231-232.
44. Savage, M.J., Trusko, S.P., Howland, D.S., Pinsker, L.R., Mistretta, S., Reaume, A.G., Greenberg, B.D., Siman, R., and Scott, R.W. (1998). Turnover of amyloid beta-protein in mouse brain and acute reduction of its level by phorbol ester. J. Neurosci. 18, 1743-1752.
45. Xia, W., Yang, T., Shankar, G., Smith, I.M., Shen, Y., Walsh, D.M., and Selkoe, D.J. (2009). A specific enzyme-linked immunosorbent assay for measuring beta-amyloid protein oligomers in human plasma and brain tissue of patients with Alzheimer disease. Arch. Neurol. 66, 190-199.
46. Stine, W.B., Jr., Dahlgren, K.N., Krafft, G.A., and LaDu, M.J. (2003). In vitro characterization of conditions for amyloid-beta peptide olig-omerization and fibrillogenesis. J. Biol. Chem. 278, 11612-11622.
47. Li, S., Jin, M., Zhang, D., Yang, T., Koeglsperger, T., Fu, H., and Selkoe, D.J. (2013). Environmental novelty activates beta2-adrenergic signaling to prevent the impairment of hippocampal LTP by Abeta oligomers. Neuron 77, 929-941.
48. Pryor, N.E., Moss, M.A., and Hestekin, C.N. (2012). Unraveling the early events of amyloid-beta protein (Abeta) aggregation: techniques for the determination of Abeta aggregate size. Int. J. Mol. Sci. 13, 3038-3072.
49. Kayed, R., Head, E., Thompson, J.L., McIntire, T.M., Milton, S.C., Cotman, C.W., and Glabe, C.G. (2003). Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489.
50. Ciallella, J.R., Ikonomovic, M.D., Paljug, W.R., Wilbur, Y.I., Dixon, C.E., Kochanek, P.M., Marion, D.W., and DeKosky, S.T. (2002). Changes in expression of amyloid precursor protein and interleukin-1beta after experimental traumatic brain injury in rats. J. Neurotrauma 19, 1555-1567.
51. Hoshino, S., Tamaoka, A., Takahashi, M., Kobayashi, S., Furukawa, T., Oaki, Y., Mori, O., Matsuno, S., Shoji, S., Inomata, M., and Ter-amoto, A. (1998). Emergence of immunoreactivities for phosphory-lated tau and amyloid-beta protein in chronic stage of fluid percussion injury in rat brain. Neuroreport 9, 1879-1883.
52. Laurer, H.L., Bareyre, F.M., Lee, V.M., Trojanowski, J.Q., Longhi, L., Hoover, R., Saatman, K.E., Raghupathi, R., Hoshino, S., Grady, M.S., and McIntosh, T.K. (2001). Mild head injury increasing the brain's vulnerability to a second concussive impact. J. Neurosurg. 95, 859-870.
53. Lewen, A., Li, G.L., Olsson, Y., and Hillered, L. (1996). Changes in microtubule-associated protein 2 and amyloid precursor protein im-munoreactivity following traumatic brain injury in rat: influence of MK-801 treatment. Brain Res. 719, 161-171.
54. Masumura, M., Hata, R., Uramoto, H., Murayama, N., Ohno, T., and Sawada, T. (2000). Altered expression of amyloid precursors proteins after traumatic brain injury in rats: in situ hybridization and immu-nohistochemical study. J. Neurotrauma 17, 123-134.
55. Pierce, J.E., Trojanowski, J.Q., Graham, D.I., Smith, D.H., and McIntosh, T.K. (1996). Immunohistochemical characterization of alterations in the distribution of amyloid precursor proteins and beta-amyloid peptide after experimental brain injury in the rat. J. Neurosci. 16, 1083-1090.
56. Stone, J.R., Okonkwo, D.O., Singleton, R.H., Mutlu, L.K., Helm, G.A., and Povlishock, J.T. (2002). Caspase-3-mediated cleavage of amyloid precursor protein and formation of amyloid Beta peptide in traumatic axonal injury. J. Neurotrauma 19, 601-614.
57. Otvos, L., Jr., Szendrei, G.I., Lee, V.M., and Mantsch, H.H. (1993). Human and rodent Alzheimer beta-amyloid peptides acquire distinct conformations in membrane-mimicking solvents. Eur. J. Biochem. 211, 249-257.
58. Johnson, V.E., Stewart, W., and Smith, D.H. (2012). Widespread tau and amyloid-beta pathology many years after a single traumatic brain injury in humans. Brain Pathol. 22, 142-149.
59. 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., and Meaney, D.F. (1999). Accumulation of amyloid beta and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig. J. Neuropathol. Exp. Neurol. 58, 982-992.
60. Nicoll, J.A., Roberts, G.W., and Graham, D.I. (1995). Apolipoprotein E epsilon 4 allele is associated with deposition of amyloid beta-protein following head injury. Nat. Med. 1, 135-137.