Characterisation of the effect of knockout of the amyloid precursor protein on outcome following mild traumatic brain injury

Brain Research

Volumn 1451, Issue , 2012, Pages 87-99

  Corrigan, Frances ^a,b   Vink, Robert ^a,b   Blumbergs, Peter C ^a,b   Masters, Colin L ^c   Cappai, Roberto ^d   Van Den Heuvel, Corinna ^a,b  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b HANSON INSTITUTE   (Australia)

^c FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Amyloid precursor protein; Caspase 3; GAP 43; sAPP ; Synaptophysin; Traumatic brain injury

Indexed keywords

AMYLOID PRECURSOR PROTEIN; NEUROMODULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXONAL INJURY; BRAIN CORTEX; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; GENE INACTIVATION; HIPPOCAMPUS; IMMUNOREACTIVITY; MOTOR DYSFUNCTION; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; TRAUMATIC BRAIN INJURY; WILD TYPE;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONS; BRAIN INJURIES; CASPASE 3; CEREBRAL CORTEX; HIPPOCAMPUS; MAZE LEARNING; MICE; MICE, KNOCKOUT; MOTOR SKILLS; NEURONS; RECOVERY OF FUNCTION; ROTAROD PERFORMANCE TEST;

MUS;

EID: 84859926572     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.02.045     Document Type: Article

References (74)

1. W. Araki, N. Kitaguchi, Y. Tokushima, K. Ishii, H. Aratake, S. Shimohama, S. Nakamura, and J. Kimura Trophic effect of beta-amyloid precursor protein on cerebral cortical neurons in culture Biochem. Biophys. Res. Commun. 181 1991 265 271
2. C.A. Barnes Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat J. Comp. Physiol. Psychol. 93 1979 74 104 (Pubitemid 9140564)
3. J.J. Bazarian, J. Zhong, B. Blyth, T. Zhu, V. Kavcic, and D. Peterson Diffusion tensor imaging detects clinically important axonal damage after mild traumatic brain injury: a pilot study J. Neurotrauma 24 2007 1447 1459 (Pubitemid 47493510)
4. K.F. Bell, L. Zheng, F. Fahrenholz, and A.C. Cuello ADAM-10 over-expression increases cortical synaptogenesis Neurobiol. Aging 29 2006 554 565
5. C. Bendotti, S. Baldessari, M. Pende, T. Southgate, F. Guglielmetti, and R. Samanin Relationship between GAP-43 expression in the dentate gyrus and synaptic reorganization of hippocampal mossy fibres in rats treated with kainic acid Eur. J. Neurosci. 9 1997 93 101
6. L. Beni-Adani, I. Gozes, Y. Cohen, Y. Assaf, R.A. Steingart, D.E. Brenneman, O. Eizenberg, V. Trembolver, and E. Shohami A peptide derived from activity-dependent neuroprotective protein (ADNP) ameliorates injury response in closed head injury in mice J. Pharmacol. Exp. Ther. 296 2001 57 63 (Pubitemid 32015060)
7. R. Bhasin, W.E. Van Nostrand, T. Saitoh, M.A. Donets, E.A. Barnes, W.W. Quitschke, and D. Goldgaber Expression of active secreted forms of human amyloid beta-protein precursor by recombinant baculovirus-infected insect cells Proc. Natl. Acad. Sci. U. S. A. 88 1991 10307 10311 (Pubitemid 21915824)
8. I. Blasko, R. Beer, M. Bigl, J. Apelt, G. Franz, D. Rudzki, G. Ransmayr, A. Kampfl, and R. Schliebs Experimental traumatic brain injury in rats stimulates the expression, production and activity of Alzheimer's disease beta-secretase (BACE-1) J. Neural Transm. 111 2004 523 536 (Pubitemid 38478920)
9. P.C. Blumbergs, G. Scott, J. Manavis, H. Wainwright, D.A. Simpson, and A.J. McLean Staining of amyloid precursor protein to study axonal damage in mild head injury Lancet 344 1994 1055 1056 (Pubitemid 24310039)
10. D. Boyd-Kimball, R. Sultana, H. Mohmmad-Abdul, and D.A. Butterfield Rodent Abeta(1-42) exhibits oxidative stress properties similar to those of human Abeta(1-42): Implications for proposed mechanisms of toxicity J. Alzheimers Dis. 6 2004 515 525 (Pubitemid 40916693)
11. I. Caille, B. Allinquant, E. Dupont, C. Bouillot, A. Langer, U. Muller, and A. Prochiantz Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone Development 131 2004 2173 2181 (Pubitemid 38702048)
12. X.H. Chen, R. Siman, A. Iwata, D.F. Meaney, J.Q. Trojanowski, and D.H. Smith Long-term accumulation of amyloid-beta, beta-secretase, presenilin-1, and caspase-3 in damaged axons following brain trauma Am. J. Pathol. 165 2004 357 371 (Pubitemid 38971368)
13. C.W. Christman, J.B. Salvant Jr., S.A. Walker, and J.T. Povlishock 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 1997 329 337 (Pubitemid 27450112)
14. J.A. Creed, A.M. DiLeonardi, D.P. Fox, A.R. Tessler, and R. Raghupathi Concussive brain trauma in the mouse results in acute cognitive deficits and sustained impairment of axonal function J. Neurotrauma 28 2011 547 563
15. G.R. Dawson, G.R. Seabrook, H. Zheng, D.W. Smith, S. Graham, G. O'Dowd, B.J. Bowery, S. Boyce, M.E. Trumbauer, H.Y. Chen, L.H. Van der Ploeg, and D.J. Sirinathsinghji Age-related cognitive deficits, impaired long-term potentiation and reduction in synaptic marker density in mice lacking the beta-amyloid precursor protein Neuroscience 90 1999 1 13 (Pubitemid 29096448)
16. D.L. Emery, R. Raghupathi, K.E. Saatman, I. Fischer, M.S. Grady, and T.K. McIntosh Bilateral growth-related protein expression suggests a transient increase in regenerative potential following brain trauma J. Comp. Neurol. 424 2000 521 531 (Pubitemid 30670448)
17. M.A. Flierl, P.F. Stahel, K.M. Beauchamp, S.J. Morgan, W.R. Smith, and E. Shohami Mouse closed head injury model induced by a weight-drop device Nat. Protoc. 4 2009 1328 1337
18. P.E. Fraser, J.T. Nguyen, D.T. Chin, and D.A. Kirschner Effects of sulfate ions on Alzheimer beta/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions J. Neurochem. 59 1992 1531 1540
19. S.T. Fujimoto, L. Longhi, K.E. Saatman, V. Conte, N. Stocchetti, and T.K. McIntosh Motor and cognitive function evaluation following experimental traumatic brain injury Neurosci. Biobehav. Rev. 28 2004 365 378 (Pubitemid 39077928)
20. K. Furukawa, B.L. Sopher, R.E. Rydel, J.G. Begley, D.G. Pham, G.M. Martin, M. Fox, and M.P. Mattson Increased activity-regulating and neuroprotective efficacy of alpha-secretase-derived secreted amyloid precursor protein conferred by a C-terminal heparin-binding domain J. Neurochem. 67 1996 1882 1896 (Pubitemid 26349661)
21. M. Gaetz The neurophysiology of brain injury Clin. Neurophysiol. 115 2004 4 18 (Pubitemid 38045590)
22. S.M. Gentleman, D.I. Graham, and G.W. Roberts Molecular pathology of head trauma: altered beta APP metabolism and the aetiology of Alzheimer's disease Prog. Brain Res. 96 1993 237 246 (Pubitemid 23185296)
23. Y. Goodman, and M.P. Mattson Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury Exp. Neurol. 128 1994 1 12
24. W. Gordon-Krajcer, and B. Gajkowska Excitotoxicity-induced expression of amyloid precursor protein (beta-APP) in the hippocampus and cortex of rat brain. An electron-microscopy and biochemical study Folia Neuropathol. 39 2001 163 173
25. S.C. Hellewell, E.B. Yan, D.A. Agyapomaa, N. Bye, and M.C. Morganti-Kossmann Post-traumatic hypoxia exacerbates brain tissue damage: analysis of axonal injury and glial responses J. Neurotrauma 27 2010 1997 2010
26. J. Herms, B. Anliker, S. Heber, S. Ring, M. Fuhrmann, H. Kretzschmar, S. Sisodia, and U. Muller Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members EMBO J. 23 2004 4106 4115 (Pubitemid 39472431)
27. A. Herreman, G. Van Gassen, M. Bentahir, O. Nyabi, K. Craessaerts, U. Mueller, W. Annaert, and B. De Strooper gamma-Secretase activity requires the presenilin-dependent trafficking of nicastrin through the Golgi apparatus but not its complex glycosylation J. Cell Sci. 116 2003 1127 1136 (Pubitemid 36395622)
28. C.E. Hulsebosch, D.S. DeWitt, L.W. Jenkins, and D.S. Prough Traumatic brain injury in rats results in increased expression of Gap-43 that correlates with behavioral recovery Neurosci. Lett. 255 1998 83 86 (Pubitemid 28494204)
29. A.A. Hyder, C.A. Wunderlich, P. Puvanachandra, G. Gururaj, and O.C. Kobusingye The impact of traumatic brain injuries: a global perspective NeuroRehabilitation 22 2007 341 353
30. M. Inglese, S. Makani, G. Johnson, B.A. Cohen, J.A. Silver, O. Gonen, and R.I. Grossman Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study J. Neurosurg. 103 2005 298 303 (Pubitemid 43193906)
31. A. Iwata, X.H. Chen, T.K. McIntosh, K.D. Browne, and D.H. Smith Long-term accumulation of amyloid-beta in axons following brain trauma without persistent upregulation of amyloid precursor protein genes J. Neuropathol. Exp. Neurol. 61 2002 1056 1068 (Pubitemid 35435024)
32. V.E. Johnson, W. Stewart, and D.H. Smith Traumatic brain injury and amyloid-beta pathology: a link to Alzheimer's disease? 2010 Nat. Rev Neurosci
33. A.D. Kay, A. Petzold, M. Kerr, G. Keir, E. Thompson, and J.A. Nicoll Alterations in cerebrospinal fluid apolipoprotein E and amyloid beta-protein after traumatic brain injury J. Neurotrauma 20 2003 943 952 (Pubitemid 37288554)
34. H.S. Kim, E.M. Kim, N.J. Kim, K.A. Chang, Y. Choi, K.W. Ahn, J.H. Lee, S. Kim, C.H. Park, and Y.H. Suh Inhibition of histone deacetylation enhances the neurotoxicity induced by the C-terminal fragments of amyloid precursor protein J. Neurosci. Res. 75 2004 117 124 (Pubitemid 38049412)
35. E.H. Koo, S.L. Squazzo, D.J. Selkoe, and C.H. Koo Trafficking of cell-surface amyloid beta-protein precursor. I. Secretion, endocytosis and recycling as detected by labeled monoclonal antibody J. Cell Sci. 109 Pt 5 1996 991 998
36. G. Koopmans, A. Blokland, P. van Nieuwenhuijzen, and J. Prickaerts Assessment of spatial learning abilities of mice in a new circular maze Physiol. Behav. 79 2003 683 693 (Pubitemid 37087962)
37. M. Leyssen, D. Ayaz, S.S. Hebert, S. Reeve, B. De Strooper, and B.A. Hassan Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain EMBO J. 24 2005 2944 2955 (Pubitemid 43079897)
38. L.H. Lin, S. Bock, K. Carpenter, M. Rose, and J.J. Norden Synthesis and transport of GAP-43 in entorhinal cortex neurons and perforant pathway during lesion-induced sprouting and reactive synaptogenesis Brain Res. Mol. Brain Res. 14 1992 147 153
39. D.J. Loane, A. Pocivavsek, C.E. Moussa, R. Thompson, Y. Matsuoka, A.I. Faden, G.W. Rebeck, and M.P. Burns Amyloid precursor protein secretases as therapeutic targets for traumatic brain injury Nat. Med. 15 2009 377 379
40. D.J. Loane, P.M. Washington, L. Vardanian, A. Pocivavsek, H.S. Hoe, K.E. Duff, I. Cernak, G.W. Rebeck, A.I. Faden, and M.P. Burns Modulation of ABCA1 by an LXR agonist reduces beta-amyloid levels and improves outcome after traumatic brain injury J. Neurotrauma 28 2011 225 236
41. R.C. Mannix, J. Zhang, J. Park, X. Zhang, K. Bilal, K. Walker, R.E. Tanzi, G. Tesco, and M.J. Whalen Age-dependent effect of apolipoprotein E4 on functional outcome after controlled cortical impact in mice J. Cereb. Blood Flow Metab. 31 2010 351 361
42. A. Marmarou, M.A. Foda, W. van den Brink, J. Campbell, H. Kita, and K. Demetriadou A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics J. Neurosurg. 80 1994 291 300 (Pubitemid 24036501)
43. C.R. Marmarou, S.A. Walker, C.L. Davis, and J.T. Povlishock Quantitative analysis of the relationship between intra- axonal neurofilament compaction and impaired axonal transport following diffuse traumatic brain injury J. Neurotrauma 22 2005 1066 1080 (Pubitemid 41532545)
44. M.P. Mattson Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives Physiol. Rev. 77 1997 1081 1132 (Pubitemid 27459580)
45. M.P. Mattson, B. Cheng, A.R. Culwell, F.S. Esch, I. Lieberburg, and R.E. Rydel Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein Neuron 10 1993 243 254 (Pubitemid 23079546)
46. R.A. McKinney, A. Luthi, C.E. Bandtlow, B.H. Gahwiler, and S.M. Thompson Selective glutamate receptor antagonists can induce or prevent axonal sprouting in rat hippocampal slice cultures Proc. Natl. Acad. Sci. U. S. A. 96 1999 11631 11636 (Pubitemid 29487432)
47. A. Messe, S. Caplain, G. Paradot, D. Garrigue, J.F. Mineo, G. Soto Ares, D. Ducreux, F. Vignaud, G. Rozec, H. Desal, M. Pelegrini-Issac, M. Montreuil, H. Benali, and S. Lehericy Diffusion tensor imaging and white matter lesions at the subacute stage in mild traumatic brain injury with persistent neurobehavioral impairment Hum. Brain Mapp. 32 2010 999 1011
48. N. Murakami, T. Yamaki, Y. Iwamoto, T. Sakakibara, N. Kobori, S. Fushiki, and S. Ueda Experimental brain injury induces expression of amyloid precursor protein, which may be related to neuronal loss in the hippocampus J. Neurotrauma 15 1998 993 1003 (Pubitemid 28530210)
49. T. Nihashi, S. Inao, Y. Kajita, T. Kawai, T. Sugimoto, M. Niwa, R. Kabeya, N. Hata, S. Hayashi, and J. Yoshida Expression and distribution of beta amyloid precursor protein and beta amyloid peptide in reactive astrocytes after transient middle cerebral artery occlusion Acta Neurochir. (Wien) 143 2001 287 295 (Pubitemid 32268603)
50. I. Ohsawa, C. Takamura, and S. Kohsaka The amino-terminal region of amyloid precursor protein is responsible for neurite outgrowth in rat neocortical explant culture Biochem. Biophys. Res. Commun. 236 1997 59 65 (Pubitemid 27341839)
51. A. Olsson, L. Csajbok, M. Ost, K. Hoglund, K. Nylen, L. Rosengren, B. Nellgard, and K. Blennow Marked increase of beta-amyloid(1-42) and amyloid precursor protein in ventricular cerebrospinal fluid after severe traumatic brain injury J. Neurol. 251 2004 870 876 (Pubitemid 39005974)
52. C. Opazo, F.H. Ruiz, and N.C. Inestrosa Amyloid-beta-peptide reduces copper(II) to copper(I) independent of its aggregation state Biol. Res. 33 2000 125 131
53. A.L. Phinney, M.E. Calhoun, D.P. Wolfer, H.P. Lipp, H. Zheng, and M. Jucker No hippocampal neuron or synaptic bouton loss in learning-impaired aged beta-amyloid precursor protein-null mice Neuroscience 90 1999 1207 1216 (Pubitemid 29170139)
54. A. Popa-Wagner, E. Schroder, L.C. Walker, and C. Kessler beta-Amyloid precursor protein and ss-amyloid peptide immunoreactivity in the rat brain after middle cerebral artery occlusion: effect of age Stroke 29 1998 2196 2202 (Pubitemid 28443539)
55. J.T. Povlishock, A. Marmarou, T. McIntosh, J.Q. Trojanowski, and J. Moroi Impact acceleration injury in the rat: evidence for focal axolemmal change and related neurofilament sidearm alteration J. Neuropathol. Exp. Neurol. 56 1997 347 359 (Pubitemid 27465017)
56. W.Q. Qiu, A. Ferreira, C. Miller, E.H. Koo, and D.J. Selkoe Cell-surface beta-amyloid precursor protein stimulates neurite outgrowth of hippocampal neurons in an isoform-dependent manner J. Neurosci. 15 1995 2157 2167
57. C.A. Raby, M.C. Morganti-Kossmann, T. Kossmann, P.F. Stahel, M.D. Watson, L.M. Evans, P.D. Mehta, K. Spiegel, Y.M. Kuo, A.E. Roher, and M.R. Emmerling Traumatic brain injury increases beta-amyloid peptide 1-42 in cerebrospinal fluid J. Neurochem. 71 1998 2505 2509 (Pubitemid 28531261)
58. R. Raghupathi, and S.S. Margulies Traumatic axonal injury after closed head injury in the neonatal pig J. Neurotrauma 19 2002 843 853 (Pubitemid 34815502)
59. S. Ring, S.W. Weyer, S.B. Kilian, E. Waldron, C.U. Pietrzik, M.A. Filippov, J. Herms, C. Buchholz, C.B. Eckman, M. Korte, D.P. Wolfer, and U.C. Muller The secreted beta-amyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral, and electrophysiological abnormalities of APP-deficient mice J. Neurosci. 27 2007 7817 7826 (Pubitemid 47093823)
60. G.W. Roberts, S.M. Gentleman, A. Lynch, and D.I. Graham beta A4 amyloid protein deposition in brain after head trauma Lancet 338 1991 1422 1423
61. T. Saitoh, M. Sundsmo, J.M. Roch, N. Kimura, G. Cole, D. Schubert, T. Oltersdorf, and D.B. Schenk Secreted form of amyloid beta protein precursor is involved in the growth regulation of fibroblasts Cell 58 1989 615 622 (Pubitemid 19210955)
62. D. Shukla, and B.I. Devi Mild traumatic brain injuries in adults J. Neurosci. Rural Pract. 1 2010 82 88
63. D.H. Smith, X.H. Chen, M. Nonaka, J.Q. Trojanowski, V.M. Lee, K.E. Saatman, M.J. Leoni, B.N. Xu, J.A. Wolf, and D.F. Meaney Accumulation of amyloid beta and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig J. Neuropathol. Exp. Neurol. 58 1999 982 992 (Pubitemid 29441926)
64. V.L. Smith-Swintosky, L.C. Pettigrew, S.D. Craddock, A.R. Culwell, R.E. Rydel, and M.P. Mattson Secreted forms of beta-amyloid precursor protein protect against ischemic brain injury J. Neurochem. 63 1994 781 784
65. J.R. Stone, D.O. Okonkwo, R.H. Singleton, L.K. Mutlu, G.A. Helm, and J.T. Povlishock Caspase-3-mediated cleavage of amyloid precursor protein and formation of amyloid Beta peptide in traumatic axonal injury J. Neurotrauma 19 2002 601 614 (Pubitemid 34587303)
66. Y.H. Suh, and F. Checler Amyloid precursor protein, presenilins, and alpha-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer's disease Pharmacol. Rev. 54 2002 469 525
67. G. Teasdale, and B. Jennett Assessment of coma and impaired consciousness. A practical scale Lancet 2 1974 81 84
68. S.N. Thompson, T.R. Gibson, B.M. Thompson, Y. Deng, and E.D. Hall Relationship of calpain-mediated proteolysis to the expression of axonal and synaptic plasticity markers following traumatic brain injury in mice Exp. Neurol. 201 2006 253 265 (Pubitemid 44223479)
69. E. Thornton, R. Vink, P.C. Blumbergs, and C. Van Den Heuvel Soluble amyloid precursor protein alpha reduces neuronal injury and improves functional outcome following diffuse traumatic brain injury in rats Brain Res. 1094 2006 38 46 (Pubitemid 43927608)
70. J. Tsenter, L. Beni-Adani, Y. Assaf, A.G. Alexandrovich, V. Trembovler, and E. Shohami Dynamic changes in the recovery after traumatic brain injury in mice: effect of injury severity on T2-weighted MRI abnormalities, and motor and cognitive functions J. Neurotrauma 25 2008 324 333 (Pubitemid 351457764)
71. C. Van den Heuvel, P.C. Blumbergs, J.W. Finnie, J. Manavis, N.R. Jones, P.L. Reilly, and R.A. Pereira Upregulation of amyloid precursor protein messenger RNA in response to traumatic brain injury: an ovine head impact model Exp. Neurol. 159 1999 441 450 (Pubitemid 29485230)
72. W.C. Wallace, C.A. Akar, and W.E. Lyons Amyloid precursor protein potentiates the neurotrophic activity of NGF Brain Res. Mol. Brain Res. 52 1997 201 212 (Pubitemid 28043463)
73. Y. Wang, and Y. Ha The X-ray structure of an antiparallel dimer of the human amyloid precursor protein E2 domain Mol. Cell 15 2004 343 353 (Pubitemid 39092751)
74. H. Zheng, M. Jiang, M.E. Trumbauer, D.J. Sirinathsinghji, R. Hopkins, D.W. Smith, R.P. Heavens, G.R. Dawson, S. Boyce, M.W. Conner, K.A. Stevens, H.H. Slunt, S.S. Sisoda, H.Y. Chen, and L.H. Van der Ploeg beta-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity Cell 81 1995 525 531