Altered expression of amyloid precursor proteins after traumatic brain injury in rats: In situ hybridization and immunohistochemical study

Journal of Neurotrauma

Volumn 17, Issue 2, 2000, Pages 123-134

  Masumura, Makoto ^a,b   Hata, Ryuji ^a   Uramoto, Hiroshi ^b   Murayama, Norihito ^b   Ohno, Tomochika ^b   Sawada, Tohru ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b SUNTORY LTD   (Japan)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Amyloid protein; Immunohistochemistry; In situ hybridization; Traumatic brain injury

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ALZHEIMER DISEASE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NONHUMAN; RAT;

EID: 0034002073     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2000.17.123     Document Type: Article

References (66)

1. ABE, K., TANZI, R.E., and KOGURE, K. (1991). Selective induction of Kunitz-type protease inhibitor domain-containing amyloid precursor protein mRNA after persistent focal ischemia in rat cerebral cortex. Neurosci. Lett. 125, 172-174.
2. ALLSOP, D., HAGA, S., BRUTON, C., ISHII, T., and ROBERTS, G.W. (1990). Neurofibrillary tangles in some cases of dementia pugilistica share antigens with amyloid beta-protein of Alzheimer's disease. Am. J. Pathol. 136, 255-260.
3. APELT, J., SCHLIEBS, R., BECK, M., ROßNER, S., and BIGL, V. (1997). Expression of amyloid precursor protein mRNA isoforms in rat brain is differentially regulated during postnatal maturation and by cholinergic activity. Int. J. Dev. Neurosci. 15, 95-112.
4. BRAMLETT, H.M., KRAYDIEH, S., GREEN, E.J., and DIETRICH, W.D. (1997). Temporal and regional patterns of axonal damage following traumatic brain injury: a beta-amyloid precursor protein immunocytochemical study in rats. J. Neuropathol. Exp. Neurol. 56, 1132-1141.
5. BLUMBERGS, P.C., SCOTT, G., MANAVIS, J., WAINWRIGHT, H., SIMPSON, D.A., and MCLEAN, A.J. (1994). Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344, 1055-1056.
6. BRUGG, B., DUBREUIL, Y.L., HUBER, G., WOLLMAN, E.E., DELHAYE-BOUCHAUD, N., and MIRIAM, J. (1995). Inflammatory processes induce β-amyloid precursor protein changes in mouse brain. Proc. Natl. Acad. Sci. U.S.A. 92, 3032-3035.
7. DENMAN, R., POTEMPSKA, A., WOLFE, G., RAMA-KRISHNA, N., and MILLER, D.L. (1991). Distribution and activity of alternatively spliced Alzheimer amyloid peptide precursor and scrapie PrP mRNAs on rat brain polysomes. Arch. Biochem. Biophys. 288, 29-38.
8. DE SILVA, H.A.R., JEN, A., WICKENDEN, C., JEN, L.-S., WILKINSON, S.L., and PATEL, A.J. (1997). Cell-specific expression of β-amyloid precursor protein isoform mRNAs and proteins in neurons and astrocytes. Mol. Brain Res. 47, 147-156.
9. DIETRICH, W.D., ALONSO, O., BUSTO, R., et al. (1998). Posttraumatic cerebral ischemia after fluid percussion brain injury: an autoradiographic and histopathological study in rats. Neurosurgery 43, 585-594.
10. GENTLEMAN, S.M., GRAHAM, D.I., and ROBERTS, G.W. (1993a). Molecular pathology of head trauma: altered βAPP metabolism and the aetiology of Alzheimer's disease. Prog. Brain Res. 96, 237-246.
11. GENTLEMAN, S.M., NASH, M.J., SWEETING, C.J., GRAHAM, D.I., and ROBERTS, G. (1993b). β-Amyloid precursor protein (βAPP) as a marker for axonal injury after head injury. Neurosci. Lett. 160, 139-144.
12. GLECKMAN, A.M., BELL, M.D., EVANS, R.J., and SMITH, T.W. (1999). Diffuse axonal injury in infants with nonaccidental craniocerebral trauma: enhanced detection by β-amyloid precursor protein immunohistochemical staining. Arch. Pathol. Lab. Med. 123, 146-151.
13. GRAHAM, D.I., GENTLEMAN, S.M., LYNCH, A., and ROBERTS, G.W. (1995). Distribution of β-amyloid protein in the brain following severe head injury. Neuropathol. Appl. Neurobiol. 21, 27-34.
14. GRAHAM, D.I., GENTLEMAN, S.M., NICOLL, J.A.R., et al. (1996). Altered β-APP metabolism after head injury and its relationship to the aetiology of Alzheimer's disease. Acta Neurochir. 66, Suppl., 96-102.
15. + channel openers prevent global ischemia-induced expression of c-fos, c-jun, heat shock protein, and amyloid β-protein precursor genes and neuronal death in rat hippocampus. Proc. Natl. Acad. Sci. U.S.A. 90, 9431-9435.
16. HILL-FELBERG, S.J., MCINTOSH, T.K., OLIVER, D.L., RAGHUPATHI, R., and BARBARESE, E. (1999). Concurrent loss and proliferation of astrocytes following lateral fluid percussion brain injury in the adult rat. J. Neurosci. Res. 57, 271-279.
17. HOLTZMAN, D.M., BAYNEY, R.M., LI, Y., et al. (1992). Dysregulation of gene expression in mouse trisomy 16, an animal model of Down syndrome. E.M.B.O. J. 11, 619-627.
18. HOSHINO, S., TAMAOKA, A., TAKAHASHI, M., et al. (1998). Emergence of immunoreactivities for phosphorylated tau and amyloid-beta protein in chronic stage of fluid percussion injury in rat brain. Neuroreport 9, 1879-1883.
19. JOHNSON, S.A., MCNEILL, T., CORDELL, B., and FINCH, C.E. (1990). Relation of neuronal APP-751/APP-695 mRNA ratio and neuritic plaque density in Alzheimer's disease. Science 248, 854-857.
20. KALARIA, R.N., BHATTI, S., PALATINSKY, E.A., et al. (1993). Accumulation of the β amyloid precursor protein at sites of ischemic injury in rat brain. Neuroreport 4, 211-214.
21. KANG, J., and MÜLLER-HILL, B. (1990). Differential splicing of Alzheimer's disease amyloid A4 precursor RNA in rat tissues: preA4695 mRNA is predominantly produced in rat and human brain. Biochem. Biophys. Res. Commun. 166, 1192-1200.
22. KAWARABAYASHI, T., SHOJI, M., HARIGAYA, Y., YAMAGUCHI, H., and HIRAI, S. (1991). Expression of APP in the early stage of brain damage. Brain Res. 563, 334-338.
23. KIM, H.S., LEE, S.H., KIM, S.S., et al. (1998). Post-ischemic changes in the expression of Alzheimer's APP isoforms in rat cerebral cortex. Neuroreport 9, 533-537.
24. KOISTINAHO, J., PYYKÖEN, I., KEINÄNEN, R., and HÖKFELT, T. (1996). Expression of β-amyloid precursor protein mRNAs following transient focal ischaemia. Neuroreport 7, 2727-2731.
25. KOMORI, N., KITTEL, A., KANG, D., et al. (1997). Reversible ischemia increases levels of Alzheimer amyloid protein precursor without increasing levels of mRNA in the rabbit spinal cord. Mol. Brain Res. 49, 103-112.
26. LEWEN, A., LI, G.L., NILSSON, P., OLSSON, Y., and HILLERED, L. (1995). Traumatic brain injury in rat produces changes of β-amyloid precursor protein immunoreactivity. Neuroreport 6, 357-360.
27. LEWIS, S.B., FINNIE, J.W., BLUMBERGS, P.C., et al., (1996). A head impact model of early axonal injury in the sheep. J. Neurotrauma 13, 505-514.
28. LI, G.L., FAROOQUE, M., HORLTZ, A., and OLSSON, Y. (1995). Changes of β-amyloid precursor protein after compression trauma to the spinal cord: an experimental study in the rat using immunohistochemistry. J. Neurotrauma 12, 269-277.
29. MASUMURA, M., MURAYAMA, N., INOUE, T., and OHNO, T. (1996). Selective induction of fibroblast growth factor receptor-1 mRNA after transient focal ischemia in the cerebral cortex of rats. Neurosci. Lett. 213, 119-122.
30. MCKENZIE, K.J., MCLELLAN, D.R., GENTLEMAN, S.M., MAXWELL, W.L., GENNARELLI, T.A., and GRAHAM, D.I. (1996). Is β-APP a marker of axonal damage in short-surviving head injury?. Acta Neuropathol. 92, 608-613.
31. MORTIMER, J.A., VAN DUIJN, C.M., CHANDRA, L., et al. (1991). Head trauma as a risk factor for Alzheimer's disease: a collaborative reanalysis of case-control studies. Int. J. Epidemiol. 20, Int. J. Epidemiol. 20, S28-S35.
32. MORTIMER, J.A., VAN DUIJN, C.M., CHANDRA, L., et al. (1991). Head trauma as a risk factor for Alzheimer's disease: a collaborative reanalysis of case-control studies. Int. J. Epidemiol. 20, Int. J. Epidemiol. 20, S28-S35.
33. MULLAN, M., and CRAWFOLD, F. (1993). Genetic and molecular advances in Alzheimer's disease. Trends Neurosci. 16, 398-403.
34. MURAI, H., PIERCE, J.E., RAGHUPATHI, R., et al. (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.
35. MURAKAMI, N., YAMAKI, T., IWAMOTO, Y., et al. (1998). Experimental brain injury induces expression of amyloid precursor protein, which may be related to neuronal loss in the hippocampus. J. Neurotrauma 15, 993-1003.
36. NAKAMURA, Y., TAKEDA, M., NIIGAWA, H., HARIGUCHI, S., and NISHIMURA, T. (1992). Amyloid β-protein precursor deposition in rat hippocampus lesioned by ibotenic acid injection. Neurosci. Lett. 136, 95-98.
37. NEVE, R.L., VALLETTA, J.S., LI, Y., VENTOSA-MICHELMAN, M., HOLTZMAN, D.M., and MOBLEY, W.C. (1996). A comprehensive study of the spatiotemporal pattern of β-amyloid precursor protein mRNA and protein in the rat brain: lack of modulation by exogenously applied nerve growth factor. Mol. Brain Res. 39, 185-197.
38. O'CONNELL, A.W., STRADA, O., EARLEY, B., and LEONALD, B.E. (1997). Altered expression of amyloid protein precursor mRNA in the rat hippocampus following trimethyltin intoxication: an in situ hybridization study. Neurochem. Int. 30, 313-320.
39. OTSUKA, N., TOMONAGA, M., and IKEDA, K. (1991). Rapid appearance of β-amyloid precursor protein immunoreactivity in damaged axons and reactive glial cells in rat brain following needle stab injury. Brain Res. 568, 335-338.
40. OYAMA, F., SHIMADA, H., OYAMA, R., TITANI, K., and IHARA, Y. (1991). Differential expression of β-amyloid protein precursor (APP) and tau mRNA in the aged human brain: individual variability and correlation between APP-751 and four-repeat tau. J. Neuropathol. Exp. Neurol. 50, 560-578.
41. PALMERT, M.R., GOLDE, T.E., COHEN, M.L., et al. (1988). Amyloid precursor protein messenger RNAs: differential expression in Alzheimer's disease. Science 241, 1080-1084.
42. PIERCE, J.E.S., 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 β-amyloid peptide after experimental brain injury in the rat. J. Neurosci. 16, 1083-1090.
43. ROBERTS, G.W., GENTLEMAN, S.M., LYNCH, A., and GRAHAM, D.I. (1991). βA4 amyloid protein deposition in brain after head trauma. Lancet 338, 1422-1423.
44. 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.
45. SCHOFIELD, P.W., TANG, M., MARDER, K., et al. (1997). Alzheimer's disease after remote head injury: an incidence study. J. Neurol. Neurosurg. Psychiatry 62, 119-124.
46. SELKOE, D.J. (1993). Physiological production of the β-amyloid protein and the mechanism of Alzheimer's disease. Trends Neurosci. 16, 403-409.
47. SEUBERT, P., OLTERSDORF, T., LEE, M.G., et al. (1993). Secretion of β-amyloid precursor protein cleaved at the amino terminus of the β-amyloid peptide. Nature 361, 260-263.
48. SHEA, T.B. (1995). Role of glial-derived nexin in neuronal differentiation and in acute brain injury and potential involvement in exacerbation of neurodegeneration in Alzheimer's disease. Brain Res. Rev. 20, 171-184.
49. SHERRIFF, F.E., BRIDGES, L.R., and SIVALOGANATHAN, S. (1994). Early detection of axonal injury after human head trauma using immunocytochemistry for β-amyloid precursor protein. Acta Neuropathol. 87, 55-62.
50. SHIVERS, B.D., HILBICH, C., MULTHAUP, G., SALBAUM, M., BEYREUTHER, K., and SEEBERG, P.H. (1988). Alzheimer's disease amyloidogenic glycoprotein: expression pattern in rat brain suggests a role in cell contact. E.M.B.O. J. 7, 1365-1370.
51. SISODIA, S.S., KOO, E.H., HOFFMAN, P.N., PERRY, G., and PRICE, D.L. (1993). Identification and transport of full-length amyloid precursor proteins in rat peripheral nervous system. J. Neurosci. 13, 3136-3142.
52. SISODIA, S.S., SLUNT, H.H., VAN KOCH, C., LO, A.C.Y., and THINAKARAN, G. (1994). Studies of APP biology: analysis of APP secretion and characterization of an APP homologue, APLP2, in: Amyloid Protein Precursor in Development, Aging and Alzheimer's Disease. C.L. Masters, K. Beyreuther, M. Trillet, and Y. Christen (eds), Springer-Verlag: Berlin, pps. 121-133.
53. SMITH, D.H., CHEN, X.-H., NONAKA, M., et al. (1999). Accumulation of amyloid β and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig. J. Neuropathol. Exp. Neurol. 58, 982-992.
54. SOLÀ, A., MENGOD, G., PROBST, A., and PALACIOS, J.M. (1993). Differential regional and cellular distribution of β-amyloid precursor protein messenger RNAs containing and lacking the Kunitz protease inhibitor domain in the brain of human, rat and mouse. Neuroscience 53, 267-295.
55. STEPHENSON, D.T., RASH, K., and CLEMENS, J.A. (1992). Amyloid precursor protein accumulates in regions of neurodegeneration following focal cerebral ischemia in the rat. Brain Res. 593, 128-135.
56. TANAKA, S., SHIOJIRI, S., TAKAHASHI, Y., et al. (1989). Tissue-specific expression of three types of β-protein precursor mRNA: enhancement of protease inhibitor-harboring types in Alzheimer's disease brain. Biochem. Biophys. Res. Commun. 165, 1406-1414.
57. TOKUDA, T., IKEDA, S., YANAGISAWA, N., IHARA, Y., and GLENNER, G.G. (1991). Re-examination of ex-boxers' brains using immunohistochemistry with antibodies to amyloid beta-protein and tau protein. Acta Neuropathol. 82, 280-285.
58. TOMIMOTO, H., WAKITA, H., AKIGUCHI, I., NAKAMURA, S., and KIMURA, J. (1994) Temporal profiles of accumulation of amyloid βA4 protein precursor in the gerbil after graded ischemic stress. J. Cereb. Blood Flow Metab. 14, 565-573.
59. TÖPPER, R., GEHRMANN, J., BANATI, R., et al. (1995). Rapid appearance of β-amyloid precursor protein immunoreactivity in glial cells following excitotoxic brain injury. Acta Neuropathol. 89, 23-28.
60. WAKITA, H., TOMIMOTO, H., AKIGUCHI, I., OHNISHI, K., NAKAMURA, S., and KIMURA, J. (1992). Regional accumulation of amyloid β/A4 protein precursor in the gerbil brain following transient cerebral ischemia. Neurosci. Lett. 146, 135-138.
61. WALLACE, W., AHLERS, S.T., GOTLIB, J., et al. (1990). Amyloid precursor protein in the cerebral cortex is rapidly and persistently induced by loss of subcortical innervation. Proc. Natl. Acad. Sci. U.S.A. 90, 8712-8716.
62. WALLACE, W.C., AKAR, C.A., and LYONS, W.E. (1997). Amyloid precursor protein potentiates the neurotrophic activity of NGF. Mol. Brain Res. 52, 201-212.
63. YAM, P.S., TAKASAGO, T., DEWAR, D., GRAHAM, D.J., and MCCULLOCH, J. (1997). Amyloid precursor protein accumulates in white matter at the margin of a focal ischaemic lesion. Brain Res. 760, 150-157.
64. YANKNER, B.A. (1996). Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932.
65. YOKOTA, M., SAIDO, T.C., TANI, E., YAMAURA, I., and MINAMI, N. (1996). Cytotoxic fragment of amyloid precursor protein accumulates in hippocampus after global forebrain ischemia. J. Cereb. Blood Flow Metab. 16, 1219-1223.
66. ZHAO, W., ALONSO, O.F., LOOR, J.Y., BUSTO, R., and GINSBERG, M.D. (1999). Influence of early posttraumatic hypothermia therapy on local cerebral blood flow and glucose metabolism after fluid percussion brain injury. J. Neurosurg. 90, 510-519.