Cellular signaling roles of TGFβ, TNFα and βAPP in brain injury responses and Alzheimer's disease

Brain Research Reviews

Volumn 23, Issue 1-2, 1997, Pages 47-61

  Mattson, Mark P ^a   Barger, Steven W ^b   Furukawa, Katsutoshi ^a   Bruce, Annadora J ^a   Wyss Coray, Tony ^c   Mark, Robert J ^a   Mucke, Lennart ^c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

amyloid precursor protein; astrocyte; calcium; inflammatory cytokine; microglial cell; reactive oxygen species; transforming growth factor; tumor necrosis factor

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CYTOKINE; NEUROPROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ASTROCYTE; BRAIN INJURY; HUMAN; HUMAN TISSUE; INFLAMMATION; MICROGLIA; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; BRAIN INJURIES; HUMANS; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0031054724     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-0173(96)00014-8     Document Type: Review

References (120)

1. Alexander, H., Doherty, G., Block, M., Kragel, P., Jensen, J., Langstein, H., Walker, E. and Norton, J., Single-dose tumor necrosis factor protection against endotoxin-induced shock and tissue injury in rats, Infect. Immun., 59 (1991) 3889-3894.
2. Araki, W., Kitaguchi, N., Tokushima, Y., Ishii, K., Aratake, H., Shimohama, S., Nakamura, S. and Kimura, J., Trophic effect of β-amyloid precursor protein on cerebral cortical neurons in culture, Biochem. Biophys. Res. Commun., 181 (1991) 265-271.
3. Arribas, J. and Massague, J., Transforming growth factor-α and β-amyloid precursor protein share a secretory mechanism, J. Cell Biol., 128 (1995) 433-441.
4. Barger, S.W. and Mattson, M.P., Secreted form of the Alzheimer's amyloid precursor protein stimulates a membrane-associated guanylate cyclase, Biochem. J., 311 (1995) 45-47.
5. 2+ accumulation, Proc. Natl. Acad. Sci. USA, 92 (1995) 9328-9332.
6. Barger, S.W. and Mattson, M.P., Secreted form of the Alzheimer's β-amyloid precursor induces neuroprotective κB-dependent transcription, Mol. Brain Res., 40 (1996) 116-126.
7. Behl, C., Davis, J., Lesley, R. and Schubert, D., Hydrogen peroxide mediates amyloid β protein toxicity, Cell, 77 (1994) 817-827.
8. Benveniste, E.N. and Benos, D.J., TNF-α- and IFN-γ-mediated signal transduction pathways: effects on glial cell gene expression and function, FASEB J., 9 (1995) 1577-1584.
9. Benveniste, E.N., Kwon, J., Chung, W.J., Sampson, J., Pandya, K. and Tang, L.P., Differential modulation of astrocyte cytokine gene expression by TGF-β, J. Immunol., 153 (1994) 5210-5221.
10. Benzi, G. and Moretti, A., Are reactive oxygen species involved in Alzheimer's disease? Neurobiol. Aging, 16 (1995) 661-674.
11. Bruce, A.J., Boling, W., Kindy, M.S., Peschon, J., Kraemer, P.J., Carpenter, M.K., Holtsberg, F.W. and Mattson, M.P., Altered neuronal and microglial responses to brain injury in mice lacking TNF receptors, Nature Med., 2 (1996) 788-794.
12. Cai, X., Golde, T. and Younkin, S., Release of excess amyloid β protein from a mutant amyloid B protein precursor, Science, 259 (1993) 514-516.
13. Campbell, I.L., Abraham, C.R., Masliah, E., Kemper, P., Inglis, J.D., Oldstone, M.B. and Mucke, L., Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6, Proc. Natl. Acad. Sci. USA, 90 (1993) 10061-10065.
14. Chao, C.C. and Hu, S., Tumor necrosis factor-α potentiates glutamate neurotoxicity in human fetal brain cell cultures, Dev. Neurosci., 16 (1994) 172-179.
15. Chao, C.C., Hu, S., Kravitz, F.H., Tsang, M., Anderson, W.R. and Peterson, P.K., Transforming growth factor-β protects human neurons against β-amyloid-induced injury, Mol. Chem. Neuropathol., 23 (1994) 159-178.
16. Cheng, B., Christakos, S. and Mattson, M.P., Tumor necrosis factors protect neurons against excitotoxic/metabolic insults and promote maintenance of calcium homeostasis, Neuron, 12 (1994) 139-153.
17. Cornelius, P., Marlowe, M., Lee, M.D. and Pekala, P.H., The growth factor-like effects of tumor necrosis factor-α, J. Biol. Chem., 265 (1990) 20506-20516.
18. Cotman, C.W. and Anderson, A.J., A potential role for apoptosis in neurodegeneration and Alzheimer's disease, Mol. Neurobiol., 10 (1995) 19-45.
19. Da Cunha, A., Jefferson, J.A., Jackson, R.W. and Vitkovic, L., Glial cell-specific mechanisms of TGF-β1 induction by IL-1 in cerebral cortex, J. Neuroimmunol., 42 (1993) 71-86.
20. Derynck, R., TGF-β-receptor-mediated signaling, Trends Biochem. Sci., 19 (1994) 548-553.
21. Dickson, D.W., Lee, S.C., Mattiace, L.A., Yen, S.H. and Brosnan, C., Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer's disease, Glia, 7 (1993) 75-83.
22. Eddleston, M. and Mucke, L., Molecular profile of reactive astrocytes-implications for their role in neurologic disease, Neuroscience, 54 (1993) 15-36.
23. Eddy, L.J., Goeddel, D.V. and Wong, G.H., Tumor necrosis factor-α pretreatment is protective in a rat model of myocardial ischemia-reperfusion injury, Biochem. Biophys. Res. Commun., 184 (1992) 1056-1059.
24. Farrah, T. and Smith, C.A., Emerging cytokine family, Nature, 358 (1992) 26.
25. Fillit, H. and Leveugle, B., Disorders of the extracellular matrix and the pathogenesis of senile dementia of the Alzheimer's type, Lab. Invest., 72 (1995) 249-253.
26. Finch, C.E., Laping, N.J., Morgan, T.E., Nichols, N.R. and Pasinetti, G.M., TGF-β1 is an organizer of responses to neurodegeneration, J. Cell. Biochem., 53 (1993) 314-322.
27. Flanders, K.C., Lippa, C.F., Smith, T.W., Pollen, D.A. and Sporn, M.B., Altered expression of transforming growth factor-beta in Alzheimer's disease, Neurology, 45 (1995) 1561-1569.
28. + channels and suppression of neuronal activity by secreted β-amyloid precursor protein, Nature, 379 (1996) 74-78.
29. Furukawa, K., Sopher, B., Rydel, R.E., Begley, J.G., Martin, G.M. and Mattson, M.P., Increased activity-regulating and neuroprotective efficacy of α-secretase-derived secreted APP is conferred by a C-terminal heparin-binding domain, J. Neurochem., 67 (1996) 1882-1896.
30. Gabuzda, D., Busciglio, J., Chen, L., Matsudaira, P. and Yankner, B., Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative, J. Biol. Chem., 269 (1994) 13623-13628.
31. Gage, F.H., Ray, J. and Fisher, L.J., Isolation, characterization, and use of stem cells from the CNS, Annu. Rev. Neurosci., 18 (1995) 159-192.
32. Galbreath, E., Kim, S.J., Park, K., Brenner, M. and Messing, A., Overexpression of TGF-β1 in the central nervous system of transgenic mice results in hydrocephalus, J. Neuropathol. Exp. Neurol., 54 (1995) 339-349.
33. Games, D., Adams, D., Alessandrinl, R., Barbour, R., Berthelette, P., Blackwell, C., Carr, T., Clemens, J., Donaldson, T., Gillespie, F., Guido, T., Hagoplan, S., Johnson-Wood, K., Khan, K., Lee, M., Lelbowitz, E., McConlogue, S., Montoya-Zavala, M., Mucke, L., Paganini, L., Penniman, E., Power, M., Schenk, D., Seubert, P., Snyder, B., Soriano, F., Tan, H., Vitale, J., Wadsworth, S., Wolozin, B., Zhao, J., Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein, Nature, 373 (1995) 523-527.
34. Gendron, R., Nestel, F., Lapp, W. and Baines, M., Expression of tumor necrosis factor α in the developing nervous system, Int. J. Neurosci., 60 (1991) 129-136.
35. Goodman, Y. and Mattson, M.P., Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury, Exp. Neurol., 128 (1994) 1-12.
36. Goodman, Y. and Mattson, M.P., Ceramide protects hippocampal neurons against excitotoxic and oxidative insults, and amyloid β-peptide toxicity, J. Neurochem., 66 (1996) 869-872.
37. + channel openers protect hippocampal neurons against oxidative injury and amyloid β-peptide toxicity, Brain Res., 706 (1996) 328-332.
38. Gray, C.W. and Patel, A.J., Regulation of β-amyloid precursor protein isoform mRNAs by transforming growth factor-β1 and interleukin-1β in astrocytes, Mol. Brain Res., 19 (1993) 251-256.
39. Gross, C.E., Bednar, M.M., Howard, D.B. and Sporn, M.B., Transforming growth factor-β1 reduces infarct size after experimental cerebral ischemia in a rabbit model, Stroke, 24 (1993) 558-562.
40. Hall, E.D. and Braughler, J.M., Free radicals in CNS injury, Res. Publ. Assoc. Res. Nerv. Ment. Dis., 71 (1993) 81-105.
41. Heine, U.I., Munoz, E.F., Flanders, K.C., Ellingsworth, L.R., Lam, H.-Y.P., Thompson, N.L., Roberts, A.B. and Sporn, M.B., Role of Transforming growth factor-β in the development of the mouse embryo, J. Cell. Biol., 105 (1987) 2861-2876.
42. Higgins, L.S., Rodems, J.M., Catalano, R., Quon, D. and Cordell, B., Early Alzheimer disease-like histopathology increases in frequency with age in mice transgenic for β-APP751, Proc. Natl. Acad. Sci. USA, 92 (1995) 4402-4406.
43. Hsiao, K.K., Borchelt, D.R., Olson, K., Johannsdottir, R., Kitt, C., Yunis, W., Xu, S., Eckman, C., Younkin, S. and Price, D., Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins, Neuron, 15 (1995) 1203-1218.
44. Ishihara, A., Saito, H. and Abe, K., Transforming growth factor-β1 and -β2 promote neurite sprouting and elongation of cultured rat hippocampal neurons, Brain Res., 639 (1994) 21-25.
45. Kalaria, R.N., Bhatti, S.U., Lust, W.D. and Perry, G., The amyloid precursor protein in ischemic brain injury and chronic hypoperfusion, Ann. NY Acad. Sci., 695 (1993) 190-193.
46. Kim, S.J., Park, K., Rudkin, B.B., Dey, B.R., Sporn, M.B. and Roberts, A.B., Nerve growth factor induces transcription of transforming growth factor-β1 through a specific promoter element in PC12 cells, J. Biol. Chem., 269 (1994) 3739-3744.
47. Koh, J., Yang, L.L. and Cotman, C.W., Beta-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage, Brain Res., 533 (1990) 315-320.
48. Kolesnick, R. and Golde, D.W., The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling, Cell, 77 (1994) 325-328.
49. Koo, E.H., Sisodia, S.S., Archer, D.R., Martin, L.J., Weidemann, A., Beyreuther, K., Fischer, P., Masters, C.L. and Price, D.L., Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport, Proc. Natl. Acad. Sci. USA, 87 (1990) 1561-1565.
50. Krieglstein, K., Rufer, M., Suter-Crazzolara, C. and Unsicker, K., Neural functions of the transforming growth factors β, Int. J. Neurosci., 13 (1995) 1-15.
51. + toxicity, EMBO J., 14 (1995) 736-742.
52. LaFerla, F.M., Tinkle, B.T., Bieberich, C.J., Haudenschild, C.C. and Jay, G., The Alzheimer's Aβ peptide induces neurodegeneration and apoptotic cell death in transgenic mice, Nature Genet., 9 (1995) 21-30.
53. Lannfelt, L., Basun, H., Wahlund, L.O., Rowe, B.A. and Wagner, S.L., Decreased α-secretase-cleaved amyloid precursor protein as a diagnostic marker for Alzheimer's disease, Nature Med., 1 (1995) 829-832.
54. Lehrmann, E., Kiefer, R., Finsen, B., Diemer, N.H., Zimmer, J. and Hartung, H.P., Cytokines in cerebral ischemia: expression of transforming growth factor β-1 (TGF-β1) mRNA in the postischemic adult rat hippocampus, Exp. Neurol., 131 (1995) 114-123.
55. Lin, L.-F.H., Doherty, D.H., Lile, J.D., Bektesh, S. and Collins, F., GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons, Science, 260 (1993) 1130-1132.
56. Lindholm, D., Castren, E., Kiefer, R., Zafra, F. and Thoenen, H., Transforming growth factor-β1 in the rat brain: increase after injury and inhibition of astrocyte proliferation, J. Cell Biol., 117 (1992) 395-400.
57. Liu, T., Clark, R.K., McDonnell, P.C., Young, P.R., White, M.S., Barone, F.C. and Feuerstein, G.Z., Tumor necrosis factor-α expression in ischemic neurons, Stroke, 25 (1994) 1481-1488.
58. Löffler, J. and Huber, G., β-Amyloid precursor protein isoforms in various rat brain regions and during brain development, J. Neurochem., 59 (1992) 1316-1324.
59. Lorenzo, A. and Yankner, B.A., β-Amyloid neurotoxicity requires fibril formation and is inhibited by Congo red, Proc. Natl. Acad. Sci. USA, 91 (1994) 12243-12247.
60. Louis, J.C., Magal, E., Takayama, S. and Varon, S., CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death, Science, 259 (1993) 689-692.
61. 2+ homeostasis and cell death, J. Neurosci., 15 (1995) 6239-6249.
62. Martinou, J.-C., Thai, L.V.A., Valette, A. and Weber, J.M., Transforming growth factor β is a potent survival factor for rat embryo motoneurons in culture, Dev. Brain Res., 52 (1990) 175-181.
63. Mattson, M.P., Cheng, B., Culwell, A., Esch, F., Lieberburg, I. and Rydel, R.E., Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of β-amyloid precursor protein, Neuron, 10 (1993) 243-254.
64. Mattson, M.P., Barger, S.W., Cheng, B., Lieberburg, I., Smith-Swintosky, V.L. and Rydel, R.E., β-Amyloid precursor protein metabolites and loss of neuronal calcium homeostasis in Alzheimer's disease, Trends Neurosci., 16 (1993) 409-415.
65. Mattson, M.P. and Scheff, S.W., Endogenous neuroprotection factors and traumatic brain injury: mechanisms of action and implications for therapy, J. Neurotrauma, 11 (1994) 3-33.
66. McCartney-Francis, N.L. and Wahl, S., Transforming growth factor β: a matter of life and death, J. Leukoc. Biol., 55 (1994) 401-409.
67. McGeer, P.L. and Rogers, J., Anti-inflammatory agents as a therapeutic approach to Alzheimer's disease, Neurology, 42 (1992) 447-449.
68. McKinnon, R.D., Piras, G., Ida, J.A. Jr. and Dubois-Dalcq, M., A role for TGF-β in oligodendrocyte differentiation, J. Cell Biol., 121 (1993) 1397-1407.
69. 1 after hypoxic/ischemic brain injury, NeuroReport, 5 (1994) 901-904.
70. Meda, L., Cassatella, M.A., Szendrei, G.I., Otvos, L. Jr., Baron, P., Villalba, M., Ferrari, D. and Rossi, F., Activation of microglial cells by β-amyloid protein and interferon-γ, Nature, 374 (1995) 647-650.
71. Miyazono, K., Dijke, P., Yamashita, H. and Heldin, C.H., Signal transduction via serine/threonine kinase receptors, Semin. Cell Biol., 5 (1994) 389-398.
72. Monning, U., Sandbrink, R., Banati, R.B., Masters, C.L. and Beyreuther, K., Transforming growth factor beta mediates increase of mature transmembrane amyloid precursor protein in microglial cells, FEBS Lett., 342 (1994) 267-272.
73. Mucke, L., Masliah, E., Johnson, W.B., Ruppe, M.D., Alford, M., Rockenstein, E.M., Forss-Petter, S., Pietropaolo, M., Mallory, M. and Abraham, C.R., Synaptotrophic effects of human amyloid β protein precursors in the cortex of transgenic mice, Brain Res., 666 (1994) 151-167.
74. Mucke, L., Abraham, C.R., Ruppe, M.D., Rockenstein, E.M., Toggas, S.M., Mallory, M., Alford, M. and Masliah, E., Protection against HIV-1 gp120-induced brain damage by neuronal expression of human amyloid precursor protein, J. Exp. Med., 181 (1995) 1551-1556.
75. Mucke, L., Abraham, C.R. and Masliah, E., Neurotrophic and neuroprotective effects of human APP in transgenic mice, Ann. NY Acad. Sci., 777 (1995) 82-89.
76. Muller, U., Cristina, N., Li, Z.W., Wolfer, D.P., Lipp, H.P., Rulicke, T., Brandner, S., Aguzzi, A. and Weissmann, C., Behavioral and anatomical deficits in mice homozygous for a modified β-amyloid precursor protein gene, Cell, 79 (1994) 755-765.
77. Nichols, N.R., Laping, N.J., Day, J.R. and Finch, C.E., Increases in transforming growth factor-β mRNA in hippocampus during response to entorhinal cortex lesions in intact and adrenalectomized rats, J. Neurosci. Res., 28 (1991) 134-139.
78. Ninomiya, H., Roch, J. and Saitoh, T., Secreted form of amyloid β/A4 protein precursor (APP) binds to two distinct APP binding sites on rat B103 neuron-like cells through two different domains, but only one site is involved in neuritotropic activity, J. Neurochem., 63 (1994) 495-500.
79. Nitsch, R.M., Farber, S.A., Growdon, J.H. and Wurtman, R.J., Release of amyloid β-protein precursor derivatives by electrical depolarization of rat hippocampal slices, Proc. Natl. Acad. Sci. USA, 90 (1993) 5191-5193.
80. Odekon, L.E., Blasi, F. and Rifkin, D.B., Requirement for receptor-bound urokinase in plasmin-dependent cellular conversion of latent TGF-β to TGF-β, J. Cell. Biol., 158 (1994) 398-407.
81. Ohata, M., Kitamoto, T., Iwaki, T., Ohgami, T., Fukui, M. and Tateishi, J., Immunohistochemical distribution of amyloid precursor protein during normal rat development, Dev. Brain Res., 75 (1993) 151-161.
82. Pfeffer, K., Matsutama, T., Kundig, T.M., Wakeham, A., Kishihara, K., Shahinian, A., Wiegmann, K., Ohashi, P.S., Kronke, M. and Mak, T.W., Mice deficient for the 55 kDa tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection, Cell, 73 (1993) 457-467.
83. Pike C.J., Cummings B.J., Monzavi R. and Cotman C.W., β-Amyloid-induced changes in cultured astrocytes parallel reactive astrocytosis associated with senile plaques in Alzheimer's disease, Neuroscience, 63 (1994) 517-531.
84. Pluta, R., Kida, E., Lossinsky, A.S., Golabek, A.A., Mossakowski, M.J. and Wisniewski, H.M., Complete cerebral ischemia with short-term survival in rats induced by cardiac arrest. I. Extracellular accumulation of Alzheimer's β-amyloid protein precursor in the brain, Brain Res., 649 (1994) 323-328.
85. Prehn, J.H.M., Backhaub, C. and Krieglstein, J., Transforming growth factor-β1 prevents glutamate neurotoxicity in rat neocortical cultures and protects mouse from ischemic injury in vivo, J. Cereb. Blood Flow Metab., 13 (1993) 521-525.
86. Prehn, J.H., Bindokas, V.P., Marcuccilli, C.J., Krajewski, S., Reed, J.C. and Miller, R.J., Regulation of neuronal Bcl-2 protein expression and calcium homeostasis by transforming growth factor type beta confers wide-ranging protection on rat hippocampal neurons, Proc. Natl. Acad. Sci. USA, 91 (1994) 12599-12603.
87. Price, D.L. and Sisodia, S.S., Cellular and molecular biology of Alzheimer's disease and animal models, Annu. Rev. Med., 45 (1994) 435-446.
88. Quitschke, W.W., Two nuclear factor binding domains activate expression from the human amyloid β-protein precursor promoter, J. Biol. Chem., 269 (1994) 21229-21233.
89. Quon, D., Wang, Y., Catalano, R., Scardina, J.M., Murakami, K. and Cordell, B., Formation of β-amyloid protein deposits in brains of transgenic mice, Nature, 352 (1991) 239-241.
90. Roberts, A.B. and Sporn, M.B., Handbk. Exp. Pharmacol, 25 (1990) 419-472.
91. Roch, J.M., Masliah, E., Roch-Levecq, A.C., Sundsmo, M.P., Otero, D.A., Veinbergs, I. and Saitoh, T., Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid β/A4 protein precursor, Proc. Natl. Acad. Sci. USA, 91 (1994) 7450-7454.
92. Rockenstein, E., McConlogue, L., Tan, H., Gordon, M., Power, M., Masliah, E. and Mucke, L., Levels and alternative splicing of amyloid β protein precursor (APP) transcripts in brains of APP transgenic mice and humans with Alzheimer's disease, J. Biol. Chem., 270 (1995) 28257-28267.
93. Rothe, J., Gehr, G., Loetscher, H. Lesslauer, W., Tumor necrosis factor receptors-structure and function, Immunol. Res., 11 (1992) 81-90.
94. Rothe, M., Pan, M.-G., Henzel, W.J., Ayres, T.M. and Goeddel, D.V., The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins, Cell, 83 (1995) 1243-1252.
95. Rothwell, N.J. and Hopkins, S.J., Cytokines and the nervous system II: actions and mechanisms of action, Trends Neurosci., 18 (1995) 130-136.
96. Schubert, D. and Behl, C., The expression of amyloid β protein precursor protects nerve cells from β-amyloid and glutamate toxicity and alters their interaction with the extracellular matrix, Brain Res., 629 (1993) 275-282.
97. Schubert, W., Prior, R., Weidemann, A., Dircksen, H., Multhaup, G., Masters, C.L. and Beyreuther, K., Localization of Alzheimer βA4 amyloid at presynaptic terminals, Brain Res., 563 (1991) 184-194.
98. Schwartz, M., Solomon, A., Lavie, V., Ben-Bassat, S., Belkin, M. and Cohen, A., Tumor necrosis factor facilitates regeneration of injured central nervous system axons, Brain Res., 545 (1991) 334-338.
99. Selkoe, D.J., Cell biology of the amyloid β-protein precursor and the mechanism of Alzheimer's disease, Annu. Rev. Cell Biol., 10 (1994) 373-403.
100. Seroogy, B.K., Lundgren, H.K., Lee, C.D., Guthrie, M.K. and Gall, M.C., Cellular localization of transforming growth factor-α mRNA in rat forebrain, J. Neurochem., 60 (1993) 1777-1782.
101. Siman, R., Card, J.P., Nelson, R.B. and Davis, L.G., Expression of β-amyloid precursor protein in reactive astrocytes following neuronal damage, Neuron, 3 (1989) 275-285.
102. Smith, C.A., Farrah, T. and Goodwin, R.G., The TNF receptor superfamily of cellular and viral proteins: activation, costimulation, and death, Cell, 76 (1994) 959-962.
103. Smith, M.A., Sayre, L.M., Monnier, V.M. and Perry, G., Radical AGEing in Alzheimer's disease, Trends Neurosci., 18 (1995) 172-176.
104. Smith-Swintosky, V.L., Pettigrew, L.C., Craddock, S.D., Culwell, A.R., Rydel, R.E. and Mattson, M.P., Secreted forms of β-amyloid precursor protein protect against ischemic brain injury, J. Neurochem., 63 (1994) 781-784.
105. Suzumura, A., Sawada, M., Yamamoto, H. and Marunouchi, T., Transforming growth factor-β suppresses activation and proliferation of microglia in vitro, J. Immunol., 151 (1993) 2150-2158.
106. Tartaglia, L.A., Weber, R.F., Figari, I.S., Reynolds, C., Palladino, M.A. and Goeddel, D.V., The two different receptors for tumor necrosis factor mediate distinct cellular responses, Proc. Natl. Acad. Sci. USA, 88 (1991) 9292-9296.
107. Toggas, S.M., Masliah, E. and Mucke, L., Prevention of HIβ-1 gp120-induced neuronal damage in the central nervous system of transgenic mice by the NMDA receptor antagonist memantine, Brain Res., 706 (1996) 303-307.
108. Tran-Thi, T.A., Decker, K. and Baeuerle, P.A., Differential activation of transcription factors NF-kappa B and AP-1 in rat liver macrophages, Hepatology, 22 (1995) 613-619.
109. Trejo, J., Massamiri, T., Deng, T., Dewji, N.N., Bayney, R.M. and Brown, J.H., A direct role for protein kinase C and the transcription factor Jun/AP-1 in the regulation of the Alzheimer's β-amyloid precursor protein gene, J. Biol Chem., 269 (1994) 21682-92160.
110. Van der Wal, E.A., Gomez-Pinilla, F. and Cotman, C.W., Transforming growth factor-β1 is in plaques in Alzheimer and Down pathologies, NeuroReport, 4 (1993) 69-72.
111. Wallace, W., Ahlers, S.T., Gotlib, J., Bragin, V., Sugar, J., Gluck, R., Shea, P.A., Davis, K.L. and Haroutunian, V., Amyloid precursor protein in the cerebral cortex is rapidly and persistently induced by loss of subcortical innervation, Proc. Natl. Acad. Sci. USA, 90 (1993) 8712-8716.
112. Wang, X., Yue, T.-L., White, R.F., Barone, F.C. and Feuerstein, G.Z., Transforming growth factor-β1 exhibits delayed gene expression following focal cerebral ischemia, Brain Res. Bull., 36 (1995) 607-609.
113. Warner, B.B., Burhans, M.S., Clark, J.C. and Wispe, J.R., Tumor necrosis factor-α increases Mn-SOD expression: protection against oxidant injury, Am. J. Physiol., 260 (1991) 296-301.
114. Wasco, W., Gurubhagavatula, S., Paradis, M.D., Romano, D.M., Sisodia, S.S., Hyman, B.T., Neve, R.L. and Tanzi, R.E., Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid beta protein precursor, Nature Genet., 5 (1993) 95-100.
115. Wiedau-Pazos, M., Goto, J.J., Rabizadeh, S., Gralla, E.B., Roe, J.A., Lee, M.K., Valentine, J.S. and Bredesen, D.E., Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis, Science, 271 (1996) 515-518.
116. Wong, G.H., Protective roles of cytokines against radiation: induction of mitochondrial MnSOD, Biochim. Biophys. Acta, 1271 (1995) 205-209.
117. Wyss-Coray, T., Feng, L., Masliah, E., Ruppe, M.D., Lee, H.S., Toggas, S.M., Rockenstein, E.M. and Mucke, L., Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-β1, Am. J. Pathol., 147 (1995) 53-67.
118. Younkin, S.G., The amyloid β protein precursor mutations linked to familial Alzheimer's disease alter processing in a way that fosters amyloid deposition, Tohoku J. Exp. Med., 174 (1994) 217-223.
119. Zheng, L., Fisher, G., Miller, R.E., Peschon, J., Lynch, D.H. and Lenardo, M.J., Induction of apoptosis in mature T cells by tumour necrosis factor, Nature, 377 (1995) 348-351.
120. Zheng, H., Jiang, M., Trumbauer, M.E., Sirinathsinghji, D.J.S., Hopkins, R., Smith, D.W., Heavens, R.P., Conner, M.W., Stevens, K.A., Slunt, H.H., Sisodia, S.S., Chen, H.Y. and Van der Ploeg, L.H.T., β-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity, Cell, 81 (1995) 525-531.