Oxidative stress, perturbed calcium homeostasis, and immune dysfunction in Alzheimer's disease

Journal of NeuroVirology

Volumn 8, Issue 6, 2002, Pages 539-550

  Mattson, Mark P ^a,b  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Apoptosis; Inositol trisphosphate; Lymphocytes; Ryanodine

Indexed keywords

3 HYDROXY 3 METHYLGLUTARYL COENZYME A; ALPHA 1 ANTICHYMOTRYPSIN; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; CALCIUM; CD28 ANTIGEN; CD4 ANTIGEN; CD7 ANTIGEN; CD8 ANTIGEN; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; GAMMA INTERFERON; GLUTAMATE TRANSPORTER; GLYCOPROTEIN GP 120; HEAT SHOCK PROTEIN 70; HLA DR ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 6; NEUROTROPHIC FACTOR; NEUROTROPHIN 3; PRESENILIN 1; PRESENILIN 2; PROTEIN BCL 2; RYANODINE RECEPTOR; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR; UNINDEXED DRUG;

ALZHEIMER DISEASE; AMNESIA; BRAIN CORTEX; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CELL LINE; CLINICAL FEATURE; COGNITIVE DEFECT; DEMENTIA; EMOTIONAL DISORDER; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE DEFICIENCY; IMMUNIZATION; IMMUNOCOMPETENT CELL; IMMUNOPATHOGENESIS; LIMBIC SYSTEM; LYMPHOBLAST; LYMPHOCYTE; MICROGLIA; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRION DISEASE; PRIORITY JOURNAL; PROTEIN CONFORMATION; REVIEW; SYMPTOM; VIRUS ENCEPHALITIS;

ALZHEIMER DISEASE; CALCIUM; HOMEOSTASIS; HUMANS; NEUROIMMUNOMODULATION; OXIDATIVE STRESS;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 0036954488     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.1080/13550280290100978     Document Type: Review

References (104)

1. Artavanis-Tsakonis S, Matsuno K, Fortini ME (1995). Notch signaling. Science 268: 225-231.
2. Atwood CS, Huang X, Khatri A, Scarpa RC, Kim YS, Moir RD, Tanzi RE, Roher AE, Bush AI (2000). Copper catalyzed oxidation of Alzheimer Abeta. Cell Mol Biol 46: 777-783.
3. Baker HF, Ridley RM, Duchen LW, Crow TJ, Bruton CJ (1994). Induction of beta (A4)-amyloid in primates by injection of Alzheimer's disease brain homogenate. Comparison with transmission of spongiform encephalopathy. Mol Neurobiol 8: 25-39.
4. Barger SW, Basile AS (2001). Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem 76: 846-854.
5. 2+ accumulation. Proc Natl Acad Sci USA 92: 9328-9332.
6. Barrow PA, Empson RM, Gladwell SJ, Anderson CM, Killick R, Yu X, Jefferys JG, Duff K (2000). Functional phenotype in transgenic mice expressing mutant human presenilin-1. Neurobiol Dis 7: 119-126.
7. Begley JG, Duan W, Chan S, Duff K, Mattson MP (1999). Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice. J Neurochem 72: 1030-1039.
8. Berridge MJ, Lipp P, Bootman MD (2000). The versatility and universality of calcium signaling, Nat Rev Mol Cell Biol 1: 11-21.
9. Blanc EM, Keller JN, Fernandez S, Mattson MP (1998). 4-Hydroxynonenal, a lipid peroxidation product, impairs glutamate transport in cortical astrocytes. Glia 22: 149-160.
10. Bongioanni P, Boccardi B, Borgna M, Castagna M, Mondino C (1997). T-cell interferon gamma binding in patients with dementia of the Alzheimer type. Arch Neurol 54: 457-462.
11. Bongioanni P, Boccardi B, Borgna M, Rossi B (1998). T-lymphocyte interleukin 6 receptor binding in patients with dementia of Alzheimer type. Arch Neurol 55: 1305-1308.
12. 2+ release. J Biol Chem 270: 7257-7260.
13. Brillantes AM, Ondrias BK, Scott A, Kobrinsky E, Ondriasova E, Moschella MC, Jararaman T, Landers M, Ehrlich BE, Marks AR (1994). Stabilization of calcium release channel (ryanodine receptor) function by FK-506 binding protein. Cell 77: 513-523.
14. Bruce-Keller AJ, Umberger G, McFall R, Mattson MP (1999). Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann Neurol 45: 8-15.
15. Bruunsgaard H, Andersen-Ranberg K, Jeune B, Pedersen AN, Skinhoj P, Pedersen BK (1999). A high plasma concentration of TNF-alpha is associated with dementia in centenarians. J Gerontol A Biol Sci Med Sci 54: M357-M364.
16. Butterfield DA, Drake J, Pocernich C, Castegna A (2001). Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol Med 7: 548-554.
17. Buxbaum JD, Choi EK, Luo Y, Lilliehook C, Crowley AC, Merriam DE, Wasco W (1998). Calsenilin: a calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment. Nat Med 4: 1177-1181.
18. 2+ flux. Cell 83: 463-472.
19. Cecchi C, Latorraca S, Sorbi S, Iantomasi T, Favilli F, Vincenzini MT, Liguri G (1999). Gluthatione level is altered in lymphoblasts from patients with familial Alzheimer's disease. Neurosci Lett 275: 152-154.
20. Chan SL, Mayne M, Holden CP, Geiger JD, Mattson MP (2000). Presenilin-1 mutations increase levels of ryanodine receptors and calcium release in PC12 cells and cortical neurons. J Biol Chem 275: 18195-18200.
21. 2+ and synaptic plasticity. Cell Calcium 24: 377-385.
22. Conlon RA, Reaume AG, Rossant J (1995). Notch 1 is required for the coordinate segmentation of somites. Development 121: 1533-1542.
23. Cruz-Sanchez F, Lafuente J, Figols J, Cervos-Navarro J (1988). Topographic analysis of neuropathologic findings in 16 cases of Creutzfeldt-Jacob disease. Arch Neurobiol (Madr) 51: 191-196.
24. Culmsee C, Zhu Z, Yu QS, Chan SL, Camandola S, Guo Z, Greig N, Mattson MP (2001). A synthetic inhibitor of p53 protects neurons against death induced by ischemic and excitotoxic insults, and amyloid β-peptide. J Neurochem 77: 220-228.
25. D'Adamio L, Lacana E, Vito P (1997). Functional cloning of genes involved in T-cell receptor-induced programmed cell death. Semin Immunol 9: 17-23.
26. DiCarlo G, Wilcock D, Henderson D, Gordon M, Morgan D (2001). Intrahippocampal LPS injections reduce Aβ load in APP+PS1 transgenic mice. Neurobiol Aging 22: 1007-1012.
27. Duan W, Mattson MP (1999). Dietary restriction and 2-deoxyglucose administration improve behavioral outcome and reduce degeneration of dopaminergic neurons in models of Parkinson's disease. J Neurosci Res 57: 195-206.
28. Eckert A, Forstl H, Zerfass R, Hartmann H, Muller WE (1996). Lymphocytes and neutrophils as peripheral models to study the effect of beta-amyloid on cellular calcium signalling in Alzheimer's disease. Life Sci 59: 499-510.
29. Eckert A, Schindowski K, Leutner S, Luckhaus C, Touchet N, Czech C, Muller WE (2001). Alzheimer's disease-like alterations in peripheral cells from presenilin-1 transgenic mice. Neurobiol Dis 8: 331-342.
30. Evans DA, Hebert LE, Beckett LA, Scherr PA, Albert MS, Chown MJ, Pilgrim DM, Taylor JO (1997). Education and other measures of socioeconomic status and risk of incident Alzheimer disease in a defined population of older persons. Arch Neurol 54: 1399-1405.
31. Fazakerley JK, Allsopp TE (2001). Programmed cell death in virus infections of the nervous system. Curr Top Microbiol Immunol 253: 95-119.
32. Flescher E, Ledbetter JA, Schieven GL, Vela-Roch N, Fossum D, Dang H, Ogawa N, Talal N (1994). Longitudinal exposure of human T lymphocytes to weak oxidative stress suppresses transmembrane and nuclear signal transduction. J Immunol 153: 4880-4889.
33. Galasko D, Hansen LA, Katzman R, Wiederholt W, Masliah E, Terry R, Hill LR, Lessin P, Thal LJ (1994). Clinical-neuropathological correlations in Alzheimer's disease and related dementias. Arch Neurol 51: 888-895.
34. Giese A, Kretzschmar HA (2001). Prion-induced neuronal damage-the mechanisms of neuronal destruction in the subacute spongiform encephalopathies. Curr Top Microbiol Immunol 253: 203-217.
35. 4+ lymphocytes in Alzheimer's disease and in older persons with Down's syndrome. Neurobiol Aging 14: 177-185.
36. Guo Q, Christakos S, Robinson N, Mattson MP (1998a). Calbindin D28k blocks the proapoptotic actions of mutant presenilin 1: reduced oxidative stress and preserved mitochondrial function. Proc Natl Acad Sci USA 95: 3227-3232.
37. Guo Q, Fu W, Sopher BL, Miller MW, Ware CB, Martin GM, Mattson MP (1999). Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knockin mice. Nat Med 5: 101-107.
38. Guo Q, Furukawa K, Sopher BL, Pham DG, Robinson N, Martin GM, Mattson MP (1996). Alzheimer's PS-1 mutation perturbs calcium homeostasis and sensitizes PC12 cells to death induced by amyloid β-peptide. NeuroReport 8: 379-383.
39. Guo Q, Robinson N, Mattson MP (1998b). Secreted beta-amyloid precursor protein counteracts the proapoptotic action of mutant presenilin-1 by activation of NF-κB and stabilization of calcium homeostasis. J Biol Chem 273: 12341-12351.
40. Guo Q, Sopher BL, Pham DG, Furukawa K, Robinson N, Martin GM, Mattson MP (1997). Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid β-peptide. J Neurosci 17: 4212-4222.
41. 2+ signaling in T-lymphocytes. Crit Rev Immunol 18: 419-448.
42. Handler M, Yang X, Shen J (2000). Presenilin-1 regulates neuronal differentiation during neurogenesis. Development 127: 2593-2606.
43. Hardy J (1997). Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci 20: 154-159.
44. 2+ homeostasis in lymphoblasts from patients with late onset Alzheimer disease. Alzheimer Dis Assoc Disord 11: 220-227.
45. Ibarreta D, Urcelay E, Parrilla R, Ayuso MS (1998). Distinct pH homeostatic features in lymphoblasts from Alzheimer's disease patients. Ann Neurol 44: 216-222.
46. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, Chishti MA, Horne P, Heslin D, French J, Mount HT, Nixon RA, Mercken M, Bergeron C, Fraser PE, St George-Hyslop P, Westaway D (2000). A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408: 979-982.
47. Karlsson JO, Blennow K, Janson I, Blomgren K, Karlsson I, Regland B, Wallin A, Gottfries CG (1995). Increased proteolytic activity in lymphocytes from patients with early onset Alzheimer's disease. Neurobiol Aging 16: 901-906.
48. Khan AA, Soloski MJ, Sharp AH, Schilling G, Sabatini DM, Li SH, Ross CA, Snyder SH (1996). Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor. Science 273: 503-507.
49. Kim WK, Ko KH (1998). Potentiation of N-methyl-D-aspartate-mediated neurotoxicity by immunostimulated murine microglia. J Neurosci Res 54: 17-26.
50. Kruman II, Nath A, Mattson MP (1998). HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp Neurol 154: 276-288.
51. Lanzrein AS, Johnston CM, Perry VH, Jobst KA, King EM, Smith AD (1998). Longitudinal study of inflammatory factors in serum, cerebrospinal fluid, and brain tissue in Alzheimer disease: interleukin-1beta, interleukin-6, interleukin-1 receptor antagonist, tumor necrosis factor-alpha, the soluble tumor necrosis factor receptors I and II, and alpha 1-antichymotrypsin. Alzheimer Dis Assoc Disord 12: 215-227.
52. Lee J, Chan SL, Taub DH, Camandola S, Mattson MP (2001). Induction of inflammatory cytokines is potentiated in the brains of presenilin-1 mutant knock-in mice. Soc Neurosci Abstr 27: Program number 860.4.
53. Lee J, Duan W, Long JM, Ingram DK, Mattson MP (2000). Dietary restriction increases survival of newly-generated neural cells and induces BDNF expression in the dentate gyrus of rats. J Mol Neurosci 15: 99-108.
54. Lee J, Seroogy KB, Mattson MP (2002). Dietary restriction enhances neurotrophin production and neurogenesis in the hippocampus of adult mice. J Neurochem 80: 539-547.
55. Leissring MA, Akbari Y, Fanger CM, Cahalan MD, Mattson MP, LaFerla FM (2000a). Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J Cell Biol 149: 793-798.
56. Leissring MA, Yamasaki TR, Wasco W, Buxbaum JD, Parker I, LaFerla FM (2000b). Calsenilin reverses presenilin-mediated enhancement of calcium signaling. Proc Natl Acad Sci USA 97: 8590-8593.
57. Lewis RS (2001). Calcium signaling mechanisms in T lymphocytes. Annu Rev Immunol 19: 497-521.
58. Licastro F, Pedrini S, Caputo L, Annoni G, Davis LJ, Ferri C, Casadei V, Grimaldi LM (2000). Increased plasma levels of interleukin-1, interleukin-6 and alpha1-antichymotrypsin in patients with Alzheimer's disease: peripheral inflammation or signals from the brain? J Neuroimmunol 103: 97-102.
59. Lipton SA (1998). Neuronal injury associated with HIV-1: approaches to treatment. Annu Rev Pharmacol Toxicol 38: 159-177.
60. Lombardi VR, Garcia M, Rey L, Cacabelos R (1999). Characterization of cytokine production, screening of lymphocyte subset patterns and in vitro apoptosis in healthy and Alzheimer's Disease (AD) individuals. J Neuroimmunol 97: 163-171.
61. Lukiw WJ, Bazan NG (2000). Neuroinflammatory signaling upregulation in Alzheimer's disease. Neurochem Res 25: 1173-1184.
62. Lye TC, Shores EA (2000). Traumatic brain injury as a risk factor for Alzheimer's disease: a review. Neuropsychol Rev 10: 115-129.
63. 2+ homeostasis and cell death. J Neurosci 15: 6239-6249.
64. Mark RJ, Pang Z, Geddes JW, Mattson MP (1997). Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: Involvement of membrane lipid peroxidation. J Neurosci 17: 1046-1054.
65. Maruyama K, Usami M, Kametani F, Tomita T, Iwatsubo T, Saido TC, Mori H, Ishiura S (2000). Molecular interactions between presenilin and calpain: inhibition of m-calpain protease activity by presenilin-1, -2 and cleavage of presenilin-1 by m-, mu-calpain. Int J Mol Med 5: 269-273.
66. Masters CL, Beyreuther K (1988). Neuropathology of unconventional virus infections: molecular pathology of spongiform change and amyloid plaque deposition. Ciba Found Symp 135: 24-36.
67. 2+ influx in cultured hippocampal neurons. Neuron 4: 105-117.
68. Mattson MP (1997). Cellular actions of β-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol Rev 77: 1081-1132.
69. Mattson MP (2000). Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 1: 120-129.
70. Mattson MP, Begley JG, Mark RJ, Furukawa K (1997b). Abeta25-35 induces rapid lysis of red blood cells: contrast with Abeta1-42 and examination of underlying mechanisms. Brain Res 771: 147-153.
71. Mattson MP, Cheng B, Culwell AR, Esch FS, Lieberburg I, Rydel RE (1993). Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein. Neuron 10: 243-254.
72. Mattson MP, Goodman Y, Luo H, Fu W, Furukawa K (1997). Activation of NF-kappaB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of manganese superoxide dismutase and suppression of peroxynitrite production and protein tyrosine nitration. J Neurosci Res 49: 681-697.
73. Mayeux R, Costa R, Bell K, Merchant C, Tung MX, Jacobs D (1999). Reduced risk of Alzheimer's disease among individuals with low calorie intake. Neurology 59: S296-S297.
74. McGeer EG, McGeer PL (1999). Brain inflammation in Alzheimer disease and the therapeutic implications. Curr Pharm Des 5: 821-836.
75. Mecocci P, Polidori MC, Ingegni T, Cherubini A, Chionne F, Cecchetti R, Senin U (1998). Oxidative damage to DNA in lymphocytes from AD patients. Neurology 51: 1014-1017.
76. Morgan D, Diamond DM, Gottschall PE, Ugen KE, Dickey C, Hardy J, Duff K, Jantzen P, DiCarlo G, Wilcock D, Connor K, Hatcher J, Hope C, Gordon M, Arendash GW (2000). A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 408: 982-985.
77. Morocz M, Kalman J, Juhasz A, Sinko I, McGlynn AP, Downes CS, Janka Z, Rasko I (2002). Elevated levels of oxidative DNA damage in lymphocytes from patients with Alzheimer's disease. Neurobiol Aging 23: 47-53.
78. Mrak RE, Griffin WS (2001). Interleukin-1, neuroinflammation, and Alzheimer's disease. Neurobiol Aging 22: 903-908.
79. Nath A (1999). Pathobiology of human immunodeficiency virus dementia. Semin Neurol 19: 113-127.
80. Osborne B, Miele L (1999). Notch and the immune system. Immunity 11: 653-663.
81. Pack-Chung E, Meyers MB, Pettingell WP, Moir RD, Brownawell AM, Cheng I, Tanzi RE, Kim TW (2000). Presenilin 2 interacts with sorcin, a modulator of the ryanodine receptor. J Biol Chem 275: 14440-14445.
82. Papassotiropoulos A, Bagli M, Jessen F, Bayer TA, Maier W, Rao ML, Heun R (1999). A genetic variation of the inflammatory cytokine interleukin-6 delays the initial onset and reduces the risk for sporadic Alzheimer's disease. Ann Neurol 45: 666-668.
83. Parent A, Linden DJ, Sisodia SS, Borchelt DR (1999). Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol Dis 6: 56-62.
84. Pickel VM, Clarke CL, Meyers MB (1997). Ultrastructural localization of sorcin, a 22 kDa calcium binding protein, in the rat caudate-putamen nucleus: association with ryanodine receptors and intracellular calcium release. J Comp Neurol 386: 625-634.
85. Prusiner SB (2001). Shattuck lecture-neurodegenerative diseases and prions. N Engl J Med 344: 1516-1526.
86. Rausch DM, Davis MR (2001). HIV in the CNS: pathogenic relationships to systemic HIV disease and other CNS diseases. J Neuro Virol 7: 85-96.
87. Rogers J, Cooper NR, Webster S, Schultz J, McGeer PL, Styren SD, Civin WH, Brachova L, Bradt B, Ward P, Lieberburg I (1992). Complement activation by beta-amyloid in Alzheimer disease. Proc Natl Acad Sci USA 89: 10016-10020.
88. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P (1999). Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400: 173-177.
89. Shalit F, Sredni B, Brodie C, Kott E, Huberman M (1995). T lymphocyte subpopulations and activation markers correlate with severity of Alzheimer's disease. Clin Immunol Immunopathol 75: 246-250.
90. Shen J, Bronson RT, Chen DF, Xia W, Selkoe DJ, Tonegawa S (1997). Skeletal and CNS defects in presenilin-1-deficient mice. Cell 89: 629-639.
91. Solerte SB, Fioravanti M, Pascale A, Ferrari E, Govoni S, Battaini F (1998). Increased natural killer cell cytotoxicity in Alzheimer's disease may involve protein kinase C dysregulation. Neurobiol Aging 19: 191-199.
92. Song C, Vandewoude M, Stevens W, De Clerck L, Van der Planken M, Whelan A, Anisman H, Dossche A, Maes M (1999). Alterations in immune functions during normal aging and Alzheimer's disease. Psychiatry Res 85: 71-80.
93. Stabler SM, Ostrowski LL, Janicki SM, Monteiro MJ (1999). A myristoylated calcium-binding protein that preferentially interacts with the Alzheimer's disease presenilin 2 protein. J Cell Biol 145: 1277-1292.
94. Struhl G, Greenwald I (2001). Presenilin-mediated transmembrane cleavage is required for Notch signal transduction in Drosophila. Proc Natl Acad Sci USA 98: 229-234.
95. Sulger J, Dumais-Huber C, Zerfass R, Henn FA, Aldenhoff JB (1999). The calcium response of human T lymphocytes is decreased in aging but increased in Alzheimer's dementia. Biol Psychiatry 45: 737-742.
96. Takahashi H, Mercken M, Honda T, Saito Y, Murayama M, Song S, Takashima A (1999). Impaired proteolytic processing of presenilin-1 in chromosome 14-linked familial Alzheimer's disease patient lymphocytes. Neurosci Lett 260: 121-124.
97. Ueki A, Shinjo H, Shimode H, Nakajima T, Morita Y (2001). Factors associated with mortality in patients with early-onset Alzheimer's disease: a five-year longitudinal study. Int J Geriatr Psychiatry 16: 810-815.
98. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, Collins F, Treanor J, Rogers G, Citron M (1999). Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735-741.
99. Webster S, Glabe C, Rogers J (1995). Multivalent binding of complement protein C1Q to the amyloid beta-peptide (A beta) promotes the nucleation phase of A beta aggregation. Biochem Biophys Res Commun 217: 869-875.
100. Williams R, Lendahl U, Lardelli M (1995). Complementary and combinatorial patterns of Notch gene family expression during early mouse development. Mech Dev 53: 357-368.
101. Yamada M, Miyawaki A, Saito K, Nakajima T, Yamamoto-Hino M, Ryo Y, Furuichi T, Mikoshiba K (1995). The calmodulin-binding domain in the mouse type 1 inositol 1,4,5-trisphosphate receptor. Biochem J 308: 83-88.
102. Yasojima K, Schwab C, McGeer EG, McGeer PL (2000). Human neurons generate C-reactive protein and amyloid P: upregulation in Alzheimer's disease. Brain Res 887: 80-89.
103. Yoo AS, Cheng I, Chung S, Grenfell TZ, Lee H, Pack-Chung E, Handler M, Shen J, Xia W, Tesco G, Saunders AJ, Ding K, Frosch MP, RE, Kim TW (2000). Presenilin-mediated modulation of capacitative calcium entry. Neuron 27: 561-572.
104. YU ZF, Mattson MP (1999). Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J Neurosci Res 57: 830-839.