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Science 12 October 1990:
Vol. 250. no. 4978, pp. 279 - 282
DOI: 10.1126/science.2218531
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Articles

Science, Vol 250, Issue 4978, 279-282
Copyright © 1990 by American Association for the Advancement of Science

articles

Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides

BA Yankner, LK Duffy, and DA Kirschner

Department of Neurology, Harvard Medical School, Boston, MA 02115.

The amyloid beta protein is deposited in the brains of patients with Alzheimer's disease but its pathogenic role is unknown. In culture, the amyloid beta protein was neurotrophic to undifferentiated hippocampal neurons at low concentrations and neurotoxic to mature neurons at higher concentrations. In differentiated neurons, amyloid beta protein caused dendritic and axonal retraction followed by neuronal death. A portion of the amyloid beta protein (amino acids 25 to 35) mediated both the trophic and toxic effects and was homologous to the tachykinin neuropeptide family. The effects of the amyloid beta protein were mimicked by tachykinin antagonists and completely reversed by specific tachykinin agonists. Thus, the amyloid beta protein could function as a neurotrophic factor for differentiating neurons, but at high concentrations in mature neurons, as in Alzheimer's disease, could cause neuronal degeneration.


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B. Urbanc, L. Cruz, R. Le, J. Sanders, K. H. Ashe, K. Duff, H. E. Stanley, M. C. Irizarry, and B. T. Hyman (2002)
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N. ARISPE and M. DOH (2002)
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Inhibition of amyloid-beta aggregation and caspase-3 activation by the Ginkgo biloba extract EGb761.
Y. Luo, J. V. Smith, V. Paramasivam, A. Burdick, K. J. Curry, J. P. Buford, I. Khan, W. J. Netzer, H. Xu, and P. Butko (2002)
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J. Neurosci. 22, 7380-7388
   Abstract »    Full Text »    PDF »
Oligomeric and Fibrillar Species of Amyloid-beta Peptides Differentially Affect Neuronal Viability.
K. N. Dahlgren, A. M. Manelli, W. B. Stine Jr., L. K. Baker, G. A. Krafft, and M. J. LaDu (2002)
J. Biol. Chem. 277, 32046-32053
   Abstract »    Full Text »    PDF »
beta -Amyloid Enhances Glial Glutamate Uptake Activity and Attenuates Synaptic Efficacy.
Y. Ikegaya, S. Matsuura, S. Ueno, A. Baba, M. K. Yamada, N. Nishiyama, and N. Matsuki (2002)
J. Biol. Chem. 277, 32180-32186
   Abstract »    Full Text »    PDF »
Probing solvent accessibility of amyloid fibrils by solution NMR spectroscopy.
J. H. Ippel, A. Olofsson, J. Schleucher, E. Lundgren, and S. S. Wijmenga (2002)
PNAS 99, 8648-8653
   Abstract »    Full Text »    PDF »
A Novel Function of Monomeric Amyloid beta -Protein Serving as an Antioxidant Molecule against Metal-Induced Oxidative Damage.
K. Zou, J.-S. Gong, K. Yanagisawa, and M. Michikawa (2002)
J. Neurosci. 22, 4833-4841
   Abstract »    Full Text »    PDF »
The Tachykinin Peptide Family.
C. Severini, G. Improta, G. Falconieri-Erspamer, S. Salvadori, and V. Erspamer (2002)
Pharmacol. Rev. 54, 285-322
   Abstract »    Full Text »    PDF »
Peroxynitrite Mediates Neurotoxicity of Amyloid beta -Peptide1-42- and Lipopolysaccharide-Activated Microglia.
Z. Xie, M. Wei, T. E. Morgan, P. Fabrizio, D. Han, C. E. Finch, and V. D. Longo (2002)
J. Neurosci. 22, 3484-3492
   Abstract »    Full Text »    PDF »
Neuronal nicotinic acetylcholine receptors: involvement in Alzheimer's disease and schizophrenia..
D. S. Woodruff-Pak and T. J. Gould (2002)
Behav Cogn Neurosci Rev 1, 5-20
   Abstract »    PDF »
Contrasting, Species-Dependent Modulation of Copper-Mediated Neurotoxicity by the Alzheimer's Disease Amyloid Precursor Protein.
A. R. White, G. Multhaup, D. Galatis, W. J. McKinstry, M. W. Parker, R. Pipkorn, K. Beyreuther, C. L. Masters, and R. Cappai (2002)
J. Neurosci. 22, 365-376
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Detailed Characterization of Neuroprotection by a Rescue Factor Humanin against Various Alzheimer's Disease-Relevant Insults.
Y. Hashimoto, T. Niikura, Y. Ito, H. Sudo, M. Hata, E. Arakawa, Y. Abe, Y. Kita, and I. Nishimoto (2001)
J. Neurosci. 21, 9235-9245
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Amyloid {beta} protein forms ion channels: implications for Alzheimer's disease pathophysiology.
H. LIN, R. BHATIA, and R. LAL (2001)
FASEB J 15, 2433-2444
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{beta}-Amyloid Induces Neuronal Apoptosis Via a Mechanism that Involves the c-Jun N-Terminal Kinase Pathway and the Induction of Fas Ligand.
Y. Morishima, Y. Gotoh, J. Zieg, T. Barrett, H. Takano, R. Flavell, R. J. Davis, Y. Shirasaki, and M. E. Greenberg (2001)
J. Neurosci. 21, 7551-7560
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Generation of Aggregated {beta}-Amyloid in the Rat Hippocampus Impairs Synaptic Transmission and Plasticity and Causes Memory Deficits.
A. Stephan, S. Laroche, and S. Davis (2001)
J. Neurosci. 21, 5703-5714
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Activation of Human Macrophages by Amyloid-{{beta}} Is Attenuated by Astrocytes.
H. A. Smits, A. J. van Beelen, N. M. de Vos, A. Rijsmus, T. van der Bruggen, J. Verhoef, F. L. van Muiswinkel, and H. S. L. M. Nottet (2001)
J. Immunol. 166, 6869-6876
   Abstract »    Full Text »    PDF »
Blockade of Long-Term Potentiation by {beta}-Amyloid Peptides in the CA1 Region of the Rat Hippocampus In Vivo.
D. B. Freir, C. Holscher, and C. E. Herron (2001)
J Neurophysiol 85, 708-713
   Abstract »    Full Text »    PDF »
Metal Chelation as a Potential Therapy for Alzheimer's Disease.
M. P. CUAJUNGCO, K. Y. FAGET, X. HUANG, R. E. TANZI, and A. I. BUSH (2000)
Ann. N.Y. Acad. Sci. 920, 292-304
   Abstract »    Full Text »    PDF »
Carboxyl-terminal fragment of Alzheimer's APP destabilizes calcium homeostasis and renders neuronal cells vulnerable to excitotoxicity.
H.-S. KIM, C. H. PARK, S. H. CHA, J.-H. LEE, S. LEE, Y. KIM, J.-C. RAH, S.-J. JEONG, and Y.-H. SUH (2000)
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Fresh and globular amyloid {beta} protein (1-42) induces rapid cellular degeneration: evidence for A{beta}P channel-mediated cellular toxicity.
R. BHATIA, H. LIN, and R. LAL (2000)
FASEB J 14, 1233-1243
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Fresh and nonfibrillar amyloid {beta} protein(1-40) induces rapid cellular degeneration in aged human fibroblasts: evidence for A{beta}P-channel-mediated cellular toxicity.
Y. J. ZHU, H. LIN, and R. LAL (2000)
FASEB J 14, 1244-1254
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Alzheimer's beta -Amyloid, Human Islet Amylin, and Prion Protein Fragment Evoke Intracellular Free Calcium Elevations by a Common Mechanism in a Hypothalamic GnRH Neuronal Cell Line.
M. Kawahara, Y. Kuroda, N. Arispe, and E. Rojas (2000)
J. Biol. Chem. 275, 14077-14083
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E2F1 Mediates Death of B-amyloid-treated Cortical Neurons in a Manner Independent of p53 and Dependent on Bax and Caspase 3.
A. Giovanni, E. Keramaris, E. J. Morris, S. T. Hou, M. O'Hare, N. Dyson, G. S. Robertson, R. S. Slack, and D. S. Park (2000)
J. Biol. Chem. 275, 11553-11560
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{beta}-Amyloid Excitotoxicity in Rat Magnocellular Nucleus Basalis: Effect of Cortical Deafferentation on Cerebral Blood Flow Regulation and Implications for Alzheimer's Disease.
T. HARKANY, B. PENKE, and P. G.M. LUITEN (2000)
Ann. N.Y. Acad. Sci. 903, 374-386
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Proteolytic processing and cell biological functions of the amyloid precursor protein.
B De Strooper and W Annaert (2000)
J. Cell Sci. 113, 1857-1870
   Abstract »    PDF »
The Alzheimer's Disease Amyloid Precursor Protein Modulates Copper-Induced Toxicity and Oxidative Stress in Primary Neuronal Cultures.
A. R. White, G. Multhaup, F. Maher, S. Bellingham, J. Camakaris, H. Zheng, A. I. Bush, K. Beyreuther, C. L. Masters, and R. Cappai (1999)
J. Neurosci. 19, 9170-9179
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Amyloid beta -Protein Fibrillogenesis. STRUCTURE AND BIOLOGICAL ACTIVITY OF PROTOFIBRILLAR INTERMEDIATES.
D. M. Walsh, D. M. Hartley, Y. Kusumoto, Y. Fezoui, M. M. Condron, A. Lomakin, G. B. Benedek, D. J. Selkoe, and D. B. Teplow (1999)
J. Biol. Chem. 274, 25945-25952
   Abstract »    Full Text »    PDF »
Activation of Neuronal Caspase-3 by Intracellular Accumulation of Wild-Type Alzheimer Amyloid Precursor Protein.
T. Uetsuki, K. Takemoto, I. Nishimura, M. Okamoto, M. Niinobe, T. Momoi, M. Miura, and K. Yoshikawa (1999)
J. Neurosci. 19, 6955-6964
   Abstract »    Full Text »    PDF »
Caspase-6 Role in Apoptosis of Human Neurons, Amyloidogenesis, and Alzheimer's Disease.
A. LeBlanc, H. Liu, C. Goodyer, C. Bergeron, and J. Hammond (1999)
J. Biol. Chem. 274, 23426-23436
   Abstract »    Full Text »    PDF »
Inhibition of NF-kappa B potentiates amyloid beta -mediated neuronal apoptosis.
B. Kaltschmidt, M. Uherek, H. Wellmann, B. Volk, and C. Kaltschmidt (1999)
PNAS 96, 9409-9414
   Abstract »    Full Text »    PDF »
Receptor for Advanced Glycation End Products (RAGE)-mediated Neurite Outgrowth and Activation of NF-kappa B Require the Cytoplasmic Domain of the Receptor but Different Downstream Signaling Pathways.
H. J. Huttunen, C. Fages, and H. Rauvala (1999)
J. Biol. Chem. 274, 19919-19924
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Involvement of Cell Cycle Elements, Cyclin-dependent Kinases, pRb, and E2F·DP, in B-amyloid-induced Neuronal Death.
A. Giovanni, F. Wirtz-Brugger, E. Keramaris, R. Slack, and D. S. Park (1999)
J. Biol. Chem. 274, 19011-19016
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beta -Amyloid Activates the Obardot 2 Forming NADPH Oxidase in Microglia, Monocytes, and Neutrophils. A POSSIBLE INFLAMMATORY MECHANISM OF NEURONAL DAMAGE IN ALZHEIMER'S DISEASE.
V. Della Bianca, S. Dusi, E. Bianchini, I. Dal Pra, and F. Rossi (1999)
J. Biol. Chem. 274, 15493-15499
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Amyloid beta  Peptides Do Not Form Peptide-derived Free Radicals Spontaneously, but Can Enhance Metal-catalyzed Oxidation of Hydroxylamines to Nitroxides.
S. I. Dikalov, M. P. Vitek, K. R. Maples, and R. P. Mason (1999)
J. Biol. Chem. 274, 9392-9399
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A ßPP Peptide Carboxyl-Terminal to Aß Is Neurotoxic.
G. Marcon, G. Giaccone, B. Canciani, L. Cajola, G. Rossi, L. De Gioia, M. Salmona, O. Bugiani, and F. Tagliavini (1999)
Am. J. Pathol. 154, 1001-1007
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Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models.
A. Y. Hsia, E. Masliah, L. McConlogue, G.-Q. Yu, G. Tatsuno, K. Hu, D. Kholodenko, R. C. Malenka, R. A. Nicoll, and L. Mucke (1999)
PNAS 96, 3228-3233
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CSF beta-amyloid, cognition, and APOE genotype in Alzheimer's disease.
S. C. Samuels, J. M. Silverman, D. B. Marin, E. R. Peskind, S. G. Younki, D. A. Greenberg, E. Schnur, J. Santoro, and K. L. Davis (1999)
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The Neurobiology and Pharmacotherapy of Alzheimer's Disease.
O. Felician and T. A. Sandson (1999)
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K. J. Ivins, J. K. Ivins, J. P. Sharp, and C. W. Cotman (1999)
J. Biol. Chem. 274, 2107-2112
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Neurotoxicity and Oxidative Damage of Beta Amyloid 1-42 versus Beta Amyloid 1-40 in the Mouse Cerebral Cortex.
A. M. KLEIN, N. W. KOWALL, and R. J. FERRANTE (1999)
Ann. N.Y. Acad. Sci. 893, 314-320
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Chronic Intracerebroventricular Infusion of {beta}-Amyloid (1-40) Results in a Selective Loss of Neuropeptides in Addition to a Reduction in Choline Acetyltransferase Activity in the Cortical Mantle and Hippocampus in the Rat.
S. NAG, B. K. YEE, and F. TANG (1999)
Ann. N.Y. Acad. Sci. 897, 420-422
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Amyloid beta  peptide alters intracellular vesicle trafficking and cholesterol homeostasis.
Y. Liu, D. A. Peterson, and D. Schubert (1998)
PNAS 95, 13266-13271
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Amyloid beta -Peptide Possesses a Transforming Growth Factor-beta Activity.
S. S. Huang, F. W. Huang, J. Xu, S. Chen, C. Y. Hsu, and J. S. Huang (1998)
J. Biol. Chem. 273, 27640-27644
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Protease Inhibitor Coinfusion with Amyloid beta -Protein Results in Enhanced Deposition and Toxicity in Rat Brain.
S. A. Frautschy, D. L. Horn, J. J. Sigel, M. E. Harris-White, J. J. Mendoza, F. Yang, T. C. Saido, and G. M. Cole (1998)
J. Neurosci. 18, 8311-8321
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Survival of Cultured Neurons from Amyloid Precursor Protein Knock-Out Mice against Alzheimer's Amyloid-beta Toxicity and Oxidative Stress.
A. R. White, H. Zheng, D. Galatis, F. Maher, L. Hesse, G. Multhaup, K. Beyreuther, C. L. Masters, and R. Cappai (1998)
J. Neurosci. 18, 6207-6217
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Increased Production of Amyloid Precursor Protein Provides a Substrate for Caspase-3 in Dying Motoneurons.
N. Y. Barnes, L. Li, K. Yoshikawa, L. M. Schwartz, R. W. Oppenheim, and C. E. Milligan (1998)
J. Neurosci. 18, 5869-5880
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beta -Amyloid Fibrils Activate Parallel Mitogen-Activated Protein Kinase Pathways in Microglia and THP1 Monocytes.
D. R. McDonald, M. E. Bamberger, C. K. Combs, and G. E. Landreth (1998)
J. Neurosci. 18, 4451-4460
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Amyloid beta  Protein-(1-42) Forms Calcium-permeable, Zn2+-sensitive Channel.
S. K. Rhee, A. P. Quist, and R. Lal (1998)
J. Biol. Chem. 273, 13379-13382
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Diffusible, nonfibrillar ligands derived from Abeta 1-42 are potent central nervous system neurotoxins.
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