The nonfibrillar amyloid β-peptide induces apoptotic neuronal cell death: Involvement of its C-terminal fusogenic domain

Journal of Neurochemistry

Volumn 73, Issue 4, 1999, Pages 1626-1634

  Pillot, Thierry ^a   Drouet, Béatrice ^a   Queillé, Sophie ^a   Labeur, Christine ^b   Vandekerckhove, Joël ^b   Rosseneu, Maryvonne ^b   Pinçon Raymond, Martine ^a   Chambaz, Jean ^a  

^a CENTRE DE RECHERCHE DES CORDELIERS   (France)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Alzheimer's disease; Amyloid peptide; Apoptosis; Cortical primary neurons; Fusogenic peptides; Neurotoxicity

Indexed keywords

AMYLOID BETA PROTEIN; MUTANT PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; CARBOXY TERMINAL SEQUENCE; CELL VIABILITY; CONTROLLED STUDY; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT;

AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; CELL MEMBRANE; CELL NUCLEUS; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO; MOLECULAR SEQUENCE DATA; NEURONS; PEPTIDE FRAGMENTS; RATS; RATS, WISTAR; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0032845739     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0731626.x     Document Type: Article

References (50)

1. Aksenov M. Y., Aksenova M. V., Butterfield D. A., Hensley K., Vigo-Pelfrey C., and Carney J. M. (1996) Glutamate synthetase-induced enhancement of β-amyloid peptide Aβ(1-40) neurotoxicity accompanied by abrogation of fibril formation and Aβ fragmentation. J. Neurochem. 66, 2050-2056.
2. Aksenova M. V., Aksenov M. Y., Butterfield D. A., and Carney J. M. (1996) α1-Antichymotrypsin interaction with Aβ(1-40) inhibits fibril formation but does not affect the peptide toxicity. Neurosci. Lett. 211, 45-48.
3. Arispe N., Rojas E., and Pollard H. B. (1993) Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockage by tromethamine and aluminium. Proc. Natl. Acad. Sci. USA 90, 567-571.
4. Behl C., Davis J. B., Klier F. G., and Schubert D. (1994a) Amyloid-β peptide induces necrosis rather than apoptosis. Brain Res. 645, 253-264.
5. Behl C., Davis J. B., Lesley R., and Schubert D. (1994b) Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827.
6. Boudreau N., Sympson C. J., Werb Z., and Bissell M. J. (1995) Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267, 891-893.
7. Bouillot C., Prochiantz A., Rougon G., and Allinquant B. (1996) Axonal amyloid precursor protein expressed by neurons in vitro is present in a membrane fraction with caveola-like properties. J. Biol. Chem. 271, 7640-7644.
8. Brasseur R., Pillot T., Lins L., Vandekerckhove J., and Rosseneu M. (1997) Peptides in membranes: tipping the balance of membrane stability. Trends Biochem. Sci. 22, 167-171.
9. Busciglio J. and Yankner B. (1995) Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro. Nature 378, 776-779.
10. Cotman C. and Anderson A. (1995) A potential role for apoptosis in neurodegeneration and Alzheimer's disease. Mol. Neurobiol. 10, 19-45.
11. Estus S., Tucker H. M., van Rooyen C., Wright S., Brigham E. F., Wogulis M., and Rydel R. E. (1997) Aggregated amyloid-β protein induces cortical neuronal apoptosis and concomitant "apoptotic" pattern of gene induction. J. Neurosci. 17, 7736-7745.
12. + channels. Science 264, 276-279.
13. Favit A., Grimaldi M., Nelson T. J., and Alkon D. L. (1998) Alzheimer's-speciftc effects of soluble β-amyloid on protein kinase C-α and -γ degradation in human fibroblasts. Proc. Natl. Acad. Sci. USA 95, 5562-5567.
14. Han Z., Malik N., Carter T., Reeves W. H., Wyche J. H., and Hendrickson E. A. (1996) DNA-dependent protein kinase is a target for a CPP32-like apoptotic protease. J. Biol. Chem. 271, 25035-25040.
15. Hardy J. (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci. 20, 154-159.
16. Hertel C., Terzi E., Hauser N., Jakob-Rotne R., Seelig J., and Kemp J. A. (1997) Inhibition of the electrostatic interaction between β-amyloid peptide and membranes prevents β-amyloid-induced toxicity. Proc. Natl. Acad. Sci. USA 94, 9412-9416.
17. Hilbich C., Kisters-Woike B., Reed J., Masters C. L., and Beyreuther K. (1991) Aggregation and secondary structure of synthetic amyloid βA4 peptides of Alzheimer's disease. J. Mol. Biol. 218, 149-163.
18. Keller J. N., Pang Z., Geddes J. W., Begley J. G., Germeyer A., Waeg G., and Mattson M. P. (1997) Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 69, 273-284.
19. Lambert M. P., Barlow A. K., Chromy B. A., Edwards C., Freed R., Liosatos M., Morgan T. E., Rozovsky I., Trommer B., Viola K. L., Wals P., Zhang C., Finch C. E., Krafft G. A., and Klein W. L. (1998) Diffusible, nonfibrillar ligands derived from Ab1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA 95, 6448-6453.
20. Lendon C. L., Ashall F., and Goate A. M. (1997) Exploring the etiology of Alzheimer disease using molecular genetics. JAMA 277, 825-831.
21. Liu Y. and Schubert D. (1997) Cytotoxic amyloid peptides inhibit cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction by enhancing MTT formazan exocytosis. J. Neurochem. 69, 2285-2293.
22. Liu Y., Dargusch R., and Schubert D. (1997) Beta amyloid toxicity does not require RAGE protein. Biochem. Biophys. Res. Commun. 237, 37-40.
23. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., and Cotman C. W. (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
24. Lorenzo A. and Yankner B. A. (1994) β-Amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc. Natl. Acad. Sci. USA 91, 12243-12247.
25. Matter M. L., Zhang Z., Nordstedt C., and Ruoslathi E. (1998) The α1β5 integrin mediates elimination of amyloid-β peptide and protects against apoptosis. J. Cell Biol. 141, 1019-1030.
26. Mattson M. P. (1995) Untangling the pathophysiochemistry of β-amyloid. Nat. Struct. Biol. 2, 926-928.
27. McLaurin J. A. and Chakrabartty A. (1996) Membrane disruption by Alzheimer β-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J. Biol. Chem. 271, 26482-26489.
28. Mirzabekov T. A., Lin M. C., and Kagan B. L. (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 271, 1988-1992.
29. Muller W. E., Koch S., Eckert A., Hartmann H., and Scheuer K. (1995) β-Amyloid peptide decreases membrane fluidity. Brain Res. 674, 133-136.
30. Muller W. E., Eckert G. P., Scheuer K., Cairns N. J., Maras A., and Gattaz W. F. (1998) Effects of β-amyloid peptides on the fluidity of membranes from frontal and parietal lobes of human brain -high potencies of A-β-1-42 and A-β-1-43. Amyloid Int. J. Exp. Clin. Invest. 5, 10-15.
31. Nicholson D. W. and Thornberry N. A. (1997) Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306.
32. Pike C. J., Cummings B. J., and Cotman C. W. (1991) In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 563, 311-314.
33. Pillot T., Goethals M., Vanloo B., Talussot C., Brasseur R., Vandekerckhove J., Rosseneu M., and Lins L. (1996a) Fusogenic properties of the C-terminal domain of the Alzheimer β-amyloid peptide. J. Biol. Chem. 271, 28757-28765.
34. Pillot T., Goethals M., Vanloo B., Lins L., Brasseur R., Vandekerckhove J., and Rosseneu M. (1996b) Specific modulation of the fusogenic properties of the Alzheimer beta-amyloid peptide by apolipoprotein E isoforms. Eur. J. Biochem. 243, 650-659.
35. Pillot T., Lins L., Goethals M., Vanloo B., Baert J., Vandekerckhove J., Rosseneu M., and Brasseur R. (1997) The 118-135 peptide of the human prion protein forms amyloid fibrils and induces liposome fusion. J. Mol. Biol. 274, 381-393.
36. 2+-sensitive channel. J. Biol. Chem. 273, 13379-13382.
37. Schubert D., Behl C., Lesley R., Brack A., Dargusch R., Sagara Y., and Kimura H. (1995) Amyloid peptides are toxic via a common oxidative mechanism. Proc. Natl. Acad. Sci. USA 92, 1989-1993.
38. Schulz J. B., Weller M., and Klockgether T. (1996) Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J. Neurosci. 16, 4696-4706.
39. Selkoe D. J. (1994) Alzheimer's disease: a central role for amyloid. J. Neuropathol Exp. Neurol 53, 438-447.
40. Skovronsky D. M., Doms R. W., and Lee V. Y.-M. (1998) Detection of a novel intraneuronal pool of insoluble amyloid β protein that accumulates with time in culture. J. Cell Biol. 141, 1031-1039.
41. Sugahara H., Kanakura Y., Furitsu T., Ishihara K., Oritani K., Ikeda H., Kitayama H., Ishikawa J., Hashimoto K., Kanayama H., and Matsuzawa Y. (1994) Induction of programmed cell death in human hematopoietic cell lines by fibronectin via its interaction with very late antigen 5. J. Exp. Med. 179, 1757-1766.
42. Suzuki A. (1997) Amyloid β-protein induces necrotic cell death mediated by ICE cascade in PC12 cells. Exp. Cell Res. 234, 507-511.
43. Tan S., Wood M., and Maher P. (1998) Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J. Neurochem. 71, 95-105.
44. Tucker H. M., Rydel R. E., Wright S., and Estus S. (1998) Human amylin induces "apoptotic" pattern of gene expression concomitant with cortical neuronal apoptosis. J. Neurochem. 71, 506-516.
45. Wujek J. R., Dority M. D., Frederickson R. C. A., and Brunden K. R. (1996) Deposits of Aβ fibrils are not toxic to cortical and hippocampal neurons in vitro. Neurobiol. Aging 17, 107-113.
46. Yaar M., Zhai S., Pilch P. F., Doyle S. M., Eisenhauer P. B., Fine R. E., and Gilchrest B. A. (1997) Binding of β-amyloid to the p75 neurotrophin receptor induces apoptosis. A possible mechanism for Alzheimer's disease. J. Clin. Invest. 100, 2333-2340.
47. Yan S. D., Chen X., Fu J., Chen M., Zhu H., Roher A., Slattery T., Zhao L., Nagashima M., Morser J., Migheli A., Nawroth P., Stern D., and Schmidt A. M. (1996) RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382, 685-691.
48. Yan S. D., Fu J., Soto C., Chen X., Zhu H., Al-Mohanna F., Collison K., Zhu A., Stern E., Saido T., Tohyama M., Ogawa S., Roher A., and Stern D. (1997) An intracellular protein that binds amyloid-β peptide and mediates neurotoxicity in Alzheimer's disease. Nature 389, 689-695.
49. Yankner B. A. (1996) Mechanism of neuronal degeneration in Alzheimer's disease. Neuron 16, 921-932.
50. Yoshikawa K., Aizawa T., and Hayashi Y. (1992) Degeneration in vitro of post-mitotic neurons overexpressing the Alzheimer amyloid protein precursor. Nature 359, 64-67.