Despite its role in assembly, methionine 35 is not necessary for amyloid β-protein toxicity

Journal of Neurochemistry

Volumn 113, Issue 5, 2010, Pages 1252-1262

  Maiti, Panchanan ^a   Lomakin, Aleksey ^b   Benedek, George B ^b   Bitan, Gal ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Amyloid protein; Neurotoxicity; Oxidative stress; Structure activity relationship

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; METHIONINE; NORLEUCINE; VALINE;

ALZHEIMER DISEASE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; OLIGOMERIZATION; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RAT;

AMINO ACID SUBSTITUTION; AMYLOID BETA-PROTEIN; ANIMALS; CELLS, CULTURED; CIRCULAR DICHROISM; COLORING AGENTS; CROSS-LINKING REAGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; IN SITU NICK-END LABELING; L-LACTATE DEHYDROGENASE; LIGHT; METHIONINE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; PEPTIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; SCATTERING, RADIATION; TETRAZOLIUM SALTS; THIAZOLES;

EID: 77951904937     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06692.x     Document Type: Article

References (58)

1. Barnham K. J., Ciccotosto G. D., Tickler A. K. et al. (2003) Neurotoxic, redox-competent Alzheimer's β-amyloid is released from lipid membrane by methionine oxidation. J. Biol. Chem. 278, 42959 42965.
2. Bernstein S. L., Dupuis N. F., Lazo N. D. et al. (2009) Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease. Nat. Chem. 1, 326 331.
3. Bitan G. (2006) Structural study of metastable amyloidogenic protein oligomers by photo-induced cross-linking of unmodified proteins. Methods Enzymol. 413, 217 236. (Pubitemid 44528693)
4. Bitan G., Lomakin A. Teplow D. B. (2001) Amyloid β-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins. J. Biol. Chem. 276, 35176 35184. (Pubitemid 37384526)
5. Bitan G., Kirkitadze M. D., Lomakin A., Vollers S. S., Benedek G. B. Teplow D. B. (2003a) Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways. Proc. Natl Acad. Sci. USA 100, 330 335. (Pubitemid 36078074)
6. 35 and amyloid β-protein oligomerization. J. Am. Chem. Soc. 125, 15359 15365. (Pubitemid 37532178)
7. Bitan G., Vollers S. S. Teplow D. B. (2003c) Elucidation of primary structure elements controlling early amyloid β-protein oligomerization. J. Biol. Chem. 278, 34882 34889. (Pubitemid 37102247)
8. Bravo R., Arimon M., Valle-Delgado J. J., Garcia R., Durany N., Castel S., Cruz M., Ventura S. Fernandez-Busquets X. (2008) Sulfated polysaccharides promote the assembly of amyloid β(1-42) peptide into stable fibrils of reduced cytotoxicity. J. Biol. Chem. 283, 32471 32483.
9. Butterfield D. A. (2002) Amyloid β-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. Free Radic. Res. 36, 1307 1313. (Pubitemid 35469517)
10. Butterfield D. A. Boyd-Kimball D. (2005) The critical role of methionine 35 in Alzheimer's amyloid β-peptide (1-42)-induced oxidative stress and neurotoxicity. Biochim. Biophys. Acta 1703, 149 156. (Pubitemid 40170438)
11. Butterfield D. A. Kanski J. (2002) Methionine residue 35 is critical for the oxidative stress and neurotoxic properties of Alzheimer's amyloid β-peptide 1-42. Peptides 23, 1299 1309. (Pubitemid 34786708)
12. Butterfield D. A., Reed T., Newman S. F. Sultana R. (2007) Roles of amyloid β-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic. Biol. Med. 43, 658 677. (Pubitemid 47102132)
13. Butterfield D. A., Galvan V., Lange M. B. et al. (2009) In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid β-peptide of APP. Free Radic. Biol. Med. 48, 136 144.
14. Ciccotosto G. D., Tew D., Curtain C. C. et al. (2004) Enhanced toxicity and cellular binding of a modified amyloid β peptide with a methionine to valine substitution. J. Biol. Chem. 279, 42528 42534. (Pubitemid 39372136)
15. Clementi M. E., Pezzotti M., Orsini F., Sampaolese B., Mezzogori D., Grassi C., Giardina B. Misiti F. (2006) Alzheimer's amyloid β-peptide (1-42) induces cell death in human neuroblastoma via bax&bcl-2 ratio increase: an intriguing role for methionine 35. Biochem. Biophys. Res. Commun. 342, 206 213. (Pubitemid 43247378)
16. Crouch P. J., Harding S. M., White A. R., Camakaris J., Bush A. I. Masters C. L. (2008) Mechanisms of Aβ mediated neurodegeneration in Alzheimer's disease. Int. J. Biochem. Cell Biol. 40, 181 198. (Pubitemid 350137874)
17. Cummings J. L. (2004) Alzheimer's disease. N. Engl. J. Med. 351, 56 67.
18. Dahlgren K. N., Manelli A. M., Stine Jr. W. B., Baker L. K., Krafft G. A. LaDu M. J. (2002) Oligomeric and fibrillar species of amyloid-β peptides differentially affect neuronal viability. J. Biol. Chem. 277, 32046 32053.
19. Decker T. Lohmann-Matthes M. L. (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Methods 115, 61 69.
20. Fancy D. A. Kodadek T. (1999) Chemistry for the analysis of protein-protein interactions: rapid and efficient cross-linking triggered by long wavelength light. Proc. Natl Acad. Sci. USA 96, 6020 6024. (Pubitemid 29256612)
21. Fradinger E. A., Monien B. H., Urbanc B. et al. (2008) C-terminal peptides coassemble into Aβ42 oligomers and protect neurons against Aβ42-induced neurotoxicity. Proc. Natl Acad. Sci. USA 105, 14175 14180.
22. Haass C. Selkoe D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8, 101 112. (Pubitemid 46432529)
23. Halliwell B. (1989) Free radicals, reactive oxygen species and human disease: a critical evaluation with special reference to atherosclerosis. Br. J. Exp. Pathol. 70, 737 757. (Pubitemid 20022141)
24. Halliwell B. (2006) Oxidative stress and neurodegeneration: where are we now? J. Neurochem. 97, 1634 1658. (Pubitemid 43873658)
25. Hardy J. Selkoe D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353 356. (Pubitemid 34790756)
26. Hou L., Kang I., Marchant R. E. Zagorski M. G. (2002) Methionine 35 oxidation reduces fibril assembly of the amyloid Aβ-(1-42) peptide of Alzheimer's disease. J. Biol. Chem. 277, 40173 40176. (Pubitemid 35215584)
27. Hou L., Shao H., Zhang Y. et al. (2004) Solution NMR studies of the Aβ(1-40) and Aβ(1-42) peptides establish that the Met35 oxidation state affects the mechanism of amyloid formation. J. Am. Chem. Soc. 126, 1992 2005. (Pubitemid 38228879)
28. Jarrett J. T., Berger E. P. Lansbury Jr. P. T. (1993) The carboxy terminus of the β amyloid protein is critical for the seeding of amyloid formation: implications for the pathogenesis of Alzheimer's disease. Biochemistry 32, 4693 4697.
29. Josephs K. A., Whitwell J. L., Ahmed Z. et al. (2008) β-Amyloid burden is not associated with rates of brain atrophy. Ann. Neurol. 63, 204 212. (Pubitemid 351355299)
30. Kirkitadze M. D., Condron M. M. Teplow D. B. (2001) Identification and characterization of key kinetic intermediates in amyloid β-protein fibrillogenesis. J. Mol. Biol. 312, 1103 1119.
31. Koffie R. M., Meyer-Luehmann M., Hashimoto T. et al. (2009) Oligomeric amyloid β associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl Acad. Sci. USA 106, 4012 4017.
32. Kuo Y. M., Kokjohn T. A., Beach T. G. et al. (2001) Comparative analysis of amyloid-β chemical structure and amyloid plaque morphology of transgenic mouse and Alzheimer's disease brains. J. Biol. Chem. 276, 12991 12998. (Pubitemid 37385224)
33. Lomakin A., Chung D. S., Benedek G. B., Kirschner D. A. Teplow D. B. (1996) On the nucleation and growth of amyloid β-protein fibrils: detection of nuclei and quantitation of rate constants. Proc. Natl Acad. Sci. USA 93, 1125 1129. (Pubitemid 26054370)
34. Markesbery W. R. Lovell M. A. (1998) Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in alzheimers-disease. Neurobiol. Aging 19, 33 36.
35. Masliah E., Sisk A., Mallory M., Mucke L., Schenk D. Games D. (1996) Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F β-amyloid precursor protein and Alzheimer's disease. J. Neurosci. 16, 5795 5811. (Pubitemid 26293401)
36. Morrissette D. A., Parachikova A., Green K. N. LaFerla F. M. (2009) Relevance of transgenic mouse models to human Alzheimer disease. J. Biol. Chem. 284, 6033 6037.
37. Murray I. V., Sindoni M. E. Axelsen P. H. (2005) Promotion of oxidative lipid membrane damage by amyloid β proteins. Biochemistry 44, 12606 12613.
38. Näslund J., Schierhorn A., Hellman U. et al. (1994) Relative abundance of Alzheimer Aβ amyloid peptide variants in Alzheimer disease and normal aging. Proc. Natl Acad. Sci. USA 91, 8378 8382. (Pubitemid 24273667)
39. Ono K., Condron M. M. Teplow D. B. (2009) Structure-neurotoxicity relationships of amyloid β-protein oligomers. Proc. Natl Acad. Sci. USA 106, 14745 14750.
40. Palmblad M., Westlind-Danielsson A. Bergquist J. (2002) Oxidation of methionine 35 attenuates formation of amyloid β -peptide 1-40 oligomers. J. Biol. Chem. 277, 19506 19510. (Pubitemid 34967462)
41. 2+-dependent apoptosis induced by amyloid β-peptide in human neuroblastoma IMR32 cells. J. Neurochem. 107, 1070 1082.
42. Rahimi F., Maiti P. Bitan G. (2009) Photo-induced cross-linking of unmodified proteins (PICUP) applied to amyloidogenic peptides. J. Vis. Exp. DOI: 10.3791&1071.
43. Reiman E. M., Chen K., Liu X. et al. (2009) Fibrillar amyloid-β burden in cognitively normal people at 3 levels of genetic risk for Alzheimer's disease. Proc. Natl Acad. Sci. USA 106, 6820 6825.
44. Roher A. E., Palmer K. C., Yurewicz E. C., Ball M. J. Greenberg B. D. (1993) Morphological and biochemical analyses of amyloid plaque core proteins purified from Alzheimer disease brain tissue. J. Neurochem. 61, 1916 1926.
45. Roychaudhuri R., Yang M., Hoshi M. M. Teplow D. B. (2009) Amyloid β-protein assembly and Alzheimer disease. J. Biol. Chem. 284, 4749 4753.
46. i in cultured rat hippocampal neurons following exposure to N-methyl-D-aspartate. J. Physiol. 448, 655 676.
47. Selkoe D. J. (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741 766.
48. Tomic J. L., Pensalfini A., Head E. Glabe C. G. (2009) Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction. Neurobiol. Dis. 35, 352 358.
49. Urbanc B., Cruz L., Yun S., Buldyrev S. V., Bitan G., Teplow D. B. Stanley H. E. (2004) In silico study of amyloid β-protein folding and oligomerization. Proc. Natl Acad. Sci. USA 101, 17345 17350. (Pubitemid 39657406)
50. Varadarajan S., Yatin S., Kanski J., Jahanshahi F. Butterfield D. A. (1999) Methionine residue 35 is important in amyloid β-peptide-associated free radical oxidative stress. Brain Res. Bull. 50, 133 141. (Pubitemid 29467333)
51. Varadarajan S., Yatin S., Aksenova M. Butterfield D. A. (2000) Review: Alzheimer's amyloid β-peptide-associated free radical oxidative stress and neurotoxicity. J. Struct. Biol. 130, 184 208.
52. Varadarajan S., Kanski J., Aksenova M., Lauderback C. Butterfield D. A. (2001) Different mechanisms of oxidative stress and neurotoxicity for Alzheimer's Aβ(1-42) and Aβ(25-35). J. Am. Chem. Soc. 123, 5625 5631. (Pubitemid 32904694)
53. Vollers S. S., Teplow D. B. Bitan G. (2005) Determination of peptide oligomerization state using rapid photochemical crosslinking. Methods Mol. Biol. 299, 11 18.
54. Wang X., Ge J., Wang K., Qian J. Zou Y. (2006) Evaluation of MTT assay for measurement of emodin-induced cytotoxicity. Assay Drug Dev. Technol. 4, 203 207. (Pubitemid 43810924)
55. White J. A., Manelli A. M., Holmberg K. H., Van Eldik L. J. LaDu M. J. (2005) Differential effects of oligomeric and fibrillar amyloid-β 1-42 on astrocyte-mediated inflammation. Neurobiol. Dis. 18, 459 465.
56. Yang M. Teplow D. B. (2008) Amyloid β-protein monomer folding: free-energy surfaces reveal alloform-specific differences. J. Mol. Biol. 384, 450 464.
57. Yatin S. M., Varadarajan S., Link C. D. Butterfield D. A. (1999) In vitro and in vivo oxidative stress associated with Alzheimer's amyloid β-peptide (1-42). Neurobiol. Aging 20, 325 330. (Pubitemid 29525418)
58. Yun S., Urbanc B., Cruz L., Bitan G., Teplow D. B. Stanley H. E. (2007) Role of electrostatic interactions in amyloid β-protein (Aβ) oligomer formation: a discrete molecular dynamics study. Biophys. J. 92, 4064 4077. (Pubitemid 46910591)