Aβ interacts with both the iron center and the porphyrin ring of heme: Mechanism of heme's action on Aβ aggregation and disaggregation

Chemical Research in Toxicology

Volumn 26, Issue 2, 2013, Pages 262-269

  Yuan, Can ^a   Gao, Zhonghong ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; HEME; IRON; PEROXIDASE; PHENYLALANINE; PORPHYRIN; PROTOPORPHYRIN; THIOFLAVINE;

ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; ENZYME ACTIVITY; FLUORESCENCE ANALYSIS; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN INTERACTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROSCOPY;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; CIRCULAR DICHROISM; HEME; HUMANS; IRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEROXIDASE; PORPHYRINS;

EID: 84874098495     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx300441e     Document Type: Article

References (44)

1. Behrouz, N., Defossez, A., Delacourte, A., and Mazzuca, M. (1991) The immunohistochemical evidence of amyloid diffuse deposits as a pathological hallmark in Alzheimer's disease J. Gerontol. 46, B209-B212
2. Bernstein, S. L., Dupuis, N. F., Lazo, N. D., Wyttenbach, T., Condron, M. M., Bitan, G., Teplow, D. B., Shea, J. E., Ruotolo, B. T., Robinson, C. V., and Bowers, M. T. (2009) Amyloid-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease Nat. Chem. 1, 326-331
3. Hardy, J. A. and Higgins, G. A. (1992) Alzheimer's disease: The amyloid cascade hypothesis Science 256, 184-185
4. Gazit, E. (2006) From green bacteria to human dementia: A novel model for discovering amyloid assembly inhibitors ACS Chem. Biol. 1, 417-419
5. Bartolini, M., Bertucci, C., Bolognesi, M. L., Cavalli, A., Melchiorre, C., and Andrisano, V. (2007) Insight Into the Kinetic of Amyloid β (1-42) Peptide Self-Aggregation: Elucidation of Inhibitors' Mechanism of Action ChemBioChem 8, 2152-2161 (Pubitemid 350220767)
6. Senguen, F. T., Lee, N. R., Gu, X., Ryan, D. M., Doran, T. M., Anderson, E. A., and Nilsson, B. L. (2011) Probing aromatic, hydrophobic, and steric effects on the self-assembly of an amyloid-beta fragment peptide Mol. BioSyst. 7, 486-496
7. Porat, Y., Abramowitz, A., and Gazit, E. (2006) Inhibition of amyloid fibril formation by polyphenols: Structural similarity and aromatic interactions as a common inhibition mechanism Chem. Biol. Drug Des. 67, 27-37 (Pubitemid 43881385)
8. Atamna, H. and Boyle, K. (2006) Amyloid-beta peptide binds with heme to form a peroxidase: Relationship to the cytopathologies of Alzheimer's disease Proc. Natl. Acad. Sci. U.S.A. 103, 3381-3386 (Pubitemid 43346478)
9. Yuan, C., Yi, L., Yang, Z., Deng, Q., Huang, Y., Li, H., and Gao, Z. (2012) Amyloid beta-heme peroxidase promoted protein nitrotyrosination: relevance to widespread protein nitration in Alzheimer's disease J. Biol. Inorg. Chem. 17, 197-207
10. Pramanik, D., Ghosh, C., and Dey, S. G. (2011) Heme-Cu bound abeta peptides: spectroscopic characterization, reactivity, and relevance to Alzheimer's disease J. Am. Chem. Soc. 133, 15545-15552
11. Pramanik, D. and Dey, S. G. (2011) Active site environment of heme-bound amyloid beta peptide associated with Alzheimer's disease J. Am. Chem. Soc. 133, 81-87
12. Bao, Q., Luo, Y., Li, W., Sun, X., Zhu, C., Li, P., Huang, Z. X., and Tan, X. (2011) The mechanism for heme to prevent Abeta(1-40) aggregation and its cytotoxicity J. Biol. Inorg. Chem. 16, 809-816
13. Atamna, H., Frey, W. H., 2nd, and Ko, N. (2009) Human and rodent amyloid-beta peptides differentially bind heme: relevance to the human susceptibility to Alzheimer's disease Arch. Biochem. Biophys. 487, 59-65
14. Atamna, H. and Frey, W. H., 2nd. (2004) A role for heme in Alzheimer's disease: heme binds amyloid beta and has altered metabolism Proc. Natl. Acad. Sci. U.S.A. 101, 11153-11158 (Pubitemid 38989599)
15. Yuan, C., Li, H., and Gao, Z. (2012) Amyloid beta modulated the selectivity of heme-catalyzed protein tyrosine nitration: an alternative mechanism for selective protein nitration J. Biol. Inorg. Chem. 17, 1083-1091
16. Atamna, H. (2009) Amino acids variations in amyloid-beta peptides, mitochondrial dysfunction, and new therapies for Alzheimer's disease J. Bioenerg. Biomembr. 41, 457-464
17. Suzuki, H., Tashiro, S., Hira, S., Sun, J., Yamazaki, C., Zenke, Y., Ikeda-Saito, M., Yoshida, M., and Igarashi, K. (2004) Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1 EMBO J. 23, 2544-2553 (Pubitemid 38988226)
18. Ye, W. and Zhang, L. (2004) Heme controls the expression of cell cycle regulators and cell growth in HeLa cells Biochem. Biophys. Res. Commun. 315, 546-554 (Pubitemid 38229378)
19. Teplow, D. B. (2006) Preparation of amyloid beta-protein for structural and functional studies Methods Enzymol. 413, 20-33 (Pubitemid 44528683)
20. Lustbader, J. W., Cirilli, M., Lin, C., Xu, H. W., Takuma, K., Wang, N., Caspersen, C., Chen, X., Pollak, S., Chaney, M., Trinchese, F., Liu, S., Gunn-Moore, F., Lue, L. F., Walker, D. G., Kuppusamy, P., Zewier, Z. L., Arancio, O., Stern, D., Yan, S. S., and Wu, H. (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease Science 304, 448-452 (Pubitemid 38495942)
21. Bush, A. I. (2003) The metallobiology of Alzheimer's disease Trends Neurosci. 26, 207-214 (Pubitemid 36412003)
22. Dong, J., Shokes, J. E., Scott, R. A., and Lynn, D. G. (2006) Modulating amyloid self-assembly and fibril morphology with Zn(II) J. Am. Chem. Soc. 128, 3540-3542
23. Morgan, D. M., Dong, J., Jacob, J., Lu, K., Apkarian, R. P., Thiyagarajan, P., and Lynn, D. G. (2002) Metal switch for amyloid formation: insight into the structure of the nucleus J. Am. Chem. Soc. 124, 12644-12645 (Pubitemid 35215972)
24. Lee, J. S. and Park, C. B. (2010) Microfluidic dissociation and clearance of Alzheimer's beta-amyloid aggregates Biomaterials 31, 6789-6795
25. Lu, K., Jacob, J., Thiyagarajan, P., Conticello, V. P., and Lynn, D. G. (2003) Exploiting amyloid fibril lamination for nanotube self-assembly J. Am. Chem. Soc. 125, 6391-6393 (Pubitemid 36605407)
26. Tycko, R. (2003) Insights into the amyloid folding problem from solid-state NMR Biochemistry 42, 3151-3159 (Pubitemid 36348623)
27. Mehta, A. K., Lu, K., Childers, W. S., Liang, Y., Dublin, S. N., Dong, J., Snyder, J. P., Pingali, S. V., Thiyagarajan, P., and Lynn, D. G. (2008) Facial symmetry in protein self-assembly J. Am. Chem. Soc. 130, 9829-9835
28. Gazit, E. (2002) A possible role for pi-stacking in the self-assembly of amyloid fibrils FASEB J. 16, 77-83 (Pubitemid 34027953)
29. Liu, D. H., Williamson, D. A., Kennedy, M. L., Williams, T. D., Morton, M. M., and Benson, D. R. (1999) Aromatic side chain-porphyrin interactions in designed hemoproteins J. Am. Chem. Soc. 121, 11798-11812
30. Thomas, D. D., Espey, M. G., Vitek, M. P., Miranda, K. M., and Wink, D. A. (2002) Protein nitration is mediated by heme and free metals through Fenton-type chemistry: An alternative to the NO/O-2(-) reaction Proc. Natl. Acad. Sci. U.S.A. 99, 12691-12696
31. Josephy, P. D., Eling, T., and Mason, R. P. (1982) The horseradish peroxidase-catalyzed oxidation of 3,5,3′,5′-tetramethylbenzidine. Free radical and charge-transfer complex intermediates J. Biol. Chem. 257, 3669-3675
32. Sánchez, L., Madurga, S., Pukala, T., Vilaseca, M., López-Iglesias, C., Robinson, C. V., Giralt, E., and Carulla, N. l. (2011) Aβ40 and Aβ42 Amyloid Fibrils Exhibit Distinct Molecular Recycling Properties J. Am. Chem. Soc. 133, 6505-6508
33. LeVine, H., 3rd. (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T Methods Enzymol. 309, 274-284
34. Ozaki, S. and Demontellano, P. R. O. (1995) Molecular Engineering of Horseradish-Peroxidase-Thioether Sulfoxidation and Styrene Epoxidation by Phe-41 Leucine and Threonine Mutants J. Am. Chem. Soc. 117, 7056-7064
35. Gengenbach, A., Syn, S., Wang, X., and Lu, Y. (1999) Redesign of cytochrome c peroxidase into a manganese peroxidase: role of tryptophans in peroxidase activity Biochemistry 38, 11425-11432
36. Rodriguez-Lopez, J. N., Lowe, D. J., Hernandez-Ruiz, J., Hiner, A. N., Garcia-Canovas, F., and Thorneley, R. N. (2001) Mechanism of reaction of hydrogen peroxide with horseradish peroxidase: identification of intermediates in the catalytic cycle J. Am. Chem. Soc. 123, 11838-11847 (Pubitemid 33135013)
37. Schlenzig, D., Manhart, S., Cinar, Y., Kleinschmidt, M., Hause, G., Willbold, D., Funke, S. A., Schilling, S., and Demuth, H. U. (2009) Pyroglutamate Formation Influences Solubility and Amyloidogenicity of Amyloid Peptides Biochemistry 48, 7072-7078
38. Bleiholder, C., Dupuis, N. F., Wyttenbach, T., and Bowers, M. T. (2011) Ion mobility-mass spectrometry reveals a conformational conversion from random assembly to beta-sheet in amyloid fibril formation Nat. Chem. 3, 172-177
39. Wang, Q., Yang, Z., Zhang, X., Xiao, X., Chang, C. K., and Xu, B. (2007) A Supramolecular-Hydrogel-Encapsulated Hemin as an Artificial Enzyme to Mimic Peroxidase Angew. Chem.-Int. Edit. 46, 4285-4289 (Pubitemid 47040822)
40. Lee, C. and Ham, S. (2011) Characterizing amyloid-beta protein misfolding from molecular dynamics simulations with explicit water J. Comput. Chem. 32, 349-355
41. Garcia-Alloza, M., Subramanian, M., Thyssen, D., Borrelli, L. A., Fauq, A., Das, P., Golde, T. E., Hyman, B. T., and Bacskai, B. J. (2009) Existing plaques and neuritic abnormalities in APP:PS1 mice are not affected by administration of the gamma-secretase inhibitor LY-411575 Mol. Neurodegener. 4, 19-27
42. Yan, P., Bero, A. W., Cirrito, J. R., Xiao, Q., Hu, X., Wang, Y., Gonzales, E., Holtzman, D. M., and Lee, J. M. (2009) Characterizing the appearance and growth of amyloid plaques in APP/PS1 mice J. Neurosci. 29, 10706-10714
43. Lansbury, P. T., Jr. (1997) Structural neurology: Are seeds at the root of neuronal degeneration? Neuron 19, 1151-1154 (Pubitemid 28030534)
44. Nonaka, T., Watanabe, S. T., Iwatsubo, T., and Hasegawa, M. (2010) Seeded aggregation and toxicity of {alpha}-synuclein and tau: Cellular models of neurodegenerative diseases J. Biol. Chem. 285, 34885-34898