Comparisons with Amyloid-β Reveal an Aspartate Residue That Stabilizes Fibrils of the Aortic Amyloid Peptide Medin

Journal of Biological Chemistry

Volumn 290, Issue 12, 2015, Pages 7791-7803

  Davies, Hannah A ^a   Madine, Jillian ^a   Middleton, David A ^b  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BLOOD VESSELS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; PROTEINS; SELF ASSEMBLY;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID-LIKE FIBRIL; ASPARTATE RESIDUE; ASSEMBLY MECHANISM; FIBRIL MORPHOLOGY; MOLECULAR ARCHITECTURE; PROTEIN COMPONENTS;

GLYCOPROTEINS;

AMYLOID; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; ASPARAGINE; ASPARTIC ACID; CARBON 13; LYSINE; MEDIN PROTEIN; NITROGEN 15; OLIGOMER; TRYPTOPHAN; UNCLASSIFIED DRUG; MEMBRANE ANTIGEN; MFGE8 PROTEIN, HUMAN; MILK PROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BETA SHEET; CELL VIABILITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FLUORESCENCE; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; WILD TYPE; AORTA; CHEMISTRY; CIRCULAR DICHROISM; COMPARATIVE STUDY; METABOLISM; MOLECULAR GENETICS; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANTIGENS, SURFACE; AORTA; ASPARTIC ACID; CIRCULAR DICHROISM; HUMANS; MILK PROTEINS; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84925337340     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.602177     Document Type: Article

References (57)

1. Sipe, J. D., Benson, M. D., Buxbaum, J. N., Ikeda, S., Merlini, G., Saraiva, M. J. M., and Westermark, P. (2014) Nomenclature 2014: amyloid fibril proteins and clinical classification of the amyloidosis. Amyloid 21, 221-224
2. Harrison, R. S., Sharpe, P. C., Singh, Y., and Fairlie, D. P. (2007) in Reviews of Physiology, Biochemistry and Pharmacology (Amara, S. G., Bamberg, E., Fleischmann, B., Gudermann, T., Hebert, S. C., Jahn, R., Lederer, W. J., Lill, R., Miyajima, A., Offermanns, S., and Zechner, R., eds) pp. 1-77, Springer, Berlin
3. Reches, M., and Gazit, E. (2004) Amyloidogenic hexapeptide fragment of medin: homology to functional amyloid polypeptide fragments. Amyloid 11, 81-89
4. Larsson, A., Söderberg, L., Westermark, G. T., Sletten, K., Engström, U., Tjernberg, L. O., Näslund, J., and Westermark, P. (2007) Unwinding fibril formation of medin, the peptide of the most common form of human amyloid. Biochem. Biophys. Res. Commun. 361, 822-828
5. Davies, H. A., Madine, J., and Middleton, D. A. (2012) Solid-state NMR reveals differences in the packing arrangements of peptide aggregates derived from the aortic amyloid polypeptide medin. J. Pept. Sci. 18, 65-72
6. Madine, J., Copland, A., Serpell, L. C., and Middleton, D. A. (2009) Cross-β spine architecture of fibrils formed by the amyloidogenic segment NFGSVQFV of medin from solid-state NMR and x-ray fiber diffraction measurements. Biochemistry 48, 3089-3099
7. Ma, B., and Nussinov, R. (2006) Simulations as analytical tools to understand protein aggregation and predict amyloid conformation. Curr. Opin. Chem. Biol. 10, 445-452
8. Tu, L.-H., and Raleigh, D. P. (2013) The role of aromatic interactions in amyloid formation by islet amyloid polypeptide. Biochemistry 52, 333-342
9. Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. U.S.A. 99, 16742-16747
10. Paravastu, A. K., Leapman, R. D., Yau, W. M., and Tycko, R. (2008) Molecular structural basis for polymorphism in Alzheimer's β-amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 105, 18349-18354
11. Gu, L., and Guo, Z. (2013) Alzheimer's Aβ42 and Aβ40 peptides form interlaced amyloid fibrils. J. Neurochem. 126, 305-311
12. Gu, L., Liu, C., and Guo, Z. (2013) Structural insights into Aβ42 oligomers using site-directed spin labeling. J. Biol. Chem. 288, 18673-18683
13. Belitzky, A., Melamed-Book, N., Weiss, A., and Raviv, U. (2011) The dynamic nature of amyloid β(1-40) aggregation. Phys. Chem. Chem. Phys. 13, 13809-13814
14. Takahashi, T., and Mihara, H. (2012) FRET detection of amyloid β-peptide oligomerization using a fluorescent protein probe presenting a pseudo-amyloid structure. Chem. Commun. 48, 1568-1570
15. Häggqvist, B., Näslund, J., Sletten, K., Westermark, G. T., Mucchiano, G., Tjernberg, L. O., Nordstedt, C., Engström, U., and Westermark, P. (1999) Medin: An integral fragment of aortic smooth muscle cell-produced lactadherin forms the most common human amyloid. Proc. Natl. Acad. Sci. U.S.A. 96, 8669-8674
16. Peng, S., Larsson, A., Wassberg, E., Gerwins, P., Thelin, S., Fu, X., and Westermark, P. (2007) Role of aggregated medin in the pathogenesis of thoracic aortic aneurysm and dissection. Lab. Invest. 87, 1195-1205
17. Peng, S., Glennert, J., and Westermark, P. (2005) Medin-amyloid: a recently characterized age-associated arterial amyloid form affects mainly arteries in the upper part of the body. Amyloid 12, 96-102
18. Fawzi, N. L., Phillips, A. H., Ruscio, J. Z., Doucleff, M., Wemmer, D. E., and Head-Gordon, T. (2008) Structure and dynamics of the Aβ(21-30) peptide from the interplay of NMR experiments and molecular simulations. J. Am. Chem. Soc. 130, 6145-6158
19. Petkova, A. T., Yau, W.-M., and Tycko, R. (2006) Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry 45, 498-512
20. Cruz, L., Rao, J. S., Teplow, D. B., and Urbanc, B. (2012) Dynamics of metastable β-hairpin structures in the folding nucleus of amyloid β-protein. J. Phys. Chem. B 116, 6311-6325
21. Berhanu, W. M., and Hansmann, U. H. E. (2012) Structure and dynamics of amyloid-β segmental polymorphisms. PLoS One 7, e41479
22. Sciarretta, K. L., Gordon, D. J., Petkova, A. T., Tycko, R., and Meredith, S. C. (2005) Aβ40-Lactam (D23/K28) models a conformation highly favorable for amyloid nucleation. Biochemistry 44, 6003-6014
23. Rezaei-Ghaleh, N., Amininasab, M., Giller, K., Kumar, S., Stündl, A., Schneider, A., Becker, S., Walter, J., and Zweckstetter, M. (2014) Turn plasticity distinguishes different modes of amyloid-β aggregation. J. Am. Chem. Soc. 136, 4913-4919
24. Levy, E., Prelli, F., and Frangione, B. (2006) Studies on the first described Alzheimer's disease amyloid β mutant, the Dutch variant. J. Alzheimers Dis. 9, 329-339
25. Nilsberth, C., Westlind-Danielsson, A., Eckman, C. B., Condron, M. M., Axelman, K., Forsell, C., Stenh, C., Luthman, J., Teplow, D. B., Younkin, S. G., Näslund, J., and Lannfelt, L. (2001) The "Arctic" APP mutation (E693G) causes Alzheimer's disease by enhanced Ab protofibril formation. Nat. Neurosci. 4, 887-893
26. Tomiyama, T., Nagata, T., Shimada, H., Teraoka, R., Fukushima, A., Kanemitsu, H., Takuma, H., Kuwano, R., Imagawa, M., Ataka, S., Wada, Y., Yoshioka, E., Nishizaki, T., Watanabe, Y., and Mori, H. (2008) A new amyloid β variant favoring oligomerization in Alzheimer's-type dementia. Ann. Neurol. 63, 377-387
27. Van Nostrand, W. E., Melchor, J. P., Cho, H. S., Greenberg, S. M., and Rebeck, G. W. (2001) Pathogenic effects of D23N Iowa mutant amyloid β-protein. J. Biol. Chem. 276, 32860-32866
28. Tagliavini, F., Rossi, G., Padovani, A., Magoni, M., Andora, G., Sgarzi, M., Bizzi, A., Savoiardo, M., Carella, F., Morbin, M., Giaccone, G., and Bugiani, O. (1999) A new βPP mutation related to hereditary cerebral haemorrhage. Alzheimers Rep. 2, S28
29. Huang, X. Q., and Miller, W. (1991) A time-efficient, linear-space local similarity algorithm. Adv. Appl. Math. 12, 337-357
30. Davies, H. A., Wilkinson, M. C., Gibson, R. P., and Middleton, D. A. (2014) Expression and purification of the aortic amyloid polypeptide medin. Protein Expr. Purif. 98, 32-37
31. Chiu, J., March, P. E., Lee, R., and Tillett, D. (2004) Site-directed, ligase-independent mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4 h. Nucleic Acids Res. 32, e174
32. Alvarez-Martinez, M. T., Fontes, P., Zomosa-Signoret, V., Arnaud, J. D., Hingant, E., Pujo-Menjouet, L., and Liautard, J. P. (2011) Dynamics of polymerization shed light on the mechanisms that lead to multiple amyloid structures of the prion protein. Biochim. Biophys. Acta 1814, 1305-1317
33. van Stokkum, I. H. M., Spoelder, H. J. W., Bloemendal, M., van Grondelle, R., and Groen, F. C. A. (1990) Estimation of protein secondary structure and error analysis from CD spectra. Anal. Biochem. 191, 110-118
34. Sreerama, N., and Woody, R. W. (2000) Estimation of protein secondary structure from CD spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
35. Manavalan, P., and Johnson W. C., Jr. (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra. Anal. Biochem. 167, 76-85
36. Dusa, A., Kaylor, J., Edridge, S., Bodner, N., Hong, D.-P., and Fink, A. L. (2006) Characterization of oligomers during α-synuclein aggregation using intrinsic tryptophan fluorescence. Biochemistry 45, 2752-2760
37. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids. J. Chem. Phys. 103, 6951-6958
38. 15N labeled membrane protein: distances between the Schiff base and aspartic acids in the active site of bacteriorhodopsin. J. Am. Chem. Soc. 123, 3507-3519
39. Wang, Y., and Jardetzky, O. (2002) Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci. 11, 852-861
40. Han, B., Liu, Y., Ginzinger, S. W., and Wishart, D. S. (2011) SHIFTX2: significantly improved protein chemical shift prediction. J. Biomol. NMR 50, 43-57
41. Ahmed, M., Davis, J., Aucoin, D., Sato, T., Ahuja, S., Aimoto, S., Elliott, J. I., Van Nostrand, W. E., and Smith, S. O. (2010) Structural conversion of neurotoxic amyloid-β(1-42) oligomers to fibrils. Nat. Struct. Mol. Biol. 17, 561-567
42. Fändrich, M. (2012) Oligomeric intermediates in amyloid formation: structure determination and mechanisms of toxicity. J. Mol. Biol. 421, 427-440
43. Kayed, R., Head, E., Sarsoza, F., Saing, T., Cotman, C. W., Necula, M., Margol, L., Wu, J., Breydo, L., Thompson, J. L., Rasool, S., Gurlo, T., Butler, P., and Glabe, C. G. (2007) Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol. Neurodegener. 2, 18
44. Glabe, C. G. (2008) Structural classification of toxic amyloid oligomers. J. Biol. Chem. 283, 29639-29643
45. Haupt, C., Leppert, J., Rönicke, R., Meinhardt, J., Yadav, J. K., Ramachandran, R., Ohlenschläger, O., Reymann, K. G., Görlach, M., and Fändrich, M. (2012) Structural basis of β-amyloid-dependent synaptic dysfunctions. Angew. Chem. Int. Ed. Engl. 51, 1576-1579
46. Madine, J., and Middleton, D. A. (2010) Comparison of aggregation enhancement and inhibition as strategies for reducing the cytotoxicity of the aortic amyloid polypeptide medin. Eur. Biophys. J. 39, 1281-1288
47. Khurana, R., Gillespie, J. R., Talapatra, A., Minert, L. J., Ionescu-Zanetti, C., Millett, I., and Fink, A. L. (2001) Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates. Biochemistry 40, 3525-3535
48. Barlow, D. J., and Thornton, J. M. (1983) Ion-pairs in proteins. J. Mol. Biol. 168, 867-885
49. Tycko, R. (2011) Solid-state NMR studies of amyloid fibril structure. Annu. Rev. Phys. Chem. 62, 279-299
50. Jayaraman, M., Kodali, R., Sahoo, B., Thakur, A. K., Mayasundari, A., Mishra, R., Peterson, C. B., and Wetzel, R. (2012) Kinetically competing huntingtin aggregation pathways control amyloid polymorphism and properties. J. Mol. Biol. 415, 881-899
51. Patke, S., Srinivasan, S., Maheshwari, R., Srivastava, S. K., Aguilera, J. J., Colón, W., and Kane, R. S. (2013) Characterization of the oligomerization and aggregation of human serum amyloid A. PLoS One 8, e64974
52. Bram, Y., Frydman-Marom, A., Yanai, I., Gilead, S., Shaltiel-Karyo, R., Amdursky, N., and Gazit, E. (2014) Apoptosis induced by islet amyloid polypeptide soluble oligomers is neutralized by diabetes-associated specific antibodies. Sci. Rep. 4, 4267
53. Lashuel, H. A., Hartley, D. M., Petre, B. M., Wall, J. S., Simon, M. N., Walz, T., and Lansbury, P. T., Jr. (2003) Mixtures of wild-type and a pathogenic (E22G) form of Aβ40 in vitro accumulate protofibrils, including amyloid pores. J. Mol. Biol. 332, 795-808
54. Caughey, B., and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298
55. Ding, T. T., Lee, S. J., Rochet, J. C., and Lansbury, P. T., Jr. (2002) Annular α-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry 41, 10209-10217
56. Kodali, R., and Wetzel, R. (2007) Polymorphism in the intermediates and products of amyloid assembly. Curr. Opin. Struct. Biol. 17, 48-57
57. Izuo, N., Murakami, K., Sato, M., Iwasaki, M., Izumi, Y., Shimizu, T., Akaike, A., Irie, K., and Kume, T. (2013) Non-toxic conformer of amyloid β may suppress amyloid β-induced toxicity in rat primary neurons: implications for a novel therapeutic strategy for Alzheimer's disease. Biochem. Biophys. Res. Commun. 438, 1-5