Nature and significance of the interactions between amyloid fibrils and biological polyelectrolytes

Biochemistry

Volumn 45, Issue 42, 2006, Pages 12806-12815

  Calamai, Martino ^a   Kumita, Janet R ^a   Mifsud, John ^a   Parrini, Claudia ^b   Ramazzotti, Matteo ^b   Ramponi, Giampietro ^b   Taddei, Niccoló ^b   Chiti, Fabrizio ^b   Dobson, Christopher M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; AGGLOMERATION; DISEASES; MUSCLE; NUCLEIC ACIDS; PH EFFECTS;

AMYLOID FIBRILS; CYTOTOXICITY; ELECTROSTATIC REPULSION; MOLECULAR COMPONENTS;

POLYELECTROLYTES;

ACYLPHOSPHATASE; ADENOSINE TRIPHOSPHATE; AMYLOID; CALCIUM ION; DNA; GLYCOSAMINOGLYCAN; HEPARAN SULFATE; HEPARIN; LYSOZYME; MAGNESIUM ION; NUCLEIC ACID; POLYELECTROLYTE;

ALZHEIMER DISEASE; AMYLOIDOSIS; ARTICLE; CYTOTOXICITY; DNA BINDING; ELECTRICITY; FLUORESCENCE; INFRARED SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN PURIFICATION;

AMYLOID; ANIMALS; ELECTROLYTES; HEPARIN; KINETICS; MICROFIBRILS; MICROSCOPY, FLUORESCENCE; SPECTROPHOTOMETRY, INFRARED; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SWINE;

EID: 33750353368     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0610653     Document Type: Article

References (52)

1. Serpell, L. C., Sunde, M., and Blake, C. C. (1997) The molecular basis of amyloidosis, Cell. Mol. Life Sci. 53, 871-87.
2. Dobson, C. M. (2003) Protein folding and misfolding, Nature 426, 884-90.
3. Selkoe, D. J. (2003) Folding proteins in fatal ways, Nature 426, 900-4.
4. Friedereich, N., and Kekule, A. (1859) Zur amyloifrage, Arch. Pathol. Physiol. Klin. Med. 16, 50-65.
5. Diaz-Nido, J., Wandosell, F., and Avila, J. (2002) Glycosaminoglycans and beta-amyloid, prion and tau peptides in neurodegenerative diseases, Peptides 23, 1323-32.
6. van Horssen, J., Wesseling, P., van den Heuvel, L. P., de Waal, R. M., and Verbeek, M. M. (2003) Heparan sulphate proteoglycans in Alzheimer's disease and amyloid-related disorders, Lancet Neurol. 2, 482-92.
7. Ancsin, J. B. (2003) Amyloidogenesis: historical and modern observations point to heparan sulfate proteoglycans as a major culprit, Amyloid 10, 67-79.
8. Castillo, G. M., Ngo, C., Cummings, J., Wight, T. N., and Snow, A. D. (1997) Perlecan binds to the beta-amyloid proteins (A beta) of Alzheimer's disease, accelerates A beta fibril formation, and maintains A beta fibril stability, J. Neurochem. 69, 2452-65.
9. McLaurin, J., Franklin, T., Zhang, X., Deng, J., and Fraser, P. E. (1999) Interactions of Alzheimer amyloid-beta peptides with glycosaminoglycans effects on fibril nucleation and growth, Eur. J. Biochem. 266, 1101-10.
10. Goedert, M., Jakes, R., Spillantini, M. G., Hasegawa, M., Smith, M. J., and Crowther, R. A. (1996) Assembly of microtubule-associated protein tau into Alzheimer-like filaments induced by sulphated glycosaminoglycans, Nature 383, 550-3.
11. Hasegawa, M., Crowther, R. A., Jakes, R., and Goedert, M. (1997) Alzheimer-like changes in microtubule-associated protein Tau induced by sulfated glycosaminoglycans. Inhibition of microtubule binding, stimulation of phosphorylation, and filament assembly depend on the degree of sulfation, J. Biol. Chem. 272, 33118-24.
12. Cohlberg, J. A., Li, J., Uversky, V. N., and Fink, A. L. (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from alpha-synuclein in vitro, Biochemistry 41, 1502-11.
13. Yamaguchi, I., Suda, H., Tsuzuike, N., Seto, K., Seki, M., Yamaguchi, Y., Hasegawa, K., Takahashi, N., Yamamoto, S., Gejyo, F., and Naiki, H. (2003) Glycosaminoglycan and proteoglycan inhibit the depolymerization of beta2-microglobulin amyloid fibrils in vitro, Kidney Int. 64, 1080-8.
14. Ginsberg, S. D., Galvin, J. E., Chiu, T. S., Lee, V. M., Masliah, E., and Trojanowski, J. Q. (1998) RNA sequestration to pathological lesions of neurodegenerative diseases, Acta Neuropathol. 96, 487-94.
15. Kampers, T., Friedhoff, P., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (1996) RNA stimulates aggregation of microtubule-associated protein tau into Alzheimer-like paired helical filaments, FEBS Lett. 399, 344-9.
16. Deleault, N. R., Lucassen, R. W., and Supattapone, S. (2003) RNA molecules stimulate prion protein conversion, Nature 425, 717-20.
17. Cherny, D., Hoyer, W., Subramaniam, V., and Jovin, T. M. (2004) Double-stranded DNA stimulates the fibrillation of alpha-synuclein in vitro and is associated with the mature fibrils: an electron microscopy study, J. Mol. Biol. 344, 929-38.
18. Cherny, I., Rockah, L., Levy-Nissenbaum, O., Gophna, U., Ron, E. Z., and Gazit, E. (2005) The formation of Escherichia coli curli amyloid fibrils is mediated by prion-like peptide repeats, J. Mol. Biol. 352, 245-52.
19. Exley, C. (1997) ATP-promoted amyloidosis of an amyloid beta peptide, NeuroReport 8, 3411-4.
20. Exley, C., and Korchazhkina, O. V. (2001) Promotion of formation of amyloid fibrils by aluminium adenosine triphosphate (AIATP), J. Inorg. Biochem. 84, 215-24.
21. Fraser, P. E., Nguyen, J. T., Chin, D. T., and Kirschner, D. A. (1992) Effects of sulfate ions on Alzheimer beta/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions, J. Neurochem. 59, 1531-40.
22. Castillo, G. M., Cummings, J. A., Yang, W., Judge, M. E., Sheardown, M. J., Rimvall, K., Hansen, J. B., and Snow, A. D. (1998) Sulfate content and specific glycosaminoglycan backbone of perlecan are critical for perlecan's enhancement of islet amyloid polypeptide (amylin) fibril formation, Diabetes 47, 612-20.
23. Castillo, G. M., Lukito, W., Wight, T. N., and Snow, A. D. (1999) The sulfate moieties of glycosaminoglycans are critical for the enhancement of beta-amyloid protein fibril formation, J. Neurochem. 72, 1681-7.
24. Raman, B., Chatani, E., Kihara, M., Ban, T., Sakai, M., Hasegawa, K., Naiki, H., Rao Ch, M., and Goto, Y. (2005) Critical balance of electrostatic and hydrophobic interactions is required for beta 2-microglobulin amyloid fibril growth and stability, Biochemistry 44, 1288-99.
25. Chiti, F., Webster, P., Taddei, N., Clark, A., Stefani, M., Ramponi, G., and Dobson, C. M. (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils, Proc. Natl. Acad. Sci. U.S.A. 96, 3590-4.
26. Morozova-Roche, L. A., Zurdo, J., Spencer, A., Noppe, W., Receveur, V., Archer, D. B., Joniau, M., and Dobson, C. M. (2000) Amyloid fibril formation and seeding by wild-type human lysozyme and its disease-related mutational variants, J. Struct. Biol. 130, 339-51.
27. Pepys, M. B., Hawkins, P. N., Booth, D. R., Vigushin, D. M., Tennent, G. A., Soutar, A. K., Totty, N., Nguyen, O., Blake, C. C., Terry, C. J., et al. (1993) Human lysozyme gene mutations cause hereditary systemic amyloidosis, Nature 362, 553-7.
28. Valleix, S., Drunat, S., Philit, J. B., Adoue, D., Piette, J. C., Droz, D., MacGregor, B., Canet, D., Delpech, M., and Grateau, G. (2002) Hereditary renal amyloidosis caused by a new variant lysozyme W64R in a French family, Kidney Int. 61, 907-12.
29. Yazaki, M., Farrell, S. A., and Benson, M. D. (2003) A novel iysozyme mutation Phe57Ile associated with hereditary renal amyloidosis, Kidney Int. 63, 1652-7.
30. Taddei, N., Stefani, M., Magherini, F., Chiti, F., Modesti, A., Raugei, G., and Ramponi, G. (1996) Looking for residues involved in the muscle acylphosphatase catalytic mechanism and structural stabilization: role of Asn41, Thr42, and Thr46, Biochemistry 35, 7077-83.
31. van Nuland, N. A., Chiti, F., Taddei, N., Raugei, G., Ramponi, G., and Dobson, C. M. (1998) Slow folding of muscle acylphosphatase in the absence of intermediates, J. Mol. Biol. 283, 883-91.
32. Booth, D. R., Sunde, M., Bellotti, V., Robinson, C. V., Hutchinson, W. L., Fraser, P. E., Hawkins, P. N., Dobson, C. M., Radford, S. E., Blake, C. C., and Pepys, M. B. (1997) Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis, Nature 385, 787-93.
33. Ramponi, G., Treves, C., and Guerritore, A. A. (1966) Aromatic acyl phosphates as substrates of acyl phosphatase, Arch. Biochem. Biophys. 115, 129-35.
34. Jones, L. S., Yazzie, B., and Middaugh, C. R. (2004) Polyanions and the proteome, Mol. Cell. Proteomics 3, 746-69.
35. Moss, J. M., Van Damme, M. P., Murphy, W. H., and Preston, B. N. (1997) Dependence of salt concentration on glycosaminoglycan-lysozyme interactions in cartilage, Arch. Biochem. Biophys. 348, 49-55.
36. Seyrek, E., Dubin, P. L., Tribet, C., and Gamble, E. A. (2003) Ionic strength dependence of protein-polyelectrolyte interactions, Biomacromolecules 4, 273-82.
37. Calamai, M., Canale, C., Relini, A., Stefani, M., Chiti, F., and Dobson, C. M. (2005) Reversal of protein aggregation provides evidence for multiple aggregated States, J. Mol. Biol. 346, 603-16.
38. Chiti, F., Calamai, M., Taddei, N., Stefani, M., Ramponi, G., and Dobson, C. M. (2002) Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases, Proc. Natl. Acad. Sci. U.S.A. 99 (Suppl. 4), 16419-26.
39. Fandrich, M., and Dobson, C. M. (2002) The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation, EMBO J. 21, 5682-90.
40. Calamai, M., Taddei, N., Stefani, M., Ramponi, G., and Chiti, F. (2003) Relative influence of hydrophobicity and net charge in the aggregation of two homologous proteins, Biochemistry 42, 15078-83.
41. Zurdo, J., Guijarro, J. I., Jimenez, J. L., Saibil, H. R., and Dobson, C. M. (2001) Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain, J. Mol. Biol. 311, 325-40.
42. Friedhoff, P., Schneider, A., Mandelkow, E. M., and Mandelkow, E. (1998) Rapid assembly of Alzheimer-like paired helical filaments from microtubule-associated protein tau monitored by fluorescence in solution, Biochemistry 37, 10223-30.
43. Goers, J., Uversky, V. N., and Fink, A. L. (2003) Polycation-induced oligomerization and accelerated fibrillation of human alpha-synuclein in vitro, Protein Sci. 12, 702-7.
44. Antony, T., Hoyer, W., Cherny, D., Heim, G., Jovin, T. M., and Subramaniam, V. (2003) Cellular polyamines promote the aggregation of alpha-synuclein, J. Biol. Chem. 278, 3235-40.
45. Nucifora, F. C., Jr., Sasaki, M., Peters, M. F., Huang, H., Cooper, J. K., Yamada, M., Takahashi, H., Tsuji, S., Troncoso, J., Dawson, V. L., Dawson, T. M., and Ross, C. A. (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity, Science 291, 2423-8.
46. Weglicki, W., Quamme, G., Tucker, K., Haigney, M., and Resnick, L. (2005) Potassium, magnesium, and electrolyte imbalance and complications in disease management, Clin. Exp. Hypertens. 27, 95-112.
47. Vink, R. (1991) Magnesium and brain trauma, Magnesium Trace Elem. 10, 1-10.
48. Durlach, J., Durlach, V., Bac, P., Rayssiguier, Y., Bara, M., and Guiet-Bara, A. (1993) Magnesium and ageing. II. Clinical data: aetiological mechanisms and pathophysiological consequences of magnesium deficit in the elderly, Magnesium Res. 6, 379-94.
49. Toescu, E. C., Verkhratsky, A., and Landfield, P. W. (2004) Ca2+-regulation and gene expression in normal brain aging, Trends Neurosci. 27, 614-20.
50. Ferris, J. P., and Ertem, G. (1992) Oligomerization of ribonucleotides on montmorillonite: reaction of the 5′-phosphorimidazolide of adenosine, Science 257, 1387-9.
51. Hanczyc, M. M., Fujikawa, S. M., and Szostak, J. W. (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division, Science 302, 618-22.
52. Dale, T. (2006) Protein and nucleic acid together: a mechanism for the emergence of biological selection, J. Theor. Biol. 240, 337-42.