Heparin promotes the rapid fibrillization of a peptide with low intrinsic amyloidogenicity

Biochemistry

Volumn 52, Issue 50, 2013, Pages 8984-8992

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

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID FORMATION; AMYLOID-LIKE FIBRIL; AMYLOIDOGENIC PROTEINS; COMPUTER PREDICTIONS; CYTOPLASMIC DOMAINS; GLYCOSAMINOGLYCANS; PEPTIDE AGGREGATION; TRANS-MEMBRANE PROTEINS;

GLYCOPROTEINS; POLYSACCHARIDES;

PEPTIDES;

AMYLOID; GLYCOSAMINOGLYCAN; HEPARIN; MEMBRANE PROTEIN; PEPTIDE; PHOSPHOLAMBAN;

AMYLOIDOSIS; AQUEOUS SOLUTION; ARTICLE; COMPUTER PREDICTION; CYTOTOXICITY; IN VITRO STUDY; MOLECULAR WEIGHT; PERIODICITY; PH; PRIORITY JOURNAL; PROTEIN STRUCTURE;

EID: 84890443382     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401231u     Document Type: Article

References (44)

1. Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. b., and Blake, C. C. F. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273, 729-739 (Pubitemid 27488813)
2. Sipe, J. D., Benson, M. D., Buxbaum, J. N., Ikeda, S.-I., Merlini, G., Saraiva, M. J. M., and Westermark, P. (2012) Amyloid fibril protein nomenclature: 2012 recommendations from the Nomenclature Committee of the International Society of Amyloidosis Amyloid 19, 167-170
3. Fowler, D. M., Koulov, A. V., Balch, W. E., and Kelly, J. W. (2007) Functional amyloid: From bacteria to humans Trends Biochem. Sci. 32, 217-224
4. Goldschmidt, L., Teng, P. K., Riek, R., and Eisenberg, D. (2010) Identifying the amylome, proteins capable of forming amyloid-like fibrils Proc. Natl. Acad. Sci. U.S.A. 107, 3487-3492
5. Conchillo-Sole, O., de Groot, N. S., Aviles, F. X., Vendrell, J., Daura, X., and Ventura, S. (2007) AGGRESCAN: A server for the prediction and evaluation of "hot spots" of aggregation in polypeptides BMC Bioinf. 8, 65
6. Tartaglia, G. G. and Vendruscolo, M. (2008) The Zyggregator method for predicting protein aggregation propensities Chem. Soc. Rev. 37, 1395-1401
7. Fernandez-Escamilla, A. M., Rousseau, F., Schymkowitz, J., and Serrano, L. (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins Nat. Biotechnol. 22, 1302-1306 (Pubitemid 39336784)
8. Ren, R., Hong, Z., Gong, H., Laporte, K., Skinner, M., Seldin, D. C., Costello, C. E., Connors, L. H., and Trinkaus-Randall, V. (2010) Role of Glycosaminoglycan Sulfation in the Formation of Immunoglobulin Light Chain Amyloid Oligomers and Fibrils J. Biol. Chem. 285, 37672-37682
9. Snow, A. D., Mar, H., Nochlin, D., Kimata, K., Kato, M., Suzuki, S., Hassell, J., and Wight, T. N. (1988) The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease Am. J. Pathol. 133, 456-463 (Pubitemid 19020577)
10. Noborn, F., O'Callaghan, P., Hermansson, E., Zhang, X., Ancsin, J. B., Damas, A. M., Dacklin, I., Presto, J., Johansson, J., Saraiva, M. J., Lundgren, E., Kisilevsky, R., Westermark, P., and Li, J.-P. (2011) Heparan sulfate/heparin promotes transthyretin fibrillization through selective binding to a basic motif in the protein Proc. Natl. Acad. Sci. U.S.A. 108, 5584-5589
11. Hawkes, C. A., Ng, V., and McLaurin, J. (2009) Small molecule inhibitors of Aβ-aggregation and neurotoxicity Drug Dev. Res. 70, 111-124
12. Wall, J. S., Richey, T., Stuckey, A., Donnell, R., Macy, S., Martin, E. B., Williams, A., Higuchi, K., and Kennel, S. J. (2011) In vivo molecular imaging of peripheral amyloidosis using heparin-binding peptides Proc. Natl. Acad. Sci. U.S.A. 108, E586-E594
13. Cohlberg, J. A., Li, J., Uversky, V. N., and Fink, A. L. (2002) Heparin and other glycosaminoglycans stimulate the formation of amyloid fibrils from α-synuclein in vitro Biochemistry 41, 1502-1511 (Pubitemid 34112739)
14. Jha, S., Patil, S. M., Gibson, J., Nelson, C. E., Alder, N. N., and Alexandrescu, A. T. (2011) Mechanism of Amylin Fibrillization Enhancement by Heparin J. Biol. Chem. 286, 22894-22904
15. 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, 550-553 (Pubitemid 26346185)
16. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R., and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death Nature 431, 805-810 (Pubitemid 39434070)
17. Madine, J. and Middleton, D. (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
18. Bodner, R. A., Outeiro, T. F., Altmann, S., Maxwell, M. M., Cho, S. H., Hyman, B. T., McLean, P. J., Young, A. B., Housman, D. E., and Kazantsev, A. G. (2006) Pharmacological promotion of inclusion formation: A therapeutic approach for Huntington's and Parkinson's diseases Proc. Natl. Acad. Sci. U.S.A. 103, 4246-4251
19. Maji, S. K., Perrin, M. H., Sawaya, M. R., Jessberger, S., Vadodaria, K., Rissman, R. A., Singru, P. S., Nilsson, K. P. R., Simon, R., Schubert, D., Eisenberg, D., Rivier, J., Sawchenko, P., Vale, W., and Riek, R. (2009) Functional Amyloids As Natural Storage of Peptide Hormones in Pituitary Secretory Granules Science 325, 328-332
20. Vilasi, S., Sarcina, R., Maritato, R., De Simone, A., Irace, G., and Sirangelo, I. (2011) Heparin Induces Harmless Fibril Formation in Amyloidogenic W7FW14F Apomyoglobin and Amyloid Aggregation in Wild-Type Protein in Vitro PLoS One 6, e22076
21. Fujii, J., Ueno, A., Kitano, K., Tanaka, S., Kadoma, M., and Tada, M. (1987) Complete complementary DNA-derived amino acid sequence of canine cardiac phospholamban J. Clin. Invest. 79, 301-304 (Pubitemid 17232533)
22. Hughes, E., Edwards, R., and Middleton, D. A. (2010) Heparin-derived oligosaccharides interact with the phospholamban cytoplasmic domain and stimulate SERCA function Biochem. Biophys. Res. Commun. 401, 370-375
23. Linding, R., Schymkowitz, J., Rousseau, F., Diella, F., and Serrano, L. (2004) A comparative study of the relationship between protein structure and β-aggregation in globular and intrinsically disordered proteins J. Mol. Biol. 342, 345-353 (Pubitemid 39094525)
24. Rousseau, F., Schymkowitz, J., and Serrano, L. (2006) Protein aggregation and amyloidosis: Confusion of the kinds? Curr. Opin. Struct. Biol. 16, 118-126 (Pubitemid 43221880)
25. Tartaglia, G. G., Pawar, A. P., Campioni, S., Dobson, C. M., Chiti, F., and Vendruscolo, M. (2008) Prediction of Aggregation-Prone Regions in Structured Proteins J. Mol. Biol. 380, 425-436
26. 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
27. Hussain, R., Javorfi, T., and Siligardi, G. (2012) Circular dichroism beamline B23 at the Diamond Light Source J. Synchrotron Radiat. 19, 132-135
28. Harper, J. D. and Lansbury, P. T. (1997) Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic Truths and Physiological Consequences of the Time-Dependent Solubility of Amyloid Proteins Annu. Rev. Biochem. 66, 385-407 (Pubitemid 27274662)
29. Wang, H., Cao, P., and Raleigh, D. P. (2013) Amyloid Formation in Heterogeneous Environments: Islet Amyloid Polypeptide Glycosaminoglycan Interactions J. Mol. Biol. 425, 492-505
30. Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Christian, R., Grothe, R., and Eisenberg, D. (2005) Structure of the cross-β spine of amyloid-like fibrils Nature 435, 773-775
31. Fändrich, M., Forge, V., Buder, K., Kittler, M., Dobson, C. M., and Diekmann, S. (2003) Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments Proc. Natl. Acad. Sci. U.S.A. 100, 15463-15468 (Pubitemid 38021012)
32. 2- microglobulin Nat. Struct. Biol. 9, 326-331 (Pubitemid 34462548)
33. Guijarro, J. I., Sunde, M., Jones, J. A., Campbell, I. D., and Dobson, C. M. (1998) Amyloid fibril formation by an SH3 domain Proc. Natl. Acad. Sci. U.S.A. 95, 4224-4228 (Pubitemid 28207893)
34. Bodner, R. A., Housman, D. E., and Kazantsev, A. G. (2006) New directions for neurodegenerative disease therapy: Using chemical compounds to boost the formation of mutant protein inclusions Cell Cycle 5, 1477-1480 (Pubitemid 44091963)
35. Cardin, A. D. and Weintraub, H. J. (1989) Molecular modeling of protein-glycosaminoglycan interactions Arteriosclerosis 9, 21-32 (Pubitemid 19046087)
36. Brunden, K. R., Richter-Cook, N. J., Chaturvedi, N., and Frederickson, R. C. (1993) pH-dependent binding of synthetic β-amyloid peptides to glycosaminoglycans J. Neurochem. 61, 2147-2154 (Pubitemid 23354072)
37. Elimova, E., Kisilevsky, R., and Ancsin, J. B. (2009) Heparan sulfate promotes the aggregation of HDL-associated serum amyloid A: Evidence for a proamyloidogenic histidine molecular switch FASEB J. 23, 3436-3448
38. Colon, W. and Kelly, J. W. (1992) Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro Biochemistry 31, 8654-8660
39. 2-microglobulin and amyloid formation in vitro Biochemistry 39, 8735-8746 (Pubitemid 30602783)
40. Swietnicki, W., Petersen, R., Gambetti, P., and Surewicz, W. K. (1997) pH-dependent stability and conformation of the recombinant human prion protein PrP(90-231) J. Biol. Chem. 272, 27517-27520 (Pubitemid 27473537)
41. Rostagno, A., Vidal, R., Kaplan, B., Chuba, J., Kumar, A., Elliott, J. I., Frangione, B., Gallo, G., and Ghiso, J. (1999) pH-dependent fibrillogenesis of a VκIII Bence Jones protein Br. J. Haematol. 107, 835-843 (Pubitemid 30020158)
42. 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 (Pubitemid 32242809)
43. 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. F., Terry, C. J., Feest, T. G., Zalin, A. M., and Hsuan, J. J. (1993) Human lysozyme gene mutations cause hereditary systemic amyloidosis Nature 362, 553-557 (Pubitemid 23113032)
44. Madine, J., Pandya, M. J., Hicks, M. R., Rodger, A., Yates, E. A., Radford, S. E., and Middleton, D. A. (2012) Site-Specific Identification of an Aβ Fibril-Heparin Interaction Site by Using Solid-State NMR Spectroscopy Angew. Chem., Int. Ed. 51, 13140-13143