Heparin binds 8 kDa gelsolin cross-β-sheet oligomers and accelerates amyloidogenesis by hastening fibril extension

Biochemistry

Volumn 50, Issue 13, 2011, Pages 2486-2498

  Solomon, James P ^a   Bourgault, Steve ^a   Powers, Evan T ^a   Kelly, Jeffery W ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID DEPOSITS; AMYLOID FIBRIL; AMYLOID FIBRIL FORMATION; AMYLOIDOGENESIS; AMYLOIDOGENIC FRAGMENTS; AMYLOIDOGENIC PEPTIDES; ANIMAL MODEL; ELECTROSTATIC INTERACTIONS; EXTRACELLULAR MATRICES; GELSOLIN; GLYCOSAMINOGLYCANS; HEPARIN BINDING; HUMAN PLASMAS; IN-VITRO; IN-VIVO; MIMETICS; OVER-EXPRESSION; PHYSIOLOGICAL CONDITION; POSITIVELY CHARGED; REACTION MIXTURE; SECONDARY STRUCTURES; SMALL MOLECULES; SPECTROSCOPIC METHOD; THERAPEUTIC STRATEGY;

DISEASES; GLYCOPROTEINS; OLIGOMERS; PROTEINS; SPECTROSCOPIC ANALYSIS;

POLYSACCHARIDES;

AMYLOID; GELSOLIN; GLYCOSAMINOGLYCAN; HEPARIN; MONOMER; OLIGOMER; POLYSACCHARIDE;

AMYLOIDOGENESIS; AMYLOIDOSIS; ARTICLE; BETA SHEET; BINDING AFFINITY; CIRCULAR DICHROISM; CONTROLLED STUDY; CROSS LINKING; DRUG BINDING; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MEDIATOR; NERVE CELL DIFFERENTIATION; NERVE FIBER; OLIGOMERIZATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BLOOD LEVEL; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; STATIC ELECTRICITY;

AMYLOID; CIRCULAR DICHROISM; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; GELSOLIN; GLYCOSAMINOGLYCANS; HEPARIN; HUMANS; KINETICS; MICROSCOPY, ATOMIC FORCE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDE FRAGMENTS; PHYSICOCHEMICAL PHENOMENA; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STABILITY; SOLUBILITY; THIAZOLES;

ANIMALIA;

EID: 79953179308     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101905n     Document Type: Article

References (45)

1. Gandhi, N. S. and Mancera, R. L. (2008) The structure of glycosaminoglycans and their interactions with proteins Chem. Biol. Drug Des. 72, 455-482
2. Snow, A. D., Willmer, J., and Kisilevsky, R. (1987) Sulfated glycosaminoglycans: A common constituent of all amyloids Lab. Invest. 56, 120-123 (Pubitemid 17011178)
3. Young, I. D., Willmer, J. P., and Kisilevsky, R. (1989) The ultrastructural localization of sulfated proteoglycans is identical in the amyloids of Alzheimer's disease and AA, AL, senile cardiac and medullary carcinoma-associated amyloidosis Acta Neuropathol. 78, 202-209 (Pubitemid 19160925)
4. Alexandrescu, A. T. (2005) Amyloid accomplices and enforcers Protein Sci. 14, 1-12 (Pubitemid 40054111)
5. Ancsin, J. B. (2003) Amyloidogenesis: Historical and modern observations point to heparan sulfate proteoglycans as a major culprit Amyloid 10, 67-79 (Pubitemid 36936537)
6. Genedani, S., Agnati, L. F., Leo, G., Buzzega, D., Maccari, F., Carone, C., Andreoli, N., Filaferro, M., and Volpi, N. (2010) β-Amyloid fibrillation and/or hyperhomocysteinemia modify striatal patterns of hyaluronic acid and dermatan sulfate: Possible role in the pathogenesis of Alzheimer's disease Curr. Alzheimer Res. 7, 150-157
7. Bergamaschini, L., Rossi, E., Storini, C., Pizzimenti, S., Distaso, M., Perego, C., De Luigi, A., Vergani, C., and De Simoni, M. G. (2004) Peripheral treatment with enoxaparin, a low molecular weight heparin, reduces plaques and β-amyloid accumulation in a mouse model of Alzheimer's disease J. Neurosci. 24, 4181-4186 (Pubitemid 38620793)
8. Timmer, N. M., Schirris, T. J. J., Bruinsma, I. B., Otte-Holler, I., van Kuppevelt, T. H., de Waal, R. M. W., and Verbeek, M. M. (2010) Aggregation and cytotoxic properties towards cultured cerebrovascular cells of Dutch-mutated Aβ40 (DAβ(1-40)) are modulated by sulfate moieties of heparin Neurosci. Res. 66, 380-389
9. Perez, M., Wandosell, F., Colaco, C., and Avila, J. (1998) Sulphated glycosaminoglycans prevent the neurotoxicity of a human prion protein fragment Biochem. J. 335, 369-374 (Pubitemid 28491072)
10. Cortijo-Arellano, M., Ponce, J., Durany, N., and Cladera, J. (2008) Amyloidogenic properties of the prion protein fragment PrP(185-208): Comparison with Alzheimer's peptide A β(1-28), influence of heparin and cell toxicity Biochem. Biophys. Res. Commun. 368, 238-242
11. McLaurin, J., Franklin, T., Zhang, X. Q., Deng, J. P., and Fraser, P. E. (1999) Interactions of Alzheimer amyloid-β peptides with glycosaminoglycans: Effects on fibril nucleation and growth Eur. J. Biochem. 266, 1101-1110 (Pubitemid 30010129)
12. 2-microglobulin amyloid fibrils in vitro Kidney Int. 64, 1080-1088 (Pubitemid 37013846)
13. 2-microglobulin amyloid fibrils in the presence of type I collagen J. Biol. Chem. 283, 4912-4920
14. Bourgault, S., Solomon, J. P., Reixach, N., and Kelly, J. W. (2011) Sulfated glycosaminoglycans accelerate transthyretin amyloidogenesis by quaternary structural conversion Biochemistry 50, 1001-1015
15. Suk, J. Y., Zhang, F. M., Balch, W. E., Linhardt, R. J., and Kelly, J. W. (2006) Heparin accelerates gelsolin amyloidogenesis Biochemistry 45, 2234-2242 (Pubitemid 43271322)
16. Maury, C. P. J. (1991) Gelsolin-related amyloidosis: Identification of the amyloid protein in Finnish hereditary amyloidosis as a fragment of variant gelsolin J. Clin. Invest. 87, 1195-1199
17. Burtnick, L. D., Koepf, E. K., Grimes, J., Jones, E. Y., Stuart, D. I., Mclaughlin, P. J., and Robinson, R. C. (1997) The crystal structure of plasma gelsolin: Implications for actin severing, capping, and nucleation Cell 90, 661-670 (Pubitemid 27357958)
18. Sun, H. Q., Yamamoto, M., Mejillano, M., and Yin, H. L. (1999) Gelsolin, a multifunctional actin regulatory protein J. Biol. Chem. 274, 33179-33182 (Pubitemid 129511609)
19. DiNubile, M. J. (2008) Plasma gelsolin as a biomarker of inflammation Arthritis Res. Ther. 10, 124
20. Lee, P. S., Sampath, K., Karumanchi, S. A., Tamez, H., Bhan, I., Isakova, T., Gutierrez, O. M., Wolf, M., Chang, Y. C., Stossel, T. P., and Thadhani, R. (2009) Plasma gelsolin and circulating actin correlate with hemodialysis mortality J. Am. Soc. Nephrol. 20, 1140-1148
21. Kwiatkowski, D. J., Mehl, R., Izumo, S., Nadalginard, B., and Yin, H. L. (1988) Muscle is the major source of plasma gelsolin J. Biol. Chem. 263, 8239-8243
22. Kazmirski, S. L., Isaacson, R. L., An, C., Buckle, A., Johnson, C. M., Daggett, V., and Fersht, A. R. (2002) Loss of a metal-binding site in gelsolin leads to familial amyloidosis-Finnish type Nat. Struct. Biol. 9, 112-116 (Pubitemid 34132412)
23. 2+ affinity determines susceptibility to furin proteolysis and familial amyloidosis of Finnish type J. Mol. Biol. 334, 119-127 (Pubitemid 37330104)
24. 2+ stabilization EMBO J. 20, 6277-6287 (Pubitemid 33078701)
25. Kangas, H., Seidan, N. G., and Paunio, D. (2002) Role of proprotein convertases in the pathogenic processing of the amyloidosis-associated form of secretory gelsolin Amyloid 9, 83-87 (Pubitemid 34787801)
26. 2+ binding by domain 2 plays a critical role in the activation and stabilization of gelsolin Proc. Natl. Acad. Sci. U.S.A. 106, 13713-13718
27. Page, L. J., Suk, J. Y., Huff, M. E., Lim, H. J., Venable, J., Yates, J., Kelly, J. W., and Balch, W. E. (2005) Metalloendoprotease cleavage triggers gelsolin amyloidogenesis EMBO J. 24, 4124-4132 (Pubitemid 41752881)
28. Kiuru-Enari, S., Keski-Oja, J., and Haltia, M. (2005) Cutis laxa in hereditary gelsolin amyloidosis Br. J. Dermatol. 152, 250-257 (Pubitemid 40343594)
29. Kiuru, S., Matikainen, E., Kupari, M., Haltia, M., and Palo, J. (1994) Autonomic nervous system and cardiac involvement in familial amyloidosis, Finnish type (FAF) J. Neurol. Sci. 126, 40-48 (Pubitemid 24305257)
30. Kivela, T., Tarkkanen, A., Frangione, B., Ghiso, J., and Haltia, M. (1994) Ocular amyloid deposition in familial amyloidosis, Finnish: An analysis of native and variant gelsolin in Meretojas syndrome Invest. Ophthalmol. Visual Sci. 35, 3759-3769 (Pubitemid 24337989)
31. Kiuru-Enari, S., Somer, H., Seppalainen, A. M., Notkola, I. L., and Haltia, M. (2002) Neuromuscular pathology in hereditary gelsolin amyloidosis J. Neuropathol. Exp. Neurol. 61, 565-571 (Pubitemid 34603005)
32. Page, L. J., Suk, J. Y., Bazhenova, L., Fleming, S. M., Wood, M., Jiang, Y., Guo, L. T., Mizisin, A. P., Kisilevsky, R., Shelton, G. D., Balch, W. E., and Kelly, J. W. (2009) Secretion of amyloidogenic gelsolin progressively compromises protein homeostasis leading to the intracellular aggregation of proteins Proc. Natl. Acad. Sci. U.S.A. 106, 11125-11130
33. Solomon, J. P., Yonemoto, I. T., Murray, A. N., Price, J., Powers, E. T., Balch, W. E., and Kelly, J. W. (2009) The 8 and 5 kDa fragments of plasma gelsolin form amyloid fibrils by a nucleated polymerization mechanism, while the 68 kDa fragment is not amyloidogenic Biochemistry 48, 11370-11380
34. Yonemoto, I. T., Wood, M. R., Balch, W. E., and Kelly, J. W. (2009) A general strategy for the bacterial expression of amyloidogenic peptides using BCL-XL-1/2 fusions Protein Sci. 18, 1978-1986
35. Glabe, C. G., Harty, P. K., and Rosen, S. D. (1983) Preparation and properties of fluorescent polysaccharides Anal. Biochem. 130, 287-294
36. Morris, A. M., Watzky, M. A., Agar, J. N., and Finke, R. G. (2008) Fitting neurological protein aggregation kinetic data via a 2-step, Minimal/"Ockham's Razor" model: The Finke-Watzky mechanism of nucleation followed by autocatalytic surface growth Biochemistry 47, 2413-2427 (Pubitemid 351304547)
37. Seo, E. S., Blaum, B. S., Vargues, T., De Cecco, M., Deakin, J. A., Lyon, M., Barran, P. E., Campopiano, D. J., and Uhrin, D. (2010) Interaction of human β-defensin 2 (HBD2) with glycosaminoglycans Biochemistry 49, 10486-10495
38. Hawe, A., Sutter, M., and Jiskoot, W. (2008) Extrinsic fluorescent dyes as tools for protein characterization Pharm. Res. 25, 1487-1499
39. Dember, L. M., Hawkins, P. N., Hazenberg, B. P. C., Gorevic, P. D., Merlini, G., Butrimiene, I., Livneh, A., Lesnyak, O., Puechal, X., Lachmann, H. J., Obici, L., Balshaw, R., Garceau, D., Hauck, W., Skinner, M., and Eprodisate for AA Amyloidosis Trial Group (2007) Eprodisate for the treatment of renal disease in AA amyloidosis N. Engl. J. Med. 356, 2349-2360 (Pubitemid 46883769)
40. Kisilevsky, R., Ancsin, J. B., Szarek, W., and Petanceska, S. (2007) Heparan sulfate as a therapeutic target in amyloidogenesis: Prospects and possible complications Amyloid 14, 21-32 (Pubitemid 46491162)
41. Kisilevsky, R., Lemieux, L. J., Fraser, P. E., Kong, X. Q., Hultin, P. G., and Szarek, W. A. (1995) Arresting amyloidosis in vivo using small-molecule anionic sulphonates or sulphates: Implications for Alzheimer's disease Nat. Med. 1, 143-148
42. Powers, E. T. and Powers, D. L. (2008) Mechanisms of protein fibril formation: Nucleated polymerization with competing off-pathway aggregation Biophys. J. 94, 379-391
43. Ferrone, F. A. (1999) Analysis of protein aggregation kinetics. Methods Enzymol. 309, 256 - 274.
44. Motamedi-Shad, N., Monsellier, E., Torrassa, S., Relini, A., and Chiti, F. (2009) Kinetic analysis of amyloid formation in the presence of heparan sulfate: Faster unfolding and change of pathway J. Biol. Chem. 284, 29921-29934
45. Watson, D. J., Lander, A. D., and Selkoe, D. J. (1997) Heparin-binding properties of the amyloidogenic peptides Aβ and amylin: Dependence on aggregation state and inhibition by Congo red J. Biol. Chem. 272, 31617-31624 (Pubitemid 28013306)