Influence of the carboxy terminus of serum amyloid A on protein oligomerization, misfolding, and fibril formation

Biochemistry

Volumn 51, Issue 14, 2012, Pages 3092-3099

  Patke, Sanket ^a   Maheshwari, Ronak ^b   Litt, Jeffrey ^a   Srinivasan, Saipraveen ^c   Aguilera, J Javier ^c   Colón, Wilfredo ^b,c   Kane, Ravi S ^a,b  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^c Rensselaer Polytechnic Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINUS; BIOPHYSICAL PROPERTIES; EQUIMOLAR AMOUNT; FIBRIL FORMATION; HEXAMERS; HIGH MOLECULAR WEIGHT; IN-VITRO; IN-VIVO; ISOFORMS; MISFOLDING; MODEL SYSTEM; MOUSE STRAIN; OCTAMERS; SERUM AMYLOID A; SOLUBLE AGGREGATES;

AMINO ACIDS; BODY FLUIDS; GLYCOPROTEINS; OLIGOMERIZATION; PROTEINS;

OLIGOMERS;

AMYLOID; PROLINE; SERUM AMYLOID A;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; AMYLOIDOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; KINETICS; MOLECULAR WEIGHT; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DENATURATION; PROTEIN FOLDING; VERTEBRATE;

AMYLOID; ANIMALS; KINETICS; MICE; MICROSCOPY, ATOMIC FORCE; MOLECULAR WEIGHT; PROTEIN FOLDING; PROTEIN ISOFORMS; SERUM AMYLOID A PROTEIN;

VERTEBRATA;

EID: 84859592416     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201903s     Document Type: Article

References (55)

1. Uhlar, C. M. and Whitehead, A. S. (1999) Serum amyloid A, the major vertebrate acute-phase reactant Eur. J. Biochem. 265, 501-523
2. McAdam, K. P. and Sipe, J. D. (1976) Murine model for human secondary amyloidosis: genetic variability of the acute-phase serum protein SAA response to endotoxins and casein J. Exp. Med. 144, 1121-1127
3. Hoffman, J. S. and Benditt, E. P. (1982) Changes in high density lipoprotein content following endotoxin administration in the mouse. Formation of serum amyloid protein-rich subfractions J. Biol. Chem. 257, 10510-10517
4. Kushner, I. (1982) The phenomenon of the acute phase response Ann. N.Y. Acad. Sci. 389, 39-48
5. Marhaug, G. (1983) 3 assays for the characterization and quantitation of human-serum amyloid-A Scand. J. Immunol. 18, 329-338
6. Gillmore, J. D., Lovat, L. B., Persey, M. R., Pepys, M. B., and Hawkins, P. N. (2001) Amyloid load and clinical outcome in AA amyloidosis in relation to circulating concentration of serum amyloid A protein Lancet 358, 24-29
7. Husebekk, A., Skogen, B., Husby, G., and Marhaug, G. (1985) Transformation of amyloid precursor SAA to protein AA and incorporation in amyloid fibrils in vivo Scand. J. Immunol. 21, 283-287
8. Westermark, G. T., Sletten, K., and Westermark, P. (1989) Massive vascular Aa-amyloidosis - a histologically and biochemically distinctive subtype of reactive systemic amyloidosis Scand. J. Immunol. 30, 605-613
9. Rocken, C. and Shakespeare, A. (2002) Pathology, diagnosis and pathogenesis of AA amyloidosis Virchows Arch. 440, 111-122
10. Gertz, M. A. and Kyle, R. A. (1991) Secondary systemic amyloidosis (Aa) - response and survival in 64 patients Amyloid Amyloidosis Int. Symp. Amyloidosis, 6th 817-820
11. Hamed, G., Heffess, C. S., Shmookler, B. M., and Wenig, B. M. (1995) Amyloid goiter - a clinicopathological study of 14 cases and review of the literature Am. J. Clin. Pathol. 104, 306-312
12. Tuglular, S., Yalcinkaya, F., Paydas, S., Oner, A., Utas, C., Bozfakioglu, S., Ataman, R., Akpolat, T., Ok, E., Sen, S., Dusunsel, R., Evrenkaya, R., and Akoglu, E. (2002) A retrospective analysis for aetiology and clinical findings of 287 secondary amyloidosis cases in Turkey Nephrol. Dial. Transplant. 17, 2003-2005
13. Husby, G., Marhaug, G., and Sletten, K. (1982) Amyloid A in systemic amyloidosis associated with cancer Cancer Res. 42, 1600-1603
14. Chung, T. F., Sipe, J. D., McKee, A., Fine, R. E., Schreiber, B. M., Liang, J. S., and Johnson, R. J. (2000) Serum amyloid A in Alzheimer's disease brain is predominantly localized to myelin sheaths and axonal membrane Amyloid 7, 105-110
15. Meek, R. L., Urielishoval, S., and Benditt, E. P. (1994) Expression of apolipoprotein serum amyloid-a messenger-RNA in human atherosclerotic lesions and cultured vascular cells - implications for serum amyloid-a function Proc. Natl. Acad. Sci. U.S.A. 91, 3186-3190
16. Liang, J. S., Sloane, J. A., Wells, J. M., Abraham, C. R., Fine, R. E., and Sipe, J. D. (1997) Evidence for local production of acute phase response apolipoprotein serum amyloid A in Alzheimer's disease brain Neurosci. Lett. 225, 73-76
17. Skinner, M., Shirahama, T., Benson, M. D., and Cohen, A. S. (1977) Murine amyloid protein Aa in casein-induced experimental amyloidosis Lab. Invest. 36, 420-427
18. Sipe, J. D., Carreras, I., Gonnerman, W. A., Cathcart, E. S., Debeer, M. C., and Debeer, F. C. (1993) Characterization of the inbred CE/J mouse strain as amyloid resistant Am. J. Pathol. 143, 1480-1485
19. Kindy, M. S. and de Beer, F. C. (1999) A mouse model for serum amyloid A amyloidosis Methods Enzymol. 309, 701-716
20. 2-terminal sequence identity with only one of two serum amyloid protein (ApoSAA) gene products J. Exp. Med. 159, 641-646
21. Meek, R. L., Hoffman, J. S., and Benditt, E. P. (1986) Amyloidogenesis - one serum amyloid-a isotype is selectively removed from the circulation J. Exp. Med. 163, 499-510
22. Shiroo, M., Kawahara, E., Nakanishi, I., and Migita, S. (1987) Specific deposition of serum amyloid A protein 2 in the mouse Scand. J. Immunol. 26, 709-716
23. 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
24. Ancsin, J. B., Elimova, E., Kisilevsky, R., and Szarek, W. A. (2004) Amyloidogenesis recapitulated in cell culture: a peptide inhibitor provides direct evidence for the role of heparan sulfate and suggests a new treatment strategy FASEB J. 18, 1749-1751
25. Wang, L., Liepnieks, J. J., Benson, M. D., and Kluve-Beckerman, B. (2000) Expression of SAA and amyloidogenesis in congenic mice of CE/J and C57BL/6 strains Amyloid 7, 26-31
26. Yu, J., Zhu, H., Guo, J., de Beer, F. C., and Kindy, M. S. (2000) Expression of mouse apolipoprotein SAA1.1 in CE/J mice: isoform-specific effects on amyloidogenesis Lab. Invest. 80, 1797-1806
27. Wang, L. M., Lashuel, H. A., Walz, T., and Colon, W. (2002) Murine apolipoprotein serum amyloid A in solution forms a hexamer containing a central channel Proc. Natl. Acad. Sci. U.S.A. 99, 15947-15952
28. Wang, L., Lashuel, H. A., and Colon, W. (2005) From hexamer to amyloid: marginal stability of apolipoprotein SAA2.2 leads to in vitro fibril formation at physiological temperature Amyloid 12, 139-148
29. Wang, Y., Srinivasan, S., Ye, Z. Q., Aguilera, J. J., Lopez, M. M., and Colon, W. (2011) Serum amyloid A 2.2 refolds into a octameric oligomer that slowly converts to a more stable hexamer Biochem. Biophys. Res. Commun. 407, 725-729
30. Westermark, G. T., Engstrom, U., and Westermark, P. (1992) The N-terminal segment of protein aa determines its fibrillogenic property Biochem. Biophys. Res. Commun. 182, 27-33
31. Ericsson, L. H., Eriksen, N., Walsh, K. A., and Benditt, E. P. (1987) Primary structure of duck amyloid protein A. The form deposited in tissues may be identical to its serum precursor FEBS Lett. 218, 11-16
32. Magy, N., Benson, M. D., Liepnieks, J. J., and Kluve-Beckerman, B. (2007) Cellular events associated with the initial phase of AA amyloidogenesis: insights from a human monocyte model Amyloid 14, 51-63
33. van der Hilst, J. (2011) Recent insights into the pathogenesis of type AA amyloidosis Sci. World J. 11, 641-650
34. Husby, G., Marhaug, G., Dowton, B., Sletten, K., and Sipe, J. D. (1994) Serum amyloid-a (SAA) - biochemistry, genetics and the pathogenesis of Aa amyloidosis Amyloid 1, 119-137
35. Zhuqiu, Y. (2008) Structural and mechanistic studies of amyloid fibril formation by serum amyloid A 2.2, in Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, Troy, NY.
36. Liang, J., Elliott-Bryant, R., Hajri, T., Sipe, J. D., and Cathcart, E. S. (1998) A unique amyloidogenic apolipoprotein serum amyloid A (apoSAA) isoform expressed by the amyloid resistant CE/J mouse strain exhibits higher affinity for macrophages than apoSAA1 and apoSAA2 expressed by amyloid susceptible CBA/J mice Biochim. Biophys. Acta 1394, 121-126
37. Jain, S. and Udgaonkar, J. B. (2008) Evidence for stepwise formation of amyloid fibrils by the mouse prion protein J. Mol. Biol. 382, 1228-1241
38. Yun, W. (2010) Investigating the structural and amyloidogenic properties of murine SAA isoforms to explore the molecular basis of amyloid A amyloidosis, in Chemistry and Chemical Biology, p 126, Rensselaer Polytechnic Institute, Troy, NY.
39. Wallace, B. A. and Mao, D. (1984) Circular-dichroism analyses of membrane-proteins-an examination of differential light-scattering and absorption flattening effects in large membrane-vesicles and membrane sheets Anal. Biochem. 142, 317-328
40. Wallace, B. A. and Teeters, C. L. (1987) Differential absorption flattening optical effects are significant in the circular dichroism spectra of large membrane fragments Biochemistry 26, 65-70
41. Ji, T. H. and Urry, D. W. (1969) Correlation of light scattering and absorption flattening effects with distortions in circular dichroism patterns of mitochondrial membrane fragments Biochem. Biophys. Res. Commun. 34, 404-411
42. Castiglioni, E., Abbate, S., Longhi, G., Gangemi, R., Lauceri, R., and Purrello, R. (2007) Absorption flattening as one cause of distortion of circular dichroism spectra of ΔRuPhen(3) ·H2TPPS complex Chirality 19, 642-646
43. Khurana, R., Coleman, C., Ionescu-Zanetti, C., Carter, S. A., Krishna, V., Grover, R. K., Roy, R., and Singh, S. (2005) Mechanism of thioflavin T binding to amyloid fibrils J. Struct. Biol. 151, 229-238
44. Naiki, H., Higuchi, K., Hosokawa, M., and Takeda, T. (1989) Fluorometric-determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin-T Anal. Biochem. 177, 244-249
45. Biancalana, M. and Koide, S. (2010) Molecular mechanism of thioflavin-T binding to amyloid fibrils Biochem. Biophys. Acta 1804, 1405-1412
46. Rasband, W. S. (1997-2005) ImageJ.
47. Abramoff, M. D., Magelhaes, P. J., and Ram, S. J. (2004) Image processing with ImageJ Biophotonics Int. 11, 36-42
48. Ancsin, J. B. and Kisilevsky, R. (1999) The heparin/heparan sulfate-binding site on apo-serum amyloid A. Implications for the therapeutic intervention of amyloidosis J. Biol. Chem. 274, 7172-7181
49. Snow, A. D. and Kisilevsky, R. (1985) Temporal relationship between glycosaminoglycan accumulation and amyloid deposition during experimental amyloidosis-a histochemical-study Lab. Invest. 53, 37-44
50. Li, J. P., Galvis, M. L. E., Gong, F., Zhang, X., Zcharia, E., Metzger, S., Vloclavsky, I., Kisilevsky, R., and Lindahl, U. (2005) In vivo fragmentation of heparan sulfate by heparanase overexpression renders mice resistant to amyloid protein A amyloidosis Proc. Natl. Acad. Sci. U.S.A. 102, 6473-6477
51. Jan, A., Hartley, D. M., and Lashuel, H. A. (2010) Preparation and characterization of toxic A β aggregates for structural and functional studies in Alzheimer's disease research Nat. Protoc. 5, 1186-1209
52. McLean, C. A., Cherny, R. A., Fraser, F. W., Fuller, S. J., Smith, M. J., Beyreuther, K., Bush, A. I., and Masters, C. L. (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease Ann. Neurol. 46, 860-866
53. 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
54. Chiti, F. and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75, 333-366
55. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300, 486-489