The sulfate moieties of glycosaminoglycans are critical for the enhancement of β-amyloid protein fibril formation

Journal of Neurochemistry

Volumn 72, Issue 4, 1999, Pages 1681-1687

  Castillo, Gerardo M ^a,b   Lukito, Widia ^a   Wight, Thomas N ^a   Snow, Alan D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b ProteoTech Inc   (United States)

Author keywords

Amyloid protein; Alzheimer's disease; Fibrillogenesis; Glycosaminoglycans; Sulfate

Indexed keywords

AMYLOID; CHONDROITIN SULFATE; CONGO RED; DERMATAN SULFATE; DEXTRAN SULFATE; GLYCOSAMINOGLYCAN; HEPARIN; PENTOSAN POLYSULFATE; PERLECAN; THIOFLAVINE;

ALZHEIMER DISEASE; ARTICLE; BINDING AFFINITY; FLUOROMETRY; HYPOTHESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; STATISTICAL ANALYSIS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOIDOSIS; ANIMALS; COLORING AGENTS; CONGO RED; FIBRINOLYTIC AGENTS; GLYCOSAMINOGLYCANS; HEPARIN; NEUROFIBRILLARY TANGLES; NEURONS; PEPTIDE FRAGMENTS; SULFATES; SWINE;

EID: 0033026552     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.721681.x     Document Type: Article

References (47)

1. Bame K. J., Danda J., Hassall A., and Tumova S. (1997) Aβ (1-40) prevents heparanase-catalyzed degradation of heparan sulfate glycosaminoglycans and proteoglycans in vitro. A role for heparan sulfate proteoglycan turnover in Alzheimer's disease. J. Biol. Chem. 272, 17005-17011.
2. Bassols A. and Massagué J. (1988) Transforming growth factor-beta regulates the expression and structure of extracellular matrix chondroitin/dermatan sulfate proteoglycans. J. Biol. Chem. 263, 3039-3045.
3. Breuer B., Schmidt G., and Kresse H. (1990) Non-uniform influence of transforming growth factor-beta on the biosynthesis of different forms of small chondroitin sulphate/dermatan sulphate proteoglycan. Biochem. J. 269, 551-554.
4. Branden 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.
5. Buee L., Ding W., Anderson J. P., Narindrasorasak S., Kisilevsky R., Boyle N. J., Robakis N. K., Delacourte A., Greenberg B., and Fillit H. M. (1993a) Binding of vascular heparan sulfate proteoglycan to Alzheimer's amyloid precursor protein is mediated in part by the N-terminal region of A4 peptide. Brain. Res. 627, 199-204.
6. Buee L., Ding W., Delacourte A., and Fillit H. (1993b) Binding of secreted human neuroblastoma proteoglycans to the Alzheimer's amyloid A4 peptide. Brain Res. 601, 154-163.
7. Castillo G. M., Ngo C., Cummings J., Wight T. N., and Snow A. D. (1997) Perlecan binds to the β-amyloid proteins (Aβ) of Alzheimer's disease, accelerates Aβ fibril formation, and maintains Aβ fibril stability. J. Neurochem. 69, 2452-2465.
8. Castillo G. M., Cummings J., Yang W., Judge M. E., Sheardown M. J., Rimvall K., Hansen J.-B., and Snow A. D. (1998) The sulfate content and specific glycosaminoglycan backbone of perlecan are critical for perlecan's enhancement of islet amyloid polypeptide fibril formation. Diabetes 47, 612-620.
9. DeWitt D. A., Silver J., Canning D. R., and Perry G. (1993) Chondroitin sulfate proteoglycans are associated with the lesions of Alzheimer's disease. Exp. Neurol. 121, 149-152.
10. Dodge G. R., Kovalszky I., Hassell J. R., and Iozzo R. V. (1990) Transforming growth factor-beta alters the expression of heparan sulfate proteoglycan in human colon carcinoma cells. J. Biol. Chem. 265, 18023-18029.
11. Dodge G. R., Boesler E. W., and Jimenez S. A. (1995) Expression of the basement membrane heparan sulfate proteoglycan (perlecan) in human synovium and in cultured human synovial cells. Lab. Invest. 73, 649-657.
12. Fransson L. A., Malström A., and Sjöberg I. (1980) Periodate oxidation and alkaline degradation of heparin related glycans. Carbohydr. Res. 80, 131-145.
13. Fraser P. E., Nguyen J. T., Chin D. T., and Kirschner D. A. (1992) Effects of sulfate ions on Alzheimerβ/A4 peptide assemblies: implications for amyloid fibril-proteoglycan interactions. J. Neurochem. 59, 1531-1540.
14. Frautschy S. A., Yang F., Calder'on L., and Cole G. M. (1996) Rodent models of Alzheimer's disease: rat Aβ infusion approaches to amyloid deposits. Neurobiol. Aging 17, 311-321.
15. Gressner A. M. (1994) Activation of proteoglycan synthesis in injured liver - a brief review of molecular and cellular aspects. Eur. J. Clin. Chem. Clin. Biochem. 32, 225-237.
16. Gupta-Bansal R., Frederickson R. C., and Brunden K. R. (1995) Proteoglycan-mediated inhibition of Aβ proteolysis. A potential cause of senile plaque accumulation. J. Biol. Chem. 270, 18666-18671.
17. Heredia A., Villena J., Romarís M., Molist A., and Bassols A. (1996) Transforming growth factor beta 1 increases the synthesis and shedding of the melanoma-specific proteoglycan in human melanoma cells. Arch. Biochem. Biophys. 333, 198-206.
18. Höök M., Lindahl U., and Iverrius P. H. (1974) Distribution of sulphate and iduronic acid residues in heparin and heparan sulphate. Biochem. J. 137, 33-43.
19. Kisilevsky R., Lemieux L. J., Fraser P. E., Kong X., 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.
20. LeVine H. III (1993) Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci. 2, 404-410.
21. LeVine H. III (1995) Thioflavin T interaction with amyloid beta-sheet structures. Amyloid Int. J. Exp. Clin. Invest. 2, 1-6.
22. Lindahl B. and Lindahl U. (1997) Amyloid-specific heparan sulfate from human liver and spleen. J. Biol. Chem. 272, 26091-26094.
23. Maresh G. A., Mueller C. Jin L.-W., and Snow A. D. (1997) Identification of a perlecan domain I (exon 5) splice variant specifically immunolocalized to the neurofibrillary tangles of Alzheimer's disease. Soc. Neurosci. Abstr. 23, 2221.
24. Naiki H. and Nakakuki K. (1996) First-order kinetic model of Alzheimer's beta-amyloid fibril extension in vitro. Lab. Invest. 74, 374-383.
25. Naiki H., Higuchi K., Nakakuki K., and Takeda T. (1991) Kinetic analysis of amyloid fibril polymerization in vitro. Lab. Invest. 65, 104-110.
26. Narindrasorasak S., Lowery D. E., Gonzalez-DeWhitt P. A., Poorman R. A., Greenberg B. D., and Kisilevsky R. (1991) High affinity interactions between the Alzheimer's beta-amyloid precursor proteins and the basement membrane form of heparan sulfate proteoglycan. J. Biol. Chem. 266, 12878-12883.
27. Perlmutter L. S. and Chui H. C. (1990) Microangiopathy, the vascular basement membrane and Alzheimer's disease: a review. Brain Res. Bull. 24, 677-686.
28. Perlmutter L. S., Barron E., and Chui H. C. (1990a) Morphologic association between microglia and senile plaque amyloid in Alzheimer's disease. Neurosci. Lett. 119, 32-36.
29. Perlmutter L. S., Chui H. C., Saperia D., and Athanikar J. (1990b) Microangiopathy and the colocalization of heparan sulfate proteoglycan with amyloid in senile plaques of Alzheimer's disease. Brain Res. 508, 13-19.
30. Puchtler H., Sweat F., and Levine M. (1962) On the binding of Congo red by amyloid. J. Histochem. Cytochem. 10, 355-364.
31. Schönherr E., Jarvelainen H. T., Sandell L. J., and Wight T. N. (1991) Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J. Biol. Chem. 266, 17640-17647.
32. Schönherr E., Beavan L. A., Hausser H., Kresse H., and Culp L. A. (1993) Differences in decorin expression by papillary and reticular fibroblasts in vivo and in vitro. Biochem. J. 290, 893-899.
33. Snow A. D. and Wight T. N. (1989) Proteoglycans in the pathogenesis of Alzheimer's disease and other amyloidoses. Neurobiol. Aging 10, 481-497.
34. 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.
35. Snow A. D., Kinsella M. G., Prather P. B., Nochlin D., Podlisny M. B., Selkoe D. J., Kisilevsky R., Hassell J. R., and Wight T. N. (1989) A characteristic binding affinity between heparan sulfate proteoglycan and the A4 amyloid protein of Alzheimer's disease. (Abstr.) J. Neurapathol. Exp. Neurol. 48, 352.
36. Snow A. D., Mar H., Nochlin D., Sekiguchi R. T., Kimata K., Koike Y., and Wight T. N. (1990) Early accumulation of heparan sulfate in neurons and in the beta-amyloid protein-containing lesions of Alzheimer's disease and Down's syndrome. Am. J. Pathol. 137, 1253-1270.
37. Snow A. D., Mar H., Nochlin D., Kresse H., and Wight T. N. (1992) Peripheral distribution of dermatan sulfate proteoglycans (decorin) in amyloid-containing plaques and their presence in neurofibrillary tangles of Alzheimer's disease. J. Histochem. Cytochem. 40, 105-113.
38. Snow A. D., Sekiguchi R., Nochlin D., Fraser P., Kimata K., Mizutani A., Arai M., Schreier W. A., and Morgan D. G. (1994a) An important role of heparan sulfate proteoglycan (perlecan) in a model system for the deposition and persistence of fibrillar Aβ-amyloid in rat brain. Neuron 12, 219-234.
39. Snow A. D., Sekiguchi R. T., Nochlin D., Kalaria R. N., and Kimata K. (1994b) Heparan sulfale proteoglycan in diffuse plaques of hippocampus but not of cerebellum in Alzheimer's disease brain. Am. J. Pathol. 144, 337-347.
40. Snow A. D., Kinsella M. G., Parks E., Sekiguchi R. T., Miller J. D., Kimata K., and Wight T. N. (1995) Differential binding of vascular cell-derived proteoglycans (perlecan, biglycan, decorin, and versican) to the beta-amyloid protein of Alzheimer's disease. Arch. Biochem. Biophys. 320, 84-95.
41. Snow A. D., Nochlin D., Sekiguchi R., and Carlson S. S. (1996) Identification in immunolocalization of a new class of proteoglycan (keratan sulfate) to the neuritic plaques of Alzheimer's disease. Exp. Neurol. 136, 305-317.
42. Su J. H., Cummings B. J., and Cotman C. (1992) Localization of heparan sulfate glycosaminoglycan and proteoglycan core protein in aged brain and Alzheimer disease. Neuroscience 51, 801-813.
43. van Gool D., David G., Lammens M., Baro R., and Dom R. (1993a) Heparan sulfate expression patterns in the amyloid deposits of patients with Alzheimer's and Lewy body type dementia. Dementia 4, 308-314.
44. van Gool D., de Strooper B., van Leuven F., Triau E., and Dom R. (1993b) Alpha 2-macroglobulin expression in neuritic-type plaques in patients with Alzheimer's disease. Neurobiol. Aging 14, 233-237.
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.
46. Wyss-Coray T., Masliah E., Mallory M., McConlogue L., Johnson-Wood K., Lin C., and Mucke L. (1997) Amyloidogenic role of cytokine TGF-β1 in transgenic mice and in Alzheimer's disease. Nature 389, 603-606.
47. Yanagishita M. and Hascall V. C. (1983) Characterization of heparan sulfate proteoglycans synthesized by rat ovarian granulosa cells in culture. J. Biol. Chem. 258, 12857-12864.