Heparan sulfate regulates amyloid precursor protein processing by BACE1, the Alzheimer's β-secretase

Journal of Cell Biology

Volumn 163, Issue 1, 2003, Pages 97-107

  Scholefield, Zoe ^a   Yates, Edwin A ^a   Wayne, Gareth ^b   Amour, Augustin ^b   McDowell, William ^b   Turnbull, Jeremy E ^a,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid processing; Neurodegeneration; Protease; Proteoglycan

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BACE1 INHIBITOR; BETA SECRETASE; ENZYME INHIBITOR; GW 642976A; HEPARAN SULFATE; PROTEIN BACE1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL CELL; ARTICLE; BINDING SITE; CELL SURFACE; CONTROLLED STUDY; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; REGULATORY MECHANISM;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ENDOPEPTIDASES; ENDOPEPTIDASES; HEPARIN; HEPARITIN SULFATE; HUMANS;

ANIMALIA;

EID: 0142059961     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200303059     Document Type: Article

References (45)

1. Brickman, Y.G., M.D. Ford, J.T. Gallagher, V. Nurcombe, P.F. Bartlett, and J.E. Turnbull. 1998. Structural modification of fibroblast growth factor-binding HS at a determinative stage of neural development. J. Biol. Chem. 273:4350-4359.
2. Castillo, G.M., C. Ngo, J. Cummings, T.N. Wight, and A.D. Snow. 1997. Perlecan binds to the beta-amyloid proteins (Aβ) of Alzheimer's disease, accelerates Aβ fibril formation, and maintains Aβ fibril stability. J. Neurochem. 69:2452-2465.
3. Clarris, H.J., R. Cappai, D. Heffernan, K. Beyreuther, C.L. Masters, and D.H. Small. 1997. Identification of heparin-binding domains in the APP of Alzheimer's disease by deletion mutagenesis and peptide mapping. J. Neurochem. 68:1164-1172.
4. de La Fourniere-Bessueille, L., D. Grange, and R. Buchet. 1997. Purification and spectroscopic characterization of APP from porcine brains. Eur. J. Biochem. 250:705-711.
5. Egeberg, M., R. Kjeken, S. Kolset, T. Berg, and K. Prydz. 2001. Internalization and stepwise degradation of HS proteoglycans in rat hepatocytes. Biochim. Biophys. Acta. 1541:135-149.
6. Ehehalt, R., P. Keller, C. Haass, C. Thiele, and K. Simons. 2003. Amyloidogenic processing of the Alzheimer's APP depends on lipid rafts. J. Cell Biol. 160:113-123.
7. Feyzi, E., T. Saldeen, E. Larsson, U. Lindahl, and M. Salmivirta. 1998. Age-dependent modulation of HS structure and function. J. Biol. Chem. 273:13395-13398.
8. Ford-Perriss, M., S. Guimond, U. Greferath, M. Kita, K. Grobe, H. Habuchi, K. Kimata, J. Esko, M. Murphy, and J.E. Turnbull. 2002. Variant HS synthesized in the developing mouse brain differentially regulate FGF signalling. Glycobiology. 12:721-727.
9. Fuki, I., M. Meyer, and K. Williams. 2000. Transmembrane and cytoplasmic domains of syndecan mediate a multi-step endocytic pathway involving detergent-insoluble membrane rafts. Biochem. J. 351:607-612.
10. Guimond, S., and J.E. Turnbull. 1999. Fibroblast growth factor receptor signalling is dictated by specific HS saccharides. Curr. Biol. 9:1343-1346.
11. Guimond, S., M. Maccarana, B.B. Olwin, U. Lindahl, and A.C. Rapraeger. 1993. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 268:23906-23914.
12. Haass, C., C.A. Lemere, A. Capell, M. Citron, P. Seubert, D. Schenk, L. Lannfelt, and D.J. Selkoe. 1995. The Swedish mutation causes early-onset Alzheimer's disease by β-secretase cleavage within the secretory pathway. Nat. Med. 1:1291-1296.
13. Hendriksen, J., H.S. Nottet, and H.A. Smits. 2002. Secretases as targets for drug design in Alzheimer's disease. Eur. J. Clin. Invest. 32:60-68.
14. Hong, L., G. Koelsch, X. Lin, S. Wu, S. Terzyan, A.K. Ghosh, X.C. Zhang, and J. Tang. 2000. Structure of the protease domain of memapsin 2 (β-secretase) complexed with inhibitor. Science. 290:150-153.
15. Howlett, D., D. Simmons, C. Dingwall, and G. Christie. 2000. In search of an enzyme: the β-secretase of Alzheimer's disease is an aspartic proteinase. Trends Neurosci. 23:565-570.
16. Hussain, I., D. Powell, D. Howlett, D. Tew, T.D. Meek, C. Chapman, I. Gloger, K. Murphy, C. Southan, D. Ryan, et al. 1999. Identification of a novel aspartic protease (Asp 2) as β-secretase. Mol. Cell. Neurosci. 14:419-427.
17. Kisilevsky, R., L. Lemieux, P. Fraser, X. Kong, P. Hultin, and W. Szarek. 1995. Arresting amyloidosis in vivo using small-molecule anionic sulphonates or sulphates: implications for Alzheimer's disease. Nat. Med. 1:143-148.
18. Lever, R., and C. Page. 2002. Novel drug development opportunities for heparin. Nat. Rev. Drug Discov. 1:140-148.
19. Leveugle, B., W. Ding, J. Durkin, S. Mistretta, J. Eisle, M. Matic, R. Siman, B. Greenberg, and H. Fillit. 1997. Heparin promotes β-secretase cleavage of the Alzheimer's APP. Neurochem. Int. 30:543-548.
20. Leveugle, B., W. Ding, F. Laurence, M. Dehouck, A. Scanameo, R. Cecchelli, and H. Fillit. 1998. Heparin oligosaccharides that pass the blood-brain barrier inhibit APP secretion and heparin binding to beta-amyloid peptide. J. Neurochem. 70:736-744.
21. Li, M., L. Phylip, W. Lees, J. Winther, B. Dunn, A. Wlodawer, J. Kay, and A. Gustchina. 2000. The aspartic proteinase from Saccharomyces cerevisiae folds its own inhibitor into a helix. Nat. Struct. Biol. 7:113-117.
22. Lin, X., G. Koelsch, S. Wu, D. Downs, A. Dashti, and J. Tang. 2000. Human aspartic protease memapsin 2 cleaves the β-secretase site of β-amyloid precursor protein. Proc. Natl. Acad. Sci. USA. 97:1456-1460.
23. Lindahl, B., L. Eriksson, and U. Lindahl. 1995. Structure of HS from human brain, with special regard to Alzheimer's disease. Biochem. J. 306:177-184.
24. Lindahl, B., C. Westling, G. Gimenez-Gallego, U. Lindahl, and M. Salmivirta. 1999. Common binding sites for β-amyloid fibrils and fibroblast growth factor-2 in HS from human cerebral cortex. J. Biol. Chem. 274:30631-30635.
25. McLaurin, J., T. Franklin, W. Kuhns, and P. Fraser. 1999. A sulfated proteoglycan aggregation factor mediates amyloid-β peptide fibril formation and neurotoxicity. Amyloid. 6:233-243.
26. Moir, R., R. Martins, A. Bush, D. Small, E. Milward, B. Rumble, G. Multhaup, K. Beyreuther, and C. Masters. 1992. Human brain βA4 APP of Alzheimer's disease: purification and partial characterization. J. Neurochem. 59:1490-1498.
27. Multhaup, G., H. Mechler, and C. Masters. 1995. Characterization of the high affinity heparin binding site of the Alzheimer's disease βA4 APP and its enhancement by zinc(II). J. Mol. Recognit. 8:247-257.
28. Ohshita, T., A. Nakatani, and Y. Hiroi. 1998. Purification by column chromatographies of APPs and their association with other 95 kDa protein in rat brain. J. Chromatogr. B. Biomed. Sci. Appl. 716:107-118.
29. Perez, R., S. Soriano, J. Hayes, B. Ostaszewski, W. Xia, D. Selkoe, X. Chen, G. Stokin, and E. Koo. 1999. Mutagenesis identifies new signals for APP endocytosis, turnover, and the generation of secreted fragments, including Aβ42. J. Biol. Chem. 274:18851-18856.
30. Powell, A.K., D.G. Fernig, and J.E. Turnbull. 2002. FGF receptors 1 and 2 interact differently with heparin/HS: implications for dynamic assembly of a ternary signaling complex. J. Biol. Chem. 277:28554-28563.
31. Sinha, S., J. Anderson, R. Barbour, G. Basi, R. Caccavello, D. Davis, M. Doan, H. Dovey, N. Frigon, J. Hong, et al. 1999. Purification and cloning of APP β-secretase from human brain. Nature. 402:537-540.
32. Sisodia, S., W. Annaert, S. Kim, and B. De Strooper. 2001. Gamma-secretase: never more enigmatic. Trends Neurosci. 24:52-56.
33. Snow, A., H. Mar, D. Nochlin, R. Sekiguchi, K. Kimata, Y. Koike, and T. Wight. 1990. Early accumulation of HS in neurons and in the β-amyloid protein-containing lesions of Alzheimer's disease and Down's syndrome. Am. J. Pathol. 137:1253-1270.
34. Snow, A., R. Sekiguchi, D. Nochlin, R. Kalaria, and K. Kimata. 1994. HSPG in diffuse plaques of hippocampus but not of cerebellum in Alzheimer's disease brain. Am. J. Pathol. 144:337-347.
35. Su, J., B. Cummings, and C. Cotman. 1992. Localization of HS glycosaminoglycan and PG core protein in aged brain and Alzheimer's disease. Neuroscience. 51:801-813.
36. Thinakaran, G., D. Teplow, R. Siman, B. Greenberg, and S. Sisodia. 1996. Metabolism of the Swedish APP variant in neuro2a (N2a) cells. Evidence that cleavage at the β-secretase site occurs in the Golgi apparatus. J. Biol. Chem. 271:9390-9397.
37. Turnbull, J.E., J. Hopwood, and J. Gallagher. 1999. A strategy for rapid sequencing of HS and heparin saccharides. Proc. Natl. Acad. Sci. USA. 96:2698-2703.
38. Vassar, R., B. Bennett, S. Babu-Khan, S. Kahn, E. Mendiaz, P. Denis, D. Teplow, S. Ross, P. Amarante, R. Loeloff, et al. 1999. β-Secretase cleavage of Alzheimer's APP by the transmembrane aspartic protease BACE. Science. 286:735-741.
39. Verbeek, M.M., I. Otte-Holler, R. Veerhuis, D.J. Ruiter, and R.M. De Waal. 1998. Distribution of Aβ-associated proteins in cerebrovascular amyloid of Alzheimer's disease. Acta Neuropathol. (Berl.). 96:628-636.
40. Warner, R., C. Hundt, S. Weiss, and J.E. Turnbull. 2002. Identification of the HS binding sites in cellular prion protein. J. Biol. Chem. 277:18421-18430.
41. Watson, D., A. Lander, and D. Selkoe. 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.
42. Yan, R., M. Bienkowski, M. Shuck, H. Miao, M. Tory, A. Pauley, J. Brashier, N. Stratman, W. Mathews, A. Buhl, et al. 1999. Membrane-anchored aspartyl protease with Alzheimer's disease β-secretase activity. Nature. 402:533-537.
43. Yanagishita, M. 1992. Glycosylphosphatidylinositol-anchored and core protein-intercalated HSPGs in rat ovarian granulosa cells have distinct secretory, endocytotic, and intracellular degradative pathways. J. Biol. Chem. 267:9505-9511.
44. Yates, E.A., F. Santini, M. Guerrini, A. Naggi, G. Torri, and B. Casu. 1996. 1H and 13C NMR spectral assignments of the major sequences of twelve systematically modified heparin derivatives. Carbohydr. Res. 294:15-27.
45. Yates, E.A., F. Santini, B. De Cristofano, N. Payre, C. Cosentino, M. Guerrini, A. Naggi, G. Torri, and M. Hricovini. 2000. Effect of substitution pattern on 1H, 13C NMR chemical shifts and 1J(CH) coupling constants in heparin derivatives. Carbohydr. Res. 329:239-247.