Targeting ADAM10 to lipid rafts in neuroblastoma SH-SY5Y cells impairs amyloidogenic processing of the amyloid precursor protein

Brain Research

Volumn 1296, Issue , 2009, Pages 203-215

  Harris, Benjamin ^a   Pereira, Isabel ^a   Parkin, Edward ^a  

^a LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

secretase; ADAM10; Alzheimer's disease; amyloid; glycosylphosphatidylinositol; rafts

Indexed keywords

A DISINTERGRIN AND METALLOPROTEINASE 10; AMYLOID; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; GLYCOSYLPHOSPHATIDYLINOSITOL; METALLOPROTEINASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOSOL; ENZYME LOCALIZATION; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LIPID RAFT; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION;

ADAM PROTEINS; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID ENDOPEPTIDASES; CELL LINE, TUMOR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLYCOSYLATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MEMBRANE MICRODOMAINS; MUTATION; NEUROBLASTOMA; PEPTIDE FRAGMENTS; RECEPTORS, CELL SURFACE; TUMOR SUPPRESSOR PROTEINS;

EID: 70349295148     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.07.105     Document Type: Article

References (39)

1. Anders A., Gilbert S., Garten W., Postina R., and Fahrenholz F. Regulation of the alpha-secretase ADAM10 by its prodomain and proprotein convertases. FASEB J. 15 (2001) 1837-1839
2. Bickel P.E., Scherer P.E., Schnitzer J.E., Oh P., Lisanti M.P., and Lodish H.F. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J. Biol. Chem. 272 (1997) 13793-13802
3. Buxbaum J.D., Liu K.N., Luo Y., Slack J.L., Stocking K.L., Peschon J.J., Johnson R.S., Castner B.J., Cerretti D.P., and Black R.A. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 273 (1998) 27765-27767
4. Capell A., Steiner H., Willem M., Kaiser H., Meyer C., Walter J., Lammich S., Multhaup G., and Haass C. Maturation and pro-peptide cleavage of beta-secretase. J. Biol. Chem. 275 (2000) 30849-30854
5. Cisse M.A., Sunyach C., Lefranc-Jullien S., Postina R., Vincent B., and Checler F. The disintegrin ADAM9 indirectly contributes to the physiological processing of cellular prion by modulating ADAM10 activity. J. Biol. Chem. 280 (2005) 40624-40631
6. Cordy J.M., Hussain I., Dingwall C., Hooper N.M., and Turner A.J. Exclusively targeting beta-secretase to lipid rafts by GPI-anchor addition up-regulates beta-site processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 11735-11740
7. Dautry-Varsat A. Receptor-mediated endocytosis: the intracellular journey of transferrin and its receptor. Biochimie 68 (1986) 375-381
8. Deuss M., Reiss K., and Hartmann D. Part-time alpha-secretases: the functional biology of ADAM 9, 10 and 17. Curr. Alzheimer Res. 5 (2008) 187-201
9. Ehehalt R., Keller P., Haass C., Thiele C., and Simons K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell. Biol. 160 (2003) 113-123
10. Escrevente C., Morais V.A., Keller S., Soares C.M., Altevogt P., and Costa J. Functional role of N-glycosylation from ADAM10 in processing, localization and activity of the enzyme. Biochim. Biophys. Acta 1780 (2008) 905-913
11. Fahrenholz F., and Postina R. Alpha-secretase activation-an approach to Alzheimer's disease therapy. Neurodegener. Dis. 3 (2006) 255-261
12. Haass C. Take five-BACE and the gamma-secretase quartet conduct Alzheimer's amyloid beta-peptide generation. EMBO J. 23 (2004) 483-488
13. Hooper N.M., and Turner A.J. Isolation of two differentially glycosylated forms of peptidyl-dipeptidase A (angiotensin converting enzyme) from pig brain: a re-evaluation of their role in neuropeptide metabolism. Biochem. J. 241 (1987) 625-633
14. Hur J.Y., Welander H., Behbahani H., Aoki M., Franberg J., Winblad B., Frykman S., and Tjernberg L.O. Active gamma-secretase is localized to detergent-resistant membranes in human brain. FEBS J. 275 (2008) 1174-1187
15. Hussain I., Hawkins J., Shikotra A., Riddell D.R., Faller A., and Dingwall C. Characterization of the ectodomain shedding of the beta-site amyloid precursor protein-cleaving enzyme 1 (BACE1). J. Biol. Chem. 278 (2003) 36264-36268
16. Koike H., Tomioka S., Sorimachi H., Saido T.C., Maruyama K., Okuyama A., Fujisawa-Sehara A., Ohno S., Suzuki K., and Ishiura S. Membrane-anchored metalloprotease MDC9 has an alpha-secretase activity responsible for processing the amyloid precursor protein. Biochem. J. 343 Pt. 2 (1999) 371-375
17. Kojro E., Gimpl G., Lammich S., Marz W., and Fahrenholz F. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the alpha-secretase ADAM 10. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5815-5820
18. Korade Z., and Kenworthy A.K. Lipid rafts, cholesterol, and the brain. Neuropharmacology 55 (2008) 1265-1273
19. Lammich S., Kojro E., Postina R., Gilbert S., Pfeiffer R., Jasionowski M., Haass C., and Fahrenholz F. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3922-3927
20. Mayer G., Boileau G., and Bendayan M. The proprotein convertase furin colocalizes with caveolin-1 in the Golgi apparatus and endosomes of hepatocytes. Cell. Tissue Res. 316 (2004) 55-63
21. Nakayama K. Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J. 327 Pt. 3 (1997) 625-635
22. Parkin E., and Harris B. A disintegrin and metalloproteinase (ADAM)-mediated ectodomain shedding of ADAM10. J. Neurochem. 108 (2009) 1464-1479
23. Parkin E.T., Turner A.J., and Hooper N.M. Isolation and characterization of two distinct low-density, Triton-insoluble, complexes from porcine lung membranes. Biochem. J. 319 Pt. 3 (1996) 887-896
24. Parkin E.T., Turner A.J., and Hooper N.M. Amyloid precursor protein, although partially detergent-insoluble in mouse cerebral cortex, behaves as an atypical lipid raft protein. Biochem. J. 344 Pt. 1 (1999) 23-30
25. Parkin E.T., Tan F., Skidgel R.A., Turner A.J., and Hooper N.M. The ectodomain shedding of angiotensin-converting enzyme is independent of its localisation in lipid rafts. J. Cell. Sci. 116 (2003) 3079-3087
26. Parkin E.T., Watt N.T., Hussain I., Eckman E.A., Eckman C.B., Manson J.C., Baybutt H.N., Turner A.J., and Hooper N.M. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 11062-11067
27. Pike L.J. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid. Res. 47 (2006) 1597-1598
28. Postina R., Schroeder A., Dewachter I., Bohl J., Schmitt U., Kojro E., Prinzen C., Endres K., Hiemke C., Blessing M., Flamez P., Dequenne A., Godaux E., van Leuven F., and Fahrenholz F. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J. Clin. Invest. 113 (2004) 1456-1464
29. Riddell D.R., Christie G., Hussain I., and Dingwall C. Compartmentalization of beta-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr. Biol. 11 (2001) 1288-1293
30. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81 (2001) 741-766
31. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
32. Sisodia S.S. Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 6075-6079
33. Skovronsky D.M., Moore D.B., Milla M.E., Doms R.W., and Lee V.M. Protein kinase C-dependent alpha-secretase competes with beta-secretase for cleavage of amyloid-beta precursor protein in the trans-Golgi network. J. Biol. Chem. 275 (2000) 2568-2575
34. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., Fujimoto E.K., Goeke N.M., Olson B.J., and Klenk D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150 (1985) 76-85
35. Taylor D.R., and Hooper N.M. Role of lipid rafts in the processing of the pathogenic prion and Alzheimer's amyloid-beta proteins. Semin. Cell. Dev. Biol. 18 (2007) 638-648
36. Taylor D.R., Parkin E.T., Cocklin S.L., Ault J.R., Ashcroft A.E., Turner A.J., and Hooper N.M. Role of adams in the ectodomain shedding and conformational conversion of the prion protein. J. Biol. Chem. (2009)
37. Tellier E., Canault M., Rebsomen L., Bonardo B., Juhan-Vague I., Nalbone G., and Peiretti F. The shedding activity of ADAM17 is sequestered in lipid rafts. Exp. Cell. Res. 312 (2006) 3969-3980
38. Wada S., Morishima-Kawashima M., Qi Y., Misono H., Shimada Y., Ohno-Iwashita Y., and Ihara Y. Gamma-secretase activity is present in rafts but is not cholesterol-dependent. Biochemistry 42 (2003) 13977-13986
39. Won J.S., Im Y.B., Khan M., Contreras M., Singh A.K., and Singh I. Lovastatin inhibits amyloid precursor protein (APP) beta-cleavage through reduction of APP distribution in Lubrol WX extractable low density lipid rafts. J. Neurochem. 105 (2008) 1536-1549