Take five - BACE and the γ-secretase quartet conduct Alzheimer's amyloid β-peptide generation

EMBO Journal

Volumn 23, Issue 3, 2004, Pages 483-488

  Haass, Christian ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Alzheimer's disease; Amyloid peptide; Processing; Secretases

Indexed keywords

AMYLOID BETA PROTEIN; ANTERIOR PHARYNX DEFECTIVE 1 PROTEIN; BETA SECRETASE; BETA SECRETASE INHIBITOR; ENZYME INHIBITOR; GAMMA SECRETASE; GENE PRODUCT; NICASTRIN; NOTCH RECEPTOR; PRESENILIN 1; PRESENILIN 2; PROTEIN PEN2; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; BIOCHEMISTRY; BIOMEDICINE; CELL FATE; CELL MATURATION; GENE; GENE IDENTIFICATION; HUMAN; MEDICAL RESEARCH; MUSIC; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIDE EFFECT; TAKE FIVE GENE; TIME;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ENDOPEPTIDASES; ENDOPEPTIDASES; HUMANS; MEMBRANE PROTEINS;

EID: 1442264828     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600061     Document Type: Review

References (48)

1. Bennett BD, Denis P, Haniu M, Teplow DB, Kahn S, Louis JC, Citron M, Vassar R (2000) A furin-like convertase mediates propeptide cleavage of BACE, the Alzheimer's beta-secretase. J Biol Chem 275: 37712-37717
2. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, Price DL, Wong PC (2001) BACE1 is the major beta-secretase for generation of Abeta peptides by neurons. Nat Neurosci 4: 233-234
3. Cao X, Südhof TC (2001) A transcriptionally active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293: 115-120
4. Capell A, Grünberg J, Pesold B, Diehlmann A, Citron M, Nixon R, Beyreuther K, Selkoe DJ, Haass C (1998) The proteolytic fragments of the Alzheimer's disease-associated presenilin-1 form heterodimers and occur as a 100-150-kDa molecular mass complex. J Biol Chem 273: 3205-3211
5. Capell A, Meyn L, Fluhrer R, Teplow DB, Walter J, Haass C (2002) Apical sorting of beta-secretase limits amyloid beta-peptide production. J Biol Chem 277: 5637-5643
6. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, Seubert P, Vigo-Pelfrey C, Lieberburg I, Selkoe DJ (1992) Mutation of the β-amyloid precursor protein in familial Alzheimer's disease increases β-protein production. Nature 360: 672-674
7. De Strooper B (2003) Aph-1, Pen-2, and nicastrin with presenilin generate an active y-secretase complex. Neuron 38: 9-12
8. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, Von Figura K, Van Leuven F (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391: 387-390
9. Edbauer D, Winkler E, Regula JT, Pesold B, Steiner H, Haass C (2003) Reconstitution of y-secretase activity. Nat Cell Biol 5: 486-488
10. Ehehalt R, Keller P, Haass C, Thiele C, Simons K (2003) Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 160: 113-123
11. Esler WP, Kimberly WT, Ostaszewski BL, Diehl TS, Moore CL, Tsai J-Y, Rahmati T, Xia W, Selkoe DJ, Wolfe MS (2000) Transition-state analogue inhibitors of y-secretase bind directly to presenilin-1. Nat Cell Biol 2: 428-433
12. Farzan M, Schnitzler CE, Vasilieva N, Leung D, Choe H (2000) BACE2, a beta-secretase homolog, cleaves at the beta site and within the amyloid-beta region of the amyloid-beta precursor protein. Proc Natl Acad Sci USA 97: 9712-9717
13. Francis R, McGrath G, Zhang J, Ruddy DA, Sym M, Apfeld J, Nicoll M, Maxwell M, Hai B, Ellis MC, Parks AL, Xu W, Li J, Gurney M, Myers RL, Himes CS, Hiebsch RD, Ruble C, Nye JS, Curtis D (2002) aph-1 and pen-2 are required for Notch pathway signaling, γ-secretase cleavage of βAPP, and presenilin protein accumulation. Dev Cell 3: 85-97
14. Geling A, Steiner H, Willem M, Bally-Cuif L, Haass C (2002) A γ-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep 3: 688-694
15. Goutte C, Tsunozaki M, Hale VA, Priess JR (2002) APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc Natl Acad Sci USA 99: 775-779
16. Haass C, Steiner H (2002) Alzheimer disease γ-secretase: a complex story of GxGD-type presenilin proteases. Trends Cell Biol 12: 556-562
17. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353-356
18. Herreman A, Serneels L, Annaert W, Collen D, Schoonjans L, De Strooper B (2000) Total inactivation of γ-secretase activity in presenilin-deficient embryonic stem cells. Nat Cell Biol 2: 461-462
19. Hock C, Konietzko U, Streffer JR, Tracy J, Signorell A, Muller-Tillmanns B, Lemke U, Henke K, Moritz E, Garcia E, Wollmer MA, Umbricht D, de Quervain DJ, Hofmann M, Maddalena A, Papassotiropoulos A, Nitsch RM (2003) Antibodies against beta-amyloid slow cognitive decline in Alzheimer's disease. Neuron 38: 547-554
20. Hong L, Koelsch G, Lin X, Wu S, Terzyan S, Ghosh AK, Zhang XC, Tang J (2000) Structure of the protease domain of memapsin 2 (beta-secretase) complexed with inhibitor. Science 290: 150-153
21. Hu Y, Fortini ME (2003) Different cofactor activities in γ-secretase assembly: evidence for a nicastrin-Aph-1 subcomplex. J Cell Biol 161: 685-690
22. Huse JT, Pijak DS, Leslie GJ, Lee VM, Doms RW (2000) Maturation and endosomal targeting of beta-site amyloid precursor protein-cleaving enzyme. The Alzheimer's disease beta-secretase. J Biol Chem 275: 33729-33737
23. Kitazume S, Tachida Y, Oka R, Shirotani K, Saido TC, Hashimoto Y (2001) Alzheimer's beta-secretase, beta-site amyloid precursor protein-cleaving enzyme, is responsible for cleavage secretion of a Golgi-resident sialyltransferase. Proc Natl Acad Sci USA 98: 13554-13559
24. LaVoie MJ, Fraering PC, Ostaszewski BL, Ye W, Kimberly WT, Wolfe MS, Selkoe DJ (2003) Assembly of the gamma-secretase complex involves early formation of an intermediate subcomplex of Aph-1 and nicastrin. J Biol Chem 278: 37213-37222
25. Li YM, Xu M, Lai MT, Huang Q, Castro JL, DiMuzio-Mower J, Harrison T, Lellis C, Nadin A, Neduvelli JG, Register RB, Sardana MK, Shearman MS, Smith AL, Shi XP, Yin KC, Shafer JA, Gardell SJ (2000) Photoactivated γ-secretase inhibitors directed to the active site covalently label presenilin 1. Nature 405: 689-694
26. Lichtenthaler SF, Dominguez DI, Westmeyer GG, Reiss K, Haass C, Saftig P, De Strooper B, Seed B (2003) The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J Biol Chem 278: 48713-48719
27. Liu K, Doms RW, Lee VM (2002) Glull site cleavage and N-terminally truncated A beta production upon BACE overexpression. Biochemistry 41: 3128-3136
28. Luo WJ, Wang H, Li H, Kim BS, Shah S, Lee HJ, Thinakaran G, Kim TW, Yu G, Xu H (2003) PEN-2 and APH-1 coordinately regulate proteolytic processing of presenilin 1. J Biol Chem 278: 7850-7854
29. Luo Y, Bolon B, Kahn S, Bennett BD, Babu-Khan S, Denis P, Fan W, Kha H, Zhang J, Gong Y, Martin L, Louis JC, Yan Q, Richards WG, Citron M, Vassar R (2001) Mice deficient in BACE1, the Alzheimer's beta-secretase, have normal phenotype and abolished beta-amyloid generation. Nat Neurosci 4: 231-232
30. Marambaud P, Wen PH, Dutt A, Shioi J, Takashima A, Siman R, Robakis NK (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114: 635-645
31. Moehlmann T, Winkler E, Xia X, Edbauer D, Murrell J, Capell A, Kaether C, Zheng H, Ghetti B, Haass C, Steiner H (2002) Presenilin-1 mutations of leucine 166 equally affect the generation of the Notch and APP intracellular domains independent of their effect on Aβ 42 production. Proc Natl Acad Sci USA 99: 8025-8030
32. Morais VA, Crystal AS, Pijak DS, Carlin D, Costa J, Lee VM, Doms RW (2003) The transmembrane domain region of nicastrin mediates direct interactions with APH-1 and the gamma-secretase complex. J Biol Chem 278: 43284-43291
33. Okochi M, Steiner H, Fukumori A, Tanii H, Tomita T, Tanaka T, Iwatsubo T, Kudo T, Takeda M, Haass C (2002) Presenilins mediate a dual intramembraneous γ-secretase cleavage of Notch-1. EMBO J 21: 5408-5416
34. Sastre M, Steiner H, Fuchs K, Capell A, Multhaup G, Condron MM, Teplow DB, Haass C (2001) Presenilin-dependent γ-secretase processing of β-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep 2: 835-841
35. Selkoe D, Kopan R (2003) Notch and presenilin: regulated intramembrane proteolysis links development and degeneration. Annu Rev Neurosci 26: 565-597
36. Sherrington R, Rogaev EI, Liang Y, Rogaeva EA, Levesque G, Ikeda M, Chi H, Lin C, Li G, Holman K, Tsuda T, Mar L, Foncin JF, Bruni AC, Montesi MP, Sorbi S, Rainero I, Pinessi L, Nee L, Chumakov I, Pollen D, Brookes A, Sanseau P, Polinsky RJ, Wasco W, Dasilva HAR, Haines JL, Pericakvance MA, Tanzi RE, Roses AD, Fraser PE, Rommens JM, Stgeorgehyslop PH (1995) Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375: 754-760
37. Shirotani K, Edbauer D, Capell A, Schmitz J, Steiner H, Haass C (2003) Secretase activity is associated with a conformational change of nicastrin. J Biol Chem 278: 16474-16477
38. Steiner H, Kostka M, Romig H, Basset G, Pesold B, Hardy J, Capell A, Meyn L, Grim MG, Baumeister R, Fechteler K, Haass C (2000) Glycine 384 is required for presenilin-1 function and is conserved in polytopic bacterial aspartyl proteases. Nat Cell Biol 2: 848-851
39. Struhl G, Adachi A (2000) Requirements for presenilin-dependent cleavage of Notch and other transmembrane proteins. Mol Cell 6: 625-636
40. Takasugi N, Tomita T, Hayashi I, Tsuruoka M, Niimura M, Takahashi Y, Thinakaran G, Iwatsubo T (2003) The role of presenilin cofactors in the γ-secretase complex. Nature 422: 438-441
41. Vassar R (2001) The β-secretase, BACE. A prime target for Alzheimeŕs disease. J Mol Neurosci 17: 157-170
42. Walter J, Fluhrer R, Hartung B, Willem M, Kaether C, Capell A, Lammich S, Multhaup G, Haass C (2001) Phosphorylation regulates intracellular trafficking of beta-secretase. J Biol Chem 276: 14634-14641
43. Weggen S, Eriksen JL, Das P, Sagi SA, Wang R, Pietrzik CU, Findlay KA, Smith TE, Murphy MP, Bulter T, Kang DE, Marquez-Sterling N, Golde TE, Koo EH (2001) A subset of NSAIDs lower amyloidogenic Aβ42 independently of cyclooxygenase activity. Nature 414: 212-216
44. Weihofen A, Martoglio B (2003) Intramembrane-cleaving proteases: controlled liberation of functional proteins and peptides from membranes. Trends Cell Biol 13: 71-78
45. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT, Selkoe DJ (1999) Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity. Nature 398: 513-517
46. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, Beach T, Sue L, Wong P, Price D, Li R, Shen Y (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9: 3-4
47. Yu G, Nishimura M, Arawaka S, Levitan D, Zhang L, Tandon A, Song YQ, Rogaeva E, Chen F, Kawarai T, Supala A, Levesque L, Yu H, Yang DS, Holmes E, Milman P, Liang Y, Zhang DM, Xu DH, Sato C, Rogaev E, Smith M, Janus C, Zhang Y, Aebersold R, Farrer LS, Sorbi S, Bruni A, Fraser P, St George-Hyslop P (2000) Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and βAPP processing. Nature 407: 48-54
48. Zhang Z, Nadeau P, Song W, Donoviel D, Yuan M, Bernstein A, Yankner BA (2000) Presenilins are required for γ-secretase cleavage of βAPP and transmembrane cleavage of Notch-1. Nat Cell Biol 2: 463-465