APPε, the ε-secretase-derived N-terminal product of the β-amyloid precursor protein, behaves as a type I protein and undergoes α-, β-, and γ-secretase cleavages

Journal of Neurochemistry

Volumn 97, Issue 3, 2006, Pages 807-817

  Lefranc Jullien, Solveig ^a   Sunyach, Claire ^a   Checler, Frédéric ^a  

^a INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

site amyloid precursor protein cleaving enzyme; secretase; secretase; Knockout; Presenilins; Processing

Indexed keywords

ALPHA SECRETASE; AMYLOID EPSILON PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; BINDING PROTEIN; DFK 167; DIFLUOROKETONE 167; GAMMA SECRETASE; GAMMA SECRETASE INHIBITOR; JLK 2; N [N (3,5 DIFLUOROPHENACETYL)ALANYL]S PHENYLGLYCINE TERT BUTYLESTER; PROTEIN KINASE C; UNCLASSIFIED DRUG; 1,2-DILINOLENOYL-3-(4-AMINOBUTYRYL)PROPANE-1,2,3-TRIOL; 3 (4 AMINOBUTYRYL) 1,2 DILINOLENOYLGLYCEROL; 4 AMINOBUTYRIC ACID; ASPARTIC PROTEINASE; BACE1 PROTEIN, HUMAN; CARBONIC ACID DERIVATIVE; DIPEPTIDE; DRUG DERIVATIVE; ENZYME INHIBITOR; HYDROXAMIC ACID; N ((2 (HYDROXYAMINOCARBONYL)METHYL) 4 METHYLPENTANOYL) 3 (2' NAPHTHYL)ALANYLALANINE, 2 AMINOETHYLAMIDE; N-((2-(HYDROXYAMINOCARBONYL)METHYL)-4-METHYLPENTANOYL)-3-(2'-NAPHTHYL)ALANYLALANINE, 2-AMINOETHYLAMIDE; PHORBOL DIBUTYRATE; PROTEINASE; SECRETASE; SODIUM CARBONATE; TRIACYLGLYCEROL;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; EMBRYO; ENZYME DEGRADATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; CELL FRACTIONATION; CELL LINE; CLASSIFICATION; COMPARATIVE STUDY; DRUG EFFECT; DRUG INTERACTION; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; IMMUNOPRECIPITATION; METABOLISM; METHODOLOGY; MUTAGENESIS; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; WESTERN BLOTTING;

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ENDOPEPTIDASES; BLOTTING, WESTERN; CARBONATES; CELL LINE, TRANSFORMED; DIPEPTIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENDOPEPTIDASES; ENZYME INHIBITORS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; HUMANS; HYDROXAMIC ACIDS; IMMUNOPRECIPITATION; MUTAGENESIS; PHORBOL 12,13-DIBUTYRATE; PROTEIN STRUCTURE, TERTIARY; SUBCELLULAR FRACTIONS; TRANSFECTION; TRIGLYCERIDES;

EID: 33645891431     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03748.x     Document Type: Article

References (60)

1. Allinson T. M. J. Parkin E. T. Turner A. J. Hooper N. M. 2003 ADAMs family members as amyloid precursor protein α-secretases. J. Neurosci. Res. 74 342 352.
2. Ancolio K. Dumanchin C. Barelli H. Warter J. M. Brice A. Campion D. Frébourg T. Checler F. 1999 Unusual phenotypic alteration of β amyloid precursor protein (βAPP) maturation by a new Val→Met βAPP-770 mutation responsible for probable early-onset Alzheimer's disease. Proc. Natl Acad. Sci. USA 96 4119 4124.
3. Andrau D. Dumanchin-Njock C. Ayral E. et al. 2003 BACE1 and BACE2 expressing human cells: characterization of βAPP-derived catabolites, design of a novel fluorimetric assay and identification of new in vitro inhibitors. J. Biol. Chem. 278 25 859 25 866.
4. Barelli H. Lebeau A. Vizzavona J. et al. 1997 Characterization of new polyclonal antibodies specific for 40 and 42 aminoacid-long amyloid β peptides: their use to examine the cell biology of presenilins and the immunohistochemistry of sporadic Alzheimer's disease and cerebral amyloid angiopathy cases. Mol. Med. 3 695 707.
5. 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. Black R. A. 1998 Evidence that tumor necrosis factor α converting enzyme is involved in regulated α-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 273 27 765 27 767.
6. Checler F. 1995 Processing of the β-amyloid precursor protein and its regulation in Alzheimer's disease. J. Neurochem. 65 1431 1444.
7. Checler F. 1999 Presenilins: multifunctional proteins involved in Alzheimer's disease pathology. Iubmb q30 LIFE 48 33 39.
8. Chen W.-J. Goldstein J. L. Brown M. S. 1990 NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265 3116 3123.
9. Chen F. Gu Y. Hasegawa H. Ruan X. Arawaka S. Fraser P. Westaway D. Mount H. St George-Hyslop P. 2002 Presenilin 1 mutations activate γ-42-secretase but reciprocally inhibit μ-secretase cleavage of APP and S3-cleavage of Notch. J. Biol. Chem. 277 36 521 36 526.
10. Chevallier N. Jiracek J. Vincent B. Baur C. P. Spillantini M. G. Goedert M. Dive V. Checler F. 1997 Examination of the role of endopeptidase 3.4.24.15 in Aβ secretion by human transfected cells. Br. J. Pharmacol. 121 556 562.
11. Citron M. 2001 Human β-secretase and Alzheimer's disease. Exp. Opin. Ther. Targets 5 341 348.
12. De Strooper B. 2003 Aph-1, Pen-2, and nicastrin with presenilin generate an active γ-secretase complex. Neuron 38 9 12.
13. Dovey H. F. John V. Anderson J. P. et al. 2001 Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J. Neurochem. 76 173 181.
14. Eggert S. Paliga K. Soba P. Evin G. Masters C. L. Weidemann A. Beyreuther K. 2004 The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves α-, β-, γ-, and ε-like cleavages. Modulation of APLP-1 processing by N-glycosylation. J. Biol. Chem. 279 18 146 18 156.
15. Esler W. P. Das C. Campbell W. A. et al. 2002 Amyloid-lowering isocoumarins are not direct inhibitors of γ-secretase. Nat. Cell. Biol. 4 E110 E111.
16. Funamoto S. Morishima-Kawashima M. Tanimura Y. Hirotani N. Saido T. C. Ihara M. 2004 Truncated carboxyl-terminal fragments of β-amyloid precursor protein are processed to amyloid β-proteins 40 and 42. Biochemistry 43 13 532 13 540.
17. Gu Y. Misonou H. Sato T. Dohmae N. Takio K. Ihara Y. 2001 Distinct intramembrane cleavages of the β-amyloid precursor protein family resembling γ-secretase-like cleavage of Notch. J. Biol. Chem. 276 35 235 35 238.
18. Haass C. 2004 Take five-BACE and the γ-secretase quartet conduct Alzheimer's amyloid β-peptide generation. EMBO J. 23 483 488.
19. Hardy J. A. Higgins G. A. 1992 Alzheimer's disease: the amyloid cascade hypothesis. Science 256 184 185.
20. Heber S. Herms J. Gajic V. et al. 2000 Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20 7951 7963.
21. Hooper N. M. Turner A. J. 2002 The search for α-secretase and its potential as a therapeutic approach to Alzheimer's disease. Curr. Med. Chem. 9 1107 1119.
22. Hooper N. M. Karran E. H. Turner A. J. 1997 Membrane protein secretases. Biochem. J. 321 265 279.
23. Kametani F. 2004 Secretion of long Aβ-related peptides processed at ε-cleavage site is dependent on the α-secretase pre-cutting. FEBS Lett. 570 73 76.
24. Koo E. H. Squazzo S. L. 1994 Evidence that production and release of amyloid β-protein involves the endocytic pathway. J. Biol. Chem. 269 17 386 17 389.
25. Kornilova A. Y. Das C. Wolfe M. S. 2003 Differential effects of inhibitors on the γ-secretasse complex: mechanistic implications. J. Biol. Chem. 278 16 470 16 473.
26. Kulic L. Walter J. Multhaup G. Teplow D. B. Baumeister R. Romig H. Capell A. Steiner H. Haass C. 2000 Separation of presenilin function in amyloid β-peptide generation and endoproteolysis of Notch. Proc. Natl Acad. Sci. USA 97 5913 5918.
27. Lai M. T. Crouthamel M. C. DiMuzio J. Pietrak B. L. Donoviel D. B. Bernstein A. Gardell S. J. Li Y. M. Hazuda D. 2006 A presenilin-independent aspartyl protease prefers the γ-42 site cleavage. J. Neurochem. 96 118 125.
28. Lammich S. Kojro E. Postina R. Gilbert S. Pfeiffer R. Jasionowski M. Haass C. Fahrenholz F. 1999 Constitutive and regulated α-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl Acad. Sci. USA 96 3922 3927.
29. Levitan D. Doyle T. G. Brousseau D. Lee M. K. Thinakaran G. Slunt H. H. Sisodia S. S. Greenwald I. 1996 Assessment of normal and mutant human presenilin function in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 93 14 940 14 944.
30. Levy-Lahad E. Wasco W. Poorkaj P. et al. 1995 Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269 973 977.
31. Liu K. Doms R. W. Lee V. M.-Y. 2002 Glu11 site cleavage and N-terminally truncated Aβ production upon BACE overexpression. Biochemistry 41 3128 3136.
32. Lopez-Perez E. Zhang Y. Franck S. J. Creemers J. Seidah N. Checler F. 2001 Constitutive α-secretase cleavage of the β-amyloid precursor protein in the furin-deficient LoVo cell line: involvement of the prohormone convertase 7 (PC7) and the disintegrin metalloprotease ADAM10. J. Neurochem. 76 1532 1539.
33. Marambaud P. Lopez-Perez E. Wilk S. Checler F. 1997 Constitutive and protein kinase C-regulated secretory cleavage of Alzheimer's β amyloid precursor protein: different control of early and late events by the proteasome. J. Neurochem. 69 2500 2505.
34. Moelhmann T. Winkler E. Xia X. et al. 2002 Presenilin-1 mutations of leucine 166 equally affect the generation of the notch and APP intracellular domains independent of their effect on Aβ42 production. Proc. Natl Acad. Sci. USA 99 8025 8030.
35. Nordstedt C. Caporaso G. L. Thyberg J. Gandy S. E. Greengard P. 1993 Identification of the Alzheimer β/A4 amyloid precursor protein in clathrin-coated vesicles purified from PC12 cells. J. Biol. Chem. 268 608 612.
36. Paganetti P. A. Lis M. Klafli H.-W. Staufenbiel M. 1996 Amyloid precursor protein truncated at any of the γ-secretase sites is not cleaved to β-amyloid. J. Neurosci. Res. 46 283 293.
37. Pardossi-Piquard R. Petit A. Kawarai T. et al. 2005 Presenilin-dependent transcriptional control of the Aβ-degrading enzyme neprilysin by intracellular domains of βAPP and APLP. Neuron 46 541 554.
38. Passer B. Pellegrini L. Russo C. Siegel R. M. Lenardio M. J. Schettini G. Bachmann M. Tabaton M. D'Adamio L. 2000 Generation of an apoptotic intracellular peptide by γ-secretase cleavage of Alzheimer's amyloid β protein precursor. J. Alz. Dis. 2 289 301.
39. Petit A. Bihel F. Alves da Costa C. Pourquié O. Kraus J. L. Checler F. 2001 New protease inhibitors prevent γ-secretase-mediated Aβ40/42 production without affecting Notch cleavage. Nat. Cell. Biol. 3 507 511.
40. Pollack S. J. Lewis H. 2005 γ-secretase inhibitors for Alzheimer's disease: challenges of a promiscuous protease. Curr. Opin. Invest. Drugs 6 35 47.
41. Rogaev E. I. Sherrington R. Rogaeva E. A. et al. 1995 Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376 775 778.
42. Sastre M. Steiner H. Fuchs K. Capell A. Multhaup G. Condron M. M. Teplow D. B. 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.
43. Sato T. Dohmae N. Qi Y. et al. 2003 Potential link between amyloid β-protein 42 and C-terminal fragment γ49-99 of β-amyloid precursor protein. J. Biol. Chem. 278 20 294 20 301.
44. Seals D. F. Courtneidgee S. A. 2003 The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17 7 30.
45. Sherrington R. Rogaev E. I. Liang Y. et al. 1995 Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375 754 760.
46. Sisodia S. 1992 β-amyloid precursor protein cleavage by a membrane-bound protease. Proc. Natl Acad. Sci. USA 89 6075 6079.
47. Sisodia S. S. St George-Hyslop P. 2002 γ-secretase, notch, Aβ and Alzheimer's disease: where do the presenilins fit in? Nat. Rev. Neurosci. 3 281 290.
48. Slack B. E. Ma L. K. Seah C. C. 2001 Constitutive shedding of the amyloid precursor protein ectodoamin is up-regulated by tumour necrosis factor-α converting enzyme. Biochem. J. 357 787 794.
49. Suh Y.-H. Checler F. 2002 Amyloid precursor protein, presenilins and α-synuclein: Molecular pathogenesis and pharmacological applications in Alzheimers' disease. Pharmacol. Rev. 54 469 525.
50. Takahara Y. Q. Morishima-Kawashima M. Tanimura Y. et al. 2005 Longer forms of amyloid β protein: implications for the mechanism of intramembrane cleavage by γ-secretase. J. Neurosci. 25 436 445.
51. Vassar R. Bennett B. D. Babu-Khan S. et al. 1999 β-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286 735 741.
52. Vincent B. Beaudet A. Dauch P. Vincent J. P. Checler F. 1996 Distinct properties of neuronal and astrocytic endopeptidase 3.4.24.16: a study on differentiation, subcellular distribution and secretion processes. J. Neurosci. 16 5049 5059.
53. Vincent B. Paitel E. Frobert Y. Lehmann S. Grassi J. Checler F. 2000 Phorbol ester-regulated cleavage of normal prion protein in HEK293 human cells and murine neurons. J. Biol. Chem. 275 35 612 35 616.
54. Weidemann A. Eggert S. Reinhard F. B. M. Vogel M. Paliga K. Baier G. Masters C. L. Beyreuther K. Evin G. 2002 A novel ε-cleavage within the transmembrane domain of the Alzheimer amyloid precursor protein demonstrates homology with the Notch processing. Biochemistry 41 2825 2835.
55. Wolfe M. S. Citron M. Diehl T. S. Xia W. Donkor I. O. Selkoe D. J. 1998 A substrate-based difluoro ketone selectively inhibits Alzheimer's γ-secretase activity. J. Med. Chem. 41 6 9.
56. Yan R. Bienkowski M. J. Shuck M. E. et al. 1999 Membrane-anchored aspartyl protease with Alzheimer's disease β-secretase activity. Nature 402 533 537.
57. Yu C. Kim S.-H. Ikeuchi T. Xu H. Gasparini L. Wang R. Sisodia S. S. 2001 Characterization of a presenilin-mediated amyloid precursor protein carboxyl terminal fragment γ: evidence for distinct mechanisms involved in γ-secretase processing of the APP and Notch 1 transmembrane domains. J. Biol. Chem. 276 43 756 43 760.
58. Zhang D. M. Levitan D. Yu G. et al. 2000 Mutation of the conserved N-terminal cysteine (Cys92) of human presenilin1 causes increased A beta secretion in mammalian cells but impaired Notch/lin-12 signalling in C. elegans. Neuroport 11 3227 3230.
59. Zhao G. Mao G. Tan J. Dong Y. Cui M.-Z. Kim S.-H. Xu X. 2004 Identification of a new presenilin-dependent ζ-cleavage site within the transmembrane domain of amyloid precursor protein. J. Biol. Chem. 279 50 647 50 650.
60. Zhao G. Cui M.-Z. Mao G. Dong Y. Tan J. Sun L. D. Xu X. 2005 γ-cleavage is dependent on ζ-cleavage during proteolytic processing of amyloid precursor protein within its transmembrane domain. J. Biol. Chem. 280 37 689 37 697.