Amyloid precursor protein mutation E682K at the alternative β-secretase cleavage β'-site increases Aβ generation

EMBO Molecular Medicine

Volumn 3, Issue 5, 2011, Pages 291-302

  Zhou, Lujia ^a,b   Brouwers, Nathalie ^a,c   Benilova, Iryna ^a,b   Vandersteen, Annelies ^a,d   Mercken, Marc ^e   Van Laere, Koen ^f   Van Damme, Philip ^b   Demedts, David ^b   Van Leuven, Fred ^b   Sleegers, Kristel ^a,c   Broersen, Kerensa ^a,d   Van Broeckhoven, Christine ^a,c   Vandenberghe, Rik ^b   De Strooper, Bart ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e JANSSEN RESEARCH FOUNDATION   (Belgium)

^f UNIVERSITY HOSPITALS LEUVEN   (Belgium)

Author keywords

' site cleavage; A ; Alzheimer's disease; APP; BACE1; E682K

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1;

ADULT; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CASE REPORT; CONTROLLED STUDY; EMBRYO; FEMALE; GENE MUTATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN PROCESSING; PROTEIN SYNTHESIS;

AMINO ACID SUBSTITUTION; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ASPARTIC ACID ENDOPEPTIDASES; HUMANS; MUTANT PROTEINS; MUTATION, MISSENSE;

EID: 79955602314     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201100138     Document Type: Article

References (49)

1. Annaert WG, Levesque L, Craessaerts K, Dierinck I, Snellings G, Westaway D, George-Hyslop PS, Cordell B, Fraser P, De Strooper B (1999) Presenilin 1 controls gamma-secretase processing of amyloid precursor protein in pre-golgi compartments of hippocampal neurons. J Cell Biol 147: 277- 294
2. Annaert WG, Esselens C, Baert V, Boeve C, Snellings G, Cupers P, Craessaerts K, De Strooper B (2001) Interaction with telencephalin and the amyloid precursor protein predicts a ring structure for presenilins. Neuron 32: 579- 589
3. Bentahir M, Nyabi O, Verhamme J, Tolia A, Horre K, Wiltfang J, Esselmann H, De Strooper B (2006) Presenilin clinical mutations can affect gamma-secretase activity by different mechanisms. J Neurochem 96: 732- 742
4. Betts V, Leissring MA, Dolios G, Wang R, Selkoe DJ, Walsh DM (2008) Aggregation and catabolism of disease-associated intra-Abeta mutations: reduced proteolysis of AbetaA21G by neprilysin. Neurobiol Dis 31: 442- 450
5. Brouwers N, Sleegers K, Van Broeckhoven C (2008) Molecular genetics of Alzheimer's disease: an update. Ann Med 40: 562- 583
6. Citron M, Oltersdorf T, Haass C, McConlogue L, Hung AY, Seubert P, Vigo-Pelfrey C, Lieberburg I, Selkoe DJ (1992) Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 360: 672- 674
7. Creemers JW, Ines Dominguez D, Plets E, Serneels L, Taylor NA, Multhaup G, Craessaerts K, Annaert W, De Strooper B (2001) Processing of beta-secretase by furin and other members of the proprotein convertase family. J Biol Chem 276: 4211- 4217
8. De Jonghe C, Esselens C, Kumar-Singh S, Craessaerts K, Serneels S, Checler F, Annaert W, Van Broeckhoven C, De Strooper B (2001) Pathogenic APP mutations near the gamma-secretase cleavage site differentially affect Abeta secretion and APP C-terminal fragment stability. Hum Mol Genet 10: 1665- 1671
9. De Strooper B (2003) Aph-1, Pen-2, and nicastrin with presenilin generate an active gamma-secretase complex. Neuron 38: 9- 12
10. De Strooper B, Annaert W (2010) Novel research horizons for presenilins and gamma-secretases in cell biology and disease. Annu Rev Cell Dev Biol 26: 235- 260
11. De Strooper B, Simons M, Multhaup G, Van Leuven F, Beyreuther K, Dotti CG (1995) Production of intracellular amyloid-containing fragments in hippocampal neurons expressing human amyloid precursor protein and protection against amyloidogenesis by subtle amino acid substitutions in the rodent sequence. EMBO J 14: 4932- 4938
12. Demeester N, Mertens C, Caster H, Goethals M, Vandekerckhove J, Rosseneu M, Labeur C (2001) Comparison of the aggregation properties, secondary structure and apoptotic effects of wild-type, Flemish and Dutch N-terminally truncated amyloid beta peptides. Eur J Neurosci 13: 2015- 2024
13. Di Fede G, Catania M, Morbin M, Rossi G, Suardi S, Mazzoleni G, Merlin M, Giovagnoli AR, Prioni S, Erbetta A, et al (2009) A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis. Science 323: 1473- 1477
14. Guerreiro RJ, Baquero M, Blesa R, Boada M, Bras JM, Bullido MJ, Calado A, Crook R, Ferreira C, Frank A, et al (2010) Genetic screening of Alzheimer's disease genes in Iberian and African samples yields novel mutations in presenilins and APP. Neurobiol Aging 31: 725- 731
15. Haass C, Hung AY, Selkoe DJ, Teplow DB (1994) Mutations associated with a locus for familial Alzheimer's disease result in alternative processing of amyloid beta-protein precursor. J Biol Chem 269: 17741- 17748
16. Hendriks L, van Duijn CM, Cras P, Cruts M, Van Hul W, van Harskamp F, Warren A, McInnis MG, Antonarakis SE, Martin JJ, et al (1992) Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the beta-amyloid precursor protein gene. Nat Genet 1: 218- 221
17. Hoey SE, Williams RJ, Perkinton MS (2009) Synaptic NMDA receptor activation stimulates alpha-secretase amyloid precursor protein processing and inhibits amyloid-beta production. J Neurosci 29: 4442- 4460
18. Huse JT, Liu K, Pijak DS, Carlin D, Lee VM, Doms RW (2002) Beta-secretase processing in the trans-golgi network preferentially generates truncated amyloid species that accumulate in Alzheimer's disease brain. J Biol Chem 277: 16278- 16284
19. Hussain I, Powell D, Howlett DR, Tew DG, Meek TD, Chapman C, Gloger IS, Murphy KE, Southan CD, Ryan DM, et al (1999) Identification of a novel aspartic protease (Asp 2) as beta-secretase. Mol Cell Neurosci 14: 419- 427
20. Kimberly WT, Zheng JB, Town T, Flavell RA, Selkoe DJ (2005) Physiological regulation of the beta-amyloid precursor protein signaling domain by c-Jun N-terminal kinase JNK3 during neuronal differentiation. J Neurosci 25: 5533- 5543
21. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, Bergstrom M, Savitcheva I, Huang GF, Estrada S, et al (2004) Imaging brain amyloid in Alzheimer's disease with Pittsburgh compound-B. Ann Neurol 55: 306- 319
22. Klunk WE, Price JC, Mathis CA, Tsopelas ND, Lopresti BJ, Ziolko SK, Bi W, Hoge JA, Cohen AD, Ikonomovic MD, et al (2007) Amyloid deposition begins in the striatum of presenilin-1 mutation carriers from two unrelated pedigrees. J Neurosci 27: 6174- 6184
23. Kwok JB, Li QX, Hallupp M, Whyte S, Ames D, Beyreuther K, Masters CL, Schofield PR (2000) Novel Leu723Pro amyloid precursor protein mutation increases amyloid beta42(43) peptide levels and induces apoptosis. Ann Neurol 47: 249- 253
24. Lichtenthaler SF, Multhaup G, Masters CL, Beyreuther K (1999) A novel substrate for analyzing Alzheimer's disease gamma-secretase. FEBS Lett 453: 288- 292
25. Lin X, Koelsch G, Wu S, Downs D, Dashti A, Tang J (2000) Human aspartic protease memapsin 2 cleaves the beta-secretase site of beta-amyloid precursor protein. Proc Natl Acad Sci USA 97: 1456- 1460
26. Liu K, Doms RW, Lee VM (2002) Glu11 site cleavage and N-terminally truncated Abeta production upon BACE overexpression. Biochemistry 41: 3128- 3136
27. Liu K, Solano I, Mann D, Lemere C, Mercken M, Trojanowski JQ, Lee VM (2006) Characterization of Abeta11-40/42 peptide deposition in Alzheimer's disease and young Down's syndrome brains: implication of N-terminally truncated Abeta species in the pathogenesis of Alzheimer's disease. Acta Neuropathol 112: 163- 174
28. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, et al (2009) Finding the missing heritability of complex diseases. Nature 461: 747- 753
29. Nelissen N, Vandenbulcke M, Fannes K, Verbruggen A, Peeters R, Dupont P, Van Laere K, Bormans G, Vandenberghe R (2007) Abeta amyloid deposition in the language system and how the brain responds. Brain 130: 2055- 2069
30. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, Forsell C, Stenh C, Luthman J, Teplow DB, Younkin SG, et al (2001) The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 4: 887- 893
31. Ono K, Condron MM, Teplow DB Effects of the english (H6R) and tottori (D7N) familial Alzheimer disease mutations on amyloid {beta}-protein assembly and toxicity. J Biol Chem 285: 23186- 23197
32. Qahwash I, He W, Tomasselli A, Kletzien RF, Yan R (2004) Processing amyloid precursor protein at the beta-site requires proper orientation to be accessed by BACE1. J Biol Chem 279: 39010- 39016
33. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, Bird TD, Hardy J, Hutton M, Kukull W, et al (1996) Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 2: 864- 870
34. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741- 766
35. Sherrington R, Froelich S, Sorbi S, Campion D, Chi H, Rogaeva EA, Levesque G, Rogaev EI, Lin C, Liang Y, et al (1996) Alzheimer's disease associated with mutations in presenilin 2 is rare and variably penetrant. Hum Mol Genet 5: 985- 988
36. Singleton AB, Hardy J, Traynor BJ, Houlden H (2010) Towards a complete resolution of the genetic architecture of disease. Trends Genet 26: 438- 442
37. Sinha S, Anderson JP, Barbour R, Basi GS, Caccavello R, Davis D, Doan M, Dovey HF, Frigon N, Hong J, et al (1999) Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 402: 537- 540
38. Suzuki N, Cheung TT, Cai XD, Odaka A, Otvos L, Jr., Eckman C, Golde TE, Younkin SG (1994) An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science 264: 1336- 1340
39. Takami M, Nagashima Y, Sano Y, Ishihara S, Morishima-Kawashima M, Funamoto S, Ihara Y (2009) Gamma-secretase: successive tripeptide and tetrapeptide release from the transmembrane domain of beta-carboxyl terminal fragment. J Neurosci 29: 13042- 13052
40. Theuns J, Marjaux E, Vandenbulcke M, Van Laere K, Kumar-Singh S, Bormans G, Brouwers N, Van den Broeck M, Vennekens K, Corsmit E, et al (2006) Alzheimer dementia caused by a novel mutation located in the APP C-terminal intracytosolic fragment. Hum Mutat 27: 888- 896
41. Tian Y, Bassit B, Chau D, Li YM (2010) An APP inhibitory domain containing the Flemish mutation residue modulates gamma-secretase activity for Abeta production. Nat Struct Mol Biol 17: 151- 158
42. Tomiyama T, Nagata T, Shimada H, Teraoka R, Fukushima A, Kanemitsu H, Takuma H, Kuwano R, Imagawa M, Ataka S, et al (2008) A new amyloid beta variant favoring oligomerization in Alzheimer's-type dementia. Ann Neurol 63: 377- 387
43. Tsubuki S, Takaki Y, Saido TC (2003) Dutch, Flemish, Italian, and Arctic mutations of APP and resistance of Abeta to physiologically relevant proteolytic degradation. Lancet 361: 1957- 1958
44. Turner RT, III, Koelsch G, Hong L, Castanheira P, Ermolieff J, Ghosh AK, Tang J (2001) Subsite specificity of memapsin 2 (beta-secretase): implications for inhibitor design. Biochemistry 40: 10001- 10006
45. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, et al (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735- 741
46. Weckx S, Del-Favero J, Rademakers R, Claes L, Cruts M, De Jonghe P, Van Broeckhoven C, De Rijk P (2005) NovoSNP, a novel computational tool for sequence variation discovery. Genome Res 15: 436- 442
47. Wilquet V, De Strooper B (2004) Amyloid-beta precursor protein processing in neurodegeneration. Curr Opin Neurobiol 14: 582- 588
48. Yan R, Bienkowski MJ, Shuck ME, Miao H, Tory MC, Pauley AM, Brashier JR, Stratman NC, Mathews WR, Buhl AE, et al (1999) Membrane-anchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature 402: 533- 537
49. Yang HC, Chai X, Mosior M, Kohn W, Boggs LN, Erickson JA, McClure DB, Yeh WK, Zhang L, Gonzalez-DeWhitt P, et al (2004) Biochemical and kinetic characterization of BACE1: investigation into the putative species-specificity for beta- and beta'-cleavage sites by human and murine BACE1. J Neurochem 91: 1249- 1259