Conformational changes induced by the A21G flemish mutation in the amyloid PRECURSOR PROTEIN LEAD to INCREASED Aβ production

Structure

Volumn 22, Issue 3, 2014, Pages 387-396

  Tang, Tzu Chun ^a   Hu, Yi ^a   Kienlen Campard, Pascal ^b   El Haylani, Laetitia ^b   Decock, Marie ^b   Van Hees, Joanne ^b   Fu, Ziao ^a   Octave, Jean Noel ^b   Constantinescu, Stefan N ^b   Smith, Steven O ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CHOLESTEROL; GLYCINE; LEUCINE; LIPID BILAYER;

ALPHA HELIX; ANIMAL CELL; ARTICLE; ARTIFICIAL MEMBRANE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; INFRARED SPECTROSCOPY; MOUSE; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; ALZHEIMER DISEASE; ANIMAL; BIOSYNTHESIS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL LINE; CRICETULUS; GENETICS; HUMAN; LIPID BILAYER; METABOLISM; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL MEMBRANE; CHO CELLS; CHOLESTEROL; CRICETULUS; HUMANS; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84896691683     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.12.012     Document Type: Article

References (35)

1. J.J. Balbach, Y. Ishii, O.N. Antzutkin, R.D. Leapman, N.W. Rizzo, F. Dyda, J. Reed, and R. Tycko Amyloid fibril formation by A beta 16-22, a seven-residue fragment of the Alzheimer's β-amyloid peptide, and structural characterization by solid state NMR Biochemistry 39 2000 13748 13759
2. P.J. Barrett, Y. Song, W.D. Van Horn, E.J. Hustedt, J.M. Schafer, A. Hadziselimovic, A.J. Beel, and C.R. Sanders The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol Science 336 2012 1168 1171
3. A.J. Beel, C.K. Mobley, H.J. Kim, F. Tian, A. Hadziselimovic, B. Jap, J.H. Prestegard, and C.R. Sanders Structural studies of the transmembrane C-terminal domain of the amyloid precursor protein (APP): does APP function as a cholesterol sensor? Biochemistry 47 2008 9428 9446
4. V. Betts, M.A. Leissring, G. Dolios, R. Wang, D.J. Selkoe, and D.M. Walsh Aggregation and catabolism of disease-associated intra-Abeta mutations: reduced proteolysis of AbetaA21G by neprilysin Neurobiol. Dis. 31 2008 442 450
5. D. Burdick, B. Soreghan, M. Kwon, J. Kosmoski, M. Knauer, A. Henschen, J. Yates, C. Cotman, and C. Glabe Assembly and aggregation properties of synthetic Alzheimer's A4/β amyloid peptide analogs J. Biol. Chem. 267 1992 546 554
6. R.O. Calderon, B. Attema, and G.H. DeVries Lipid composition of neuronal cell bodies and neurites from cultured dorsal root ganglia J. Neurochem. 64 1995 424 429
7. C. De Jonghe, C. Zehr, D. Yager, C.M. Prada, S. Younkin, L. Hendriks, C. Van Broeckhoven, and C.B. Eckman Flemish and Dutch mutations in amyloid β precursor protein have different effects on amyloid β secretion Neurobiol. Dis. 5 1998 281 286
8. S. Funamoto, M. Morishima-Kawashima, Y. Tanimura, N. Hirotani, T.C. Saido, and Y. Ihara Truncated carboxyl-terminal fragments of β-amyloid precursor protein are processed to amyloid β-proteins 40 and 42 Biochemistry 43 2004 13532 13540
9. T.J. Grabowski, H.S. Cho, J.P. Vonsattel, G.W. Rebeck, and S.M. Greenberg Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy Ann. Neurol. 49 2001 697 705
10. L. Hendriks, C.M. van Duijn, P. Cras, M. Cruts, W. Van Hul, F. van Harskamp, A. Warren, M.G. McInnis, S.E. Antonarakis, and J.J. Martin et al. Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the β-amyloid precursor protein gene Nat. Genet. 1 1992 218 221
11. H. Inouye, K.A. Gleason, D. Zhang, S.M. Decatur, and D.A. Kirschner Differential effects of Phe19 and Phe20 on fibril formation by amyloidogenic peptide A β 16-22 (Ac-KLVFFAE-NH2) Proteins 78 2010 2306 2321
12. K. Kamino, H.T. Orr, H. Payami, E.M. Wijsman, M.E. Alonso, S.M. Pulst, L. Anderson, S. O'dahl, E. Nemens, and J.A. White et al. Linkage and mutational analysis of familial Alzheimer disease kindreds for the APP gene region Am. J. Hum. Genet. 51 1992 998 1014
13. P. Kienlen-Campard, B. Tasiaux, J. Van Hees, M. Li, S. Huysseune, T. Sato, J.Z. Fei, S. Aimoto, P.J. Courtoy, and S.O. Smith et al. Amyloidogenic processing but not amyloid precursor protein (APP) intracellular C-terminal domain production requires a precisely oriented APP dimer assembled by transmembrane GXXXG motifs J. Biol. Chem. 283 2008 7733 7744
14. M. Kivipelto, E.L. Helkala, M.P. Laakso, T. Hänninen, M. Hallikainen, K. Alhainen, H. Soininen, J. Tuomilehto, and A. Nissinen Midlife vascular risk factors and Alzheimer's disease in later life: longitudinal, population based study BMJ 322 2001 1447 1451
15. T.L. Kukar, T.B. Ladd, P. Robertson, S.A. Pintchovski, B. Moore, M.A. Bann, Z. Ren, K. Jansen-West, K. Malphrus, and S. Eggert et al. Lysine 624 of the amyloid precursor protein (APP) is a critical determinant of amyloid β peptide length: support for a sequential model of γ-secretase intramembrane proteolysis and regulation by the amyloid β precursor protein (APP) juxtamembrane region J. Biol. Chem. 286 2011 39804 39812
16. M.A. Lemmon, J.M. Flanagan, H.R. Treutlein, J. Zhang, and D.M. Engelman Sequence specificity in the dimerization of transmembrane α-helices Biochemistry 31 1992 12719 12725
17. E. Levy, M.D. Carman, I.J. Fernandez-Madrid, M.D. Power, I. Lieberburg, S.G. van Duinen, G.T. Bots, W. Luyendijk, and B. Frangione Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type Science 248 1990 1124 1126
18. E. London How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells Biochim. Biophys. Acta 1746 2005 203 220
19. Z. Lu, W.D. Van Horn, J. Chen, S. Mathew, R. Zent, and C.R. Sanders Bicelles at low concentrations Mol. Pharmacol. 9 2012 752 761
20. D.L. Minor Jr., and P.S. Kim Measurement of the β-sheet-forming propensities of amino acids Nature 367 1994 660 663
21. L.M. Munter, P. Voigt, A. Harmeier, D. Kaden, K.E. Gottschalk, C. Weise, R. Pipkorn, M. Schaefer, D. Langosch, and G. Multhaup GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of Abeta42 EMBO J. 26 2007 1702 1712
22. K.D. Nadezhdin, O.V. Bocharova, E.V. Bocharov, and A.S. Arseniev Dimeric structure of transmembrane domain of amyloid precursor protein in micellar environment FEBS Lett. 586 2012 1687 1692
23. C. Paul, J.P. Wang, W.C. Wimley, R.M. Hochstrasser, and P.H. Axelsen Vibrational coupling, isotopic editing, and β-sheet structure in a membrane-bound polypeptide J. Am. Chem. Soc. 126 2004 5843 5850
24. S.A. Petty, and S.M. Decatur Experimental evidence for the reorganization of β-strands within aggregates of the Abeta(16-22) peptide J. Am. Chem. Soc. 127 2005 13488 13489
25. Z. Ren, D. Schenk, G.S. Basi, and I.P. Shapiro Amyloid β-protein precursor juxtamembrane domain regulates specificity of γ-secretase- dependent cleavages J. Biol. Chem. 282 2007 35350 35360
26. T. Sato, T.C. Tang, G. Reubins, J.Z. Fei, T. Fujimoto, P. Kienlen-Campard, S.N. Constantinescu, J.N. Octave, S. Aimoto, and S.O. Smith A helix-to-coil transition at the ε-cut site in the transmembrane dimer of the amyloid precursor protein is required for proteolysis Proc. Natl. Acad. Sci. USA 106 2009 1421 1426
27. D.J. Selkoe American College of Physicians; American Physiological Society Alzheimer disease: mechanistic understanding predicts novel therapies Ann. Intern. Med. 140 2004 627 638
28. M. Simons, P. Keller, B. De Strooper, K. Beyreuther, C.G. Dotti, and K. Simons Cholesterol depletion inhibits the generation of β-amyloid in hippocampal neurons Proc. Natl. Acad. Sci. USA 95 1998 6460 6464
29. S.O. Smith, M. Eilers, D. Song, E. Crocker, W.W. Ying, M. Groesbeek, G. Metz, M. Ziliox, and S. Aimoto Implications of threonine hydrogen bonding in the glycophorin A transmembrane helix dimer Biophys. J. 82 2002 2476 2486
30. Y. Song, E.J. Hustedt, S. Brandon, and C.R. Sanders Competition between homodimerization and cholesterol binding to the C99 domain of the amyloid precursor protein Biochemistry 52 2013 5051 5064
31. 1H dipolar-assisted rotational resonance in magic-angle spinning NMR Chem. Phys. Lett. 344 2001 631 637
32. Y. Tian, B. Bassit, D.M. Chau, and Y.M. Li An APP inhibitory domain containing the Flemish mutation residue modulates γ-secretase activity for Abeta production Nat. Struct. Mol. Biol. 17 2010 151 158
33. T. Umeda, T. Tomiyama, E. Kitajima, T. Idomoto, S. Nomura, M.P. Lambert, W.L. Klein, and H. Mori Hypercholesterolemia accelerates intraneuronal accumulation of Aβ oligomers resulting in memory impairment in Alzheimer's disease model mice Life Sci. 91 2012 1169 1176
34. S. Wahrle, P. Das, A.C. Nyborg, C. McLendon, M. Shoji, T. Kawarabayashi, L.H. Younkin, S.G. Younkin, and T.E. Golde Cholesterol-dependent γ-secretase activity in buoyant cholesterol-rich membrane microdomains Neurobiol. Dis. 9 2002 11 23
35. Y.I. Yin, B. Bassit, L. Zhu, X. Yang, C. Wang, and Y.M. Li γ-Secretase substrate concentration modulates the Abeta42/Abeta40 ratio: implications for Alzheimer disease J. Biol. Chem. 282 2007 23639 23644