Effects of membrane lipids on the activity and processivity of purified γ-secretase

Biochemistry

Volumn 51, Issue 17, 2012, Pages 3565-3575

  Holmes, Oliver ^a,b   Paturi, Swetha ^a,b   Ye, Wenjuan ^a,b   Wolfe, Michael S ^a,b   Selkoe, Dennis J ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S DISEASE; AMYLOID PRECURSOR PROTEINS; CARBON-CHAIN LENGTH; DOUBLE BONDS; DOUBLE-BOND ISOMERIZATION; GEL SYSTEMS; INTRACELLULAR DOMAIN; INTRAMEMBRANE PROTEOLYSIS; LIPID MEMBRANES; MEMBRANE LIPID COMPOSITION; MEMBRANE LIPIDS; MICROENVIRONMENTS; MULTISUBUNIT; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; POLAR HEADGROUPS; PRESENILINS; PROCESSIVITY; PROTEIN COMPLEXES; PROTEOLIPOSOMES; SECRETASE COMPLEX; SECRETASES; TRANS ISOMERS; TRANS-MEMBRANE DOMAINS;

ACTIVATION ANALYSIS; CHAIN LENGTH; ENZYME ACTIVITY; GLYCOPROTEINS; PEPTIDES; PURIFICATION;

LIPIDS;

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; ARACHIDONIC ACID; DOCOSAHEXAENOIC ACID; ELAIDIC ACID; ERUCIC ACID; GAMMA SECRETASE; ICOSENOIC ACID; LINOLEIC ACID; MEMBRANE LIPID; MYRISTELAIDIC ACID; MYRISTELEIC ACID; OLEIC ACID; PALMITELAIDIC ACID; PALMITIC ACID; PETROSELINIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; PROTEIN PRECURSOR; PROTEOLIPOSOME; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PURIFICATION; IN VITRO STUDY; ISOMERIZATION; LIPID COMPOSITION; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FUNCTION; WESTERN BLOTTING;

AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CHO CELLS; CRICETINAE; ENZYME ACTIVATION; FATTY ACIDS; HUMANS; LIPID BILAYERS; MEMBRANE LIPIDS; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; SUBSTRATE SPECIFICITY;

EID: 84860459631     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300303g     Document Type: Article

References (49)

1. Selkoe, D. J. (2001) Alzheimer's disease: Genes, proteins, and therapy Physiol. Rev. 81, 741-766
2. Seubert, P., Oltersdorf, T., Lee, M. G., Barbour, R., Blomquist, C., Davis, D. L., Bryant, K., Fritz, L. C., Galasko, D., and Thal, L. J. 1993, Secretion of β-amyloid precursor protein cleaved at the amino terminus of the β-amyloid peptide Nature 361, 260-263
3. Sinha, S., Anderson, J. P., Barbour, R., Basi, G. S., Caccavello, R., Davis, D., Doan, M., Dovey, H. F., Frigon, N., Hong, J., Jacobson-Croak, K., Jewett, N., Keim, P., Knops, J., Lieberburg, I., Power, M., Tan, H., Tatsuno, G., Tung, J., Schenk, D., Seubert, P., Suomensaari, S. M., Wang, S., Walker, D., Zhao, J., McConlogue, L., and John, V. (1999) Purification and cloning of amyloid precursor protein β-secretase from human brain Nature 402, 537-540
4. Esch, F. S., Keim, P. S., Beattie, E. C., Blacher, R. W., Culwell, A. R., Oltersdorf, T., McClure, D., and Ward, P. J. (1990) Cleavage of amyloid β peptide during constitutive processing of its precursor Science 248, 1122-1124
5. Xia, W. and Wolfe, M. S. (2003) Intramembrane proteolysis by presenilin and presenilin-like proteases J. Cell Sci. 116, 2839-2844
6. Haass, C., Schlossmacher, M. G., Hung, A. Y., Vigo-Pelfrey, C., Mellon, A., Ostaszewski, B. L., Lieberburg, I., Koo, E. H., Schenk, D., and Teplow, D. B. 1992, Amyloid β-peptide is produced by cultured cells during normal metabolism Nature 359, 322-325
7. Kimberly, W. T., LaVoie, M. J., Ostaszewski, B. L., Ye, W., Wolfe, M. S., and Selkoe, D. J. (2003) γ-Secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2 Proc. Natl. Acad. Sci. U.S.A. 100, 6382-6387
8. Edbauer, D., Winkler, E., Regula, J. T., Pesold, B., Steiner, H., and Haass, C. (2003) Reconstitution of γ-secretase activity Nat. Cell Biol. 5, 486-488
9. Takasugi, N., Tomita, T., Hayashi, I., Tsuruoka, M., Niimura, M., Takahashi, Y., Thinakaran, G., and Iwatsubo, T. (2003) The role of presenilin cofactors in the γ-secretase complex Nature 422, 438-441
10. Kopan, R. and Ilagan, M. X. (2004) γ-Secretase: Proteasome of the membrane? Nat. Rev. 5, 499-504
11. Takami, M., Nagashima, Y., Sano, Y., Ishihara, S., Morishima-Kawashima, M., Funamoto, S., and Ihara, Y. (2009) γ-Secretase: Successive tripeptide and tetrapeptide release from the transmembrane domain of β-carboxyl terminal fragment J. Neurosci. 29, 13042-13052
12. Saito, T., Suemoto, T., Brouwers, N., Sleegers, K., Funamoto, S., Mihira, N., Matsuba, Y., Yamada, K., Nilsson, P., Takano, J., Nishimura, M., Iwata, N., Van Broeckhoven, C., Ihara, Y., and Saido, T. C. (2011) Potent amyloidogenicity and pathogenicity of Aβ43 Nat. Neurosci. 14, 1023-1032
13. Quintero-Monzon, O., Martin, M. M., Fernandez, M. A., Cappello, C. A., Krzysiak, A. J., Osenkowski, P., and Wolfe, M. S. (2011) Dissociation between the processivity and total activity of γ-secretase: Implications for the mechanism of Alzheimer's disease-causing presenilin mutations Biochemistry 50, 9023-9035
14. Borchelt, D. R., Thinakaran, G., Eckman, C. B., Lee, M. K., Davenport, F., Ratovitsky, T., Prada, C. M., Kim, G., Seekins, S., Yager, D., Slunt, H. H., Wang, R., Seeger, M., Levey, A. I., Gandy, S. E., Copeland, N. G., Jenkins, N. A., Price, D. L., Younkin, S. G., and Sisodia, S. S. (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo Neuron 17, 1005-1013
15. Herl, L., Thomas, A. V., Lill, C. M., Banks, M., Deng, A., Jones, P. B., Spoelgen, R., Hyman, B. T., and Berezovska, O. (2009) Mutations in amyloid precursor protein affect its interactions with presenilin/γ-secretase Mol. Cell. Neurosci. 41, 166-174
16. Berezovska, O., Lleo, A., Herl, L. D., Frosch, M. P., Stern, E. A., Bacskai, B. J., and Hyman, B. T. (2005) Familial Alzheimer's disease presenilin 1 mutations cause alterations in the conformation of presenilin and interactions with amyloid precursor protein J. Neurosci. 25, 3009-3017
17. He, G., Luo, W., Li, P., Remmers, C., Netzer, W. J., Hendrick, J., Bettayeb, K., Flajolet, M., Gorelick, F., Wennogle, L. P., and Greengard, P. (2010) γ-Secretase activating protein is a therapeutic target for Alzheimer's disease Nature 467, 95-98
18. Chen, F., Hasegawa, H., Schmitt-Ulms, G., Kawarai, T., Bohm, C., Katayama, T., Gu, Y., Sanjo, N., Glista, M., Rogaeva, E., Wakutani, Y., Pardossi-Piquard, R., Ruan, X., Tandon, A., Checler, F., Marambaud, P., Hansen, K., Westaway, D., St George-Hyslop, P., and Fraser, P. (2006) TMP21 is a presenilin complex component that modulates γ-secretase but not μ-secretase activity Nature 440, 1208-1212
19. Weggen, S., Eriksen, J. L., Das, P., Sagi, S. A., Wang, R., Pietrzik, C. U., Findlay, K. A., Smith, T. E., Murphy, M. P., Bulter, T., Kang, D. E., Marquez-Sterling, N., Golde, T. E., and Koo, E. H. (2001) A subset of NSAIDs lower amyloidogenic Aβ42 independently of cyclooxygenase activity Nature 414, 212-216
20. Lleo, A., Berezovska, O., Herl, L., Raju, S., Deng, A., Bacskai, B. J., Frosch, M. P., Irizarry, M., and Hyman, B. T. (2004) Nonsteroidal anti-inflammatory drugs lower Aβ42 and change presenilin 1 conformation Nat. Med. 10, 1065-1066
21. Wells, K., Farooqui, A. A., Liss, L., and Horrocks, L. A. (1995) Neural membrane phospholipids in Alzheimer disease Neurochem. Res. 20, 1329-1333
22. Prasad, M. R., Lovell, M. A., Yatin, M., Dhillon, H., and Markesbery, W. R. (1998) Regional membrane phospholipid alterations in Alzheimer's disease Neurochem. Res. 23, 81-88
23. Cordy, J. M., Hussain, I., Dingwall, C., Hooper, N. M., and Turner, A. J. (2003) Exclusively targeting β-secretase to lipid rafts by GPI-anchor addition up-regulates β-site processing of the amyloid precursor protein Proc. Natl. Acad. Sci. U.S.A. 100, 11735-11740
24. Ehehalt, R., Keller, P., Haass, C., Thiele, C., and Simons, K. (2003) Amyloidogenic processing of the Alzheimer β-amyloid precursor protein depends on lipid rafts J. Cell Biol. 160, 113-123
25. Cordy, J. M., Hooper, N. M., and Turner, A. J. (2006) The involvement of lipid rafts in Alzheimer's disease Mol. Membr. Biol. 23, 111-122
26. Shepardson, N. E., Shankar, G. M., and Selkoe, D. J. (2011) Cholesterol level and statin use in Alzheimer disease: II. Review of human trials and recommendations Arch. Neurol. 68, 1385-1392
27. Escriba, P. V., Gonzalez-Ros, J. M., Goni, F. M., Kinnunen, P. K., Vigh, L., Sanchez-Magraner, L., Fernandez, A. M., Busquets, X., Horvath, I., and Barcelo-Coblijn, G. (2008) Membranes: A meeting point for lipids, proteins and therapies J. Cell. Mol. Med. 12, 829-875
28. Hartmann, T., Bieger, S. C., Bruhl, B., Tienari, P. J., Ida, N., Allsop, D., Roberts, G. W., Masters, C. L., Dotti, C. G., Unsicker, K., and Beyreuther, K. (1997) Distinct sites of intracellular production for Alzheimer's disease Aβ40/42 amyloid peptides Nat. Med. 3, 1016-1020
29. Teegala, S. M., Willett, W. C., and Mozaffarian, D. (2009) Consumption and health effects of trans fatty acids: A review J. AOAC Int. 92, 1250-1257
30. Grimm, M. O., Rothhaar, T. L., Grosgen, S., Burg, V. K., Hundsdorfer, B., Haupenthal, V. J., Friess, P., Kins, S., Grimm, H. S., and Hartmann, T. (2011) Trans fatty acids enhance amyloidogenic processing of the Alzheimer amyloid precursor protein (APP) J. Nut.r Biochem. DOI: 10.1016/j.jnutbio.2011.06.015
31. Morris, M. C., Evans, D. A., Bienias, J. L., Tangney, C. C., Bennett, D. A., Aggarwal, N., Schneider, J., and Wilson, R. S. (2003) Dietary fats and the risk of incident Alzheimer disease Arch. Neurol. 60, 194-200
32. Engelhart, M. J., Geerlings, M. I., Ruitenberg, A., Van Swieten, J. C., Hofman, A., Witteman, J. C., and Breteler, M. M. (2002) Diet and risk of dementia: Does fat matter?: The Rotterdam Study Neurology 59, 1915-1921
33. Osenkowski, P., Ye, W., Wang, R., Wolfe, M. S., and Selkoe, D. J. (2008) Direct and potent regulation of γ-secretase by its lipid microenvironment J. Biol. Chem. 283, 22529-22540
34. Osenkowski, P., Li, H., Ye, W., Li, D., Aeschbach, L., Fraering, P. C., Wolfe, M. S., and Selkoe, D. J. (2009) Cryoelectron microscopy structure of purified γ-secretase at 12 Å resolution J. Mol. Biol. 385, 642-652
35. Kimberly, W. T., Esler, W. P., Ye, W., Ostaszewski, B. L., Gao, J., Diehl, T., Selkoe, D. J., and Wolfe, M. S. (2003) Notch and the amyloid precursor protein are cleaved by similar γ-secretase(s) Biochemistry 42, 137-144
36. Osawa, S., Funamoto, S., Nobuhara, M., Wada-Kakuda, S., Shimojo, M., Yagishita, S., and Ihara, Y. (2008) Phosphoinositides suppress γ-secretase in both the detergent-soluble and -insoluble states J. Biol. Chem. 283, 19283-19292
37. Nesic, I., Guix, F. X., Vennekens, K., Michaki, V., Van Veldhoven, P. P., Feiguin, F., De Strooper, B., Dotti, C. G., and Wahle, T. (2012) Alterations in phosphatidylethanolamine levels affect the generation of Aβ Aging Cell 11, 63-72
38. Fong, T. M. and McNamee, M. G. (1986) Correlation between acetylcholine receptor function and structural properties of membranes Biochemistry 25, 830-840
39. Cevc, G. (1991) How membrane chain-melting phase-transition temperature is affected by the lipid chain asymmetry and degree of unsaturation: An effective chain-length model Biochemistry 30, 7186-7193
40. Qi-Takahara, Y., Morishima-Kawashima, M., Tanimura, Y., Dolios, G., Hirotani, N., Horikoshi, Y., Kametani, F., Maeda, M., Saido, T. C., Wang, R., and Ihara, Y. (2005) Longer forms of amyloid β protein: Implications for the mechanism of intramembrane cleavage by γ-secretase J. Neurosci. 25, 436-445
41. Contreras, F. X., Ernst, A. M., Haberkant, P., Bjorkholm, P., Lindahl, E., Gonen, B., Tischer, C., Elofsson, A., von Heijne, G., Thiele, C., Pepperkok, R., Wieland, F., and Brugger, B. (2012) Molecular recognition of a single sphingolipid species by a protein's transmembrane domain Nature 481, 525-529
42. Koumanov, K. S., Tessier, C., Momchilova, A. B., Rainteau, D., Wolf, C., and Quinn, P. J. (2005) Comparative lipid analysis and structure of detergent-resistant membrane raft fractions isolated from human and ruminant erythrocytes Arch. Biochem. Biophys. 434, 150-158
43. Fukumori, A., Fluhrer, R., Steiner, H., and Haass, C. (2010) Three-amino acid spacing of presenilin endoproteolysis suggests a general stepwise cleavage of γ-secretase-mediated intramembrane proteolysis J. Neurosci. 30, 7853-7862
44. Furukawa, K., Ohmi, Y., Ohkawa, Y., Tokuda, N., Kondo, Y., and Tajima, O. (2011) Regulatory mechanisms of nervous systems with glycosphingolipids Neurochem. Res. 36, 1578-1586
45. Bernardo, A., Harrison, F. E., McCord, M., Zhao, J., Bruchey, A., Davies, S. S., Jackson Roberts, L., II, Mathews, P. M., Matsuoka, Y., Ariga, T., Yu, R. K., Thompson, R., and McDonald, M. P. (2009) Elimination of GD3 synthase improves memory and reduces amyloid-β plaque load in transgenic mice Neurobiol. Aging 30, 1777-1791
46. Fairn, G. D., Schieber, N. L., Ariotti, N., Murphy, S., Kuerschner, L., Webb, R. I., Grinstein, S., and Parton, R. G. (2011) High-resolution mapping reveals topologically distinct cellular pools of phosphatidylserine J. Cell Biol. 194, 257-275
47. Stokes, C. E. and Hawthorne, J. N. (1987) Reduced phosphoinositide concentrations in anterior temporal cortex of Alzheimer-diseased brains J. Neurochem. 48, 1018-1021
48. Chan, R. B., Oliveira, T. G., Cortes, E. P., Honig, L. S., Duff, K. E., Small, S. A., Wenk, M. R., Shui, G., and Di Paolo, G. (2011) Comparative lipidomic analysis of mouse and human brain with Alzheimer disease J. Biol. Chem. 287, 2678-2688
49. Yao, J. K., Wengenack, T. M., Curran, G. L., and Poduslo, J. F. (2009) Reduced membrane lipids in the cortex of Alzheimer's disease transgenic mice Neurochem. Res. 34, 102-108