Effect of different phospholipids on α-secretase activity in the non-amyloidogenic pathway of Alzheimer's disease

International Journal of Molecular Sciences

Volumn 14, Issue 3, 2013, Pages 5879-5898

  Grimm, Marcus O W ^a   Haupenthal, Viola J ^a   Rothhaar, Tatjana L ^a   Zimmer, Valerie C ^a   Grösgen, Sven ^a   Hundsdörfer, Benjamin ^a   Lehmann, Johannes ^a   Grimm, Heike S ^a   Hartmann, Tobias ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

ADAM10; Alzheimer's disease; Chain length; Headgroup; Lipids; Phospholipids; Saturation; Secretase

Indexed keywords

ADAM10 ENDOPEPTIDASE; ALPHA SECRETASE; FATTY ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLSERINE; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID;

ALZHEIMER DISEASE; ARTICLE; BRAIN HOMOGENATE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MASS SPECTROMETRY;

EID: 84875534788     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14035879     Document Type: Article

References (76)

1. Masters, C.L.; Simms, G.; Weinman, N.A.; Multhaup, G.; McDonald, B.L.; Beyreuther, K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc. Natl. Acad. Sci. USA 1985, 82, 4245-4249.
2. Selkoe, D.J. Alzheimer's disease: Genes, proteins, and therapy. Physiol. Rev. 2001, 81, 741-766.
3. Dyrks, T.; Weidemann, A.; Multhaup, G.; Salbaum, J.M.; Lemaire, H.G.; Kang, J.; Muller-Hill, B.; Masters, C.L.; Beyreuther, K. Identification, transmembrane orientation and biogenesis of the amyloid A4 precursor of Alzheimer's disease. EMBO J. 1988, 7, 949-957.
4. Vassar, R.; Bennett, B.D.; Babu-Khan, S.; Kahn, S.; Mendiaz, E.A.; Denis, P.; Teplow, D.B.; Ross, S.; Amarante, P.; Loeloff, R.; et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999, 286, 735-741.
5. Sinha, S.; Anderson, J.P.; Barbour, R.; Basi, G.S.; Caccavello, R.; Davis, D.; Doan, M.; Dovey, H.F.; Frigon, N.; Hong, J.; et al. Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature 1999, 402, 537-540.
6. Haass, C.; Schlossmacher, M.G.; Hung, A.Y.; Vigo-Pelfrey, C.; Mellon, A.; Ostaszewski, B.L.; Lieberburg, I.; Koo, E.H.; Schenk, D.; Teplow, D.B.; et al. Amyloid beta-peptide is produced by cultured cells during normal metabolism. Nature 1992, 359, 322-325.
7. Shoji, M.; Golde, T.E.; Ghiso, J.; Cheung, T.T.; Estus, S.; Shaffer, L.M.; Cai, X.D.; McKay, D.M.; Tintner, R.; Frangione, B.; et al. Production of the Alzheimer amyloid beta protein by normal proteolytic processing. Science 1992, 258, 126-129.
8. Herreman, A.; Serneels, L.; Annaert, W.; Collen, D.; Schoonjans, L.; de Strooper, B. Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nat. Cell. Biol. 2000, 2, 461-462.
9. Takasugi, N.; Tomita, T.; Hayashi, I.; Tsuruoka, M.; Niimura, M.; Takahashi, Y.; Thinakaran, G.; Iwatsubo, T. The role of presenilin cofactors in the gamma-secretase complex. Nature 2003, 422, 438-441.
10. Kimberly, W.T.; LaVoie, M.J.; Ostaszewski, B.L.; Ye, W.; Wolfe, M.S.; Selkoe, D.J. Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc. Natl. Acad. Sci. USA 2003, 100, 6382-6387.
11. Duering, M.; Grimm, M.O.; Grimm, H.S.; Schroder, J.; Hartmann, T. Mean age of onset in familial Alzheimer's disease is determined by amyloid beta 42. Neurobiol. Aging 2005, 26, 785-788.
12. Haass, C.; Hung, A.Y.; Schlossmacher, M.G.; Teplow, D.B.; Selkoe, D.J. Beta-Amyloid peptide and a 3-kDa fragment are derived by distinct cellular mechanisms. J. Biol. Chem. 1993, 268, 3021-3024.
13. Lichtenthaler, S.F. Alpha-secretase in Alzheimer's disease: Molecular identity, regulation and therapeutic potential. J. Neurochem. 2011, 116, 10-21.
14. 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. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor. J. Biol. Chem. 1998, 273, 27765-27767.
15. Lammich, S.; Kojro, E.; Postina, R.; Gilbert, S.; Pfeiffer, R.; Jasionowski, M.; Haass, C.; Fahrenholz, F. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc. Natl. Acad. Sci. USA 1999, 96, 3922-3927.
16. Koike, H.; Tomioka, S.; Sorimachi, H.; Saido, T.C.; Maruyama, K.; Okuyama, A.; Fujisawa-Sehara, A.; Ohno, S.; Suzuki, K.; Ishiura, S. Membrane-anchored metalloprotease MDC9 has an alpha-secretase activity responsible for processing the amyloid precursor protein. Biochem. J. 1999, 343, 371-375.
17. Allinson, T.M.; Parkin, E.T.; Turner, A.J.; Hooper, N.M. ADAMs family members as amyloid precursor protein alpha-secretases. J. Neurosci. Res. 2003, 74, 342-352.
18. Hartmann, T.; Kuchenbecker, J.; Grimm, M.O. Alzheimer's disease: The lipid connection. J. Neurochem. 2007, 103, 159-170.
19. Osenkowski, P.; Ye, W.; Wang, R.; Wolfe, M.S.; Selkoe, D.J. Direct and potent regulation of gamma-secretase by its lipid microenvironment. J. Biol. Chem. 2008, 283, 22529-22540.
20. Grimm, M.O.; Rothhaar, T.L.; Hartmann, T. The role of APP proteolytic processing in lipid metabolism. Exp. Brain Res. 2012, 217, 365-375.
21. Lemkul, J.A.; Bevan, D.R. Lipid composition influences the release of Alzheimer's amyloid beta-peptide from membranes. Protein Sci. 2011, 20, 1530-1545.
22. Grimm, M.O.; Rothhaar, T.L.; Grösgen, S.; Burg, V.K.; Hundsdorfer, B.; Haupenthal, V.J.; Friess, P.; Kins, S.; Grimm, H.S.; Hartmann, T. Trans fatty acids enhance amyloidogenic processing of the Alzheimer amyloid precursor protein (APP). J. Nutr. Biochem. 2012, 23, 1214-1223.
23. Rothhaar, T.L.; Grosgen, S.; Haupenthal, V.J.; Burg, V.K.; Hundsdorfer, B.; Mett, J.; Riemenschneider, M.; Grimm, H.S.; Hartmann, T.; Grimm, M.O. Plasmalogens inhibit APP processing by directly affecting gamma-secretase activity in Alzheimer's disease. Sci. World J. 2012, 2012, 141240.
24. Marenchino, M.; Williamson, P.T.; Murri, S.; Zandomeneghi, G.; Wunderli-Allenspach, H.; Meier, B.H.; Kramer, S.D. Dynamics and Cleavability at the alpha-cleavage site of APP(684-726) in different lipid environments. Biophys. J. 2008, 95, 1460-1473.
25. Barrett, P.J.; Song, Y.; van Horn, W.D.; Hustedt, E.J.; Schafer, J.M.; Hadziselimovic, A.; Beel, A.J.; Sanders, C.R. The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 2012, 336, 1168-1171.
26. Simons, M.; Keller, P.; de Strooper, B.; Beyreuther, K.; Dotti, C.G.; Simons, K. Cholesterol depletion inhibits the generation of beta-amyloid in hippocampal neurons. Proc. Natl. Acad. Sci. USA 1998, 95, 6460-6464.
27. Grösgen, S.; Grimm, M.O.; Friess, P.; Hartmann, T. Role of amyloid beta in lipid homeostasis. Biochim. Biophys. Acta 2010, 1801, 966-974.
28. Grimm, M.O.; Grimm, H.S.; Tomic, I.; Beyreuther, K.; Hartmann, T.; Bergmann, C. Independent inhibition of Alzheimer disease beta-and gamma-secretase cleavage by lowered cholesterol levels. J. Biol. Chem. 2008, 283, 11302-11311.
29. Grimm, M.O.; Grimm, H.S.; Patzold, A.J.; Zinser, E.G.; Halonen, R.; Duering, M.; Tschape, J.A.; De Strooper, B.; Muller, U.; Shen, J.; et al. Regulation of cholesterol and sphingomyelin metabolism by amyloid-beta and presenilin. Nat. Cell. Biol. 2005, 7, 1118-1123.
30. Zha, Q.; Ruan, Y.; Hartmann, T.; Beyreuther, K.; Zhang, D. GM1 ganglioside regulates the proteolysis of amyloid precursor protein. Mol. Psychiatry 2004, 9, 946-952.
31. Grimm, M.O.; Zinser, E.G.; Grösgen, S.; Hundsdorfer, B.; Rothhaar, T.L.; Burg, V.K.; Kaestner, L.; Bayer, T.A.; Lipp, P.; Muller, U.; et al. Amyloid precursor protein (APP) mediated regulation of ganglioside homeostasis linking Alzheimer's disease pathology with ganglioside metabolism. PLoS One 2012, 7, e34095.
32. Svennerholm, L.; Gottfries, C.G. Membrane lipids, selectively diminished in Alzheimer brains, suggest synapse loss as a primary event in early-onset form (type I) and demyelination in late-onset form (type II). J. Neurochem. 1994, 62, 1039-1047.
33. Wells, K.; Farooqui, A.A.; Liss, L.; Horrocks, L.A. Neural membrane phospholipids in Alzheimer disease. Neurochem. Res. 1995, 20, 1329-1333.
34. Prasad, M.R.; Lovell, M.A.; Yatin, M.; Dhillon, H.; Markesbery, W.R. Regional membrane phospholipid alterations in Alzheimer's disease. Neurochem. Res. 1998, 23, 81-88.
35. Holmes, O.; Paturi, S.; Ye, W.; Wolfe, M.S.; Selkoe, D.J. Effects of membrane lipids on the activity and processivity of purified gamma-secretase. Biochemistry 2012, 51, 3565-3575.
36. Simons, K.; Ikonen, E. Functional rafts in cell membranes. Nature 1997, 387, 569-572.
37. Vetrivel, K.S.; Thinakaran, G. Membrane rafts in Alzheimer's disease beta-amyloid production. Biochim. Biophys. Acta 2010, 1801, 860-867.
38. Riddell, D.R.; Christie, G.; Hussain, I.; Dingwall, C. Compartmentalization of beta-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr. Biol. 2001, 11, 1288-1293.
39. Vetrivel, K.S.; Cheng, H.; Lin, W.; Sakurai, T.; Li, T.; Nukina, N.; Wong, P.C.; Xu, H.; Thinakaran, G. Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J. Biol. Chem. 2004, 279, 44945-44954.
40. Vetrivel, K.S.; Cheng, H.; Kim, S.H.; Chen, Y.; Barnes, N.Y.; Parent, A.T.; Sisodia, S.S.; Thinakaran, G. Spatial segregation of gamma-secretase and substrates in distinct membrane domains. J. Biol. Chem. 2005, 280, 25892-25900.
41. Koumanov, K.S.; Tessier, C.; Momchilova, A.B.; Rainteau, D.; Wolf, C.; Quinn, P.J. Comparative lipid analysis and structure of detergent-resistant membrane raft fractions isolated from human and ruminant erythrocytes. Arch. Biochem. Biophys. 2005, 434, 150-158.
42. Kojro, E.; Gimpl, G.; Lammich, S.; Marz, W.; Fahrenholz, F. Low cholesterol stimulates the nonamyloidogenic pathway by its effect on the α-secretase ADAM 10. Proc. Natl. Acad. Sci. USA 2001, 98, 5815-5820.
43. Ehehalt, R.; Keller, P.; Haass, C.; Thiele, C.; Simons, K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 2003, 160, 113-123.
44. Parr-Sturgess, C.A.; Rushton, D.J.; Parkin, E.T. Ectodomain shedding of the Notch ligand Jagged1 is mediated by ADAM17, but is not a lipid-raft-associated event. Biochem. J. 2010, 432, 283-294.
45. Kuhn, P.H.; Wang, H.; Dislich, B.; Colombo, A.; Zeitschel, U.; Ellwart, J.W.; Kremmer, E.; Rossner, S.; Lichtenthaler, S.F. ADAM10 is the physiologically relevant, constitutive alpha-secretase of the amyloid precursor protein in primary neurons. EMBO J. 2010, 29, 3020-3032.
46. Stokes, C.E.; Hawthorne, J.N. Reduced phosphoinositide concentrations in anterior temporal cortex of Alzheimer-diseased brains. J. Neurochem. 1987, 48, 1018-1021.
47. Nitsch, R.M.; Blusztajn, J.K.; Pittas, A.G.; Slack, B.E.; Growdon, J.H.; Wurtman, R.J. Evidence for a membrane defect in Alzheimer disease brain. Proc. Natl. Acad. Sci. USA 1992, 89, 1671-1675.
48. Nesic, I.; Guix, F.X.; Vennekens, K.; Michaki, V.; van Veldhoven, P.P.; Feiguin, F.; de Strooper, B.; Dotti, C.G.; Wahle, T. Alterations in phosphatidylethanolamine levels affect the generation of Abeta. Aging Cell 2012, 11, 63-72.
49. 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.; Barcelo-Coblijn, G. Membranes: A meeting point for lipids, proteins and therapies. J. Cell. Mol. Med. 2008, 12, 829-875.
50. Bazan, N.G.; Scott, B.L. Dietary omega-3 fatty acids and accumulation of docosahexaenoic acid in rod photoreceptor cells of the retina and at synapses. Ups. J. Med. Sci. Suppl. 1990, 48, 97-107.
51. Ansari, K.A.; Shoeman, D.W. Arachidonic and docosahexanoic acid content of bovine brain myelin: Implications for the pathogenesis of multiple sclerosis. Neurochem. Res. 1990, 15, 7-11.
52. Horrocks, L.A.; Farooqui, A.A. Docosahexaenoic acid in the diet: Its importance in maintenance and restoration of neural membrane function. Prostaglandins Leukot Essent Fatty Acids 2004, 70, 361-372.
53. Yang, X.; Sheng, W.; Sun, G.Y.; Lee, J.C. Effects of fatty acid unsaturation numbers on membrane fluidity and alpha-secretase-dependent amyloid precursor protein processing. Neurochem. Int. 2011, 58, 321-329.
54. Eckert, G.P.; Chang, S.; Eckmann, J.; Copanaki, E.; Hagl, S.; Hener, U.; Muller, W.E.; Kogel, D. Liposome-incorporated DHA increases neuronal survival by enhancing non-amyloidogenic APP processing. Biochim. Biophys. Acta 2011, 1808, 236-243.
55. Soderberg, M.; Edlund, C.; Kristensson, K.; Dallner, G. Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 1991, 26, 421-425.
56. Tully, A.M.; Roche, H.M.; Doyle, R.; Fallon, C.; Bruce, I.; Lawlor, B.; Coakley, D.; Gibney, M.J. Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer's disease: A case-control study. Br. J. Nutr. 2003, 89, 483-489.
57. Cunnane, S.C.; Schneider, J.A.; Tangney, C.; Tremblay-Mercier, J.; Fortier, M.; Bennett, D.A.; Morris, M.C. Plasma and brain fatty acid profiles in mild cognitive impairment and Alzheimer's disease. J. Alzheimers Dis. 2012, 29, 691-697.
58. Barberger-Gateau, P.; Letenneur, L.; Deschamps, V.; Peres, K.; Dartigues, J.F.; Renaud, S. Fish, meat, and risk of dementia: Cohort study. Br. Med. J. 2002, 325, 932-933.
59. Morris, M.C.; Evans, D.A.; Bienias, J.L.; Tangney, C.C.; Bennett, D.A.; Wilson, R.S.; Aggarwal, N.; Schneider, J. Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch. Neurol. 2003, 60, 940-946.
60. Schaefer, E.J.; Bongard, V.; Beiser, A.S.; Lamon-Fava, S.; Robins, S.J.; Au, R.; Tucker, K.L.; Kyle, D.J.; Wilson, P.W.; Wolf, P.A. Plasma phosphatidylcholine docosahexaenoic acid content and risk of dementia and Alzheimer disease: The Framingham Heart Study. Arch. Neurol. 2006, 63, 1545-1550.
61. Van Gelder, B.M.; Tijhuis, M.; Kalmijn, S.; Kromhout, D. Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: The Zutphen Elderly Study. Am. J. Clin. Nutr. 2007, 85, 1142-1147.
62. Lukiw, W.J.; Cui, J.G.; Marcheselli, V.L.; Bodker, M.; Botkjaer, A.; Gotlinger, K.; Serhan, C.N.; Bazan, N.G. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J. Clin. Invest. 2005, 115, 2774-2783.
63. Perez, S.E.; Berg, B.M.; Moore, K.A.; He, B.; Counts, S.E.; Fritz, J.J.; Hu, Y.S.; Lazarov, O.; Lah, J.J.; Mufson, E.J. DHA diet reduces AD pathology in young APPswe/PS1 Delta E9 transgenic mice: Possible gender effects. J. Neurosci. Res. 2010, 88, 1026-1040.
64. Oksman, M.; Iivonen, H.; Hogyes, E.; Amtul, Z.; Penke, B.; Leenders, I.; Broersen, L.; Lutjohann, D.; Hartmann, T.; Tanila, H. Impact of different saturated fatty acid, polyunsaturated fatty acid and cholesterol containing diets on beta-amyloid accumulation in APP/PS1 transgenic mice. Neurobiol. Dis. 2006, 23, 563-572.
65. Calon, F.; Lim, G.P.; Yang, F.; Morihara, T.; Teter, B.; Ubeda, O.; Rostaing, P.; Triller, A.; Salem, N., Jr.; Ashe, K.H.; et al. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43, 633-645.
66. Hooijmans, C.R.; Rutters, F.; Dederen, P.J.; Gambarota, G.; Veltien, A.; van Groen, T.; Broersen, L.M.; Lutjohann, D.; Heerschap, A.; Tanila, H.; et al. Changes in cerebral blood volume and amyloid pathology in aged Alzheimer APP/PS1 mice on a docosahexaenoic acid (DHA) diet or cholesterol enriched Typical Western Diet (TWD). Neurobiol. Dis. 2007, 28, 16-29.
67. Cole, G.M.; Ma, Q.L.; Frautschy, S.A. Omega-3 fatty acids and dementia. Prostaglandins Leukot Essent Fatty Acids 2009, 81, 213-221.
68. Grimm, M.O.; Kuchenbecker, J.; Grösgen, S.; Burg, V.K.; Hundsdorfer, B.; Rothhaar, T.L.; Friess, P.; de Wilde, M.C.; Broersen, L.M.; Penke, B.; et al. Docosahexaenoic acid reduces amyloid beta production via multiple pleiotropic mechanisms. J. Biol. Chem. 2011, 286, 14028-14039.
69. Grziwa, B.; Grimm, M.O.; Masters, C.L.; Beyreuther, K.; Hartmann, T.; Lichtenthaler, S.F. The transmembrane domain of the amyloid precursor protein in microsomal membranes is on both sides shorter than predicted. J. Biol. Chem. 2003, 278, 6803-6808.
70. Duyckaerts, C.; Hauw, J.J. Diagnosis and staging of Alzheimer disease. Neurobiol. Aging 1997, 18, S33-S42.
71. Smith, P.K.; Krohn, R.I.; Hermanson, G.T.; Mallia, A.K.; Gartner, F.H.; Provenzano, M.D.; Fujimoto, E.K.; Goeke, N.M.; Olson, B.J.; Klenk, D.C. Measurement of protein using bicinchoninic acid. Anal. Biochem. 1985, 150, 76-85.
72. Grimm, M.O.; Grösgen, S.; Rothhaar, T.L.; Burg, V.K.; Hundsdorfer, B.; Haupenthal, V.J.; Friess, P.; Muller, U.; Fassbender, K.; Riemenschneider, M.; et al. Intracellular APP domain regulates serine-palmitoyl-coa transferase expression and is affected in Alzheimer's disease. Int. J. Alzheimers Dis. 2011, 2011, 695413.
73. Bligh, E.G.; Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37, 911-917.
74. Grimm, M.O.; Kuchenbecker, J.; Rothhaar, T.L.; Grösgen, S.; Hundsdorfer, B.; Burg, V.K.; Friess, P.; Muller, U.; Grimm, H.S.; Riemenschneider, M.; et al. Plasmalogen synthesis is regulated via alkyl-dihydroxyacetonephosphate-synthase by amyloid precursor protein processing and is affected in Alzheimer's disease. J. Neurochem. 2011, 116, 916-925.
75. Ruiz, J.I.; Ochoa, B. Quantification in the subnanomolar range of phospholipids and neutral lipids by monodimensional thin-layer chromatography and image analysis. J. Lipid Res. 1997, 38, 1482-1489.
76. Grimm, M.O.; Grösgen, S.; Riemenschneider, M.; Tanila, H.; Grimm, H.S.; Hartmann, T. From brain to food: Analysis of phosphatidylcholins, lyso-phosphatidylcholins and phosphatidylcholin-plasmalogens derivates in Alzheimer's disease human post mortem brains and mice model via mass spectrometry. J. Chromatogr. A 2011, 1218, 7713-7722.