Imbalance in fatty-acid-chain length of gangliosides triggers Alzheimer amyloid deposition in the precuneus

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Oikawa, Naoto ^a   Matsubara, Teruhiko ^b   Fukuda, Ryoto ^b   Yasumori, Hanaki ^b   Hatsuta, Hiroyuki ^c   Murayama, Shigeo ^c   Sato, Toshinori ^b   Suzuki, Akemi ^d   Yanagisawa, Katsuhiko ^a  

^a NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^d TOKAI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; FATTY ACID; GANGLIOSIDE; GANGLIOSIDE GD 1B; LIPID; CHOLESTEROL; GANGLIOSIDE, GD1B; SPHINGOMYELIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BIOACCUMULATION; CALCARINE SULCUS; CLINICAL ARTICLE; FEMALE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MIDDLE AGED; PRECUNEUS; PROTEIN ASSEMBLY; SYNAPTIC MEMBRANE; VERY ELDERLY; METABOLISM; NERVE ENDING; PARIETAL LOBE;

AGED; AGED, 80 AND OVER; AMYLOID BETA-PEPTIDES; CHOLESTEROL; FATTY ACIDS; FEMALE; GANGLIOSIDES; HUMANS; MALE; PARIETAL LOBE; PRESYNAPTIC TERMINALS; SPHINGOMYELINS; SYNAPTIC MEMBRANES;

EID: 84925881407     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0121356     Document Type: Article

References (54)

1. Esparza TJ, Zhao H, Cirrito JR, Cairns NJ, Bateman RJ, Holtzman DM, et al. Amyloid-β oligomerization in Alzheimer dementia versus high-pathology controls. Ann Neurol. 2013;73:104-119. doi: 10.1002/ana.23748 PMID: PMID: 23225543.
2. Kirkwood CM, Ciuchta J, Ikonomovic MD, Fish KN, Abrahamson EE, Murray PS, et al. Dendritic spine density, morphology, and fibrillar actin content surrounding amyloid-β plaques in a mouse model of amyloid-β deposition. J Neuropathol Exp Neurol. 2013;72:791-800. doi: 10.1097/NEN. 0b013e31829ecc89 PMID: PMID: 23860033.
3. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, et al. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci U S A. 2009;106:4012-4017. doi: 10.1073/pnas.0811698106 PMID: PMID: 19228947.
4. Cohen SI, Linse S, Luheshi LM, Hellstrand E, White DA, Rajah L, et al. Proliferation of amyloid-β42 aggregates occurs through a secondary nucleation mechanism. Proc Natl Acad Sci U S A. 2013;110:9758-9763. doi: 10.1073/pnas.1218402110 PMID: PMID: 23703910.
5. Mucke L, Selkoe DJ. Neurotoxicity of amyloid β-protein: synaptic and network dysfunction. Cold Spring Harb Perspect Med. 2012;2:a006338. doi: 10.1101/cshperspect.a006338 PMID: PMID: 22762015.
6. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 2002;297:353-356. doi: 10.1126/science.1072994 PMID: PMID: 12130773.
7. Yanagisawa K, Odaka A, Suzuki N, Ihara Y. GM1 ganglioside-bound amyloid beta-protein (A beta): a possible form of preamyloid in Alzheimer's disease. Nat Med. 1995;1:1062-1066. PMID: PMID: 7489364.
8. Choo-Smith LP, Garzon-Rodriguez W, Glabe CG, Surewicz WK. Acceleration of amyloid fibril formation by specific binding of Abeta-(1-40) peptide to ganglioside-containing membrane vesicles. J Biol Chem. 1997;272:22987-22990. PMID: PMID: 9287293.
9. Hayashi H, Kimura N, Yamaguchi H, Hasegawa K, Yokoseki T, Shibata M, et al. A seed for Alzheimer amyloid in the brain. J Neurosci. 2004;24:4894-4902. doi: 10.1523/JNEUROSCI.0861-04.2004 PMID: PMID: 15152051.
10. Ariga T, McDonald MP, Yu RK. Role of ganglioside metabolism in the pathogenesis of Alzheimer's disease - a review. J Lipid Res. 2008;49:1157-1175. doi: 10.1194/jlr. R800007-JLR200 PMID: PMID: 18334715.
11. Matsuzaki K, Kato K, Yanagisawa K. Abeta polymerization through interaction with membrane gangliosides. Biochim Biophys Acta. 2010;1801:868-877. doi: 10.1016/j.bbalip. 2010.01.008 PMID: PMID: 20117237.
12. Posse De Chaves E, Sipione S. Sphingolipids and gangliosides of the nervous system in membrane function and dysfunction. FEBS Lett. 2010;584:1748-1759. doi: 10.1016/j.febslet.2009.12.010 PMID: PMID: 20006608.
13. Walter J, Van Echten-Deckert G. Cross-talk of membrane lipids and Alzheimer-related proteins. Mol Neurodegener. 2013;8:34. doi: 10.1186/1750-1326-8-34 PMID: PMID: 24148205.
14. Yanagisawa K. Role of gangliosides in Alzheimer's disease. Biochim Biophys Acta. 2007;1768:1943-1951. doi: 10.1016/j.bbamem.2007.01.018 PMID: PMID: 17321494.
15. Hong S, Ostaszewski BL, Yang T, O'Malley TT, Jin M, Yanagisawa K, et al. Soluble Aβ Oligomers Are Rapidly Sequestered from Brain ISF In Vivo and Bind GM1 Ganglioside on Cellular Membranes. Neuron. 2014;82:308-319. doi: 10.1016/j.neuron. 2014.02.027 PMID: PMID: 24685176.
16. Ikonomovic MD, Klunk WE, Abrahamson EE, Wuu J, Mathis CA, Scheff SW, et al. Precuneus amyloid burden is associated with reduced cholinergic activity in Alzheimer disease. Neurology. 2011;77:39-47. doi: 10.1212/WNL.0b013e3182231419 PMID: PMID: 21700583.
17. Mintun MA, Larossa GN, Sheline YI, Dence CS, Lee SY, Mach RH, et al. [11C]PIB in a nondemented population: potential antecedent marker of Alzheimer disease. Neurology. 2006;67:446-452. doi: 10. 1212/01.wnl.0000228230.26044.a4 PMID: PMID: 16894106.
18. Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, La Violette PS, Vitolo OV, et al. Functional alterations in memory networks in early Alzheimer's disease. Neuromolecular Med. 2010;12:27-43. doi: 10.1007/s12017-009-8109-7 PMID: PMID: 20069392.
19. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82:239-259. PMID: PMID: 1759558.
20. Kakio A, Nishimoto SI, Yanagisawa K, Kozutsumi Y, Matsuzaki K. Cholesterol-dependent formation of GM1 ganglioside-bound amyloid beta-protein, an endogenous seed for Alzheimer amyloid. J Biol Chem. 2001;276:24985-24990. doi: 10.1074/jbc. M100252200 PMID: PMID: 11342534.
21. Yuyama K, Yanagisawa K. Sphingomyelin accumulation provides a favorable milieu for GM1 gangliosideinduced assembly of amyloid beta-protein. Neurosci Lett. 2010;481:168-172. doi: 10.1016/j. neulet.2010.06.080 PMID: PMID: 20599476.
22. Yamamoto N, Fukata Y, Fukata M, Yanagisawa K. GM1-ganglioside-induced Abeta assembly on synaptic membranes of cultured neurons. Biochim Biophys Acta. 2007;1768:1128-1137. doi: 10.1016/j. bbamem.2007.01.009 PMID: PMID: 17306220.
23. Yamamoto N, Matsubara T, Sato T, Yanagisawa K. Age-dependent high-density clustering of GM1 ganglioside at presynaptic neuritic terminals promotes amyloid beta-protein fibrillogenesis. Biochim Biophys Acta. 2008;1778:2717-2726. doi: 10.1016/j.bbamem.2008.07.028 PMID: PMID: 18727916.
24. Adachi T, Saito Y, Hatsuta H, Funabe S, Tokumaru AM, Ishii K, et al. Neuropathological asymmetry in argyrophilic grain disease. J Neuropathol Exp Neurol. 2010;69:737-744. doi: 10.1097/NEN. 0b013e3181e5ae5c PMID: PMID: 20535032.
25. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, et al. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology. 1991;41:479-486. PMID: PMID: 2011243.
26. Hughes CP, Berg L, Danziger WL, Coben LA, Martin RL. A new clinical scale for the staging of dementia. Br J Psychiatry. 1982;140:566-572. PMID: PMID: 7104545.
27. Oikawa N, Hatsuta H, Murayama S, Suzuki A, Yanagisawa K. Influence of APOE genotype and the presence of Alzheimer's pathology on synaptic membrane lipids of human brains. J Neurosci Res. 2014;92:641-650. doi: 10.1002/jnr.23341 PMID: PMID: 24446209.
28. Oikawa N, Goto M, Ikeda K, Taguchi R, Yanagisawa K. The γ-secretase inhibitor DAPT increases the levels of gangliosides at neuritic terminals of differentiating PC12 cells. Neurosci Lett. 2012;525:49-53. doi: 10.1016/j.neulet.2012.07.027 PMID: PMID: 22867970.
29. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226:497-509. PMID: PMID: 13428781.
30. Nagafuku M, Okuyama K, Onimaru Y, Suzuki A, Odagiri Y, Yamashita T, et al. CD4 and CD8 T cells require different membrane gangliosides for activation. Proc Natl Acad Sci U S A. 2012;109:E336-342. doi: 10.1073/pnas.1114965109 PMID: PMID: 22308377.
31. Ikeda K, Taguchi R. Highly sensitive localization analysis of gangliosides and sulfatides including structural isomers in mouse cerebellum sections by combination of laser microdissection and hydrophilic interaction liquid chromatography/electrospray ionization mass spectrometry with theoretically expanded multiple reaction monitoring. Rapid Commun Mass Spectrom. 2010;24:2957-2965. doi: 10.1002/rcm. 4716 PMID: PMID: 20872628.
32. Iijima K, Soga N, Matsubara T, Sato T. Observations of the distribution of GM3 in membrane microdomains by atomic force microscopy. J Colloid Interface Sci. 2009;337:369-374. doi: 10.1016/j.jcis. 2009.05.032 PMID: PMID: 19524935.
33. Matsubara T, Iijima K, Yamamoto N, Yanagisawa K, Sato T. Density of GM1 in nanoclusters is a critical factor in the formation of a spherical assembly of amyloid β-protein on synaptic plasma membranes. Langmuir. 2013;29:2258-2264. doi: 10.1021/la3038999 PMID: PMID: 23294326.
34. Naiki H, Gejyo F. Kinetic analysis of amyloid fibril formation. Methods Enzymol. 1999;309:305-318. PMID: PMID: 10507032.
35. Petkova AT, Leapman RD, Guo Z, Yau WM, Mattson MP, Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science. 2005;307:262-265. doi: 10.1126/science. 1105850 PMID: PMID: 15653506.
36. Kraɥun I, Rösner H, Cosović C, Stavljenić A. Topographical atlas of the gangliosides of the adult human brain. J Neurochem. 1984;43:979-989. PMID: PMID: 6470716.
37. Ando S, Yu RK. Fatty acid and long-chain base composition of gangliosides isolated from adult human brain. J Neurosci Res. 1984;12:205-211. doi: 10.1002/jnr.490120208 PMID: PMID: 6502750.
38. Van Echten-Deckert G, Walter J. Sphingolipids: critical players in Alzheimer's disease. Prog Lipid Res. 2012;51:378-393. doi: 10.1016/j.plipres.2012.07.001 PMID: PMID: 22835784.
39. Crino PB, Ullman MD, Vogt BA, Bird ED, Volicer L. Brain gangliosides in dementia of the Alzheimer type. Arch Neurol. 1989;46:398-401. PMID: PMID: 2705899.
40. Kracun I, Kalanj S, Cosovic C, Talan-Hranilovic J. Brain gangliosides in Alzheimer's disease. J Hirnforsch. 1990;31:789-793. PMID: PMID: 2092064.
41. Kracun I, Rosner H, Drnovsek V, Heffer-Lauc M, Cosović C, Lauc G. Human brain gangliosides in development, aging and disease. Int J Dev Biol. 1991;35:289-295. PMID: PMID: 1814411.
42. Greenshields KN, Halstead SK, Zitman FM, Rinaldi S, Brennan KM, O'Leary C, et al. The neuropathic potential of anti-GM1 autoantibodies is regulated by the local glycolipid environment in mice. J Clin Invest. 2009;119:595-610. doi: 10.1172/JCI37338 PMID: PMID: 19221437.
43. Mauri L, Casellato R, Ciampa MG, Uekusa Y, Kato K, Kaida K, et al. Anti-GM1/GD1a complex antibodies in GBS sera specifically recognize the hybrid dimer GM1-GD1a. Glycobiology. 2012;22:352-360. doi: 10.1093/glycob/cwr139 PMID: PMID: 21921061.
44. Moyano AL, Comín R, Vilcaes AA, Funes SC, Roth GA, Irazoqui FJ, et al. Novel antibodies reacting with two neighboring gangliosides are induced in rabbits immunized with bovine brain gangliosides. Glycobiology. 2012;22:1768-1774. doi: 10.1093/glycob/cws117 PMID: PMID: 22843673.
45. Bernardo A, Harrison FE, McCord M, Zhao J, Bruchey A, Davies SS, et al. Elimination of GD3 synthase improves memory and reduces amyloid-beta plaque load in transgenic mice. Neurobiol Aging. 2009;30:1777-1791. doi: 10.1016/j.neurobiolaging.2007.12.022 PMID: PMID: 18258340.
46. Masserini M, Freire E. Thermotropic characterization of phosphatidylcholine vesicles containing ganglioside GM1 with homogeneous ceramide chain length. Biochemistry. 1986;25:1043-1049. PMID: PMID: 3754459.
47. Masserini M, Palestini P, Freire E. Influence of glycolipid oligosaccharide and long-chain base composition on the thermotropic properties of dipalmitoylphosphatidylcholine large unilamellar vesicles containing gangliosides. Biochemistry. 1989;28:5029-5034. PMID: PMID: 2765523.
48. Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006;129:564-583. doi: 10.1093/brain/awl004 PMID: PMID: 16399806.
49. Greicius MD, Srivastava G, Reiss AL, Menon V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A. 2004;101:4637-4642. doi: 10.1073/pnas.0308627101 PMID: PMID: 15070770.
50. Sorg C, Riedl V, Mühlau M, Calhoun VD, Eichele T, Läer L, et al. Selective changes of resting-state networks in individuals at risk for Alzheimer's disease. Proc Natl Acad Sci U S A. 2007;104:18760-18765. doi: 10.1073/pnas.0708803104 PMID: PMID: 18003904.
51. Mansson JE, Vanier MT, Svennerholm L. Changes in the fatty acid and sphingosine composition of the major gangliosides of human brain with age. J Neurochem. 1978;30:273-275. PMID: PMID: 621516.
52. Rosenberg A, Stern N. Changes in sphingosine and fatty acid components of the gangliosides in developing rat and human brain. J Lipid Res. 1966;7:122-131. PMID: PMID: 5900210.
53. Rouser G, Yamamoto A. The fatty acid composition of total gangliosides in normal human whole brain at different ages. J Neurochem. 1972;19:2697-2698. PMID: PMID: 5086252.
54. Katsel P, Li C, Haroutunian V. Gene expression alterations in the sphingolipid metabolism pathways during progression of dementia and Alzheimer's disease: a shift toward ceramide accumulation at the earliest recognizable stages of Alzheimer's disease? Neurochem Res. 2007;32:845-856. doi: 10. 1007/s11064-007-9297-x PMID: PMID: 17342407.