The Role of Lipid Environment in Ganglioside GM1-Induced Amyloid β Aggregation
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic
Document type Journal Article, Review
PubMed
32916822
PubMed Central
PMC7558528
DOI
10.3390/membranes10090226
PII: membranes10090226
Knihovny.cz E-resources
- Keywords
- Alzheimer’s disease, GM1, amyloid oligomers, amyloid β, fibrils, gangliosides, membrane microdomains,
- Publication type
- Journal Article MeSH
- Review MeSH
Ganglioside GM1 is the most common brain ganglioside enriched in plasma membrane regions known as lipid rafts or membrane microdomains. GM1 participates in many modulatory and communication functions associated with the development, differentiation, and protection of neuronal tissue. It has, however, been demonstrated that GM1 plays a negative role in the pathophysiology of Alzheimer's disease (AD). The two features of AD are the formation of intracellular neurofibrillary bodies and the accumulation of extracellular amyloid β (Aβ). Aβ is a peptide characterized by intrinsic conformational flexibility. Depending on its partners, Aβ can adopt different spatial arrangements. GM1 has been shown to induce specific changes in the spatial organization of Aβ, which lead to enhanced peptide accumulation and deleterious effect especially on neuronal membranes containing clusters of this ganglioside. Changes in GM1 levels and distribution during the development of AD may contribute to the aggravation of the disease.
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Apostolova L.G. Alzheimer Disease. Continuum (Minneap. Minn.) 2016;22:419–434. doi: 10.1212/CON.0000000000000307. PubMed DOI PMC
GBD 2015 Disease and Injury Incidence and Prevalence Collaborators Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1545–1602. doi: 10.1016/S0140-6736(16)31678-6. PubMed DOI PMC
Chen X.Q., Mobley W.C. Exploring the Pathogenesis of Alzheimer Disease in Basal Forebrain Cholinergic Neurons: Converging Insights from Alternative Hypotheses. Front. Neurosci. 2019;13:446. doi: 10.3389/fnins.2019.00446. PubMed DOI PMC
Jan A., Adolfsson O., Allaman I., Buccarello A.L., Magistretti P.J., Pfeifer A., Muhs A., Lashuel H.A. Abeta42 neurotoxicity is mediated by ongoing nucleated polymerization process rather than by discrete Abeta42 species. J. Biol. Chem. 2011;286:8585–8596. doi: 10.1074/jbc.M110.172411. PubMed DOI PMC
Villemagne V.L., Burnham S., Bourgeat P., Brown B., Ellis K.A., Salvado O., Szoeke C., Macaulay S.L., Martins R., Maruff P., et al. Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer’s disease: A prospective cohort study. Lancet Neurol. 2013;12:357–367. doi: 10.1016/S1474-4422(13)70044-9. PubMed DOI
Hardy J., Selkoe D.J. 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. PubMed DOI
Selkoe D.J., Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol. Med. 2016;8:595–608. doi: 10.15252/emmm.201606210. PubMed DOI PMC
Palmqvist S., Scholl M., Strandberg O., Mattsson N., Stomrud E., Zetterberg H., Blennow K., Landau S., Jagust W., Hansson O. Earliest accumulation of beta-amyloid occurs within the default-mode network and concurrently affects brain connectivity. Nat. Commun. 2017;8:1214. doi: 10.1038/s41467-017-01150-x. PubMed DOI PMC
Wong P.T., Schauerte J.A., Wisser K.C., Ding H., Lee E.L., Steel D.G., Gafni A. Amyloid-beta membrane binding and permeabilization are distinct processes influenced separately by membrane charge and fluidity. J. Mol. Biol. 2009;386:81–96. doi: 10.1016/j.jmb.2008.11.060. PubMed DOI
Evangelisti E., Cascella R., Becatti M., Marrazza G., Dobson C.M., Chiti F., Stefani M., Cecchi C. Binding affinity of amyloid oligomers to cellular membranes is a generic indicator of cellular dysfunction in protein misfolding diseases. Sci. Rep. 2016;6:32721. doi: 10.1038/srep32721. PubMed DOI PMC
Wakabayashi M., Matsuzaki K. Formation of amyloids by Abeta-(1-42) on NGF-differentiated PC12 cells: Roles of gangliosides and cholesterol. J. Mol. Biol. 2007;371:924–933. doi: 10.1016/j.jmb.2007.06.008. PubMed DOI
Amar F., Sherman M.A., Rush T., Larson M., Boyle G., Chang L., Gotz J., Buisson A., Lesne S.E. The amyloid-beta oligomer A beta*56 induces specific alterations in neuronal signaling that lead to tau phosphorylation and aggregation. Sci. Signal. 2017;10:eaal2021. doi: 10.1126/scisignal.aal2021. PubMed DOI PMC
Vahed M., Neya S., Matsuzaki K., Hoshino T. Analysis of Physicochemical Interaction of Abeta40 with a GM1 Ganglioside-Containing Lipid Membrane. J. Phys. Chem. B. 2018;122:3771–3781. doi: 10.1021/acs.jpcb.8b00139. PubMed DOI
Micelli S., Meleleo D., Picciarelli V., Gallucci E. Effect of sterols on beta-amyloid peptide (AbetaP 1-40) channel formation and their properties in planar lipid membranes. Biophys. J. 2004;86:2231–2237. doi: 10.1016/S0006-3495(04)74281-2. PubMed DOI PMC
Demuro A., Mina E., Kayed R., Milton S.C., Parker I., Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 2005;280:17294–17300. doi: 10.1074/jbc.M500997200. PubMed DOI
Fantini J., Yahi N. Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: Common mechanisms in neurodegenerative diseases. Expert Rev. Mol. Med. 2010;12:e27. doi: 10.1017/S1462399410001602. PubMed DOI PMC
Di Scala C., Chahinian H., Yahi N., Garmy N., Fantini J. Interaction of Alzheimer’s beta-amyloid peptides with cholesterol: Mechanistic insights into amyloid pore formation. Biochemistry. 2014;53:4489–4502. doi: 10.1021/bi500373k. PubMed DOI
Sepulveda F.J., Fierro H., Fernandez E., Castillo C., Peoples R.W., Opazo C., Aguayo L.G. Nature of the neurotoxic membrane actions of amyloid-beta on hippocampal neurons in Alzheimer’s disease. Neurobiol. Aging. 2014;35:472–481. doi: 10.1016/j.neurobiolaging.2013.08.035. PubMed DOI
Revett T.J., Baker G.B., Jhamandas J., Kar S. Glutamate system, amyloid ss peptides and tau protein: Functional interrelationships and relevance to Alzheimer disease pathology. J. Psychiatry Neurosci. 2013;38:6–23. doi: 10.1503/jpn.110190. PubMed DOI PMC
Kocahan S., Dogan Z. Mechanisms of Alzheimer’s Disease Pathogenesis and Prevention: The Brain, Neural Pathology, N-methyl-D-aspartate Receptors, Tau Protein and Other Risk Factors. Clin. Psychopharmacol. Neurosci. 2017;15:1–8. doi: 10.9758/cpn.2017.15.1.1. PubMed DOI PMC
Baker-Nigh A., Vahedi S., Davis E.G., Weintraub S., Bigio E.H., Klein W.L., Geula C. Neuronal amyloid-beta accumulation within cholinergic basal forebrain in ageing and Alzheimer’s disease. Brain. 2015;138:1722–1737. doi: 10.1093/brain/awv024. PubMed DOI PMC
Richter N., Beckers N., Onur O.A., Dietlein M., Tittgemeyer M., Kracht L., Neumaier B., Fink G.R., Kukolja J. Effect of cholinergic treatment depends on cholinergic integrity in early Alzheimer’s disease. Brain. 2018;141:903–915. doi: 10.1093/brain/awx356. PubMed DOI
Sultzer D.L. Cognitive ageing and Alzheimer’s disease: The cholinergic system redux. Brain. 2018;141:626–628. doi: 10.1093/brain/awy040. PubMed DOI
Machova E., Rudajev V., Smyckova H., Koivisto H., Tanila H., Dolezal V. Functional cholinergic damage develops with amyloid accumulation in young adult APPswe/PS1dE9 transgenic mice. Neurobiol. Dis. 2010;38:27–35. doi: 10.1016/j.nbd.2009.12.023. PubMed DOI
Janickova H., Rudajev V., Zimcik P., Jakubik J., Tanila H., El-Fakahany E.E., Dolezal V. Uncoupling of M1 muscarinic receptor/G-protein interaction by amyloid beta(1-42) Neuropharmacology. 2013;67:272–283. doi: 10.1016/j.neuropharm.2012.11.014. PubMed DOI
Janickova H., Rudajev V., Dolejsi E., Koivisto H., Jakubik J., Tanila H., El-Fakahany E.E., Dolezal V. Lipid-Based Diets Improve Muscarinic Neurotransmission in the Hippocampus of Transgenic APPswe/PS1dE9 Mice. Curr. Alzheimer Res. 2015;12:923–931. doi: 10.2174/1567205012666151027130350. PubMed DOI
Ferreira-Vieira T.H., Guimaraes I.M., Silva F.R., Ribeiro F.M. Alzheimer’s disease: Targeting the Cholinergic System. Curr. Neuropharmacol. 2016;14:101–115. doi: 10.2174/1570159X13666150716165726. PubMed DOI PMC
Viola K.L., Klein W.L. Amyloid beta oligomers in Alzheimer’s disease pathogenesis, treatment, and diagnosis. Acta Neuropathol. 2015;129:183–206. doi: 10.1007/s00401-015-1386-3. PubMed DOI PMC
Chen G.F., Xu T.H., Yan Y., Zhou Y.R., Jiang Y., Melcher K., Xu H.E. Amyloid beta: Structure, biology and structure-based therapeutic development. Acta Pharmacol. Sin. 2017;38:1205–1235. doi: 10.1038/aps.2017.28. PubMed DOI PMC
Molander-Melin M., Blennow K., Bogdanovic N., Dellheden B., Mansson J.E., Fredman P. Structural membrane alterations in Alzheimer brains found to be associated with regional disease development; increased density of gangliosides GM1 and GM2 and loss of cholesterol in detergent-resistant membrane domains. J. Neurochem. 2005;92:171–182. doi: 10.1111/j.1471-4159.2004.02849.x. PubMed DOI
Pernber Z., Blennow K., Bogdanovic N., Mansson J.E., Blomqvist M. Altered distribution of the gangliosides GM1 and GM2 in Alzheimer’s disease. Dement. Geriatr. Cogn. Disord. 2012;33:174–188. doi: 10.1159/000338181. PubMed DOI
Arbor S.C., Lafontaine M., Cumbay M. Amyloid-beta Alzheimer targets—Protein processing, lipid rafts, and amyloid-beta pores. Yale J. Biol. Med. 2016;89:5–21. PubMed PMC
Owen M.C., Kulig W., Poojari C., Rog T., Strodel B. Physiologically-relevant levels of sphingomyelin, but not GM1, induces a beta-sheet-rich structure in the amyloid-beta(1-42) monomer. Biochim. Biophys. Acta Biomembr. 2018;1860:1709–1720. doi: 10.1016/j.bbamem.2018.03.026. PubMed DOI
Yanagisawa K. GM1 ganglioside and Alzheimer’s disease. Glycoconj. J. 2015;32:87–91. doi: 10.1007/s10719-015-9579-5. PubMed DOI
Yuyama K., Yanagisawa K. Sphingomyelin accumulation provides a favorable milieu for GM1 ganglioside-induced assembly of amyloid beta-protein. Neurosci. Lett. 2010;481:168–172. doi: 10.1016/j.neulet.2010.06.080. PubMed DOI
Kakio A., Nishimoto S., 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. PubMed DOI
Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron. 2003;37:925–937. doi: 10.1016/S0896-6273(03)00124-7. PubMed DOI
Luhrs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Dobeli H., Schubert D., Riek R. 3D structure of Alzheimer’s amyloid-beta(1-42) fibrils. Proc. Natl. Acad. Sci. USA. 2005;102:17342–17347. doi: 10.1073/pnas.0506723102. PubMed DOI PMC
Ahmed M., Davis J., Aucoin D., Sato T., Ahuja S., Aimoto S., Elliott J.I., Van Nostrand W.E., Smith S.O. Structural conversion of neurotoxic amyloid-beta(1-42) oligomers to fibrils. Nat. Struct. Mol. Biol. 2010;17:561–567. doi: 10.1038/nsmb.1799. PubMed DOI PMC
Gouras G.K. Aging, Metabolism, Synaptic Activity, and Abeta in Alzheimer’s Disease. Front. Aging Neurosci. 2019;11:185. doi: 10.3389/fnagi.2019.00185. PubMed DOI PMC
Nasica-Labouze J., Nguyen P.H., Sterpone F., Berthoumieu O., Buchete N.V., Cote S., De Simone A., Doig A.J., Faller P., Garcia A., et al. Amyloid beta Protein and Alzheimer’s Disease: When Computer Simulations Complement Experimental Studies. Chem. Rev. 2015;115:3518–3563. doi: 10.1021/cr500638n. PubMed DOI PMC
Verma M., Vats A., Taneja V. Toxic species in amyloid disorders: Oligomers or mature fibrils. Ann. Indian Acad. Neurol. 2015;18:138–145. PubMed PMC
Tran J., Chang D., Hsu F., Wang H., Guo Z. Cross-seeding between Abeta40 and Abeta42 in Alzheimer’s disease. FEBS Lett. 2017;591:177–185. doi: 10.1002/1873-3468.12526. PubMed DOI PMC
Xue C., Tran J., Wang H., Park G., Hsu F., Guo Z. Abeta42 fibril formation from predominantly oligomeric samples suggests a link between oligomer heterogeneity and fibril polymorphism. R. Soc. Open Sci. 2019;6:190179. doi: 10.1098/rsos.190179. PubMed DOI PMC
Ono K., Tsuji M. Protofibrils of Amyloid-beta are Important Targets of a Disease-Modifying Approach for Alzheimer’s Disease. Int. J. Mol. Sci. 2020;21:952. doi: 10.3390/ijms21030952. PubMed DOI PMC
Roychaudhuri R., Yang M., Hoshi M.M., Teplow D.B. Amyloid beta-protein assembly and Alzheimer disease. J. Biol. Chem. 2009;284:4749–4753. doi: 10.1074/jbc.R800036200. PubMed DOI PMC
Williams T.L., Johnson B.R., Urbanc B., Jenkins A.T., Connell S.D., Serpell L.C. Abeta42 oligomers, but not fibrils, simultaneously bind to and cause damage to ganglioside-containing lipid membranes. Biochem. J. 2011;439:67–77. doi: 10.1042/BJ20110750. PubMed DOI
Bobo C., Chaignepain S., Henry S., Vignaud H., Ameadan A., Marchal C., Prado E., Doutch J., Schmitter J.M., Nardin C., et al. Synthetic toxic Abeta1-42 oligomers can assemble in different morphologies. Biochim. Biophys. Acta Gen. Subj. 2017;1861:1168–1176. doi: 10.1016/j.bbagen.2017.03.001. PubMed DOI
Xue W.F., Hellewell A.L., Gosal W.S., Homans S.W., Hewitt E.W., Radford S.E. Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 2009;284:34272–34282. doi: 10.1074/jbc.M109.049809. PubMed DOI PMC
Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., et al. Diffusible, nonfibrillar ligands derived from A beta(1-42) are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. USA. 1998;95:6448–6453. doi: 10.1073/pnas.95.11.6448. PubMed DOI PMC
Lesne S., Koh M.T., Kotilinek L., Kayed R., Glabe C.G., Yang A., Gallagher M., Ashe K.H. A specific amyloid-beta protein assembly in the brain impairs memory. Nature. 2006;440:352–357. doi: 10.1038/nature04533. PubMed DOI
Yamamoto N., Matsubara E., Maeda S., Minagawa H., Takashima A., Maruyama W., Michikawa M., Yanagisawa K. A ganglioside-induced toxic soluble Abeta assembly. Its enhanced formation from Abeta bearing the Arctic mutation. J. Biol. Chem. 2007;282:2646–2655. doi: 10.1074/jbc.M606202200. PubMed DOI
Ewald M., Henry S., Lambert E., Feuillie C., Bobo C., Cullin C., Lecomte S., Molinari M. High speed atomic force microscopy to investigate the interactions between toxic Abeta1-42 peptides and model membranes in real time: Impact of the membrane composition. Nanoscale. 2019;11:7229–7238. doi: 10.1039/C8NR08714H. PubMed DOI
Bernstein S.L., Dupuis N.F., Lazo N.D., Wyttenbach T., Condron M.M., Bitan G., Teplow D.B., Shea J.E., Ruotolo B.T., Robinson C.V., et al. Amyloid-beta protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer’s disease. Nat. Chem. 2009;1:326–331. doi: 10.1038/nchem.247. PubMed DOI PMC
Lesne S.E., Sherman M.A., Grant M., Kuskowski M., Schneider J.A., Bennett D.A., Ashe K.H. Brain amyloid-beta oligomers in ageing and Alzheimer’s disease. Brain. 2013;136:1383–1398. doi: 10.1093/brain/awt062. PubMed DOI PMC
Spencer R.K., Li H., Nowick J.S. X-ray crystallographic structures of trimers and higher-order oligomeric assemblies of a peptide derived from Abeta(17-36) J. Am. Chem. Soc. 2014;136:5595–5598. doi: 10.1021/ja5017409. PubMed DOI PMC
Cline E.N., Bicca M.A., Viola K.L., Klein W.L. The Amyloid-beta Oligomer Hypothesis: Beginning of the Third Decade. J. Alzheimers Dis. 2018;64:S567–S610. doi: 10.3233/JAD-179941. PubMed DOI PMC
Esparza T.J., Zhao H., Cirrito J.R., Cairns N.J., Bateman R.J., Holtzman D.M., Brody D.L. Amyloid-beta oligomerization in Alzheimer dementia versus high-pathology controls. Ann. Neurol. 2013;73:104–119. doi: 10.1002/ana.23748. PubMed DOI PMC
Hong S., Ostaszewski B.L., Yang T., O’malley T.T., Jin M., Yanagisawa K., Li S., Bartels T., Selkoe D.J. Soluble Abeta 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. PubMed DOI PMC
Jeong J.S., Ansaloni A., Mezzenga R., Lashuel H.A., Dietler G. Novel mechanistic insight into the molecular basis of amyloid polymorphism and secondary nucleation during amyloid formation. J. Mol. Biol. 2013;425:1765–1781. doi: 10.1016/j.jmb.2013.02.005. PubMed DOI
Tycko R. Amyloid polymorphism: Structural basis and neurobiological relevance. Neuron. 2015;86:632–645. doi: 10.1016/j.neuron.2015.03.017. PubMed DOI PMC
Qiang W., Yau W.M., Lu J.X., Collinge J., Tycko R. Structural variation in amyloid-beta fibrils from Alzheimer’s disease clinical subtypes. Nature. 2017;541:217–221. doi: 10.1038/nature20814. PubMed DOI PMC
Petkova A.T., Leapman R.D., Guo Z., Yau W.M., Mattson M.P., Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer’s beta-amyloid fibrils. Science. 2005;307:262–265. doi: 10.1126/science.1105850. PubMed DOI
Niu Z., Zhang Z., Zhao W., Yang J. Interactions between amyloid beta peptide and lipid membranes. Biochim. Biophys. Acta Biomembr. 2018;1860:1663–1669. doi: 10.1016/j.bbamem.2018.04.004. PubMed DOI
Rasmussen J., Mahler J., Beschorner N., Kaeser S.A., Hasler L.M., Baumann F., Nystrom S., Portelius E., Blennow K., Lashley T., et al. Amyloid polymorphisms constitute distinct clouds of conformational variants in different etiological subtypes of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA. 2017;114:13018–13023. doi: 10.1073/pnas.1713215114. PubMed DOI PMC
Larini L., Shea J.E. Role of beta-Hairpin Formation in Aggregation: The Self-Assembly of the Amyloid-beta(25-35) Peptide. Biophys. J. 2012;103:576–586. doi: 10.1016/j.bpj.2012.06.027. PubMed DOI PMC
Nag S., Sarkar B., Chandrakesan M., Abhyanakar R., Bhowmik D., Kombrabail M., Dandekar S., Lerner E., Haas E., Maiti S. A folding transition underlies the emergence of membrane affinity in amyloid-beta. Phys. Chem. Chem. Phys. 2013;15:19129–19133. doi: 10.1039/c3cp52732h. PubMed DOI
Wei G., Shea J.E. Effects of solvent on the structure of the Alzheimer amyloid-beta(25-35) peptide. Biophys. J. 2006;91:1638–1647. doi: 10.1529/biophysj.105.079186. PubMed DOI PMC
Choo L.P., Wetzel D.L., Halliday W.C., Jackson M., Levine S.M., Mantsch H.H. In situ characterization of beta-amyloid in Alzheimer’s diseased tissue by synchrotron Fourier transform infrared microspectroscopy. Biophys. J. 1996;71:1672–1679. doi: 10.1016/S0006-3495(96)79411-0. PubMed DOI PMC
Shao H., Jao S., Ma K., Zagorski M.G. Solution structures of micelle-bound amyloid beta-(1-40) and beta-(1-42) peptides of Alzheimer’s disease. J. Mol. Biol. 1999;285:755–773. doi: 10.1006/jmbi.1998.2348. PubMed DOI
Vivekanandan S., Brender J.R., Lee S.Y., Ramamoorthy A. A partially folded structure of amyloid-beta(1-40) in an aqueous environment. Biochem. Biophys. Res. Commun. 2011;411:312–316. doi: 10.1016/j.bbrc.2011.06.133. PubMed DOI PMC
Bhowmik D., Maclaughlin C.M., Chandrakesan M., Ramesh P., Venkatramani R., Walker G.C., Maiti S. pH changes the aggregation propensity of amyloid-beta without altering the monomer conformation. Phys. Chem. Chem. Phys. 2014;16:885–889. doi: 10.1039/C3CP54151G. PubMed DOI
Lockhart C., Klimov D.K. Alzheimer’s Abeta10-40 peptide binds and penetrates DMPC bilayer: An isobaric-isothermal replica exchange molecular dynamics study. J. Phys. Chem. B. 2014;118:2638–2648. doi: 10.1021/jp412153s. PubMed DOI
Tycko R. Molecular Structure of Aggregated Amyloid-beta: Insights from Solid-State Nuclear Magnetic Resonance. Cold Spring Harb. Perspect. Med. 2016;6:a024083. doi: 10.1101/cshperspect.a024083. PubMed DOI PMC
Jang H., Arce F.T., Ramachandran S., Capone R., Lal R., Nussinov R. beta-Barrel topology of Alzheimer’s beta-amyloid ion channels. J. Mol. Biol. 2010;404:917–934. doi: 10.1016/j.jmb.2010.10.025. PubMed DOI PMC
Schmidt M., Sachse C., Richter W., Xu C., Fandrich M., Grigorieff N. Comparison of Alzheimer Abeta(1-40) and Abeta(1-42) amyloid fibrils reveals similar protofilament structures. Proc. Natl. Acad. Sci. USA. 2009;106:19813–19818. doi: 10.1073/pnas.0905007106. PubMed DOI PMC
Xiao Y., Ma B., Mcelheny D., Parthasarathy S., Long F., Hoshi M., Nussinov R., Ishii Y. Abeta(1-42) fibril structure illuminates self-recognition and replication of amyloid in Alzheimer’s disease. Nat. Struct. Mol. Biol. 2015;22:499–505. doi: 10.1038/nsmb.2991. PubMed DOI PMC
Barz B., Olubiyi O.O., Strodel B. Early amyloid beta-protein aggregation precedes conformational change. Chem. Commun. (Camb.) 2014;50:5373–5375. doi: 10.1039/C3CC48704K. PubMed DOI
Vignaud H., Bobo C., Lascu I., Sorgjerd K.M., Zako T., Maeda M., Salin B., Lecomte S., Cullin C. A structure-toxicity study of Ass42 reveals a new anti-parallel aggregation pathway. PLoS ONE. 2013;8:e80262. doi: 10.1371/journal.pone.0080262. PubMed DOI PMC
Bonhommeau S., Talaga D., Hunel J., Cullin C., Lecomte S. Tip-Enhanced Raman Spectroscopy to Distinguish Toxic Oligomers from Abeta1-42 Fibrils at the Nanometer Scale. Angew. Chem. Int. Ed. Engl. 2017;56:1771–1774. doi: 10.1002/anie.201610399. PubMed DOI
Davis C.H., Berkowitz M.L. A molecular dynamics study of the early stages of amyloid-beta(1-42) oligomerization: The role of lipid membranes. Proteins. 2010;78:2533–2545. doi: 10.1002/prot.22763. PubMed DOI PMC
Fernandez-Perez E.J., Sepulveda F.J., Peoples R., Aguayo L.G. Role of membrane GM1 on early neuronal membrane actions of Abeta during onset of Alzheimer’s disease. Biochim. Biophys. Acta Mol. Basis Dis. 2017;1863:3105–3116. doi: 10.1016/j.bbadis.2017.08.013. PubMed DOI
Simakova O., Arispe N.J. The cell-selective neurotoxicity of the Alzheimer’s Abeta peptide is determined by surface phosphatidylserine and cytosolic ATP levels. Membrane binding is required for Abeta toxicity. J. Neurosci. 2007;27:13719–13729. doi: 10.1523/JNEUROSCI.3006-07.2007. PubMed DOI PMC
Mclaurin J., Chakrabartty A. Membrane disruption by Alzheimer beta-amyloid peptides mediated through specific binding to either phospholipids or gangliosides. Implications for neurotoxicity. J. Biol. Chem. 1996;271:26482–26489. doi: 10.1074/jbc.271.43.26482. PubMed DOI
Korshavn K.J., Bhunia A., Lim M.H., Ramamoorthy A. Amyloid-beta adopts a conserved, partially folded structure upon binding to zwitterionic lipid bilayers prior to amyloid formation. Chem. Commun. (Camb.) 2016;52:882–885. doi: 10.1039/C5CC08634E. PubMed DOI PMC
Yates E.A., Owens S.L., Lynch M.F., Cucco E.M., Umbaugh C.S., Legleiter J. Specific domains of Abeta facilitate aggregation on and association with lipid bilayers. J. Mol. Biol. 2013;425:1915–1933. doi: 10.1016/j.jmb.2013.03.022. PubMed DOI
Sasahara K., Morigaki K., Shinya K. Effects of membrane interaction and aggregation of amyloid beta-peptide on lipid mobility and membrane domain structure. Phys. Chem. Chem. Phys. 2013;15:8929–8939. doi: 10.1039/c3cp44517h. PubMed DOI
Ji S.R., Wu Y., Sui S.F. Cholesterol is an important factor affecting the membrane insertion of beta-amyloid peptide (A beta 1-40), which may potentially inhibit the fibril formation. J. Biol. Chem. 2002;277:6273–6279. doi: 10.1074/jbc.M104146200. PubMed DOI
Wakabayashi M., Okada T., Kozutsumi Y., Matsuzaki K. GM1 ganglioside-mediated accumulation of amyloid beta-protein on cell membranes. Biochem. Biophys. Res. Commun. 2005;328:1019–1023. doi: 10.1016/j.bbrc.2005.01.060. PubMed DOI
Nicholson A.M., Ferreira A. Increased membrane cholesterol might render mature hippocampal neurons more susceptible to beta-amyloid-induced calpain activation and tau toxicity. J. Neurosci. 2009;29:4640–4651. doi: 10.1523/JNEUROSCI.0862-09.2009. PubMed DOI PMC
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. doi: 10.1038/nm1095-1062. PubMed DOI
Amaro M., Sachl R., Aydogan G., Mikhalyov I., Vacha R., Hof M. GM1 Ganglioside Inhibits beta-Amyloid Oligomerization Induced by Sphingomyelin. Angew. Chem. Int. Ed. Engl. 2016;55:9411–9415. doi: 10.1002/anie.201603178. PubMed DOI PMC
Zhou X., Xu J. Free cholesterol induces higher beta-sheet content in Abeta peptide oligomers by aromatic interaction with Phe19. PLoS ONE. 2012;7:e46245. PubMed PMC
Van Weering J.R.T., Scheper W. Endolysosome and Autolysosome Dysfunction in Alzheimer’s Disease: Where Intracellular and Extracellular Meet. CNS Drugs. 2019;33:639–648. doi: 10.1007/s40263-019-00643-1. PubMed DOI PMC
Yu X., Zheng J. Cholesterol promotes the interaction of Alzheimer beta-amyloid monomer with lipid bilayer. J. Mol. Biol. 2012;421:561–571. doi: 10.1016/j.jmb.2011.11.006. PubMed DOI
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. PubMed DOI
Mori K., Mahmood M.I., Neya S., Matsuzaki K., Hoshino T. Formation of GM1 ganglioside clusters on the lipid membrane containing sphingomyeline and cholesterol. J. Phys. Chem. B. 2012;116:5111–5121. doi: 10.1021/jp207881k. PubMed DOI
Ahmed S.N., Brown D.A., London E. On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: Physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry. 1997;36:10944–10953. doi: 10.1021/bi971167g. PubMed DOI
Anderson R.G., Jacobson K. A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science. 2002;296:1821–1825. doi: 10.1126/science.1068886. PubMed DOI
Pike L.J. Lipid rafts: Heterogeneity on the high seas. Biochem. J. 2004;378:281–292. doi: 10.1042/bj20031672. PubMed DOI PMC
Garner A.E., Smith D.A., Hooper N.M. Visualization of detergent solubilization of membranes: Implications for the isolation of rafts. Biophys. J. 2008;94:1326–1340. doi: 10.1529/biophysj.107.114108. PubMed DOI PMC
Sonnino S., Aureli M., Mauri L., Ciampa M.G., Prinetti A. Membrane lipid domains in the nervous system. Front. Biosci. (Landmark Ed.) 2015;20:280–302. doi: 10.2741/4309. PubMed DOI
Haughey N.J., Bandaru V.V., Bae M., Mattson M.P. Roles for dysfunctional sphingolipid metabolism in Alzheimer’s disease neuropathogenesis. Biochim. Biophys. Acta. 2010;1801:878–886. doi: 10.1016/j.bbalip.2010.05.003. PubMed DOI PMC
Lingwood D., Simons K. Lipid Rafts as a Membrane-Organizing Principle. Science. 2010;327:46–50. doi: 10.1126/science.1174621. PubMed DOI
Lisanti M.P., Scherer P.E., Tang Z., Sargiacomo M. Caveolae, Caveolin and Caveolin-Rich Membrane Domains: A Signalling Hypothesis. Trends Cell Biol. 1994;4:231–235. doi: 10.1016/0962-8924(94)90114-7. PubMed DOI
Eckert G.P., Igbavboa U., Muller W.E., Wood W.G. Lipid rafts of purified mouse brain synaptosomes prepared with or without detergent reveal different lipid and protein domains. Brain Res. 2003;962:144–150. doi: 10.1016/S0006-8993(02)03986-0. PubMed DOI
Moravcova Z., Rudajev V., Stohr J., Novotny J., Cerny J., Parenti M., Milligan G., Svoboda P. Long-term agonist stimulation of IP prostanoid receptor depletes the cognate G(s)alpha protein in membrane domains but does not change the receptor level. Biochim. Biophys. Acta. 2004;1691:51–65. doi: 10.1016/j.bbamcr.2003.12.004. PubMed DOI
Matousek P., Novotny J., Rudajev V., Svoboda P. Prolonged agonist stimulation does not alter the protein composition of membrane domains in spite of dramatic changes induced in a specific signaling cascade. Cell Biochem. Biophys. 2005;42:21–40. doi: 10.1385/CBB:42:1:021. PubMed DOI
Rudajev V., Novotny J., Hejnova L., Milligan G., Svoboda P. Dominant portion of thyrotropin-releasing hormone receptor is excluded from lipid domains. Detergent-resistant and detergent-sensitive pools of TRH receptor and Gqalpha/G11alpha protein. J. Biochem. 2005;138:111–125. doi: 10.1093/jb/mvi114. PubMed DOI
Chakrabarti S., Chang A., Gintzler A.R. Subcellular localization of mu-opioid receptor G(s) signaling. J. Pharmacol. Exp. Ther. 2010;333:193–200. doi: 10.1124/jpet.109.165142. PubMed DOI PMC
Lauren J., Gimbel D.A., Nygaard H.B., Gilbert J.W., Strittmatter S.M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature. 2009;457:1128–U1184. doi: 10.1038/nature07761. PubMed DOI PMC
Rushworth J.V., Hooper N.M. Lipid Rafts: Linking Alzheimer’s Amyloid-beta Production, Aggregation, and Toxicity at Neuronal Membranes. Int. J. Alzheimers Dis. 2010;2011:603052. doi: 10.4061/2011/603052. PubMed DOI PMC
Staneva G., Puff N., Stanimirov S., Tochev T., Angelova M.I., Seigneuret M. The Alzheimer’s disease amyloid-beta peptide affects the size-dynamics of raft-mimicking Lo domains in GM1-containing lipid bilayers. Soft Matter. 2018;14:9609–9618. doi: 10.1039/C8SM01636D. PubMed DOI
Azouz M., Cullin C., Lecomte S., Lafleur M. Membrane domain modulation of Abeta1-42 oligomer interactions with supported lipid bilayers: An atomic force microscopy investigation. Nanoscale. 2019;11:20857–20867. doi: 10.1039/C9NR06361G. PubMed DOI
Terakawa M.S., Lin Y., Kinoshita M., Kanemura S., Itoh D., Sugiki T., Okumura M., Ramamoorthy A., Lee Y.H. Impact of membrane curvature on amyloid aggregation. Biochim. Biophys. Acta Biomembr. 2018;1860:1741–1764. doi: 10.1016/j.bbamem.2018.04.012. PubMed DOI PMC
Drolle E., Negoda A., Hammond K., Pavlov E., Leonenko Z. Changes in lipid membranes may trigger amyloid toxicity in Alzheimer’s disease. PLoS ONE. 2017;12:e0182194. doi: 10.1371/journal.pone.0182194. PubMed DOI PMC
Fabelo N., Martin V., Marin R., Santpere G., Aso E., Ferrer I., Diaz M. Evidence for premature lipid raft aging in APP/PS1 double-transgenic mice, a model of familial Alzheimer disease. J. Neuropathol. Exp. Neurol. 2012;71:868–881. doi: 10.1097/NEN.0b013e31826be03c. PubMed DOI
Fabelo N., Martin V., Marin R., Moreno D., Ferrer I., Diaz M. Altered lipid composition in cortical lipid rafts occurs at early stages of sporadic Alzheimer’s disease and facilitates APP/BACE1 interactions. Neurobiol. Aging. 2014;35:1801–1812. doi: 10.1016/j.neurobiolaging.2014.02.005. PubMed DOI
Malchiodi-Albedi F., Contrusciere V., Raggi C., Fecchi K., Rainaldi G., Paradisi S., Matteucci A., Santini M.T., Sargiacomo M., Frank C., et al. Lipid raft disruption protects mature neurons against amyloid oligomer toxicity. Biochim. Biophys. Acta. 2010;1802:406–415. doi: 10.1016/j.bbadis.2010.01.007. PubMed DOI
Santos G., Diaz M., Torres N.V. Lipid Raft Size and Lipid Mobility in Non-raft Domains Increase during Aging and Are Exacerbated in APP/PS1 Mice Model of Alzheimer’s Disease. Predictions from an Agent-Based Mathematical Model. Front. Physiol. 2016;7:90. doi: 10.3389/fphys.2016.00090. PubMed DOI PMC
Chan R.B., Oliveira T.G., Cortes E.P., Honig L.S., Duff K.E., Small S.A., Wenk M.R., Shui G., Di Paolo G. Comparative lipidomic analysis of mouse and human brain with Alzheimer disease. J. Biol. Chem. 2012;287:2678–2688. doi: 10.1074/jbc.M111.274142. PubMed DOI PMC
Yu R.K., Nakatani Y., Yanagisawa M. The role of glycosphingolipid metabolism in the developing brain. J. Lipid Res. 2009;50:S440–S445. doi: 10.1194/jlr.R800028-JLR200. PubMed DOI PMC
Ariga T., Mcdonald M.P., Yu R.K. 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. PubMed DOI PMC
Yagi-Utsumi M., Kato K. Structural and dynamic views of GM1 ganglioside. Glycoconj. J. 2015;32:105–112. doi: 10.1007/s10719-015-9587-5. PubMed DOI
Magistretti P.J., Geisler F.H., Schneider J.S., Li P.A., Fiumelli H., Sipione S. Gangliosides: Treatment Avenues in Neurodegenerative Disease. Front. Neurol. 2019;10:859. doi: 10.3389/fneur.2019.00859. PubMed DOI PMC
Mojumdar E.H., Grey C., Sparr E. Self-Assembly in Ganglioside-Phospholipid Systems: The Co-Existence of Vesicles, Micelles, and Discs. Int. J. Mol. Sci. 2019;21:56. doi: 10.3390/ijms21010056. PubMed DOI PMC
Sonnino S., Mauri L., Chigorno V., Prinetti A. Gangliosides as components of lipid membrane domains. Glycobiology. 2007;17:1R–13R. doi: 10.1093/glycob/cwl052. PubMed DOI
Ohmi Y., Tajima O., Ohkawa Y., Yamauchi Y., Sugiura Y., Furukawa K., Furukawa K. Gangliosides are essential in the protection of inflammation and neurodegeneration via maintenance of lipid rafts: Elucidation by a series of ganglioside-deficient mutant mice. J. Neurochem. 2011;116:926–935. doi: 10.1111/j.1471-4159.2010.07067.x. PubMed DOI
Herzer S., Meldner S., Rehder K., Grone H.J., Nordstrom V. Lipid microdomain modification sustains neuronal viability in models of Alzheimer’s disease. Acta Neuropathol. Commun. 2016;4:103. doi: 10.1186/s40478-016-0354-z. PubMed DOI PMC
Herzer S., Hagan C., Von Gerichten J., Dieterle V., Munteanu B., Sandhoff R., Hopf C., Nordstrom V. Deletion of Specific Sphingolipids in Distinct Neurons Improves Spatial Memory in a Mouse Model of Alzheimer’s Disease. Front. Mol. Neurosci. 2018;11:206. doi: 10.3389/fnmol.2018.00206. PubMed DOI PMC
Vajn K., Viljetic B., Degmecic I.V., Schnaar R.L., Heffer M. Differential distribution of major brain gangliosides in the adult mouse central nervous system. PLoS ONE. 2013;8:e75720. doi: 10.1371/journal.pone.0075720. PubMed DOI PMC
Fukami Y., Ariga T., Yamada M., Yuki N. Brain Gangliosides in Alzheimer’s Disease: Increased Expression of Cholinergic Neuron-Specific Gangliosides. Curr. Alzheimer Res. 2017;14:586–591. doi: 10.2174/1567205014666170117094038. PubMed DOI
Caughlin S., Maheshwari S., Agca Y., Agca C., Harris A.J., Jurcic K., Yeung K.K., Cechetto D.F., Whitehead S.N. Membrane-lipid homeostasis in a prodromal rat model of Alzheimer’s disease: Characteristic profiles in ganglioside distributions during aging detected using MALDI imaging mass spectrometry. Biochim. Biophys. Acta Gen. Subj. 2018;1862:1327–1338. doi: 10.1016/j.bbagen.2018.03.011. PubMed DOI
Hicks D.A., Nalivaeva N.N., Turner A.J. Lipid rafts and Alzheimer’s disease: Protein-lipid interactions and perturbation of signaling. Front. Physiol. 2012;3:189. doi: 10.3389/fphys.2012.00189. PubMed DOI PMC
Chiricozzi E., Lunghi G., Di Biase E., Fazzari M., Sonnino S., Mauri L. GM1 Ganglioside Is A Key Factor in Maintaining the Mammalian Neuronal Functions Avoiding Neurodegeneration. Int. J. Mol. Sci. 2020;21:868. doi: 10.3390/ijms21030868. PubMed DOI PMC
Kim S.I., Yi J.S., Ko Y.G. Amyloid beta oligomerization is induced by brain lipid rafts. J. Cell. Biochem. 2006;99:878–889. doi: 10.1002/jcb.20978. PubMed DOI
Marconi S., De Toni L., Lovato L., Tedeschi E., Gaetti L., Acler M., Bonetti B. Expression of gangliosides on glial and neuronal cells in normal and pathological adult human brain. J. Neuroimmunol. 2005;170:115–121. doi: 10.1016/j.jneuroim.2005.03.025. PubMed DOI
Matsuzaki K. How do membranes initiate Alzheimer’s Disease? Formation of toxic amyloid fibrils by the amyloid beta-protein on ganglioside clusters. Acc. Chem. Res. 2014;47:2397–2404. doi: 10.1021/ar500127z. PubMed DOI
Yamamoto N., Igbabvoa U., Shimada Y., Ohno-Iwashita Y., Kobayashi M., Wood W.G., Fujita S.C., Yanagisawa K. Accelerated Abeta aggregation in the presence of GM1-ganglioside-accumulated synaptosomes of aged apoE4-knock-in mouse brain. FEBS Lett. 2004;569:135–139. doi: 10.1016/j.febslet.2004.05.037. PubMed DOI
Gylys K.H., Fein J.A., Yang F., Miller C.A., Cole G.M. Increased cholesterol in Abeta-positive nerve terminals from Alzheimer’s disease cortex. Neurobiol. Aging. 2007;28:8–17. doi: 10.1016/j.neurobiolaging.2005.10.018. PubMed DOI
Kaya I., Jennische E., Dunevall J., Lange S., Ewing A.G., Malmberg P., Baykal A.T., Fletcher J.S. Spatial Lipidomics Reveals Region and Long Chain Base Specific Accumulations of Monosialogangliosides in Amyloid Plaques in Familial Alzheimer’s Disease Mice (5xFAD) Brain. ACS Chem. Neurosci. 2020;11:14–24. doi: 10.1021/acschemneuro.9b00532. PubMed DOI
Choo-Smith L.P., Surewicz W.K. The interaction between Alzheimer amyloid beta(1-40) peptide and ganglioside GM1-containing membranes. FEBS Lett. 1997;402:95–98. doi: 10.1016/S0014-5793(96)01504-9. PubMed DOI
Hayashi H., Kimura N., Yamaguchi H., Hasegawa K., Yokoseki T., Shibata M., Yamamoto N., Michikawa M., Yoshikawa Y., Terao K., et al. A seed for Alzheimer amyloid in the brain. J. Neurosci. 2004;24:4894–4902. doi: 10.1523/JNEUROSCI.0861-04.2004. PubMed DOI PMC
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. PubMed DOI
Kakio A., Nishimoto S., Yanagisawa K., Kozutsumi Y., Matsuzaki K. Interactions of amyloid beta-protein with various gangliosides in raft-like membranes: Importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid. Biochemistry. 2002;41:7385–7390. doi: 10.1021/bi0255874. PubMed DOI
Matsubara T., Nishihara M., Yasumori H., Nakai M., Yanagisawa K., Sato T. Size and Shape of Amyloid Fibrils Induced by Ganglioside Nanoclusters: Role of Sialyl Oligosaccharide in Fibril Formation. Langmuir. 2017;33:13874–13881. doi: 10.1021/acs.langmuir.7b02091. PubMed DOI
Chi E.Y., Frey S.L., Lee K.Y. Ganglioside G(M1)-mediated amyloid-beta fibrillogenesis and membrane disruption. Biochemistry. 2007;46:1913–1924. doi: 10.1021/bi062177x. PubMed DOI
Tachi Y., Okamoto Y., Okumura H. Conformational Change of Amyloid-beta 40 in Association with Binding to GM1-Glycan Cluster. Sci. Rep. 2019;9:6853. doi: 10.1038/s41598-019-43117-6. PubMed DOI PMC
Ariga T., Kobayashi K., Hasegawa A., Kiso M., Ishida H., Miyatake T. Characterization of high-affinity binding between gangliosides and amyloid beta-protein. Arch. Biochem. Biophys. 2001;388:225–230. doi: 10.1006/abbi.2001.2304. PubMed DOI
Yamasaki Y., Tsuda L., Suzuki A., Yanagisawa K. Induction of ganglioside synthesis in Drosophila brain accelerates assembly of amyloid beta protein. Sci. Rep. 2018;8:8345. doi: 10.1038/s41598-018-26294-8. PubMed DOI PMC
Bera S., Korshavn K.J., Kar R.K., Lim M.H., Ramamoorthy A., Bhunia A. Biophysical insights into the membrane interaction of the core amyloid-forming Abeta40 fragment K16-K28 and its role in the pathogenesis of Alzheimer’s disease. Phys. Chem. Chem. Phys. 2016;18:16890–16901. doi: 10.1039/C6CP02023B. PubMed DOI
Manna M., Mukhopadhyay C. Binding, conformational transition and dimerization of amyloid-beta peptide on GM1-containing ternary membrane: Insights from molecular dynamics simulation. PLoS ONE. 2013;8:e71308. doi: 10.1371/journal.pone.0071308. PubMed DOI PMC
Matsuzaki K. Abeta-ganglioside interactions in the pathogenesis of Alzheimer’s disease. Biochim. Biophys. Acta Biomembr. 2020;1862:183233. doi: 10.1016/j.bbamem.2020.183233. PubMed DOI
Nicastro M.C., Spigolon D., Librizzi F., Moran O., Ortore M.G., Bulone D., Biagio P.L., Carrotta R. Amyloid beta-peptide insertion in liposomes containing GM1-cholesterol domains. Biophys. Chem. 2016;208:9–16. doi: 10.1016/j.bpc.2015.07.010. PubMed DOI
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 beta-protein on synaptic plasma membranes. Langmuir. 2013;29:2258–2264. doi: 10.1021/la3038999. PubMed DOI
Thomaier M., Gremer L., Dammers C., Fabig J., Neudecker P., Willbold D. High-Affinity Binding of Monomeric but Not Oligomeric Amyloid-beta to Ganglioside GM1 Containing Nanodiscs. Biochemistry. 2016;55:6662–6672. doi: 10.1021/acs.biochem.6b00829. PubMed DOI
Dukhinova M., Veremeyko T., Yung A.W.Y., Kuznetsova I.S., Lau T.Y.B., Kopeikina E., Chan A.M.L., Ponomarev E.D. Fresh evidence for major brain gangliosides as a target for the treatment of Alzheimer’s disease. Neurobiol. Aging. 2019;77:128–143. doi: 10.1016/j.neurobiolaging.2019.01.020. PubMed DOI
Mikhalyov I., Olofsson A., Grobner G., Johansson L.B. Designed fluorescent probes reveal interactions between amyloid-beta(1-40) peptides and GM1 gangliosides in micelles and lipid vesicles. Biophys. J. 2010;99:1510–1519. doi: 10.1016/j.bpj.2010.06.043. PubMed DOI PMC
Michno W., Wehrli P.M., Zetterberg H., Blennow K., Hanrieder J. GM1 locates to mature amyloid structures implicating a prominent role for glycolipid-protein interactions in Alzheimer pathology. Biochim. Biophys. Acta Proteins Proteom. 2019;1867:458–467. doi: 10.1016/j.bbapap.2018.09.010. PubMed DOI
Ikeda K., Yamaguchi T., Fukunaga S., Hoshino M., Matsuzaki K. Mechanism of amyloid beta-protein aggregation mediated by GM1 ganglioside clusters. Biochemistry. 2011;50:6433–6440. doi: 10.1021/bi200771m. PubMed DOI
Ahyayauch H., De La Arada I., Masserini M.E., Arrondo J.L.R., Goni F.M., Alonso A. The Binding of Abeta42 Peptide Monomers to Sphingomyelin/Cholesterol/Ganglioside Bilayers Assayed by Density Gradient Ultracentrifugation. Int. J. Mol. Sci. 2020;21:1674. doi: 10.3390/ijms21051674. PubMed DOI PMC
Okada Y., Okubo K., Ikeda K., Yano Y., Hoshino M., Hayashi Y., Kiso Y., Itoh-Watanabe H., Naito A., Matsuzaki K. Toxic Amyloid Tape: A Novel Mixed Antiparallel/Parallel beta-Sheet Structure Formed by Amyloid beta-Protein on GM1 Clusters. ACS Chem. Neurosci. 2019;10:563–572. doi: 10.1021/acschemneuro.8b00424. PubMed DOI
Fukunaga S., Ueno H., Yamaguchi T., Yano Y., Hoshino M., Matsuzaki K. GM1 cluster mediates formation of toxic Abeta fibrils by providing hydrophobic environments. Biochemistry. 2012;51:8125–8131. doi: 10.1021/bi300839u. PubMed DOI
Matsubara T., Yasumori H., Ito K., Shimoaka T., Hasegawa T., Sato T. Amyloid-beta fibrils assembled on ganglioside-enriched membranes contain both parallel beta-sheets and turns. J. Biol. Chem. 2018;293:14146–14154. doi: 10.1074/jbc.RA118.002787. PubMed DOI PMC
Dai Y., Zhang M., Shi X., Wang K., Gao G., Shen L., Sun T. Kinetic study of Abeta(1-42) amyloidosis in the presence of ganglioside-containing vesicles. Colloids Surf. B Biointerfaces. 2020;185:110615. doi: 10.1016/j.colsurfb.2019.110615. PubMed DOI
Itoh S.G., Yagi-Utsumi M., Kato K., Okumura H. Effects of a Hydrophilic/Hydrophobic Interface on Amyloid-beta Peptides Studied by Molecular Dynamics Simulations and NMR Experiments. J. Phys. Chem. B. 2019;123:160–169. doi: 10.1021/acs.jpcb.8b11609. PubMed DOI
Hirai M., Ajito S., Sato S., Ohta N., Igarashi N., Shimizu N. Preferential Intercalation of Human Amyloid-beta Peptide into Interbilayer Region of Lipid-Raft Membrane in Macromolecular Crowding Environment. J. Phys. Chem. B. 2018;122:9482–9489. doi: 10.1021/acs.jpcb.8b08006. PubMed DOI
Yuyama K., Yanagisawa K. Late endocytic dysfunction as a putative cause of amyloid fibril formation in Alzheimer’s disease. J. Neurochem. 2009;109:1250–1260. doi: 10.1111/j.1471-4159.2009.06046.x. PubMed DOI
Fantini J., Yahi N., Garmy N. Cholesterol accelerates the binding of Alzheimer’s beta-amyloid peptide to ganglioside GM1 through a universal hydrogen-bond-dependent sterol tuning of glycolipid conformation. Front. Physiol. 2013;4:120. doi: 10.3389/fphys.2013.00120. PubMed DOI PMC
Mao Y., Shang Z., Imai Y., Hoshino T., Tero R., Tanaka M., Yamamoto N., Yanagisawa K., Urisu T. Surface-induced phase separation of a sphingomyelin/cholesterol/ganglioside GM1-planar bilayer on mica surfaces and microdomain molecular conformation that accelerates Abeta oligomerization. Biochim. Biophys. Acta. 2010;1798:1090–1099. doi: 10.1016/j.bbamem.2010.03.003. PubMed DOI
Yanagisawa K. Pathological significance of ganglioside clusters in Alzheimer’s disease. J. Neurochem. 2011;116:806–812. doi: 10.1111/j.1471-4159.2010.07006.x. PubMed DOI
Cebecauer M., Hof M., Amaro M. Impact of GM1 on Membrane-Mediated Aggregation/Oligomerization of beta-Amyloid: Unifying View. Biophys. J. 2017;113:1194–1199. doi: 10.1016/j.bpj.2017.03.009. PubMed DOI PMC
Svennerholm L. Gangliosides--a new therapeutic agent against stroke and Alzheimer’s disease. Life Sci. 1994;55:2125–2134. doi: 10.1016/0024-3205(94)00393-9. PubMed DOI
Calamai M., Pavone F.S. Partitioning and confinement of GM1 ganglioside induced by amyloid aggregates. FEBS Lett. 2013;587:1385–1391. doi: 10.1016/j.febslet.2013.03.014. PubMed DOI
Svennerholm L., Brane G., Karlsson I., Lekman A., Ramstrom I., Wikkelso C. Alzheimer disease—Effect of continuous intracerebroventricular treatment with GM1 ganglioside and a systematic activation programme. Dement. Geriatr. Cogn. Disord. 2002;14:128–136. doi: 10.1159/000063604. PubMed DOI
Sokolova T.V., Zakharova I.O., Furaev V.V., Rychkova M.P., Avrova N.F. Neuroprotective effect of ganglioside GM1 on the cytotoxic action of hydrogen peroxide and amyloid beta-peptide in PC12 cells. Neurochem. Res. 2007;32:1302–1313. doi: 10.1007/s11064-007-9304-2. PubMed DOI
Yang R., Wang Q., Min L., Sui R., Li J., Liu X. Monosialoanglioside improves memory deficits and relieves oxidative stress in the hippocampus of rat model of Alzheimer’s disease. Neurol. Sci. 2013;34:1447–1451. doi: 10.1007/s10072-012-1263-y. PubMed DOI
Kreutz F., Scherer E.B., Ferreira A.G.K., Petry F.D., Pereira C.L., Santana F., Wyse A.T.D., Salbego C.G., Trindade V.M.T. Alterations on Na+,K+-ATPase and Acetylcholinesterase Activities Induced by Amyloid-beta Peptide in Rat Brain and GM1 Ganglioside Neuroprotective Action. Neurochem. Res. 2013;38:2342–2350. doi: 10.1007/s11064-013-1145-6. PubMed DOI
Matsuoka Y., Saito M., Lafrancois J., Saito M., Gaynor K., Olm V., Wang L., Casey E., Lu Y., Shiratori C., et al. Novel therapeutic approach for the treatment of Alzheimer’s disease by peripheral administration of agents with an affinity to beta-amyloid. J. Neurosci. 2003;23:29–33. doi: 10.1523/JNEUROSCI.23-01-00029.2003. PubMed DOI PMC
Tsai Y.F., Yang D.J., Ngo T.H., Shih C.H., Wu Y.F., Lee C.K., Phraekanjanavichid V., Yen S.F., Kao S.H., Lee H.M., et al. Ganglioside Hp-s1 Analogue Inhibits Amyloidogenic Toxicity in Alzheimer’s Disease Model Cells. ACS Chem. Neurosci. 2019;10:528–536. doi: 10.1021/acschemneuro.8b00406. PubMed DOI
Cholesterol as a key player in amyloid β-mediated toxicity in Alzheimer's disease