Impact of GM1 on Membrane-Mediated Aggregation/Oligomerization of β-Amyloid: Unifying View
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, přehledy
PubMed
28410623
PubMed Central
PMC5606962
DOI
10.1016/j.bpj.2017.03.009
PII: S0006-3495(17)30298-9
Knihovny.cz E-zdroje
- MeSH
- amyloidní beta-protein chemie metabolismus MeSH
- G(M1) gangliosid chemie metabolismus MeSH
- lidé MeSH
- mozek metabolismus MeSH
- patologická konformace proteinů metabolismus MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
- Názvy látek
- amyloidní beta-protein MeSH
- G(M1) gangliosid MeSH
In this perspective we summarize current knowledge of the effect of monosialoganglioside GM1 on the membrane-mediated aggregation of the β-amyloid (Aβ) peptide. GM1 has been suggested to be actively involved in the development of Alzheimer's disease due to its ability to seed the aggregation of Aβ. However, GM1 is known to be neuroprotective against Aβ-induced toxicity. Here we suggest that the two scenarios are not mutually exclusive but rather complementary, and might depend on the organization of GM1 in membranes. Improving our understanding of the molecular details behind the role of gangliosides in neurodegenerative amyloidoses might help in developing disease-modifying treatments.
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Selkoe D.J., Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol. Med. 2016;8:595–608. PubMed PMC
Viola K.L., Klein W.L. Amyloid β oligomers in Alzheimer’s disease pathogenesis, treatment, and diagnosis. Acta Neuropathol. 2015;129:183–206. PubMed PMC
Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer’s and Parkinson’s diseases. Nat. Cell Biol. 2004;6:1054–1061. PubMed
Zhang Y.-J., Shi J.-M., Ji S.-R. Intra-membrane oligomerization and extra-membrane oligomerization of amyloid-β peptide are competing processes as a result of distinct patterns of motif interplay. J. Biol. Chem. 2012;287:748–756. PubMed PMC
Koo E.H., Squazzo S.L. Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J. Biol. Chem. 1994;269:17386–17389. PubMed
Cirrito J.R., Kang J.-E., Holtzman D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-β in vivo. Neuron. 2008;58:42–51. PubMed PMC
Amaro M., Birch D.J.S., Rolinski O.J. β-amyloid oligomerisation monitored by intrinsic tyrosine fluorescence. Phys. Chem. Chem. Phys. 2011;13:6434–6441. PubMed
Narayan P., Orte A., Klenerman D. The extracellular chaperone clusterin sequesters oligomeric forms of the amyloid-β (1-40) peptide. Nat. Struct. Mol. Biol. 2011;19:79–83. PubMed PMC
Vácha R., Linse S., Lund M. Surface effects on aggregation kinetics of amyloidogenic peptides. J. Am. Chem. Soc. 2014;136:11776–11782. PubMed
Zhu D., Bungart B.L., Askarova S. Role of membrane biophysics in Alzheimer’s-related cell pathways. Front. Neurosci. 2015;9:186. PubMed 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. PubMed PMC
Yanagisawa K. GM1 ganglioside and Alzheimer’s disease. Glycoconj. J. 2015;32:87–91. PubMed
Tettamanti G., Anastasia L. Chemistry, tissue and cellular distribution, and developmental profiles of neural sphingolipids. In: Lajtha A., Tettamanti G., Goracci G., editors. Handbook of Neurochemistry and Molecular Neurobiology. Springer; Boston, MA: 2010. pp. 99–171.
Matsuzaki K., Kato K., Yanagisawa K. Aβ polymerization through interaction with membrane gangliosides. Biochim. Biophys. Acta. 2010;1801:868–877. PubMed
Matsuzaki K. How do membranes initiate Alzheimer’s disease? Formation of toxic amyloid fibrils by the amyloid β-protein on ganglioside clusters. Acc. Chem. Res. 2014;47:2397–2404. PubMed
Mocchetti I. Exogenous gangliosides, neuronal plasticity and repair, and the neurotrophins. Cell. Mol. Life Sci. 2005;62:2283–2294. PubMed PMC
Kreutz F., Frozza R.L., Trindade V.M.T. Amyloid-β induced toxicity involves ganglioside expression and is sensitive to GM1 neuroprotective action. Neurochem. Int. 2011;59:648–655. PubMed
Kreutz F., Scherer E.B., Trindade V.M.T. Alterations on Na+,K+-ATPase and acetylcholinesterase activities induced by amyloid-β peptide in rat brain and GM1 ganglioside neuroprotective action. Neurochem. Res. 2013;38:2342–2350. PubMed
Sokolova T.V., Zakharova I.O., Avrova N.F. Neuroprotective effect of ganglioside GM1 on the cytotoxic action of hydrogen peroxide and amyloid β-peptide in PC12 cells. Neurochem. Res. 2007;32:1302–1313. PubMed
Yang R., Wang Q., 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. PubMed
Sagle L.B., Ruvuna L.K., Van Duyne R.P. Single plasmonic nanoparticle tracking studies of solid supported bilayers with ganglioside lipids. J. Am. Chem. Soc. 2012;134:15832–15839. PubMed PMC
Yuan C., Furlong J., Johnston L.J. The size of lipid rafts: an atomic force microscopy study of ganglioside GM1 domains in sphingomyelin/DOPC/cholesterol membranes. Biophys. J. 2002;82:2526–2535. PubMed PMC
Shi J., Yang T., Cremer P.S. GM1 clustering inhibits cholera toxin binding in supported phospholipid membranes. J. Am. Chem. Soc. 2007;129:5954–5961. PubMed PMC
Sachl R., Amaro M., Hof M. On multivalent receptor activity of GM1 in cholesterol containing membranes. Biochim. Biophys. Acta. 2015;1853:850–857. PubMed
Amaro M., Šachl R., Hof M. GM1 ganglioside inhibits β-amyloid oligomerization induced by sphingomyelin. Angew. Chem. Int. Ed. Engl. 2016;55:9411–9415. PubMed PMC
Štefl M., Šachl R., Hof M. Dynamics and size of cross-linking-induced lipid nanodomains in model membranes. Biophys. J. 2012;102:2104–2113. PubMed PMC
Kopitz J., von Reitzenstein C., Gabius H.-J. Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J. Biol. Chem. 1998;273:11205–11211. PubMed
Wu G., Lu Z.-H., Ledeen R.W. Induction of calcium influx through TRPC5 channels by cross-linking of GM1 ganglioside associated with α5β1 integrin initiates neurite outgrowth. J. Neurosci. 2007;27:7447–7458. PubMed PMC
Ichikawa N., Iwabuchi K., Arikawa-Hirasawa E. Binding of laminin-1 to monosialoganglioside GM1 in lipid rafts is crucial for neurite outgrowth. J. Cell Sci. 2009;122:289–299. PubMed PMC
Ewers H., Römer W., Johannes L. GM1 structure determines SV40-induced membrane invagination and infection. Nat. Cell Biol. 2010;12:11–18. 1–12. PubMed
Fujita A., Cheng J., Fujimoto T. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol. Biol. Cell. 2007;18:2112–2122. PubMed PMC
Fujita A., Cheng J., Fujimoto T. Segregation of GM1 and GM3 clusters in the cell membrane depends on the intact actin cytoskeleton. Biochim. Biophys. Acta. 2009;1791:388–396. PubMed
Mahfoud R., Manis A., Lingwood C.A. A major fraction of glycosphingolipids in model and cellular cholesterol-containing membranes is undetectable by their binding proteins. J. Biol. Chem. 2010;285:36049–36059. PubMed PMC
Kiyokawa E., Baba T., Kobayashi T. Spatial and functional heterogeneity of sphingolipid-rich membrane domains. J. Biol. Chem. 2005;280:24072–24084. PubMed
Parton R.G. Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J. Histochem. Cytochem. 1994;42:155–166. PubMed
Möbius W., Herzog V., Schwarzmann G. Intracellular distribution of a biotin-labeled ganglioside, GM1, by immunoelectron microscopy after endocytosis in fibroblasts. J. Histochem. Cytochem. 1999;47:1005–1014. PubMed
Rajendran L., Simons K. Lipid rafts and membrane dynamics. J. Cell Sci. 2005;118:1099–1102. PubMed
Pang H., Le P.U., Nabi I.R. Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus. J. Cell Sci. 2004;117:1421–1430. PubMed
Waschuk S.A., Elton E.A., McLaurin J.A. Cellular membrane composition defines Aβ-lipid interactions. J. Biol. Chem. 2001;276:33561–33568. PubMed
Kakio A., Nishimoto S., Matsuzaki K. Interactions of amyloid β-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. PubMed
Kim S.-I., Yi J.-S., Ko Y.-G. Amyloid β oligomerization is induced by brain lipid rafts. J. Cell. Biochem. 2006;99:878–889. PubMed
Ogawa M., Tsukuda M., Matsuzaki K. Ganglioside-mediated aggregation of amyloid β-proteins (Aβ): comparison between Aβ-(1-42) and Aβ-(1-40) J. Neurochem. 2011;116:851–857. PubMed
Ikeda K., Yamaguchi T., Matsuzaki K. Mechanism of amyloid β-protein aggregation mediated by GM1 ganglioside clusters. Biochemistry. 2011;50:6433–6440. PubMed
Yamamoto N., Matsubara T., Yanagisawa K. Age-dependent high-density clustering of GM1 ganglioside at presynaptic neuritic terminals promotes amyloid β-protein fibrillogenesis. Biochim. Biophys. Acta. 2008;1778:2717–2726. PubMed
Matsuzaki K., Horikiri C. Interactions of amyloid β-peptide (1-40) with ganglioside-containing membranes. Biochemistry. 1999;38:4137–4142. PubMed
Hu X., Crick S.L., Lee J.-M. Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-β peptide. Proc. Natl. Acad. Sci. USA. 2009;106:20324–20329. PubMed PMC
Gylys K.H., Fein J.A., Cole G.M. Increased cholesterol in Aβ-positive nerve terminals from Alzheimer’s disease cortex. Neurobiol. Aging. 2007;28:8–17. PubMed
Manna M., Mukhopadhyay C. Binding, conformational transition and dimerization of amyloid-β peptide on GM1-containing ternary membrane: insights from molecular dynamics simulation. PLoS One. 2013;8:e71308. PubMed PMC
Devarajan S., Sharmila J.S. Molecular dynamics study of GM1 ganglioside complex with amyloid β peptide (Aβ42) in lipid membrane. J. Mol. Liq. 2014;195:59–64.
Valdes-Gonzalez T., Inagawa J., Ido T. Neuropeptides interact with glycolipid receptors: a surface plasmon resonance study. Peptides. 2001;22:1099–1106. PubMed
Mandal P.K., Pettegrew J.W. Alzheimer’s disease: NMR studies of asialo (GM1) and trisialo (GT1b) ganglioside interactions with Aβ (1-40) peptide in a membrane mimic environment. Neurochem. Res. 2004;29:447–453. PubMed
Hong S., Ostaszewski B.L., Selkoe D.J. Soluble Aβ oligomers are rapidly sequestered from brain ISF in vivo and bind GM1 ganglioside on cellular membranes. Neuron. 2014;82:308–319. PubMed PMC
Linse S., Cabaleiro-Lago C., Dawson K.A. Nucleation of protein fibrillation by nanoparticles. Proc. Natl. Acad. Sci. USA. 2007;104:8691–8696. PubMed PMC
Giacomelli C.E., Norde W. Conformational changes of the amyloid β-peptide (1-40) adsorbed on solid surfaces. Macromol. Biosci. 2005;5:401–407. PubMed
Ryu J., Joung H.A., Park C.B. Surface plasmon resonance analysis of Alzheimer’s β-amyloid aggregation on a solid surface: from monomers to fully-grown fibrils. Anal. Chem. 2008;80:2400–2407. PubMed
Minton A.P. Effects of excluded surface area and adsorbate clustering on surface adsorption of proteins I. Equilibrium models. Biophys. Chem. 2000;86:239–247. PubMed
Minton A.P. Effects of excluded surface area and adsorbate clustering on surface adsorption of proteins. II. Kinetic models. Biophys. J. 2001;80:1641–1648. PubMed PMC
Byström R., Aisenbrey C., Gröbner G. Disordered proteins: biological membranes as two-dimensional aggregation matrices. Cell Biochem. Biophys. 2008;52:175–189. PubMed
Janich P., Corbeil D. GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett. 2007;581:1783–1787. PubMed
Crino P.B., Ullman M.D., Volicer L. Brain gangliosides in dementia of the Alzheimer type. Arch. Neurol. 1989;46:398–401. PubMed
Kracun I., Rosner H., Lauc G. Human brain gangliosides in development, aging and disease. Int. J. Dev. Biol. 1991;35:289–295. PubMed
Svennerholm L., Boström K., Olsson L. Membrane lipids of adult human brain: lipid composition of frontal and temporal lobe in subjects of age 20 to 100 years. J. Neurochem. 1994;63:1802–1811. PubMed
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. PubMed
Grimm M.O.W., Grimm H.S., Hartmann T. Regulation of cholesterol and sphingomyelin metabolism by amyloid-β and presenilin. Nat. Cell Biol. 2005;7:1118–1123. PubMed
Huang M., Hu M., Gao X. GM1-modified lipoprotein-like nanoparticle: multifunctional nanoplatform for the combination therapy of Alzheimer’s disease. ACS Nano. 2015;9:10801–10816. PubMed
Yuyama K., Sun H., Igarashi Y. Decreased amyloid-β pathologies by intracerebral loading of glycosphingolipid-enriched exosomes in Alzheimer model mice. J. Biol. Chem. 2014;289:24488–24498. PubMed PMC