Impact of GM1 on Membrane-Mediated Aggregation/Oligomerization of β-Amyloid: Unifying View

. 2017 Sep 19 ; 113 (6) : 1194-1199. [epub] 20170411

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid28410623
Odkazy

PubMed 28410623
PubMed Central PMC5606962
DOI 10.1016/j.bpj.2017.03.009
PII: S0006-3495(17)30298-9
Knihovny.cz E-zdroje

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

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