Neurobiology of Aging
Volume 30, Issue 11 , Pages 1777-1791 , November 2009

Elimination of GD3 synthase improves memory and reduces amyloid-β plaque load in transgenic mice

  • Alexandra Bernardo

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN, United States
    • Program in Neuroscience, Vanderbilt University, Nashville, TN, United States
  • ,
  • Fiona E. Harrison

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN, United States
    • Program in Neuroscience, Vanderbilt University, Nashville, TN, United States
  • ,
  • Meghan McCord

      Affiliations

    • Program in Neuroscience, Vanderbilt University, Nashville, TN, United States
  • ,
  • Jiali Zhao

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN, United States
  • ,
  • Aleksandra Bruchey

      Affiliations

    • Program in Neuroscience, Vanderbilt University, Nashville, TN, United States
  • ,
  • Sean S. Davies

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN, United States
  • ,
  • L. Jackson Roberts II

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN, United States
  • ,
  • Paul M. Mathews

      Affiliations

    • Center for Dementia Research, Nathan Kline Institute for Psychiatric Research, Department of Psychiatry, New York University Medical Center, Orangeburg, NY, United States
  • ,
  • Yasuji Matsuoka

      Affiliations

    • Department of Neurology, Georgetown University, Washington, DC, United States
  • ,
  • Toshio Ariga

      Affiliations

    • Institute of Molecular Medicine and Genetics and Institute of Neuroscience, Medical College of Georgia, Augusta, GA, United States
  • ,
  • Robert K. Yu

      Affiliations

    • Institute of Molecular Medicine and Genetics and Institute of Neuroscience, Medical College of Georgia, Augusta, GA, United States
  • ,
  • Rebecca Thompson

      Affiliations

    • Program in Neuroscience, Vanderbilt University, Nashville, TN, United States
  • ,
  • Michael P. McDonald

      Affiliations

    • Department of Pharmacology, Vanderbilt University, Nashville, TN, United States
    • Program in Neuroscience, Vanderbilt University, Nashville, TN, United States
    • Departments of Neurology and Anatomy & Neurobiology, University of Tennessee Health Science Center, Memphis, TN, United States
    • Corresponding Author InformationCorresponding author at: University of Tennessee Health Science Center, 855 Monroe Avenue, Link Building, Room 415, Memphis, TN 38163, United States. Tel.: +1 901 448 4648.

Received 11 October 2007 ,Revised 21 December 2007 ,Accepted 21 December 2007.

References 

  1. Ariga T, Yu RK. GM1 inhibits amyloid beta-protein-induced cytokine release. Neurochem. Res. 1999;24:219–226
  2. Ariga T, Kobayashi K, Kuroda Y, Yu RK, Suzuki M, Kitagawa H, et al. Characterization of tumor-associated fucogangliosides from PC 12 pheochromocytoma cells. J. Biol. Chem. 1987;262:14146–14153
  3. 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
  4. Augustinsson LE, Blennow K, Blomstrand C, Brane G, Ekman R, Fredman P, et al. Intracerebroventricular administration of GM1 ganglioside to presenile Alzheimer patients. Dement. Geriatr. Cogn. Disord. 1997;8:26–33
  5. Bachis A, Rabin SJ, Del Fiacco M, Mocchetti I. Gangliosides prevent excitotoxicity through activation of TrkB receptor. Neurotox. Res. 2002;4:225–234
  6. Bambrick LL, de Grip A, Seenivasan V, Krueger BK, Yarowsky PJ. Expression of glial antigens in mouse astrocytes: species differences and regulation in vitro. J. Neurosci. Res. 1996;46:305–315
  7. Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 1979;93:74–104
  8. Barnes CA. Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat. Trends Neurosci. 1988;11:163–169
  9. Bernardo A, McCord M, Troen AM, Allison JD, McDonald MP. Impaired spatial memory in APP-overexpressing mice on a homocysteinemia-inducing diet. Neurobiol. Ageing. 2007;28:1195–1205
  10. Bornemann KD, Wiederhold KH, Pauli C, Ermini F, Stalder M, Schnell L, et al. Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am. J. Pathol. 2001;158:63–73
  11. Casamenti F, Bracco L, Bartolini L, Pepeu G. Effects of ganglioside treatment in rats with a lesion of the cholinergic forebrain nuclei. Brain Res. 1985;338:45–52
  12. Choo-Smith LP, Surewicz WK. The interaction between Alzheimer amyloid beta(1–40) peptide and ganglioside GM1-containing membranes. FEBS Lett. 1997;402:95–98
  13. 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
  14. Copani A, Melchiorri D, Caricasole A, Martini F, Sale P, Carnevale R, et al. Beta-amyloid-induced synthesis of the ganglioside GD3 is a requisite for cell cycle reactivation and apoptosis in neurons. J. Neurosci. 2002;22:3963–3968
  15. De Maria R, Lenti L, Malisan F, d’Agostino F, Tomassini B, Zeuner A, et al. Requirement for GD3 ganglioside in CD95- and ceramide-induced apoptosis. Science. 1997;277:1652–1655
  16. Drago J, Reid KL, Bartlett PF. Induction of the ganglioside marker A2B5 on cultured cerebellar neural cells by growth factors. Neurosci. Lett. 1989;107:245–250
  17. Eckert A, Keil U, Marques CA, Bonert A, Frey C, Schussel K, et al. Mitochondrial dysfunction, apoptotic cell death, and Alzheimer's disease. Biochem. Pharmacol. 2003;66:1627–1634
  18. Emerich DF, Walsh TJ. Selective working memory impairments following intradentate injection of colchicine: attenuation of the behavioral but not the neuropathological effects by gangliosides GM1 and AGF2. Physiol. Behav. 1989;45:93–101
  19. Ferrari G, Greene LA. Prevention of neuronal apoptotic death by neurotrophic agents and ganglioside GM1: insights and speculations regarding a common mechanism. Perspect. Dev. Neurobiol. 1996;3:93–100
  20. Fighera MR, Royes LF, Furian AF, Oliveira MS, Fiorenza NG, Frussa-Filho R, et al. GM1 ganglioside prevents seizures, Na+, K+-ATPase activity inhibition and oxidative stress induced by glutaric acid and pentylenetetrazole. Neurobiol. Dis. 2006;22:611–623
  21. Flicker C, Ferris SH, Kalkstein D, Serby M. A double-blind, placebo-controlled crossover study of ganglioside GM1 treatment for Alzheimer's disease. Am. J. Psychiatry. 1994;151:126–129
  22. Fong TG, Neff NH, Hadjiconstantinou M. GM1 ganglioside improves spatial learning and memory of aged rats. Behav. Brain Res. 1997;85:203–211
  23. Garcia-Ruiz C, Colell A, Paris R, Fernandez-Checa JC. Direct interaction of GD3 ganglioside with mitochondria generates reactive oxygen species followed by mitochondrial permeability transition, cytochrome c release, and caspase activation. FASEB J. 2000;14:847–858
  24. Gellermann GP, Appel TR, Tannert A, Radestock A, Hortschansky P, Schroeckh V, et al. Raft lipids as common components of human extracellular amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 2005;102:6297–6302
  25. Glasier MM, Sutton RL, Stein DG. Effects of unilateral entorhinal cortex lesion and ganglioside GM1 treatment on performance in a novel water maze task. Neurobiol. Learn Mem. 1995;64:203–214
  26. Glasier MM, Janis LS, Goncalves MI, Stein DG. GM1 produces attenuation of short-term memory deficits in Hebb-Williams maze performance after unilateral entorhinal cortex lesions. Physiol. Behav. 1999;66:441–446
  27. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ. Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature. 1992;357:500–503
  28. Harrison FE, Reiserer RS, Tomarken AJ, McDonald MP. Spatial and nonspatial escape strategies in the Barnes maze. Learn Mem. 2006;13:809–819
  29. 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
  30. Hicks D, Heidinger V, Mohand-Said S, Sahel J, Dreyfus H. Growth factors and gangliosides as neuroprotective agents in excitotoxicity and ischemia. Gen. Pharmacol. 1998;30:265–273
  31. Hof PR, Young WG, Bloom FE, Belichenko PV, Celio MR. Comparative Cytoarchitectonic Atlas of the C57BL6 and 129Sv Mouse Brains. New York: Elsevier; 2000;
  32. Holmes A, Wrenn CC, Harris AP, Thayer KE, Crawley JN. Behavioral profiles of inbred strains on novel olfactory, spatial and emotional tests for reference memory in mice. Genes Brain Behav. 2002;1:55–69
  33. Horikoshi Y, Sakaguchi G, Becker AG, Gray AJ, Duff K, Aisen PS, et al. Development of Abeta terminal end-specific antibodies and sensitive ELISA for Abeta variant. Biochem. Biophys. Res. Commun. 2004;319:733–737
  34. Huettner JE, Baughman RW. Primary culture of identified neurons from the visual cortex of postnatal rats. J. Neurosci. 1986;6:3044–3060
  35. Itagaki S, McGeer PL, Akiyama H, Zhu S, Selkoe D. Relationship of microglia and astrocytes to amyloid deposits of Alzheimer disease. J. Neuroimmunol. 1989;24:173–182
  36. 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
  37. 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
  38. Kalanj S, Kracun I, Rosner H, Cosovic C. Regional distribution of brain gangliosides in Alzheimer's disease. Neurol. Croat. 1991;40:269–281
  39. Kawai H, Allende ML, Wada R, Kono M, Sango K, Deng C, et al. Mice expressing only monosialoganglioside GM3 exhibit lethal audiogenic seizures. J. Biol. Chem. 2001;276:6885–6888
  40. Kim SI, Yi JS, Ko YG. Amyloid beta oligomerization is induced by brain lipid rafts. J. Cell Biochem. 2006;99:878–889
  41. Knapp PE. Studies of glial lineage and proliferation in vitro using an early marker for committed oligodendrocytes. J. Neurosci. Res. 1991;30:336–345
  42. Kracun I, Kalanj S, Talan-Hranilovic J, Cosovic C. Cortical distribution of gangliosides in Alzheimer's disease. Neurochem. Int. 1992;20:433–438
  43. Kristal BS, Brown AM. Apoptogenic ganglioside GD3 directly induces the mitochondrial permeability transition. J. Biol. Chem. 1999;274:23169–23175
  44. Kurganov B, Doh M, Arispe N. Aggregation of liposomes induced by the toxic peptides Alzheimer's Abetas, human amylin and prion (106–126): facilitation by membrane-bound GM1 ganglioside. Peptides. 2004;25:217–232
  45. Lalonde R, Kim HD, Fukuchi K. Exploratory activity, anxiety, and motor coordination in bigenic APPswe+PS1/DeltaE9 mice. Neurosci. Lett. 2004;369:156–161
  46. Lalonde R, Kim HD, Maxwell JA, Fukuchi K. Exploratory activity and spatial learning in 12-month-old APP(695)SWE/co+PS1/DeltaE9 mice with amyloid plaques. Neurosci. Lett. 2005;390:87–92
  47. Liao MQ, Tzeng YJ, Chang LY, Huang HB, Lin TH, Chyan CL, et al. The correlation between neurotoxicity, aggregative ability and secondary structure studied by sequence truncated Abeta peptides. FEBS Lett. 2007;581:1161–1165
  48. Liu Y, Hoffmann A, Grinberg A, Westphal H, McDonald MP, Miller KM, et al. Mouse model of GM2 activator deficiency manifests cerebellar pathology and motor impairment. Proc. Natl. Acad. Sci. U.S.A. 1997;94:8138–8143
  49. Lombardi G, Zanoni R, Moroni F. Systemic treatments with GM1 ganglioside reduce quinolinic acid-induced striatal lesions in the rat. Eur. J. Pharmacol. 1989;174:123–125
  50. Magoski NS, Walz W, Juurlink BH. Identification of mouse type-2-like astrocytes: demonstration of glutamate and GABA transmitter activated responses. J. Neurosci. Res. 1992;33:91–102
  51. Mahadik SP, Vilim F, Korenovsky A, Karpiak SE. GM1 ganglioside protects nucleus basalis from excitotoxin damage: reduced cortical cholinergic losses and animal mortality. J. Neurosci. Res. 1988;20:479–483
  52. Mahadik SP, Hungund BL, Gokhale VS, Ortiz A, Makar TK, Karpiak SE. Monosialoganglioside (GM1) restores membrane fatty acid levels in ischemic tissue after cortical focal ischemia in rat. Neurochem. Int. 1993;23:163–172
  53. Malisan F, Testi R. The ganglioside GD3 as the Greek goddess Hecate: several faces turned towards as many directions. IUBMB Life. 2005;57:477–482
  54. Masliah E, Hansen L, Albright T, Mallory M, Terry RD. Immunoelectron microscopic study of synaptic pathology in Alzheimer's disease. Acta Neuropathol. (Berl.). 1991;81:428–433
  55. Matsuoka Y, Saito M, LaFrancois J, Gaynor K, Olm V, Wang L, 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
  56. Matsuzaki K, Horikiri C. Interactions of amyloid beta-peptide (1–40) with ganglioside-containing membranes. Biochemistry. 1999;38:4137–4142
  57. McDonald MP, Overmier JB. Present imperfect: a critical review of animal models of the mnemonic impairments in Alzheimer's disease. Neurosci. Biobehav. Rev. 1998;22:99–120
  58. McDonald MP, Dahl EE, Overmier JB, Mantyh P, Cleary J. Effects of an exogenous beta-amyloid peptide on retention for spatial learning. Behav. Neural. Biol. 1994;62:60–67
  59. McDonald MP, Overmier JB, Bandyopadhyay S, Babcock D, Cleary J. Reversal of beta-amyloid-induced retention deficit after exposure to training and state cues. Neurobiol. Learn Mem. 1996;65:35–47
  60. McDonald MP, Wenk GL, Crawley JN. Analysis of galanin and the galanin antagonist M40 on delayed non-matching-to-position performance in rats lesioned with the cholinergic immunotoxin 192 IgG-saporin. Behav. Neurosci. 1997;111:552–563
  61. McDonald MP, Willard LB, Wenk GL, Crawley JN. Coadministration of galanin antagonist M40 with a muscarinic M1 agonist improves delayed nonmatching to position choice accuracy in rats with cholinergic lesions. J. Neurosci. 1998;18:5078–5085
  62. 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
  63. McLaurin J, Franklin T, Fraser PE, Chakrabartty A. Structural transitions associated with the interaction of Alzheimer beta-amyloid peptides with gangliosides. J. Biol. Chem. 1998;273:4506–4515
  64. Meda L, Cassatella MA, Szendrei GI, Otvos L, Baron P, Villalba M, et al. Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature. 1995;374:647–650
  65. Melnikova T, Savonenko A, Wang Q, Liang X, Hand T, Wu L, et al. Cycloxygenase-2 activity promotes cognitive deficits but not increased amyloid burden in a model of Alzheimer's disease in a sex-dimorphic pattern. Neuroscience. 2006;141:1149–1162
  66. Miyakawa T, Yamada M, Duttaroy A, Wess J. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J. Neurosci. 2001;21:5239–5250
  67. Miyakawa T, Yared E, Pak JH, Huang FL, Huang KP, Crawley JN. Neurogranin null mutant mice display performance deficits on spatial learning tasks with anxiety related components. Hippocampus. 2001;11:763–775
  68. Nishitomi K, Sakaguchi G, Horikoshi Y, Gray AJ, Maeda M, Hirata-Fukae C, et al. BACE1 inhibition reduces endogenous Abeta and alters APP processing in wild-type mice. J. Neurochem. 2006;99:1555–1563
  69. Nobile-Orazio E, Carpo M, Meucci N, Grassi MP, Capitani E, Sciacco M, et al. Guillain-Barre syndrome associated with high titers of anti-GM1 antibodies. J. Neurol. Sci. 1992;109:200–206
  70. Odaka M, Yuki N, Nobile-Orazio E, Carpo M, Hirata K. Antibodies to GM1(NeuGc) in Guillain-Barre syndrome after ganglioside therapy. J. Neurol. Sci. 2000;175:96–106
  71. Pompl PN, Mullan MJ, Bjugstad K, Arendash GW. Adaptation of the circular platform spatial memory task for mice: use in detecting cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer's disease. J. Neurosci. Methods. 1999;87:87–95
  72. Rahmann H. Brain gangliosides and memory formation. Behav. Brain Res. 1995;66:105–116
  73. Reiserer RS, Harrison FE, Syverud DC, McDonald MP. Impaired spatial learning in the APP+PSEN1 DeltaE9 bigenic mouse model of Alzheimer's disease. Genes Brain Behav. 2007;6:54–65
  74. Roberts LJ, Montine TJ, Markesbery WR, Tapper AR, Hardy P, Chemtob S, et al. Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid. J. Biol. Chem. 1998;273:13605–13612
  75. Roeser C, Cassel JC, Kelche C. Behavioral effects of GM1 ganglioside treatment and intrahippocampal septal grafts in rats with fimbria-fornix lesions. Exp. Brain Res. 1997;115:520–530
  76. Sango K, McDonald MP, Crawley JN, Mack ML, Tifft CJ, Skop E, et al. Mice lacking both subunits of lysosomal beta-hexosaminidase display gangliosidosis and mucopolysaccharidosis. Nat. Genet. 1996;14:348–352
  77. Santucci AC, Gluck R, Kanof PD, Haroutunian V. Induction of memory and cortical cholinergic neurochemical recovery with combine fetal transplantation and GM1 treatments in rats with lesions of the NBM. Dementia. 1993;4:273–281
  78. Sasaki A, Shoji M, Harigaya Y, Kawarabayashi T, Ikeda M, Naito M, et al. Amyloid cored plaques in Tg2576 transgenic mice are characterized by giant plaques, slightly activated microglia, and the lack of paired helical filament-typed, dystrophic neurites. Virchows Arch. 2002;441:358–367
  79. Schneider JS, Roeltgen DP, Mancall EL, Chapas-Crilly J, Rothblat DS, Tatarian GT. Parkinson's disease: improved function with GM1 ganglioside treatment in a randomized placebo-controlled study. Neurology. 1998;50:1630–1636
  80. Scorrano L, Petronilli V, Di Lisa F, Bernardi P. Commitment to apoptosis by GD3 ganglioside depends on opening of the mitochondrial permeability transition pore. J. Biol. Chem. 1999;274:22581–22585
  81. Silva RH, Felicio LF, Nasello AG, Vital MA, Frussa-Filho R. Effect of ganglioside (GM1) on memory in senescent rats. Neurobiol. Ageing. 1996;17:583–586
  82. Silva RH, Felicio LF, Frussa-Filho R. Ganglioside GM1 attenuates scopolamine-induced amnesia in rats and mice. Psychopharmacology (Berl.). 1999;141:111–117
  83. Skaper SD, Leon A, Facci L. Death of cultured hippocampal pyramidal neurons induced by pathological activation of N-methyl-d-aspartate receptors is reduced by monosialogangliosides. J. Pharmacol. Exp. Ther. 1991;259:452–457
  84. 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
  85. Sweeney WA, Luedtke J, McDonald MP, Overmier JB. Intrahippocampal injections of exogenous beta-amyloid induce postdelay errors in an eight-arm radial maze. Neurobiol. Learn Mem. 1997;68:97–101
  86. Tamboli IY, Prager K, Barth E, Heneka M, Sandhoff K, Walter J. Inhibition of glycosphingolipid biosynthesis reduces secretion of the beta-amyloid precursor protein and amyloid beta-peptide. J. Biol. Chem. 2005;280:28110–28117
  87. Tashima Y, Oe R, Lee S, Sugihara G, Chambers EJ, Takahashi M, et al. The effect of cholesterol and monosialoganglioside (GM1) on the release and aggregation of amyloid beta-peptide from liposomes prepared from brain membrane-like lipids. J. Biol. Chem. 2004;279:17587–17595
  88. 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
  89. Walsh TJ, Emerich DF, Schmechel DE. GM1 ganglioside attenuates the behavioral deficits but not the granule cell damage produced by intradentate colchicine. Brain Res. 1989;478:24–33
  90. Williams MA, McCluer RH. The use of Sep-Pak C18 cartridges during the isolation of gangliosides. J. Neurochem. 1980;35:266–269
  91. 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
  92. Yu RK, Ledeen RW. Gangliosides of human, bovine, and rabbit plasma. J. Lipid Res. 1972;13:680–686
  93. Yuki N, Sato S, Miyatake T, Sugiyama K, Katagiri T, Sasaki H. Motoneuron-disease-like disorder after ganglioside therapy. Lancet. 1991;337:1109–1110
  94. Zhu MY, Hasty AH, Harris C, Linton MF, Fazio S, Swift LL. Physiological relevance of apolipoprotein E recycling: studies in primary mouse hepatocytes. Metabolism. 2005;54:1309–1315

PII: S0197-4580(07)00498-8

doi: 10.1016/j.neurobiolaging.2007.12.022

Neurobiology of Aging
Volume 30, Issue 11 , Pages 1777-1791 , November 2009