Neurobiology of Aging
Volume 30, Issue 8 , Pages 1245-1253 , August 2009

Ganglioside GM1 binding the N-terminus of amyloid precursor protein

  • Handi Zhang

      Affiliations

    • Institute of Mental Health, Peking University, Key Laboratories for Mental Health, Ministry of Health, 51 Hua Yuan Bei Road, 100083 Beijing, China
    • These authors equally contributed to this work.
    • ,
  • Jixin Ding

      Affiliations

    • Institute of Mental Health, Peking University, Key Laboratories for Mental Health, Ministry of Health, 51 Hua Yuan Bei Road, 100083 Beijing, China
    • These authors equally contributed to this work.
    • ,
  • Wenqiang Tian

      Affiliations

    • Institute of Mental Health, Peking University, Key Laboratories for Mental Health, Ministry of Health, 51 Hua Yuan Bei Road, 100083 Beijing, China
    • ,
  • Lijun Wang

      Affiliations

    • Department of Biophysics, School of Basic Medical Sciences, Peking University, 38 Xue Yuan Road, 100083 Beijing, China
    • ,
  • Lixin Huang

      Affiliations

    • Department of Biophysics, School of Basic Medical Sciences, Peking University, 38 Xue Yuan Road, 100083 Beijing, China
    • ,
  • Yan Ruan

      Affiliations

    • Institute of Mental Health, Peking University, Key Laboratories for Mental Health, Ministry of Health, 51 Hua Yuan Bei Road, 100083 Beijing, China
    • ,
  • Tianlan Lu

      Affiliations

    • Institute of Mental Health, Peking University, Key Laboratories for Mental Health, Ministry of Health, 51 Hua Yuan Bei Road, 100083 Beijing, China
    • ,
  • Yinlin Sha

      Affiliations

    • Department of Biophysics, School of Basic Medical Sciences, Peking University, 38 Xue Yuan Road, 100083 Beijing, China
    • Corresponding Author InformationCorresponding author. Tel.: +86 10 82801278; fax: +86 10 82332096.
    • ,
  • Dai Zhang

      Affiliations

    • Institute of Mental Health, Peking University, Key Laboratories for Mental Health, Ministry of Health, 51 Hua Yuan Bei Road, 100083 Beijing, China
    • Corresponding Author InformationCorresponding author. Tel.: +86 10 82801937; fax: +86 10 62078246.

Received 6 August 2007 ,Revised 29 October 2007 ,Accepted 3 November 2007.

References 

  1. Ames B. Assay of inorganic phosphate, total phosphate and phosphatases. Meth. Enzymol. 1966;8:115–118
  2. Beher D, Hesse L, Masters CL, Multhaup G. Regulation of amyloid protein precursor (APP) binding to collagen and mapping of the binding sites on APP and collagen type I. J. Biol. Chem. 1996;271:1613–1620
  3. Blennow K, Davidsson P, Wallin A, Fredman P, Gottfries CG, Karlsson I, et al. Gangliosides in cerebrospinal fluid in ’probable Alzheimer's disease’. Arch. Neurol. 1991;48:1032–1035
  4. Blennow K, Davidsson P, Wallin A, Fredman P, Gottfries CG, Mansson JE, et al. Differences in cerebrospinal fluid gangliosides between “probable Alzheimer's disease” and normal aging. Aging (Milano). 1992;4:301–306
  5. Borchardt T, Camakaris J, Cappai R, Masters CL, Beyreuther K, Multhaup G. Copper inhibits beta-amyloid production and stimulates the non-amyloidogenic pathway of amyloid-precursor-protein secretion. Biochem. J. 1999;344(Pt 2):461–467
  6. Bush AI, Multhaup G, Moir RD, Williamson TG, Small DH, Rumble B, et al. A novel zinc(II) binding site modulates the function of the beta A4 amyloid protein precursor of Alzheimer's disease. J. Biol. Chem. 1993;268:16109–16112
  7. Chapman J, Sela BA, Wertman E, Michaelson DM. Antibodies to ganglioside GM1 in patients with Alzheimer's disease. Neurosci. Lett. 1988;86:235–240
  8. Clarris HJ, Cappai R, Heffernan D, Beyreuther K, Masters CL, Small DH. Identification of heparin-binding domains in the amyloid precursor protein of Alzheimer's disease by deletion mutagenesis and peptide mapping. J. Neurochem. 1997;68:1164–1172
  9. Cordy JM, Hussain I, Dingwall C, Hooper NM, Turner AJ. Exclusively targeting beta-secretase to lipid rafts by GPI-anchor addition up-regulates beta-site processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. U.S.A. 2003;100:11735–11740
  10. Ehehalt R, Keller P, Haass C, Thiele C, Simons K. Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 2003;160:113–123
  11. Fishman PH. Role of membrane gangliosides in the binding and action of bacterial toxins. J. Membr. Biol. 1982;69:85–97
  12. Haas C, Cazorla P, Miguel CD, Valdivieso F, Vazquez J. Apolipoprotein E forms stable complexes with recombinant Alzheimer's disease beta-amyloid precursor protein. Biochem. J. 1997;325(Pt 1):169–175
  13. Hartmann T, Bergsdorf C, Sandbrink R, Tienari PJ, Multhaup G, Ida N, et al. Alzheimer's disease betaA4 protein release and amyloid precursor protein sorting are regulated by alternative splicing. J. Biol. Chem. 1996;271:13208–13214
  14. Hass S, Fresser F, Kochl S, Beyreuther K, Utermann G, Baier G. Physical interaction of ApoE with amyloid precursor protein independent of the amyloid Abeta region in vitro. J. Biol. Chem. 1998;273:13892–13897
  15. Hesse L, Beher D, Masters CL, Multhaup G. The beta A4 amyloid precursor protein binding to copper. FEBS Lett. 1994;349:109–116
  16. Ho A, Sudhof TC. Binding of F-spondin to amyloid-{beta} precursor protein: a candidate amyloid-{beta} precursor protein ligand that modulates amyloid-{beta} precursor protein cleavage. PNAS. 2004;101:2548–2553
  17. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, et al. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature. 1987;325:733–736
  18. Kracun I, Kalanj S, Talan-Hranilovic J, Cosovic C. Cortical distribution of gangliosides in Alzheimer's disease. Neurochem. Int. 1992;20:433–438
  19. Lee SJ, Liyanage U, Bickel PE, Xia W, Lansbury PT, Kosik KS. A detergent-insoluble membrane compartment contains A beta in vivo. Nat. Med. 1998;4:730–734
  20. Liu H, Wang Y, Zhang Y, Song Q, Di C, Chen G, et al. TFAR19, a novel apoptosis-related gene cloned from human leukemia cell line TF-1, could enhance apoptosis of some tumor cells induced by growth factor withdrawal. Biochem. Biophys. Res. Commun. 1999;254:203–210
  21. Martinez Z, Zhu M, Han S, Fink AL. GM1 specifically interacts with alpha-synuclein and inhibits fibrillation. Biochemistry. 2007;46:1868–1877
  22. Miles LA, Dahlberg CM, Levin EG, Plow EF. Gangliosides interact directly with plasminogen and urokinase and may mediate binding of these fibrinolytic components to cells. Biochemistry. 1989;28:9337–9343
  23. Miljan EA, Bremer EG. Regulation of growth factor receptors by gangliosides. Sci. STKE. 2002;RE15;2002
  24. Miljan EA, Meuillet EJ, Mania-Farnell B, George D, Yamamoto H, Simon HG, et al. Interaction of the extracellular domain of the epidermal growth factor receptor with gangliosides. J. Biol. Chem. 2002;277:10108–10113
  25. Mok SS, Sberna G, Heffernan D, Cappai R, Galatis D, Clarris HJ, et al. Expression and analysis of heparin-binding regions of the amyloid precursor protein of Alzheimer's disease. FEBS Lett. 1997;415:303–307
  26. Molander-Melin M, Blennow K, Bogdanovic N, Dellheden B, Mansson E, Fredman P. Lipid analyses of human brain rafts. J. Neurochem. 2003;85:34
  27. Molander-Melin M, Blennow K, Bogdanovic N, Dellheden B, Mansson JE, 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
  28. Morishima-Kawashima M, Ihara Y. The presence of amyloid beta-protein in the detergent-insoluble membrane compartment of human neuroblastoma cells. Biochemistry. 1998;37:15247–15253
  29. Multhaup G, Schlicksupp A, Hesse L, Beher D, Ruppert T, Masters CL, et al. The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science. 1996;271:1406–1409
  30. Parkin ET, Turner AJ, Hooper NM. Amyloid precursor protein, although partially detergent-insoluble in mouse cerebral cortex, behaves as an atypical lipid raft protein. Biochem. J. 1999;344(Pt 1):23–30
  31. Peraus GC, Masters CL, Beyreuther K. Late compartments of amyloid precursor protein transport in SY5Y cells are involved in beta-amyloid secretion. J. Neurosci. 1997;17:7714–7724
  32. Riddell DR, Christie G, Hussain I, Dingwall C. Compartmentalization of beta-secretase (Asp2) into low-buoyant density, noncaveolar lipid rafts. Curr. Biol. 2001;11:1288–1293
  33. Ross RA, Spengler BA, Biedler JL. Coordinate morphological and biochemical interconversion of human neuroblastoma cells. J. Natl. Cancer Inst. 1983;71:741–747
  34. Rusnati M, Urbinati C, Tanghetti E, Dell’Era P, Lortat-Jacob H, Presta M. Cell membrane GM1 ganglioside is a functional coreceptor for fibroblast growth factor 2. Proc. Natl. Acad. Sci. U.S.A. 2002;99:4367–4372
  35. Sawamura N, Ko M, Yu W, Zou K, Hanada K, Suzuki T, et al. Modulation of amyloid precursor protein cleavage by cellular sphingolipids. J. Biol. Chem. 2004;279:11984–11991
  36. Spiegel S, Fishman PH, Weber RJ. Direct evidence that endogenous GM1 ganglioside can mediate thymocyte proliferation. Science. 1985;230:1285–1287
  37. Svennerholm L, Gottfries CG. 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
  38. 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
  39. Vetrivel KS, Cheng H, Lin W, Sakurai T, Li T, Nukina N, et al. Association of gamma-secretase with lipid rafts in post-Golgi and endosome membranes. J. Biol. Chem. 2004;279:44945–44954
  40. Weidemann A, Konig G, Bunke D, Fischer P, Salbaum JM, Masters CL, et al. Identification, biogenesis and localization of precursor of Alzheimer's disease A4 amyloid protein. Cell. 1989;57:115–126
  41. Zha Q, Ruan Y, Hartmann T, Beyreuther K, Zhang D. GM1 ganglioside regulates the proteolysis of amyloid precursor protein. Mol. Psychiatry. 2004;9:946–952

PII: S0197-4580(07)00444-7

doi: 10.1016/j.neurobiolaging.2007.11.013

Neurobiology of Aging
Volume 30, Issue 8 , Pages 1245-1253 , August 2009

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