Neurobiology of Aging
Volume 27, Issue 12 , Pages 1740-1750 , December 2006

siRNA targeted against amyloid precursor protein impairs synaptic activity in vivo

  • A.S. Hérard

      Affiliations

    • CEA-CNRS URA 2210, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
    • MIRCen, 18, Route du Panorama, F-92265 Fontenay-Aux-Roses Cedex, France
  • ,
  • L. Besret

      Affiliations

    • CEA-CNRS URA 2210, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
  • ,
  • A. Dubois

      Affiliations

    • CEA-UIIBP, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
  • ,
  • J. Dauguet

      Affiliations

    • CEA-UIIBP, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
  • ,
  • T. Delzescaux

      Affiliations

    • CEA-UIIBP, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
  • ,
  • P. Hantraye

      Affiliations

    • CEA-CNRS URA 2210, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
    • CEA-UIIBP, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
    • MIRCen, 18, Route du Panorama, F-92265 Fontenay-Aux-Roses Cedex, France
  • ,
  • G. Bonvento

      Affiliations

    • CEA-CNRS URA 2210, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
    • These authors contributed equally to this work.
    • Corresponding Author InformationCorresponding author.
  • ,
  • K.L. Moya

      Affiliations

    • CEA-CNRS URA 2210, Service Hospitalier Frédéric Joliot, 4, Place du Général Leclerc, F-91401 Orsay Cedex, France
    • These authors contributed equally to this work.
    • Corresponding Author InformationCorresponding author. Present address: CNRS UMR 8542, Ecole Normale Supérieure, 46, rue d’Ulm, 75231 Paris Cedex 05, France. Tel.: +33 1 44 32 37 19; fax: +33 1 44 32 23 23.

Received 30 June 2005 ,Revised 7 October 2005 ,Accepted 20 October 2005.

References 

  1. Ashley J, Packard M, Ataman B, Budnik V. Fasciclin II signals new synapse formation through amyloid precursor protein and the scaffolding protein dx11/Mint. J Neurosci. 2005;25:5943–5955
  2. Baranes D, Lederfein D, Huang YY, Chen M, Bailey CH, Kandel ER. Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron. 1998;21:813–825
  3. Berardi N, Pizzorusso T, Maffei L. Extracellular matrix and visual cortical plasticity: freeing the synapse. Neuron. 2004;44:905–908
  4. Binns KE. The synaptic pharmacology underlying sensory processing in the superior colliculus. Prog Neurobiol. 1999;59:129–159
  5. Bonvento G, Sibson N, Pellerin L. Does glutamate image your thoughts?. TINS. 2002;25:359–364
  6. Breen KC, Bruce M, Anderton BH. Beta amyloid precursor protein mediates neuronal cell-cell and cell-surface adhesion. J Neurosci Res. 1991;28:90–100
  7. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156–159
  8. Coulson EJ, Paliga K, Beyreuther K, Masters CL. What the evolution of the amyloid precursor protein supergene family tells us about its function. Neurochem Int. 2000;36:175–184
  9. Dawson GR, Seabrook GR, Zheng H, Smith DW, Graham S, O’Dowd G, et al. Age-related cognitive deficits, impaired long-term potentiation and reduction in synaptic marker density in mice lacking the β-amyloid precursor protein. Neuroscience. 1999;90:1–13
  10. DeKosky ST, Scheff SW, Styren SD. Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration. 1996;5:417–421
  11. Dityatev A, Schachner M. Extracellular matrix molecules and synaptic plasticity. Nat Rev Neurosci. 2003;4:456–468
  12. Eggert S, Paliga K, Soba P, Evin G, Masters CL, Weidemann A, et al. The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves alpha-, beta-, gamma-, and epsilon-like cleavages: modulation of APLP-1 processing by N-glycosylation. J Biol Chem. 2004;279:18146–18156
  13. Endo R, Murakami S, Masuda Y, Taguchi T, Ohtsuka A, Nishizaki K, et al. The perineuronal proteoglycan surface coat in the adult rat brain, with special reference to its reactions to Gomori's ammoniacal silver. Acta Med Okayama. 2000;54:111–118
  14. Furukawa K, Barger SW, Blalock EM, Mattson MP. Activation of K+ channels and suppression of neuronal activity by secreted beta-amyloid-precursor protein. Nature. 1996;379:74–78
  15. Hannon GJ, Rossi JJ. Unlocking the potential of the human genome with RNA interference. Nature. 2004;431:371–378
  16. Hess DT, Slater TM, Wilson MC, Skene JH. The 25kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J Neurosci. 1992;12:4634–4641
  17. Hilbich C, Monning U, Grund C, Masters CL, Beyreuther K. Amyloid-like properties of peptides flanking the epitope of amyloid precursor protein-specific monoclonal antibody 22C11. J Biol Chem. 1993;268:26571–26577
  18. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS. Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature. 2001;414:643–648
  19. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, et al. APP processing and synaptic function. Neuron. 2003;37:925–937
  20. Kelly BL, Vassard R, Ferreira A. β-Amyloid-induced dynamin 1 depletion in hippocampal neuron. A potential mechanism for early cognitive decline in Alzheimer disease. J Biol Chem. 2005;280:31746–31753
  21. Kennedy C, Des Rosiers MH, Sakurada O, Shinohara M, Reivich M, Jehle JW, et al. Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [14C]deoxyglucose technique. Proc Natl Acad Sci USA. 1976;73:4230–4234
  22. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, Beyreuther K, et al. Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci USA. 1990;87:1561–1565
  23. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neuropysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–156
  24. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, et al. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol. 1999;155:853–862
  25. Lyckman AW, Confaloni AM, Thinakaran G, Sisodia SS, Moya KL. Post-translational processing and turnover kinetics of presynaptically targeted amyloid precursor superfamily proteins in the central nervous system. J Biol Chem. 1998;273:11100–11106
  26. Lyckman AW, Moya KL, Confaloni A, Jhaveri S. Early postnatal expression of L1 by retinal fibers in the optic tract and synaptic targets of the Syrian hamster. J Comp Neurol. 2000;423:40–51
  27. Masliah E. Mechanisms of synaptic dysfunction in Alzheimer's disease. Histol Histopathol. 1995;10:509–519
  28. Masliah E, Mallory M, Hansen L, DeTeresa R, Alford M, Terry R. Synaptic and neuritic alterations during the progression of Alzheimer's disease. Neurosci Lett. 1994;174:67–72
  29. Mataga N, Mizuguchi Y, Hensch TK. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron. 2004;44:1031–1041
  30. McFarlane I, Breen KC, Di Giamberardino L, Moya KL. Inhibition of N-glycan processing alters axonal transport of synaptic glycoproteins in vivo. Neuroreport. 2001;11:1543–1547
  31. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, et al. Soluble pool of a beta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol. 1999;46:860–866
  32. Mize RR, Butler GD. Postembedding immunocytochemistry demonstrates directly that both retinal and cortical terminals in the cat superior colliculus are glutamate immunoreactive. J Comp Neurol. 1996;371:633–648
  33. Morin PJ, Abraham CR, Amaratunga A, Johnson RJ, Huber G, Sandell JH, et al. Amyloid precursor protein is synthesized by retinal ganglion cells, rapidly transported to the optic nerve plasma membrane and nerve terminals, and metabolized. J Neurochem. 1993;61:464–473
  34. Moya KL, Benowitz LI, Jhaveri S, Schneider GE. Changes in rapidly transported proteins in developing hamster retinofugal axons. J Neurosci. 1988;8:4445–4454
  35. Moya KL, Benowitz LI, Sabel BA, Schneider GE. Changes in rapidly transported proteins associated with development of abnormal projections in the diencephalon. Brain Res. 1992;586:265–272
  36. Moya KL, Benowitz LI, Schneider GE, Allinquant B. The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol. 1994;161:597–603
  37. Moya KL, Confaloni AM, Lyckman AW. Metabolism of a synaptic protein in mature retinal terminals in vivo: implications for Alzheimer's disease. In:  Musio C editors. Vision: The Approach of Biophysics and Neurosciences, Series on Biophysics and Biocybernetics. Singapore/New Jersey/London/Hong Kong: World Scientific; 2001;p. 89–100
  38. Nordstedt C, Gandy SE, Alafuzoff I, Caporaso GL, Iverfeldt K, Grebb JA, et al. β/A4 amyloid precursor protein in human brain: aging-associated increases in holoprotein and in a proteolytic fragment. Proc Natl Acad Sci USA. 1991;88:8910–8914
  39. Oray S, Majewska A, Sur M. Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron. 2004;44:1021–1030
  40. Ourselin S, Roche A, Subsol G, Pennec X, Ayache N. Reconstructing a 3-D structure from serial histological sections. Image Vis Comput. 2001;19:25–31
  41. Rapoport SI, Hatanpaa K, Brady DR, Chandrasekaran K. Brain energy metabolism, cognitive function and down-regulated oxidative phosphorylation in Alzheimer disease. Neurodegeneration. 1996;5:473–476
  42. Reivich M, Kuhl D, Wolf A, Greenberg J, Phelps M, Ido T, et al. The [18F]fluorodeoxyglucose method for the measurement of local cerebral glucose utilization in man. Circ Res. 1979;44:127–137
  43. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, Khvorova A. Rational siRNA design for RNA interference. Nat Biotechnol. 2004;22:326–330
  44. Rivière D, Regis J, Cointepas Y, Papadopoulos-Orfanos D, Cachia A, Mangin JF. A freely available Anatomist/BrainVISA package for structural morphometry of the cortical sulci. In: Proceedings of the 9th HBM, Neuroimage, vol. 19. 2003;p. 934
  45. Rumble R, Retallack R, Hilbich C, Simms G, Multhaup G, Martins R, et al. Amyloid A4 protein and its precursor in Down's syndrome and Alzheimer's disease. N Engl J Med. 1989;320:1446–1452
  46. Scheff SW, DeKosky ST, Price DA. Quantitative assessment of cortical synaptic density in Alzheimer's disease. Neurobiol Aging. 1990;11:29–37
  47. Scheff SW, Price DA. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol Aging. 2003;24:1029–1046
  48. Schnitzer MJ, Block SM. Kinesin hydrolyses one ATP per 8-nm step. Nature. 1997;388:386–390
  49. Schubert D, LaCorbiere M, Saitoh T, Cole G. Characterization of an amyloid beta precursor protein that binds heparin and contains tyrosine sulfate. Proc Natl Acad Sci USA. 1989;86:2066–2069
  50. Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev. 2001;81:741–766
  51. Small GW, Ercoli LM, Silverman DH, Huang SC, Komo S, Bookheimer SY, et al. Cerebral metabolic and cognitive decline in persons at genetic risk for Alzheimer's disease. Proc Natl Acad Sci USA. 2000;97:6037–6042
  52. Sokoloff L. The [14C]deoxyglucose method: four years later. Acta Neurol Scand Suppl. 1979;72:640–649
  53. Sokoloff L. Measurement of local cerebral glucose utilization and its relation to local functional activity in the brain. Adv Exp Med Biol. 1991;291:21–42
  54. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, et al. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science. 2005;307:1282–1288
  55. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, et al. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991;30:572–580
  56. Thinakaran G, Kitt CA, Roskams AJ, Slunt HH, Masliah E, von Koch C, et al. Distribution of an APP homolog, APLP2, in the mouse olfactory system: a potential role for APLP2 in axogenesis. J Neurosci. 1995;15:6314–6326
  57. Toga AW, Collins RC. Metabolic response to optic centers to visual stimuli in the albino rat: anatomical and physiological considerations. J Comp Neurol. 1981;199:443–464
  58. von Koch CS, Zheng H, Chen H, Trumbauer M, Thinakaran G, van der Ploeg LH, et al. Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol Aging. 1997;18:661–669
  59. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 2002;416:535–539
  60. Wang P, Yang G, Mosier DR, Chang P, Zaidi T, Gong YD, et al. Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-like protein 2. J Neurosci. 2005;25:1219–1225
  61. Weidemann A, Konig G, Bunke D, Fischer P, Salbaum JM, Masters CL, et al. Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell. 1989;57:115–126
  62. Wu YP, Siao CJ, Lu W, Sung TC, Frohman MA, Milev P, et al. The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J Cell Biol. 2000;148:1295–1304
  63. Zheng H, Jiang M, Trumbauer ME, Hopkins R, Sirinathsinghji DJ, Stevens KA, et al. Mice deficient for the amyloid precursor protein gene. Ann NY Acad Sci. 1996;777:421–426
  64. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJ, Hopkins R, Smith DW, et al. Beta-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell. 1995;81:525–531

PII: S0197-4580(05)00343-X

doi: 10.1016/j.neurobiolaging.2005.10.020

Neurobiology of Aging
Volume 27, Issue 12 , Pages 1740-1750 , December 2006