Neuronal Aβ42 is enriched in small vesicles at the presynaptic side of synapses

Life Science Alliance

Volumn 1, Issue 3, 2018, Pages

  Yu, Yang ^a   Jans, Daniel C ^b   Winblad, Bengt ^a   Tjernberg, Lars O ^a   Schedin Weiss, Sophia ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85057059718     PISSN: None     EISSN: 25751077     Source Type: Journal    
DOI: 10.26508/lsa.201800028     Document Type: Article

References (38)

1. Raskin J, Cummings J, Hardy J, Schuh K, Dean RA (2015) Neurobiology of Alzheimer’s disease: Integrated molecular, physiological, anatomical, biomarker, and cognitive dimensions. Curr Alzheimer Res 12: 712–712. doi:10.2174/1567205012666150701103107
2. Jack CR Jr, Holtzman, DM (2013) Biomarker modeling of Alzheimer’s disease. Neuron 80: 1347–1358. doi:10.1016/j.neuron.2013.12.003
3. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: Lessons from the Alzheimer’s amyloid beta-peptide. Nat Rev Mol Cell Biol 8: 101–112. doi:10.1038/nrm2101
4. Wilcox KC, Lacor PN, Pitt J, Klein WL (2011) Abeta oligomer-induced synapse degeneration in Alzheimer’s disease. Cell Mol Neurobiol 31: 939–948. doi:10.1007/s10571-011-9691-4
5. De Strooper B, Karran E (2016) The cellular phase of Alzheimer’s disease. Cell 164: 603–615. doi:10.1016/j.cell.2015.12.056.
6. Hashimoto M, Bogdanovic N, Nakagawa H, Volkmann I, Aoki M, Winblad B, Sakai J, Tjernberg LO (2012) Analysis of microdissected neurons by 18O mass spectrometry reveals altered protein expression in Alzheimer’s disease. J Cell Mol Med 16: 1686–1700. doi:10.1111/j.1582-4934.2011.01441.x
7. Takahashi RH, Milner TA, Li F, Nam EE, Edgar MA, Yamaguchi H, Beal MF, Xu H, Greengard P, Gouras GK (2002) Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 161: 1869–1879. doi:10.1016/s0002-9440(10)64463-x
8. Nilsson P, Loganathan K, Sekiguchi M, Matsuba Y, Hui K, Tsubuki S, Tanaka M, Iwata N, Saito T, Saido TC (2013) Aβ secretion and plaque formation depend on autophagy. Cell Rep 5: 61–69. doi:10.1016/j.celrep.2013.08.042
9. Spires-Jones TL, Hyman BT (2014) The intersection of amyloid beta and tau at synapses in Alzheimer’s disease. Neuron 82: 756–771. doi:10.1016/j.neuron.2014.05.004
10. Steiner H, Fluhrer R, Haass C (2008) Intramembrane proteolysis by gamma-secretase. J Biol Chem 283: 29627–29631. doi:10.1074/jbc.r800010200
11. Willem M, Lammich S, Haass C (2009) Function, regulation and therapeutic properties of beta-secretase (BACE1). Semin Cell Dev Biol 20: 175–182. doi:10.1016/j.semcdb.2009.01.003
12. Jan A, Hartley DM, Lashuel HA (2010) Preparation and characterization of toxic Abeta aggregates for structural and functional studies in Alzheimer’s disease research. Nat Protoc 5: 1186–1209. doi:10.1038/nprot.2010.72
13. Welander H, Franberg J, Graff C, Sundstrom E, Winblad B, Tjernberg LO (2009) Abeta43 is more frequent than Abeta40 in amyloid plaque cores from Alzheimer disease brains. J Neurochem 110: 697–706. doi:10.1111/j.1471-4159.2009.06170.x
14. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APPAbeta43 is more frequent than Abeta40 in amyloid plaque cores from Alzheimer disease brains. Nature 414: 643–648. doi:10.1038/414643a
15. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, Beyreuther K, Fischer P, Masters CL, Price DL (1990) Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci USA 87: 1561–1565. doi:10.1073/pnas.87.4.1561
16. Gouras GK, Tampellini D, Takahashi RH, Capetillo-Zarate E (2010) Intraneuronal beta-amyloid accumulation and synapse pathology in Alzheimer’s disease. Acta Neuropathol 119: 523–541. doi:10.1007/s00401-010-0679-9
17. Lundgren JL, Ahmed S, Schedin-Weiss S, Gouras GK, Winblad B, Tjernberg LO, Frykman S (2015) ADAM10 and BACE1 are localized to synaptic vesicles. J Neurochem 135: 606–615. doi:10.1111/jnc.13287
18. Schedin-Weiss S, Caesar I, Winblad B, Blom H, Tjernberg LO (2016) Super-resolution microscopy reveals gamma-secretase at both sides of the neuronal synapse. Acta Neuropathol Commun 4: 29. doi:10.1186/s40478-016-0296-5
19. Lundgren JL, Ahmed S, Winblad B, Gouras GK, Tjernberg LO, Frykman S (2014) Activity-independent release of the amyloid beta-peptide from rat brain nerve terminals. Neurosci Lett 566: 125–130. doi:10.1016/j.neulet.2014.02.050
20. Aoki M, Volkmann I, Tjernberg LO, Winblad B, Bogdanovic N (2008) Amyloid beta-peptide levels in laser capture microdissected cornu ammonis 1 pyramidal neurons of Alzheimer’s brain. Neuroreport 19: 1085–1089. doi:10.1097/wnr.0b013e328302c858
21. Hashimoto M, Bogdanovic N, Volkmann I, Aoki M, Winblad B, Tjernberg LO (2010) Analysis of microdissected human neurons by a sensitive ELISA reveals a correlation between elevated intracellular concentrations of Abeta42 and Alzheimer’s disease neuropathology. Acta Neuropathol 119: 543–554. doi:10.1007/s00401-010-0661-6
22. Scheff SW, Price DA (2003) Synaptic pathology in Alzheimer’s disease: A review of ultrastructural studies. Neurobiol Aging 24: 1029–1046. doi:10.1016/j.neurobiolaging.2003.08.002
23. Coleman PD, Yao PJ (2003) Synaptic slaughter in Alzheimer’s disease. Neurobiol Aging 24: 1023–1027. doi:10.1016/j.neurobiolaging.2003.09.001
24. Dani A, Huang B, Bergan J, Dulac C, Zhuang X (2010) Superresolution imaging of chemical synapses in the brain. Neuron 68: 843–856. doi:10.1016/j.neuron.2010.11.021
25. Naslund J, Haroutunian V, Mohs R, Davis KL, Davies P, Greengard P, Buxbaum JD (2000) Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283: 1571–1577. doi:10.1001/jama.283.12.1571
26. Philipson O, Lord A, Lalowski M, Soliymani R, Baumann M, Thyberg J, Bogdanovic N, Olofsson T, Tjernberg LO, Ingelsson M, et al (2012) The arctic amyloid-beta precursor protein (AbetaPP) mutation results in distinct plaques and accumulation of N- and C-truncated Abeta. Neurobiol Aging 33: 1010.e1–1010.e13. doi:10.1016/j.neurobiolaging.2011.10.022
27. Schedin-Weiss S, Inoue M, Hromadkova L, Teranishi Y, Yamamoto NG, Wiehager B, Bogdanovic N, Winblad B, Sandebring-Matton A, Frykman S, et al (2017) Monoamine oxidase B is elevated in Alzheimer disease neurons, is associated with gamma-secretase and regulates neuronal amyloid beta-peptide levels. Alzheimers Res Ther 9: 57. doi:10.1186/s13195-017-0279-1
28. Imig C, Min SW, Krinner S, Arancillo M, Rosenmund C, Sudhof TC, Rhee J, Brose N, Cooper BH (2014) The morphological and molecular nature of synaptic vesicle priming at presynaptic active zones. Neuron 84: 416–431. doi:10.1016/j.neuron.2014.10.009
29. Yu WH, Cuervo AM, Kumar A, Peterhoff CM, Schmidt SD, Lee JH, Mohan PS, Mercken M, Farmery MR, Tjernberg LO, et al (2005) Macroautophagy: A novel Beta-amyloid peptide-generating pathway activated in Alzheimer’s disease. J Cell Biol 171: 87–98. doi:10.1083/jcb.200505082
30. Sahl SJ, Hell SW, Jakobs S (2017) Fluorescence nanoscopy in cell biology. Nat Rev Mol Cell Biol 18: 685–701. doi:10.1038/nrm.2017.71
31. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3: 793–795. doi:10.1038/nmeth929
32. Heilemann M, van de Linde S, Schuttpelz M, Kasper R, Seefeldt B, Mukherjee A, Tinnefeld P, Sauer M (2008) Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angewandte Chemie 47: 6172–6176. doi:10.1002/anie.200802376
33. Folling J, Bossi M, Bock H, Medda R, Wurm CA, Hein B, Jakobs S, Eggeling C, Hell SW (2008) Fluorescence nanoscopy by ground-state depletion and single-molecule return. Nat Methods 5: 943–945. doi:10.1038/nmeth.1257
34. Fath T, Ke YD, Gunning P, Gotz J, Ittner LM (2009) Primary support cultures of hippocampal and substantia nigra neurons. Nat Protoc 4: 78–85. doi:10.1038/nprot.2008.199
35. Schedin-Weiss S, Inoue M, Teranishi Y, Yamamoto NG, Karlstrom H, Winblad B, Tjernberg LO (2013) Visualizing active enzyme complexes using a photoreactive inhibitor for proximity ligation: Application on gamma-secretase. PLoS One 8: e63962. doi:10.1371/journal.pone.0063962
36. Dempsey GT, Vaughan JC, Chen KH, Bates M, Zhuang X (2011) Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat Methods 8: 1027–1036. doi:10.1038/nmeth.1768
37. Tokunaga M, Imamoto N, Sakata-Sogawa K (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 5: 159–161. doi:10.1038/nmeth1171
38. Bernhem K, Brismar H (2018) SMLocalizer, a GPU accelerated ImageJ plugin for single molecule localization microscopy. Bioinformatics 34: 137–138. doi:10.1093/bioinformatics/btx553