The Amyloid Precursor Protein—A Novel Player within the Molecular Array of Presynaptic Nanomachines

Frontiers in Synaptic Neuroscience

Volumn 7, Issue , 2016, Pages

  Laßek, Melanie ^a   Weingarten, Jens ^a   Wegner, Martin ^a   Volknandt, Walter ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Alzheimer s disease; amyloid precursor protein; calcium homeostasis; mitochondria; presynaptic active zone

Indexed keywords

EID: 85011009234     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2015.00021     Document Type: Review

References (59)

1. Abrahamsson T. Gustafsson B. Hanse E. (2007). Reversible synaptic depression in developing rat CA3 CA1 synapses explained by a novel cycle of AMPA silencing-unsilencing. J. Neurophysiol. 98, 2604–2611. 10.1152/jn.00602.200717804578
2. Bezprozvanny I. Mattson M. P. (2008). Neuronal calcium mishandling and the pathogenesis of Alzheimer’s disease. Trends Neurosci. 31, 454–463. 10.1016/j.tins.2008.06.00518675468
3. Burré J. Sharma M. Tsetsenis T. Buchman V. Etherton M. R. Südhof T. C. (2010). Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329, 1663–1667. 10.1126/science.119522720798282
4. Deák F. Xu Y. Chang W.-P. Dulubova I. Khvotchev M. Liu X. et al. (2009). Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J. Cell Biol. 184, 751–764. 10.1083/jcb.200812026
5. Doert A. Pilatus U. Zanella F. Müller W. E. Eckert G. P. (2015). 1H- and 13C-NMR spectroscopy of Thy-1-APPSL mice brain extracts indicates metabolic changes in Alzheimer’s disease. J. Neural. Transm. (Vienna). 122, 541–550. 10.1007/s00702-015-1387-325742870
6. Drexler K. E. (1987). Engines of Creation: The Coming Era of Nanotechnology. New York, NY: Anchor Press.
7. Eckert A. Keil U. Marques C. A. Bonert A. Frey C. Schüssel K. et al. (2003). Mitochondrial dysfunction, apoptotic cell death and Alzheimer’s disease. Biochem. Pharmacol. 66, 1627–1634. 10.1016/s0006-2952(03)00534-314555243
8. Eckert G. P. Renner K. Eckert S. H. Eckmann J. Hagl S. Abdel-Kader R. M. et al. (2012). Mitochondrial dysfunction—a pharmacological target in Alzheimer’s disease. Mol. Neurobiol. 46, 136–150. 10.1007/s12035-012-8271-z22552779
9. Fanutza T. Del Prete D. Ford M. J. Castillo P. E. D’Adamio L. (2015). APP and APLP2 interact with the synaptic release machinery and facilitate transmitter release at hippocampal synapses. Elife [Epub ahead of print]. 10.7554/eLife.0974326551565
10. Fitzjohn S. M. Morton R. A. Kuenzi F. Davies C. H. Seabrook G. R. Collingridge G. L. (2000). Similar levels of long-term potentiation in amyloid precursor protein-null and wild-type mice in the CA1 region of picrotoxin treated slices. Neurosci. Lett. 288, 9–12. 10.1016/s0304-3940(00)01204-010869803
11. Glenner G. G. Wong C. W. (1984). Alzheimer’s disease and Down’s syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem. Biophys. Res. Commun. 122, 1131–1135. 10.1016/0006-291x(84)91209-96236805
12. Harper M. E. Bevilacqua L. Hagopian K. Weindruch R. Ramsey J. J. (2004). Ageing, oxidative stress and mitochondrial uncoupling. Acta Physiol. Scand. 182, 321–331. 10.1111/j.1365-201x.2004.01370.x15569093
13. Heber S. Herms J. Gajic V. Hainfellner J. Aguzzi A. Rülicke T. et al. (2000). Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J. Neurosci. 20, 7951–7963. 11050115
14. Hick M. Herrmann U. Weyer S. W. Mallm J. P. Tschäpe J. A. Borgers M. et al. (2015). Acute function of secreted amyloid precursor protein fragment APPsα in synaptic plasticity. Acta. Neuropathol. 129, 21–37. 10.1007/s00401-014-1368-x25432317
15. Hsieh H. Boehm J. Sato C. Iwatsubo T. Tomita T. Sisodia S. et al. (2006). AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52, 831–843. 10.1016/j.neuron.2006.10.03517145504
16. Kaido M. Fujimura H. Soga F. Toyooka K. Yoshikawa H. Nishimura T. et al. (1996). Alzheimer-type pathology in a patient with mitochondrial myopathy, encephalopathy, lactic acidosis and stroke-like episodes (MELAS). Acta. Neuropathol. 92, 312–318. 10.1007/s0040100505248870835
17. Kamenetz F. Tomita T. Hsieh H. Seabrook G. Borchelt D. Iwatsubo T. et al. (2003). APP processing and synaptic function. Neuron 37, 925–937. 10.1016/s0896-6273(03)00124-712670422
18. Kang J. Lemaire H. G. Unterbeck A. Salbaum J. M. Masters C. L. Grzeschik K. H. et al. (1987). The precursor of Alzheimer’s disease amyloid A4 protein resembles a cell-surface receptor. Nature 325, 733–736. 10.1038/325733a02881207
19. Khachaturian Z. S. (1987). Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neurobiol. Aging 8, 345–346. 10.1016/0197-4580(87)90073-x3627349
20. Korge P. Ping P. Weiss J. N. (2008). Reactive oxygen species production in energized cardiac mitochondria during hypoxia/reoxygenation: modulation by nitric oxide. Circ. Res. 103, 873–880. 10.1161/circresaha.108.18086918776040
21. Korte M. Herrmann U. Zhang X. Draguhn A. (2012). The role of APP and APLP for synaptic transmission, plasticity and network function. lessons from genetic mouse models. Exp. Brain Res. 217, 435–440. 10.1007/s00221-011-2894-622006270
22. Landfield P. W. (1987). ‘Increased calcium-current’ hypothesis of brain aging. Neurobiol. Aging 8, 346–347. 10.1016/0197-4580(87)90074-13627350
23. Landfield P. W. Campbell L. W. Hao S. Y. Kerr D. S. (1989). Aging-related increases in voltage-sensitive, inactivating calcium currents in rat hippocampus implications for mechanisms of brain aging and Alzheimer’s disease. Ann. N. Y. Acad. Sci. 568, 95–105. 10.1111/j.1749-6632.1989.tb12495.x2560904
24. Laßek M. Weingarten J. Acker-Palmer A. Bajjalieh S. M. Muller U. Volknandt W. (2014a). Amyloid precursor protein knockout diminishes synaptic vesicle proteins at the presynaptic active zone in mouse brain. Curr. Alzheimer. Res. 11, 971–980. 10.2174/156720501166614110715245825387333
25. Laßek M. Weingarten J. Volknandt W. (2014b). The proteome of the murine presynaptic active zone. Proteomes 2, 243–257. 10.3390/proteomes2020243
26. Laßek M. Weingarten J. Einsfelder U. Brendel P. Müller U. Volknandt W. (2013). Amyloid precursor proteins are constituents of the presynaptic active zone. J. Neurochem. 127, 48–56. 10.1111/jnc.1235823815291
27. Laßek M. Weingarten J. Volknandt W. (2015). The synaptic proteome. Cell Tissue Res 359, 255–265. 10.1007/s00441-014-1943-425038742
28. Leuner K. Kurz C. Guidetti G. Orgogozo J. M. Müller W. E. (2010). Improved mitochondrial function in brain aging and Alzheimer disease—the new mechanism of action of the old metabolic enhancer piracetam. Front. Neurosci. 4:44. 10.3389/fnins.2010.0004420877425
29. Leuner K. Müller W. E. Reichert A. S. (2012a). From mitochondrial dysfunction to amyloid beta formation. novel insights into the pathogenesis of Alzheimer’s disease. Mol. Neurobiol. 46, 186–193. 10.1007/s12035-012-8307-422833458
30. Leuner K. Schütt T. Kurz C. Eckert S. H. Schiller C. Occhipinti A. et al. (2012b). Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid. Redox Signal. 16, 1421–1433. 10.1089/ars.2011.417322229260
31. Littleton J. T. Barnard R. J. Titus S. A. Slind J. Chapman E. R. Ganetzky B. (2001). SNARE-complex disassembly by NSF follows synaptic-vesicle fusion. Proc. Natl. Acad. Sci U S A 98, 12233–12238. 10.1073/pnas.22145019811593041
32. Mamelak M. (2012). Sporadic Alzheimer’s disease: the starving brain. J. Alzheimers. Dis. 31, 459–474. 10.3233/JAD-2012-12037022571985
33. Mann E. O. Paulsen O. (2007). Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 30, 343–349. 10.1016/j.tins.2007.05.00317532059
34. Mattson M. P. (2007). Calcium and neurodegeneration. Aging Cell 6, 337–350. 10.1111/j.1474-9726.2007.00275.x17328689
35. Müller W. E. Eckert A. Kurz C. Eckert G. P. Leuner K. (2010). Mitochondrial dysfunction: common final pathway in brain aging and Alzheimer’s disease—therapeutic aspects. Mol. Neurobiol. 41, 159–171. 10.1007/s12035-010-8141-520461558
36. Murphy M. P. (2009). How mitochondria produce reactive oxygen species. Biochem. J. 417, 1–13. 10.1042/bj2008138619061483
37. Phinney A. L. Calhoun M. E. Wolfer D. P. Lipp H. P. Zheng H. Jucker M. (1999). No hippocampal neuron or synaptic bouton loss in learning-impaired aged beta-amyloid precursor protein-null mice. Neuroscience 90, 1207–1216. 10.1016/s0306-4522(98)00645-910338291
38. Poyton R. O. Ball K. A. Castello P. R. (2009). Mitochondrial generation of free radicals and hypoxic signaling. Trends Endocrinol. Metab. 20, 332–340. 10.1016/j.tem.2009.04.00119733481
39. Priller C. Bauer T. Mitteregger G. Krebs B. Kretzschmar H. A. Herms J. (2006). Synapse formation and function is modulated by the amyloid precursor protein. J. Neurosci. 26, 7212–7221. 10.1523/jneurosci.1450-06.200616822978
40. Rhein V. Song X. Wiesner A. Ittner L. M. Baysang G. Meier F. et al. (2009). Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer’s disease mice. Proc. Natl. Acad. Sci. U S A 106, 20057–20062. 10.1073/pnas.090552910619897719
41. Ring S. Weyer S. W. Kilian S. B. Waldron E. Pietrzik C. U. Filippov M. A. et al. (2007). The secreted beta-amyloid precursor protein ectodomain APPs alpha is sufficient to rescue the anatomical, behavioral and electrophysiological abnormalities of APP-deficient mice. J. Neurosci. 27, 7817–7826. 17634375
42. Robinson S. R. (2000). Neuronal expression of glutamine synthetase in Alzheimer’s disease indicates a profound impairment of metabolic interactions with astrocytes. Neurochem. Int. 36, 471–482. 10.1016/s0197-0186(99)00150-310733015
43. Small D. H. (2008). Network dysfunction in Alzheimer’s disease: Does synaptic scaling drive disease progression? Trends Mol. Med. 14, 103–108. 10.1016/j.molmed.200718262842
44. Small D. H. Gasperini R. Vincent A. J. Hung A. C. Foa L. (2009). The role of Abeta-induced calcium dysregulation in the pathogenesis of Alzheimer’s disease. J. Alzheimers Dis. 16, 225–233. 10.3233/JAD-2009-095119221414
45. Südhof T. C. (2012). The presynaptic active zone. Neuron 75, 11–25. 10.1016/j.neuron.2012.06.01222794257
46. Südhof T. C. (2013a). A molecular machine for neurotransmitter release: synaptotagmin and beyond. Nat. Med. 19, 1227–1231. 10.1038/nm.333824100992
47. Südhof T. C. (2013b). Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 80, 675–690. 10.1016/j.neuron.2013.10.02224183019
48. Südhof T. C. Rizo J. (2011). Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol. 3:a005637. 10.1002/cphy.c13002122026965
49. Thibault O. Hadley R. Landfield P. W. (2001). Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J. Neurosci. 21, 9744–9756. 11739583
50. Thibault O. Landfield P. W. (1996). Increase in single L-Type calcium channels in hippocampal neurons during aging. Science 272, 1017–1020. 10.1126/science.272.5264.10178638124
51. Valtorta F. Pennuto M. Bonanomi D. Benfenati F. (2004). Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? Bioessays 26, 445–453. 10.1002/bies.2001215057942
52. Wang P. Yang G. Mosier D. R. Chang P. Zaidi T. Gong Y. D. et al. (2005). Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J. Neurosci. 25, 1219–1225. 10.1523/jneurosci.4660-04.200515689559
53. Wang X. Su B. Lee H. Li X. Perry G. Smith M. A. et al. (2009a). Impaired balance of mitochondrial fission and fusion in Alzheimer’s disease. J. Neurosci. 29, 9090–9103. 10.1523/jneurosci.1357-09.2009
54. Wang Z. Wang B. Yang L. Guo Q. Aithmitti N. Songyang Z. et al. (2009b). Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J. Neurosci. 29, 10788–10801. 10.1523/jneurosci.2132-09.200919726636
55. Wasling P. Daborg J. Riebe I. Andersson M. Portelius E. Blennow K. et al. (2009). Synaptic retrogenesis and amyloid-beta in Alzheimer’s disease. J. Alzheimers Dis. 16, 1–14. 10.3233/JAD-2009-091819158416
56. Weingarten J. Laßek M. Mueller B. Rohmer M. Baeumlisberger D. Beckert B. et al. (2015). Regional specializations of the PAZ proteomes derived from mouse hippocampus, olfactory bulb and cerebellum. Proteomes 3, 74–88. 10.3390/proteomes3020074
57. Weingarten J. Lassek M. Mueller B. F. Rohmer M. Lunger I. Baeumlisberger D. et al. (2014). The proteome of the presynaptic active zone from mouse brain. Mol. Cell. Neurosci. 59C, 106–118. 10.1016/j.mcn.2014.02.00324534009
58. Weyer S. W. Klevanski M. Delekate A. Voikar V. Aydin D. Hick M. et al. (2011). APP and APLP2 are essential at PNS and CNS synapses for transmission, spatial learning and LTP. EMBO J. 30, 2266–2280. 10.1038/emboj.2011.11921522131
59. Yang L. Wang Z. Wang B. Justice N. J. Zheng H. (2009). Amyloid precursor protein regulates Cav1.2 L-type calcium channel levels and function to influence GABAergic short-term plasticity. J. Neurosci. 29, 15660–15668. 10.1523/jneurosci.4104-09.200920016080