Visualization and Quantification of APP Intracellular Domain-Mediated Nuclear Signaling by Bimolecular Fluorescence Complementation

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Riese, Florian ^a   Grinschgl, Sonja ^a   Gersbacher, Manuel T ^a   Russi, Natalie ^a   Hock, Christoph ^a   Nitsch, Roger M ^a   Konietzko, Uwe ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; HISTONE ACETYLTRANSFERASE; HYBRID PROTEIN; PHENYLALANINE; TYROSINE;

ALZHEIMER DISEASE; ARTICLE; CELL CULTURE; CELL DEATH; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; FLUORESCENCE IMAGING; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; OXIDATIVE STRESS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION;

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; CELL NUCLEUS; FLOW CYTOMETRY; FLUORESCENCE; GENE EXPRESSION REGULATION; HISTONE ACETYLTRANSFERASES; HUMANS; MICROSCOPY, CONFOCAL; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OXIDATIVE STRESS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION;

EID: 84884537710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076094     Document Type: Article

References (46)

1. Hardy JA, Higgins GA, (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-185. doi:10.1126/science.1566067. PubMed: 1566067.
2. Benilova I, Karran E, de Strooper B, (2012) The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci 15: 349-357. doi:10.1038/nn.3028. PubMed: 22286176.
3. Huang Y, Mucke L, (2012) Alzheimer Mechanisms and Therapeutic Strategies. Cell 148: 1204-1222. doi:10.1016/j.cell.2012.02.040. PubMed: 22424230.
4. Hardy J, Selkoe DJ, (2002) The Amyloid Hypothesis of Alzheimer's Disease: Progress and Problems on the Road to Therapeutics. Science, 297: 353-6. PubMed: 12130773.
5. Fraering PC, Ye W, Strub JM, Dolios G, LaVoie MJ, et al. (2004) Purification and characterization of the human gamma-secretase complex. Biochemistry 43: 9774-9789. doi:10.1021/bi0494976. PubMed: 15274632.
6. Cao X, Südhof TC, (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293: 115-120. doi:10.1126/science.1058783. PubMed: 11441186.
7. Rotz, von RC, Kohli BM, Bosset J, Meier M, Suzuki T, et al. (2004) The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J Cell Sci 117: 4435-4448. doi:10.1242/jcs.01323. PubMed: 15331662.
8. Konietzko U, Goodger ZV, Meyer M, Kohli BM, Bosset J, et al. (2010) Co-localization of the amyloid precursor protein and Notch intracellular domains in nuclear transcription factories. Neurobiol Aging 31: 58-73. doi:10.1016/j.neurobiolaging.2008.03.001. PubMed: 18403052.
9. Gersbacher MT, Goodger ZV, Trutzel A, Bundschuh D, Nitsch RM, et al. (2013) Turnover of amyloid precursor protein family members determines their nuclear signaling capability. PLOS ONE 8: e69363. doi:10.1371/journal.pone.0069363. PubMed: 23874953.
10. Goodger ZV, Rajendran L, Trutzel A, Kohli BM, Nitsch RM, et al. (2009) Nuclear signaling by the APP intracellular domain occurs predominantly through the amyloidogenic processing pathway. J Cell Sci 122: 3703-3714. doi:10.1242/jcs.048090. PubMed: 19773363.
11. Haass C, Lemere CA, Capell A, Citron M, Seubert P, et al. (1995) The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat Med 1: 1291-1296. doi:10.1038/nm1295-1291. PubMed: 7489411.
12. Shen J, Kelleher RJ, (2007) The presenilin hypothesis of Alzheimer's disease: evidence for a loss-of-function pathogenic mechanism. Proc Natl Acad Sci U S A 104: 403-409. doi:10.1073/pnas.0608332104. PubMed: 17197420.
13. Cacquevel M, Aeschbach L, Houacine J, Fraering PC, (2012) Alzheimer's Disease-Linked Mutations in Presenilin-1 Result in a Drastic Loss of Activity in Purified γ-Secretase Complexes. PLOS ONE 7: e35133. doi:10.1371/journal.pone.0035133.g005. PubMed: 22529981.
14. Chavez-Gutierrez L, Bammens L, Benilova I, Vandersteen A, Benurwar M, et al. (2012) The mechanism of gamma-Secretase dysfunction in familial Alzheimer disease. EMBO J: pp. 1-14. doi:10.1038/emboj.2012.79.
15. Konietzko U, (2012) AICD nuclear signaling and its possible contribution to Alzheimer's disease. Curr Alzheimer Res 9: 200-216. doi:10.2174/156720512799361673. PubMed: 21605035.
16. Kerppola TK, (2006) Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat Protoc 1: 1278-1286. doi:10.1038/nprot.2006.201. PubMed: 17406412.
17. Ventura S, (2011) Bimolecular fluorescence complementation: illuminating cellular protein interactions. Curr Mol Med 11: 582-598. doi:10.2174/156652411800615117. PubMed: 21707513.
18. Kodama Y, Hu C-D, (2012) Bimolecular fluorescence complementation (BiFC): a 5-year update and future perspectives. BioTechniques 53: 285-298. doi:10.2144/000113943. PubMed: 23148879.
19. Morell M, Espargaro A, Aviles FX, Ventura S, (2008) Study and selection of in vivo protein interactions by coupling bimolecular fluorescence complementation and flow cytometry. Nat Protoc 3: 22-33. doi:10.1038/nprot.2007.496. PubMed: 18193018.
20. Gonçalves SA, Matos JE, Outeiro TF, (2010) Zooming into protein oligomerization in neurodegeneration using BiFC. Trends Biochem Sci 35: 643-651. doi:10.1016/j.tibs.2010.05.007. PubMed: 20561791.
21. Outeiro TF, Putcha P, Tetzlaff JE, Spoelgen R, Koker M, et al. (2008) Formation of toxic oligomeric alpha-synuclein species in living cells. PLOS ONE 3: e1867. doi:10.1371/journal.pone.0001867. PubMed: 18382657.
22. Tetzlaff JE, Putcha P, Outeiro TF, Ivanov A, Berezovska O, et al. (2008) CHIP targets toxic alpha-Synuclein oligomers for degradation. J Biol Chem 283: 17962-17968. doi:10.1074/jbc.M802283200. PubMed: 18436529.
23. Isbert S, Wagner K, Eggert S, Schweitzer A, Multhaup G, et al. (2011) APP dimer formation is initiated in the endoplasmic reticulum and differs between APP isoforms. Cell Mol Life Sci 69: 1353-1375. doi:10.1007/s00018-011-0882-4. PubMed: 22105709.
24. Ben Khalifa N, Tyteca D, Marinangeli C, Depuydt M, Collet JF, et al. (2012) Structural features of the KPI domain control APP dimerization, trafficking, and processing. FASEB J 26: 855-867. doi:10.1096/fj.11-190207. PubMed: 22085646.
25. So PP, Khodr CE, Chen C-D, Abraham CR, (2013) Comparable dimerization found in wildtype and familial Alzheimer's disease amyloid precursor protein mutants. Am J Neurodegener Dis 2: 15-28 PubMed: 23515184.
26. Chen C-D, Oh S-Y, Hinman JD, Abraham CR, (2006) Visualization of APP dimerization and APP-Notch2 heterodimerization in living cells using bimolecular fluorescence complementation. J Neurochem 97: 30-43. doi:10.1111/j.1471-4159.2006.03705.x. PubMed: 16515557.
27. Oh S-Y, Chen C-D, Abraham CR, (2010) Cell-type dependent modulation of Notch signaling by the amyloid precursor protein. J Neurochem 113: 262-274. doi:10.1111/j.1471-4159.2010.06603.x. PubMed: 20089128.
28. Weyer SW, Klevanski M, Delekate A, Voikar V, (2011) APP and APLP2 are essential at PNS and CNS synapses for transmission, spatial learning and LTP: Article: The EMBO Journal. The EMBO.
29. Waldron E, Heilig C, Schweitzer A, Nadella N, Jaeger S, et al. (2008) LRP1 modulates APP trafficking along early compartments of the secretory pathway. Neurobiol Dis 31: 188-197. doi:10.1016/j.nbd.2008.04.006. PubMed: 18559293.
30. Hu C-D, Chinenov Y, Kerppola TK, (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol Cell 9: 789-798. doi:10.1016/S1097-2765(02)00496-3. PubMed: 11983170.
31. Kohli BM, Pflieger D, Mueller LN, Carbonetti G, Aebersold R, et al. (2012) The interactome of the amyloid precursor protein APP in brain reveals a protein network involved in synaptic vesicle turnover and a close association with synaptotagmin1. J Proteome Res. doi:10.1021/pr300123g.
32. Mullan M, Crawford F, Axelman K, Houlden H, Lilius L, et al. (1992) A pathogenic mutation for probable Alzheimer's disease in the APP gene at the N-terminus of beta-amyloid. Nat Genet 1: 345-347. doi:10.1038/ng0892-345. PubMed: 1302033.
33. Banning C, Votteler J, Hoffmann D, Koppensteiner H, Warmer M, et al. (2010) A flow cytometry-based FRET assay to identify and analyse protein-protein interactions in living cells. PLOS ONE 5: e9344. doi:10.1371/journal.pone.0009344. PubMed: 20179761.
34. Tamayev R, Zhou D, D'Adamio L, (2009) The interactome of the amyloid beta precursor protein family members is shaped by phosphorylation of their intracellular domains. Mol Neurodegener 4: 28. doi:10.1186/1750-1326-4-28. PubMed: 19602287.
35. Pardossi-Piquard R, Checler F, (2011) The physiology of the β-amyloid precursor protein intracellular domain AICD. J Neurochem 120: 109-124. doi:10.1111/j.1471-4159.2011.07475.x. PubMed: 22122663.
36. Xu X, Zhou H, Boyer TG, (2011) Mediator is a transducer of amyloid-precursor-protein-dependent nuclear signalling. EMBO Rep, 12: 1-7. doi:10.1038/embor.2010.210. PubMed: 21293490.
37. Iborra FJ, Pombo A, Jackson DA, Cook PR, (1996) Active RNA polymerases are localized within discrete transcription "factories' in human nuclei. J Cell Sci 109(6):: 1427-1436. PubMed: 8799830.
38. Pombo A, Jackson DA, Hollinshead M, Wang Z, Roeder RG, et al. (1999) Regional specialization in human nuclei: visualization of discrete sites of transcription by RNA polymerase III. EMBO J 18: 2241-2253. doi:10.1093/emboj/18.8.2241. PubMed: 10205177.
39. Belyaev ND, Kellett KAB, Beckett C, Makova NZ, Revett TJ, et al. (2010) The transcriptionally active amyloid precursor protein (APP) intracellular domain is preferentially produced from the 695 isoform of APP in a {beta}-secretase-dependent pathway. J Biol Chem 285: 41443-41454. doi:10.1074/jbc.M110.141390. PubMed: 20961856.
40. Flammang B, Pardossi-Piquard R, Sevalle J, Debayle D, Dabert-Gay A-S, et al. (2012) Evidence that the amyloid-β protein precursor intracellular domain, AICD, derives from β-secretase-generated C-terminal fragment. J Alzheimers Dis 30: 145-153. doi:10.3233/JAD-2012-112186. PubMed: 22406447.
41. Tarr PE, Contursi C, Roncarati R, Noviello C, Ghersi E, et al. (2002) Evidence for a role of the nerve growth factor receptor TrkA in tyrosine phosphorylation and processing of beta-APP. Biochem Biophys Res Commun 295: 324-329. doi:10.1016/S0006-291X(02)00678-2. PubMed: 12150951.
42. Minopoli G, Passaro F, Aloia L, Carlomagno F, Melillo RM, et al. (2007) Receptor- and non-receptor tyrosine kinases induce processing of the amyloid precursor protein: role of the low-density lipoprotein receptor-related protein. Neurodegener Dis 4: 94-100. doi:10.1159/000101833. PubMed: 17596703.
43. Zambrano N, Bruni P, Minopoli G, Mosca R, Molino D, et al. (2001) The beta-amyloid precursor protein APP is tyrosine-phosphorylated in cells expressing a constitutively active form of the Abl protoncogene. J Biol Chem 276: 19787-19792. doi:10.1074/jbc.M100792200. PubMed: 11279131.
44. Zhou D, Zambrano N, Russo T, D'Adamio L, (2009) Phosphorylation of a tyrosine in the amyloid-beta protein precursor intracellular domain inhibits Fe65 binding and signaling. J Alzheimers Dis 16: 301-307. doi:10.3233/JAD-2009-0970. PubMed: 19221419.
45. Matrone C, Barbagallo APM, La Rosa LR, Florenzano F, Ciotti MT, et al. (2011) APP is phosphorylated by TrkA and regulates NGF/TrkA signaling. J Neurosci 31: 11756-11761. doi:10.1523/JNEUROSCI.1960-11.2011. PubMed: 21849536.
46. Butterfield DA, Drake J, Pocernich C, Castegna A, (2001) Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol Med 7: 548-554. doi:10.1016/S1471-4914(01)02173-6. PubMed: 11733217.