Multiplex assay for live-cell monitoring of cellular fates of amyloid-β precursor protein (APP)

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Merezhko, Maria ^a   Muggalla, Pranuthi ^a   Nykänen, Niko Petteri ^a   Yan, Xu ^a   Sakha, Prasanna ^a   Huttunen, Henri J ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE 1; ASPARTIC PROTEINASE; BACE1 PROTEIN, MOUSE; CULTURE MEDIUM; PEPTIDE FRAGMENT; PROTEIN BINDING; SECRETASE;

ANIMAL CELL; ARTICLE; BIOLOGICAL MONITORING; CELL ASSAY; CELL FATE; CELL ISOLATION; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; EXOSOME; MOUSE; MULTIPLEX ASSAY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; ANIMAL; CELL LINE; CHEMISTRY; CULTURE MEDIUM; HALF LIFE TIME; HIGH THROUGHPUT SCREENING; METABOLISM; PROCEDURES; SECRETION (PROCESS);

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CELL LINE; CULTURE MEDIA, CONDITIONED; EXOSOMES; HALF-LIFE; HIGH-THROUGHPUT SCREENING ASSAYS; MICE; PEPTIDE FRAGMENTS; PROTEIN BINDING;

EID: 84903289396     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098619     Document Type: Article

References (63)

1. De Strooper B, Annaert W (2000) Proteolytic processing and cell biological functions of the amyloid precursor protein. J Cell Sci 113: 1857-1870. (Pubitemid 30386490)
2. Muller UC, Zheng H (2012) Physiological functions of APP family proteins. Cold Spring Harb Perspect Med 2: a006288.
3. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120: 885-890. (Pubitemid 14104991)
4. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R et al. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539. (Pubitemid 34288854)
5. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D et al. (2003) APP processing and synaptic function. Neuron 37: 925-937. (Pubitemid 36398299)
6. Gandy S (2005) The role of cerebral amyloid beta accumulation in common forms of Alzheimer disease. J Clin Invest 115: 1121-1129.
7. Vetrivel KS, Thinakaran G (2006) Amyloidogenic processing of beta-amyloid precursor protein in intracellular compartments. Neurology 66: S69-73. (Pubitemid 43739988)
8. Kimberly WT, Zheng JB, Guenette SY, Selkoe DJ (2001) The Intracellular Domain of the beta -Amyloid Precursor Protein Is Stabilized by Fe65 and Translocates to the Nucleus in a Notch-like Manner. J Biol Chem 276: 40288-40292.
9. Liu Q, Zerbinatti CV, Zhang J, Hoe HS, Wang B et al. (2007) Amyloid precursor protein regulates brain apolipoprotein E and cholesterol metabolism through lipoprotein receptor LRP1. Neuron 56: 66-78. (Pubitemid 47484175)
10. Ring S, Weyer SW, Kilian SB, Waldron E, Pietrzik CU 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. (Pubitemid 47093823)
11. Wang W, Mutka AL, Zmrzljak UP, Rozman D, Tanila H et al. (2014) Amyloid precursor protein alpha- and beta-cleaved ectodomains exert opposing control of cholesterol homeostasis via SREBP2. FASEB J 28: 849-860.
12. Gervais FG, Xu D, Robertson GS, Vaillancourt JP, Zhu Y et al. (1999) Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid- beta precursor protein and amyloidogenic A beta peptide formation. Cell 97: 395-406.
13. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457: 981-989.
14. Huttunen HJ, Puglielli L, Ellis BC, Mackenzie Ingano LA, Kovacs DM (2009) Novel N-terminal Cleavage of APP Precludes Abeta Generation in ACAT-Defective AC29 Cells. J Mol Neurosci 37: 6-15.
15. Vella LJ, Cappai R (2012) Identification of a novel amyloid precursor protein processing pathway that generates secreted N-terminal fragments. FASEB J 26: 2930-2940.
16. Weidemann A, Konig G, Bunke D, Fischer P, Salbaum JM et al. (1989) Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57: 115-126. (Pubitemid 19098873)
17. Huttunen HJ, Peach C, Bhattacharyya R, Barren C, Pettingell W et al. (2009) Inhibition of acyl-coenzyme A: cholesterol acyl transferase modulates amyloid precursor protein trafficking in the early secretory pathway. FASEB J 23: 3819-3828.
18. Thinakaran G, Koo EH (2008) Amyloid precursor protein trafficking, processing, and function. J Biol Chem 283: 29615-29619.
19. Koo EH, Squazzo SL (1994) Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem 269: 17386-17389. (Pubitemid 24218009)
20. Perez RG, Soriano S, Hayes JD, Ostaszewski B, Xia W et al. (1999) Mutagenesis identifies new signals for beta-amyloid precursor protein endocytosis, turnover, and the generation of secreted fragments, including Abeta42. J Biol Chem 274: 18851-18856.
21. Grbovic OM, Mathews PM, Jiang Y, Schmidt SD, Dinakar R et al. (2003) Rab5-stimulated up-regulation of the endocytic pathway increases intracellular beta-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Abeta production. J Biol Chem 278: 31261-31268. (Pubitemid 36994643)
22. Small SA, Gandy S (2006) Sorting through the cell biology of Alzheimer's disease: intracellular pathways to pathogenesis. Neuron 52: 15-31. (Pubitemid 44466354)
23. Gabuzda D, Busciglio J, Chen LB, Matsudaira P, Yankner BA (1994) Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative. J Biol Chem 269: 13623-13628. (Pubitemid 24206141)
24. Buxbaum JD, Ruefli AA, Parker CA, Cypess AM, Greengard P (1994) Calcium regulates processing of the Alzheimer amyloid protein precursor in a protein kinase C-independent manner. Proc Natl Acad Sci U S A 91: 4489-4493. (Pubitemid 24143459)
25. Bodovitz S, Klein WL (1996) Cholesterol modulates alpha-secretase cleavage of amyloid precursor protein. J Biol Chem 271: 4436-4440.
26. Domingues SC, Henriques AG, Wu W, Da Cruz e Silva EF, Da Cruz e Silva OA (2007) Altered subcellular distribution of the Alzheimer's amyloid precursor protein under stress conditions. Ann N Y Acad Sci 1096: 184-195. (Pubitemid 47092512)
27. Yang Y, Wu Y, Zhang S, Song W (2013) High Glucose Promotes Abeta Production by Inhibiting APP Degradation. PLoS One 8: e69824.
28. Perreau VM, Orchard S, Adlard PA, Bellingham SA, Cappai R et al. (2010) A domain level interaction network of amyloid precursor protein and Abeta of Alzheimer's disease. Proteomics 10: 2377-2395.
29. Barrett PJ, Song Y, Van Horn WD, Hustedt EJ, Schafer JM et al. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol. Science 336: 1168-1171.
30. Hicks DA, Nalivaeva NN, Turner AJ (2012) Lipid rafts and Alzheimer's disease: protein-lipid interactions and perturbation of signaling. Front Physiol 3: 189.
31. Bai Y, Markham K, Chen F, Weerasekera R, Watts J et al. (2008) The in vivo brain interactome of the amyloid precursor protein. Mol Cell Proteomics 7: 15-34. (Pubitemid 351255432)
32. Kohli BM, Pflieger D, Mueller LN, Carbonetti G, Aebersold R et al. (2012) Interactome of the amyloid precursor protein APP in brain reveals a protein network involved in synaptic vesicle turnover and a close association with Synaptotagmin-1. J Proteome Res 11: 4075-4090.
33. Kinoshita A, Fukumoto H, Shah T, Whelan CM, Irizarry MC et al. (2003) Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes. J Cell Sci 116: 3339-3346. (Pubitemid 37038982)
34. Thomas AV, Berezovska O, Hyman BT, von Arnim CA (2008) Visualizing interaction of proteins relevant to Alzheimer's disease in intact cells. Methods 44: 299-303. (Pubitemid 351406504)
35. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA et al. (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286: 735-741.
36. Remy I, Michnick SW (2006) A highly sensitive protein-protein interaction assay based on Gaussia luciferase. Nat Methods 3: 977-979. (Pubitemid 44782695)
37. Lichtenthaler SF, Dominguez DI, Westmeyer GG, Reiss K, Haass C et al. (2003) The cell adhesion protein P-selectin glycoprotein ligand-1 is a substrate for the aspartyl protease BACE1. J Biol Chem 278: 48713-48719. (Pubitemid 41079512)
38. Tesco G, Koh YH, Kang EL, Cameron AN, Das S et al. (2007) Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 54: 721-737. (Pubitemid 46843521)
39. Small SA, Kent K, Pierce A, Leung C, Kang MS et al. (2005) Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann Neurol 58: 909-919. (Pubitemid 41746881)
40. Haass C, Hung AY, Selkoe DJ, Teplow DB (1994) Mutations associated with a locus for familial Alzheimer's disease result in alternative processing of amyloid β-protein precursor. J Biol Chem 269: 17741-17748.
41. Prabhu Y, Burgos PV, Schindler C, Farias GG, Magadan JG et al. (2012) Adaptor protein 2-mediated endocytosis of the beta-secretase BACE1 is dispensable for amyloid precursor protein processing. Mol Biol Cell 23: 2339-2351.
42. Kouchi Z, Kinouchi T, Sorimachi H, Ishiura S, Suzuki K (1998) The deletion of the C-terminal tail and addition of an endoplasmic reticulum targeting signal to Alzheimer's amyloid precursor protein change its localization, secretion, and intracellular proteolysis. Eur J Biochem 258: 291-300. (Pubitemid 28557892)
43. Nordstedt C, Caporaso GL, Thyberg J, Gandy SE, Greengard P (1993) Identification of the Alzheimer beta/A4 amyloid precursor protein in clathrin-coated vesicles purified from PC12 cells. J Biol Chem 268: 608-612. (Pubitemid 23021365)
44. Koo EH, Squazzo SL, Selkoe DJ, Koo CH (1996) Trafficking Of Cell-Surface Amyloid β-Protein Precursor.1. Secretion, Endocytosis And Recycling As Detected By Labeled Monoclonal Antibody. JCell Science 109: 991-998.
45. Ehehalt R, Keller P, Haass C, Thiele C, Simons K (2003) Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J Cell Biol 160: 113-123. (Pubitemid 36091721)
46. Carey RM, Balcz BA, Lopez-Coviella I, Slack BE (2005) Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid beta protein. BMC Cell Biol 6: 30.
47. Hill TA, Gordon CP, McGeachie AB, Venn-Brown B, Odell LR et al. (2009) Inhibition of dynamin mediated endocytosis by the dynoles-synthesis and functional activity of a family of indoles. J Med Chem 52: 3762-3773.
48. Perez-Gonzalez R, Gauthier SA, Kumar A, Levy E (2012) The exosome secretory pathway transports amyloid precursor protein carboxyl-terminal fragments from the cell into the brain extracellular space. J Biol Chem 287: 43108-43115.
49. Yuyama K, Sun H, Mitsutake S, Igarashi Y (2012) Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J Biol Chem 287: 10977-10989.
50. Thery C, Amigorena S, Raposo G, Clayton A (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 3: Unit 3.22.
51. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D et al. (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244-1247. (Pubitemid 351323020)
52. von Arnim CA, Spoelgen R, Peltan ID, Deng M, Courchesne S et al. (2006) GGA1 acts as a spatial switch altering amyloid precursor protein trafficking and processing. J Neurosci 26: 9913-9922. (Pubitemid 44477153)
53. Sittampalam GS, Neely G-E, Arkin M, Auld D, Austin C et al. (editors) (2004) Assay Guidance Manual. Eli Lilly & Company and the National Center for Advancing Translational Sciences. Available from: http://www.ncbi.nlm.nih. gov/books/NBK53196/. Accessed 2010 Mar 1.
54. Dovey HF, John V, Anderson JP, Chen LZ, de Saint Andrieu P et al. (2001) Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J Neurochem 76: 173-181. (Pubitemid 32044380)
55. Knops J, Suomensaari S, Lee M, McConlogue L, Seubert P et al. (1995) Cell-type and amyloid precursor protein-type specific inhibition of A beta release by bafilomycin A1, a selective inhibitor of vacuolar ATPases. J Biol Chem 270: 2419-2422.
56. Savina A, Furlan M, Vidal M, Colombo MI (2003) Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem 278: 20083-20090. (Pubitemid 36799202)
57. Milhas D, Clarke CJ, Hannun YA (2010) Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett 584: 1887-1894.
58. Puglielli L, Ellis BC, Saunders AJ, Kovacs DM (2003) Ceramide stabilizes beta-site amyloid precursor protein-cleaving enzyme 1 and promotes amyloid beta-peptide biogenesis. J Biol Chem 278: 19777-19783. (Pubitemid 36799164)
59. Lin X, Koelsch G, Wu S, Downs D, Dashti A et al. (2000) Human aspartic protease memapsin 2 cleaves the beta-secretase site of beta-amyloid precursor protein. Proc Natl Acad Sci U S A 97: 1456-1460. (Pubitemid 30118462)
60. Kyriazis GA, Wei Z, Vandermey M, Jo DG, Xin O et al. (2008) Numb endocytic adapter proteins regulate the transport and processing of the amyloid precursor protein in an isoform-dependent manner: implications for Alzheimer disease pathogenesis. J Biol Chem 283: 25492-25502.
61. Wen L, Tang FL, Hong Y, Luo SW, Wang CL et al. (2011) VPS35 haploinsufficiency increases Alzheimer's disease neuropathology. J Cell Biol 195: 765-779.
62. Sullivan CP, Jay AG, Stack EC, Pakaluk M, Wadlinger E et al. (2011) Retromer disruption promotes amyloidogenic APP processing. Neurobiol Dis 43: 338-345.
63. Sharples RA, Vella LJ, Nisbet RM, Naylor R, Perez K et al. (2008) Inhibition of gamma-secretase causes increased secretion of amyloid precursor protein C-terminal fragments in association with exosomes. FASEB J 22: 1469-1478. (Pubitemid 351656787)