Amyloid precursor protein dimerization and synaptogenic function depend on copper binding to the growth factor-like domain

Journal of Neuroscience

Volumn 34, Issue 33, 2014, Pages 11159-11172

  Baumkötter, Frederik ^a   Schmidt, Nadine ^a   Vargas, Carolyn ^a   Schilling, Sandra ^a   Weber, Rebecca ^a   Wagner, Katja ^a   Fiedler, Sebastian ^a   Klug, Wilfried ^b   Radzimanowski, Jens ^c   Nickolaus, Sebastian ^a   Keller, Sandro ^a   Eggert, Simone ^a   Wild, Klemens ^b   Kins, Stefan ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIV GRENOBLE ALPES   (France)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Copper; Dimerization; Metal homeostasis; Synaptogenesis

Indexed keywords

AMYLOID PRECURSOR PROTEIN; COPPER; GROWTH FACTOR; NEUROLIGIN 1; SYNAPTOPHYSIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BINDING AFFINITY; BINDING SITE; CELL VIABILITY; CIRCULAR DICHROISM; COCULTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CULTURE MEDIUM; DIMERIZATION; GENE MUTATION; GENETIC TRANSFECTION; GUINEA PIG; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; ISOTHERMAL TITRATION CALORIMETRY; METAL BINDING; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN PURIFICATION; SYNAPTOGENESIS; WESTERN BLOTTING; X RAY CRYSTALLOGRAPHY; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

AMYLOID BETA-PROTEIN PRECURSOR; BINDING SITES; COPPER; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; NEURONS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

EID: 84905851549     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0180-14.2014     Document Type: Article

References (61)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213-221. CrossRef Medline
2. Altan-Bonnet N, Sougrat R, Liu W, Snapp EL, Ward T, Lippincott-Schwartz J (2006) Golgi inheritance in mammalian cells is mediated through endoplasmic reticulum export activities. Mol Biol Cell 17:990-1005. CrossRef Medline
3. Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P (2010) Affinity gradients drive copper to cellular destinations. Nature 465:645-648. CrossRef Medline
4. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67:271-281. CrossRef Medline
5. Baumgartner W, Hinterdorfer P, Ness W, Raab A, Vestweber D, Schindler H, Drenckhahn D (2000) Cadherin interaction probed by atomic force microscopy. Proc Natl Acad Sci U S A 97:4005-4010. CrossRef Medline
6. Baumkötter F, Wagner K, Eggert S, Wild K, Kins S (2012) Structural aspects and physiological consequences of APP/APLP trans-dimerization. Exp Brain Res 217:389-395. CrossRef Medline
7. Bayer TA, Schäfer S, Breyhan H, Wirths O, Treiber C, Multhaup G (2006) A vicious circle: role of oxidative stress, intraneuronal Abeta and Cu in Alzheimer's disease. Clin Neuropathol 25:163-171. Medline
8. Biederer T, Scheiffele P (2007) Mixed-culture assays for analyzing neuronal synapse formation. Nat Protoc 2:670-676. CrossRef Medline
9. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232. CrossRef Medline
10. Bush AI, Multhaup G, Moir RD, Williamson TG, Small DH, Rumble B, Pollwein P, Beyreuther K, Masters CL (1993) A novel zinc(II) binding site modulates the function of the beta A4 amyloid protein precursor of Alzheimer's disease. J Biol Chem 268:16109-16112. Medline
11. Chappuis-Flament S, Wong E, Hicks LD, Kay CM, Gumbiner BM (2001) Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J Cell Biol 154:231-243. CrossRef Medline
12. Chavda AP, Prole DL, Taylor CW (2013) A bead aggregation assay for detection of low-affinity protein-protein interactions reveals interactions between N-terminal domains of inositol 1,4,5-trisphosphate receptors. PLoS One 8:e60609. CrossRef Medline
13. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010) MolProbity: allatom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12-21. CrossRef Medline
14. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50:760-763.
15. Dahms SO, Hoefgen S, Roeser D, Schlott B, Guhrs KH, Than ME (2010) Structure and biochemical analysis of the heparin-induced E1 dimer of the amyloid precursor protein. Proc Natl Acad Sci U S A 107:5381-5386. CrossRef Medline
16. Dahms SO, Könnig I, Roeser D, Guhrs KH, Mayer MC, Kaden D, Multhaup G, Than ME (2012) Metal binding dictates conformation and function of the amyloid precursor protein (APP) E2 domain. J Mol Biol 416:438-452. CrossRef Medline
17. Duce JA, Tsatsanis A, Cater MA, James SA, Robb E, Wikhe K, Leong SL, Perez K, Johanssen T, Greenough MA, Cho HH, Galatis D, Moir RD, Masters CL, McLean C, Tanzi RE, Cappai R, Barnham KJ, Ciccotosto GD, Rogers JT, Bush AI (2010) Iron-export ferroxidase activity of beta-amyloid precursor protein is inhibited by zinc in Alzheimer's disease. Cell 142:857-867. CrossRef Medline
18. Eggert S, Midthune B, Cottrell B, Koo EH (2009) Induced dimerization of the amyloid precursor protein (APP) leads to decreased amyloid-beta protein (Abeta) production. J Biol Chem 284:28943-28952. CrossRef Medline
19. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66:486-501. CrossRef Medline
20. Gaier ED, Eipper BA, Mains RE (2013) Copper signaling in the mammalian nervous system: synaptic effects. J Neurosci Res 91:2-19. CrossRef Medline
21. Galuska SP, Rollenhagen M, Kaup M, Eggers K, OltmannNorden I, Schiff M, Hartmann M, Weinhold B, Hildebrandt H, Geyer R, Muhlenhoff M, Geyer H (2010) Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proc Natl Acad Sci U S A 107:10250-10255. CrossRef Medline
22. Graf ER, Zhang X, Jin SX, Linhoff MW, Craig AM (2004) Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119:1013-1026. CrossRef Medline
23. Gralle M, Oliveira CL, Guerreiro LH, McKinstry WJ, Galatis D, Masters CL, Cappai R, Parker MW, Ramos CH, Torriani I, Ferreira ST (2006) Solution conformation and heparin-induced dimerization of the full-length extracellular domain of the human amyloid precursor protein. J Mol Biol 357:493-508. CrossRef Medline
24. Hatcher LQ, Hong L, Bush WD, Carducci T, Simon JD (2008) Quantification of the binding constant of copper(II) to the amyloid-beta peptide. J Phys Chem B 112:8160-8164. CrossRef Medline
25. Hesse L, Beher D, Masters CL, Multhaup G (1994) The beta A4 amyloid precursor protein binding to copper. FEBS Lett 349:109-116. CrossRef Medline
26. Hong L, Bush WD, Hatcher LQ, Simon J (2008) Determining thermodynamic parameters from isothermal calorimetric isotherms of the binding of macromolecules to metal cations originally chelated by a weak ligand. J Phys Chem B 112:604-611. CrossRef Medline
27. Houtman JC, Brown PH, Bowden B, Yamaguchi H, Appella E, Samelson LE, Schuck P (2007) Studying multisite binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: application to adaptor protein complexes in cell signaling. Protein Sci 16:30-42. CrossRef Medline
28. Isbert S, Wagner K, Eggert S, Schweitzer A, Multhaup G, Weggen S, Kins S, Pietrzik CU (2012) APP dimer formation is initiated in the endoplasmic reticulum and differs between APP isoforms. Cell Mol Life Sci 69:1353-1375. CrossRef Medline
29. Kaden D, Munter LM, Joshi M, Treiber C, Weise C, Bethge T, Voigt P, Schaefer M, Beyermann M, Reif B, Multhaup G (2008) Homophilic interactions of the amyloid precursor protein (APP) ectodomain are regulated by the loop region and affect beta-secretase cleavage of APP. J Biol Chem 283:7271-7279. CrossRef Medline
30. Kaden D, Munter LM, Reif B, Multhaup G (2012) The amyloid precursor protein and its homologues: structural and functional aspects of native and pathogenic oligomerization. Eur J Cell Biol 91:234-239. CrossRef Medline
31. Kardos J, Kovács I, Hajós F, Kálmán M, Simonyi M (1989) Nerve endings from rat brain tissue release copper upon depolarization. A possible role in regulating neuronal excitability. Neurosci Lett 103:139-144. CrossRef Medline
32. Keller S, Vargas C, Zhao H, Piszczek G, Brautigam CA, Schuck P (2012) High-precision isothermal titration calorimetry with automated peakshape analysis. Anal Chem 84:5066-5073. CrossRef Medline
33. Kemmer G, Keller S (2010) Nonlinear least-squares data fitting in Excel spreadsheets. Nat Protoc 5:267-281. CrossRef Medline
34. Kong GK, Adams JJ, Cappai R, Parker MW (2007a) Structure of Alzheimer's disease amyloid precursor protein copper-binding domain at atomic resolution. Acta Crystallogr Sect F Struct Biol Cryst Commun 63:819-824. CrossRef Medline
35. Kong GK, Adams JJ, Harris HH, Boas JF, Curtain CC, Galatis D, Masters CL, Barnham KJ, McKinstry WJ, Cappai R, Parker MW (2007b) Structural studies of the Alzheimer's amyloid precursor protein copper-binding domain reveal how it binds copper ions. J Mol Biol 367:148-161. CrossRef Medline
36. Kong GK, Miles LA, Crespi GA, Morton CJ, Ng HL, Barnham KJ, McKinstry WJ, Cappai R, Parker MW (2008) Copper binding to the Alzheimer's disease amyloid precursor protein. Eur Biophys J 37:269-279. CrossRef Medline
37. Lambert M, Padilla F, Mège RM (2000) Immobilized dimers of N-cadherin-Fc chimera mimic cadherin-mediated cell contact formation: contribution of both outside-in and inside-out signals. J Cell Sci 113:2207-2219. Medline
38. Lee S, Xue Y, Hu J, Wang Y, Liu X, Demeler B, Ha Y (2011) The E2 domains of APP and APLP1 share a conserved mode of dimerization. Biochemistry 50:5453-5464. CrossRef Medline
39. Lutsenko S, Bhattacharjee A, Hubbard AL (2010) Copper handling machinery of the brain. Metallomics 2:596-608. CrossRef Medline
40. Martell A, RM Smith, Motekaitis R (2004) NIST critically selected stability constants of metal complexes. In: NIST Standard Reference Database 46, version 80. College Station, TX; National Institute of Standards and Technology.
41. Masters CL, Beyreuther K (2006) Alzheimer's centennial legacy: prospects for rational therapeutic intervention targeting the Abeta amyloid pathway. Brain 129:2823-2839. CrossRef Medline
42. Maynard CJ, Cappai R, Volitakis I, Cherny RA, White AR, Beyreuther K, Masters CL, Bush AI, Li QX (2002) Overexpression of Alzheimer's disease amyloid-beta opposes the age-dependent elevations of brain copper and iron. J Biol Chem 277:44670-44676. CrossRef Medline
43. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40:658-674. CrossRef Medline
44. Muller UC, Zheng H (2012) Physiological functions of APP family proteins. Cold Spring Harb Perspect Med 2:a006288. CrossRef Medline
45. Multhaup G, Schlicksupp A, Hesse L, Beher D, Ruppert T, Masters CL, Beyreuther K (1996) The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 271:1406-1409. CrossRef Medline
46. Noda Y, Asada M, Kubota M, Maesako M, Watanabe K, Uemura M, Kihara T, Shimohama S, Takahashi R, Kinoshita A, Uemura K (2013) Copper enhances APP dimerization and promotes Abeta production. Neurosci Lett 547:10-15. CrossRef Medline
47. Putnam CD, Hammel M, Hura GL, Tainer JA (2007) X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q Rev Biophys 40:191-285. CrossRef Medline
48. Roberts BR, Ryan TM, Bush AI, Masters CL, Duce JA (2012) The role of metallobiology and amyloid-beta peptides in Alzheimer's disease. J Neurochem 120 [SUPPL 1]:149-166. CrossRef
49. Rossjohn J, Cappai R, Feil SC, Henry A, McKinstry WJ, Galatis D, Hesse L, Multhaup G, Beyreuther K, Masters CL, Parker MW (1999) Crystal structure of the N-terminal, growth factor-like domain of Alzheimer amyloid precursor protein. Nat Struct Biol 6:327-331. CrossRef Medline
50. Sato T, Tang TC, Reubins G, Fei JZ, Fujimoto T, Kienlen-Campard P, Constantinescu SN, Octave JN, Aimoto S, Smith SO (2009) A helix-to-coil transition at the epsilon-cut site in the transmembrane dimer of the amyloid precursor protein is required for proteolysis. Proc Natl Acad Sci USA 106:1421-1426. CrossRefMedline
51. Scheiffele P, Fan J, Choih J, Fetter R, Serafini T (2000) Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101:657-669. CrossRef Medline
52. Schmidt V, Baum K, Lao A, Rateitschak K, Schmitz Y, Teichmann A, Wiesner B, Petersen CM, Nykjaer A, Wolf J, Wolkenhauer O, Willnow TE (2012) Quantitative modelling of amyloidogenic processing and its influence by SORLA in Alzheimer's disease. EMBO J 31:187-200. CrossRef Medline
53. Siddiqui TJ, Craig AM (2011) Synaptic organizing complexes. Curr Opin Neurobiol 21:132-143. CrossRef Medline
54. Smith DG, Cappai R, Barnham KJ (2007) The redox chemistry of the Alzheimer's disease amyloid beta peptide. Biochim Biophys Acta 1768:1976-1990. CrossRef Medline
55. Soba P, Eggert S, Wagner K, Zentgraf H, Siehl K, Kreger S, Löwer A, Langer A, Merdes G, Paro R, Masters CL, Muller U, Kins S, Beyreuther K (2005) Homo and heterodimerization of APP family members promotes intercellular adhesion. EMBO J 24:3624-3634. CrossRef Medline
56. Spoerri L, Vella LJ, Pham CL, Barnham KJ, Cappai R (2012) The amyloid precursor protein copper binding domain histidine residues 149 and 151 mediate APP stability and metabolism. J Biol Chem 287:26840-26853. CrossRef Medline
57. Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76:2879-2886. CrossRef Medline
58. Tamano H, Takeda A (2011) Dynamic action of neurometals at the synapse. Metallomics 3:656-661. CrossRef Medline
59. Wang Y, Ha Y (2004) The X-ray structure of an antiparallel dimer of the human amyloid precursor protein E2 domain. Mol Cell 15:343-353. CrossRef Medline
60. Wang Z, Wang B, Yang L, Guo Q, Aithmitti N, Songyang Z, Zheng H (2009) Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis. J Neurosci 29: 10788-10801. CrossRef Medline
61. White AR, Multhaup G, Maher F, Bellingham S, Camakaris J, Zheng H, Bush AI, Beyreuther K, Masters CL, Cappai R (1999) The Alzheimer's disease amyloid precursor protein modulates copper-induced toxicity and oxidative stress in primary neuronal cultures. J Neurosci 19:9170-9179. Medline