Y682 G mutation of amyloid precursor protein promotes endo-lysosomal dysfunction by disrupting APP–SorLA interaction

Frontiers in Cellular Neuroscience

Volumn 9, Issue APR, 2015, Pages

  La Rosa, Luca Rosario ^a   Perrone, Lorena ^b   Nielsen, Morten Schallburg ^c   Calissano, Pietro ^d   Andersen, Olav Michael ^c,e   Matrone, Carmela ^c  

^a CNR   (Italy)

^b UNIVERSITÉ DE POITIERS   (France)

^c AARHUS UNIVERSITY   (Denmark)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e Danish Research Institute of Translational Neuroscience (DANDRITE) Nordic EMBL Partnership   (Denmark)

Author keywords

Abeta; Alzheimer s disease; APP; Endosome; Lysosomes; Neuronal trafficking; SorLA; Y682G mutation

Indexed keywords

AMYLOID PRECURSOR PROTEIN; CATHEPSIN B; CATHEPSIN D; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; RAB7 PROTEIN; SORTILIN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDO LYSOSOMAL DYSFUNCTION; ENZYME ACTIVITY; GENE MUTATION; HIPPOCAMPAL NEURONAL CULTURE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; LYSOSOME STORAGE DISEASE; MALE; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN INTERACTION; QUANTITATIVE ASSAY; SIGNAL TRANSDUCTION; WESTERN BLOTTING; Y682G MUTATION;

EID: 84927628042     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00109     Document Type: Article

References (40)

1. Alexopoulos, P., Guo, L. H., Kratzer, M., Westerteicher, C., Kurz, A., and Perneczky, R. (2011). Impact of SORL1 single nucleotide polymorphisms on Alzheimer's disease cerebrospinal fluid markers. Dement. Geriatr. Cogn. Disord. 32, 164-170. doi:10.1159/000332017
2. Andersen, O. M., Reiche, J., Schmidt, V., Gotthardt, M., Spoelgen, R., Behlke, J., et al. (2005). Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. U.S.A. 102, 13461-13466. doi:10.1073/pnas.0503689102
3. Andersen, O. M., Schmidt, V., Spoelgen, R., Gliemann, J., Behlke, J., Galatis, D., et al. (2006). Molecular dissection of the interaction between amyloid precursor protein and its neuronal trafficking receptor SorLA/LR11. Biochemistry 45, 2618-2628. doi:10.1021/bi052120v
4. Barbagallo, A. P., Wang, Z., Zheng, H., and D'Adamio, L. (2011). A single tyrosine residue in the amyloid precursor protein intracellular domain is essential for developmental function. J. Biol. Chem. 286, 8717-8721. doi:10.1074/jbc.C111.219873
5. Barbagallo, A. P., Weldon, R., Tamayev, R., Zhou, D., Giliberto, L., Foreman, O., et al. (2010). Tyr(682) in the intracellular domain of APP regulates amyloidogenic APP processing in vivo. PLoS ONE 5:e15503. doi:10.1371/journal.pone.0015503
6. Basso, E., and Matrone, C. (2013). NGF and APP interplay: focus on YENPTY motif of amyloid precursor protein and Y682 residue. Cell Biol. Res. Ther. 2:2. doi:10.4172/2324-9293.1000106
7. Caglayan, S., Takagi-Niidome, S., Liao, F., Carlo, A. S., Schmidt, V., Burgert, T., et al. (2014). Lysosomal sorting of amyloid-beta by the SORLA receptor is impaired by a familial Alzheimer's disease mutation. Sci. Transl. Med. 6, 223ra20. doi:10.1126/scitranslmed.3007747
8. Caster, A. H., and Kahn, R. A. (2013). Recruitment of the Mint3 adaptor is necessary for export of the amyloid precursor protein (APP) from the Golgi complex. J. Biol. Chem. 288, 28567-28580. doi:10.1074/jbc.M113.481101
9. Cuervo, A. M. (2008). Autophagy and aging: keeping that old broom working. Trends Genet. 24, 604-612. doi:10.1016/j.tig.2008.10.002
10. Dodson, S. E., Andersen, O. M., Karmali, V., Fritz, J. J., Cheng, D., Peng, J., et al. (2008). Loss of LR11/SORLA enhances early pathology in a mouse model of amyloidosis: evidence for a proximal role in Alzheimer's disease. J. Neurosci. 28, 12877-12886. doi:10.1523/JNEUROSCI.4582-08.2008
11. Fjorback, A. W., Seaman, M., Gustafsen, C., Mehmedbasic, A., Gokool, S., Wu, C., et al. (2012). Retromer binds the FANSHY sorting motif in SorLA to regulate amyloid precursor protein sorting and processing. J. Neurosci. 32, 1467-1480. doi:10.1523/JNEUROSCI.2272-11.2012
12. Guo, Q., Wang, Z., Li, H., Wiese, M., and Zheng, H. (2012a). APP physiological and pathophysiological functions: insights from animal models. Cell Res. 22, 78-89. doi:10.1038/cr.2011.116
13. Guo, L. H., Westerteicher, C., Wang, X. H., Kratzer, M., Tsolakidou, A., Jiang, M., et al. (2012b). SORL1 genetic variants and cerebrospinal fluid biomarkers of Alzheimer's disease. Eur. Arch. Psychiatry Clin. Neurosci. 262, 529-534. doi:10.1007/s00406-012-0295-x
14. Ikeuchi, T., Hirayama, S., Miida, T., Fukamachi, I., Tokutake, T., Ebinuma, H., et al. (2010). Increased levels of soluble LR11 in cerebrospinal fluid of patients with Alzheimer disease. Dement. Geriatr. Cogn. Disord. 30, 28-32. doi:10.1159/000315539
15. Jiang, S., Li, Y., Zhang, X., Bu, G., Xu, H., and Zhang, Y. W. (2014). Trafficking regulation of proteins in Alzheimer's disease. Mol. Neurodegener. 9, 6. doi:10.1186/1750-1326-9-6
16. La Rosa, L. R., Matrone, C., Ferraina, C., Panico, M. B., Piccirilli, S., Di Certo, M. G., et al. (2013). Age-related changes of hippocampal synaptic plasticity in AbetaPP-null mice are restored by NGF through p75NTR. J. Alzheimers Dis. 33, 265-272. doi:10.3233/JAD-2012-112108
17. Lee, C. Y., and Landreth, G. E. (2010). The role of microglia in amyloid clearance from the AD brain. J. Neural Transm. 117, 949-960. doi:10.1007/s00702-010-0433-4
18. Luzio, J. P., Pryor, P. R., and Bright, N. A. (2007). Lysosomes: fusion and function. Nat. Rev. Mol. Cell Biol. 8, 622-632. doi:10.1038/nrm2217
19. Ma, Q. L., Galasko, D. R., Ringman, J. M., Vinters, H. V., Edland, S. D., Pomakian, J., et al. (2009). Reduction of SorLA/LR11, a sorting protein limiting beta-amyloid production, in Alzheimer disease cerebrospinal fluid. Arch. Neurol. 66, 448-457. doi:10.1001/archneurol.2009.22
20. Matrone, C. (2013). A new molecular explanation for age-related neurodegeneration: the Tyr682 residue of amyloid precursor protein. Bioessays 35, 847-852. doi:10.1002/bies.201300041
21. Matrone, C., Barbagallo, A. P., La Rosa, L. R., Florenzano, F., Ciotti, M. T., Mercanti, D., 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
22. Matrone, C., Ciotti, M. T., Mercanti, D., Marolda, R., and Calissano, P. (2008). NGF and BDNF signaling control amyloidogenic route and Abeta production in hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 105, 13139-13144. doi:10.1073/pnas.0806133105
23. Matrone, C., Luvisetto, S., La Rosa, L. R., Tamayev, R., Pignataro, A., Canu, N., et al. (2012). Tyr682 in the Abeta-precursor protein intracellular domain regulates synaptic connectivity, cholinergic function, and cognitive performance. Aging Cell 11, 1084-1093. doi:10.1111/acel.12009
24. Matrone, C., Marolda, R., Ciafre, S., Ciotti, M. T., Mercanti, D., and Calissano, P. (2009). Tyrosine kinase nerve growth factor receptor switches from prosurvival to proapoptotic activity via Abeta-mediated phosphorylation. Proc. Natl. Acad. Sci. U.S.A. 106, 11358-11363. doi:10.1073/pnas.0904998106
25. Mehmedbasic, A., Christensen, S. K., Nilsson, J., Ruetschi, U., Gustafsen, C., Poulsen, A. S., et al. (2015). SorLA complement-type repeat domains protect the amyloid precursor protein against processing. J. Biol. Chem. 290, 3359-3376. doi:10.1074/jbc.M114.619940
26. Muller, U. C., and Zheng, H. (2012). Physiological functions of APP family proteins. Cold Spring Harb. Perspect. Med. 2, a006288. doi:10.1101/cshperspect.a006288
27. Nixon, R. A., Wegiel, J., Kumar, A., Yu, W. H., Peterhoff, C., Cataldo, A., et al. (2005). Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 64, 113-122.
28. Nixon, R. A., and Yang, D. S. (2011). Autophagy failure in Alzheimer's disease - locating the primary defect. Neurobiol. Dis. 43, 38-45. doi:10.1016/j.nbd.2011.01.021
29. Rogaeva, E., Meng, Y., Lee, J. H., Gu, Y., Kawarai, T., Zou, F., et al. (2007). The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat. Genet. 39, 168-177. doi:10.1038/ng1943
30. Russo, C., Dolcini, V., Salis, S., Venezia, V., Zambrano, N., Russo, T., et al. (2002). Signal transduction through tyrosine-phosphorylated C-terminal fragments of amyloid precursor protein via an enhanced interaction with Shc/Grb2 adaptor proteins in reactive astrocytes of Alzheimer's disease brain. J. Biol. Chem. 277, 35282-35288. doi:10.1074/jbc.M110785200
31. Salminen, A., and Kaarniranta, K. (2009). Regulation of the aging process by autophagy. Trends Mol. Med. 15, 217-224. doi:10.1016/j.molmed.2009.03.004
32. Schmidt, V., Baum, K., Lao, A., Rateitschak, K., Schmitz, Y., Teichmann, A., et al. (2012). Quantitative modelling of amyloidogenic processing and its influence by SORLA in Alzheimer's disease. EMBO J. 31, 187-200. doi:10.1038/emboj.2011.352
33. Spoelgen, R., von Arnim, C. A., Thomas, A. V., Peltan, I. D., Koker, M., Deng, A., et al. (2006). Interaction of the cytosolic domains of sorLA/LR11 with the amyloid precursor protein (APP) and beta-secretase beta-site APP-cleaving enzyme. J. Neurosci. 26, 418-428. doi:10.1523/JNEUROSCI.3882-05.2006
34. Tamayev, R., Zhou, D., and 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
35. Tarr, P. E., Roncarati, R., Pelicci, G., Pelicci, P. G., and D'Adamio, L. (2002). Tyrosine phosphorylation of the beta-amyloid precursor protein cytoplasmic tail promotes interaction with Shc. J. Biol. Chem. 277, 16798-16804. doi:10.1074/jbc.M110286200
36. Willnow, T. E., and Andersen, O. M. (2013). Sorting receptor SORLA - a trafficking path to avoid Alzheimer disease. J. Cell. Sci. 126(Pt 13), 2751-2760. doi:10.1242/jcs.125393
37. Yang, D. S., Stavrides, P., Mohan, P. S., Kaushik, S., Kumar, A., Ohno, M., et al. (2011). Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134(Pt 1), 258-277. doi:10.1093/brain/awq341
38. Yu, W. H., Cuervo, A. M., Kumar, A., Peterhoff, C. M., Schmidt, S. D., Lee, J. H., 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
39. Zhou, D., Noviello, C., D'Ambrosio, C., Scaloni, A., and D'Adamio, L. (2004). Growth factor receptor-bound protein 2 interaction with the tyrosine-phosphorylated tail of amyloid beta precursor protein is mediated by its Src homology 2 domain. J. Biol. Chem. 279, 25374-25380. doi:10.1074/jbc.M400488200
40. Zhou, D., Zambrano, N., Russo, T., and 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