Artículo

Otero, M.G.; Bessone, I.F.; Hallberg, A.E.; Cromberg, L.E.; De Rossi, M.C.; Saez, T.M.; Levi, V.; Almenar-Queralt, A.; Falzone, T.L. "Proteasome stress leads to APP axonal transport defects by promoting its amyloidogenic processing in lysosomes" (2018) Journal of Cell Science. 131(11)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Alzheimer disease (AD) pathology includes the accumulation of poly-ubiquitylated (also known as poly-ubiquitinated) proteins and failures in proteasome-dependent degradation. Whereas the distribution of proteasomes and its role in synaptic function have been studied, whether proteasome activity regulates the axonal transport and metabolism of the amyloid precursor protein (APP), remains elusive. By using live imaging in primary hippocampal neurons, we showed that proteasome inhibition rapidly and severely impairs the axonal transport of APP. Fluorescence cross-correlation analyses andmembrane internalization blockage experiments showed that plasma membrane APP does not contribute to transport defects. Moreover, by western blotting and double-color APP imaging, we demonstrated that proteasome inhibition precludes APP axonal transport by enhancing its endo-lysosomal delivery, where β- cleavage is induced. Taken together, we found that proteasomes control the distal transport of APP and can re-distribute Golgi-derived vesicles to the endo-lysosomal pathway. This crosstalk between proteasomes and lysosomes regulates the intracellular APP dynamics, and defects in proteasome activity can be considered a contributing factor that leads to abnormal APP metabolism in AD. © 2018. Published by The Company of Biologists Ltd.

Registro:

Documento: Artículo
Título:Proteasome stress leads to APP axonal transport defects by promoting its amyloidogenic processing in lysosomes
Autor:Otero, M.G.; Bessone, I.F.; Hallberg, A.E.; Cromberg, L.E.; De Rossi, M.C.; Saez, T.M.; Levi, V.; Almenar-Queralt, A.; Falzone, T.L.
Filiación:Instituto de Biologiá Celular y Neurociencias IBCN (CONICET-UBA), Facultad de Medicina, Universidad de Buenos Aires, Paraguay 2155, Buenos Aires, CP1121, Argentina
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Quimíca Biológica-IQUIBICEN UBA-CONICET, Buenos Aires, CP1428EGA, Argentina
Instituto de Biología y Medicina Experimental, IBYME (CONICET), Vuelta de obligado 2490, Buenos Aires, CP 1428, Argentina
Department of Cellular and Molecular Medicine, School of Medicine, University of California San Diego, La Jolla, CA 92093, United States
Palabras clave:Alzheimer disease; Amyloid precursor protein; Axonal transport; Lysosome; Proteasome; amyloid precursor protein; proteasome; animal cell; animal tissue; Article; cell membrane; controlled study; fluorescence analysis; Golgi complex; hippocampus; live cell imaging; lysosome; molecular interaction; mouse; nerve cell; nerve fiber transport; newborn; nonhuman; priority journal; protein aggregation; protein degradation; protein localization; protein metabolism; protein processing; protein transport; Western blotting
Año:2018
Volumen:131
Número:11
DOI: http://dx.doi.org/10.1242/jcs214536
Título revista:Journal of Cell Science
Título revista abreviado:J. Cell Sci.
ISSN:00219533
CODEN:JNCSA
CAS:proteasome, 140879-24-9
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219533_v131_n11_p_Otero

Referencias:

  • Agholme, L., Hallbeck, M., Benedikz, E., Marcusson, J., Kågedal, K., Amyloid-β secretion, generation, and lysosomal sequestration in response to proteasome inhibition: involvement of autophagy (2012) J. Alzheimer's Dis, 31, pp. 343-358
  • Agholme, L., Nath, S., Domert, J., Marcusson, J., Kågedal, K., Hallbeck, M., Proteasome inhibition induces stress kinase dependent transport deficits-implications for Alzheimer's disease (2014) Mol. Cell. Neurosci, 58, pp. 29-39
  • Allinquant, B., Hantraye, P., Mailleux, P., Moya, K., Bouillot, C., Prochiantz, A., Downregulation of amyloid precursor protein inhibits neurite outgrowth in vitro (1995) J. Cell Biol, 128, pp. 919-927
  • Almeida, C.G., Takahashi, R.H., Gouras, G.K., β-amyloid accumulation impairs multivesicular body sorting by inhibiting the ubiquitinproteasome system (2006) J. Neurosci, 26, pp. 4277-4288
  • Almenar-Queralt, A., Falzone, T.L., Shen, Z., Lillo, C., Killian, R.L., Arreola, A.S., Niederst, E.D., Briggs, S.P., UV irradiation accelerates amyloid precursor protein (APP) processing and disrupts APP axonal transport (2014) J. Neurosci, 34, pp. 3320-3339
  • Amaratunga, A., Fine, R.E., Generation of amyloidogenic C-terminal fragments during rapid axonal transport in vivo of-amyloid precursor protein in the optic nerve (1995) J. Biol. Chem, 270, pp. 17268-17272
  • Arastu-Kapur, S., Anderl, J.L., Kraus, M., Parlati, F., Shenk, K.D., Lee, S.J., Muchamuel, T., Ball, A.J., Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events (2011) Clin. Cancer Res, 17, pp. 2734-2743
  • Bence, N.F., Sampat, R.M., Kopito, R.R., Impairment of the ubiquitinproteasome system by protein aggregation (2001) Science, 292, pp. 1552-1555
  • Bloom, G.S., Amyloid-β and tau: the trigger and bullet in alzheimer disease pathogenesis (2014) JAMA Neurol, 71, pp. 505-508
  • Brojatsch, J., Lima, H., Kar, A.K., Jacobson, L.S., Muehlbauer, S.M., Chandran, K., Diaz-Griffero, F., A proteolytic cascade controls lysosome rupture and necrotic cell death mediated by lysosome-destabilizing adjuvants (2014) PLoS ONE, 9
  • Cai, D., Leem, J.Y., Greenfield, J.P., Wang, P., Kim, B.S., Wang, R., Lopes, K.O., Greengard, P., Presenilin-1 regulates intracellular trafficking and cell surface delivery of β-amyloid precursor protein (2003) J. Biol. Chem, 278, pp. 3446-3454
  • Caporaso, G.L., Takei, K., Gandy, S.E., Matteoli, M., Mundigl, O., Greengard, P., De Camilli, P., Morphologic and biochemical analysis of the intracellular trafficking of the Alzheimer beta/A4 amyloid precursor protein (1994) J. Neurosci, 14, pp. 3122-3138
  • Carey, R.M., Balcz, B.A., Lopez-Coviella, I., Slack, B.E., Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid β protein (2005) BMC Cell Biol, 6, p. 30
  • Cataldo, A.M., Nixon, R.A., Enzymatically active lysosomal proteases are associated with amyloid deposits in Alzheimer brain (1990) Proc. Natl. Acad. Sci. USA, 87, pp. 3861-3865
  • Cataldo, A.M., Thayer, C.Y., Bird, E.D., Wheelock, T.R., Nixon, R.A., Lysosomal proteinase antigens are prominently localized within senile plaques of Alzheimer's disease: evidence for a neuronal origin (1990) Brain Res, 513, pp. 181-192
  • Cecarini, V., Bonfili, L., Cuccioloni, M., Mozzicafreddo, M., Rossi, G., Keller, J.N., Angeletti, M., Eleuteri, A.M., Wild type and mutant amyloid precursor proteins influence downstream effects of proteasome and autophagy inhibition (2014) Biochim. Biophys. Acta, 1842, pp. 127-134
  • Chen, H., Polo, S., Di Fiore, P.P., De Camilli, P.V., Rapid Ca2+-dependent decrease of protein ubiquitination at synapses (2003) Proc. Natl. Acad. Sci. USA, 100, pp. 14908-14913
  • Choy, R.W.-Y., Cheng, Z., Schekman, R., Amyloid precursor protein (APP) traffics from the cell surface via endosomes for amyloid β (Aβ) production in the trans-Golgi network (2012) Proc. Natl Acad. Sci. USA, 109, pp. E2077-E2082
  • Ciechanover, A., Brundin, P., The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg (2003) Neuron, 40, pp. 427-446
  • Das, U., Wang, L., Ganguly, A., Saikia, J.M., Wagner, S.L., Koo, E.H., Roy, S., Visualizing APP and BACE-1 approximation in neurons yields insight into the amyloidogenic pathway (2016) Nat. Neurosci, 19, p. 55
  • Dehvari, N., Mahmud, T., Persson, J., Bengtsson, T., Graff, C., Winblad, B., Rönnbäck, A., Behbahani, H., Amyloid precursor protein accumulates in aggresomes in response to proteasome inhibitor (2012) Neurochem. Int, 60, pp. 533-542
  • Dikic, I., Proteasomal and autophagic degradation systems (2017) Annu. Rev. Biochem, 86, pp. 193-224
  • Djakovic, S.N., Schwarz, L.A., Barylko, B., DeMartino, G.N., Patrick, G.N., Regulation of the proteasome by neuronal activity and calcium/ calmodulin-dependent protein kinase II (2009) J. Biol. Chem, 284, pp. 26655-26665
  • Ebrahimi-Fakhari, D., Cantuti-Castelvetri, I., Fan, Z., Rockenstein, E., Masliah, E., Hyman, B.T., McLean, P.J., Unni, V.K., Distinct roles in vivo for the ubiquitin-proteasome system and the autophagy-lysosomal pathway in the degradation of α-synuclein (2011) J. Neurosci, 31, pp. 14508-14520
  • Falzone, T.L., Stokin, G.B., Imaging amyloid precursor protein in vivo: an axonal transport assay (2012) Methods Mol. Biol, 846, pp. 295-303
  • Falzone, T.L., Stokin, G.B., Lillo, C., Rodrigues, E.M., Westerman, E.L., Williams, D.S., Goldstein, L.S.B., Axonal stress kinase activation and tau misbehavior induced by kinesin-1 transport defects (2009) J. Neurosci, 29, pp. 5758-5767
  • Farizatto, K.L.G., Ikonne, U.S., Almeida, M.F., Ferrari, M.F.R., Bahr, B.A., Aβ(42)-mediated proteasome inhibition and associated tau pathology in hippocampus are governed by a lysosomal response involving cathepsin B: evidence for protective crosstalk between protein clearance pathways (2017) PLoS ONE, 12
  • Fischer, D.F., van Dijk, R., van Tijn, P., Hobo, B., Verhage, M.C., van der Schors, R.C., Wan Li, K., van Leeuwen, F.W., Long-term proteasome dysfunction in the mouse brain by expression of aberrant ubiquitin (2009) Neurobiol. Aging, 30, pp. 847-863
  • Fortun, J., Dunn, W.A., Joy, S., Li, J., Notterpek, L., Emerging role for autophagy in the removal of aggresomes in Schwann cells (2003) J. Neurosci, 23, pp. 10672-10680
  • Frick, M., Schmidt, K., Nichols, B.J., Modulation of lateral diffusion in the plasma membrane by protein density (2007) Curr. Biol, 17, pp. 462-467
  • Geetha T.andWooten, M.W., TrkA receptor endolysosomal degradation is both ubiquitin and proteasome dependent (2008) Traffic, 9, pp. 1146-1156
  • Goldstein, L.S.B., Axonal transport and neurodegenerative disease: can we see the elephant? (2012) Prog. Neurobiol, 99, pp. 186-190
  • Gruenberg, J., Stenmark, H., The biogenesis of multivesicular endosomes (2004) Nat. Rev. Mol. Cell Biol, 5, p. 317
  • Gunawardena, S., Goldstein, L.S.B., Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila (2001) Neuron, 32, pp. 389-401
  • Haass, C., Koo, E.H., Mellon, A., Hung, A.Y., Selkoe, D.J., Targeting of cell-surface [beta]-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments (1992) Nature, 357, pp. 500-503
  • Haass, C., Schlossmacher, M.G., Hung, A.Y., Vigo-Pelfrey, C., Mellon, A., Ostaszewski, B.L., Lieberburg, I., Teplow, D.B., Amyloid [beta]-peptide is produced by cultured cells during normal metabolism (1992) Nature, 359, pp. 322-325
  • Hsu, M.-T., Guo, C.-L., Liou, A.Y., Chang, T.-Y., Ng, M.-C., Florea, B.I., Overkleeft, H.S., Cheng, P.-L., Stagedependent axon transport of proteasomes contributes to axon development (2015) Dev. Cell, 35, pp. 418-431
  • Huse, J.T., Liu, K., Pijak, D.S., Carlin, D., Lee, V.M.-Y., Doms, R.W., β-secretase processing in the trans-Golgi network preferentially generates truncated amyloid species that accumulate in Alzheimer's disease brain (2002) J. Biol. Chem, 277, pp. 16278-16284
  • Ihara, Y., Morishima-Kawashima, M., Nixon, R., The ubiquitin-proteasome system and the autophagic-lysosomal system in Alzheimer disease (2012) Cold Spring Harb. Perspect. Med, 2
  • Jones, S.M., Howell, K.E., Phosphatidylinositol 3-kinase is required for the formation of constitutive transport vesicles from the TGN (1997) J. Cell Biol, 139, pp. 339-349
  • Joshi, G., Wang, Y., Golgi defects enhance APP amyloidogenic processing in Alzheimer's disease (2015) BioEssays, 37, pp. 240-247
  • Joshi, G., Chi, Y., Huang Z.andWang, Y., Aβ-induced Golgi fragmentation in Alzheimer's disease enhances Aβ production (2014) Proc. Natl Acad. Sci. USA, 111, pp. E1230-E1239
  • Kaether, C., Skehel, P., Dotti, C.G., Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons (2000) Mol. Biol. Cell, 11, pp. 1213-1224
  • Kamal, A., Almenar-Queralt, A., LeBlanc, J.F., Roberts, E.A., Goldstein, L.S.B., Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP (2001) Nature, 414, pp. 643-648
  • Katzmann, D.J., Odorizzi, G., Emr, S.D., Receptor downregulation and multivesicular-body sorting (2002) Nat. Rev. Mol. Cell Biol, 3, p. 893
  • Keck, S., Nitsch, R., Grune, T., Ullrich, O., Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease (2003) J. Neurochem, 85, pp. 115-122
  • Keller, J.N., Hanni, K.B., Markesbery, W.R., Impaired proteasome function in Alzheimer's disease (2000) J. Neurochem, 75, pp. 436-439
  • Kienlen-Campard, P., Feyt, C., Huysseune, S., de Diesbach, P., N'Kuli, F., Courtoy, P.J., Octave, J.-N., Lactacystin decreases amyloid-beta peptide production by inhibiting beta-secretase activity (2006) J. Neurosci. Res, 84, pp. 1311-1322
  • Koo, E.H., Sisodia, S.S., Archer, D.R., Martin, L.J., Weidemann, A., Beyreuther, K., Fischer, P., Price, D.L., Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport (1990) Proc. Natl. Acad. Sci. USA, 87, pp. 1561-1565
  • Korolchuk, V.I., Mansilla, A., Menzies, F.M., Rubinsztein, D.C., Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates (2009) Mol. Cell, 33, pp. 517-527
  • Kumar, P., Ambasta, R.K., Veereshwarayya, V., Rosen, K.M., Kosik, K.S., Band, H., Mestril, R., Querfurth, H.W., CHIP and HSPs interact with β-APP in a proteasome-dependent manner and influence Aβ metabolism (2007) Hum. Mol. Genet, 16, pp. 848-864
  • Lam, Y.A., Pickart, C.M., Alban, A., Landon, M., Jamieson, C., Ramage, R., Mayer, R.J., Layfield, R., Inhibition of the ubiquitin-proteasome system in Alzheimer's disease (2000) Proc. Natl. Acad. Sci. USA, 97, pp. 9902-9906
  • Leyssen, M., Ayaz, D., Hébert, S.S., Reeve, S., De Strooper, B., Hassan, B.A., Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain (2005) EMBO J, 24, pp. 2944-2955
  • Liu, Y., Hettinger, C.L., Zhang, D., Rezvani, K., Wang, X., Wang, H., The proteasome function reporter GFPu accumulates in young brains of the APPswe/PS1dE9 Alzheimer's disease mouse model (2014) Cell. Mol. Neurobiol, 34, pp. 315-322
  • Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., Kirchhausen, T., Dynasore, a cell-permeable inhibitor of dynamin (2006) Dev. Cell, 10, pp. 839-850
  • Melikova, M.S., Kondratov, K.A., Kornilova, E.S., Two different stages of epidermal growth factor (EGF) receptor endocytosis are sensitive to free ubiquitin depletion produced by proteasome inhibitor MG132 (2006) Cell Biol. Int, 30, pp. 31-43
  • Moises, T., Wüller, S., Saxena, S., Senderek, J., Weis, J., Krüttgen, A., Proteasomal inhibition alters the trafficking of the neurotrophin receptor TrkA (2009) Biochem. Biophys. Res. Commun, 387, pp. 360-364
  • Muresan, V., Varvel, N.H., Lamb, B.T., Muresan, Z., The cleavage products of amyloid-beta precursor protein are sorted to distinct carrier vesicles that are independently transported within neurites (2009) J. Neurosci, 29, pp. 3565-3578
  • Niederst, E.D., Reyna, S.M., Goldstein, L.S.B., Axonal amyloid precursor protein and its fragments undergo somatodendritic endocytosis and processing (2015) Mol. Biol. Cell, 26, pp. 205-217
  • Nunan, J., Shearman, M.S., Checler, F., Cappai, R., Evin, G., Beyreuther, K., Masters, C.L., Small, D.H., The C-terminal fragment of the Alzheimer's disease amyloid protein precursor is degraded by a proteasomedependent mechanism distinct from gamma-secretase (2001) Eur. J. Biochem, 268, pp. 5329-5336
  • Otero, M.G., Alloatti, M., Cromberg, L.E., Almenar-Queralt, A., Encalada, S.E., Pozo Devoto, V.M., Bruno, L., Falzone, T.L., Fast axonal transport of the proteasome complex depends on membrane interaction and molecular motor function (2014) J. Cell Sci, 127, pp. 1537-1549
  • Pandey, U.B., Batlevi, Y., Baehrecke, E.H., Taylor, J.P., HDAC6 at the intersection of autophagy, the ubiquitin-proteasome system and neurodegeneration (2007) Autophagy, 3, pp. 643-645
  • Patrick, G.N., Bingol, B., Weld, H.A., Schuman, E.M., Ubiquitinmediated proteasome activity is required for agonist-induced endocytosis of GluRs (2003) Curr. Biol, 13, pp. 2073-2081
  • Pigino, G., Morfini, G., Pelsman, A., Mattson, M.P., Brady, S.T., Busciglio, J., Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport (2003) J. Neurosci, 23, pp. 4499-4508
  • Querfurth, H.W., LaFerla, F.M., Alzheimer's disease (2010) N. Engl. J. Med, 362, pp. 329-344
  • Ries, J., Schwille, P., Fluorescence correlation spectroscopy (2012) BioEssays, 34, pp. 361-368
  • Rodrigues, E.M., Weissmiller, A.M., Goldstein, L.S.B., Enhanced beta-secretase processing alters APP axonal transport and leads to axonal defects (2012) Hum. Mol. Genet, 21, pp. 4587-4601
  • Salehi, A., Delcroix, J.-D., Belichenko, P.V., Zhan, K., Wu, C., Valletta, J.S., Takimoto-Kimura, R., Chung, P.P., Increased App expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration (2006) Neuron, 51, pp. 29-42
  • Selkoe, D.J., The molecular pathology of Alzheimer's disease (1991) Neuron, 6, pp. 487-498
  • Sisodia, S., Koo, E., Beyreuther, K., Unterbeck, A., Price, D., Evidence that beta-amyloid protein in Alzheimer's disease is not derived by normal processing (1990) Science, 248, pp. 492-495
  • Smith, D.H., Chen, X., Iwata, A., Graham, D.I., Amyloid β accumulation in axons after traumatic brain injury in humans (2003) J. Neurosurg, 98, pp. 1072-1077
  • Soba, P., Eggert, S., Wagner, K., Zentgraf, H., Siehl, K., Kreger, S., Löwer, A., Paro, R., Homo-and heterodimerization of APP family members promotes intercellular adhesion (2005) EMBO J, 24, pp. 3624-3634
  • Soldano, A., Okray, Z., Janovska, P., Tmejová, K., Reynaud, E., Claeys, A., Yan, J., Dura, J.-M., The Drosophila homologue of the amyloid precursor protein is a conserved modulator of Wnt PCP signaling (2013) PLoS Biol, 11
  • Steuble, M., Diep, T.-M., Schätzle, P., Ludwig, A., Tagaya, M., Kunz, B., Sonderegger, P., Calsyntenin-1 shelters APP from proteolytic processing during anterograde axonal transport (2012) Biol. Open, 1, pp. 761-774
  • Stieber, A., Mourelatos, Z., Gonatas, N.K., In Alzheimer's disease the Golgi apparatus of a population of neurons without neurofibrillary tangles is fragmented and atrophic (1996) Am. J. Pathol, 148, pp. 415-426
  • Stokin, G.B., Goldstein, L.S.B., Axonal transport and Alzheimer's disease (2006) Annu. Rev. Biochem, 75, pp. 607-627
  • Stokin, G.B., Lillo, C., Falzone, T.L., Brusch, R.G., Rockenstein, E., Mount, S.L., Raman, R., Williams, D.S., Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease (2005) Science, 307, pp. 1282-1288
  • Szodorai, A., Kuan, Y.-H., Hunzelmann, S., Engel, U., Sakane, A., Sasaki, T., Takai, Y., Beyreuther, K., APP anterograde transport requires Rab3A GTPase activity for assembly of the transport vesicle (2009) J. Neurosci, 29, pp. 14534-14544
  • Tokuda, T., Kametani, F., Tanaka, K., Sahara, N., Ikeda, S., Yanagisawa, N., Amyloid β protein and its 3-kDa fragment are present in the axoplasm fraction of the white matter in human brain (1996) Biochem. Biophys. Res. Commun, 223, pp. 165-169
  • Torroja, L., Packard, M., Gorczyca, M., White, K., Budnik, V., The Drosophila β-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction (1999) J. Neurosci, 19, pp. 7793-7803
  • Traub, L.M., Kornfeld, S., The trans-Golgi network: a late secretory sorting station (1997) Curr. Opin. Cell Biol, 9, pp. 527-533
  • Trojanowski, J.Q., Lee, V.M.Y., Fatal attractions. of proteins: a comprehensive hypothetical mechanism underlying Alzheimer's disease and other neurodegenerative disorders (2000) Ann. N. Y. Acad. Sci, 924, pp. 62-67
  • van Leeuwen, F.W., de Kleijn, D.P.V., van den Hurk, H.H., Neubauer, A., Sonnemans, M.A.F., Sluijs, J.A., Köycü, S., Martens, G.J., Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients (1998) Science, 279, pp. 242-247
  • Vonderheit, A., Helenius, A., Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes (2005) PLoS Biol, 3, p. e233
  • Wang, Z., Wang, B., Yang, L., Guo, Q., Aithmitti, N., Songyang, Z., Zheng, H., Presynaptic and postsynaptic interaction of the amyloid precursor protein promotes peripheral and central synaptogenesis (2009) J. Neurosci, 29, pp. 10788-10801
  • Wang, B., Li, H., Mutlu, S.A., Bowser, D.A., Moore, M.J., Wang, M.C., Zheng, H., The amyloid precursor protein is a conserved receptor for slit to mediate axon guidance (2017) eNeuro, 4
  • Webb, J.L., Ravikumar, B., Atkins, J., Skepper, J.N., Rubinsztein, D.C., Alpha-Synuclein is degraded by both autophagy and the proteasome (2003) J Biol Chem, 278, pp. 25009-25013
  • Willeumier, K., Pulst, S.M., Schweizer, F.E., Proteasome inhibition triggers activity-dependent increase in the size of the recycling vesicle pool in cultured hippocampal neurons (2006) J. Neurosci, 26, pp. 11333-11341

Citas:

---------- APA ----------
Otero, M.G., Bessone, I.F., Hallberg, A.E., Cromberg, L.E., De Rossi, M.C., Saez, T.M., Levi, V.,..., Falzone, T.L. (2018) . Proteasome stress leads to APP axonal transport defects by promoting its amyloidogenic processing in lysosomes. Journal of Cell Science, 131(11).
http://dx.doi.org/10.1242/jcs214536
---------- CHICAGO ----------
Otero, M.G., Bessone, I.F., Hallberg, A.E., Cromberg, L.E., De Rossi, M.C., Saez, T.M., et al. "Proteasome stress leads to APP axonal transport defects by promoting its amyloidogenic processing in lysosomes" . Journal of Cell Science 131, no. 11 (2018).
http://dx.doi.org/10.1242/jcs214536
---------- MLA ----------
Otero, M.G., Bessone, I.F., Hallberg, A.E., Cromberg, L.E., De Rossi, M.C., Saez, T.M., et al. "Proteasome stress leads to APP axonal transport defects by promoting its amyloidogenic processing in lysosomes" . Journal of Cell Science, vol. 131, no. 11, 2018.
http://dx.doi.org/10.1242/jcs214536
---------- VANCOUVER ----------
Otero, M.G., Bessone, I.F., Hallberg, A.E., Cromberg, L.E., De Rossi, M.C., Saez, T.M., et al. Proteasome stress leads to APP axonal transport defects by promoting its amyloidogenic processing in lysosomes. J. Cell Sci. 2018;131(11).
http://dx.doi.org/10.1242/jcs214536