TrkB receptor cleavage by delta-secretase abolishes its phosphorylation of APP, aggravating Alzheimer’s disease pathologies

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  • 1.

    Reichardt LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci. 2006;361:1545–64.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 2.

    Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science. 2002;297:353–6.

    CAS 

    Google Scholar
     

  • 3.

    Elliott E, Ginzburg I. The role of neurotrophins and insulin on tau pathology in Alzheimer’s disease. Rev Neurosci. 2006;17:635–42.

    CAS 
    PubMed 

    Google Scholar
     

  • 4.

    Svendsen CN, Cooper JD, Sofroniew MV. Trophic factor effects on septal cholinergic neurons. Ann NY Acad Sci. 1991;640:91–94.

    CAS 
    PubMed 

    Google Scholar
     

  • 5.

    Crutcher KA, Scott SA, Liang S, Everson WV, Weingartner J. Detection of NGF-like activity in human brain tissue: increased levels in Alzheimer’s disease. J Neurosci. 1993;13:2540–50.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 6.

    Hellweg R, Gericke CA, Jendroska K, Hartung HD, Cervos-Navarro J. NGF content in the cerebral cortex of non-demented patients with amyloid-plaques and in symptomatic Alzheimer’s disease. Int J Dev Neurosci. 1998;16:787–94.

    CAS 
    PubMed 

    Google Scholar
     

  • 7.

    Peng S, Wuu J, Mufson EJ, Fahnestock M. Increased proNGF levels in subjects with mild cognitive impairment and mild Alzheimer disease. J Neuropathol Exp Neurol. 2004;63:641–9.

    CAS 
    PubMed 

    Google Scholar
     

  • 8.

    Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW. BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer’s disease. Neuron. 1991;7:695–702.

    CAS 
    PubMed 

    Google Scholar
     

  • 9.

    Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M. Brain-derived neurotrophic factor is reduced in Alzheimer’s disease. Brain Res Mol Brain Res. 1997;49:71–81.

    CAS 
    PubMed 

    Google Scholar
     

  • 10.

    Ferrer I, Marin C, Rey MJ, Ribalta T, Goutan E, Blanco R, et al. BDNF and full-length and truncated TrkB expression in Alzheimer disease. Implications in therapeutic strategies. J Neuropathol Exp Neurol. 1999;58:729–39.

    CAS 
    PubMed 

    Google Scholar
     

  • 11.

    Rohe M, Synowitz M, Glass R, Paul SM, Nykjaer A, Willnow TE. Brain-derived neurotrophic factor reduces amyloidogenic processing through control of SORLA gene expression. J Neurosci. 2009;29:15472–8.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 12.

    Matrone C, Ciotti MT, Mercanti D, Marolda R, Calissano PNGF. and BDNF signaling control amyloidogenic route and Abeta production in hippocampal neurons. Proc Natl Acad Sci USA. 2008;105:13139–44.

    CAS 
    PubMed 

    Google Scholar
     

  • 13.

    Murer MG, Boissiere F, Yan Q, Hunot S, Villares J, Faucheux B, et al. An immunohistochemical study of the distribution of brain-derived neurotrophic factor in the adult human brain, with particular reference to Alzheimer’s disease. Neuroscience. 1999;88:1015–32.

    CAS 
    PubMed 

    Google Scholar
     

  • 14.

    Ando S, Kobayashi S, Waki H, Kon K, Fukui F, Tadenuma T, et al. Animal model of dementia induced by entorhinal synaptic damage and partial restoration of cognitive deficits by BDNF and carnitine. J Neurosci Res. 2002;70:519–27.

    CAS 
    PubMed 

    Google Scholar
     

  • 15.

    Kitiyanant N, Kitiyanant Y, Svendsen CN, Thangnipon W. BDNF-, IGF-1- and GDNF-secreting human neural progenitor cells rescue amyloid beta-induced toxicity in cultured rat septal neurons. Neurochem Res. 2012;37:143–52.

    CAS 
    PubMed 

    Google Scholar
     

  • 16.

    Arancibia S, Silhol M, Mouliere F, Meffre J, Hollinger I, Maurice T, et al. Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol Dis. 2008;31:316–26.

    CAS 
    PubMed 

    Google Scholar
     

  • 17.

    Wang ZH, Xiang J, Liu X, Yu SP, Manfredsson FP, Sandoval IM, et al. Deficiency in BDNF/TrkB Neurotrophic Activity Stimulates delta-Secretase by Upregulating C/EBPbeta in Alzheimer’s Disease. Cell Rep. 2019;28:655–669. e655.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 18.

    Wang ZH, Gong K, Liu X, Zhang Z, Sun X, Wei ZZ, et al. C/EBPbeta regulates delta-secretase expression and mediates pathogenesis in mouse models of Alzheimer’s disease. Nat Commun. 2018;9:1784.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 19.

    Xiang J, Wang ZH, Ahn EH, Liu X, Yu SP, Manfredsson FP, et al. Delta-secretase-cleaved Tau antagonizes TrkB neurotrophic signalings, mediating Alzheimer’s disease pathologies. Proc Natl Acad Sci USA. 2019;116:9094–102.

    CAS 
    PubMed 

    Google Scholar
     

  • 20.

    Chen C, Wang Z, Zhang Z, Liu X, Kang SS, Zhang Y, et al. The prodrug of 7,8-dihydroxyflavone development and therapeutic efficacy for treating Alzheimer’s disease. Proc Natl Acad Sci USA. 2018;115:578–83.

    CAS 
    PubMed 

    Google Scholar
     

  • 21.

    Zhang Z, Liu X, Schroeder JP, Chan CB, Song M, Yu SP, et al. 7,8-dihydroxyflavone prevents synaptic loss and memory deficits in a mouse model of Alzheimer’s disease. Neuropsychopharmacology. 2014;39:638–50.

    PubMed 

    Google Scholar
     

  • 22.

    Jang SW, Liu X, Yepes M, Shepherd KR, Miller GW, Liu Y, et al. A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc Natl Acad Sci USA. 2010;107:2687–92.

    CAS 
    PubMed 

    Google Scholar
     

  • 23.

    Liu Z, Jang SW, Liu X, Cheng D, Peng J, Yepes M, et al. Neuroprotective actions of PIKE-L by inhibition of SET proteolytic degradation by asparagine endopeptidase. Mol Cell. 2008;29:665–78.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 24.

    Zhang Z, Song M, Liu X, Su Kang S, Duong DM, Seyfried NT, et al. Delta-secretase cleaves amyloid precursor protein and regulates the pathogenesis in Alzheimer’s disease. Nat Commun. 2015;6:8762.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 25.

    Zhang Z, Song M, Liu X, Kang SS, Kwon IS, Duong DM, et al. Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer’s disease. Nat Med. 2014;20:1254–62.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 26.

    Bao J, Qin M, Mahaman YAR, Zhang B, Huang F, Zeng K et al. BACE1 SUMOylation increases its stability and escalates the protease activity in Alzheimer’s disease. Proc Natl Acad Sci USA. 2018;115:3954–9.

    CAS 
    PubMed 

    Google Scholar
     

  • 27.

    Matrone C, Barbagallo AP, La Rosa LR, Florenzano F, Ciotti MT, Mercanti D, et al. APP is phosphorylated by TrkA and regulates NGF/TrkA signaling. J Neurosci. 2011;31:11756–61.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 28.

    Canu N, Amadoro G, Triaca V, Latina V, Sposato V, Corsetti V et al. The intersection of NGF/TrkA signaling and amyloid precursor protein processing in Alzheimer’s disease neuropathology. Int J Mol Sci. 2017;18:1319–35.

    PubMed Central 

    Google Scholar
     

  • 29.

    Zhang Z, Kang SS, Liu X, Ahn EH, Zhang Z, He L, et al. Asparagine endopeptidase cleaves alpha-synuclein and mediates pathologic activities in Parkinson’s disease. Nat Struct Mol Biol. 2017;24:632–42.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 30.

    Wang ZH, Liu P, Liu X, Manfredsson FP, Sandoval IM, Yu SP, et al. Delta-secretase phosphorylation by SRPK2 enhances its enzymatic activity, provoking pathogenesis in Alzheimer’s disease. Mol cell. 2017;67:812–825 e815.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 31.

    Edgington LE, Verdoes M, Ortega A, Withana NP, Lee J, Syed S, et al. Functional imaging of legumain in cancer using a new quenched activity-based probe. J Am Chem Soc. 2013;135:174–82.

    CAS 
    PubMed 

    Google Scholar
     

  • 32.

    Li DN, Matthews SP, Antoniou AN, Mazzeo D, Watts C. Multistep autoactivation of asparaginyl endopeptidase in vitro and in vivo. J Biol Chem. 2003;278:38980–90.

    CAS 
    PubMed 

    Google Scholar
     

  • 33.

    Zhang Z, Obianyo O, Dall E, Du Y, Fu H, Liu X, et al. Inhibition of delta-secretase improves cognitive functions in mouse models of Alzheimer’s disease. Nat Commun. 2017;8:14740.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 34.

    Lunde NN, Haugen MH, Bodin Larsen KB, Damgaard I, Pettersen SJ, Kasem R, et al. Glycosylation is important for legumain localization and processing to active forms but not for cystatin E/M inhibitory functions. Biochimie. 2017;139:27–37.

    CAS 
    PubMed 

    Google Scholar
     

  • 35.

    Lee MS, Kao SC, Lemere CA, Xia W, Tseng HC, Zhou Y, et al. APP processing is regulated by cytoplasmic phosphorylation. J Cell Biol. 2003;163:83–95.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 36.

    Scheinfeld MH, Ghersi E, Davies P, D’Adamio L. Amyloid beta protein precursor is phosphorylated by JNK-1 independent of, yet facilitated by, JNK-interacting protein (JIP)-1. J Biol Chem. 2003;278:42058–63.

    CAS 
    PubMed 

    Google Scholar
     

  • 37.

    Barbagallo AP, Wang Z, Zheng H, D’Adamio L. A single tyrosine residue in the amyloid precursor protein intracellular domain is essential for developmental function. J Biol Chem. 2011;286:8717–21.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 38.

    Barbagallo AP, Weldon R, Tamayev R, Zhou D, Giliberto L, Foreman O, et al. Tyr(682) in the intracellular domain of APP regulates amyloidogenic APP processing in vivo. PLoS ONE. 2010;5:e15503.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 39.

    Russo C, Dolcini V, Salis S, Venezia V, Violani E, Carlo P, et al. Signal transduction through tyrosine-phosphorylated carboxy-terminal fragments of APP via an enhanced interaction with Shc/Grb2 adaptor proteins in reactive astrocytes of Alzheimer’s disease brain. Ann NY Acad Sci. 2002;973:323–33.

    CAS 
    PubMed 

    Google Scholar
     

  • 40.

    Tamayev R, Zhou D, D’Adamio L. The interactome of the amyloid beta precursor protein family members is shaped by phosphorylation of their intracellular domains. Mol Neurodegener. 2009;4:28.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 41.

    Tarr PE, Roncarati R, Pelicci G, Pelicci PG, D’Adamio L. Tyrosine phosphorylation of the beta-amyloid precursor protein cytoplasmic tail promotes interaction with Shc. J Biol Chem. 2002;277:16798–804.

    CAS 
    PubMed 

    Google Scholar
     

  • 42.

    Alonso M, Medina JH, Pozzo-Miller L. ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn Mem. 2004;11:172–8.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • 43.

    Amaral MD, Pozzo-Miller L. TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci. 2007;27:5179–89.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 44.

    Rex CS, Lin CY, Kramar EA, Chen LY, Gall CM, Lynch G. Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci. 2007;27:3017–29.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 45.

    Triaca V, Sposato V, Bolasco G, Ciotti MT, Pelicci P, Bruni AC, et al. NGF controls APP cleavage by downregulating APP phosphorylation at Thr668: relevance for Alzheimer’s disease. Aging Cell. 2016;15:661–72.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 46.

    Rebelo S, Vieira SI, Esselmann H, Wiltfang J, da Cruz e Silva EF, da Cruz e Silva OA. Tyr687 dependent APP endocytosis and Abeta production. J Mol Neurosci. 2007;32:1–8.

    CAS 
    PubMed 

    Google Scholar
     

  • 47.

    Rebelo S, Vieira SI, Esselmann H, Wiltfang J, da Cruz e Silva EF, da Cruz e Silva OA. Tyrosine 687 phosphorylated Alzheimer’s amyloid precursor protein is retained intracellularly and exhibits a decreased turnover rate. Neurodegener Dis. 2007;4:78–87.

    CAS 
    PubMed 

    Google Scholar
     

  • 48.

    Manucat-Tan NB, Saadipour K, Wang YJ, Bobrovskaya L, Zhou XF. Cellular trafficking of amyloid precursor protein in amyloidogenesis physiological and pathological significance. Mol Neurobiol. 2019;56:812–30.

    CAS 
    PubMed 

    Google Scholar
     

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