Death Induced by Survival gene Elimination (DISE) correlates with neurotoxicity in Alzheimer's disease and aging.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
18 Jan 2024
18 Jan 2024
Historique:
received:
02
02
2023
accepted:
13
12
2023
medline:
19
1
2024
pubmed:
19
1
2024
entrez:
18
1
2024
Statut:
epublish
Résumé
Alzheimer's disease (AD) is characterized by progressive neurodegeneration, but the specific events that cause cell death remain poorly understood. Death Induced by Survival gene Elimination (DISE) is a cell death mechanism mediated by short (s) RNAs acting through the RNA-induced silencing complex (RISC). DISE is thus a form of RNA interference, in which G-rich 6mer seed sequences in the sRNAs (position 2-7) target hundreds of C-rich 6mer seed matches in genes essential for cell survival, resulting in the activation of cell death pathways. Here, using Argonaute precipitation and RNAseq (Ago-RP-Seq), we analyze RISC-bound sRNAs to quantify 6mer seed toxicity in several model systems. In mouse AD models and aging brain, in induced pluripotent stem cell-derived neurons from AD patients, and in cells exposed to Aβ42 oligomers, RISC-bound sRNAs show a shift to more toxic 6mer seeds compared to controls. In contrast, in brains of "SuperAgers", humans over age 80 who have superior memory performance, RISC-bound sRNAs are shifted to more nontoxic 6mer seeds. Cells depleted of nontoxic sRNAs are sensitized to Aβ42-induced cell death, and reintroducing nontoxic RNAs is protective. Altogether, the correlation between DISE and Aβ42 toxicity suggests that increasing the levels of nontoxic miRNAs in the brain or blocking the activity of toxic RISC-bound sRNAs could ameliorate neurodegeneration.
Identifiants
pubmed: 38238311
doi: 10.1038/s41467-023-44465-8
pii: 10.1038/s41467-023-44465-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
264Informations de copyright
© 2024. The Author(s).
Références
Hardy, J. A. & Higgins, G. A. Alzheimer’s disease: the amyloid cascade hypothesis. Science 256, 184–185 (1992).
pubmed: 1566067
doi: 10.1126/science.1566067
Bhat, A. H. et al. Oxidative stress, mitochondrial dysfunction and neurodegenerative diseases; a mechanistic insight. Biomed. Pharmacother. 74, 101–110 (2015).
pubmed: 26349970
doi: 10.1016/j.biopha.2015.07.025
Dawson, T. M. & Dawson, V. L. Mitochondrial mechanisms of neuronal cell death: potential therapeutics. Annu Rev. Pharm. Toxicol. 57, 437–454 (2017).
doi: 10.1146/annurev-pharmtox-010716-105001
Kumari, S., Dhapola, R. & Reddy, D. H. Apoptosis in Alzheimer’s disease: insight into the signaling pathways and therapeutic avenues. Apoptosis 28, 943–957 (2023).
pubmed: 37186274
doi: 10.1007/s10495-023-01848-y
Velez-Pardo, C., Arroyave, S. T., Lopera, F., Castano, A. D. & Jimenez Del Rio, M. Ultrastructure evidence of necrotic neural cell death in familial Alzheimer’s disease brains bearing presenilin-1 E280A mutation. J. Alzheimers Dis. 3, 409–415 (2001).
pubmed: 12214045
doi: 10.3233/JAD-2001-3408
Zhang, R., Song, Y. & Su, X. Necroptosis and Alzheimer’s disease: pathogenic mechanisms and therapeutic opportunities. J. Alzheimers Dis. 94, S367–S386 (2023).
pubmed: 36463451
pmcid: 10473100
doi: 10.3233/JAD-220809
Wang, Q. et al. Ferroptosis, Pyroptosis, and Cuproptosis in Alzheimer’s Disease. ACS Chem. Neurosci. 14, 3564–3587 (2023).
Salech, F., Ponce, D. P., Paula-Lima, A. C., SanMartin, C. D. & Behrens, M. I. Nicotinamide, a Poly [ADP-Ribose] Polymerase 1 (PARP-1) inhibitor, as an adjunctive therapy for the treatment of Alzheimer’s disease. Front. Aging Neurosci. 12, 255 (2020).
pubmed: 32903806
pmcid: 7438969
doi: 10.3389/fnagi.2020.00255
Caponio, D. et al. Compromised autophagy and mitophagy in brain ageing and Alzheimer’s diseases. Aging Brain 2, 100056 (2022).
pubmed: 36908880
pmcid: 9997167
doi: 10.1016/j.nbas.2022.100056
Younkin, S. G. The role of A beta 42 in Alzheimer’s disease. J. Physiol. Paris 92, 289–292 (1998).
pubmed: 9789825
doi: 10.1016/S0928-4257(98)80035-1
Hutton, M., Perez-Tur, J. & Hardy, J. Genetics of Alzheimer’s disease. Essays Biochem 33, 117–131 (1998).
pubmed: 10488446
doi: 10.1042/bse0330117
Wang, H., Lautrup, S., Caponio, D., Zhang, J. & Fang, E. F. DNA damage-induced neurodegeneration in accelerated ageing and Alzheimer’s Disease. Int J. Mol. Sci. 22, 6748 (2021).
pubmed: 34201700
pmcid: 8268089
doi: 10.3390/ijms22136748
Miller, M. B. et al. Somatic genomic changes in single Alzheimer’s disease neurons. Nature 604, 714–722 (2022).
pubmed: 35444284
pmcid: 9357465
doi: 10.1038/s41586-022-04640-1
Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P. & Burge, C. B. Prediction of mammalian microRNA targets. Cell 115, 787–798 (2003).
pubmed: 14697198
doi: 10.1016/S0092-8674(03)01018-3
Lai, E. C. Micro RNAs are complementary to 3’ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet 30, 363–364 (2002).
pubmed: 11896390
doi: 10.1038/ng865
Eulalio, A., Huntzinger, E. & Izaurralde, E. GW182 interaction with Argonaute is essential for miRNA-mediated translational repression and mRNA decay. Nat. Struct. Mol. Biol. 15, 346–353 (2008).
pubmed: 18345015
doi: 10.1038/nsmb.1405
Lee, Y. et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051–4060 (2004).
pubmed: 15372072
pmcid: 524334
doi: 10.1038/sj.emboj.7600385
Han, J. et al. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016–3027 (2004).
pubmed: 15574589
pmcid: 535913
doi: 10.1101/gad.1262504
Yi, R., Qin, Y., Macara, I. G. & Cullen, B. R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011–3016 (2003).
pubmed: 14681208
pmcid: 305252
doi: 10.1101/gad.1158803
Bernstein, E., Caudy, A. A., Hammond, S. M. & Hannon, G. J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363–366 (2001).
pubmed: 11201747
doi: 10.1038/35053110
Hutvagner, G. et al. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834–838 (2001).
pubmed: 11452083
doi: 10.1126/science.1062961
Wang, Y., Sheng, G., Juranek, S., Tuschl, T. & Patel, D. J. Structure of the guide-strand-containing argonaute silencing complex. Nature 456, 209–213 (2008).
pubmed: 18754009
pmcid: 4689319
doi: 10.1038/nature07315
Kim, Y. K., Kim, B. & Kim, V. N. Re-evaluation of the roles of DROSHA, Exportin 5, and DICER in microRNA biogenesis. Proc. Natl Acad. Sci. USA 113, E1881–1889 (2016).
pubmed: 26976605
pmcid: 4822641
doi: 10.1073/pnas.1602532113
Gao, Q. Q. et al. 6mer seed toxicity in tumor suppressive miRNAs. Nat. Comm. 9, 4504 (2018).
doi: 10.1038/s41467-018-06526-1
Patel, M. et al. Identification of the toxic 6mer seed consensus in human cancer cells. Sci. Rep. 12, 5130 (2022).
pubmed: 35332222
pmcid: 8948288
doi: 10.1038/s41598-022-09051-w
Hadji, A. et al. Death induced by CD95 or CD95 ligand elimination. Cell Rep. 7, 208–222 (2014).
pubmed: 24656822
pmcid: 4083055
doi: 10.1016/j.celrep.2014.02.035
Putzbach, W. et al. Many si/shRNAs can kill cancer cells by targeting multiple survival genes through an off-target mechanism. eLife 6, e29702 (2017).
pubmed: 29063830
pmcid: 5655136
doi: 10.7554/eLife.29702
Patel, M. et al. The ratio of toxic-to-nontoxic microRNAs predicts platinum sensitivity in ovarian cancer. Cancer Res 81, 3985–4000 (2021).
pubmed: 34224372
pmcid: 8338879
doi: 10.1158/0008-5472.CAN-21-0953
Murmann, A. E. et al. 6mer seed toxicity in viral microRNAs. iScience 23, 100737 (2019).
pubmed: 31838022
pmcid: 7033618
doi: 10.1016/j.isci.2019.11.031
Karanth, S. D. et al. Cancer diagnosis is associated with a lower burden of dementia and less Alzheimer’s-type neuropathology. Brain 145, 2518–2527 (2022).
pubmed: 35094057
pmcid: 9612796
doi: 10.1093/brain/awac035
Musicco, M. et al. Inverse occurrence of cancer and Alzheimer disease: a population-based incidence study. Neurology 81, 322–328 (2013).
pubmed: 23843468
doi: 10.1212/WNL.0b013e31829c5ec1
Majd, S., Power, J. & Majd, Z. Alzheimer’s Disease and Cancer: When Two Monsters Cannot Be Together. Front Neurosci. 13, 155 (2019).
pubmed: 30881282
pmcid: 6407038
doi: 10.3389/fnins.2019.00155
Haluck-Kangas, A. et al. DISE/6mer Seed Toxicity - A powerful anti-cancer mechanism with implications for other diseases. J. Exp. Clin. Cancer Res 40, 389 (2021).
pubmed: 34893072
pmcid: 8662895
doi: 10.1186/s13046-021-02177-1
Oakley, H. et al. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129–10140 (2006).
pubmed: 17021169
pmcid: 6674618
doi: 10.1523/JNEUROSCI.1202-06.2006
Park, H., Lee, Y. B. & Chang, K. A. miR-200c suppression increases tau hyperphosphorylation by targeting 14-3-3gamma in early stage of 5xFAD mouse model of Alzheimer’s disease. Int J. Biol. Sci. 18, 2220–2234 (2022).
pubmed: 35342350
pmcid: 8935215
doi: 10.7150/ijbs.66604
Martinez, J. et al. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat. Cell Biol. 17, 893–906 (2015).
pubmed: 26098576
pmcid: 4612372
doi: 10.1038/ncb3192
Teitz, T. et al. Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat. Med 6, 529–535 (2000).
pubmed: 10802708
doi: 10.1038/75007
Heckmann, B. L. et al. LC3-Associated Endocytosis Facilitates beta-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease. Cell 178, 536–551.e514 (2019).
pubmed: 31257024
pmcid: 6689199
doi: 10.1016/j.cell.2019.05.056
Bartom, E. T. et al. SPOROS: A pipeline to analyze DISE/6mer seed toxicity. PLOS Comp. Biol. 18, e1010022 (2021).
doi: 10.1371/journal.pcbi.1010022
Roberson, E. D. et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model. Science 316, 750–754 (2007).
pubmed: 17478722
doi: 10.1126/science.1141736
Rapoport, M., Dawson, H. N., Binder, L. I., Vitek, M. P. & Ferreira, A. Tau is essential to beta -amyloid-induced neurotoxicity. Proc. Natl Acad. Sci. USA 99, 6364–6369 (2002).
pubmed: 11959919
pmcid: 122954
doi: 10.1073/pnas.092136199
Ferreira, A. & Bigio, E. H. Calpain-mediated tau cleavage: a mechanism leading to neurodegeneration shared by multiple tauopathies. Mol. Med 17, 676–685 (2011).
pubmed: 21442128
pmcid: 3146621
doi: 10.2119/molmed.2010.00220
Hernandez, F., Merchan-Rubira, J., Valles-Saiz, L., Rodriguez-Matellan, A. & Avila, J. Differences Between Human and Murine Tau at the N-terminal End. Front Aging Neurosci. 12, 11 (2020).
pubmed: 32063841
pmcid: 6999090
doi: 10.3389/fnagi.2020.00011
Lang, A. E., Riherd Methner, D. N. & Ferreira, A. Neuronal degeneration, synaptic defects, and behavioral abnormalities in tau(4)(5)(-)(2)(3)(0) transgenic mice. Neuroscience 275, 322–339 (2014).
pubmed: 24952329
doi: 10.1016/j.neuroscience.2014.06.017
Afreen, S. & Ferreira, A. The formation of small aggregates contributes to the neurotoxic effects of tau(45-230). Neurochem Int 152, 105252 (2022).
pubmed: 34856321
doi: 10.1016/j.neuint.2021.105252
Sethi, P. & Lukiw, W. J. Micro-RNA abundance and stability in human brain: Specific alterations in Alzheimer’s disease temporal lobe neocortex. Neurosci. Lett. 459, 100–104 (2009).
pubmed: 19406203
doi: 10.1016/j.neulet.2009.04.052
Chen, M. L. et al. Inhibition of miR-331-3p and miR-9-5p ameliorates Alzheimer’s disease by enhancing autophagy. Theranostics 11, 2395–2409 (2021).
pubmed: 33500732
pmcid: 7797673
doi: 10.7150/thno.47408
Rossi, R. L. et al. Distinct microRNA signatures in human lymphocyte subsets and enforcement of the naive state in CD4+ T cells by the microRNA miR-125b. Nat. Immunol. 12, 796–803 (2011).
pubmed: 21706005
doi: 10.1038/ni.2057
Roy, S. miRNA in Macrophage Development and Function. Antioxid. Redox Signal 25, 795–804 (2016).
pubmed: 27353423
pmcid: 5107671
doi: 10.1089/ars.2016.6728
Jovicic, A. et al. Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J. Neurosci. 33, 5127–5137 (2013).
pubmed: 23516279
pmcid: 6705001
doi: 10.1523/JNEUROSCI.0600-12.2013
Kosik, K. S. The neuronal microRNA system. Nat. Rev. Neurosci. 7, 911–920 (2006).
pubmed: 17115073
doi: 10.1038/nrn2037
Schaefer, A. et al. Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med 204, 1553–1558 (2007).
pubmed: 17606634
pmcid: 2118654
doi: 10.1084/jem.20070823
Davis, T. H. et al. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322–4330 (2008).
pubmed: 18434510
pmcid: 3844796
doi: 10.1523/JNEUROSCI.4815-07.2008
Mori, M. A. et al. Role of microRNA processing in adipose tissue in stress defense and longevity. Cell Metab. 16, 336–347 (2012).
pubmed: 22958919
pmcid: 3461823
doi: 10.1016/j.cmet.2012.07.017
Mertens, J., Reid, D., Lau, S., Kim, Y. & Gage, F. H. Aging in a Dish: iPSC-Derived and Directly Induced Neurons for Studying Brain Aging and Age-Related Neurodegenerative Diseases. Annu Rev. Genet 52, 271–293 (2018).
pubmed: 30208291
pmcid: 6415910
doi: 10.1146/annurev-genet-120417-031534
Min, K. W. et al. Profiling of m6A RNA modifications identified an age-associated regulation of AGO2 mRNA stability. Aging Cell 17, e12753 (2018).
pubmed: 29573145
pmcid: 5946072
doi: 10.1111/acel.12753
Rogalski, E. J. et al. Youthful memory capacity in old brains: anatomic and genetic clues from the Northwestern SuperAging Project. J. Cogn. Neurosci. 25, 29–36 (2013).
pubmed: 23198888
pmcid: 3541673
doi: 10.1162/jocn_a_00300
Feng, M. G. et al. MiR-21 attenuates apoptosis-triggered by amyloid-beta via modulating PDCD4/ PI3K/AKT/GSK-3beta pathway in SH-SY5Y cells. Biomed. Pharmacother. 101, 1003–1007 (2018).
pubmed: 29635890
doi: 10.1016/j.biopha.2018.02.043
Higaki, S. et al. Defensive effect of microRNA-200b/c against amyloid-beta peptide-induced toxicity in Alzheimer’s disease models. PLoS One 13, e0196929 (2018).
pubmed: 29738527
pmcid: 5940223
doi: 10.1371/journal.pone.0196929
Lambert, M. P. et al. Beta/A4-evoked degeneration of differentiated SH-SY5Y human neuroblastoma cells. J. Neurosci. Res 39, 377–385 (1994).
pubmed: 7533843
doi: 10.1002/jnr.490390404
Krishtal, J., Bragina, O., Metsla, K., Palumaa, P. & Tougu, V. In situ fibrillizing amyloid-beta 1-42 induces neurite degeneration and apoptosis of differentiated SH-SY5Y cells. PLoS One 12, e0186636 (2017).
pubmed: 29065138
pmcid: 5655426
doi: 10.1371/journal.pone.0186636
Ferreira, A., Busciglio, J., Landa, C. & Caceres, A. Ganglioside-enhanced neurite growth: evidence for a selective induction of high-molecular-weight MAP-2. J. Neurosci. 10, 293–302 (1990).
pubmed: 2153774
pmcid: 6570343
doi: 10.1523/JNEUROSCI.10-01-00293.1990
Kaplan, D. R., Matsumoto, K., Lucarelli, E. & Thiele, C. J. Induction of TrkB by retinoic acid mediates biologic responsiveness to BDNF and differentiation of human neuroblastoma cells. Eukaryotic Signal Transduction Group. Neuron 11, 321–331 (1993).
pubmed: 8394722
doi: 10.1016/0896-6273(93)90187-V
Murmann, A. E. et al. Small interfering RNAs based on huntingtin trinucleotide repeats are highly toxic to cancer cells. EMBO Rep. 19, e45336 (2018).
pubmed: 29440125
pmcid: 5836092
doi: 10.15252/embr.201745336
Putzbach, W. et al. CD95/Fas ligand mRNA is toxic to cells. eLife 7, e38621 (2018).
pubmed: 30324908
pmcid: 6191286
doi: 10.7554/eLife.38621
Vaidyanathan, A. et al. Analysis of the contribution of 6mer seed toxicity to HIV-1 induced cytopathicity. J. Virol. 97, e0065223 (2023).
pubmed: 37310263
doi: 10.1128/jvi.00652-23
Tan, G. S. et al. Small molecule inhibition of RISC loading. ACS Chem. Biol. 7, 403–410 (2012).
pubmed: 22026461
doi: 10.1021/cb200253h
Murmann, A. E. et al. The length of uninterrupted CAG repeats in stem regions of repeat disease associated hairpins determines the amount of short CAG oligonucleotides that are toxic to cells through RNA interference. Cell Death Dis. 13, 1078 (2022).
pubmed: 36585400
pmcid: 9803637
doi: 10.1038/s41419-022-05494-1
Hallick, R. B., Chelm, B. K., Gray, P. W. & Orozco, E. M. Jr. Use of aurintricarboxylic acid as an inhibitor of nucleases during nucleic acid isolation. Nucleic Acids Res 4, 3055–3064 (1977).
pubmed: 410006
pmcid: 342634
doi: 10.1093/nar/4.9.3055
Loo, D. T. et al. Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc. Natl Acad. Sci. USA 90, 7951–7955 (1993).
pubmed: 8367446
pmcid: 47265
doi: 10.1073/pnas.90.17.7951
Shan, G. et al. A small molecule enhances RNA interference and promotes microRNA processing. Nat. Biotechnol. 26, 933–940 (2008).
pubmed: 18641635
pmcid: 2831467
doi: 10.1038/nbt.1481
Melo, S. et al. Small molecule enoxacin is a cancer-specific growth inhibitor that acts by enhancing TAR RNA-binding protein 2-mediated microRNA processing. Proc. Natl Acad. Sci. USA 108, 4394–4399 (2011).
pubmed: 21368194
pmcid: 3060242
doi: 10.1073/pnas.1014720108
Chmielarz, P. et al. Dicer and microRNAs protect adult dopamine neurons. Cell Death Dis. 8, e2813 (2017).
pubmed: 28542144
pmcid: 5520729
doi: 10.1038/cddis.2017.214
Gioia, U. et al. Pharmacological boost of DNA damage response and repair by enhanced biogenesis of DNA damage response RNAs. Sci. Rep. 9, 6460 (2019).
pubmed: 31015566
pmcid: 6478851
doi: 10.1038/s41598-019-42892-6
Francia, S. et al. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 488, 231–235 (2012).
pubmed: 22722852
pmcid: 3442236
doi: 10.1038/nature11179
Sola, M. et al. Tau affects P53 function and cell fate during the DNA damage response. Commun. Biol. 3, 245 (2020).
pubmed: 32427887
pmcid: 7237658
doi: 10.1038/s42003-020-0975-4
Pan, Y. et al. Dysregulation and diagnostic potential of microRNA in Alzheimer’s disease. J. Alzheimers Dis. 49, 1–12 (2016).
pubmed: 26484912
doi: 10.3233/JAD-150451
Samadian, M., Gholipour, M., Hajiesmaeili, M., Taheri, M. & Ghafouri-Fard, S. The Eminent Role of microRNAs in the Pathogenesis of Alzheimer’s Disease. Front Aging Neurosci. 13, 641080 (2021).
pubmed: 33790780
pmcid: 8005705
doi: 10.3389/fnagi.2021.641080
Flores, O., Kennedy, E. M., Skalsky, R. L. & Cullen, B. R. Differential RISC association of endogenous human microRNAs predicts their inhibitory potential. Nucleic Acids Res 42, 4629–4639 (2014).
pubmed: 24464996
pmcid: 3985621
doi: 10.1093/nar/gkt1393
Jiang, F. et al. Dicer-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev. 19, 1674–1679 (2005).
pubmed: 15985611
pmcid: 1176004
doi: 10.1101/gad.1334005
Bilen, J., Liu, N., Burnett, B. G., Pittman, R. N. & Bonini, N. M. MicroRNA pathways modulate polyglutamine-induced neurodegeneration. Mol. Cell 24, 157–163 (2006).
pubmed: 17018300
doi: 10.1016/j.molcel.2006.07.030
Haramati, S. et al. miRNA malfunction causes spinal motor neuron disease. Proc. Natl Acad. Sci. USA 107, 13111–13116 (2010).
pubmed: 20616011
pmcid: 2919953
doi: 10.1073/pnas.1006151107
Schaefer, A. et al. Argonaute 2 in dopamine 2 receptor-expressing neurons regulates cocaine addiction. J. Exp. Med 207, 1843–1851 (2010).
pubmed: 20643829
pmcid: 2931161
doi: 10.1084/jem.20100451
Bailey, R. R. & Peddie, B. A. Enoxacin for the treatment of urinary tract infection. N. Z. Med J. 98, 286–288 (1985).
pubmed: 3857511
Emde, A. et al. Dysregulated miRNA biogenesis downstream of cellular stress and ALS-causing mutations: a new mechanism for ALS. EMBO J. 34, 2633–2651 (2015).
pubmed: 26330466
pmcid: 4641530
doi: 10.15252/embj.201490493
Wu, W., Lee, I., Spratt, H., Fang, X. & Bao, X. tRNA-Derived Fragments in Alzheimer’s Disease: Implications for New Disease Biomarkers and Neuropathological Mechanisms. J. Alzheimers Dis. 79, 793–806 (2021).
pubmed: 33337366
pmcid: 8485948
doi: 10.3233/JAD-200917
Wiesen, J. L. & Tomasi, T. B. Dicer is regulated by cellular stresses and interferons. Mol. Immunol. 46, 1222–1228 (2009).
pubmed: 19118902
doi: 10.1016/j.molimm.2008.11.012
Machitani, M. et al. Type I Interferons Impede Short Hairpin RNA-Mediated RNAi via Inhibition of Dicer-Mediated Processing to Small Interfering RNA. Mol. Ther. Nucleic Acids 6, 173–182 (2017).
pubmed: 28325284
doi: 10.1016/j.omtn.2016.12.007
Yang, Q. et al. Stress induces p38 MAPK-mediated phosphorylation and inhibition of Drosha-dependent cell survival. Mol. Cell 57, 721–734 (2015).
pubmed: 25699712
pmcid: 4502444
doi: 10.1016/j.molcel.2015.01.004
Xu, H. et al. p38 MAPK-mediated loss of nuclear RNase III enzyme Drosha underlies amyloid beta-induced neuronal stress in Alzheimer’s disease. Aging Cell 20, e13434 (2021).
pubmed: 34528746
pmcid: 8521488
doi: 10.1111/acel.13434
Goel, P. et al. Neuronal cell death mechanisms in Alzheimer’s disease: An insight. Front. Mol. Neurosci. 15, 937133 (2022).
pubmed: 36090249
pmcid: 9454331
doi: 10.3389/fnmol.2022.937133
Zott, B., Busche, M. A., Sperling, R. A. & Konnerth, A. What Happens with the Circuit in Alzheimer’s Disease in Mice and Humans? Annu Rev. Neurosci. 41, 277–297 (2018).
pubmed: 29986165
pmcid: 6571139
doi: 10.1146/annurev-neuro-080317-061725
Hengst, U., Cox, L. J., Macosko, E. Z. & Jaffrey, S. R. Functional and selective RNA interference in developing axons and growth cones. J. Neurosci. 26, 5727–5732 (2006).
pubmed: 16723529
pmcid: 6675254
doi: 10.1523/JNEUROSCI.5229-05.2006
Soto-Palma, C., Niedernhofer, L. J., Faulk, C. D. & Dong, X. Epigenetics, DNA damage, and aging. J. Clin. Invest. 132, e158446 (2022).
Balendra, R. & Isaacs, A. M. C9orf72-mediated ALS and FTD: multiple pathways to disease. Nat. Rev. Neurol. 14, 544–558 (2018).
pubmed: 30120348
pmcid: 6417666
doi: 10.1038/s41582-018-0047-2
Moujalled, D., Strasser, A. & Liddell, J. R. Molecular mechanisms of cell death in neurological diseases. Cell Death Differ. 28, 2029–2044 (2021).
pubmed: 34099897
pmcid: 8257776
doi: 10.1038/s41418-021-00814-y
Johnson, E. C. B. et al. Large-scale proteomic analysis of Alzheimer’s disease brain and cerebrospinal fluid reveals early changes in energy metabolism associated with microglia and astrocyte activation. Nat. Med 26, 769–780 (2020).
pubmed: 32284590
pmcid: 7405761
doi: 10.1038/s41591-020-0815-6
Johnson, E. C. B. et al. Large-scale deep multi-layer analysis of Alzheimer’s disease brain reveals strong proteomic disease-related changes not observed at the RNA level. Nat. Neurosci. 25, 213–225 (2022).
pubmed: 35115731
pmcid: 8825285
doi: 10.1038/s41593-021-00999-y
Bertram, L. & Tanzi, R. E. Alzheimer disease risk genes: 29 and counting. Nat. Rev. Neurol. 15, 191–192 (2019).
pubmed: 30833695
doi: 10.1038/s41582-019-0158-4
Crist, A. M. et al. Transcriptomic analysis to identify genes associated with selective hippocampal vulnerability in Alzheimer’s disease. Nat. Commun. 12, 2311 (2021).
pubmed: 33875655
pmcid: 8055900
doi: 10.1038/s41467-021-22399-3
Khachaturian, A. S. et al. Future prospects and challenges for Alzheimer’s disease drug development in the era of the NIA-AA Research Framework. Alzheimers Dement 14, 532–534 (2018).
pubmed: 29653605
doi: 10.1016/j.jalz.2018.03.003
Hyman, B. T. et al. National Institute on Aging-Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease. Alzheimers Dement 8, 1–13 (2012).
pubmed: 22265587
pmcid: 3266529
doi: 10.1016/j.jalz.2011.10.007
Fa, M. et al. Preparation of oligomeric beta-amyloid 1-42 and induction of synaptic plasticity impairment on hippocampal slices. J. Vis. Exp. 41, 1884 (2010).
Stine, W. B., Jungbauer, L., Yu, C. & LaDu, M. J. Preparing synthetic Abeta in different aggregation states. Methods Mol. Biol. 670, 13–32 (2011).
pubmed: 20967580
pmcid: 3752843
doi: 10.1007/978-1-60761-744-0_2
Krishtal, J., Metsla, K., Bragina, O., Tõugu, V. & Palumaa, P. Toxicity of Amyloid-β Peptides Varies Depending on Differentiation Route of SH-SY5Y Cells. J. Alzheimers Dis. 71, 879–887 (2019).
pubmed: 31450506
doi: 10.3233/JAD-190705
Encinas, M. et al. Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J. Neurochem 75, 991–1003 (2000).
pubmed: 10936180
doi: 10.1046/j.1471-4159.2000.0750991.x
Tagai, N., Tanaka, A., Sato, A., Uchiumi, F. & Tanuma, S. I. Low Levels of Brain-Derived Neurotrophic Factor Trigger Self-aggregated Amyloid β-Induced Neuronal Cell Death in an Alzheimer’s Cell Model. Biol. Pharm. Bull. 43, 1073–1080 (2020).
pubmed: 32612070
doi: 10.1248/bpb.b20-00082
Wadhwani, A. R., Affaneh, A., Van Gulden, S. & Kessler, J. A. Neuronal apolipoprotein E4 increases cell death and phosphorylated tau release in alzheimer disease. Ann. Neurol. 85, 726–739 (2019).
pubmed: 30840313
pmcid: 8123085
doi: 10.1002/ana.25455
Zhang, Y. et al. Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78, 785–798 (2013).
pubmed: 23764284
pmcid: 3751803
doi: 10.1016/j.neuron.2013.05.029
Mazzulli, J. R., Zunke, F., Isacson, O., Studer, L. & Krainc, D. alpha-Synuclein-induced lysosomal dysfunction occurs through disruptions in protein trafficking in human midbrain synucleinopathy models. Proc. Natl Acad. Sci. USA 113, 1931–1936 (2016).
pubmed: 26839413
pmcid: 4763774
doi: 10.1073/pnas.1520335113
Hauptmann, J. et al. Biochemical isolation of Argonaute protein complexes by Ago-APP. Proc. Natl Acad. Sci. USA 112, 11841–11845 (2015).
pubmed: 26351695
pmcid: 4586862
doi: 10.1073/pnas.1506116112
Hafner, M. et al. Barcoded cDNA library preparation for small RNA profiling by next-generation sequencing. Methods 58, 164–170 (2012).
pubmed: 22885844
pmcid: 3508525
doi: 10.1016/j.ymeth.2012.07.030
Patel, N. et al. MicroRNAs can regulate human APP levels. Mol. Neurodegener. 3, 10 (2008).
pubmed: 18684319
pmcid: 2529281
doi: 10.1186/1750-1326-3-10