MicroRNA-153 Physiologically Inhibits Expression of Amyloid-β Precursor Protein in Cultured Human Fetal Brain Cells and Is Dysregulated in a Subset of Alzheimer Disease Patients

Long, Justin M.; Ray, Balmiki; Lahiri, Debomoy K.

doi:10.1074/jbc.m112.366336

Cited by 198Alzheimer's disease research and treatmentsMicroRNA in disease regulationNeuroinflammation and Neurodegeneration Mechanisms

MicroRNA-153 Physiologically Inhibits Expression of Amyloid-β Precursor Protein in Cultured Human Fetal Brain Cells and Is Dysregulated in a Subset of Alzheimer Disease Patients

Open access

Long, Justin M., Ray, Balmiki, Lahiri, Debomoy K.·2012·Journal of Biological Chemistry

DOI 10.1074/jbc.m112.366336PMC PMC3438960

Open this paper in CoChat — free account

Abstract

Regulation of amyloid-β (Aβ) precursor protein (APP) expression is complex. MicroRNAs (miRNAs) are expected to participate in the molecular network that controls this process. The composition of this network is, however, still undefined. Elucidating the complement of miRNAs that regulate APP expression should reveal novel drug targets capable of modulating Aβ production in AD. Here, we investigated the contribution of miR-153 to this regulatory network. A miR-153 target site within the APP 3'-untranslated region (3'-UTR) was predicted by several bioinformatic algorithms. We found that miR-153 significantly reduced reporter expression when co-transfected with an APP 3'-UTR reporter construct. Mutation of the predicted miR-153 target site eliminated this reporter response. miR-153 delivery in both HeLa cells and primary human fetal brain cultures significantly reduced APP expression. Delivery of a miR-153 antisense inhibitor to human fetal brain cultures significantly elevated APP expression. miR-153 delivery also reduced expression of the APP paralog APLP2. High functional redundancy between APP and APLP2 suggests that miR-153 may target biological pathways in which they both function. Interestingly, in a subset of human AD brain specimens with moderate AD pathology, miR-153 levels were reduced. This same subset also exhibited elevated APP levels relative to control specimens. Therefore, endogenous miR-153 inhibits expression of APP in human neurons by specifically interacting with the APP 3'-UTR. This regulatory interaction may have relevance to AD etiology, where low miR-153 levels may drive increased APP expression in a subset of AD patients.

Integrity signals

Registry

Crossref · 10.1074/jbc.m112.366336

Cites

94 of 94 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

miRNAs are abundantly expressed in the brain, and miRNA dysfunction contributes to neurological diseases.
“miRNAs have been shown to be abundantly expressed in the brain, and miRNA dysfunction contributes to neurological diseases.22,23”
From Microglia secrete miR-146a-5p-containing exosomes to regulate neurogenesis in depression (2022) · cites this paper as [22]
Earlier reviews have largely focused on global miRNA expression shifts in AD brain tissue, therapeutic miRNA candidates, or body-fluid biomarker signatures, but do not present how miRNA dysfunction propagates across interacting CNS cell types.
“Earlier reviews have largely focused on global miRNA expression shifts in AD brain tissue, therapeutic miRNA candidates, or body-fluid biomarker signatures (Li et al., 2024; Long et al., 2012; Salta and De Strooper, 2017; Samadian et al., 2021; Walgrave et al., 2021b; Wei et al., 2020; Yoon et al., 2022). Although these approaches are valuable, they do not present how miRNA dysfunction propagates”
From Cell-specific MicroRNA networks orchestrate the pathogenesis of Alzheimer’s disease (2026) · cites this paper as Long et al., 2012

MicroRNAs: Target Recognition and Regulatory Functions
Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.01.002 · Cited by 20,068 · see citing works
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002) · Genome Biology · doi:10.1186/gb-2002-3-7-research0034 · Cited by 20,038 · see citing works
Neuropathological stageing of Alzheimer-related changes.
Braak, H., & Braak, E. (1991) · Acta Neuropathologica · doi:10.1007/bf00308809 · Cited by 16,123 · see citing works
The Amyloid Hypothesis of Alzheimer’s Disease: Progress and Problems on the Road to Therapeutics
Hardy, J., & Selkoe, D. J. (2002) · Science · doi:10.1126/science.1072994 · Cited by 13,864 · see citing works
Conserved Seed Pairing, Often Flanked by Adenosines, Indicates that Thousands of Human Genes are MicroRNA Targets
Lewis, B. P., Burge, C. B., & Bartel, D. P. (2005) · Cell · doi:10.1016/j.cell.2004.12.035 · Cited by 11,855 · see citing works
Most mammalian mRNAs are conserved targets of microRNAs
Friedman, R. C., Farh, K. K.-H., Burge, C. B., & Bartel, D. P. (2009) · Genome Research · doi:10.1101/gr.082701.108 · Cited by 8,462 · see citing works
Untitled work
(2008) · doi:10.1038/nrg2290 · Cited by 5,199 · see citing works
Combinatorial microRNA target predictions
Krek, A., Grün, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., et al. (2005) · Nature Genetics · doi:10.1038/ng1536 · Cited by 4,603 · see citing works
Prediction of Mammalian MicroRNA Targets
Lewis, B. P., Shih, I.-H., Jones-Rhoades, M. W., Bartel, D. P., & Burge, C. B. (2003) · Cell · doi:10.1016/s0092-8674(03)01018-3 · Cited by 4,333 · see citing works
qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., & Vandesompele, J. (2007) · Genome Biology · doi:10.1186/gb-2007-8-2-r19 · Cited by 4,023 · see citing works
Mammalian microRNAs predominantly act to decrease target mRNA levels
Guo, H., Ingolia, N. T., Weissman, J. S., & Bartel, D. P. (2010) · Nature · doi:10.1038/nature09267 · Cited by 3,886 · see citing works
Human MicroRNA Targets
John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., & Marks, D. S. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020363 · Cited by 3,796 · see citing works
MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing
Grimson, A., Farh, K. K.-H., Johnston, W. K., Garrett-Engele, P., Lim, L. P., & Bartel, D. P. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.06.017 · Cited by 3,766 · see citing works
CNS stem cells express a new class of intermediate filament protein
Lendahl, U., Zimmerman, L. B., & McKay, R. D. G. (1990) · Cell · doi:10.1016/0092-8674(90)90662-x · Cited by 3,164 · see citing works
The microRNA.org resource: targets and expression
Betel, D., Wilson, M. T., Gabow, A. P., Marks, D. S., & Sander, C. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm995 · Cited by 2,490 · see citing works
The Glial Nature of Embryonic and Adult Neural Stem Cells
Kriegstein, A., & Alvarez-Buylla, A. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135600 · Cited by 2,475 · see citing works
The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics
Karran, E., Mercken, M., & Strooper, B. D. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3505 · Cited by 2,188 · cited 1× · see citing works
“Alzheimer disease (AD),(2) the most common form of dementia (1), is thought to arise in part from excess accumulation of the amyloid- peptide (A ) (2, 3).”
Background
A Pattern-Based Method for the Identification of MicroRNA Binding Sites and Their Corresponding Heteroduplexes
Miranda, K. C., Huynh, T., Tay, Y., Ang, Y.-S., Tam, W.-L., Thomson, A. M., Lim, B., & Rigoutsos, I. (2006) · Cell · doi:10.1016/j.cell.2006.07.031 · Cited by 1,739 · see citing works
Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies.
(1998) · Europe PMC (PubMed Central) · Cited by 1,594 · see citing works
Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites
Betel, D., Koppal, A., Agius, P., Sander, C., & Leslie, C. (2010) · Genome Biology · doi:10.1186/gb-2010-11-8-r90 · Cited by 1,592 · see citing works
Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation
Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., & Ambros, V. (2004) · Genome Biology · doi:10.1186/gb-2004-5-3-r13 · Cited by 1,578 · see citing works
APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy
Rovelet‐Lecrux, A., Hannequin, D., Raux, G., Meur, N. L., Laquerrière, A., Vital, A., Dumanchin‐Njock, C., Feuillette, S., Brice, A., Vercelletto, M., et al. (2005) · Nature Genetics · doi:10.1038/ng1718 · Cited by 1,249 · see citing works
Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/β-secretase expression
Hébert, S. S., Horré, K., Nicolaï, L., Papadopoulou, A. S., Mandemakers, W., Silahtaroglu, A. N., Kauppinen, S., Delacourte, A., & De Strooper, B. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710263105 · Cited by 1,183 · see citing works
Amyloid Precursor Protein Trafficking, Processing, and Function
Thinakaran, G., & Koo, E. H. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.r800019200 · Cited by 1,141 · see citing works
The Lewy body variant of Alzheimer's disease: A clinical and pathologic entity
Hansen, L., Salmon, D., Galasko, D., Masliah, E., Katzman, R., DeTeresa, R., Thal, L., Pay, M. M., Hofstetter, R., Klauber, M., et al. (1990) · Neurology · doi:10.1212/wnl.40.1.1 · Cited by 1,068 · see citing works
Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways
Cogswell, J. P., Ward, J., Taylor, I. A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., et al. (2008) · Journal of Alzheimer s Disease · doi:10.3233/jad-2008-14103 · Cited by 943 · see citing works
2011 Alzheimer's disease facts and figures
Alzheimer's Association (2011) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2011.02.004 · Cited by 914 · see citing works
Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs
Garcia, D. M., Baek, D., Shin, C., Bell, G. W., Grimson, A., & Bartel, D. P. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2115 · Cited by 859 · see citing works
Impaired mitochondrial dynamics and abnormal interaction of amyloid beta with mitochondrial protein Drp1 in neurons from patients with Alzheimer's disease: implications for neuronal damage
Mańczak, M., Calkins, M. J., & Reddy, P. H. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr139 · Cited by 830 · see citing works
The Expression of MicroRNA miR-107 Decreases Early in Alzheimer's Disease and May Accelerate Disease Progression through Regulation of β-Site Amyloid Precursor Protein-Cleaving Enzyme 1
Wang, W., Rajeev, B. W., Stromberg, A. J., Ren, N., Tang, G., Huang, Q., Rigoutsos, I., & Nelson, P. T. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5065-07.2008 · Cited by 827 · see citing works
Lewy Bodies in Alzheimer's Disease: A Neuropathological Review of 145 Cases Using α‐Synuclein Immunohistochemistry
Hamilton, R. L. (2000) · Brain Pathology · doi:10.1111/j.1750-3639.2000.tb00269.x · Cited by 754 · see citing works
Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus
Lukiw, W. J. (2007) · Neuroreport · doi:10.1097/wnr.0b013e3280148e8b · Cited by 662 · see citing works
Amyloid A4 Protein and Its Precursor in Down's Syndrome and Alzheimer's Disease
Rumble, B. A., Retallack, R. W., Hilbich, C., Simms, G., Multhaup, G., Martins, R. N., Hockey, A., Montgomery, P., Beyreuther, K. T., & Masters, C. L. (1989) · New England Journal of Medicine · doi:10.1056/nejm198906013202203 · Cited by 652 · see citing works
Neuropathology and Cognitive Impairment in Alzheimer Disease: A Complex but Coherent Relationship
Nelson, P. T., Braak, H., & Markesbery, W. R. (2009) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3181919a48 · Cited by 643 · see citing works
The RNA-induced Silencing Complex: A Versatile Gene-silencing Machine
Pratt, A. J., & MacRae, I. J. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.r900012200 · Cited by 602 · see citing works
Characterization of MicroRNA Expression Levels and Their Biological Correlates in Human Cancer Cell Lines
Gaur, A., Jewell, D. A., Liang, Y., Ridzon, D., Moore, J. H., Chen, C., Ambros, V. R., & Israel, M. A. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2698 · Cited by 593 · see citing works
Synergistic Interactions between Aβ, Tau, and α-Synuclein: Acceleration of Neuropathology and Cognitive Decline
Clinton, L. K., Blurton-Jones, M., Myczek, K., Trojanowski, J. Q., & LaFerla, F. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.0490-10.2010 · Cited by 576 · see citing works
An iron-responsive element type II in the 5'-untranslated region of the Alzheimer's amyloid precursor protein transcript
Rogers, J. T., Randall, J. D., Cahill, C. M., Eder, P. S., Huang, X., Gunshin, H., Leiter, L., McPhee, J., Sarang, S. S., Utsuki, T., et al. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207435200 · Cited by 551 · see citing works
Mice with Combined Gene Knock-Outs Reveal Essential and Partially Redundant Functions of Amyloid Precursor Protein Family Members
Heber, S., Herms, J. W., Gajic, V., Hainfellner, J. A., Aguzzi, A., Rülicke, T., Kretzschmar, H. A., von Koch, C., Sisodia, S. S., Tremml, P., et al. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-07951.2000 · Cited by 495 · see citing works
Post-transcriptional Regulation of α-Synuclein Expression by mir-7 and mir-153
Doxakis, E. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.086827 · Cited by 485 · see citing works
MicroRNA regulation of Alzheimer's Amyloid precursor protein expression
Hébert, S. S., Horré, K., Nicolaï, L., Bergmans, B., Papadopoulou, A. S., Delacourte, A., & De Strooper, B. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.11.009 · Cited by 436 · see citing works
DIANA-microT web server: elucidating microRNA functions through target prediction
Maragkakis, M., Reczko, M., Simossis, V., Alexiou, P., Papadopoulos, G. L., Dalamagas, T., Giannopoulos, G., Goumas, G., Koukis, E., Kourtis, K., et al. (2009) · Nucleic Acids Res. · doi:10.1093/nar/gkp292 · Cited by 405 · see citing works
Astroglia in dementia and Alzheimer's disease
Rodriguez, J. J., Olabarria, M., Chvátal, A., & Verkhratsky, A. (2008) · Cell Death and Differentiation · doi:10.1038/cdd.2008.172 · Cited by 396 · see citing works
Joint Genome-Wide Profiling of miRNA and mRNA Expression in Alzheimer's Disease Cortex Reveals Altered miRNA Regulation
Nunez-Iglesias, J., Liu, C.-C., Morgan, T. E., Finch, C. E., & Zhou, X. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008898 · Cited by 320 · see citing works
MicroRNAs in Alzheimer’s Disease
Wang, M., Qin, L., & Tang, B. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00153 · Cited by 307 · see citing works
Cognitive decline is faster in Lewy body variant than in Alzheimer's disease
Olichney, J., Galasko, D. R., Salmon, D. P., Hofstetter, C. R., Hansen, L. A., Katzman, R., & Thal, L. J. (1998) · Neurology · doi:10.1212/wnl.51.2.351 · Cited by 305 · see citing works
Clinicopathologic Correlations in a Large Alzheimer Disease Center Autopsy Cohort: Neuritic Plaques and Neurofibrillary Tangles "Do Count" When Staging Disease Severity
Nelson, P. T., Jicha, G. A., Schmitt, F. A., Liu, H., Davis, D. G., Mendiondo, M. S., Abner, E. L., & Markesbery, W. R. (2007) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/nen.0b013e31815c5efb · Cited by 292 · see citing works
Translation of the Alzheimer Amyloid Precursor Protein mRNA Is Up-regulated by Interleukin-1 through 5′-Untranslated Region Sequences
Rogers, J. T., Leiter, L. M., McPhee, J., Cahill, C. M., Zhan, S.-S., Potter, H., & Nilsson, L. N. G. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.10.6421 · Cited by 290 · see citing works
Cognitive differences in dementia patients with autopsy-verified AD, Lewy body pathology, or both
Kraybill, M., Larson, E. B., Tsuang, D. W., Teri, L. L., McCormick, W. C., Bowen, J. D., Kukull, W. A., Leverenz, J. B., & Cherrier, M. M. (2005) · Neurology · doi:10.1212/01.wnl.0000165987.89198.65 · Cited by 286 · see citing works
MicroRNA Expression in Alzheimer Blood Mononuclear Cells
Schipper, H. M., Maes, O. C., Chertkow, H. M., & Wang, E. (2007) · Gene Regulation and Systems Biology · doi:10.4137/grsb.s361 · Cited by 244 · see citing works
MicroRNA-101 Regulates Amyloid Precursor Protein Expression in Hippocampal Neurons
Vilardo, E., Barbato, C., Ciotti, M., Cogoni, C., & Ruberti, F. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.112664 · Cited by 238 · see citing works
The Lewy-Body Variant of Alzheimer's Disease
Förstl, H., Burns, A. S., Luthert, P. J., Cairns, N. J., & Levy, R. (1993) · The British Journal of Psychiatry · doi:10.1192/bjp.162.3.385 · Cited by 221 · see citing works
In vivo regulation of amyloid precursor protein neuronal splicing by microRNAs
Smith, P. Y., Hashimi, A. A., Girard, J., Delay, C., & Hébert, S. S. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.07097.x · Cited by 209 · see citing works
MicroRNA-101 downregulates Alzheimer’s amyloid-β precursor protein levels in human cell cultures and is differentially expressed
Long, J. M., & Lahiri, D. K. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.12.053 · Cited by 209 · see citing works
MicroRNAs can regulate human APP levels
Patel, N., Hoang, D. M., Miller, N., Ansaloni, S., Huang, Q., Rogers, J. T., Lee, J. C., & Saunders, A. J. (2008) · Molecular Neurodegeneration · doi:10.1186/1750-1326-3-10 · Cited by 205 · see citing works
MicroRNA-16 targets amyloid precursor protein to potentially modulate Alzheimer's-associated pathogenesis in SAMP8 mice
Liu, W., Chang, L., Zhu, J.-X., Shu, P., Yin, B., Gong, Y., Qiang, B., Yuan, J., & Peng, X. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.04.034 · Cited by 188 · see citing works
Promoter Mutations That Increase Amyloid Precursor-Protein Expression Are Associated with Alzheimer Disease
Theuns, J., Brouwers, N., Engelborghs, S., Sleegers, K., Bogaerts, V., Corsmit, E., Pooter, T. D., van Duijn, C. M., Deyn, P. P. D., & Broeckhoven, C. V. (2006) · The American Journal of Human Genetics · doi:10.1086/504044 · Cited by 187 · see citing works
MicroRNAs in Alzheimer's disease
Delay, C., Mandemakers, W., & Hébert, S. S. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.01.003 · Cited by 185 · see citing works
Copper Depletion Down-regulates Expression of the Alzheimer's Disease Amyloid-β Precursor Protein Gene
Bellingham, S. A., Lahiri, D. K., Maloney, B., Fontaine, S. L., Multhaup, G., & Camakaris, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400805200 · Cited by 165 · see citing works
DIANA-microT Web server upgrade supports Fly and Worm miRNA target prediction and bibliographic miRNA to disease association
Maragkakis, M., Vergoulis, T., Alexiou, P., Reczko, M., Plomaritou, K., Gousis, M., Kourtis, K., Koziris, N., Dalamagas, T., & Hatzigeorgiou, A. (2011) · Nucleic Acids Res. · doi:10.1093/nar/gkr294 · Cited by 149 · see citing works
Transforming Growth Factor-β1 Potentiates Amyloid-β Generation in Astrocytes and in Transgenic Mice
Lesné, S., Docagne, F., Gabriel, C., Liot, G., Lahiri, D. K., Buée, L., Plawinski, L., Delacourte, A., MacKenzie, E. T., Buisson, A., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300819200 · Cited by 142 · see citing works
Alzheimer-specific variants in the 3'UTR of Amyloid precursor protein affect microRNA function
Delay, C., Calon, F., Mathews, P. M., & Hébert, S. S. (2011) · Molecular Neurodegeneration · doi:10.1186/1750-1326-6-70 · Cited by 130 · see citing works
hnRNP C increases amyloid precursor protein (APP) production by stabilizing APP mRNA
Rajagopalan, L. E., Westmark, C. J., Jarzembowski, J. A., & Malter, J. S. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.14.3418 · Cited by 126 · see citing works
Deregulation of miR‐519a, 153, and 485‐5p and its clinicopathological relevance in ovarian epithelial tumours
Kim, T., Kim, Y. K., Kwon, Y.-D., Heo, J. H., Kang, H., Kim, G., & An, H. J. (2010) · Histopathology · doi:10.1111/j.1365-2559.2010.03686.x · Cited by 123 · see citing works
Downregulations of B‐cell lymphoma 2 and myeloid cell leukemia sequence 1 by microRNA 153 induce apoptosis in a glioblastoma cell line DBTRG‐05MG
Xu, J., Liao, X., & Wong, C. (2009) · International Journal of Cancer · doi:10.1002/ijc.24823 · Cited by 116 · see citing works
Comparison of Lewy body variant of Alzheimer’s disease with pure Alzheimer’s disease
Heyman, A., Fillenbaum, G. G., Gearing, M., Mirra, S. S., Welsh-Bohmer, K. A., Peterson, B. L., & Pieper, C. F. (1999) · Neurology · doi:10.1212/wnl.52.9.1839 · Cited by 109 · see citing works
MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2
Liang, C., Zhu, H., Xu, Y., Huang, L. J., Ma, C., Deng, W., Liu, Y. M., & Qin, C. (2011) · Brain Research · doi:10.1016/j.brainres.2011.10.051 · Cited by 109 · see citing works
Comprehensive microRNA analysis in bleomycin-induced pulmonary fibrosis identifies multiple sites of molecular regulation
Xie, T., Liang, J., Guo, R., Liu, N., Noble, P. W., & Jiang, D. (2011) · Physiological Genomics · doi:10.1152/physiolgenomics.00222.2010 · Cited by 107 · see citing works
miR-20a promotes proliferation and invasion by targeting APP in human ovarian cancer cells
Fan, X., Liu, Y., Jiang, J., Ma, Z., Wu, H., Liu, T., Liu, M., Li, X., & Tang, H. (2010) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmq026 · Cited by 95 · see citing works
Amyloid precursor protein mRNA stability is controlled by a 29-base element in the 3'-untranslated region.
Zaidi, S. H., & Malter, J. S. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)51039-0 · Cited by 94 · see citing works
The promoter activity of the gene encoding Alzheimer β-amyloid precursor protein (APP) is regulated by two blocks of upstream sequences
Lahiri, D. K., & Robakis, N. K. R. K. (1991) · Molecular Brain Research · doi:10.1016/0169-328x(91)90009-m · Cited by 94 · see citing works
MicroRNA networks surrounding APP and amyloid-β metabolism — Implications for Alzheimer's disease
Schönrock, N., Matamales, M., Ittner, L. M., & Götz, J. (2011) · Experimental Neurology · doi:10.1016/j.expneurol.2011.11.013 · Cited by 93 · see citing works
The expression of the amyloid precursor protein (APP) is regulated by two GC-elements in the promoter
Pollwein, P., Masters, C. L., & Beyreuther, K. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.1.63 · Cited by 91 · see citing works
Role of cytokines in the gene expression of amyloid β–protein precursor: Identification of a 5'-UTR-Binding nuclear factor and its implications in Alzheimer's disease
Lahiri, D. K., Chen, D., Vivien, D., Ge, Y.-W., Greig, N. H., & Rogers, J. T. (2003) · Journal of Alzheimer s Disease · doi:10.3233/jad-2003-5203 · Cited by 81 · see citing works
The amyloid beta-protein precursor promoter. A region essential for transcriptional activity contains a nuclear factor binding domain.
Quitschke, W. W., & Goldgaber, D. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)41934-5 · Cited by 78 · see citing works
A population of human brain parenchymal cells express markers of glial, neuronal and early neural cells and differentiate into cells of neuronal and glial lineages
Rieske, P., Azizi, S. A., Augelli, B. J., Gaughan, J., & Krynska, B. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05254.x · Cited by 61 · see citing works
Chromatin‐modifying drugs induce miRNA‐153 expression to suppress Irs‐2 in glioblastoma cell lines
Xu, J., Liao, X., Lü, N., Liu, W., & Wong, C. (2011) · International Journal of Cancer · doi:10.1002/ijc.25917 · Cited by 59 · see citing works
Multiple proteins interact at a unique cis-element in the 3'-untranslated region of amyloid precursor protein mRNA.
Zaidi, S. H., Denman, R. B., & Malter, J. S. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)51038-9 · Cited by 57 · see citing works
Alternative polyadenylation of the amyloid protein precursor mRNA regulates translation.
de Sauvage, F. J., Kruys, V., Marinx, O., Huez, G. A., & Octave, J. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05382.x · Cited by 57 · see citing works
Amyloid Precursor Protein Revisited
Guo, Q.-X., Li, H., Gaddam, S. S., Justice, N., Robertson, C., & Zheng, H. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.315051 · Cited by 48 · see citing works
Characterization of the APP proximal promoter and 5′‐untranslated regions: identification of cell‐type specific domains and implications in APP gene expression and Alzheimer's disease
Lahiri, D. K., Ge, Y., & Maloney, B. (2005) · The FASEB Journal · doi:10.1096/fj.04-2900fje · Cited by 43 · see citing works
Functional identification of the promoter of the gene encoding the Rhesus monkey β-amyloid precursor protein
Song, W., & Lahiri, D. K. (1998) · Gene · doi:10.1016/s0378-1119(98)00340-0 · Cited by 43 · see citing works
Advances in microRNA experimental approaches to study physiological regulation of gene products implicated in CNS disorders
Long, J. M., & Lahiri, D. K. (2012) · Experimental Neurology · doi:10.1016/j.expneurol.2011.12.043 · Cited by 42 · see citing works
Presence of a “CAGA box” in the APP gene unique to amyloid plaque‐forming species and absent in all APLP ‐1/2 genes: implications in Alzheimer's disease
Maloney, B., Ge, Y., Greig, N. H., & Lahiri, D. K. (2004) · The FASEB Journal · doi:10.1096/fj.03-1703fje · Cited by 42 · see citing works
Regulating amyloid precursor protein synthesis through an internal ribosomal entry site
Beaudoin, M. E., Poirel, V., & Krushel, L. A. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn792 · Cited by 40 · see citing works
Characterization of two APP gene promoter polymorphisms that appear to influence risk of late-onset Alzheimer's disease
Lahiri, D. K., Ge, Y., Maloney, B., Vrièze, F. W., & Hardy, J. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.11.005 · Cited by 39 · see citing works
Lewy Body Variant of Alzheimer's Disease: Selective Neocortical Loss of t-SNARE Proteins and Loss of MAP2 and α-Synuclein in Medial Temporal Lobe
Mukaetova‐Ladinska, E. B., Xuereb, J. H., García‐Sierra, F., Hurt, J., Gertz, H.-J., Hills, R., Brayne, C., Huppert, F. A., Paykel, E. S., McGee, M. A., et al. (2009) · The Scientific World JOURNAL · doi:10.1100/tsw.2009.151 · Cited by 36 · see citing works
A GG Nucleotide Sequence of the 3′ Untranslated Region of Amyloid Precursor Protein mRNA Plays a Key Role in the Regulation of Translation and the Binding of Proteins
Mbella, E. G. M., Bertrand, S., Huez, G. A., & Octave, J. N. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.13.4572-4579.2000 · Cited by 33 · see citing works
Molecular and immunocytochemical characterization of primary neuronal cultures from adult rat brain: Differential expression of neuronal and glial protein markers
Ray, B., Bailey, J. A., Sarkar, S., & Lahiri, D. K. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.08.018 · Cited by 32 · see citing works
Current Drug Targets for Modulating Alzheimer's Amyloid Precursor Protein: Role of Specific Micro-RNA Species
Long, J. M., & Lahiri, D. K. (2011) · Current Medicinal Chemistry · doi:10.2174/092986711796504592 · Cited by 31 · see citing works
Decoy mRNAs reduce β-amyloid precursor protein mRNA in neuronal cells
Westmark, P. R., Shin, H. C., Westmark, C. J., Soltaninassab, S. R., Reinke, E. K., & Malter, J. S. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.03.003 · Cited by 17 · see citing works
Cytosine methylation in miR-153 gene promoters increases the expression of holocarboxylase synthetase, thereby increasing the abundance of histone H4 biotinylation marks in HEK-293 human kidney cells
Bao, B., Rodrı́guez-Meléndez, R., & Zempleni, J. (2011) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2011.03.007 · Cited by 14 · see citing works
LEWY BODIES IN ALZHEIMER??S DISEASE
Pollanen, M. S., & Bergeron, C. (1988) · Alzheimer Disease & Associated Disorders · doi:10.1097/00002093-198802030-00096 · Cited by 4 · see citing works
Lewy Body Variant of Alzheimer's Disease
Morris, J. N. (1999) · Journal watch · doi:10.1056/jn199911010000008 · Cited by 4 · see citing works

Flagged first, then by citations

Sorted by citations

The epigenetics of aging and neurodegeneration
Lardenoije, R., Iatrou, A., Kenis, G., Kompotis, K., Steinbusch, H. W. M., Mastroeni, D., Coleman, P., Lemere, C. A., Hof, P. R., van den Hove, D. L. A., et al. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.05.002 · Cited by 381 · see citing works
Circulating miRNA Biomarkers for Alzheimer's Disease
Kumar, P., Dezső, Z., MacKenzie, C. J., Oestreicher, J., Agoulnik, S. I., Byrne, M., Bernier, F., Yanagimachi, M., Aoshima, K., & Oda, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069807 · Cited by 386 · see citing works
Systematic Review of miRNA as Biomarkers in Alzheimer’s Disease
Swarbrick, S., Wragg, N. M., Ghosh, S. K., & Stolzing, A. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1500-y · Cited by 353 · see citing works
Molecular Basis of Familial and Sporadic Alzheimer's Disease
Dorszewska, J., Prendecki, M., Oczkowska, A., Dezor, M., & Kozubski, W. P. (2016) · Current Alzheimer Research · doi:10.2174/1567205013666160314150501 · Cited by 329 · see citing works
MicroRNAs in Alzheimer’s Disease
Wang, M., Qin, L., & Tang, B. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00153 · Cited by 307 · see citing works
De-repression of FOXO3a death axis by microRNA-132 and -212 causes neuronal apoptosis in Alzheimer's disease
Wong, H. K., Veremeyko, T., Patel, N., Lemere, C. A., Walsh, D. M., Esau, C., Vanderburg, C. R., & Krichevsky, A. M. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt164 · Cited by 293 · see citing works
The amyloid precursor protein: A biochemical enigma in brain development, function and disease
Nalivaeva, N. N., & Turner, A. J. (2013) · FEBS Letters · doi:10.1016/j.febslet.2013.05.010 · Cited by 271 · see citing works
Microglia secrete miR-146a-5p-containing exosomes to regulate neurogenesis in depression
Fan, C., Li, Y., Lan, T., Wang, W., Long, Y., & Yu, S. Y. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2021.11.006 · Cited by 227 · see citing works
Brain microRNAs and insights into biological functions and therapeutic potential of brain enriched miRNA-128
Adlakha, Y. K., & Saini, N. (2014) · Molecular Cancer · doi:10.1186/1476-4598-13-33 · Cited by 213 · see citing works
Activation of the miR-34a-Mediated SIRT1/mTOR Signaling Pathway by Urolithin A Attenuates d-Galactose-Induced Brain Aging in Mice
Chen, P., Chen, F., Lei, J., Li, Q., & Zhou, B. (2019) · Neurotherapeutics · doi:10.1007/s13311-019-00753-0 · Cited by 208 · see citing works
Interplay between MicroRNAs and Oxidative Stress in Neurodegenerative Diseases
Konovalova, J., Gerasymchuk, D., Parkkinen, I., Chmielarz, P., & Domanskyi, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20236055 · Cited by 199 · see citing works
Cdk5 activity in the brain – multiple paths of regulation
Shah, K., & Lahiri, D. K. (2014) · Journal of Cell Science · doi:10.1242/jcs.147553 · Cited by 196 · see citing works
MicroRNAs and neurodegeneration: role and impact
Abe, M., & Bonini, N. M. (2013) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.08.013 · Cited by 190 · see citing works
Neurobiology of Alzheimer’s Disease: Integrated Molecular, Physiological, Anatomical, Biomarker, and Cognitive Dimensions
Raskin, J., Cummings, J. L., Hardy, J., Schuh, K. J., & Dean, R. A. (2015) · Current Alzheimer Research · doi:10.2174/1567205012666150701103107 · Cited by 190 · see citing works
MicroRNA-339-5p Down-regulates Protein Expression of β-Site Amyloid Precursor Protein-Cleaving Enzyme 1 (BACE1) in Human Primary Brain Cultures and Is Reduced in Brain Tissue Specimens of Alzheimer Disease Subjects
Long, J. M., Ray, B., & Lahiri, D. K. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.518241 · Cited by 187 · see citing works
Neuronal dark matter: the emerging role of microRNAs in neurodegeneration
Goodall, E. F., Heath, P. R., Bandmann, O., Kirby, J., & Shaw, P. J. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00178 · Cited by 187 · see citing works
Stress-induced changes in miRNA biogenesis and functioning
Olejniczak, M., Kotowska‐Zimmer, A., & Krzyżosiak, W. J. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2591-0 · Cited by 179 · see citing works
Modifications and Trafficking of APP in the Pathogenesis of Alzheimer’s Disease
Wang, X., Zhou, X., Li, G., Zhang, Y., Wu, Y., & Song, W. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00294 · Cited by 173 · see citing works
miR-7 and miR-153 protect neurons against MPP+-induced cell death via upregulation of mTOR pathway
Fragkouli, A., & Doxakis, E. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00182 · Cited by 147 · see citing works
Linking deregulation of non-coding RNA to the core pathophysiology of Alzheimer’s disease: An integrative review
Millan, M. J. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.03.004 · Cited by 146 · see citing works
Epigenetic mechanisms during ageing and neurogenesis as novel therapeutic avenues in human brain disorders
Delgado‐Morales, R., Agís‐Balboa, R. C., Esteller, M., & Berdasco, M. (2017) · Clinical Epigenetics · doi:10.1186/s13148-017-0365-z · Cited by 143 · see citing works
Novel upregulation of amyloid-β precursor protein (APP) by microRNA-346 via targeting of APP mRNA 5′-untranslated region: Implications in Alzheimer’s disease
Long, J. M., Maloney, B., Rogers, J. T., & Lahiri, D. K. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0266-3 · Cited by 141 · see citing works
MicroRNAs in Alzheimer’s Disease: Diagnostic Markers or Therapeutic Agents?
Angelucci, F., Čechová, K., Vališ, M., Kuča, K., Zhang, B., & Hort, J. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00665 · Cited by 141 · see citing works
The promise of microRNA-based therapies in Alzheimer’s disease: challenges and perspectives
Walgrave, H., Zhou, L., Strooper, B. D., & Salta, E. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00496-7 · Cited by 132 · see citing works
miRNAs: Key Players in Neurodegenerative Disorders and Epilepsy
Karnati, H. K., Panigrahi, M. K., Gutti, R. K., Greig, N. H., & Tamargo, I. A. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150395 · Cited by 125 · see citing works
A study of small RNAs from cerebral neocortex of pathology-verified Alzheimer’s disease, dementia with lewy bodies, hippocampal sclerosis, frontotemporal lobar dementia, and non-demented human controls
Hébert, S. S., Wang, W.-X., Zhu, Q., & Nelson, P. T. (2013) · Journal of Alzheimer's Disease · doi:10.3233/jad-122350 · Cited by 110 · see citing works
The Role of microRNAs in Alzheimer’s Disease and Their Therapeutic Potentials
Shaik, M. M., Tamargo, I. A., Abubakar, M. B., Kamal, M. A., Greig, N. H., & Gan, S. H. (2018) · Genes · doi:10.3390/genes9040174 · Cited by 114 · see citing works
Salivary microR‐153 and microR‐223 Levels as Potential Diagnostic Biomarkers of Idiopathic Parkinson's Disease
Cressatti, M., Juwara, L., Galindez, J. M., Velly, A. M., Nkurunziza, E. S., Marier, S., Canie, O., Gornistky, M., & Schipper, H. M. (2019) · Movement Disorders · doi:10.1002/mds.27935 · Cited by 112 · see citing works
The Regulation of microRNAs in Alzheimer's Disease
Kou, X., Chen, D., & Chen, N. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00288 · Cited by 112 · see citing works
Osthole decreases beta amyloid levels through up-regulation of miR-107 in Alzheimer’s disease
Jiao, Y., Kong, L., Yao, Y., Li, S., Tao, Z., Yan, Y., & Yang, J. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.04.046 · Cited by 104 · see citing works
Amyloid Beta and MicroRNAs in Alzheimer’s Disease
Amakiri, N., Kubosumi, A., Tran, J., & Reddy, P. H. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00430 · Cited by 107 · see citing works
MicroRNA-298 reduces levels of human amyloid-β precursor protein (APP), β-site APP-converting enzyme 1 (BACE1) and specific tau protein moieties
Chopra, N., Wang, R., Maloney, B., Nho, K. T., Beck, J. S., Pourshafie, N., Niculescu, A. B., Saykin, A. J., Rinaldi, C., Counts, S., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-019-0610-2 · Cited by 101 · see citing works
MicroRNAs in Alzheimer’s Disease: Function and Potential Applications as Diagnostic Biomarkers
Wei, W., Wang, Z.-Y., Ma, L.-N., Zhang, T.-T., Cao, Y., & Li, H. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00160 · Cited by 102 · see citing works
Environmental Enrichment Improves Cognitive Deficits, AD Hallmarks and Epigenetic Alterations Presented in 5xFAD Mouse Model
Griñán-Ferré, C., Izquierdo, V., Otero, E., Puigoriol-Illamola, D., Corpas, R., Sanfeliu, C., Ortuño-Sahagún, D., & Pallàs, M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00224 · Cited by 94 · see citing works
The neurobiology of non-coding RNAs and Alzheimer’s disease pathogenesis: Pathways, mechanisms and translational opportunities
Lauretti, E., Dabrowski, K. R., & Praticò, D. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101425 · Cited by 94 · see citing works
Nrf2 Pathway in Age-Related Neurological Disorders: Insights into MicroRNAs
Paladino, S., Conte, A., Caggiano, R., Pierantoni, G. M., & Faraonio, R. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000491465 · Cited by 92 · see citing works
Getting miRNA Therapeutics into the Target Cells for Neurodegenerative Diseases: A Mini-Review
Wen, M. M. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00129 · Cited by 89 · see citing works
Rivastigmine modifies the α-secretase pathway and potentially early Alzheimer’s disease
Ray, B., Maloney, B., Sambamurti, K., Karnati, H. K., Nelson, P. T., Greig, N. H., & Lahiri, D. K. (2020) · Translational Psychiatry · doi:10.1038/s41398-020-0709-x · Cited by 91 · see citing works
Lessons from a BACE1 inhibitor trial: Off‐site but not off base
Lahiri, D. K., Maloney, B., Long, J. M., & Greig, N. H. (2014) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.11.004 · Cited by 82 · see citing works
Early Life Stress and Epigenetics in Late-onset Alzheimer’s Dementia: A Systematic Review
Lemche, E. (2018) · Current Genomics · doi:10.2174/1389202919666171229145156 · Cited by 82 · see citing works
Functional microRNAs in Alzheimer’s disease and cancer: differential regulation of common mechanisms and pathway
Nudelman, K. N. H., Lahiri, D. K., Schneider, B. P., Foroud, T., & Saykin, A. J. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2012.00323 · Cited by 76 · see citing works
Studying micro RNA Function and Dysfunction in Alzheimer’s Disease
Lukiw, W. J., Андреева, Т. В., Grigorenko, A. P., & Rogaev, E. I. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2012.00327 · Cited by 75 · see citing works
Transcriptomics in Alzheimer’s Disease: Aspects and Challenges
Bagyinszky, E., Giau, V. V., & An, S. A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103517 · Cited by 75 · see citing works
Oxidative stress and pro-inflammatory cytokines may act as one of the signals for regulating microRNAs expression in Alzheimer’s disease
Prasad, K. N. (2016) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.12.003 · Cited by 71 · see citing works
MicroRNA in Alzheimer’s disease revisited: implications for major neuropathological mechanisms
Dehghani, R., Rahmani, F., & Rezaei, N. (2017) · Reviews in the Neurosciences · doi:10.1515/revneuro-2017-0042 · Cited by 72 · see citing works
The Eminent Role of microRNAs in the Pathogenesis of Alzheimer's Disease
Samadian, M. M., Gholipour, M., Hajiesmaeili, M., Taheri, M. N., & Ghafouri‐Fard, S. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.641080 · Cited by 70 · see citing works
SNHG1 promotes MPP+-induced cytotoxicity by regulating PTEN/AKT/mTOR signaling pathway in SH-SY5Y cells via sponging miR-153-3p
Zhao, J., Geng, L., Chen, Y., & Wu, C. (2020) · Biological Research · doi:10.1186/s40659-019-0267-y · Cited by 70 · see citing works
RNA Dynamics in Alzheimer’s Disease
Rybak‐Wolf, A., & Plass, M. (2021) · Molecules · doi:10.3390/molecules26175113 · Cited by 70 · see citing works
The Role of Non-coding RNAs in Alzheimer’s Disease: From Regulated Mechanism to Therapeutic Targets and Diagnostic Biomarkers
Zhang, Y., Zhao, Y., Ao, X., Yu, W., Zhang, L., Wang, Y., & Chang, W. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.654978 · Cited by 68 · see citing works
Systematic Characterization of Circular RNA-Associated CeRNA Network Identified Novel circRNA Biomarkers in Alzheimer's Disease
Zhang, Y., Yu, F., Bao, S., & Sun, J. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00222 · Cited by 67 · see citing works
Human microRNA (miR-20b-5p) modulates Alzheimer’s disease pathways and neuronal function, and a specific polymorphism close to the MIR20B gene influences Alzheimer’s biomarkers
Wang, R., Chopra, N., Nho, K. T., Maloney, B., Obukhov, A. G., Nelson, P. T., Counts, S., & Lahiri, D. K. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01351-3 · Cited by 66 · see citing works
Inhibition of miR-128 Abates Aβ-Mediated Cytotoxicity by Targeting PPAR-γ via NF-κB Inactivation in Primary Mouse Cortical Neurons and Neuro2a Cells
Geng, L., Zhang, T., Liu, W., & Chen, Y. (2018) · Yonsei Medical Journal · doi:10.3349/ymj.2018.59.9.1096 · Cited by 65 · see citing works
MicroRNA-29b Regulates Ethanol-induced Neuronal Apoptosis in the Developing Cerebellum through SP1/RAX/PKR Cascade
Qi, Y., Zhang, M., Li, H., Frank, J. A., Dai, L., Liu, H., & Chen, G. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.535195 · Cited by 64 · see citing works
MicroRNAs and human diseases: diagnostic and therapeutic potential
Maqbool, R., & Hussain, M. U. (2014) · Cell and Tissue Research · doi:10.1007/s00441-013-1787-3 · Cited by 64 · see citing works
The epigenetic dimension of Alzheimer's disease: causal, consequence, or curiosity?
Millan, M. J. (2014) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2014.16.3/mmillan · Cited by 63 · see citing works
Epigenetic regulation of adult neural stem cells: implications for Alzheimer’s disease
Fitzsimons, C. P., van Bodegraven, E. J., Schouten, M., Lardenoije, R., Kompotis, K., Kenis, G., van den Hurk, M., Boks, M. P., Biojone, C., Joca, S. R. L., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-25 · Cited by 63 · see citing works
lncRNA SNHG1 Knockdown Alleviates Amyloid-β-Induced Neuronal Injury by Regulating ZNF217 via Sponging miR-361-3p in Alzheimer’s Disease
Gao, Y., Zhang, N., Lv, C., Li, N., Li, X., & Li, W. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-191303 · Cited by 60 · see citing works
MicroRNAs alteration as early biomarkers for cancer and neurodegenerative diseases: New challenges in pesticides exposure
Costa, C., Teodoro, M., Rugolo, C. A., Alibrando, C., Giambò, F., Briguglio, G., & Fenga, C. (2020) · Toxicology Reports · doi:10.1016/j.toxrep.2020.05.003 · Cited by 60 · see citing works
MiR-153 targets the nuclear factor-1 family and protects against teratogenic effects of ethanol exposure in fetal neural stem cells
Tsai, P.-C., Bake, S., Balaraman, S., Rawlings, J. A., Holgate, R., DuBois, D. W., & Miranda, R. C. (2014) · Biology Open · doi:10.1242/bio.20147765 · Cited by 59 · see citing works
Epigenetic signatures of methylated DNA cytosine in Alzheimer’s disease
Fetahu, I. S., Ma, D., Rabidou, K., Argueta, C. E., Smith, M., Liu, H., Wu, F., & Shi, Y. G. (2019) · Science Advances · doi:10.1126/sciadv.aaw2880 · Cited by 58 · see citing works
Modulation of MicroRNAs as a Potential Molecular Mechanism Involved in the Beneficial Actions of Physical Exercise in Alzheimer Disease
Caria, A. C. I., Nonaka, C. K. V., Cavalcante, B. R. R., Sousa, R. A. L. D., Aras, R., & Souza, B. S. D. F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144977 · Cited by 56 · see citing works
MicroRNA and diseases: Therapeutic potential as new generation of drugs
Wahid, F., Khan, T., & Kim, Y. Y. (2014) · Biochimie · doi:10.1016/j.biochi.2014.05.004 · Cited by 54 · see citing works
Human primary mixed brain cultures: preparation, differentiation, characterization and application to neuroscience research
Ray, B., Chopra, N., Long, J. M., & Lahiri, D. K. (2014) · Molecular Brain · doi:10.1186/s13041-014-0063-0 · Cited by 47 · see citing works
Epigenetics: Recent Advances and Its Role in the Treatment of Alzheimer's Disease
Xiao, X., Liu, X., & Jiao, B. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.538301 · Cited by 49 · see citing works
Tanshinone IIA protects dopaminergic neurons against 6-hydroxydopamine-induced neurotoxicity through miR-153/NF-E2-related factor 2/antioxidant response element signaling pathway
Zhang, X. S., Ha, S., Wang, X. L., Shi, Y.-X., Duan, S., & Li, Z. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.06.030 · Cited by 49 · see citing works
A lentiviral sponge for miR-101 regulates RanBP9 expression and amyloid precursor protein metabolism in hippocampal neurons
Barbato, C., Pezzola, S., Caggiano, C., Antonelli, M., Frisone, P., Ciotti, M. T., & Ruberti, F. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00037 · Cited by 48 · see citing works
Inhibition of microRNA-155 Alleviates Cognitive Impairment in Alzheimer’s Disease and Involvement of Neuroinflammation
Liu, D., Zhao, D., Zhao, Y., Wang, Y., Zhao, Y., & Wen, C. (2019) · Current Alzheimer Research · doi:10.2174/1567205016666190503145207 · Cited by 49 · see citing works
Co-regulation of intragenic microRNA miR-153 and its host gene Ia-2 β: identification of miR-153 target genes with functions related to IA-2β in pancreas and brain
Mandemakers, W. J., Abuhatzira, L., Xu, H., Caromile, L. A., Hébert, S. S., Snellinx, A., Morais, V. A., Matta, S., Cai, T., Notkins, A. L., et al. (2013) · Diabetologia · doi:10.1007/s00125-013-2901-5 · Cited by 47 · see citing works
Potential Implications of miRNAs in the Pathogenesis, Diagnosis, and Therapeutics of Alzheimer’s Disease
Wang, L., Shui, X., Diao, Y., Chen, D., Zhou, Y., & Lee, T. H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216259 · Cited by 46 · see citing works
New insights into the role of microRNAs and long noncoding RNAs in most common neurodegenerative diseases
Maniati, M. S., Maniati, M., Yousefi, T., Ahangar, A. A., & Tehrani, S. S. (2019) · Journal of Cellular Biochemistry · doi:10.1002/jcb.28361 · Cited by 44 · see citing works
MicroRNA biomarkers as next-generation diagnostic tools for neurodegenerative diseases: a comprehensive review
Azam, H. M. H., Rößling, R., Geithe, C., Khan, M. M., Dinter, F., Hanack, K., Prüß, H., Husse, B., Roggenbuck, D., Schierack, P., et al. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1386735 · Cited by 45 · see citing works
CircLPAR1/miR-212-3p/ZNF217 feedback loop promotes amyloid β-induced neuronal injury in Alzheimer’s Disease
Wu, L., Du, Q., & Wu, C. (2021) · Brain Research · doi:10.1016/j.brainres.2021.147622 · Cited by 43 · see citing works
MicroRNAs in Extracellular Vesicles of Alzheimer’s Disease
Li, W., & Zheng, Y. (2023) · Cells · doi:10.3390/cells12101378 · Cited by 43 · see citing works
RETRACTED: Osthole attenuates APP-induced Alzheimer's disease through up-regulating miRNA-101a-3p
Lin, Y., Liang, X., Yao, Y., Xiao, H., Shi, Y., & Yang, J. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.04.004 · Cited by 41 · see citing works
Retracted
Opposite Dysregulation of Fragile-X Mental Retardation Protein and Heteronuclear Ribonucleoprotein C Protein Associates with Enhanced APP Translation in Alzheimer Disease
Borreca, A., Gironi, K., Amadoro, G., & Ammassari‐Teule, M. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9229-8 · Cited by 41 · see citing works
Hidden Risk Genes with High-Order Intragenic Epistasis in Alzheimer's Disease
Sun, J., Song, F., Wang, J., Han, G., Bai, Z., Xie, B., Feng, X., Jia, J., Duan, Y., & Lei, H. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-140054 · Cited by 40 · see citing works
Amyloid-β precursor protein facilitates the regulator of calcineurin 1-mediated apoptosis by downregulating proteasome subunit α type-5 and proteasome subunit β type-7
Wu, Y., Deng, Y., Zhang, S., Luo, Y., Cai, F., Zhang, Z., Zhou, W., Li, T., & Song, W. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.07.029 · Cited by 39 · see citing works
miR-15b-5p targeting amyloid precursor protein is involved in the anti-amyloid eflect of curcumin in swAPP695-HEK293 cells
Liu, H., Fu, X., Li, Y., Li, X.-L., E, Z., Zhang, Y., & Gao, Q. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.255979 · Cited by 38 · see citing works
MicroRNA-574 is involved in cognitive impairment in 5-month-old APP/PS1 mice through regulation of neuritin
Li, F., Wei, G., Bai, Y., Li, Y., Huang, F., Lin, J., Hou, Q., Deng, R., Zhou, J. H., Zhang, S. X., et al. (2015) · Brain Research · doi:10.1016/j.brainres.2015.09.022 · Cited by 37 · see citing works
Neuroepigenetics of Aging and Age-Related Neurodegenerative Disorders
Lardenoije, R., Pishva, E., Lunnon, K., & van den Hove, D. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2018.04.008 · Cited by 38 · see citing works
Emerging Role of microRNAs in Dementia
Ramakrishna, S., & Muddashetty, R. S. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.01.046 · Cited by 38 · see citing works
The Ia-2β intronic miRNA, miR-153, is a negative regulator of insulin and dopamine secretion through its effect on the Cacna1c gene in mice
Xu, H., Abuhatzira, L., Carmona, G. N., Vadrevu, S., Satin, L. S., & Notkins, A. L. (2015) · Diabetologia · doi:10.1007/s00125-015-3683-8 · Cited by 37 · see citing works
Inhibition of microRNA‐153 protects neurons against ischemia/reperfusion injury in an oxygen–glucose deprivation and reoxygenation cellular model by regulating Nrf2/HO‐1 signaling
Ji, Q., Gao, J., Zheng, Y., Liu, X., Zhou, Q., Shi, C., Yao, M., & Chen, X. (2017) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.21905 · Cited by 36 · see citing works
A microRNA negative feedback loop downregulates vesicle transport and inhibits fear memory
Mathew, R. S., Tatarakis, A., Rudenko, A., Johnson‐Venkatesh, E., Yang, Y. J., Murphy, E. A., Todd, T. P., Schepers, S. T., Siuti, N., Martorell, A. J., et al. (2016) · eLife · doi:10.7554/elife.22467 · Cited by 36 · see citing works
Biomarkers in neurodegenerative diseases: a broad overview
Sathish, S., & Ayyavoo, V. (2024) · Exploration of Neuroprotective Therapy · doi:10.37349/ent.2024.00075 · Cited by 38 · see citing works
Prediction of P-tau/Aβ42 in the cerebrospinal fluid with blood microRNAs in Alzheimer’s disease
Jia, L., Zhu, M., Yang, J., Pang, Y., Wang, Q., Li, Y., Li, T., Li, F., Wang, Q., Li, Y., et al. (2021) · BMC Medicine · doi:10.1186/s12916-021-02142-x · Cited by 37 · see citing works
Mutation in the 3’untranslated region of APP as a genetic determinant of cerebral amyloid angiopathy
Nicolas, G., Wallon, D., Goupil, C., Richard, A., Pottier, C. P., Dorval, V., Sarov-Rivière, M., Riant, F., Hervé, D., Amouyel, P., et al. (2015) · European Journal of Human Genetics · doi:10.1038/ejhg.2015.61 · Cited by 35 · see citing works
GlialHMOX1expression promotes central and peripheral α‐synuclein dysregulation and pathogenicity in parkinsonian mice
Cressatti, M., Song, W., Turk, A. Z., Garabed, L. R., Benchaya, J. A., Galindez, C., Liberman, A., & Schipper, H. M. (2019) · Glia · doi:10.1002/glia.23645 · Cited by 35 · see citing works
New RNA-Based Breakthroughs in Alzheimer’s Disease Diagnosis and Therapeutics
Riscado, M., Baptista, B., & de Sousa, F. P. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13091397 · Cited by 34 · see citing works
Clinical and preclinical evaluation of miR‐144‐5p as a key target for major depressive disorder
Wu, X., Zhang, Y., Wang, P., Li, X., Song, Z., Wei, C., Zhang, Q., Luo, B., Liu, Z., Yang, Y., et al. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14291 · Cited by 32 · see citing works
A novel kit for early diagnosis of Alzheimer’s disease using a fluorescent nanoparticle imaging
Park, J. S., Kim, S. T., Kim, S., Jo, M. G., Choi, M. J., & Kim, M. O. (2019) · Scientific Reports · doi:10.1038/s41598-019-49711-y · Cited by 33 · see citing works
Novel miRNA PC-5P-12969 in Ischemic Stroke
Vijayan, M., Alamri, F. F., Shoyaib, A. A., Karamyan, V. T., & Reddy, P. H. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1562-x · Cited by 32 · see citing works
Repeated electromagnetic field stimulation lowers amyloid-β peptide levels in primary human mixed brain tissue cultures
Perez, F. P., Maloney, B., Chopra, N., Morisaki, J., & Lahiri, D. K. (2021) · Scientific Reports · doi:10.1038/s41598-020-77808-2 · Cited by 32 · see citing works
Expression of Amyloid-Associated miRNAs in Both the Forebrain Cortex and Hippocampus of Middle-Aged Rat
Che, H., Sun, L.-H., Guo, F., Niu, H.-F., Su, X.-L., Bao, Y.-N., Fu, Z. D., Liu, H.-L., Hou, X., Yang, B.-F., et al. (2014) · Cellular Physiology and Biochemistry · doi:10.1159/000356646 · Cited by 35 · see citing works
Targeting MicroRNAs in Prevention and Treatment of Neurodegenerative Disorders
Gupta, S. N., Verma, S., Mantri, S. S., Berman, N. E. J., & Sandhir, R. (2015) · Drug Development Research · doi:10.1002/ddr.21277 · Cited by 31 · see citing works
miR-153-3p, a new bio-target, is involved in the pathogenesis of acute graft-versus-host disease via inhibition of indoleamine- 2,3-dioxygenase
Zhao, X., Wang, Y., Lv, M., Kong, Y., Luo, H., Ye, X., Wu, Q., Zhao, T., Hu, Y.-H., Zhang, H., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.10220 · Cited by 31 · see citing works
Posttranscriptional regulation of Nrf2 through miRNAs and their role in Alzheimer's disease
Kaundal, R. K., Datusalia, A. K., & Sharma, S. S. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.106018 · Cited by 31 · see citing works
Exosomal MicroRNA-Based Predictive Model for Preclinical Alzheimer’s Disease: A Multicenter Study
Jia, L., Zhu, M., Yang, J., Pang, Y., Wang, Q., Li, T., Li, F., Wang, Q., Li, Y., & Wei, Y. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2021.12.015 · Cited by 30 · see citing works
Alzheimer’s Disease-Related Epigenetic Changes: Novel Therapeutic Targets
Paniri, A., Hosseini, M. M., & Akhavan‐Niaki, H. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03626-y · Cited by 32 · see citing works
Late-Onset Alzheimer's Disease, Heating up and Foxed by Several Proteins: Pathomolecular Effects of the Aging Process
Perez, F. P., Bose, D., Maloney, B., Nho, K. T., Shah, K., & Lahiri, D. K. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-131544 · Cited by 30 · see citing works

MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2
Liang, C., Zhu, H., Xu, Y., Huang, L. J., Ma, C., Deng, W., Liu, Y. M., & Qin, C. (2011) · Brain Research · doi:10.1016/j.brainres.2011.10.051 · Cited by 109 · see citing works
S4‐03‐03: Novel Specific MicroRNAs in Regulating Neuronal Genes Implicated In Alzheimer's Disease
Long, J. M., & Lahiri, D. K. (2010) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2010.08.042 · Cited by 2 · see citing works
MicroRNA-101 downregulates Alzheimer’s amyloid-β precursor protein levels in human cell cultures and is differentially expressed
Long, J. M., & Lahiri, D. K. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.12.053 · Cited by 209 · see citing works
P4‐316: A specific microRNA (miR‐339–5p) is reduced in Alzheimer's disease brain and able to lower BACE1 and BETA‐AMYLOID peptide levels in human fetal brain cultures, suggesting a novel drug target for ALZHEIMER'S
Lahiri, D. K., Long, J. M., & Ray, B. (2012) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.08.097
MicroRNA-339-5p Down-regulates Protein Expression of β-Site Amyloid Precursor Protein-Cleaving Enzyme 1 (BACE1) in Human Primary Brain Cultures and Is Reduced in Brain Tissue Specimens of Alzheimer Disease Subjects
Long, J. M., Ray, B., & Lahiri, D. K. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.518241 · Cited by 187 · see citing works

Authors: Long, J. M., Ray, B., & Lahiri, D. K.
Affiliations: Indiana University Indianapolis (US)
Corresponding author: Lahiri, Debomoy K.
ORCID: Long, Justin M.
Lahiri, Debomoy K.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2012-09
Volume: 287
Issue: 37
Pages: 31298-31310
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m112.366336
PMC: PMC3438960
OpenAlex: W2056488510
Cited by: 198
References: 94
Citations by year: 2026: 3 · 2025: 10 · 2024: 15 · 2023: 16 · 2022: 18 · 2021: 23 · 2020: 16 · 2019: 24 · 2018: 7 · 2017: 12 · 2016: 8 · 2015: 14 · 2014: 19 · 2013: 12 · 2012: 1
FWCI: 9.87
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 2937 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (AG 18379, R01AG018884, AG18884, R01AG018379)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: amyloid precursor protein, 3' untranslated region, APLP2, Alzheimer's disease, microRNA binding sites, fetal brain cells, gene expression dysregulation
MeSH terms: Alzheimer Disease, Brain, Female, Fetus, Gene Expression Regulation, HeLa Cells, Humans, Male, Nerve Tissue Proteins, Amyloid beta-Protein Precursor, 3' Untranslated Regions, MicroRNAs

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

MicroRNA-153 Physiologically Inhibits Expression of Amyloid-β Precursor Protein in Cultured Human Fetal Brain Cells and Is Dysregulated in a Subset of Alzheimer Disease Patients

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks