Therapeutic correction of ApoER2 splicing in Alzheimer's disease mice using antisense oligonucleotides
Open accessAbstract
Apolipoprotein E receptor 2 (ApoER2) is an apolipoprotein E receptor involved in long‐term potentiation, learning, and memory. Given its role in cognition and its association with the Alzheimer's disease (AD) risk gene, apoE, ApoER2 has been proposed to be involved in AD, though a role for the receptor in the disease is not clear. ApoER2 signaling requires amino acids encoded by alternatively spliced exon 19. Here, we report that the balance of ApoER2 exon 19 splicing is deregulated in postmortem brain tissue from AD patients and in a transgenic mouse model of AD. To test the role of deregulated ApoER2 splicing in AD, we designed an antisense oligonucleotide (ASO) that increases exon 19 splicing. Treatment of AD mice with a single dose of ASO corrected ApoER2 splicing for up to 6 months and improved synaptic function and learning and memory. These results reveal an association between ApoER2 isoform expression and AD, and provide preclinical evidence for the utility of ASOs as a therapeutic approach to mitigate Alzheimer's disease symptoms by improving ApoER2 exon 19 splicing. ApoER2 splicing is deregulated in Alzheimer's disease (AD) patients and mouse models of AD. Correcting this splicing defect using antisense oligonucleotides (ASOs) improves synaptic function, learning, and memory in mice, suggesting ApoER2 ASOs as a promising therapeutic strategy against AD. ApoER2 splicing is deregulated in Alzheimer's disease (AD) patients and mouse models of AD. Correcting this splicing defect using antisense oligonucleotides (ASOs) improves synaptic function, learning and memory in mice, suggesting ApoER2 ASOs as a promising therapeutic strategy against AD.
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Alternative splicing deficits observed in both AD mice and human brains lead to reduced inclusion of the proline-rich cytoplasmic domain of ApoER2, which would reduce the ability of Reelin to modulate synaptic strength.
“Furthermore, alternative splicing deficits observed in both AD mice and human brains leads to reduced inclusion of the proline-rich cytoplasmic domain of ApoER2 (91), which would reduce the ability of Reelin to modulate synaptic strength.”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [91]
Enhancing Reelin signaling by either exogenous supplementation of Reelin or reversing the ApoER2 splicing deficit with antisense oligonucleotides can improve the cognitive performance of AD mice.
“Enhancing Reelin signaling by either exogenous supplementation of Reelin (95) or reversing the ApoER2 splicing deficit with antisense oligonucleotides (91) can improve the cognitive performance of AD mice in a murine model of AD.”
From Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses (2017) · cites this paper as [91]
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Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Developments of a water-maze procedure for studying spatial learning in the rat
Morris, R. (1984) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(84)90007-4 · Cited by 7,180 · see citing works
Morris water maze: procedures for assessing spatial and related forms of learning and memory
Vorhees, C. V., & Williams, M. T. (2006) · Nature Protocols · doi:10.1038/nprot.2006.116 · Cited by 4,629 · see citing works
Morris, R. G. M., Anderson, E., Lynch, G. S., & Baudry, M. (1986) · Nature · doi:10.1038/319774a0 · Cited by 3,640 · see citing works
APP Processing and Synaptic Function
Kamenetz, F., Tomita, T., Hsieh, H., Seabrook, G., Borchelt, D., Iwatsubo, T., Sisodia, S., & Malinow, R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00124-7 · Cited by 1,644 · see citing works
ESEfinder: a web resource to identify exonic splicing enhancers
Cartegni, L. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg616 · Cited by 1,593 · see citing works
Regulation of NMDA receptor trafficking by amyloid-β
Snyder, E. M., Nong, Y., Almeida, C. G., Paul, S., Moran, T., Choi, E. Y., Nairn, A. C., Salter, M. W., Lombroso, P. J., Gouras, G. K., et al. (2005) · Nature Neuroscience · doi:10.1038/nn1503 · Cited by 1,561 · cited 3× · see citing works
“Reelin signaling, potentially through ApoER2, has been shown to counteract this Ab toxicity (Kamenetz et al, 2003; Snyder et al, 2005; Durakoglugil et al, 2009).”
InfluentialAβ peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease
Janus, C., Pearson, J., McLaurin, J., Mathews, P. M., Jiang, Y., Schmidt, S. D., Chishti, M. A., Horne, P., Heslin, D., French, J., et al. (2000) · Nature · doi:10.1038/35050110 · Cited by 1,431 · see citing works
RNA therapeutics: beyond RNA interference and antisense oligonucleotides
Kole, R., Krainer, A. R., & Altman, S. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3625 · Cited by 1,152 · see citing works
Apolipoprotein E in sporadic Alzheimer's disease: Allelic variation and receptor interactions
William Rebeck, G., Reiter, J. S., Strickland, D. K., & Hyman, B. T. (1993) · Neuron · doi:10.1016/0896-6273(93)90070-8 · Cited by 1,107 · see citing works
Natural history of mild cognitive impairment in older persons
Bennett, D. A., Wilson, R. S., Schneider, J. A., Evans, D. A., Beckett, L. A., Aggarwal, N. T., Barnes, L. L., Fox, J. H., & Bach, J. (2002) · Neurology · doi:10.1212/wnl.59.2.198 · Cited by 1,037 · see citing works
Self-citationClinical epidemiology of Alzheimer’s disease: assessing sex and gender differences
Mielke, M., Vemuri, P., & Rocca, W. (2014) · Clinical Epidemiology · doi:10.2147/clep.s37929 · Cited by 1,021 · see citing works
Chishti, M. A., Yang, D.-S., Janus, C., Phinney, A. L., Horne, P., Pearson, J., Strome, R., Zuker, N., Loukides, J., French, J., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100710200 · Cited by 955 · see citing works
Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice
Chapman, P. F., White, G. L., Jones, M. W., Cooper-Blacketer, D., Marshall, V. J., Irizarry, M., Younkin, L., Good, M. A., Bliss, T. V. P., Hyman, B. T., et al. (1999) · Nature Neuroscience · doi:10.1038/6374 · Cited by 946 · see citing works
Individual differences in rates of change in cognitive abilities of older persons.
Wilson, R. S., Beckett, L. A., Barnes, L. L., Schneider, J. A., Bach, J., Evans, D. A., & Bennett, D. A. (2002) · Psychology and Aging · doi:10.1037/0882-7974.17.2.179 · Cited by 842 · see citing works
Self-citationOverview and Findings from the Rush Memory and Aging Project
Bennett, D. A., Schneider, J. A., Buchman, A. S., Barnes, L. L., Boyle, P. A., & Wilson, R. S. (2012) · Current Alzheimer Research · doi:10.2174/156720512801322663 · Cited by 837 · see citing works
Self-citationApolipoprotein E and Apolipoprotein E Receptors: Normal Biology and Roles in Alzheimer Disease
Holtzman, D. M., Herz, J., & Bu, G. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006312 · Cited by 782 · see citing works
Hua, Y., Sahashi, K., Rigo, F., Hung, G., Horev, G., Bennett, C. F., & Krainer, A. R. (2011) · Nature · doi:10.1038/nature10485 · Cited by 744 · see citing works
Self-citationEarly-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease
Jacobsen, J. S., Wu, C.-C., Redwine, J. M., Comery, T. A., Arias, R., Bowlby, M., Martone, R., Morrison, J. H., Pangalos, M. N., Reinhart, P. H., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600948103 · Cited by 701 · see citing works
Schneider, L. S., Mangialasche, F., Andreasen, N., Feldman, H., Giacobini, E., Jones, R., Mantua, V., Mecocci, P., Pani, L., Winblad, B., et al. (2014) · Journal of Internal Medicine · doi:10.1111/joim.12191 · Cited by 651 · see citing works
Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning
Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Förster, E., Sweatt, J. D., & Herz, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205147200 · Cited by 623 · see citing works
ApoE and Aβ in Alzheimer’s Disease: Accidental Encounters or Partners?
Kanekiyo, T., Xu, H., & Bu, G. (2014) · Neuron · doi:10.1016/j.neuron.2014.01.045 · Cited by 608 · see citing works
Hua, Y., Vickers, T. A., Okunola, H. L., Bennett, C. F., & Krainer, A. R. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.01.014 · Cited by 570 · see citing works
Lagier‐Tourenne, C., Baughn, M. W., Rigo, F., Sun, S., Liu, P., Li, H., Jiang, J., Watt, A. T., Chun, S. J., Katz, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318835110 · Cited by 555 · see citing works
Self-citationTrommsdorff, M., Borg, J., Margolis, B. L., & Herz, J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.50.33556 · Cited by 540 · see citing works
Mild cognitive impairment is related to Alzheimer disease pathology and cerebral infarctions
Bennett, D. A., Schneider, J. A., Bienias, J. L., Evans, D. A., & Wilson, R. S. (2005) · Neurology · doi:10.1212/01.wnl.0000152982.47274.9e · Cited by 537 · see citing works
Self-citationReelin, lipoprotein receptors and synaptic plasticity
Herz, J., & Chen, Y. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2009 · Cited by 524 · see citing works
Alzheimer's disease: synaptic dysfunction and Aβ
Shankar, G. M., & Walsh, D. M. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-48 · Cited by 522 · see citing works
Towards a therapy for Angelman syndrome by targeting a long non-coding RNA
Meng, L., Ward, A. J., Chun, S. J., Bennett, C. F., Beaudet, A. L., & Rigo, F. (2014) · Nature · doi:10.1038/nature13975 · Cited by 520 · see citing works
Self-citationSelenoprotein P—Expression, functions, and roles in mammals
Burk, R. F., & Hill, K. E. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.03.026 · Cited by 516 · see citing works
Smith, P. J., Zhang, C., Wang, J., Chew, S. L., Zhang, M. Q., & Krainer, A. R. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl171 · Cited by 514 · see citing works
Beffert, U., Weeber, E. J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J. D., Li, W.-P., Adelmann, G., Frotscher, M., Hammer, R. E., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.07.007 · Cited by 497 · see citing works
Zhang, Z., Song, M., Liu, X., Kang, S. S., Kwon, I.-S., Duong, D. M., Seyfried, N. T., Hu, W. T., Liu, Z., Wang, J.-Z., et al. (2014) · Nature Medicine · doi:10.1038/nm.3700 · Cited by 494 · see citing works
Apolipoprotein E and Alzheimer's disease
Strittmatter, W. J., & Roses, A. D. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.000413 · Cited by 477 · see citing works
Implications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476 · see citing works
Huelga, S. C., Vu, A. Q., Arnold, J. D., Liang, T. Y., Liu, P. P., Yan, B. Y., Donohue, J. P., Shiue, L., Hoon, S., Brenner, S., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.02.001 · Cited by 470 · see citing works
Gotthardt, M., Trommsdorff, M., Nevitt, M. F., Shelton, J., Richardson, J. A., Stockinger, W., Nimpf, J., & Herz, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000955200 · Cited by 450 · see citing works
Bennett, D. A., Schneider, J. A., Aggarwal, N. T., Arvanitakis, Z., Shah, R. C., Kelly, J. F., Fox, J. H., Cochran, E. J., Arends, D., Treinkman, A., et al. (2006) · Neuroepidemiology · doi:10.1159/000096129 · Cited by 407 · see citing works
Self-citationBaker, B. F., Lot, S. S., Condon, T. P., Cheng-Flournoy, S., Lesnik, E. A., Sasmor, H. M., & Bennett, C. F. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.18.11994 · Cited by 374 · see citing works
A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin
Prange, O., Wong, T. P., Gerrow, K., Wang, Y. T., & El-Husseini, A. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0405939101 · Cited by 363 · see citing works
U1 small nuclear ribonucleoprotein complex and RNA splicing alterations in Alzheimer’s disease
Bai, B., Hales, C. M., Chen, P.-C., Gozal, Y., Dammer, E. B., Fritz, J. J., Wang, X., Xia, Q., Duong, D. M., Street, C., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1310249110 · Cited by 335 · see citing works
Self-citationTwine, N. A., Janitz, K., Wilkins, M. R., & Janitz, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016266 · Cited by 295 · see citing works
Rigo, F., Chun, S. J., Norris, D. A., Hung, G., Lee, S., Matson, J., Fey, R. A., Gaus, H., Hua, Y., Grundy, J. S., et al. (2014) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.113.212407 · Cited by 283 · see citing works
Self-citationThe involvement of Reelin in neurodevelopmental disorders
Folsom, T. D., & Fatemi, S. H. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.08.015 · Cited by 275 · see citing works
Analysis of alternative splicing associated with aging and neurodegeneration in the human brain
Tollervey, J. R., Wang, Z., Hortobágyi, T., Witten, J. T., Zarnack, K., Kayikci, M., Clark, T. A., Schweitzer, A. C., Rot, G., Curk, T., et al. (2011) · Genome Research · doi:10.1101/gr.122226.111 · Cited by 252 · see citing works
The reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2
Stockinger, W., Brandes, C., Fasching, D., Hermann, M., Gotthardt, M., Herz, J., Schneider, W. J., & Nimpf, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m004119200 · Cited by 239 · cited 2× · see citing works
“…of ApoER2 with PSD-95 to activate NMDA receptors and also with c-Jun amino-terminal kinase (JNK)-interacting proteins (JIP), which have been implicated in neuronal survival through interactions with JNK (Gotthardt et al, 2000; Stockinger et al, 2000; Beffert et al, 2005, 2006; Hoe et al, 2006).”
InfluentialLentz, J. J., Jodelka, F. M., Hinrich, A. J., McCaffrey, K. E., Farris, H. E., Spalitta, M. J., Bazan, N. G., Duelli, D. M., Rigo, F., & Hastings, M. L. (2013) · Nature Medicine · doi:10.1038/nm.3106 · Cited by 229 · see citing works
Self-citationFitzjohn, S. M., Morton, R. A., Kuenzi, F. M., Rosahl, T. W., Shearman, M. S., Lewis, H. D., Smith, D., Reynolds, D. S., Davies, C. H., Collingridge, G. L., et al. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-13-04691.2001 · Cited by 210 · see citing works
Search Strategies Used byAPPTransgenic Mice During Navigation in the Morris Water MazePreprint
Janus, C. (2004) · Learning & Memory · doi:10.1101/lm.70104 · Cited by 194 · see citing works
Chin, J., Massaro, C. M., Palop, J. J., Thwin, M. T., Yu, G.-Q., Bien-Ly, N., Bender, A., & Mucke, L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3758-06.2007 · Cited by 188 · see citing works
Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density
Rogers, J. T., Rusiana, I., Trotter, J., Zhao, L., Donaldson, E., Pak, D. T. S., Babus, L. W., Peters, M., Banko, J. L., Chavis, P., et al. (2011) · Learning & Memory · doi:10.1101/lm.2153511 · Cited by 181 · see citing works
LRP8-Reelin-regulated neuronal enhancer signature underlying learning and memory formation
Telese, F., Ma, Q., Perez, P. M., Notani, D., Oh, S., Li, W., Comoletti, D., Ohgi, K. A., Taylor, H., & Rosenfeld, M. G. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.033 · Cited by 166 · see citing works
Antisense oligonucleotides: treating neurodegeneration at the level of RNA
DeVos, S. L., & Miller, T. M. (2013) · Neurotherapeutics · doi:10.1007/s13311-013-0194-5 · Cited by 164 · see citing works
Targeting RNA splicing for disease therapy
Havens, M. A., Duelli, D. M., & Hastings, M. L. (2013) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1158 · Cited by 163 · see citing works
Self-citationReelin signaling antagonizes β-amyloid at the synapse
Durakoglugil, M. S., Chen, Y., White, C. L., Kavalali, E. T., & Herz, J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908176106 · Cited by 153 · see citing works
Kim, J., Yoon, H., Basak, J., & Kim, J. (2014) · Molecules and Cells · doi:10.14348/molcells.2014.0248 · Cited by 141 · cited 2× · see citing works
“To test the role of deregulated ApoER2 splicing in AD, we designed an antisense oligonucleotide (ASO) that increases exon 19 splicing.”
Kocherhans, S., Madhusudan, A., Doehner, J., Breu, K. S., Nitsch, R. M., Fritschy, J.-M., & Knuesel, I. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0418-10.2010 · Cited by 132 · see citing works
Pujadas, L., Rossi, D., Andrés, R., Teixeira, C. M., Serra-Vidal, B., Parcerisas, A., Maldonado, R., Giralt, E., Carulla, N., & Soriano, E. (2014) · Nature Communications · doi:10.1038/ncomms4443 · Cited by 129 · see citing works
He, X., Cooley, K., Chung, C. H. Y., Dashti, N., & Tang, J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3993-06.2007 · Cited by 107 · see citing works
c-Jun N-terminal kinase has a key role in Alzheimer disease synaptic dysfunction in vivo
Sclip, A., Tozzi, A., Abaza, A., Cardinetti, D., Colombo, I., Calabresi, P., Salmona, M., Welker, E., & Borsello, T. (2014) · Cell Death and Disease · doi:10.1038/cddis.2013.559 · Cited by 103 · see citing works
Long-Term Potentiation Is Increased in the CA1 Area of the Hippocampus of APPswe/ind CRND8 Mice
Jolas, T. (2002) · Neurobiology of Disease · doi:10.1006/nbdi.2002.0557 · Cited by 98 · see citing works
Reelin protects against amyloid β toxicity in vivo
Lane-Donovan, C., Philips, G. T., Wasser, C. R., Durakoglugil, M. S., Masiulis, I., Upadhaya, A., Pohlkamp, T., Coskun, C., Kotti, T., Steller, L., et al. (2015) · Science Signaling · doi:10.1126/scisignal.aaa6674 · Cited by 96 · see citing works
Reelin depletion is an early phenomenon of Alzheimer's pathology
Herring, A., Donath, A., Steiner, K. M., Widera, M. P., Hamzehian, S., Kanakis, D., Kölble, K., ElAli, A., Hermann, D. M., Paulus, W., et al. (2012) · Journal of Alzheimer's Disease · doi:10.3233/jad-2012-112069 · Cited by 92 · see citing works
Apolipoprotein E Receptor 2 Interactions with the N-Methyl-D-aspartate Receptor
Hoe, H., Pocivavsek, A., Chakraborty, G., Fu, Z., Vicini, S., Ehlers, M., & Rebeck, G. W. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509380200 · Cited by 89 · see citing works
NMDA Neurotransmission Dysfunction in Behavioral and Psychological Symptoms of Alzheimer's Disease
Huang, Y.-J., Lin, C., Lane, H., & Tsaid, G. E. (2012) · Current Neuropharmacology · doi:10.2174/157015912803217288 · Cited by 85 · see citing works
ApoE receptor 2 controls neuronal survival in the adult brain
Beffert, U., Nematollah Farsian, F., Masiulis, I., Hammer, R. E., Yoon, S. O., Giehl, K. M., & Herz, J. (2006) · Current Biology · doi:10.1016/j.cub.2006.10.029 · Cited by 84 · see citing works
A feedback loop regulates splicing of the spinal muscular atrophy-modifying gene, SMN2
Jodelka, F. M., Ebert, A. D., Duelli, D. M., & Hastings, M. L. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq425 · Cited by 83 · see citing works
Self-citationWalker, J. M., Fowler, S., Miller, D. K., Sun, A. Y., Weisman, G. A., Wood, W. G., Sun, G. Y., Simonyi, Á., & Schachtman, T. R. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.049 · Cited by 77 · see citing works
Carvedilol as a potential novel agent for the treatment of Alzheimer's disease
Wang, J., Ono, K., Dickstein, D. L., Arrieta‐Cruz, I., Zhao, W., Qian, X., Lamparello, A. J., Subnani, R., Ferruzzi, M. G., Pavlides, C., et al. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.05.004 · Cited by 74 · see citing works
Expression and alternate splicing of apolipoprotein E receptor 2 in brain
Clatworthy, A. E., Stockinger, W., Christie, R. H., Schneider, W. J., Nimpf, J., Hyman, B. T., & Rebeck, G. W. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00489-8 · Cited by 70 · see citing works
Kimura, R., MacTavish, D., Yang, J., Westaway, D. A., & Jhamandas, J. H. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3028-12.2012 · Cited by 67 · see citing works
Dubal, D. B., Broestl, L., & Worden, K. (2012) · Biology of Sex Differences · doi:10.1186/2042-6410-3-24 · Cited by 58 · see citing works
Targeting SR Proteins Improves SMN Expression in Spinal Muscular Atrophy Cells
Wee, C. D., Havens, M. A., Jodelka, F. M., & Hastings, M. L. (2014) · PLoS ONE · doi:10.1371/journal.pone.0115205 · Cited by 57 · see citing works
Self-citationLi, X., Kypreos, K. E., Zanni, E. E., & Zannis, V. I. (2003) · Biochemistry · doi:10.1021/bi027093c · Cited by 49 · see citing works
Differential splicing and glycosylation of Apoer2 alters synaptic plasticity and fear learning
Wasser, C. R., Masiulis, I., Durakoglugil, M. S., Lane-Donovan, C., Xian, X., Beffert, U., Agarwala, A., Hammer, R. E., & Herz, J. (2014) · Science Signaling · doi:10.1126/scisignal.2005438 · Cited by 48 · see citing works
Splicing modulation therapy in the treatment of genetic diseases
Aartsma-Rus, A. M., Arechavala‐Gomeza, V., & Khoo, B. C. E. (2014) · The Application of Clinical Genetics · doi:10.2147/tacg.s71506 · Cited by 47 · see citing works
Beta-Amyloid Impairs Reelin Signaling
Cuchillo‐Ibáñez, I., Balmaceda, V., Botella-López, A., Rábano, A., Ávila, J., & Sáez‐Valero, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072297 · Cited by 43 · see citing works
Carvedilol Reestablishes Long-Term Potentiation in a Mouse Model of Alzheimer's Disease
Arrieta‐Cruz, I., Wang, J., Pavlides, C., et al. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-100225 · Cited by 37 · see citing works
Decisive role of Reelin signaling during early stages of Alzheimer’s disease
Krstic, D., Pfister, S., Notter, T., & Knuesel, I. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.04.042 · Cited by 33 · see citing works
Antisense-Mediated Exon Inclusion
Hua, Y., & Krainer, A. R. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-767-5_20 · Cited by 28 · see citing works
Waring, J. F., Anderson, D. J., & Kroeger, P. E. (2012) · Journal of Drug Metabolism & Toxicology · doi:10.4172/2157-7609.1000115 · Cited by 5 · see citing works
Splicing modulation therapy in the treatment of genetic diseases
Arechavala‐Gomeza, V., Khoo, B. C. E., & Aartsma-Rus, A. M. (2014) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 4 · see citing works
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Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses
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“Furthermore, alternative splicing deficits observed in both AD mice and human brains leads to reduced inclusion of the proline-rich cytoplasmic domain of ApoER2 (91), which would reduce the ability of Reelin to modulate synaptic strength.”
Functional Roles of the Interaction of APP and Lipoprotein Receptors
Pohlkamp, T., Wasser, C. R., & Herz, J. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00054 · Cited by 92 · see citing works
- Authors
- Hinrich, A. J., Jodelka, F. M., Chang, J. L., Brutman, D., Bruno, A. M., Briggs, C. A., James, B. D., Stutzmann, G. E., Bennett, D. A., Miller, S. A., Rigo, F., Marr, R. A., & Hastings, M. L.
- Affiliations
- Rosalind Franklin University of Medicine and Science (US)
- Lake Forest College (US)
- Rush University Medical Center (US)
- Ionis Pharmaceuticals (United States) (US)
- Corresponding author
- Hastings, Michelle L
- ORCID
- Venue
- EMBO Molecular Medicine
- Published
- 2016-02-22
- Volume
- 8
- Issue
- 4
- Pages
- 328-345
- ISSN
- 1757-4676 (ISSN-L)
- 1757-4684
- PMC
- PMC4818756
- OpenAlex
- W2285838982
- Cited by
- 127
- References
- 82
- Citations by year
- 2026: 9 · 2025: 5 · 2024: 7 · 2023: 27 · 2022: 17 · 2021: 9 · 2020: 8 · 2019: 9 · 2018: 17 · 2017: 12 · 2016: 7
- FWCI
- 11.98
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- EMBO Molecular Medicine (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- NIH (NS069759)
- Midwest Proteome Center (S10 OD010662, P30AG10161, R01AG15819)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- ApoER2, Alzheimer's disease, alternative splicing, exon 19, antisense oligonucleotides, splicing correction, synaptic function, learning and memory, transgenic mouse model, apolipoprotein E receptor, gene therapy
- MeSH terms
- Alzheimer Disease, Animals, Brain, Disease Models, Animal, Humans, Learning, Memory, Mice, Transgenic, RNA Splicing, Oligonucleotides, Antisense, Treatment Outcome, LDL-Receptor Related Proteins, Mice
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