LncRNA Xist, X-chromosome Instability and Alzheimer’s Disease

Page: [499 - 507] Pages: 9

  • * (Excluding Mailing and Handling)

Abstract

Neurodegenerative Diseases (NDD) are the major contributors to age-related causes of mental disability on a global scale. Most NDDs, like Alzheimer’s Disease (AD), are complex in nature - implying that they are multi-parametric both in terms of heterogeneous clinical outcomes and underlying molecular paradigms. Emerging evidence from high throughput genomic, transcriptomic and small RNA sequencing experiments hint at the roles of long non-coding RNAs (lncRNAs) in AD. X-inactive Specific Transcript (XIST), a component of the Xic, the X-chromosome inactivation centre, is an RNA gene on the X chromosome of the placental mammals indispensable for the X inactivation process. An extensive literature survey shows that aberrations in Xist expression and in some cases, a disruption of the Xchromosome inactivation as a whole play a significant role in AD. Considering the enormous potential of Xist as an endogenous silencing molecule, the idea of using Xist as a non-conventional chromosome silencer to treat diseases harboring chromosomal alterations is also being implemented. Comprehensive knowledge about how Xist could play such a role in AD is still elusive. In this review, we have collated the available knowledge on the possible Xist involvement and deregulation from the perspective of molecular mechanisms governing NDDs with a primary focus on Alzheimer’s disease. Possibilities of XIST mediated therapeutic intervention and linkages between XIC and preferential predisposition of females to AD have also been discussed.

Keywords: Alzheimer's disease, long non-coding RNA, X chromosome instability, Xist, neurodegenerative diseases, Huntington's disease.

[1]
Pringsheim T, Fiest K, Jette N. The international incidence and prevalence of neurologic conditions: how common are they? Neurology 2014; 83(18): 1661-4.
[http://dx.doi.org/10.1212/WNL.0000000000000929] [PMID: 25349272]
[2]
Bajić VP, Spremo-Potparević B, Zivković L, et al. The X-chromosome instability phenotype in Alzheimer’s disease: A clinical sign of accelerating aging? Med Hypotheses 2009; 73(6): 917-20.
[http://dx.doi.org/10.1016/j.mehy.2009.06.046] [PMID: 19647374]
[3]
Corbo RM, Gambina G, Ruggeri M, Scacchi R. Association of estrogen receptor alpha (ESR1) PvuII and XbaI polymorphisms with sporadic Alzheimer’s disease and their effect on apolipoprotein E concentrations. Dement Geriatr Cogn Disord 2006; 22(1): 67-72.
[http://dx.doi.org/10.1159/000093315] [PMID: 16699281]
[4]
Casadesus G, Atwood CS, Zhu X, et al. Evidence for the role of gonadotropin hormones in the development of Alzheimer disease. Cell Mol Life Sci 2005; 62(3): 293-8.
[http://dx.doi.org/10.1007/s00018-004-4384-0] [PMID: 15723165]
[5]
Corbo RM, Gambina G, Ulizzi L, Moretto G, Scacchi R. Genetic variation of CYP19 (aromatase) gene influences age at onset of Alzheimer’s disease in women. Dement Geriatr Cogn Disord 2009; 27(6): 513-8.
[http://dx.doi.org/10.1159/000221832] [PMID: 19478482]
[6]
Casadesus G, Puig ER, Webber KM, et al. Targeting gonadotropins: An alternative option for Alzheimer disease treatment. J Biomed Biotechnol 2006; 2006(3): 39508.
[http://dx.doi.org/10.1155/JBB/2006/39508] [PMID: 17047306]
[7]
Bajic V, Mandusic V, Stefanova E, et al. Skewed X-chromosome inactivation in women affected by Alzheimer’s disease. J Alzheimers Dis 2015; 43(4): 1251-9.
[http://dx.doi.org/10.3233/JAD-141674] [PMID: 25159673]
[8]
Kopp F, Mendell JT. Functional classification and experimental dissection of long noncoding RNAs. Cell 2018; 172(3): 393-407.
[http://dx.doi.org/10.1016/j.cell.2018.01.011] [PMID: 29373828]
[9]
Böhmdorfer G, Wierzbicki AT. Control of chromatin structure by long noncoding RNA. Trends Cell Biol 2015; 25(10): 623-32.
[http://dx.doi.org/10.1016/j.tcb.2015.07.002] [PMID: 26410408]
[10]
Sin O, Nollen EA. Regulation of protein homeostasis in neurodegenerative diseases: the role of coding and non-coding genes. Cell Mol Life Sci 2015; 72(21): 4027-47.
[http://dx.doi.org/10.1007/s00018-015-1985-0] [PMID: 26190021]
[11]
Elling R, Chan J, Fitzgerald KA. Emerging role of long noncoding RNAs as regulators of innate immune cell development and inflammatory gene expression. Eur J Immunol 2016; 46(3): 504-12.
[http://dx.doi.org/10.1002/eji.201444558] [PMID: 26820238]
[12]
Szcześniak MW, Makałowska I. lncRNA-RNA interactions across the human transcriptome. PLoS One 2016; 11(3) e0150353
[http://dx.doi.org/10.1371/journal.pone.0150353] [PMID: 26930590]
[13]
Barry G. Integrating the roles of long and small non-coding RNA in brain function and disease. Mol Psychiatry 2014; 19(4): 410-6.
[http://dx.doi.org/10.1038/mp.2013.196] [PMID: 24468823]
[14]
Quinn JJ, Chang HY. Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet 2016; 17(1): 47-62.
[http://dx.doi.org/10.1038/nrg.2015.10] [PMID: 26666209]
[15]
Kapranov P, Cheng J, Dike S, et al. RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 2007; 316(5830): 1484-8.
[http://dx.doi.org/10.1126/science.1138341] [PMID: 17510325]
[16]
Hon CC, Ramilowski JA, Harshbarger J, et al. An atlas of human long non-coding RNAs with accurate 5′ ends. Nature 2017; 543(7644): 199-204.
[http://dx.doi.org/10.1038/nature21374] [PMID: 28241135]
[17]
Qureshi IA, Mehler MF. Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease. Nat Rev Neurosci 2012; 13(8): 528-41.
[http://dx.doi.org/10.1038/nrn3234] [PMID: 22814587]
[18]
Ma L, Bajic VB, Zhang Z. On the classification of long non-coding RNAs. RNA Biol 2013; 10(6): 925-33.
[http://dx.doi.org/10.4161/rna.24604] [PMID: 23696037]
[19]
Wu H, Yang L, Chen LL. The diversity of long noncoding rnas and their generation. trends in genetics. TIG 2017; 33(8): 540-52.
[http://dx.doi.org/10.1016/j.tig.2017.05.004] [PMID: 28629949]
[20]
Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell 2011; 43(6): 904-14.
[http://dx.doi.org/10.1016/j.molcel.2011.08.018]
[21]
Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009; 136(4): 629-41.
[http://dx.doi.org/10.1016/j.cell.2009.02.006] [PMID: 19239885]
[22]
Quinodoz S, Guttman M. Long noncoding RNAs: An emerging link between gene regulation and nuclear organization. Trends Cell Biol 2014; 24(11): 651-63.
[http://dx.doi.org/10.1016/j.tcb.2014.08.009] [PMID: 25441720]
[23]
Chen LL, Carmichael GG. Decoding the function of nuclear long non-coding RNAs. Curr Opin Cell Biol 2010; 22(3): 357-64.
[http://dx.doi.org/10.1016/j.ceb.2010.03.003] [PMID: 20356723]
[24]
Riva P, Ratti A, Venturin M. The long non-coding RNAs in neurodegenerative diseases: novel mechanisms of pathogenesis. Curr Alzheimer Res 2016; 13(11): 1219-31.
[http://dx.doi.org/10.2174/1567205013666160622112234] [PMID: 27338628]
[25]
Salta E, De Strooper B. Noncoding RNAs in neurodegeneration. Nat Rev Neurosci 2017; 18(10): 627-40.
[http://dx.doi.org/10.1038/nrn.2017.90]
[26]
Faghihi MA, Modarresi F, Khalil AM, et al. Expression of a noncoding RNA is elevated in Alzheimer’s disease and drives rapid feed-forward regulation of beta-secretase. Nat Med 2008; 14(7): 723-30.
[http://dx.doi.org/10.1038/nm1784] [PMID: 18587408]
[27]
Muddashetty R, Khanam T, Kondrashov A, et al. Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J Mol Biol 2002; 321(3): 433-45.
[http://dx.doi.org/10.1016/S0022-2836(02)00655-1] [PMID: 12162957]
[28]
Massone S, Vassallo I, Fiorino G, et al. 17A, a novel non-coding RNA, regulates GABA B alternative splicing and signaling in response to inflammatory stimuli and in Alzheimer disease. Neurobiol Dis 2011; 41(2): 308-17.
[http://dx.doi.org/10.1016/j.nbd.2010.09.019] [PMID: 20888417]
[29]
Chung DW, Rudnicki DD, Yu L, Margolis RL. A natural antisense transcript at the Huntington’s disease repeat locus regulates HTT expression. Hum Mol Genet 2011; 20(17): 3467-77.
[http://dx.doi.org/10.1093/hmg/ddr263] [PMID: 21672921]
[30]
Sunwoo JS, Lee ST, Im W, et al. Altered expression of the long noncoding RNA NEAT1 in Huntington’s disease. Mol Neurobiol 2017; 54(2): 1577-86.
[http://dx.doi.org/10.1007/s12035-016-9928-9] [PMID: 27221610]
[31]
Scheele C, Petrovic N, Faghihi MA, et al. The human PINK1 locus is regulated in vivo by a non-coding natural antisense RNA during modulation of mitochondrial function. BMC Genomics 2007; 8: 74.
[http://dx.doi.org/10.1186/1471-2164-8-74] [PMID: 17362513]
[32]
Zhang QS, Wang ZH, Zhang JL, Duan YL, Li GF, Zheng DL. Beta-asarone protects against MPTP-induced Parkinson’s disease via regulating long non-coding RNA MALAT1 and inhibiting α-synuclein protein expression. Biomed Pharmacother 2016; 83: 153-9.
[http://dx.doi.org/10.1016/j.biopha.2016.06.017] [PMID: 27470562]
[33]
Ramos AD, Diaz A, Nellore A, et al. Integration of genome-wide approaches identifies lncRNAs of adult neural stem cells and their progeny in vivo. Cell Stem Cell 2013; 12(5): 616-28.
[http://dx.doi.org/10.1016/j.stem.2013.03.003] [PMID: 23583100]
[34]
Ramos AD, Andersen RE, Liu SJ, et al. The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell 2015; 16(4): 439-47.
[http://dx.doi.org/10.1016/j.stem.2015.02.007] [PMID: 25800779]
[35]
Aprea J, Prenninger S, Dori M, et al. Transcriptome sequencing during mouse brain development identifies long non-coding RNAs functionally involved in neurogenic commitment. EMBO J 2013; 32(24): 3145-60.
[http://dx.doi.org/10.1038/emboj.2013.245] [PMID: 24240175]
[36]
Ng SY, Bogu GK, Soh BS, Stanton LW. The long noncoding RNA RMST interacts with SOX2 to regulate neurogenesis. Mol Cell 2013; 51(3): 349-59.
[http://dx.doi.org/10.1016/j.molcel.2013.07.017] [PMID: 23932716]
[37]
Zhu X, Wu YB, Zhou J, Kang DM. Upregulation of lncRNA MEG3 promotes hepatic insulin resistance via increasing FoxO1 expression. Biochem Biophys Res Commun 2016; 469(2): 319-25.
[http://dx.doi.org/10.1016/j.bbrc.2015.11.048] [PMID: 26603935]
[38]
Brown CJ, Hendrich BD, Rupert JL, et al. The human XIST gene: Analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 1992; 71(3): 527-42.
[http://dx.doi.org/10.1016/0092-8674(92)90520-M] [PMID: 1423611]
[39]
Brown CJ, Hendrich BD, Rupert JL, Lafrenière RG, Xing Y, Lawrence J, Willard HF (October 1992).. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 71(3): 527-42.
[40]
Ng K, Pullirsch D, Leeb M, Wutz A. Xist and the order of silencing (Review Article). EMBO Reports 2007; 8: 349.
[http://dx.doi.org/10.1038/sj.embor.7400871]
[41]
Chow JC, Yen Z, Ziesche SM, Brown CJ. Silencing of the mammalian X chromosome. Annu Rev Genomics Hum Genet 2005; 6: 69-92.
[http://dx.doi.org/10.1146/annurev.genom.6.080604.162350] [PMID: 16124854]
[42]
Chureau C, Chantalat S, Romito A, et al. Ftx is a non-coding RNA which affects Xist expression and chromatin structure within the X-inactivation center region. Hum Mol Genet 2011; 20(4): 705-18.
[http://dx.doi.org/10.1093/hmg/ddq516] [PMID: 21118898]
[43]
Tian D, Sun S, Lee JT. The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 2010; 143(3): 390-403.
[http://dx.doi.org/10.1016/j.cell.2010.09.049] [PMID: 21029862]
[44]
Lee JT, Davidow LS, Warshawsky D. Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 1999; 21(4): 400-4.
[http://dx.doi.org/10.1038/7734] [PMID: 10192391]
[45]
Augui S, Nora EP, Heard E. Regulation of X-chromosome inactivation by the X-inactivation centre. Nat Rev Genet 2011; 12(6): 429-42.
[http://dx.doi.org/10.1038/nrg2987] [PMID: 21587299]
[46]
Chureau C, Prissette M, Bourdet A, et al. Comparative sequence analysis of the X-inactivation center region in mouse, human, and bovine. Genome Res 2002; 12(6): 894-908.
[PMID: 12045143]
[47]
Brockdorff N, Ashworth A, Kay GF, et al. The product of the mouse Xist gene is a 15 kb inactive X-specific transcript containing no conserved ORF and located in the nucleus. Cell 1992; 71(3): 515-26.
[http://dx.doi.org/10.1016/0092-8674(92)90519-I] [PMID: 1423610]
[48]
Fang R, Moss WN, Rutenberg-Schoenberg M, Simon MD. probing xist rna structure in cells using targeted structure-seq. PLoS Genet 2015; 11(12) e1005668
[http://dx.doi.org/10.1371/journal.pgen.1005668] [PMID: 26646615]
[49]
Kawaguchi R, Kiryu H. Parallel computation of genome-scale RNA secondary structure to detect structural constraints on human genome. BMC Bioinformatics 2016; 17(1): 203.
[http://dx.doi.org/10.1186/s12859-016-1067-9] [PMID: 27153986]
[50]
Chu C, Zhang QC, da Rocha ST, et al. Systematic discovery of Xist RNA binding proteins. Cell 2015; 161(2): 404-16.
[http://dx.doi.org/10.1016/j.cell.2015.03.025] [PMID: 25843628]
[51]
da Rocha ST, Boeva V, Escamilla-Del-Arenal M, et al. Jarid2 is implicated in the initial Xist-induced targeting of PRC2 to the inactive X chromosome. Mol Cell 2014; 53(2): 301-16.
[http://dx.doi.org/10.1016/j.molcel.2014.01.002] [PMID: 24462204]
[52]
Sarma K, Levasseur P, Aristarkhov A, Lee JT. Locked nucleic acids (LNAs) reveal sequence requirements and kinetics of Xist RNA localization to the X chromosome. Proc Natl Acad Sci USA 2010; 107(51): 22196-201.
[http://dx.doi.org/10.1073/pnas.1009785107] [PMID: 21135235]
[53]
Cirillo D, Blanco M, Armaos A, et al. Quantitative predictions of protein interactions with long noncoding RNAs. Nat Methods 2016; 14(1): 5-6.
[http://dx.doi.org/10.1038/nmeth.4100] [PMID: 28032625]
[54]
McHugh CA, Chen CK, Chow A, et al. The Xist lncRNA interacts directly with SHARP to silence transcription through HDAC3. Nature 2015; 521(7551): 232-6.
[http://dx.doi.org/10.1038/nature14443] [PMID: 25915022]
[55]
Dominissini D, Moshitch-Moshkovitz S, Schwartz S, et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 2012; 485(7397): 201-6.
[http://dx.doi.org/10.1038/nature11112] [PMID: 22575960]
[56]
Patil DP, Chen CK, Pickering BF, et al. m(6)A RNA methylation promotes XIST-mediated transcriptional repression. Nature 2016; 537(7620): 369-73.
[http://dx.doi.org/10.1038/nature19342] [PMID: 27602518]
[57]
Shevchenko AI, Malakhova AA, Elisaphenko EA, et al. Variability of sequence surrounding the Xist gene in rodents suggests taxon-specific regulation of X chromosome inactivation. PLoS One 2011; 6(8) e22771
[http://dx.doi.org/10.1371/journal.pone.0022771] [PMID: 21826206]
[58]
Benoît MH, Hudson TJ, Maire G, et al. Global analysis of chromosome X gene expression in primary cultures of normal ovarian surface epithelial cells and epithelial ovarian cancer cell lines. Int J Oncol 2007; 30(1): 5-17.
[http://dx.doi.org/10.3892/ijo.30.1.5] [PMID: 17143508]
[59]
Kawakami T, Zhang C, Taniguchi T, et al. Characterization of loss-of-inactive X in Klinefelter syndrome and female-derived cancer cells. Oncogene 2004; 23(36): 6163-9.
[http://dx.doi.org/10.1038/sj.onc.1207808] [PMID: 15195139]
[60]
Ganesan S, Silver DP, Greenberg RA, et al. BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell 2002; 111(3): 393-405.
[http://dx.doi.org/10.1016/S0092-8674(02)01052-8] [PMID: 12419249]
[61]
Looijenga LH, Gillis AJ, van Gurp RJ, Verkerk AJ, Oosterhuis JW. X inactivation in human testicular tumors. XIST expression and androgen receptor methylation status. Am J Pathol 1997; 151(2): 581-90.
[PMID: 9250171]
[62]
Chen DL, Chen LZ, Lu YX, et al. Long noncoding RNA XIST expedites metastasis and modulates epithelial-mesenchymal transition in colorectal cancer. Cell Death Dis 2017; 8(8) e3011
[http://dx.doi.org/10.1038/cddis.2017.421] [PMID: 28837144]
[63]
Yu H, Xue Y, Wang P, et al. Knockdown of long non-coding RNA XIST increases blood-tumor barrier permeability and inhibits glioma angiogenesis by targeting miR-137. Oncogenesis 2017; 6(3) e303
[http://dx.doi.org/10.1038/oncsis.2017.7] [PMID: 28287613]
[64]
Chen X, Xiong D, Ye L, et al. Up-regulated lncRNA XIST contributes to progression of cervical cancer via regulating miR-140-5p and ORC1. Cancer Cell Int 2019; 19: 45.
[http://dx.doi.org/10.1186/s12935-019-0744-y] [PMID: 30858762]
[65]
Zhou X, Xu X, Gao C, Cui Y. XIST promote the proliferation and migration of non-small cell lung cancer cells via sponging miR-16 and regulating CDK8 expression. Am J Transl Res 2019; 11(9): 6196-206.
[PMID: 31632587]
[66]
Barati M, Ebrahim M. A gene expression profile of alzheimer’s disease using microarray technology. Zahedan J Res Med Sci 2016; 18(8) e7950
[http://dx.doi.org/10.17795/zjrms-7950]
[67]
Barati M, Ebrahimi M. Identification of genes involved in the early stages of Alzheimer disease using a neural network algorithm. Gene Cell Tissue 2016; 3(3) e38415
[http://dx.doi.org/10.17795/gct-38415]
[68]
Wang X, Wang C, Geng C, Zhao K. LncRNA XIST knockdown attenuates Aβ25-35-induced toxicity, oxidative stress, and apoptosis in primary cultured rat hippocampal neurons by targeting miR-132. Int J Clin Exp Pathol 2018; 11(8): 3915-24.
[PMID: 31949779]
[69]
Chanda K, Das S, Chakraborty J, et al. Altered levels of long NcRNAs Meg3 and Neat1 in cell and animal models of Huntington’s disease. RNA Biol 2018; 15(10): 1348-63.
[http://dx.doi.org/10.1080/15476286.2018.1534524] [PMID: 30321100]
[70]
Majumder P, Roy K, Singh BK, Jana NR, Mukhopadhyay D. Cellular levels of Grb2 and cytoskeleton stability are correlated in a neurodegenerative scenario. Dis Model Mech 2017; 10(5): 655-69.
[http://dx.doi.org/10.1242/dmm.027748] [PMID: 28360125]
[71]
Bamburg JR, Bloom GS. Cytoskeletal pathologies of Alzheimer disease. Cell Motil Cytoskeleton 2009; 66(8): 635-49.
[http://dx.doi.org/10.1002/cm.20388] [PMID: 19479823]
[72]
Liem RKH, Messing A. Dysfunctions of neuronal and glial intermediate filaments in disease. J Clin Invest 2009; 119(7): 1814-24.
[http://dx.doi.org/10.1172/JCI38003] [PMID: 19587456]
[73]
Ghosal K, Vogt DL, Liang M, Shen Y, Lamb BT, Pimplikar SW. Alzheimer’s disease-like pathological features in transgenic mice expressing the APP intracellular domain. Proc Natl Acad Sci USA 2009; 106(43): 18367-72.
[http://dx.doi.org/10.1073/pnas.0907652106] [PMID: 19837693]
[74]
Brown CJ, Ballabio A, Rupert JL, et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature 1991; 349(6304): 38-44.
[http://dx.doi.org/10.1038/349038a0] [PMID: 1985261]
[75]
Mielke MM, Vemuri P, Rocca WA. Clinical epidemiology of Alzheimer’s disease: Assessing sex and gender differences. Clin Epidemiol 2014; 6: 37-48.
[http://dx.doi.org/10.2147/CLEP.S37929] [PMID: 24470773]
[76]
Bajic VP, Essack M, Zivkovic L, et al. The X Files: “The mystery of X chromosome instability in Alzheimer’s disease". Front Genet 2020; 10: 1368.
[http://dx.doi.org/10.3389/fgene.2019.01368] [PMID: 32047510]
[77]
Yue D, Guanqun G, Jingxin L, et al. Silencing of long noncoding RNA XIST attenuated Alzheimer’s disease-related BACE1 alteration through miR-124. Cell Biol Int 2020; 44(2): 630-6.
[http://dx.doi.org/10.1002/cbin.11263] [PMID: 31743528]
[78]
Kerschbamer E, Biagioli M. Huntington’s disease as neurodevelopmental disorder: altered chromatin regulation, coding, and non-coding RNA transcription. Front Neurosci 2016; 9: 509.
[http://dx.doi.org/10.3389/fnins.2015.00509] [PMID: 26793052]
[79]
Seong IS, Woda JM, Song JJ, et al. Huntingtin facilitates polycomb repressive complex 2. Hum Mol Genet 2010; 19(4): 573-83.
[http://dx.doi.org/10.1093/hmg/ddp524] [PMID: 19933700]
[80]
Singer E, Walter C, Weber JJ, et al. Reduced cell size, chromosomal aberration and altered proliferation rates are characteristics and confounding factors in the STHdh cell model of Huntington disease. Sci Rep 2017; 7(1): 16880.
[http://dx.doi.org/10.1038/s41598-017-17275-4] [PMID: 29203806]
[81]
Jiang J, Jing Y, Cost GJ, et al. Translating dosage compensation to trisomy 21. Nature 2013; 500(7462): 296-300.
[http://dx.doi.org/10.1038/nature12394] [PMID: 23863942]
[82]
Kouznetsova VL, Tchekanov A, Li X, Yan X, Tsigelny IF. Polycomb repressive 2 complex-Molecular mechanisms of function. Protein Sci 2019; 28(8): 1387-99.
[http://dx.doi.org/10.1002/pro.3647] [PMID: 31095801]
[83]
van Bergeijk P, Seneviratne U, Aparicio-Prat E, Stanton R, Hasson SA. SRSF1 and PTBP1 are trans-acting factors that suppress the formation of a CD33 splicing isoform linked to Alzheimer’s disease risk. Mol Cell Biol 2019; 39(18): e00568-18.
[http://dx.doi.org/10.1128/MCB.00568-18] [PMID: 31208978]
[84]
Brouwers N, Bettens K, Gijselinck I, et al. Contribution of TARDBP to Alzheimer’s disease genetic etiology. J Alzheimers Dis 2010; 21(2): 423-30.
[http://dx.doi.org/10.3233/JAD-2010-100198] [PMID: 20555136]
[85]
Cohen D, Pilozzi A, Huang X. Network medicine approach for analysis of Alzheimer’s disease gene expression data. Int J Mol Sci 2020; 21(1): 332.
[http://dx.doi.org/10.3390/ijms21010332] [PMID: 31947790]