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CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Systematic Review Article

Role of Imaging Genetics in Alzheimer’s Disease: A Systematic Review and Current Update

Author(s): Aakash Chhetri, Kashish Goel, Abhilash Ludhiadch, Paramdeep Singh and Anjana Munshi*

Volume 23, Issue 9, 2024

Published on: 12 January, 2024

Page: [1143 - 1156] Pages: 14

DOI: 10.2174/0118715273264879231027070642

Price: $65

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Abstract

Background: Alzheimer’s disease is a neurodegenerative disorder characterized by severe cognitive, behavioral, and psychological symptoms, such as dementia, cognitive decline, apathy, and depression. There are no accurate methods to diagnose the disease or proper therapeutic interventions to treat AD. Therefore, there is a need for novel diagnostic methods and markers to identify AD efficiently before its onset. Recently, there has been a rise in the use of imaging techniques like Magnetic Resonance Imaging (MRI) and functional Magnetic Resonance Imaging (fMRI) as diagnostic approaches in detecting the structural and functional changes in the brain, which help in the early and accurate diagnosis of AD. In addition, these changes in the brain have been reported to be affected by variations in genes involved in different pathways involved in the pathophysiology of AD.

Methodology: A literature review was carried out to identify studies that reported the association of genetic variants with structural and functional changes in the brain in AD patients. Databases like PubMed, Google Scholar, and Web of Science were accessed to retrieve relevant studies. Keywords like ‘fMRI’, ‘Alzheimer’s’, ‘SNP’, and ‘imaging’ were used, and the studies were screened using different inclusion and exclusion criteria.

Results: 15 studies that found an association of genetic variations with structural and functional changes in the brain were retrieved from the literature. Based on this, 33 genes were identified to play a role in the development of disease. These genes were mainly involved in neurogenesis, cell proliferation, neural differentiation, inflammation and apoptosis. Few genes like FAS, TOM40, APOE, TRIB3 and SIRT1 were found to have a high association with AD. In addition, other genes that could be potential candidates were also identified.

Conclusion: Imaging genetics is a powerful tool in diagnosing and predicting AD and has the potential to identify genetic biomarkers and endophenotypes associated with the development of the disorder.

Keywords: Alzheimer’s disease, neurodegenerative disorder, functional magnetic resonance imaging, imaging genetics, structural endophenotypes, functional endophenotypes, Alzheimer’s disease neuroimaging initiative.

Graphical Abstract
[1]
Ferrari AJ, Somerville AJ, Baxter AJ, et al. Global variation in the prevalence and incidence of major depressive disorder: A systematic review of the epidemiological literature. Psychol Med 2013; 43(3): 471-81.
[http://dx.doi.org/10.1017/S0033291712001511] [PMID: 22831756]
[2]
Knopman DS, Jagust WJ, et al. Update on hypothetical model of Alzheimer’s disease biomarkers. Lancet Neurol 2013; 12(2): 207.
[http://dx.doi.org/10.1016/S1474-4422(12)70291-0] [PMID: 23332364]
[3]
Woolard AA, Heckers S. Anatomical and functional correlates of human hippocampal volume asymmetry. Psychiatry Res Neuroimaging 2012; 201(1): 48-53.
[http://dx.doi.org/10.1016/j.pscychresns.2011.07.016] [PMID: 22285719]
[4]
Medland SE, Jahanshad N, Neale BM, Thompson PM. Whole-genome analyses of whole-brain data: Working within an expanded search space. Nat Neurosci 2014; 17(6): 791-800.
[http://dx.doi.org/10.1038/nn.3718] [PMID: 24866045]
[5]
Hashimoto R, Ohi K, Yamamori H, et al. Imaging genetics and psychiatric disorders. Curr Mol Med 2015; 15(2): 168-75.
[http://dx.doi.org/10.2174/1566524015666150303104159] [PMID: 25732148]
[6]
Choudhury A, Sahu T, Ramanujam PL, et al. Neurochemicals, behaviours and psychiatric perspectives of neurological diseases. Neuropsychiatry 2018; 8(1): 395-424.
[http://dx.doi.org/10.4172/Neuropsychiatry.1000361]
[7]
Jiang W, King TZ, Turner JA. Imaging genetics towards a refined diagnosis of schizophrenia. Front Psychiatry 2019; 10: 494.
[http://dx.doi.org/10.3389/fpsyt.2019.00494] [PMID: 31354550]
[8]
Uher R, Zwicker A. Etiology in psychiatry: Embracing the reality of poly‐gene‐environmental causation of mental ill-ness. World Psychiatry 2017; 16(2): 121-9.
[http://dx.doi.org/10.1002/wps.20436] [PMID: 28498595]
[9]
Rasetti R, Weinberger DR. Intermediate phenotypes in psychiatric disorders. Curr Opin Genet Dev 2011; 21(3): 340-8.
[http://dx.doi.org/10.1016/j.gde.2011.02.003] [PMID: 21376566]
[10]
Zhang D, Wang Y, Zhou L, Yuan H, Shen D. Multimodal classification of Alzheimer’s disease and mild cognitive impairment. Neuroimage 2011; 55(3): 856-67.
[http://dx.doi.org/10.1016/j.neuroimage.2011.01.008] [PMID: 21236349]
[11]
Cash DM, Rohrer JD, Ryan NS, Ourselin S, Fox NC. Imaging endpoints for clinical trials in Alzheimer’s disease. Alzheimers Res Ther 2014; 6(9): 87.
[http://dx.doi.org/10.1186/s13195-014-0087-9] [PMID: 25621018]
[12]
Cuenco KT, Lunetta KL, Baldwin CT, et al. Association of distinct variants in SORL1 with cerebrovascular and neurodegenerative changes related to Alzheimer disease. Arch Neurol 2008; 65(12): 1640-8.
[13]
Joyner AH, Roddey CJ, Bloss CS, Dale AM. A common MECP2 haplotype associates with reduced cortical surface area in humans in two independent populations. Proc Natl Acad Sci USA 2009; 106(36): 15483-8.
[http://dx.doi.org/10.1073/pnas.0901866106] [PMID: 19717458]
[14]
Potkin SG, Guffanti G, Lakatos A, et al. Hippocampal atrophy as a quantitative trait in a genome-wide association study identifying novel susceptibility genes for Alzheimer’s disease. PLoS One 2009; 4(8): e6501.
[http://dx.doi.org/10.1371/journal.pone.0006501] [PMID: 19668339]
[15]
Erten-Lyons D, Jacobson A, Kramer P, Grupe A, Kaye J. The FAS gene, brain volume, and disease progression in Alzheimer’s disease. Alzheimers Dement 2010; 6(2): 118-24.
[http://dx.doi.org/10.1016/j.jalz.2009.05.663] [PMID: 19766542]
[16]
Stein JL, Hua X, Morra JH, et al. Genome-wide analysis reveals novel genes influencing temporal lobe structure with relevance to neurodegeneration in Alzheimer’s disease. Neuroimage 2010; 51(2): 542-54.
[http://dx.doi.org/10.1016/j.neuroimage.2010.02.068] [PMID: 20197096]
[17]
Shen L, Kim S, Risacher SL, et al. Whole genome association study of brain-wide imaging phenotypes for identifying quantitative trait loci in MCI and AD: A study of the ADNI cohort. Neuroimage 2010; 53(3): 1051-63.
[http://dx.doi.org/10.1016/j.neuroimage.2010.01.042] [PMID: 20100581]
[18]
Stein JL, Hua X, Lee S, et al. Voxelwise genome-wide association study (vGWAS). Neuroimage 2010; 53(3): 1160-74.
[http://dx.doi.org/10.1016/j.neuroimage.2010.02.032] [PMID: 20171287]
[19]
Hänggi J, Mondadori CRA, Buchmann A, Henke K, Hock CA. CYP46 T/C SNP modulates parahippocampal and hippocampal morphology in young subjects. Neurobiol Aging 2011; 32(6): 1023-32.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.07.001] [PMID: 19647891]
[20]
Furney SJ, Simmons A, Breen G, et al. Genome-wide association with MRI atrophy measures as a quantitative trait locus for Alzheimer’s disease. Mol Psychiatry 2011; 16(11): 1130-8.
[http://dx.doi.org/10.1038/mp.2010.123] [PMID: 21116278]
[21]
Khondoker M, Newhouse S, Westman E, et al. Linking genetics of brain changes to alzheimer’s disease: Sparse whole genome association scan of regional MRI volumes in the adni and addneuromed cohorts. J Alzheimers Dis 2015; 45(3): 851-64.
[http://dx.doi.org/10.3233/JAD-142214] [PMID: 25649652]
[22]
Lorenzi M, Altmann A, Gutman B, et al. Susceptibility of brain atrophy to TRIB3 in Alzheimer’s disease, evidence from functional prioritization in imaging genetics. Proc Natl Acad Sci USA 2018; 115(12): 3162-7.
[http://dx.doi.org/10.1073/pnas.1706100115] [PMID: 29511103]
[23]
Kim HR, Lee T, Choi JK, Jeong Y. Polymorphism in the MAGI2 gene modifies the effect of amyloid β on neurodegeneration. Alzheimer Dis Assoc Disord 2021; 35(2): 114-20.
[http://dx.doi.org/10.1097/WAD.0000000000000422] [PMID: 33323781]
[24]
Macedo A, Gómez C, Rebelo MÂ, et al. Risk variants in three alzheimer’s disease genes show association with EEG endophenotypes. J Alzheimers Dis 2021; 80(1): 209-23.
[http://dx.doi.org/10.3233/JAD-200963] [PMID: 33522999]
[25]
Franzmeier N, Ossenkoppele R, Brendel M, et al. The BIN1 rs744373 Alzheimer’s disease risk SNP is associated with faster Aβ-associated tau accumulation and cognitive decline. Alzheimers Dement 2022; 18(1): 103-15.
[http://dx.doi.org/10.1002/alz.12371] [PMID: 34060233]
[26]
Liu Y-B, et al. A genome-wide association study of longitudinal change in CSF tau among non-demented elders 2022.
[http://dx.doi.org/10.21203/rs.3.rs-1549485/v1]
[27]
Weiner MW, Veitch DP, Aisen PS, et al. The alzheimer’s disease neuroimaging initiative: A review of papers published since its inception. Alzheimers Dement 2013; 9(5): e111-94.
[http://dx.doi.org/10.1016/j.jalz.2013.05.1769] [PMID: 23932184]
[28]
Liu E, Luthman J, Cedarbaum JM, et al. Perspective: The alzheimer’s disease neuroimaging initiative and the role and contributions of the private partner scientific board (PPSB). Alzheimers Dement 2015; 11(7): 840-9.
[http://dx.doi.org/10.1016/j.jalz.2015.04.001] [PMID: 26194317]
[29]
Jones-Davis DM, Buckholtz N. The impact of the Alzheimer’s disease neuroimaging initiative 2: What role do public-private partnerships have in pushing the boundaries of clinical and basic science research on Alzheimer’s disease? Alzheimers Dement 2015; 11(7): 860-4.
[http://dx.doi.org/10.1016/j.jalz.2015.05.006] [PMID: 26194319]
[30]
Anderson DC, Kodukula K. Biomarkers in pharmacology and drug discovery. Biochem Pharmacol 2014; 87(1): 172-88.
[http://dx.doi.org/10.1016/j.bcp.2013.08.026] [PMID: 24001556]
[31]
Weiner MW, Veitch DP. Introduction to special issue: Overview of Alzheimer’s disease neuroimaging initiative. Alzheimers Dement 2015; 11(7): 730-3.
[http://dx.doi.org/10.1016/j.jalz.2015.05.007] [PMID: 26194308]
[32]
Villemagne VL, Kim SY, Rowe CC, Iwatsubo T. Imago mundi, imago AD, imago ADNI. Alzheimers Res Ther 2014; 6(5-8): 62.
[http://dx.doi.org/10.1186/s13195-014-0062-5] [PMID: 25478022]
[33]
Kadir A, Darreh-Shori T, Almkvist O, et al. PET imaging of the in vivo brain acetylcholinesterase activity and nicotine binding in galantamine-treated patients with AD. Neurobiol Aging 2008; 29(8): 1204-17.
[http://dx.doi.org/10.1016/j.neurobiolaging.2007.02.020] [PMID: 17379359]
[34]
Nordberg A. Amyloid imaging in Alzheimer’s disease. Neuropsychologia 2008; 46(6): 1636-41.
[http://dx.doi.org/10.1016/j.neuropsychologia.2008.03.020] [PMID: 18468648]
[35]
Jagust WJ, Landau SM, Koeppe RA, et al. The Alzheimer’s disease neuroimaging initiative 2 PET core: 2015. Alzheimers Dement 2015; 11(7): 757-71.
[http://dx.doi.org/10.1016/j.jalz.2015.05.001] [PMID: 26194311]
[36]
Landau SM, Fero A, Baker SL, et al. Measurement of longitudinal β-amyloid change with 18F-florbetapir PET and standardized uptake value ratios. J Nucl Med 2015; 56(4): 567-74.
[http://dx.doi.org/10.2967/jnumed.114.148981] [PMID: 25745095]
[37]
Chen K, Roontiva A, Thiyyagura P, et al. Improved power for characterizing longitudinal amyloid-β PET changes and evaluating amyloid-modifying treatments with a cerebral white matter reference region. J Nucl Med 2015; 56(4): 560-6.
[http://dx.doi.org/10.2967/jnumed.114.149732] [PMID: 25745091]
[38]
Chiotis K, Carter SF, Farid K, Savitcheva I, Nordberg A. Amyloid PET in european and north american cohorts; And exploring age as a limit to clinical use of amyloid imaging. Eur J Nucl Med Mol Imaging 2015; 42(10): 1492-506.
[http://dx.doi.org/10.1007/s00259-015-3115-5] [PMID: 26130168]
[39]
Landau SM, Thomas BA, Thurfjell L, et al. Amyloid PET imaging in Alzheimer’s disease: A comparison of three radiotracers. Eur J Nucl Med Mol Imaging 2014; 41(7): 1398-407.
[http://dx.doi.org/10.1007/s00259-014-2753-3] [PMID: 24647577]
[40]
Jack CR Jr, Barnes J, Bernstein MA, et al. Magnetic resonance imaging in Alzheimer’s disease neuroimaging initiative 2. Alzheimers Dement 2015; 11(7): 740-56.
[http://dx.doi.org/10.1016/j.jalz.2015.05.002] [PMID: 26194310]
[41]
Boccardi M, Bocchetta M, Apostolova LG, et al. Establishing magnetic resonance images orientation for the EADC-ADNI manual hippocampal segmentation protocol. J Neuroimaging 2014; 24(5): 509-14.
[http://dx.doi.org/10.1111/jon.12065] [PMID: 24279479]
[42]
Boccardi M, Bocchetta M, Ganzola R, et al. Operationalizing protocol differences for EADC-ADNI manual hippocampal segmentation. Alzheimers Dement 2015; 11(2): 184-94.
[http://dx.doi.org/10.1016/j.jalz.2013.03.001] [PMID: 23706515]
[43]
Boccardi M, Bocchetta M, Apostolova LG, et al. Delphi definition of the EADC-ADNI harmonized protocol for hippocampal segmentation on magnetic resonance. Alzheimers Dement 2015; 11(2): 126-38.
[http://dx.doi.org/10.1016/j.jalz.2014.02.009] [PMID: 25130658]
[44]
Frisoni GB, Jack CR. HarP: The EADC-ADNI harmonized protocol for manual hippocampal segmentation. In: A standard of reference from a global working group. 2015; pp. 107-10.
[45]
Apostolova LG, Zarow C, Biado K, et al. Relationship between hippocampal atrophy and neuropathology markers: A 7T MRI validation study of the EADC-ADNI harmonized hippocampal segmentation protocol. Alzheimers Dement 2015; 11(2): 139-50.
[http://dx.doi.org/10.1016/j.jalz.2015.01.001] [PMID: 25620800]
[46]
Sheng J, Xin Y, Zhang Q, Wang L, Yang Z, Yin J. Predictive classification of Alzheimer’s disease using brain imaging and genetic data. Sci Rep 2022; 12(1): 2405.
[http://dx.doi.org/10.1038/s41598-022-06444-9] [PMID: 35165327]
[47]
Small SA, Gandy S. Sorting through the cell biology of Alzheimer’s disease: Intracellular pathways to pathogenesis. Neuron 2006; 52(1): 15-31.
[http://dx.doi.org/10.1016/j.neuron.2006.09.001] [PMID: 17015224]
[48]
Moog U, Smeets EEJ, van Roozendaal KEP, et al. Neurodevelopmental disorders in males related to the gene causing Rett syndrome in females (MECP2). Eur J Paediatr Neurol 2003; 7(1): 5-12.
[http://dx.doi.org/10.1016/S1090-3798(02)00134-4] [PMID: 12615169]
[49]
Kurian JR, Forbes-Lorman RM, Auger AP. Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics 2007; 2(3): 173-8.
[http://dx.doi.org/10.4161/epi.2.3.4841] [PMID: 17965589]
[50]
Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science 2001; 292(5521): 1552-5.
[http://dx.doi.org/10.1126/science.292.5521.1552] [PMID: 11375494]
[51]
Irie K, Murakami K, Masuda Y, et al. The toxic conformation of the 42-residue amyloid beta peptide and its relevance to oxidative stress in Alzheimer’s disease. Mini Rev Med Chem 2007; 7(10): 1001-8.
[http://dx.doi.org/10.2174/138955707782110187] [PMID: 17979802]
[52]
Noren NK, Pasquale EB. Eph receptor–ephrin bidirectional signals that target Ras and Rho proteins. Cell Signal 2004; 16(6): 655-66.
[http://dx.doi.org/10.1016/j.cellsig.2003.10.006] [PMID: 15093606]
[53]
Feuk L, Prince J, Breen G, et al. Apolipoprotein-E dependent role for the FAS receptor in early onset Alzheimer’s disease: Finding of a positive association for a polymorphism in the TNFRSF6 gene. Hum Genet 2000; 107(4): 391-6.
[http://dx.doi.org/10.1007/s004390000383] [PMID: 11129341]
[54]
He X, Zhang Z, Zhang J, et al. The Fas gene A-670G polymorphism is not associated with sporadic Alzheimer disease in a Chinese Han population. Brain Res 2006; 1082(1): 192-5.
[http://dx.doi.org/10.1016/j.brainres.2006.01.086] [PMID: 16703675]
[55]
Theuns J, Feuk L, Dermaut B, et al. TheTNFRSF6 gene is not implicated in familial early-onset Alzheimer’s disease. Hum Genet 2001; 108(6): 552-3.
[http://dx.doi.org/10.1007/s004390100508] [PMID: 11499683]
[56]
Rosenmann H, Meiner Z, Kahana E, et al. The Fas promoter polymorphism at position -670 is not associated with late-onset sporadic Alzheimer’s disease. Dement Geriatr Cogn Disord 2004; 17(3): 143-6.
[http://dx.doi.org/10.1159/000076347] [PMID: 14739535]
[57]
Peper JS, Brouwer RM, Boomsma DI, Kahn RS, Hulshoff Pol HE. Genetic influences on human brain structure: A review of brain imaging studies in twins. Hum Brain Mapp 2007; 28(6): 464-73.
[http://dx.doi.org/10.1002/hbm.20398] [PMID: 17415783]
[58]
Andreoli V, De Marco EV, Trecroci F, Cittadella R, Di Palma G, Gambardella A. Potential involvement of GRIN2B encoding the NMDA receptor subunit NR2B in the spectrum of Alzheimer’s disease. J Neural Transm (Vienna) 2014; 121(5): 533-42.
[PMID: 24292895]
[59]
Chang CH, Lin CH, Lane HY. d-glutamate and Gut Microbiota in Alzheimer’s Disease. Int J Mol Sci 2020; 21(8): 2676.
[http://dx.doi.org/10.3390/ijms21082676] [PMID: 32290475]
[60]
van den Oord EJCG, Kuo PH, Hartmann AM, et al. Genomewide association analysis followed by a replication study implicates a novel candidate gene for neuroticism. Arch Gen Psychiatry 2008; 65(9): 1062-71.
[http://dx.doi.org/10.1001/archpsyc.65.9.1062] [PMID: 18762592]
[61]
Lau WL, Scholnick SB. Identification of two new members of the CSMD gene family. Genomics 2003; 82(3): 412-5.
[http://dx.doi.org/10.1016/S0888-7543(03)00149-6] [PMID: 12906867]
[62]
Brunk I, Blex C, Speidel D, Brose N, Ahnert-Hilger G. Ca2+-dependent activator proteins of secretion promote vesicular monoamine uptake. J Biol Chem 2009; 284(2): 1050-6.
[http://dx.doi.org/10.1074/jbc.M805328200] [PMID: 19008227]
[63]
Cisternas FA, Vincent JB, Scherer SW, Ray PN. Cloning and characterization of human CADPS and CADPS2, new members of the Ca2+-dependent activator for secretion protein family. Genomics 2003; 81(3): 279-91.
[http://dx.doi.org/10.1016/S0888-7543(02)00040-X] [PMID: 12659812]
[64]
Sadakata T, Washida M, Iwayama Y, et al. Autistic-like phenotypes in Cadps2-knockout mice and aberrant CADPS2 splicing in autistic patients. J Clin Invest 2007; 117(4): 931-43.
[http://dx.doi.org/10.1172/JCI29031] [PMID: 17380209]
[65]
Poejo J, Salazar J, Mata AM, Gutierrez-Merino C. The relevance of amyloid β-calmodulin complexation in neurons and brain degeneration in Alzheimer’s disease. Int J Mol Sci 2021; 22(9): 4976.
[http://dx.doi.org/10.3390/ijms22094976] [PMID: 34067061]
[66]
Mirzaa GM, Chong JX, Piton A, et al. De novo and inherited variants in ZNF292 underlie a neurodevelopmental disorder with features of autism spectrum disorder. Genet Med 2020; 22(3): 538-46.
[http://dx.doi.org/10.1038/s41436-019-0693-9] [PMID: 31723249]
[67]
Harold D, Abraham R, Hollingworth P, et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer’s disease. Nat Genet 2009; 41(10): 1088-93.
[http://dx.doi.org/10.1038/ng.440] [PMID: 19734902]
[68]
Parisiadou L, Bethani I, Michaki V, Krousti K, Rapti G, Efthimiopoulos S. Homer2 and Homer3 interact with amyloid precursor protein and inhibit Aβ production. Neurobiol Dis 2008; 30(3): 353-64.
[http://dx.doi.org/10.1016/j.nbd.2008.02.004] [PMID: 18387811]
[69]
Antonell A, Gelpi E, Sánchez-Valle R, Martínez R, Molinuevo JL, Lladó A. Breakpoint sequence analysis of an AβPP locus duplication associated with autosomal dominant Alzheimer’s disease and severe cerebral amyloid angiopathy. J Alzheimers Dis 2012; 28(2): 303-8.
[http://dx.doi.org/10.3233/JAD-2011-110911] [PMID: 22008262]
[70]
Guffanti G, Torri F, Rasmussen J, et al. Increased CNV-Region deletions in mild cognitive impairment (MCI) and Alzheimer’s disease (AD) subjects in the ADNI sample. Genomics 2013; 102(2): 112-22.
[http://dx.doi.org/10.1016/j.ygeno.2013.04.004] [PMID: 23583670]
[71]
Mirnics ZK, Mirnics K, Terrano D, Lewis DA, Sisodia SS, Schor NF. DNA microarray profiling of developing PS1-deficient mouse brain reveals complex and coregulated expression changes. Mol Psychiatry 2003; 8(10): 863-78.
[http://dx.doi.org/10.1038/sj.mp.4001389] [PMID: 14515137]
[72]
Tomashevski A, Husseman J, Jin LW, Nochlin D, Vincent I. Constitutive Wee1 activity in adult brain neurons with M phase-type alterations in Alzheimer neurodegeneration. J Alzheimers Dis 2001; 3(2): 195-207.
[http://dx.doi.org/10.3233/JAD-2001-3205] [PMID: 12214061]
[73]
Crowther RA. Straight and paired helical filaments in Alzheimer disease have a common structural unit. Proc Natl Acad Sci USA 1991; 88(6): 2288-92.
[http://dx.doi.org/10.1073/pnas.88.6.2288] [PMID: 1706519]
[74]
Montalvo-Ortiz JL, Cheng Z, Kranzler HR, Zhang H, Gelernter J. Genomewide study of epigenetic biomarkers of opioid dependence in european- american women. Sci Rep 2019; 9(1): 4660.
[http://dx.doi.org/10.1038/s41598-019-41110-7] [PMID: 30874594]
[75]
Gabay C, Lamacchia C, Palmer G. IL-1 pathways in inflammation and human diseases. Nat Rev Rheumatol 2010; 6(4): 232-41.
[http://dx.doi.org/10.1038/nrrheum.2010.4] [PMID: 20177398]
[76]
Rothwell N, Luheshi GN. Interleukin 1 in the brain: Biology, pathology and therapeutic target. Trends Neurosci 2000; 23(12): 618-25.
[http://dx.doi.org/10.1016/S0166-2236(00)01661-1] [PMID: 11137152]
[77]
Anderson JM, Hampton DW, Patani R, et al. Abnormally phosphorylated tau is associated with neuronal and axonal loss in experimental autoimmune encephalomyelitis and multiple sclerosis. Brain 2008; 131(7): 1736-48.
[http://dx.doi.org/10.1093/brain/awn119] [PMID: 18567922]
[78]
Mondragón-Rodríguez S, Salas-Gallardo A, González-Pereyra P, et al. Phosphorylation of Tau protein correlates with changes in hippocampal theta oscillations and reduces hippocampal excitability in Alzheimer’s model. J Biol Chem 2018; 293(22): 8462-72.
[http://dx.doi.org/10.1074/jbc.RA117.001187] [PMID: 29632073]
[79]
Hashimoto Y, Toyama Y, Kusakari S, Nawa M, Matsuoka M. An alzheimer disease-linked rare mutation potentiates netrin receptor uncoordinated-5c-induced signaling that merges with amyloid β precursor protein signaling. J Biol Chem 2016; 291(23): 12282-93.
[http://dx.doi.org/10.1074/jbc.M115.698092] [PMID: 27068745]
[80]
Wetzel-Smith MK, Hunkapiller J, Bhangale TR, et al. A rare mutation in UNC5C predisposes to late-onset Alzheimer’s disease and increases neuronal cell death. Nat Med 2014; 20(12): 1452-7.
[http://dx.doi.org/10.1038/nm.3736] [PMID: 25419706]
[81]
McNeill EM, Roos KP, Moechars D, Clagett-Dame M. Nav2 is necessary for cranial nerve development and blood pressure regulation. Neural Dev 2010; 5(1): 6.
[http://dx.doi.org/10.1186/1749-8104-5-6] [PMID: 20184720]
[82]
Marzinke MA, Mavencamp T, Duratinsky J, Clagett-Dame M. 14-3-3ε and NAV2 interact to regulate neurite outgrowth and axon elongation. Arch Biochem Biophys 2013; 540(1-2): 94-100.
[http://dx.doi.org/10.1016/j.abb.2013.10.012] [PMID: 24161943]
[83]
De Rossi P, Nomura T, Andrew RJ, et al. Neuronal BIN1 regulates presynaptic neurotransmitter release and memory consolidation. Cell Rep 2020; 30(10): 3520-3535.e7.
[http://dx.doi.org/10.1016/j.celrep.2020.02.026] [PMID: 32160554]
[84]
Voskobiynyk Y, Roth JR, Cochran JN, et al. Alzheimer’s disease risk gene BIN1 induces Tau-dependent network hyperexcitability. eLife 2020; 9: e57354.
[http://dx.doi.org/10.7554/eLife.57354] [PMID: 32657270]
[85]
Crotti A, Sait HR, McAvoy KM, et al. BIN1 favors the spreading of Tau via extracellular vesicles. Sci Rep 2019; 9(1): 9477.
[http://dx.doi.org/10.1038/s41598-019-45676-0] [PMID: 31263146]
[86]
Shen L, Thompson PM. Brain imaging genomics: Integrated analysis and machine learning. Proc IEEE 2020; 108(1): 125-62.
[http://dx.doi.org/10.1109/JPROC.2019.2947272] [PMID: 31902950]
[87]
Yiannopoulou KG, Papageorgiou SG. Current and future treatments in Alzheimer disease: An update. J Cent Nerv Syst Dis 2020; 12.
[http://dx.doi.org/10.1177/1179573520907397] [PMID: 32165850]

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