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Transcriptomics Meta-Analysis Reveals Phagosome and Innate Immune System Dysfunction as Potential Mechanisms in the Cortex of Alzheimer’s Disease Mouse Strains

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Abstract

Immune-related pathways can affect the immune system directly, such as the chemokine signaling pathway, or indirectly, such as the phagosome pathway. Alzheimer’s disease (AD) is reportedly associated with several immune-related pathways. However, exploring its underlying mechanism is challenging in animal studies because AD mouse strains differentially express immune-related pathway characteristics. To overcome this problem, we performed a meta-analysis to identify significant and consistent immune-related AD pathways that are expressed in different AD mouse strains. Next-generation RNA sequencing (RNA-seq) and microarray datasets for the cortex of AD mice from different strains such as APP/PSEN1, APP/PS2, 3xTg, TREM, and 5xFAD were collected from the NCBI GEO database. Each dataset’s quality control and normalization were already processed from each original study source using various methods depending on the high-throughput analysis platform (FastQC, median of ratios, RMA, between array normalization). Datasets were analyzed using DESeq2 for RNA-seq and GEO2R for microarray to identify differentially expressed (DE) genes. Significantly DE genes were meta-analyzed using Stouffer’s method, with significant genes further analyzed for functional enrichment. Ten datasets representing 20 conditions were obtained from the NCBI GEO database, comprising 116 control and 120 AD samples. The DE analysis identified 284 significant DE genes. The meta-analysis identified three significantly enriched immune-related AD pathways: phagosome, the complement and coagulation cascade, and chemokine signaling. Phagosomes-related genes correlated with complement and immune system. Meanwhile, phagosomes and chemokine signaling genes overlapped with B cells receptors pathway genes indicating potential correlation between phagosome, chemokines, and adaptive immune system as well. The transcriptomic meta-analysis showed that AD is associated with immune-related pathways in the brain’s cortex through the phagosome, complement and coagulation cascade, and chemokine signaling pathways. Interestingly, phagosome and chemokine signaling pathways had potential correlation with B cells receptors pathway.

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Availability of Data and Materials

The data in this meta-analysis can be accessed from NCBI GEO website. All data generated or analyzed during this study are included in this published article and supplementary tables.

References

  • Aken BL, Ayling S, Barrell D, Clarke L, Curwen V, Fairley S et al (2016) The Ensembl gene annotation system. Database (Oxford) baw093

  • Bagaria J, Nho K, An SSA (2021) Importance of GWAS in finding un-targeted genetic association of sporadic Alzheimer’s disease. Mol Cell Toxicol 17(3):233–244

    Article  CAS  Google Scholar 

  • Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M et al (2013) NCBI GEO: archive for functional genomics data sets--update. Nucleic Acids Res 41(Database issue):D991–D995

  • Berkowitz S, Chapman J, Dori A, Gofrit SG, Maggio N, Shavit-Stein E (2021) Complement and coagulation system crosstalk in synaptic and neural conduction in the central and peripheral nervous systems. Biomedicines 9(12):1–15

    Article  Google Scholar 

  • Boon BDC, Hoozemans JJM, Lopuhaä B, Eigenhuis KN, Scheltens P, Kamphorst W et al (2018) Neuroinflammation is increased in the parietal cortex of atypical Alzheimer’s disease. J Neuroinflammation 15(1):170

    Article  PubMed  PubMed Central  Google Scholar 

  • Britschgi M, Takeda-Uchimura Y, Rockenstein E, Johns H, Masliah E, Wyss-Coray T (2012) Deficiency of terminal complement pathway inhibitor promotes neuronal tau pathology and degeneration in mice. J Neuroinflammation 9(1):220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brooks LRK, Mias GI (2019) Data-driven analysis of age, sex, and tissue effects on gene expression variability in Alzheimer’s disease. Front Neurosci 13:21

    Article  Google Scholar 

  • Bulati M, Buffa S, Martorana A, Gervasi F, Camarda C, Azzarello DM et al (2015) Double negative (IgG(+)IgD(-)CD27(-)) B cells are increased in a cohort of moderate-severe Alzheimer’s disease patients and show a pro-inflammatory trafficking receptor phenotype. J Alzheimers Dis 44(4):1241–1251

    Article  CAS  PubMed  Google Scholar 

  • Carbajosa G, Malki K, Lawless N, Wang H, Ryder JW, Wozniak E et al (2018) Loss of Trem2 in microglia leads to widespread disruption of cell coexpression networks in mouse brain. Neurobiol Aging 69:151–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo E, Leon J, Mazzei G, Abolhassani N, Haruyama N, Saito T et al (2017) Comparative profiling of cortical gene expression in Alzheimer’s disease patients and mouse models demonstrates a link between amyloidosis and neuroinflammation. Sci Rep 7(1):17762

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang L-C, Lin H-M, Sibille E, Tseng GC (2013) Meta-analysis methods for combining multiple expression profiles: comparisons, statistical characterization and an application guideline. BMC Bioinformatics 14:368-

  • Daborg J, Andreasson U, Pekna M, Lautner R, Hanse E, Minthon L et al (2012) Cerebrospinal fluid levels of complement proteins C3, C4 and CR1 in Alzheimer’s disease. J Neural Transm 119(7):789–797

    Article  CAS  PubMed  Google Scholar 

  • Das S, Li Z, Noori A, Hyman BT, Serrano-Pozo A (2020) Meta-analysis of mouse transcriptomic studies supports a context-dependent astrocyte reaction in acute CNS injury versus neurodegeneration. J Neuroinflammation 17(1):227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dewey M (2019) Metap: meta-analysis of significance values. R Package Version 11

  • Faridar A, Vasquez M, Thome AD, Yin Z, Xuan H, Wang JH et al (2022) Ex vivo expanded human regulatory T cells modify neuroinflammation in a preclinical model of Alzheimer’s disease. Acta Neuropathol Commun 10(1):144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng WX, Zhang YL, Wang Z, Xu HR, Wu T, Marshall C et al (2020) Microglia prevent beta-amyloid plaque formation in the early stage of an Alzheimer’s disease mouse model with suppression of glymphatic clearance. Alzheimers Res Ther 12(1):15

    Article  Google Scholar 

  • Ferretti MT, Merlini M, Spani C, Gericke C, Schweizer N, Enzmann G et al (2016) T-cell brain infiltration and immature antigen-presenting cells in transgenic models of Alzheimer’s disease-like cerebral amyloidosis. Brain Behav Immun 54:211–225

    Article  CAS  PubMed  Google Scholar 

  • Forero AD (2019) Available software for meta-analyses of genome-wide expression studies. Curr Genomics 20(5):325–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedman BA, Srinivasan K, Ayalon G, Meilandt WJ, Lin H, Huntley MA et al (2018) Diverse brain myeloid expression profiles reveal distinct microglial activation states and aspects of Alzheimer’s disease not evident in mouse models. Cell Rep 22(3):832–847

    Article  CAS  PubMed  Google Scholar 

  • Frost GR, Jonas LA, Li Y-M (2019) Friend, foe or both? Immune activity in Alzheimer’s disease. Front Aging Neurosci 11:1–20

    Article  Google Scholar 

  • Fujimoto M, Fujimoto Y, Poe JC, Jansen PJ, Lowell CA, DeFranco AL et al (2000) CD19 regulates Src family protein tyrosine kinase activation in B lymphocytes through processive amplification. Immunity 13(1):47–57

    Article  CAS  PubMed  Google Scholar 

  • Hampel H, Lista S, Neri C, Vergallo A (2019) Time for the systems-level integration of aging: resilience enhancing strategies to prevent Alzheimer’s disease. Prog Neurobiol 181:21

    Article  Google Scholar 

  • Haure-Mirande JV, Audrain M, Fanutza T, Kim SH, Klein WL, Glabe C et al (2017) Deficiency of TYROBP, an adapter protein for TREM2 and CR3 receptors, is neuroprotective in a mouse model of early Alzheimer’s pathology. Acta Neuropathol 134(5):769–788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He B, Chen W, Zeng JS, Tong WS, Zheng P (2020) MicroRNA-326 decreases tau phosphorylation and neuron apoptosis through inhibition of the JNK signaling pathway by targeting VAV1 in Alzheimer’s disease. J Cell Physiol 235(1):480–493

    Article  CAS  PubMed  Google Scholar 

  • Ibanez KR, McFarland KN, Phillips J, Allen M, Lessard CB, Zobel L et al (2022) Deletion of Abi3/Gngt2 influences age-progressive amyloid beta and tau pathologies in distinctive ways. Alzheimers Res Ther 14(1):27

    Article  Google Scholar 

  • Islam R, Rajan R, Choudhary H, Vrionis F, Hanafy KA (2022) Gender differences in Alzheimer’s may be associated with TLR4-LYN expression in damage associated microglia and neuronal phagocytosis. J Cell Physiol 11:1–11

    Google Scholar 

  • Jacobs HIL, Radua J, Luckmann HC, Sack AT (2013) Meta-analysis of functional network alterations in Alzheimer’s disease: toward a network biomarker. Neurosci Biobehav Rev 37(5):753–765

    Article  PubMed  Google Scholar 

  • Kam TI, Song S, Gwon Y, Park H, Yan JJ, Im I et al (2013) FcγRIIb mediates amyloid-β neurotoxicity and memory impairment in Alzheimer’s disease. J Clin Invest 123(7):2791–2802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28(1):27–30

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kodamullil AT, Iyappan A, Karki R, Madan S, Younesi E, Hofmann-Apitius M (2017) Of mice and men: comparative analysis of neuro-inflammatory mechanisms in human and mouse using cause-and-effect models. J Alzheimers Dis 59(3):1045–1055

    Article  PubMed  PubMed Central  Google Scholar 

  • Li T, Zhu J (2019) Entanglement of CCR5 and Alzheimer’s disease. Front Aging Neurosci 11:209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu C, Zhang X, Chai H, Xu S, Liu Q, Luo Y et al (2022) Identification of immune cells and key genes associated with Alzheimer’s disease. Int J Med Sci 19(1):112–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo W, Brouwer C (2013) Pathview: an R/Bioconductor package for pathway-based data integration and visualization. Bioinformatics 29(14):1830–1831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsh SE, Abud EM, Lakatos A, Karimzadeh A, Yeung ST, Davtyan H et al (2016) The adaptive immune system restrains Alzheimer’s disease pathogenesis by modulating microglial function. Proc Natl Acad Sci U S A 113(9):E1316–E1325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martín-Sánchez A, Piñero J, Nonell L, Arnal M, Ribe EM, Nevado-Holgado A et al (2021) Comorbidity between Alzheimer’s disease and major depression: a behavioural and transcriptomic characterization study in mice. Alzheimer’s Res Ther 13(1):73

    Article  Google Scholar 

  • Mattson MP (2002) Oxidative stress, perturbed calcium homeostasis, and immune dysfunction in Alzheimer’s disease. J Neurovirol 8(6):539–550

    Article  CAS  PubMed  Google Scholar 

  • Momtazmanesh S, Perry G, Rezaei N (2020) Toll-like receptors in Alzheimer’s disease. J Neuroimmunol 348:14

    Article  Google Scholar 

  • Morgan SL, Naderi P, Koler K, Pita-Juarez Y, Prokopenko D, Vlachos IS et al (2022) Most pathways can be related to the pathogenesis of Alzheimer’s disease. Front Aging Neurosci 14:1–13

    Article  CAS  Google Scholar 

  • Muraoka S, Jedrychowski MP, Iwahara N, Abdullah M, Onos KD, Keezer KJ et al (2021) Enrichment of neurodegenerative microglia signature in brain-derived extracellular vesicles isolated from Alzheimer’s disease mouse models. J Proteome Res 20(3):1733–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myhre O, Utkilen H, Duale N, Brunborg G, Hofer T (2013) Metal dyshomeostasis and inflammation in Alzheimer’s and Parkinson’s diseases: possible impact of environmental exposures. Oxid Med Cell Longev 2013:726954

    Article  PubMed  PubMed Central  Google Scholar 

  • Nixon RA (2020) The aging lysosome: an essential catalyst for late-onset neurodegenerative diseases. Biochim Biophys Acta Proteins Proteom 1868(9):140443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orre M, Kamphuis W, Osborn LM, Jansen AHP, Kooijman L, Bossers K et al (2014) Isolation of glia from Alzheimer’s mice reveals inflammation and dysfunction. Neurobiol Aging 35(12):2746–2760

    Article  CAS  PubMed  Google Scholar 

  • Oyelami T DBA, Van den Wyngaert I, Van Hoorde K, Dewachter I, Kemp J (2020) Transcriptional gender specific changes in the APP/PS1 mouse model of Alzheimer’s disease pathology NCBI GEO database. [Available from: https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE85162

  • Pagoni P, Korologou-Linden RS, Howe LD, Davey Smith G, Ben-Shlomo Y, Stergiakouli E et al (2022) Causal effects of circulating cytokine concentrations on risk of Alzheimer’s disease and cognitive function. Brain Behav Immun 104:54–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panda C, Mahapatra RK (2022) Bi-directional relationship between autophagy and inflammasomes in neurodegenerative disorders. Cell Mol Neurobiol 23:115–137

    Google Scholar 

  • Paranjpe MD, Belonwu S, Wang JK, Oskotsky T, Gupta A, Taubes A et al (2021) Sex-specific cross tissue meta-analysis identifies immune dysregulation in women with Alzheimer’s disease. Front Aging Neurosci 13:19

    Article  Google Scholar 

  • Park YH, Hodges A, Risacher SL, Lin K, Jang JW, Ahn S et al (2020) Dysregulated Fc gamma receptor-mediated phagocytosis pathway in Alzheimer’s disease: network-based gene expression analysis. Neurobiol Aging 88:24–32

    Article  PubMed  Google Scholar 

  • Patel H, Dobson RJB, Newhouse SJ (2019) A meta-analysis of Alzheimer’s disease brain transcriptomic data. J Alzheimers Dis 68(4):1635–1656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phung DM, Lee J, Hong S, Kim YE, Yoon J, Kim YJ (2020) Meta-analysis of differentially expressed genes in the substantia nigra in Parkinson’s disease supports phenotype-specific transcriptome changes. Front Neurosci 14:596105

    Article  PubMed  PubMed Central  Google Scholar 

  • Pritchard NR, Smith KG (2003) B cell inhibitory receptors and autoimmunity. Immunology 108(3):263–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Propson NE, Gedam M, Zheng H (2021) Complement in neurologic disease. Annu Rev Pathol Mech Dis 16(1):277–298

    Article  CAS  Google Scholar 

  • Puntambekar SS, Moutinho M, Lin PB-C, Jadhav V, Tumbleson-Brink D, Balaji A et al (2022) CX3CR1 deficiency aggravates amyloid driven neuronal pathology and cognitive decline in Alzheimer’s disease. Mol Neurodegener 17(1):47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholefield M, Church SJ, Xu J, Robinson AC, Gardiner NJ, Roncaroli F et al (2020) Effects of alterations of post-mortem delay and other tissue-collection variables on metabolite levels in human and rat brain. Metabolites 10(11):438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi X, Ohta Y, Liu X, Shang J, Morihara R, Nakano Y et al (2019) Chronic cerebral hypoperfusion activates the coagulation and complement cascades in Alzheimer’s disease mice. Neuroscience 416:126–136

    Article  CAS  PubMed  Google Scholar 

  • Shukla U, Hatani T, Nakashima K, Ogi K, Sada K (2009) Tyrosine phosphorylation of 3BP2 regulates B cell receptor-mediated activation of NFAT*. J Biol Chem 284(49):33719–33728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srinivasan K, Friedman BA, Larson JL, Lauffer BE, Goldstein LD, Appling LL et al (2016) Untangling the brain’s neuroinflammatory and neurodegenerative transcriptional responses. Nat Commun 7(1):11295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St-Amour I, Cicchetti F, Calon F (2016) Immunotherapies in Alzheimer’s disease: too much, too little, too late or off-target? Acta Neuropathol 131(4):481–504

    Article  CAS  PubMed  Google Scholar 

  • Su L, Chen S, Zheng C, Wei H, Song X (2019) Meta-analysis of gene expression and identification of biological regulatory mechanisms in Alzheimer’s disease. Front Neurosci 13:633

    Article  PubMed  PubMed Central  Google Scholar 

  • Sykora P, Misiak M, Wang Y, Ghosh S, Leandro GS, Liu D et al (2015) DNA polymerase β deficiency leads to neurodegeneration and exacerbates Alzheimer disease phenotypes. Nucleic Acids Res 43(2):943–959

    Article  CAS  PubMed  Google Scholar 

  • Tokar T, Pastrello C, Jurisica I (2020) GSOAP: a tool for visualization of gene set over-representation analysis. Bioinformatics 36(9):2923–2925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Ba IAT, Marchal S, Francois F, Silhol M, Lleres C, Michel B et al (2012) Regenerating Islet-derived 1 alpha (Reg-1 alpha) protein is new neuronal secreted factor that stimulates neurite outgrowth via exostosin tumor-like 3 (EXTL3) receptor. J Biol Chem 287(7):4726–4739

    Article  CAS  Google Scholar 

  • vom Berg J, Prokop S, Miller KR, Obst J, Kalin RE, Lopategui-Cabezas I et al (2012) Inhibition of IL-12/IL-23 signaling reduces Alzheimer’s disease-like pathology and cognitive decline. Nat Med 18(12):1812-+

  • Walker RL (2006) Human and animal subjects of research: the moral significance of respect versus welfare. Theor Med Bioeth 27(4):305–331

    Article  PubMed  Google Scholar 

  • Wang WY, Tan MS, Yu JT, Tan L (2015) Role of pro-inflammatory cytokines released from microglia in Alzheimer’s disease. Ann Transl Med 3(10):136

    PubMed  PubMed Central  Google Scholar 

  • Wang E, Zhu H, Wang X, Gower AC, Wallack M, Blusztajn JK et al (2017) Amylin treatment reduces neuroinflammation and ameliorates abnormal patterns of gene expression in the cerebral cortex of an Alzheimer’s disease mouse model. J Alzheimer’s Dis 56:47–61

    Article  Google Scholar 

  • Wang MM, Miao D, Cao XP, Tan L, Tan L (2018) Innate immune activation in Alzheimer’s disease. Ann Transl Med 6(10):14

    Article  Google Scholar 

  • Wang MH, Song WM, Ming C, Wang Q, Zhou XX, Xu P et al (2022) Guidelines for bioinformatics of single-cell sequencing data analysis in Alzheimer’s disease: review, recommendation, implementation and application. Mol Neurodegener 17(1):52

    Article  Google Scholar 

  • Whyte LS, Hassiotis S, Hattersley KJ, Hemsley KM, Hopwood JJ, Lau AA et al (2020) Lysosomal dysregulation in the murine AppNL-G-F/NL-G-F model of Alzheimer’s disease. Neuroscience 429:143–155

    Article  CAS  PubMed  Google Scholar 

  • Xue F, Du H (2021) TREM2 mediates microglial anti-inflammatory activations in Alzheimer’s disease: lessons learned from transcriptomics. Cells 10(2):14

    Article  Google Scholar 

  • Yamashima T (2013) Reconsider Alzheimer’s disease by the ‘calpain–cathepsin hypothesis’—a perspective review. Prog Neurobiol 105:1–23

    Article  CAS  PubMed  Google Scholar 

  • Yin W, Cerda-Hernández N, Castillo-Morales A, Ruiz-Tejada-Segura ML, Monzón-Sandoval J, Moreno-Castilla P et al (2020) Transcriptional, behavioral and biochemical profiling in the 3xTg-AD mouse model reveals a specific signature of amyloid deposition and functional decline in Alzheimer’s disease. Front Neurosci 14:1–12

    Article  Google Scholar 

  • Yokoyama M, Kobayashi H, Tatsumi L, Tomita T (2022) Mouse models of Alzheimer’s disease. Front Mol Neurosci 15:1–14

    Article  Google Scholar 

  • Yu G, Wang L-G, Han Y, He Q-Y (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16(5):284–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu JT, Xu W, Tan CC, Andrieu S, Suckling J, Evangelou E et al (2020) Evidence-based prevention of Alzheimer’s disease: systematic review and meta-analysis of 243 observational prospective studies and 153 randomised controlled trials. J Neurol Neurosurg Psychiatry 91(11):1201–1209

    Article  PubMed  Google Scholar 

  • Yuen SC, Zhu H, Leung S-W (2020) A systematic bioinformatics workflow with meta-analytics identified potential pathogenic factors of Alzheimer’s disease. Front Neurosci 14:1–23

    Article  Google Scholar 

  • Zalocusky KA, Najm R, Taubes AL, Hao YX, Yoon SY, Koutsodendris N et al (2021) Neuronal ApoE upregulates MHC-I expression to drive selective neurodegeneration in Alzheimer’s disease. Nat Neurosci 24(6):786–798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Special thanks for NOVA editing service for editing the English language manuscript.

Funding

This work was supported by National Science and Technology Council, Taiwan, R.O.C. [NSTC 112-2311-B-039 -001 and NSTC 111-2622-E-039 -004], China Medical University, Taiwan, R.O.C. [CMU112-MF-25, CMU111-MF-72, and CMU111-IP-04], China Medical University Hospital, Taiwan, R.O.C [DMR-111-075, DMR-112-237, and DMR-112-056]. Furthermore, This work was financially supported by the “Cancer Biology and Precision Therapeutics Center, China Medical University" from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) in Taiwan.

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Authors and Affiliations

  1. Graduate Institute of Biomedical Sciences, College of Medicine, China Medical University, Taichung, 40402, Taiwan

    Michael Anekson Widjaya

  2. Cancer Biology and Precision Therapeutics Center, China Medical University and Academia Sinica China Medical University, Taichung, 40403, Taiwan

    Chia-Hsin Liu & Wei-Chung Cheng

  3. Department of Physical Therapy, PhD program in Healthcare Science, China Medical University, Taichung, 406040, Taiwan

    Shin-Da Lee

  4. Ph.D. Program for Cancer Biology and Drug Discovery, China Medical University and Academia Sinica, Taichung, Taiwan

    Wei-Chung Cheng

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M.A, S.D.L, and C.W.C contributed to conception and design of this study. M.A and C.H.L analyzed the data and wrote the first draft of the manuscript. M.A and C.H.L contributed to data interpretation. S.D.L and C.W.C contributed to manuscript revision, read, and approved the submitted revision.

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Correspondence to Shin-Da Lee or Wei-Chung Cheng.

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Widjaya, M.A., Liu, CH., Lee, SD. et al. Transcriptomics Meta-Analysis Reveals Phagosome and Innate Immune System Dysfunction as Potential Mechanisms in the Cortex of Alzheimer’s Disease Mouse Strains. J Mol Neurosci 73, 773–786 (2023). https://doi.org/10.1007/s12031-023-02152-9

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