Early epigenetic changes of Alzheimer’s disease in the human hippocampus

References

• Wimo A, Jonsson L, Bond J, et al. The worldwide economic impact of dementia 2010. Alzheimer’s Dementia 2013; 9(1): 1–11 e13.
   PubMed Web of Science ®Google Scholar
• Molinuevo JL, Gispert JD, Dubois B, et al. The AD-CSF-index discriminates Alzheimer’s disease patients from healthy controls: a validation study. J Alzheimers Dis. 2013;36(1):67–77. .
   PubMed Web of Science ®Google Scholar
• McKhann GM, Knopman DS, Chertkow H, et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s Dementia. 2011;7(3):263–269.
   PubMed Web of Science ®Google Scholar
• Arbizu J, Garcia-Ribas G, Carrio I, et al. Recommendations for the use of PET imaging biomarkers in the diagnosis of neurodegenerative conditions associated with dementia: SEMNIM and SEN consensus. Revista espanola de medicina nuclear e imagen Molecular. 2015;34(5):303–313.
   PubMed Web of Science ®Google Scholar
• Costa-Pinheiro P, Montezuma D, Henrique R, et al. Diagnostic and prognostic epigenetic biomarkers in cancer. Epigenomics. 2015;7(6):1003–1015.
   PubMed Web of Science ®Google Scholar
• Bakulski KM, Dolinoy DC, Sartor MA, et al. Genome-wide DNA methylation differences between late-onset Alzheimer’s disease and cognitively normal controls in human frontal cortex. J Alzheimers Dis. 2012;29(3):571–588.
   PubMed Web of Science ®Google Scholar
• Sanchez-Mut JV, Aso E, Heyn H, et al. Promoter hypermethylation of the phosphatase DUSP22 mediates PKA-dependent TAU phosphorylation and CREB activation in Alzheimer’s disease. Hippocampus. 2014;24(4):363–368.
   PubMed Web of Science ®Google Scholar
• Lunnon K, Smith R, Hannon E, et al. Methylomic profiling implicates cortical deregulation of ANK1 in Alzheimer’s disease. Nat Neurosci. 2014;17(9):1164–1170.
   PubMed Web of Science ®Google Scholar
• De Jager PL, Srivastava G, Lunnon K, et al. Alzheimer’s disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci. Nat Neurosci. 2014;17(9):1156–1163.
   PubMed Web of Science ®Google Scholar
• Yu L, Chibnik LB, Srivastava GP, et al. Association of Brain DNA methylation in SORL1, ABCA7, HLA-DRB5, SLC24A4, and BIN1 with pathological diagnosis of Alzheimer disease. JAMA Neurol. 2015;72(1):15–24. .
   PubMed Web of Science ®Google Scholar
• Watson CT, Roussos P, Garg P, et al. Genome-wide DNA methylation profiling in the superior temporal gyrus reveals epigenetic signatures associated with Alzheimer’s disease. Genome Med. 2016;8(1):5.
   PubMedGoogle Scholar
• Wenk GL. Neuropathologic changes in Alzheimer’s disease. J Clin Psychiatry. 2003;64(Suppl 9):7–10.
   PubMed Web of Science ®Google Scholar
• Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991;82(4):239–259.
   PubMed Web of Science ®Google Scholar
• Braak H, Alafuzoff I, Arzberger T, et al. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol. 2006;112(4):389–404.
   PubMed Web of Science ®Google Scholar
• Lace G, Savva GM, Forster G, et al. Hippocampal tau pathology is related to neuroanatomical connections: an ageing population-based study. Brain. 2009;132(Pt 5):1324–1334.
   PubMedGoogle Scholar
• Altuna M, Urdánoz-Casado A, Sánchez-ruiz de Gordoa J, et al. DNA methylation signature of human hippocampus in Alzheimer’s disease is linked to neurogenesis. Clin Epigenetics. 2019;11(1):91.
   PubMedGoogle Scholar
• Bell JE, Alafuzoff I, Al-Sarraj S, et al. Management of a twenty-first century brain bank: experience in the BrainNet Europe consortium. Acta Neuropathol. 2008;115(5):497–507.
   PubMed Web of Science ®Google Scholar
• Montine TJ, Phelps CH, Beach TG, et al. National Institute on Aging-Alzheimer’s Association guidelines for the neuropathologic assessment of Alzheimer’s disease: a practical approach. Acta Neuropathol. 2012;123(1):1–11.
   PubMed Web of Science ®Google Scholar
• Mirra SS, Heyman A, McKeel D, et al. The consortium to establish a registry for Alzheimer’s Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology. 1991;41(4):479–486.
   PubMed Web of Science ®Google Scholar
• Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215.
   PubMed Web of Science ®Google Scholar
• Celarain N, Sanchez-ruiz de Gordoa J, Zelaya MV, et al. TREM2 upregulation correlates with 5-hydroxymethycytosine enrichment in Alzheimer’s disease hippocampus. Clin Epigenetics. 2016;8:37.
   PubMed Web of Science ®Google Scholar
• de Antueno RJ, Knickle LC, Smith H, et al. Activity of human Delta5 and Delta6 desaturases on multiple n-3 and n-6 polyunsaturated fatty acids. FEBS Lett. 2001;509(1):77–80.
   PubMed Web of Science ®Google Scholar
• Leonard AE, Kelder B, Bobik EG, et al. Identification and expression of mammalian long-chain PUFA elongation enzymes. Lipids. 2002;37(8):733–740.
   PubMed Web of Science ®Google Scholar
• Aldahmesh MA, Mohamed JY, Alkuraya HS, et al. Recessive mutations in ELOVL4 cause ichthyosis, intellectual disability, and spastic quadriplegia. Am J Hum Genet. 2011;89(6):745–750.
   PubMed Web of Science ®Google Scholar
• Kou J, Kovacs GG, Höftberger R, et al. Peroxisomal alterations in Alzheimer’s disease. Acta Neuropathol. 2011;122(3):271–283.
   PubMed Web of Science ®Google Scholar
• Zarrouk A, Vejux A, Nury T, et al. Induction of mitochondrial changes associated with oxidative stress on very long chain fatty acids (C22:0, C24:0, or C26:0)-treated human neuronal cells (SK-NB-E). Oxid Med Cell Longev. 2012;2012:623257.
   PubMed Web of Science ®Google Scholar
• Pauter AM, Olsson P, Asadi A, et al. Elovl2 ablation demonstrates that systemic DHA is endogenously produced and is essential for lipid homeostasis in mice. J Lipid Res. 2014;55(4):718–728.
   PubMed Web of Science ®Google Scholar
• Thomas J, Thomas CJ, Radcliffe J, et al. Omega-3 fatty acids in early prevention of inflammatory neurodegenerative disease: a focus on Alzheimer’s disease. Biomed Res Int. 2015;2015:172801.
   PubMed Web of Science ®Google Scholar
• Cadieux-Dion M, Turcotte-Gauthier M, Noreau A, et al. Expanding the clinical phenotype associated with ELOVL4 mutation: study of a large French-Canadian family with autosomal dominant spinocerebellar ataxia and erythrokeratodermia. JAMA Neurol. 2014;71(4):470–475.
   PubMed Web of Science ®Google Scholar
• Talamonti E, Pauter AM, Asadi A, et al. Impairment of systemic DHA synthesis affects macrophage plasticity and polarization: implications for DHA supplementation during inflammation. Cell Mol Life Sci. 2017;74(15):2815–2826.
   PubMed Web of Science ®Google Scholar
• Gimple RC, Kidwell RL, Kim LJY, et al. Glioma stem cell specific super enhancer promotes polyunsaturated fatty acid synthesis to support EGFR Signaling. Cancer Discov. 2019;9(9):1248–1267.
   Web of Science ®Google Scholar
• Slieker RC, Relton CL, Gaunt TR, et al. Age-related DNA methylation changes are tissue-specific with ELOVL2 promoter methylation as exception. Epigenetics Chromatin. 2018;11(1):25.
   PubMedGoogle Scholar
• Garagnani P, Bacalini MG, Pirazzini C, et al. Methylation of ELOVL2 gene as a new epigenetic marker of age. Aging Cell. 2012;11(6):1132–1134.
   PubMed Web of Science ®Google Scholar
• Melé M, Ferreira PG, Reverter F, et al. Human genomics. The human transcriptome across tissues and individuals. Science. 2015;348(6235):660–665.
   PubMed Web of Science ®Google Scholar
• Manabe R, Kovalenko M, Webb DJ, et al. GIT1 functions in a motile, multi-molecular signaling complex that regulates protrusive activity and cell migration. J Cell Sci. 2002;115(Pt 7):1497–1510.
   PubMed Web of Science ®Google Scholar
• Pang J, Hoefen R, Pryhuber GS, et al. G-protein-coupled receptor kinase interacting protein-1 is required for pulmonary vascular development. Circulation. 2009;119(11):1524–1532.
   PubMed Web of Science ®Google Scholar
• Jones CA, Nishiya N, London NR, et al. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat Cell Biol. 2009;11(11):1325–1331.
   PubMed Web of Science ®Google Scholar
• Liu J, Zeng L, Kennedy RM, et al. βPix plays a dual role in cerebral vascular stability and angiogenesis, and interacts with integrin αvβ8. Dev Biol. 2012;363(1):95–105.
   PubMed Web of Science ®Google Scholar
• Slevin M, Elasbali AB, Miguel Turu M, et al. Identification of differential protein expression associated with development of unstable human carotid plaques. Am J Pathol. 2006;168(3):1004–1021.
   PubMed Web of Science ®Google Scholar
• Wang J, Taba Y, Pang J, et al. GIT1 mediates VEGF-induced podosome formation in endothelial cells: critical role for PLCgamma. Arterioscler Thromb Vasc Biol. 2009;29(2):202–208.
   PubMed Web of Science ®Google Scholar
• Kehoe LA, Bellone C, De Roo M, et al. GluN3A promotes dendritic spine pruning and destabilization during postnatal development. J Neurosci. 2014;34(28):9213–9221.
   PubMed Web of Science ®Google Scholar
• Hong ST, Mah W. A critical role of GIT1 in vertebrate and invertebrate brain development. Exp Neurobiol. 2015;24(1):8–16.
   PubMed Web of Science ®Google Scholar
• Smith KR, Davenport EC, Wei J, et al. GIT1 and βPIX are essential for GABA A receptor synaptic stability and inhibitory neurotransmission. Cell Rep. 2014;9(1):298–310.
   PubMed Web of Science ®Google Scholar
• Lim J, Ritt DA, Zhou M, et al. The CNK2 scaffold interacts with vilse and modulates Rac cycling during spine morphogenesis in hippocampal neurons. Curr Biol. 2014;24(7):786–792.
   PubMed Web of Science ®Google Scholar
• Menon P, Deane R, Sagare A, et al. Impaired spine formation and learning in GPCR kinase 2 interacting protein-1 (GIT1) knockout mice. Brain Res. 2010;1317:218–226.
   PubMed Web of Science ®Google Scholar
• Zhang H, Webb DJ, Asmussen H, et al. Synapse formation is regulated by the signaling adaptor GIT1. J Cell Biol. 2003;161(1):131–142.
   PubMed Web of Science ®Google Scholar
• Martyn AC, Toth K, Schmalzigaug R, et al. GIT1 regulates synaptic structural plasticity underlying learning. PLoS One. 2018;13(3):e0194350.
   PubMed Web of Science ®Google Scholar
• Franchi SA, Astro V, Macco R, et al. Identification of a protein network driving neuritogenesis of MGE-derived GABAergic interneurons. Front Cell Neurosci. 2016;10:289.
   PubMed Web of Science ®Google Scholar
• Li YS, Qin LX, Liu J, et al. GIT1 enhances neurite outgrowth by stimulating microtubule assembly. Neural Regen Res. 2016;11(3):427–434.
   PubMed Web of Science ®Google Scholar
• Kim MJ, Biag J, Fass DM, et al. Functional analysis of rare variants found in schizophrenia implicates a critical role for GIT1-PAK3 signaling in neuroplasticity. Mol Psychiatry. 2017;22(3):417–429.
   PubMed Web of Science ®Google Scholar
• Smithson LJ, Gutmann DH. Proteomic analysis reveals GIT1 as a novel mTOR complex component critical for mediating astrocyte survival. Genes Dev. 2016;30(12):1383–1388.
   PubMed Web of Science ®Google Scholar
• Th’ng JP, Sung R, Ye M, et al. H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J Biol Chem. 2005;280(30):27809–27814.
   PubMed Web of Science ®Google Scholar
• Albig W, Kardalinou E, Drabent B, et al. Isolation and characterization of two human H1 histone genes within clusters of core histone genes. Genomics. 1991;10(4):940–948.
   PubMed Web of Science ®Google Scholar
• Widlak P, Kalinowska M, Parseghian MH, et al. The histone H1 C-terminal domain binds to the apoptotic nuclease, DNA fragmentation factor (DFF40/CAD) and stimulates DNA cleavage. Biochemistry. 2005;44(21):7871–7878.
   PubMed Web of Science ®Google Scholar
• Funayama R, Saito M, Tanobe H, et al. Loss of linker histone H1 in cellular senescence. J Cell Biol. 2006;175(6):869–880.
   PubMed Web of Science ®Google Scholar
• Williams KA, Lee M, Winter JM, et al. Prostate cancer susceptibility gene. Oncotarget. 2018;9(47):28532–28546.
   PubMedGoogle Scholar
• Harshman SW, Hoover ME, Huang C, et al. Histone H1 phosphorylation in breast cancer. J Proteome Res. 2014;13(5):2453–2467.
   PubMed Web of Science ®Google Scholar
• Tiberi G, Pekowska A, Oudin C, et al. PcG methylation of the HIST1 cluster defines an epigenetic marker of acute myeloid leukemia. Leukemia. 2015;29(5):1202–1206.
   PubMed Web of Science ®Google Scholar
• Grünblatt E, Zehetmayer S, Jacob CP, et al. Pilot study: peripheral biomarkers for diagnosing sporadic Parkinson’s disease. J Neural Transm (Vienna). 2010;117(12):1387–1393.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Tang H, Wang Z, et al. MiR-185 targets the DNA methyltransferases 1 and regulates global DNA methylation in human glioma. Mol Cancer. 2011;10:124.
   PubMed Web of Science ®Google Scholar
• Daugaard I, Dominguez D, Kjeldsen TE, et al. Identification and validation of candidate epigenetic biomarkers in lung adenocarcinoma. Sci Rep. 2016;6:35807.
   PubMed Web of Science ®Google Scholar