{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,24]],"date-time":"2026-07-24T11:23:11Z","timestamp":1784892191287,"version":"3.55.0"},"reference-count":70,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2020,6,13]],"date-time":"2020-06-13T00:00:00Z","timestamp":1592006400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["AG045541"],"award-info":[{"award-number":["AG045541"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["U24 DK092993"],"award-info":[{"award-number":["U24 DK092993"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nutrients"],"abstract":"<jats:p>The Western diet (WD) and hyperlipidemia are risk factors for vascular disease, dementia, and cognitive impairment. However, the molecular mechanisms are poorly understood. This pilot study investigated the genomic pathways by which the WD and hyperlipidemia regulate gene expression in brain microvessels. Five-week-old C57BL\/6J wild type (WT) control and low-density lipoprotein receptor deficient (LDL-R\u2212\/\u2212) male mice were fed the WD for eight weeks. Differential gene expression, gene networks and pathways, transcription factors, and non-protein coding RNAs were evaluated by a genome-wide microarray and bioinformatics analysis of laser-captured hippocampal microvessels. The WD resulted in the differential expression of 1972 genes. Much of the differentially expressed gene (DEG) was attributable to the differential regulation of cell signaling proteins and their transcription factors, approximately 4% was attributable to the differential expression of miRNAs, and 10% was due to other non-protein coding RNAs, primarily long non-coding RNAs (lncRNAs) and small nucleolar RNAs (snoRNAs) not previously described to be modified by the WD. Lipotoxic injury resulted in complex and multilevel molecular regulation of the hippocampal microvasculature involving transcriptional and post-transcriptional regulation and may provide a molecular basis for a better understanding of hyperlipidemia-associated dementia risk.<\/jats:p>","DOI":"10.3390\/nu12061771","type":"journal-article","created":{"date-parts":[[2020,6,15]],"date-time":"2020-06-15T03:17:32Z","timestamp":1592191052000},"page":"1771","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Lipotoxic Injury Differentially Regulates Brain Microvascular Gene Expression in Male Mice"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3007-6335","authenticated-orcid":false,"given":"Saivageethi","family":"Nuthikattu","sequence":"first","affiliation":[{"name":"Division of Cardiovascular Medicine, Department of Internal Medicine, University of California, One Shields Ave., The Grove, Rm 1159, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6353-0912","authenticated-orcid":false,"given":"Dragan","family":"Milenkovic","sequence":"additional","affiliation":[{"name":"Division of Cardiovascular Medicine, Department of Internal Medicine, University of California, One Shields Ave., The Grove, Rm 1159, Davis, CA 95616, USA"},{"name":"INRA, UNH, Universit\u00e9 Clermont Auvergne, 63000 Clermont-Ferrand, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John C.","family":"Rutledge","sequence":"additional","affiliation":[{"name":"Division of Cardiovascular Medicine, Department of Internal Medicine, University of California, One Shields Ave., The Grove, Rm 1159, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amparo C.","family":"Villablanca","sequence":"additional","affiliation":[{"name":"Division of Cardiovascular Medicine, Department of Internal Medicine, University of California, One Shields Ave., The Grove, Rm 1159, Davis, CA 95616, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,6,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/nrneurol.2011.2","article-title":"Epidemiology of Alzheimer disease","volume":"7","author":"Reitz","year":"2011","journal-title":"Nat. Rev. Neurol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3988\/jcn.2006.2.1.1","article-title":"Small vessel disease and subcortical vascular dementia","volume":"2","author":"Kalaria","year":"2006","journal-title":"J. Clin. Neurol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2340","DOI":"10.1093\/brain\/aww183","article-title":"Distinct pathways for cognitive decline in the presence of Alzheimer\u2019s disease pathology or cerebrovascular disease","volume":"139","author":"Cohen","year":"2016","journal-title":"Brain A J. Neurol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1017\/S0029665117002014","article-title":"The relationship between obesity and cognitive health and decline","volume":"76","author":"Dye","year":"2017","journal-title":"Proc. Nutr. Soc."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Schilling, S., Tzourio, C., Soumar\u00e9, A., Kaffashian, S., Dartigues, J.F., Ancelin, M.L., Samieri, C., Dufouil, C., and Debette, S. (2017). Differential associations of plasma lipids with incident dementia and dementia subtypes in the 3C Study: A longitudinal, population-based prospective cohort study. PLoS Med., 14.","DOI":"10.1371\/journal.pmed.1002265"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.appet.2012.12.018","article-title":"The longer-term impacts of Western diet on human cognition and the brain","volume":"63","author":"Francis","year":"2013","journal-title":"Appetite"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Rutkowsky, J.M., Lee, L.L., Puchowicz, M., Golub, M.S., Befroy, D.E., Wilson, D.W., Anderson, S., Cline, G., Bini, J., and Borkowski, K. (2018). Reduced cognitive function, increased blood-brain-barrier transport and inflammatory responses, and altered brain metabolites in LDLr-\/-and C57BL\/6 mice fed a western diet. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0191909"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"643","DOI":"10.3233\/JAD-2011-110368","article-title":"The role of the blood brain barrier in neurodegenerative disorders and their treatment","volume":"24","author":"Palmer","year":"2011","journal-title":"J. Alzheimers Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.neuron.2014.12.032","article-title":"Blood-brain barrier breakdown in the aging human hippocampus","volume":"85","author":"Montagne","year":"2015","journal-title":"Neuron"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"955","DOI":"10.1194\/jlr.M061853","article-title":"Lipotoxic brain microvascular injury is mediated by activating transcription factor 3-dependent inflammatory and oxidative stress pathways","volume":"57","author":"Aung","year":"2016","journal-title":"J. Lipid Res."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1186\/s12944-016-0401-6","article-title":"Effects of the duration of hyperlipidemia on cerebral lipids, vessels and neurons in rats","volume":"16","author":"Yang","year":"2017","journal-title":"Lipids Health Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"4307","DOI":"10.1038\/s41598-017-04412-2","article-title":"Effect of high fat diet on phenotype, brain transcriptome and lipidome in Alzheimer\u2019s model mice","volume":"7","author":"Nam","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"8344","DOI":"10.1038\/s41598-018-26631-x","article-title":"MicroRNA Expression Profiling in the Prefrontal Cortex: Putative Mechanisms for the Cognitive Effects of Adolescent High Fat Feeding","volume":"8","author":"Labouesse","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"83","DOI":"10.3389\/fgene.2019.00083","article-title":"Transcriptomic Analysis of High Fat Diet Fed Mouse Brain Cortex","volume":"10","author":"Yoon","year":"2019","journal-title":"Front. Genet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s00441-017-2711-z","article-title":"Forging our understanding of lncRNAs in the brain","volume":"371","author":"Andersen","year":"2018","journal-title":"Cell Tissue Res."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Bieghs, V., Van Gorp, P.J., Wouters, K., Hendrikx, T., Gijbels, M.J., van Bilsen, M., Bakker, J., Binder, C.J., Lutjohann, D., and Staels, B. (2012). LDL receptor knock-out mice are a physiological model particularly vulnerable to study the onset of inflammation in non-alcoholic fatty liver disease. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0030668"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"19058","DOI":"10.1038\/s41598-019-55533-9","article-title":"The Western Diet Regulates Hippocampal Microvascular Gene Expression: An Integrated Genomic Analyses in Female Mice","volume":"9","author":"Nuthikattu","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_18","first-page":"1","article-title":"Deaths: Final Data for 2014","volume":"65","author":"Kochanek","year":"2016","journal-title":"Cent. Dis. Control Prev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/S1385-299X(02)00147-2","article-title":"Isolating vessels from the mouse brain for gene expression analysis using laser capture microdissection","volume":"9","author":"Ball","year":"2002","journal-title":"Brain Res. Brain Res. Protoc."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e115","DOI":"10.1093\/nar\/gks596","article-title":"Primer3--new capabilities and interfaces","volume":"40","author":"Untergasser","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/nprot.2008.211","article-title":"Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources","volume":"4","author":"Sherman","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/nar\/gkn923","article-title":"Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists","volume":"37","author":"Sherman","year":"2009","journal-title":"Nucleic Acids Res."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Supek, F., Bosnjak, M., Skunca, N., and Smuc, T. (2011). REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0021800"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1502","DOI":"10.1093\/bioinformatics\/btv770","article-title":"Multi-omics enrichment analysis using the GeneTrail2 web service","volume":"32","author":"Stockel","year":"2016","journal-title":"Bioinformatics"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1016\/j.jbi.2011.05.002","article-title":"miRWalk--database: Prediction of possible miRNA binding sites by \u201cwalking\u201d the genes of three genomes","volume":"44","author":"Dweep","year":"2011","journal-title":"J. Biomed. Inform."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1280","DOI":"10.1093\/bioinformatics\/bti141","article-title":"PermutMatrix: A graphical environment to arrange gene expression profiles in optimal linear order","volume":"21","author":"Caraux","year":"2005","journal-title":"Bioinformatics"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1038\/s41467-019-09234-6","article-title":"Metascape provides a biologist-oriented resource for the analysis of systems-level datasets","volume":"10","author":"Zhou","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A software environment for integrated models of biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"W486","DOI":"10.1093\/nar\/gky310","article-title":"MetaboAnalyst 4.0: Towards more transparent and integrative metabolomics analysis","volume":"46","author":"Chong","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"D92","DOI":"10.1093\/nar\/gkt1248","article-title":"starBase v2.0: Decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data","volume":"42","author":"Li","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2062","DOI":"10.1093\/bioinformatics\/bts344","article-title":"miRcode: A map of putative microRNA target sites in the long non-coding transcriptome","volume":"28","author":"Jeggari","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"(2019). RNAcentral: A hub of information for non-coding RNA sequences. Nucleic Acids Res., 47, D1250\u2013D1251.","DOI":"10.1093\/nar\/gky1206"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"956854","DOI":"10.1155\/2015\/956854","article-title":"Cholesterol-induced hepatic inflammation does not underlie the predisposition to insulin resistance in dyslipidemic female LDL receptor knockout mice","volume":"2015","author":"Gruben","year":"2015","journal-title":"J. Diabetes Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"5226","DOI":"10.1210\/en.2010-0496","article-title":"Ldlr-\/-mice display decreased susceptibility to Western-type diet-induced obesity due to increased thermogenesis","volume":"151","author":"Ngai","year":"2010","journal-title":"Endocrinology"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Mehus, A.A., Dickey, A.M., Smith, T.P.L., Yeater, K.M., and Picklo, M.J. (2019). Next-Generation Sequencing Identifies Polyunsaturated Fatty Acid Responsive Genes in the Juvenile Rat Cerebellum. Nutrients, 11.","DOI":"10.3390\/nu11020407"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1086\/677356","article-title":"Mechanisms Regulating Endothelial Permeability","volume":"4","author":"Sukriti","year":"2014","journal-title":"Pulm. Circ."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1038\/jcbfm.2011.197","article-title":"Neurological Diseases in Relation to the Blood\u2013Brain Barrier","volume":"32","author":"Rosenberg","year":"2012","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.ajps.2018.06.004","article-title":"Small GTPases: Structure, biological function and its interaction with nanoparticles","volume":"14","author":"Song","year":"2019","journal-title":"Asian J. Pharm. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2869","DOI":"10.1016\/j.celrep.2018.08.025","article-title":"Activation of Ras in the Vascular Endothelium Induces Brain Vascular Malformations and Hemorrhagic Stroke","volume":"24","author":"Li","year":"2018","journal-title":"Cell Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"8954201","DOI":"10.1155\/2019\/8954201","article-title":"Monoamine Oxidase-Related Vascular Oxidative Stress in Diseases Associated with Inflammatory Burden","volume":"2019","author":"Sturza","year":"2019","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Kataoka, H., Ariyama, Y., Deushi, M., Osaka, M., Nitta, K., and Yoshida, M. (2016). Inhibitory Effect of Serotonin Antagonist on Leukocyte-Endothelial Interactions In Vivo and In Vitro. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0147929"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1016\/j.brainresbull.2019.02.014","article-title":"Ceasing exercise induces depression-like, anxiety-like, and impaired cognitive-like behaviours and altered hippocampal gene expression","volume":"148","author":"Morgan","year":"2019","journal-title":"Brain Res. Bull."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s11010-010-0609-0","article-title":"Effect of dietary saturated fatty acids on HNF-4alpha DNA binding activity and ApoCIII mRNA in sedentary rat liver","volume":"347","author":"Ceccarelli","year":"2011","journal-title":"Mol. Cell. Biochem."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Yamanishi, K., Doe, N., Sumida, M., Watanabe, Y., Yoshida, M., Yamamoto, H., Xu, Y., Li, W., Yamanishi, H., and Okamura, H. (2015). Hepatocyte nuclear factor 4 alpha is a key factor related to depression and physiological homeostasis in the mouse brain. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0119021"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"10521","DOI":"10.1038\/ncomms10521","article-title":"Endothelial Dicer promotes atherosclerosis and vascular inflammation by miRNA-103-mediated suppression of KLF4","volume":"7","author":"Hartmann","year":"2016","journal-title":"Nat. Commun."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3389\/fncel.2018.00325","article-title":"The Role of KLF4 in Alzheimer\u2019s Disease","volume":"12","author":"Cheng","year":"2018","journal-title":"Front. Cell. Neurosci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s10020-018-0020-y","article-title":"Effects of CREB1 gene silencing on cognitive dysfunction by mediating PKA-CREB signaling pathway in mice with vascular dementia","volume":"24","author":"Han","year":"2018","journal-title":"Mol. Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"34161","DOI":"10.1038\/srep34161","article-title":"Impact of high fat diet on long non-coding RNAs and messenger RNAs expression in the aortas of ApoE (-\/-) mice","volume":"6","author":"Bao","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"388","DOI":"10.3389\/fnmol.2018.00388","article-title":"MicroRNA-210-5p Contributes to Cognitive Impairment in Early Vascular Dementia Rat Model Through Targeting Snap25","volume":"11","author":"Ren","year":"2018","journal-title":"Front. Mol. Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"15878","DOI":"10.1074\/jbc.M800731200","article-title":"MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3","volume":"283","author":"Fasanaro","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1016\/j.nlm.2011.08.005","article-title":"Brain insulin signaling: A key component of cognitive processes and a potential basis for cognitive impairment in type 2 diabetes","volume":"96","author":"McNay","year":"2011","journal-title":"Neurobiol. Learn. Mem."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/j.cmet.2010.03.013","article-title":"Loss of insulin signaling in vascular endothelial cells accelerates atherosclerosis in apolipoprotein E null mice","volume":"11","author":"Li","year":"2010","journal-title":"Cell Metab."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e15","DOI":"10.1161\/CIRCRESAHA.108.177386","article-title":"Neurotrophin p75 receptor (p75NTR) promotes endothelial cell apoptosis and inhibits angiogenesis: Implications for diabetes-induced impaired neovascularization in ischemic limb muscles","volume":"103","author":"Caporali","year":"2008","journal-title":"Circ. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0166-4328(05)80134-2","article-title":"Hippocampal nerve growth factor levels are related to spatial learning ability in aged rats","volume":"48","author":"Henriksson","year":"1992","journal-title":"Behav. Brain Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"711","DOI":"10.3389\/fimmu.2019.00711","article-title":"PECAM-1 Stabilizes Blood-Brain Barrier Integrity and Favors Paracellular T-Cell Diapedesis Across the Blood-Brain Barrier During Neuroinflammation","volume":"10","author":"Wimmer","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"206849","DOI":"10.1155\/2015\/206849","article-title":"Regulatory role of small nucleolar RNAs in human diseases","volume":"2015","author":"Stepanov","year":"2015","journal-title":"BioMed Res. Int."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"3089","DOI":"10.1111\/j.1460-9568.2003.03026.x","article-title":"Contextual fear conditioning regulates the expression of brain-specific small nucleolar RNAs in hippocampus","volume":"18","author":"Rogelj","year":"2003","journal-title":"Eur. J. Neurosci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2062384","DOI":"10.1155\/2017\/2062384","article-title":"Long Noncoding RNAs and RNA-Binding Proteins in Oxidative Stress, Cellular Senescence, and Age-Related Diseases","volume":"2017","author":"Kim","year":"2017","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"2414","DOI":"10.1111\/febs.13679","article-title":"Emerging roles of lncRNAs in senescence","volume":"283","author":"Montes","year":"2016","journal-title":"FEBS J."},{"key":"ref_60","first-page":"161","article-title":"Long Non-Coding RNA LncKdm2b Regulates Cortical Neuronal Differentiation by Cis-Activating Kdm2b","volume":"11","author":"Li","year":"2018","journal-title":"bioRxiv"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1007\/s00439-016-1668-4","article-title":"An atypical 12q24.31 microdeletion implicates six genes including a histone demethylase KDM2B and a histone methyltransferase SETD1B in syndromic intellectual disability","volume":"135","author":"Labonne","year":"2016","journal-title":"Hum. Genet."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"218","DOI":"10.2174\/1567205012666150302160145","article-title":"Identification of novel quantitative traits-associated susceptibility loci for APOE epsilon 4 non-carriers of Alzheimer\u2019s disease","volume":"12","author":"Jiang","year":"2015","journal-title":"Curr. Alzheimer Res."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1038\/s41434-018-0026-7","article-title":"LncRNA FTX sponges miR-215 and inhibits phosphorylation of vimentin for promoting colorectal cancer progression","volume":"25","author":"Yang","year":"2018","journal-title":"Gene Ther."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1111\/micc.12111","article-title":"Vimentin as an integral regulator of cell adhesion and endothelial sprouting","volume":"21","author":"Dave","year":"2014","journal-title":"Microcirculation"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1038\/nature05016","article-title":"Mutations in progranulin cause tau-negative frontotemporal dementia linked to chromosome 17","volume":"442","author":"Baker","year":"2006","journal-title":"Nature"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1194","DOI":"10.1177\/1352458511406164","article-title":"Progranulin expression in brain tissue and cerebrospinal fluid levels in multiple sclerosis","volume":"17","author":"Vercellino","year":"2011","journal-title":"Mult. Scler."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.ajpath.2010.11.002","article-title":"Progranulin is a chemoattractant for microglia and stimulates their endocytic activity","volume":"178","author":"Pickford","year":"2011","journal-title":"Am. J. Pathol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"183","DOI":"10.3389\/fgene.2017.00183","article-title":"Wnt\/beta-catenin Signaling Pathway Regulates Specific lncRNAs That Impact Dermal Fibroblasts and Skin Fibrosis","volume":"8","author":"Mullin","year":"2017","journal-title":"Front. Genet."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"96340","DOI":"10.18632\/oncotarget.22047","article-title":"The molecular classification of astrocytic tumors","volume":"8","author":"Mao","year":"2017","journal-title":"Oncotarget"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e3881","DOI":"10.7717\/peerj.3881","article-title":"Integration of lncRNA-miRNA-mRNA reveals novel insights into oviposition regulation in honey bees","volume":"5","author":"Chen","year":"2017","journal-title":"PeerJ"}],"container-title":["Nutrients"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6643\/12\/6\/1771\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:38:34Z","timestamp":1760175514000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6643\/12\/6\/1771"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,13]]},"references-count":70,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,6]]}},"alternative-id":["nu12061771"],"URL":"https:\/\/doi.org\/10.3390\/nu12061771","relation":{},"ISSN":["2072-6643"],"issn-type":[{"value":"2072-6643","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,6,13]]}}}