{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T18:56:16Z","timestamp":1791572176763,"version":"4.3.4"},"reference-count":69,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2025,3,29]],"date-time":"2025-03-29T00:00:00Z","timestamp":1743206400000},"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":["NS069566"],"award-info":[{"award-number":["NS069566"]}],"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":["NS110409"],"award-info":[{"award-number":["NS110409"]}],"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":["NS076896"],"award-info":[{"award-number":["NS076896"]}],"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":["AG061251"],"award-info":[{"award-number":["AG061251"]}],"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":["HL107150"],"award-info":[{"award-number":["HL107150"]}],"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":["GM93131"],"award-info":[{"award-number":["GM93131"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000049","name":"NIA","doi-asserted-by":"publisher","award":["P30 AG062429"],"award-info":[{"award-number":["P30 AG062429"]}],"id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,5,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Cerebral amyloid angiopathy (CAA) is a common feature of Alzheimer\u2019s disease in which amyloid-\u03b2 (A\u03b2) deposits in cerebral and leptomeningeal vessel walls, predisposing vessels to micro- and macro-hemorrhages. The vessel walls contain distinct proteins and heparan sulfate (HS), yet how vascular proteins and HS jointly associate with A\u03b2 is unknown. We conducted the first multi-omics study to systematically characterize the proteins as well as the HS abundance, sulfation level, and disaccharide composition of leptomeninges from 23 moderate to severe CAA cases and controls. We then analyzed the associations between A\u03b2 and other proteins, HS, and apolipoprotein E genotype. We found an increase in a minor HS disaccharide containing unsubstituted glucosamine, as well as 6-O sulfated disaccharides; A\u03b240 levels positively correlated with unsubstituted glucosamine. There was also an increase in extracellular proteins derived from brain parenchyma or plasma, including olfactomedin-like protein 3, fibrinogen, serum amyloid protein, apolipoprotein E, and secreted frizzled related protein-3. Our findings of vascular HS and protein alterations specific to CAA-affected leptomeningeal vessels provide molecular insight into the extracellular remodeling that co-occurs with A\u03b2 deposits and may indicate a basis for antemortem diagnostic assay development and therapeutic strategies to impede A\u03b2-HS interactions.<\/jats:p>","DOI":"10.1093\/jnen\/nlaf018","type":"journal-article","created":{"date-parts":[[2025,3,3]],"date-time":"2025-03-03T04:15:18Z","timestamp":1740975318000},"page":"398-411","source":"Crossref","is-referenced-by-count":3,"title":["Multi-omic analysis of meningeal cerebral amyloid angiopathy reveals enrichment of unsubstituted glucosamine and extracellular proteins"],"prefix":"10.1093","volume":"84","author":[{"given":"Joshua E","family":"Mayfield","sequence":"first","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander J","family":"Rajic","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]},{"name":"Neurology Service, Veterans Affairs Medical Center , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patricia","family":"Aguilar-Calvo","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katrin","family":"Soldau","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samantha","family":"Flores","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Roger","family":"Lawrence","sequence":"additional","affiliation":[{"name":"Department of Cellular and Molecular Medicine, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Biwsa","family":"Choudhury","sequence":"additional","affiliation":[{"name":"Department of Cellular and Molecular Medicine, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Majid","family":"Ghassemian","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Biochemistry, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donald P","family":"Pizzo","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven L","family":"Wagner","sequence":"additional","affiliation":[{"name":"Department of Neurosciences, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Garrett A","family":"Danque","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paige","family":"Sumowski","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lawrence A","family":"Hansen","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanessa","family":"Goodwill","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffery D","family":"Esko","sequence":"additional","affiliation":[{"name":"Department of Cellular and Molecular Medicine, University of California, San Diego , La Jolla, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christina J","family":"Sigurdson","sequence":"additional","affiliation":[{"name":"Department of Pathology, University of California, San Diego , La Jolla, CA,","place":["United States"]},{"name":"Department of Medicine, University of California, San Diego , La Jolla, CA,","place":["United States"]},{"name":"Department of Pathology, Microbiology, and Immunology, University of California, Davis , Davis, CA,","place":["United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,3,29]]},"reference":[{"key":"2025042203515942000_nlaf018-B1","doi-asserted-by":"crossref","first-page":"3708","DOI":"10.1002\/alz.13809","article-title":"2024 Alzheimer's disease facts and figures","volume":"20","year":"2024","journal-title":"Alzheimers Dement"},{"key":"2025042203515942000_nlaf018-B2","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1046\/j.1440-1789.2000.00268.x","article-title":"Cerebral amyloid angiopathy: an overview","volume":"20","author":"Yamada","year":"2000","journal-title":"Neuropathology"},{"key":"2025042203515942000_nlaf018-B3","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1111\/j.1365-2990.2010.01137.x","article-title":"Review: sporadic cerebral amyloid angiopathy","volume":"37","author":"Attems","year":"2011","journal-title":"Neuropathol Appl Neurobiol"},{"key":"2025042203515942000_nlaf018-B4","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1007\/s11883-012-0254-z","article-title":"The pathophysiology and clinical presentation of cerebral amyloid angiopathy","volume":"14","author":"Auriel","year":"2012","journal-title":"Curr Atheroscler Rep"},{"key":"2025042203515942000_nlaf018-B5","doi-asserted-by":"crossref","first-page":"e1809","DOI":"10.1212\/WNL.0000000000012778","article-title":"Spontaneous ARIA-like events in cerebral amyloid angiopathy-related inflammation: a multicenter prospective longitudinal cohort study","volume":"97","author":"Antolini","year":"2021","journal-title":"Neurology"},{"key":"2025042203515942000_nlaf018-B6","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1001\/jamaneurol.2021.4161","article-title":"Amyloid-related imaging abnormalities in 2 phase 3 studies evaluating aducanumab in patients with early Alzheimer disease","volume":"79","author":"Salloway","year":"2022","journal-title":"JAMA Neurol"},{"key":"2025042203515942000_nlaf018-B7","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.jalz.2011.05.2351","article-title":"Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: recommendations from the Alzheimer's Association Research Roundtable Workgroup","volume":"7","author":"Sperling","year":"2011","journal-title":"Alzheimers Dement"},{"key":"2025042203515942000_nlaf018-B8","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1007\/BF00687367","article-title":"Sulfated glycosaminoglycans in amyloid plaques of prion diseases","volume":"77","author":"Snow","year":"1989","journal-title":"Acta Neuropathol"},{"key":"2025042203515942000_nlaf018-B9","first-page":"456","article-title":"The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease","volume":"133","author":"Snow","year":"1988","journal-title":"Am J Pathol"},{"key":"2025042203515942000_nlaf018-B10","first-page":"1253","article-title":"Early accumulation of heparan sulfate in neurons and in the beta-amyloid protein-containing lesions of Alzheimer's disease and Down's syndrome","volume":"137","author":"Snow","year":"1990","journal-title":"Am J Pathol"},{"key":"2025042203515942000_nlaf018-B11","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.jocn.2008.04.009","article-title":"Interaction between beta-amyloid protein and heparan sulfate proteoglycans from the cerebral capillary basement membrane in Alzheimer's disease","volume":"16","author":"Shimizu","year":"2009","journal-title":"J Clin Neurosci"},{"key":"2025042203515942000_nlaf018-B12","doi-asserted-by":"crossref","first-page":"C893","DOI":"10.1152\/ajpcell.00247.2022","article-title":"Heparan sulfate proteoglycan in Alzheimer's disease: aberrant expression and functions in molecular pathways related to amyloid-\u03b2 metabolism","volume":"324","author":"Ozsan McMillan","year":"2023","journal-title":"Am J Physiol Cell Physiol"},{"key":"2025042203515942000_nlaf018-B13","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1146\/annurev.biochem.71.110601.135458","article-title":"Order out of chaos: assembly of ligand binding sites in heparan sulfate","volume":"71","author":"Esko","year":"2002","journal-title":"Annu Rev Biochem"},{"key":"2025042203515942000_nlaf018-B14","doi-asserted-by":"crossref","first-page":"a004952","DOI":"10.1101\/cshperspect.a004952","article-title":"Heparan sulfate proteoglycans","volume":"3","author":"Sarrazin","year":"2011","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"2025042203515942000_nlaf018-B15","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/s00401-009-0498-z","article-title":"Microvasculature changes and cerebral amyloid angiopathy in Alzheimer's disease and their potential impact on therapy","volume":"118","author":"Weller","year":"2009","journal-title":"Acta Neuropathol"},{"key":"2025042203515942000_nlaf018-B16","doi-asserted-by":"crossref","first-page":"2187","DOI":"10.1021\/acs.jpcb.5b12235","article-title":"Interaction of the heparin-binding consensus sequence of \u03b2-amyloid peptides with heparin and heparin-derived oligosaccharides","volume":"120","author":"Nguyen","year":"2016","journal-title":"J Phys Chem B"},{"key":"2025042203515942000_nlaf018-B17","doi-asserted-by":"crossref","first-page":"13140","DOI":"10.1002\/anie.201204459","article-title":"Site-specific identification of an a\u03b2 fibril-heparin interaction site by using solid-state NMR spectroscopy","volume":"51","author":"Madine","year":"2012","journal-title":"Angew Chem Int Ed Engl"},{"key":"2025042203515942000_nlaf018-B18","doi-asserted-by":"crossref","first-page":"1681","DOI":"10.1046\/j.1471-4159.1999.721681.x","article-title":"The sulfate moieties of glycosaminoglycans are critical for the enhancement of beta-amyloid protein fibril formation","volume":"72","author":"Castillo","year":"1999","journal-title":"J Neurochem"},{"key":"2025042203515942000_nlaf018-B19","doi-asserted-by":"crossref","first-page":"24210","DOI":"10.1074\/jbc.M115.652545","article-title":"Cellular interaction and cytotoxicity of the iowa mutation of apolipoprotein A-I (ApoA-IIowa) amyloid mediated by sulfate moieties of heparan sulfate","volume":"290","author":"Kuwabara","year":"2015","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B20","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1093\/glycob\/cwp205","article-title":"Heparan sulfate mediates amyloid-beta internalization and cytotoxicity","volume":"20","author":"Sandwall","year":"2010","journal-title":"Glycobiology"},{"key":"2025042203515942000_nlaf018-B21","doi-asserted-by":"crossref","first-page":"710683","DOI":"10.3389\/fnagi.2021.710683","article-title":"The unifying hypothesis of Alzheimer's Disease: heparan sulfate proteoglycans\/glycosaminoglycans are key as first hypothesized over 30 years ago","volume":"13","author":"Snow","year":"2021","journal-title":"Front Aging Neurosci"},{"key":"2025042203515942000_nlaf018-B22","doi-asserted-by":"crossref","first-page":"332ra44","DOI":"10.1126\/scitranslmed.aad3650","article-title":"Neuronal heparan sulfates promote amyloid pathology by modulating brain amyloid-\u03b2 clearance and aggregation in Alzheimer's disease","volume":"8","author":"Liu","year":"2016","journal-title":"Sci Transl Med"},{"key":"2025042203515942000_nlaf018-B23","doi-asserted-by":"crossref","first-page":"3300","DOI":"10.1177\/0271678X17722436","article-title":"The vascular basement membrane in the healthy and pathological brain","volume":"37","author":"Thomsen","year":"2017","journal-title":"J Cereb Blood Flow Metab"},{"key":"2025042203515942000_nlaf018-B24","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1111\/nan.12295","article-title":"Early changes in extracellular matrix in Alzheimer's disease","volume":"43","author":"Lepelletier","year":"2017","journal-title":"Neuropathol Appl Neurobiol"},{"key":"2025042203515942000_nlaf018-B25","doi-asserted-by":"crossref","first-page":"eadf6232","DOI":"10.1126\/sciadv.adf6232","article-title":"Increased 3-O-sulfated heparan sulfate in Alzheimer's disease brain is associated with genetic risk gene HS3ST1","volume":"9","author":"Wang","year":"2023","journal-title":"Science Advances"},{"key":"2025042203515942000_nlaf018-B26","doi-asserted-by":"crossref","first-page":"e0209573","DOI":"10.1371\/journal.pone.0209573","article-title":"Glycosaminoglycans from Alzheimer's disease hippocampus have altered capacities to bind and regulate growth factors activities and to bind tau","volume":"14","author":"Huynh","year":"2019","journal-title":"PLoS One"},{"key":"2025042203515942000_nlaf018-B27","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1093\/jnen\/nlab028","article-title":"Alterations in the expression of the genes responsible for the synthesis of heparan sulfate in brains with Alzheimer Disease","volume":"80","author":"P\u00e9rez-L\u00f3pez","year":"2021","journal-title":"J Neuropathol Exp Neurol"},{"key":"2025042203515942000_nlaf018-B28","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1038\/s41593-021-00999-y","article-title":"Large-scale deep multi-layer analysis of Alzheimer's disease brain reveals strong proteomic disease-related changes not observed at the RNA level","volume":"25","author":"Johnson","year":"2022","journal-title":"Nat Neurosci"},{"key":"2025042203515942000_nlaf018-B29","doi-asserted-by":"crossref","first-page":"3964","DOI":"10.3390\/ijms25073964","article-title":"Vascular heparan sulfate and amyloid-\u03b2 in Alzheimer's disease patients","volume":"25","author":"McMillan","year":"2024","journal-title":"Int J Mol Sci"},{"key":"2025042203515942000_nlaf018-B30","doi-asserted-by":"crossref","first-page":"31303","DOI":"10.1074\/jbc.270.52.31303","article-title":"Presence of N-unsubstituted glucosamine units in native heparan sulfate revealed by a monoclonal antibody","volume":"270","author":"van den Born","year":"1995","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B31","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1016\/j.neuron.2010.08.018","article-title":"Modulation of gamma-secretase reduces beta-amyloid deposition in a transgenic mouse model of Alzheimer's disease","volume":"67","author":"Kounnas","year":"2010","journal-title":"Neuron"},{"key":"2025042203515942000_nlaf018-B32","doi-asserted-by":"crossref","first-page":"5016","DOI":"10.1002\/pmic.200900457","article-title":"Interactions of the NPXY microdomains of the low density lipoprotein receptor-related protein 1","volume":"9","author":"Guttman","year":"2009","journal-title":"Proteomics"},{"key":"2025042203515942000_nlaf018-B33","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1021\/ac960799q","article-title":"Direct analysis and identification of proteins in mixtures by LC\/MS\/MS and database searching at the low-femtomole level","volume":"69","author":"McCormack","year":"1997","journal-title":"Anal Chem"},{"key":"2025042203515942000_nlaf018-B34","doi-asserted-by":"crossref","first-page":"33674","DOI":"10.1074\/jbc.M804288200","article-title":"Evolutionary differences in glycosaminoglycan fine structure detected by quantitative glycan reductive isotope labeling","volume":"283","author":"Lawrence","year":"2008","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B35","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1038\/nchembio.766","article-title":"Disease-specific non-reducing end carbohydrate biomarkers for mucopolysaccharidoses","volume":"8","author":"Lawrence","year":"2012","journal-title":"Nat Chem Biol"},{"key":"2025042203515942000_nlaf018-B36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00401-011-0910-3","article-title":"National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: a practical approach","volume":"123","author":"Montine","year":"2012","journal-title":"Acta Neuropathol"},{"key":"2025042203515942000_nlaf018-B37","doi-asserted-by":"crossref","first-page":"7013","DOI":"10.1074\/jbc.270.13.7013","article-title":"Amyloid beta protein (A beta) in Alzheimer's disease brain. Biochemical and immunocytochemical analysis with antibodies specific for forms ending at A beta 40 or A beta 42(43)","volume":"270","author":"Gravina","year":"1995","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B38","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1186\/s40478-022-01356-1","article-title":"The amyloid plaque proteome in early onset Alzheimer's disease and Down syndrome","volume":"10","author":"Drummond","year":"2022","journal-title":"Acta Neuropathol Commun"},{"key":"2025042203515942000_nlaf018-B39","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1007\/s12035-018-1103-z","article-title":"Impaired Wnt signaling in the prefrontal cortex of Alzheimer's disease","volume":"56","author":"Folke","year":"2019","journal-title":"Mol Neurobiol"},{"key":"2025042203515942000_nlaf018-B40","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/s41582-024-00988-2","article-title":"Multifaceted roles of APOE in Alzheimer disease","volume":"20","author":"Jackson","year":"2024","journal-title":"Nat Rev Neurol"},{"key":"2025042203515942000_nlaf018-B41","doi-asserted-by":"crossref","first-page":"227","DOI":"10.3389\/fncel.2019.00227","article-title":"Wnt signaling deregulation in the aging and Alzheimer's brain","volume":"13","author":"Palomer","year":"2019","journal-title":"Front Cell Neurosci"},{"key":"2025042203515942000_nlaf018-B42","doi-asserted-by":"crossref","first-page":"4299","DOI":"10.1073\/pnas.92.10.4299","article-title":"Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis","volume":"92","author":"Tennent","year":"1995","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025042203515942000_nlaf018-B43","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s40478-021-01303-6","article-title":"Proteomic profiling in cerebral amyloid angiopathy reveals an overlap with CADASIL highlighting accumulation of HTRA1 and its substrates","volume":"10","author":"Zellner","year":"2022","journal-title":"Acta Neuropathol Commun"},{"key":"2025042203515942000_nlaf018-B44","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1007\/s00401-024-02767-1","article-title":"Differences in the cerebral amyloid angiopathy proteome in Alzheimer's disease and mild cognitive impairment","volume":"148","author":"Leitner","year":"2024","journal-title":"Acta Neuropathol"},{"key":"2025042203515942000_nlaf018-B45","doi-asserted-by":"crossref","first-page":"740","DOI":"10.1016\/j.neuron.2014.01.045","article-title":"ApoE and A\u03b2 in Alzheimer's disease: accidental encounters or partners?","volume":"81","author":"Kanekiyo","year":"2014","journal-title":"Neuron"},{"key":"2025042203515942000_nlaf018-B46","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1038\/nrneurol.2012.263","article-title":"Apolipoprotein E and Alzheimer disease: risk, mechanisms and therapy","volume":"9","author":"Liu","year":"2013","journal-title":"Nat Rev Neurol"},{"key":"2025042203515942000_nlaf018-B47","doi-asserted-by":"crossref","first-page":"4695","DOI":"10.1038\/s41467-024-49028-z","article-title":"Co-aggregation with apolipoprotein E modulates the function of amyloid-\u03b2 in Alzheimer's disease","volume":"15","author":"Xia","year":"2024","journal-title":"Nat Commun"},{"key":"2025042203515942000_nlaf018-B48","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.blre.2014.09.003","article-title":"Fibrinolysis and the control of blood coagulation","volume":"29","author":"Chapin","year":"2015","journal-title":"Blood Rev"},{"key":"2025042203515942000_nlaf018-B49","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1016\/S0092-8674(00)81922-4","article-title":"Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8","volume":"88","author":"Wang","year":"1997","journal-title":"Cell"},{"key":"2025042203515942000_nlaf018-B50","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.ymgme.2013.07.016","article-title":"Glycan-based biomarkers for mucopolysaccharidoses","volume":"111","author":"Lawrence","year":"2014","journal-title":"Mol Genet Metab"},{"key":"2025042203515942000_nlaf018-B51","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1042\/bj3220499","article-title":"Structural differences and the presence of unsubstituted amino groups in heparan sulphates from different tissues and species","volume":"322 ( Pt 2)","author":"Toida","year":"1997","journal-title":"Biochem J"},{"key":"2025042203515942000_nlaf018-B52","doi-asserted-by":"crossref","first-page":"14942","DOI":"10.1074\/jbc.M610691200","article-title":"Regulation of heparan sulfate 6-O-sulfation by beta-secretase activity","volume":"282","author":"Nagai","year":"2007","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B53","doi-asserted-by":"crossref","first-page":"20516","DOI":"10.1074\/jbc.M502065200","article-title":"Novel heparan sulfate structures revealed by monoclonal antibodies","volume":"280","author":"van den Born","year":"2005","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B54","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/B978-0-12-385883-2.00006-0","article-title":"Cerebral amyloid angiopathy","volume":"107","author":"Yamada","year":"2012","journal-title":"Prog Mol Biol Transl Sci"},{"key":"2025042203515942000_nlaf018-B55","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1006\/mcne.1999.0816","article-title":"Agrin binds to beta-amyloid (Abeta), accelerates abeta fibril formation, and is localized to Abeta deposits in Alzheimer's disease brain","volume":"15","author":"Cotman","year":"2000","journal-title":"Mol Cell Neurosci"},{"key":"2025042203515942000_nlaf018-B56","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1007\/s004150070144","article-title":"Crucial role of heparan sulfate proteoglycan (agrin) in beta-amyloid formation in Alzheimer's disease","volume":"247","author":"Reilly","year":"2000","journal-title":"J Neurol"},{"key":"2025042203515942000_nlaf018-B57","doi-asserted-by":"crossref","first-page":"10826","DOI":"10.1074\/jbc.RA117.000378","article-title":"Specific glycosaminoglycan chain length and sulfation patterns are required for cell uptake of tau versus \u03b1-synuclein and \u03b2-amyloid aggregates","volume":"293","author":"Stopschinski","year":"2018","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B58","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s00401-009-0577-1","article-title":"Sulfation of heparan sulfate associated with amyloid-beta plaques in patients with Alzheimer's disease","volume":"119","author":"Bruinsma","year":"2010","journal-title":"Acta Neuropathol"},{"key":"2025042203515942000_nlaf018-B59","doi-asserted-by":"crossref","first-page":"18881","DOI":"10.1016\/S0021-9258(17)32250-0","article-title":"Cell surface syndecan-1 on distinct cell types differs in fine structure and ligand binding of its heparan sulfate chains","volume":"269","author":"Kato","year":"1994","journal-title":"J Biol Chem"},{"key":"2025042203515942000_nlaf018-B60","doi-asserted-by":"crossref","first-page":"6911","DOI":"10.1523\/JNEUROSCI.0505-06.2006","article-title":"Heparan sulphation patterns generated by specific heparan sulfotransferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm","volume":"26","author":"Pratt","year":"2006","journal-title":"J Neurosci"},{"key":"2025042203515942000_nlaf018-B61","doi-asserted-by":"crossref","first-page":"8328","DOI":"10.1021\/jacs.6b02816","article-title":"Atomic details of the interactions of glycosaminoglycans with amyloid-beta fibrils","volume":"138","author":"Stewart","year":"2016","journal-title":"J Am Chem Soc"},{"key":"2025042203515942000_nlaf018-B62","doi-asserted-by":"crossref","first-page":"2056","DOI":"10.1016\/j.ajpath.2012.01.015","article-title":"Heparan sulfate subdomains that are degraded by Sulf accumulate in cerebral amyloid \u00df plaques of Alzheimer's disease: evidence from mouse models and patients","volume":"180","author":"Hosono-Fukao","year":"2012","journal-title":"Am J Pathol"},{"key":"2025042203515942000_nlaf018-B63","doi-asserted-by":"crossref","first-page":"112127","DOI":"10.1016\/j.celrep.2023.112127","article-title":"Circadian regulator CLOCK promotes tumor angiogenesis in glioblastoma","volume":"42","author":"Pang","year":"2023","journal-title":"Cell Reports"},{"key":"2025042203515942000_nlaf018-B64","doi-asserted-by":"crossref","first-page":"770","DOI":"10.1158\/2326-6066.CIR-21-0559","article-title":"Circadian regulator CLOCK drives immunosuppression in glioblastoma","volume":"10","author":"Xuan","year":"2022","journal-title":"Cancer Immunol Res"},{"key":"2025042203515942000_nlaf018-B65","doi-asserted-by":"crossref","first-page":"578411","DOI":"10.1016\/j.jneuroim.2024.578411","article-title":"Co-localization and co-expression of Olfml3 with Iba1 in brain of mice","volume":"394","author":"Yadav","year":"2024","journal-title":"J Neuroimmunol"},{"key":"2025042203515942000_nlaf018-B66","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/s13024-024-00757-1","article-title":"Heparin-enriched plasma proteome is significantly altered in Alzheimer's disease","volume":"19","author":"Guo","year":"2024","journal-title":"Mol Neurodegener"},{"key":"2025042203515942000_nlaf018-B67","doi-asserted-by":"crossref","first-page":"16679","DOI":"10.1038\/s41598-020-73845-z","article-title":"Wnt antagonist FRZB is a muscle biomarker of denervation atrophy in amyotrophic lateral sclerosis","volume":"10","author":"Kwan","year":"2020","journal-title":"Sci Rep"},{"key":"2025042203515942000_nlaf018-B68","doi-asserted-by":"crossref","first-page":"BSR20203204","DOI":"10.1042\/BSR20203204","article-title":"FRZB as a key molecule in abdominal aortic aneurysm progression affecting vascular integrity","volume":"41","author":"Oh","year":"2021","journal-title":"Biosci Rep"},{"key":"2025042203515942000_nlaf018-B69","doi-asserted-by":"crossref","first-page":"D543","DOI":"10.1093\/nar\/gkab1038","article-title":"The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences","volume":"50","author":"Perez-Riverol","year":"2022","journal-title":"Nucleic Acids Res"}],"container-title":["Journal of Neuropathology &amp; Experimental Neurology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jnen\/article-pdf\/84\/5\/398\/62810831\/nlaf018.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jnen\/article-pdf\/84\/5\/398\/62810831\/nlaf018.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,4,22]],"date-time":"2025-04-22T07:52:14Z","timestamp":1745308334000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jnen\/article\/84\/5\/398\/8100437"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,29]]},"references-count":69,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,3,29]]},"published-print":{"date-parts":[[2025,5,1]]}},"URL":"https:\/\/doi.org\/10.1093\/jnen\/nlaf018","relation":{},"ISSN":["0022-3069","1554-6578"],"issn-type":[{"value":"0022-3069","type":"print"},{"value":"1554-6578","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,5]]},"published":{"date-parts":[[2025,3,29]]}}}