{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T07:03:05Z","timestamp":1792047785128,"version":"4.4.0"},"reference-count":45,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T00:00:00Z","timestamp":1690848000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T00:00:00Z","timestamp":1690848000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,6,12]],"date-time":"2023-06-12T00:00:00Z","timestamp":1686528000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["kidney-international.org","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Kidney International"],"published-print":{"date-parts":[[2023,8]]},"DOI":"10.1016\/j.kint.2023.03.039","type":"journal-article","created":{"date-parts":[[2023,5,8]],"date-time":"2023-05-08T20:49:07Z","timestamp":1683578947000},"page":"353-366","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":23,"title":["Hemolysis is associated with altered heparan sulfate of the endothelial glycocalyx and with local complement activation in thrombotic microangiopathies"],"prefix":"10.1016","volume":"104","author":[{"given":"Timoth\u00e9e","family":"Laboux","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mehdi","family":"Maanaoui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabrice","family":"Allain","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric","family":"Boulanger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Agn\u00e8s","family":"Denys","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jean-Baptiste","family":"Gibier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7ois","family":"Glowacki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ga\u00eblle","family":"Grolaux","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne","family":"Grunenwald","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mike","family":"Howsam","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steve","family":"Lancel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C\u00e9line","family":"Lebas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin","family":"Lopez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lubka","family":"Roumenina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fran\u00e7ois","family":"Prov\u00f4t","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Viviane","family":"Gnemmi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marie","family":"Frimat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.kint.2023.03.039_bib1","doi-asserted-by":"crossref","first-page":"654","DOI":"10.1056\/NEJMra1312353","article-title":"Syndromes of thrombotic microangiopathy","volume":"371","author":"George","year":"2014","journal-title":"N\u00a0Engl J Med"},{"key":"10.1016\/j.kint.2023.03.039_bib2","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1038\/s41581-021-00424-4","article-title":"Thrombotic microangiopathy in aHUS and beyond: clinical clues from complement genetics","volume":"17","author":"Fakhouri","year":"2021","journal-title":"Nat Rev Nephrol"},{"key":"10.1016\/j.kint.2023.03.039_bib3","doi-asserted-by":"crossref","first-page":"4182","DOI":"10.1182\/blood-2011-10-383281","article-title":"A\u00a0prevalent C3 mutation in aHUS patients causes a direct C3 convertase gain of function","volume":"119","author":"Roumenina","year":"2012","journal-title":"Blood"},{"key":"10.1016\/j.kint.2023.03.039_bib4","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1038\/s41581-018-0098-z","article-title":"Endothelium structure and function in kidney health and disease","volume":"15","author":"Jourde-Chiche","year":"2019","journal-title":"Nat Rev Nephrol"},{"key":"10.1016\/j.kint.2023.03.039_bib5","doi-asserted-by":"crossref","first-page":"660","DOI":"10.3390\/toxins11110660","article-title":"Hemolysis derived products toxicity and endothelium: model of the second hit","volume":"11","author":"Frimat","year":"2019","journal-title":"Toxins"},{"key":"10.1016\/j.kint.2023.03.039_bib6","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1016\/j.ejim.2012.12.016","article-title":"The endothelial glycocalyx as a potential modifier of the hemolytic uremic syndrome","volume":"24","author":"Boels","year":"2013","journal-title":"Eur J Intern Med"},{"key":"10.1016\/j.kint.2023.03.039_bib7","doi-asserted-by":"crossref","first-page":"956","DOI":"10.1152\/ajprenal.00532.2014","article-title":"A\u00a0microscopic view on the renal endothelial glycocalyx","volume":"308","author":"Dane","year":"2015","journal-title":"Am J Physiol Renal Physiol"},{"key":"10.1016\/j.kint.2023.03.039_bib8","doi-asserted-by":"crossref","DOI":"10.3389\/fcell.2021.734276","article-title":"Update on the role of the endothelial glycocalyx in angiogenesis and vascular inflammation","volume":"9","author":"Hu","year":"2021","journal-title":"Front Cell Dev Biol"},{"key":"10.1016\/j.kint.2023.03.039_bib9","doi-asserted-by":"crossref","first-page":"2697","DOI":"10.1016\/j.molimm.2006.12.001","article-title":"The C-terminus of complement factor H is essential for host cell protection","volume":"44","author":"J\u00f3zsi","year":"2007","journal-title":"Mol Immunol"},{"key":"10.1016\/j.kint.2023.03.039_bib10","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.molimm.2014.08.005","article-title":"The role of heparan sulfate as determining pathogenic factor in complement factor H-associated diseases","volume":"63","author":"Loeven","year":"2015","journal-title":"Mol Immunol"},{"key":"10.1016\/j.kint.2023.03.039_bib11","doi-asserted-by":"crossref","first-page":"235","DOI":"10.3389\/fimmu.2019.00235","article-title":"C5b9 deposition in glomerular capillaries is associated with poor kidney allograft survival in antibody-mediated rejection","volume":"10","author":"Goutaudier","year":"2019","journal-title":"Front Immunol"},{"key":"10.1016\/j.kint.2023.03.039_bib12","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1097\/01.hjh.0000431740.32696.cc","article-title":"2013 ESH\/ESC guidelines for the management of arterial hypertension: the Task Force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC)","volume":"31","author":"Mancia","year":"2013","journal-title":"J\u00a0Hypertens"},{"key":"10.1016\/j.kint.2023.03.039_bib13","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.kint.2016.10.005","article-title":"Atypical hemolytic uremic syndrome and C3 glomerulopathy: conclusions from a \u201cKidney Disease: Improving Global Outcomes\u201d (KDIGO) controversies conference","volume":"91","author":"Goodship","year":"2017","journal-title":"Kidney Int"},{"key":"10.1016\/j.kint.2023.03.039_bib14","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1016\/S0140-6736(17)30062-4","article-title":"Haemolytic uraemic syndrome","volume":"390","author":"Fakhouri","year":"2017","journal-title":"Lancet"},{"key":"10.1016\/j.kint.2023.03.039_bib15","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1038\/sj.ki.5000277","article-title":"Conditionally immortalized human glomerular endothelial cells expressing fenestrations in response to VEGF","volume":"69","author":"Satchell","year":"2006","journal-title":"Kidney Int"},{"key":"10.1016\/j.kint.2023.03.039_bib16","doi-asserted-by":"crossref","first-page":"2745","DOI":"10.1172\/JCI107470","article-title":"Culture of human endothelial cells derived from umbilical veins: identification by morphologic and immunologic criteria","volume":"52","author":"Jaffe","year":"1973","journal-title":"J\u00a0Clin Invest"},{"key":"10.1016\/j.kint.2023.03.039_bib17","doi-asserted-by":"crossref","first-page":"3008","DOI":"10.3389\/fimmu.2018.03008","article-title":"Heme drives susceptibility of glomerular endothelium to complement overactivation due to inefficient upregulation of heme oxygenase-1","volume":"9","author":"May","year":"2018","journal-title":"Front Immunol"},{"key":"10.1016\/j.kint.2023.03.039_bib18","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.biocel.2016.09.021","article-title":"Tumour-necrosis factor-\u03b1 induces heparan sulfate 6-O-endosulfatase 1 (Sulf-1) expression in fibroblasts","volume":"80","author":"Sikora","year":"2016","journal-title":"Int J Biochem Cell Biol"},{"key":"10.1016\/j.kint.2023.03.039_bib19","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1186\/s12860-022-00462-1","article-title":"The 3-O sulfation of heparan sulfate proteoglycans contributes to the cellular internalization of tau aggregates","volume":"23","author":"Ferreira","year":"2022","journal-title":"BMC Mol Biol"},{"key":"10.1016\/j.kint.2023.03.039_bib20","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1093\/glycob\/cwu137","article-title":"Macrophage polarization alters the expression and sulfation pattern of glycosaminoglycans","volume":"25","author":"Martinez","year":"2015","journal-title":"Glycobiology"},{"key":"10.1016\/j.kint.2023.03.039_bib21","doi-asserted-by":"crossref","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A\u00a0new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001","journal-title":"Nucleic Acids Res"},{"key":"10.1016\/j.kint.2023.03.039_bib22","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1182\/blood-2013-03-489245","article-title":"Complement activation by heme as a secondary hit for atypical hemolytic uremic syndrome","volume":"122","author":"Frimat","year":"2013","journal-title":"Blood"},{"key":"10.1016\/j.kint.2023.03.039_bib23","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1038\/ki.1993.67","article-title":"Distribution of GBM heparan sulfate proteoglycan core protein and side chains in human glomerular diseases","volume":"43","author":"van den Born","year":"1993","journal-title":"Kidney Int"},{"key":"10.1016\/j.kint.2023.03.039_bib24","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1007\/BF00398060","article-title":"Expression of glomerular extracellular matrix components in human diabetic nephropathy: decrease of heparan sulphate in the glomerular basement membrane","volume":"37","author":"Tamsma","year":"1994","journal-title":"Diabetologia"},{"key":"10.1016\/j.kint.2023.03.039_bib25","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1152\/ajpheart.00104.2018","article-title":"Advanced age results in a diminished endothelial glycocalyx","volume":"315","author":"Machin","year":"2018","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"10.1016\/j.kint.2023.03.039_bib26","article-title":"Syndecan-1 and free indoxyl sulfate levels are associated with miR-126 in chronic kidney disease","volume":"22","author":"Fourdinier","year":"2021","journal-title":"IJMS"},{"key":"10.1016\/j.kint.2023.03.039_bib27","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1186\/s12882-020-02219-4","article-title":"Endothelial glycocalyx damage in kidney disease correlates with uraemic toxins and endothelial dysfunction","volume":"22","author":"Liew","year":"2021","journal-title":"BMC Nephrol"},{"key":"10.1016\/j.kint.2023.03.039_bib28","doi-asserted-by":"crossref","first-page":"2997","DOI":"10.1681\/ASN.2005020137","article-title":"Protection of endothelial cells by dextran sulfate in rats with thrombotic microangiopathy","volume":"16","author":"Eto","year":"2005","journal-title":"JASN"},{"key":"10.1016\/j.kint.2023.03.039_bib29","doi-asserted-by":"crossref","first-page":"e341","DOI":"10.1097\/TXD.0000000000000881","article-title":"Complement-mediated damage to the glycocalyx plays a role in renal ischemia-reperfusion injury in mice","volume":"5","author":"Bongoni","year":"2019","journal-title":"Transplant Direct"},{"key":"10.1016\/j.kint.2023.03.039_bib30","doi-asserted-by":"crossref","first-page":"262","DOI":"10.3389\/fimmu.2015.00262","article-title":"Complement system part I - molecular mechanisms of activation and regulation","volume":"6","author":"Merle","year":"2015","journal-title":"Front Immunol"},{"key":"10.1016\/j.kint.2023.03.039_bib31","doi-asserted-by":"crossref","first-page":"6935","DOI":"10.4049\/jimmunol.169.12.6935","article-title":"Complement C3b\/C3d and cell surface polyanions are recognized by overlapping binding sites on the most carboxyl-terminal domain of complement factor H","volume":"169","author":"Hellwage","year":"2002","journal-title":"J\u00a0Immunol"},{"key":"10.1016\/j.kint.2023.03.039_bib32","doi-asserted-by":"crossref","first-page":"4974","DOI":"10.1074\/jbc.M115.702506","article-title":"Mutations in complement factor H impair alternative pathway regulation on mouse glomerular endothelial cells in\u00a0vitro","volume":"291","author":"Loeven","year":"2016","journal-title":"J\u00a0Biol Chem"},{"key":"10.1016\/j.kint.2023.03.039_bib33","doi-asserted-by":"crossref","first-page":"554","DOI":"10.2215\/CJN.04760512","article-title":"Genetics and outcome of atypical hemolytic uremic syndrome: a nationwide French series comparing children and adults","volume":"8","author":"Fremeaux-Bacchi","year":"2013","journal-title":"Clin J Am Soc Nephrol"},{"key":"10.1016\/j.kint.2023.03.039_bib34","doi-asserted-by":"crossref","first-page":"2057","DOI":"10.2174\/138161207781039742","article-title":"Heparanase: structure, biological functions, and inhibition by heparin-derived mimetics of heparan sulfate","volume":"13","author":"Vlodavsky","year":"2007","journal-title":"Curr Pharm Des"},{"key":"10.1016\/j.kint.2023.03.039_bib35","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1186\/s13041-017-0305-z","article-title":"Heme molecule functions as an endogenous agonist of astrocyte TLR2 to contribute to secondary brain damage after intracerebral hemorrhage","volume":"10","author":"Min","year":"2017","journal-title":"Mol Brain"},{"key":"10.1016\/j.kint.2023.03.039_bib36","doi-asserted-by":"crossref","first-page":"5801","DOI":"10.2147\/JIR.S331020","article-title":"Syndecan-1 shedding by matrix metalloproteinase-9 signaling regulates alveolar epithelial tight junction in lipopolysaccharide-induced early acute lung injury","volume":"14","author":"Zhang","year":"2021","journal-title":"J\u00a0Inflamm Res"},{"issue":"pt 1","key":"10.1016\/j.kint.2023.03.039_bib37","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1042\/BJ20050630","article-title":"Oxidation of heparan sulphate by hypochlorite: role of N-chloro derivatives and dichloramine-dependent fragmentation","volume":"391","author":"Rees","year":"2005","journal-title":"Biochem J"},{"key":"10.1016\/j.kint.2023.03.039_bib38","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1046\/j.1523-1755.2000.00858.x","article-title":"Glomerular heparan sulfate alterations: mechanisms and relevance for proteinuria","volume":"57","author":"Raats","year":"2000","journal-title":"Kidney Int"},{"key":"10.1016\/j.kint.2023.03.039_bib39","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.matbio.2013.12.001","article-title":"Heparan sulfate 3-O-sulfation: a rare modification in search of a function","volume":"35","author":"Thacker","year":"2014","journal-title":"Matrix Biol"},{"key":"10.1016\/j.kint.2023.03.039_bib40","doi-asserted-by":"crossref","DOI":"10.1016\/j.mbplus.2022.100121","article-title":"Alteration in heparan sulfate proteoglycan synthesis and sulfation and the impact on vascular endothelial functions","volume":"16","author":"Pretorius","year":"2022","journal-title":"Matrix Biol Plus"},{"key":"10.1016\/j.kint.2023.03.039_bib41","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/bs.ircmb.2016.02.009","article-title":"Heparan sulfate: biosynthesis, structure, and function","volume":"325","author":"Li","year":"2016","journal-title":"Int Rev Cell Mol Biol"},{"key":"10.1016\/j.kint.2023.03.039_bib42","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1002\/ajh.25742","article-title":"Complement activation in sickle-cell disease: dependence on cell density, hemolysis and modulation by hydroxyurea therapy","volume":"95","author":"Roumenina","year":"2020","journal-title":"Am J Hematol"},{"key":"10.1016\/j.kint.2023.03.039_bib43","doi-asserted-by":"crossref","first-page":"307","DOI":"10.3324\/haematol.12027","article-title":"Sickle cell patients are characterized by a reduced glycocalyx volume","volume":"93","author":"van Beers","year":"2008","journal-title":"Haematologica"},{"key":"10.1016\/j.kint.2023.03.039_bib44","doi-asserted-by":"crossref","first-page":"91350","DOI":"10.18632\/oncotarget.20518","article-title":"Sulodexide recovers endothelial function through reconstructing glycocalyx in the balloon-injury rat carotid artery model","volume":"8","author":"Li","year":"2017","journal-title":"Oncotarget"},{"key":"10.1016\/j.kint.2023.03.039_bib45","doi-asserted-by":"crossref","first-page":"2429","DOI":"10.2337\/db15-1413","article-title":"Atrasentan reduces albuminuria by restoring the glomerular endothelial glycocalyx barrier in diabetic nephropathy","volume":"65","author":"Boels","year":"2016","journal-title":"Diabetes"}],"container-title":["Kidney International"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0085253823003277?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0085253823003277?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,25]],"date-time":"2025-09-25T01:05:12Z","timestamp":1758762312000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0085253823003277"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8]]},"references-count":45,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2023,8]]}},"alternative-id":["S0085253823003277"],"URL":"https:\/\/doi.org\/10.1016\/j.kint.2023.03.039","relation":{},"ISSN":["0085-2538"],"issn-type":[{"value":"0085-2538","type":"print"}],"subject":[],"published":{"date-parts":[[2023,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Hemolysis is associated with altered heparan sulfate of the endothelial glycocalyx and with local complement activation in thrombotic microangiopathies","name":"articletitle","label":"Article Title"},{"value":"Kidney International","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.kint.2023.03.039","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 International Society of Nephrology. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}