{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T20:47:33Z","timestamp":1783543653614,"version":"3.55.0"},"reference-count":39,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,3,25]],"date-time":"2016-03-25T00:00:00Z","timestamp":1458864000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Histochem Cell Biol"],"published-print":{"date-parts":[[2016,7]]},"DOI":"10.1007\/s00418-016-1425-8","type":"journal-article","created":{"date-parts":[[2016,3,24]],"date-time":"2016-03-24T20:59:37Z","timestamp":1458853177000},"page":"85-97","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["SULF1\/SULF2 reactivation during liver damage and tumour growth"],"prefix":"10.1007","volume":"146","author":[{"given":"Kurtis","family":"Graham","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua I.","family":"Murphy","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gurtej K.","family":"Dhoot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,3,25]]},"reference":[{"issue":"2","key":"1425_CR1","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1083\/jcb.200212083","volume":"162","author":"X Ai","year":"2003","unstructured":"Ai X, Do AT, Lozynska O, Kusche-Gullberg M, Lindahl U, Emerson CP Jr (2003) QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J Cell Biol 162(2):341\u2013351. doi: 10.1083\/jcb.200212083","journal-title":"J Cell Biol"},{"issue":"18","key":"1425_CR2","doi-asserted-by":"publisher","first-page":"3327","DOI":"10.1242\/dev.007674","volume":"134","author":"X Ai","year":"2007","unstructured":"Ai X, Kitazawa T, Do AT, Kusche-Gullberg M, Labosky PA, Emerson CP Jr (2007) SULF1 and SULF2 regulate heparan sulfate-mediated GDNF signaling for esophageal innervation. Development 134(18):3327\u20133338. doi: 10.1242\/dev.007674","journal-title":"Development"},{"issue":"13","key":"1425_CR3","doi-asserted-by":"crossref","first-page":"12346","DOI":"10.1074\/jbc.M313523200","volume":"279","author":"S Ashikari-Hada","year":"2004","unstructured":"Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K (2004) Characterization of growth factor-binding structures in heparin\/heparan sulfate using an octasaccharide library. J Biol Chem 279(13):12346\u201312354","journal-title":"J Biol Chem"},{"issue":"42","key":"1425_CR4","doi-asserted-by":"crossref","first-page":"41003","DOI":"10.1074\/jbc.M302267200","volume":"278","author":"H Barth","year":"2003","unstructured":"Barth H, Schafer C, Adah MI, Zhang F, Linhardt RJ, Toyoda H, Kinoshita-Toyoda A, Toida T, Van Kuppevelt TH, Depla E, Von Weizsacker F, Blum HE, Baumert TF (2003) Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem 278(42):41003\u201341012","journal-title":"J Biol Chem"},{"key":"1425_CR5","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1186\/1479-5876-9-72","volume":"9","author":"C Bret","year":"2011","unstructured":"Bret C, Moreaux J, Schved JF, Hose D, Klein B (2011) SULFs in human neoplasia: implication as progression and prognosis factors. J Transl Med 9:72. doi: 10.1186\/1479-5876-9-72","journal-title":"J Transl Med"},{"key":"1425_CR6","first-page":"137","volume":"2","author":"GK Dhoot","year":"2012","unstructured":"Dhoot GK (2012) Recent progress and related patents on the applications of SULF1\/SULF2 enzymes in regenerative medicine and cancer therapies. Recent Pat Regen Med 2:137\u2013145","journal-title":"Recent Pat Regen Med"},{"issue":"5535","key":"1425_CR7","doi-asserted-by":"publisher","first-page":"1663","DOI":"10.1126\/science.293.5535.1663","volume":"293","author":"GK Dhoot","year":"2001","unstructured":"Dhoot GK, Gustafsson MK, Ai X, Sun W, Standiford DM, Emerson CP Jr (2001) Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science 293(5535):1663\u20131666. doi: 10.1126\/science.293.5535.1663","journal-title":"Science"},{"issue":"11","key":"1425_CR8","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1093\/glycob\/cwf072","volume":"12","author":"M Ford-Perriss","year":"2002","unstructured":"Ford-Perriss M, Guimond SE, Greferath U, Kita M, Grobe K, Habuchi H, Kimata K, Esko JD, Murphy M, Turnbull JE (2002) Variant heparan sulfates synthesized in developing mouse brain differentially regulate FGF signaling. Glycobiology 12(11):721\u2013727","journal-title":"Glycobiology"},{"issue":"4","key":"1425_CR9","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1155\/2015\/172356","volume":"29","author":"A Giakoustidis","year":"2015","unstructured":"Giakoustidis A, Giakoustidis D, Mudan S, Sklavos A, Williams R (2015) Molecular signalling in hepatocellular carcinoma: role of and crosstalk among WNT\/\u00df-catenin, Sonic Hedgehog, Notch and Dickkopf-1. Can J Gastroenterol Hepatol 29(4):209\u2013217","journal-title":"Can J Gastroenterol Hepatol"},{"issue":"Pt 11","key":"1425_CR10","doi-asserted-by":"publisher","first-page":"1873","DOI":"10.1242\/jcs.061242","volume":"123","author":"R Gill","year":"2010","unstructured":"Gill R, Hitchins L, Fletcher F, Dhoot GK (2010) Sulf1A and HGF regulate satellite-cell growth. J Cell Sci 123(Pt 11):1873\u20131883. doi: 10.1242\/jcs.061242","journal-title":"J Cell Sci"},{"issue":"3","key":"1425_CR11","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1016\/j.bbrc.2011.09.088","volume":"414","author":"RB Gill","year":"2011","unstructured":"Gill RB, Day A, Barstow A, Liu H, Zaman G, Dhoot GK (2011) Sulf2 gene is alternatively spliced in mammalian developing and tumour tissues with functional implications. Biochem Biophys Res Commun 414(3):468\u2013473. doi: 10.1016\/j.bbrc.2011.09.088","journal-title":"Biochem Biophys Res Commun"},{"issue":"5","key":"1425_CR12","doi-asserted-by":"publisher","first-page":"1669","DOI":"10.1007\/s13277-012-0423-2","volume":"33","author":"RB Gill","year":"2012","unstructured":"Gill RB, Day A, Barstow A, Zaman G, Chenu C, Dhoot GK (2012) Mammalian Sulf1 RNA alternative splicing and its significance to tumour growth regulation. Tumour Biol J Int Soc Oncodev Biol Med 33(5):1669\u20131680. doi: 10.1007\/s13277-012-0423-2","journal-title":"Tumour Biol J Int Soc Oncodev Biol Med"},{"issue":"2","key":"1425_CR13","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.yexcr.2014.04.001","volume":"324","author":"RM Gill","year":"2014","unstructured":"Gill RM, Michael A, Westley L, Kocher HM, Murphy JI, Dhoot GK (2014) SULF1\/SULF2 splice variants differentially regulate pancreatic tumour growth progression. Exp Cell Res 324(2):157\u2013171. doi: 10.1016\/j.yexcr.2014.04.001","journal-title":"Exp Cell Res"},{"key":"1425_CR14","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.fob.2012.11.007","volume":"3","author":"L Hitchins","year":"2013","unstructured":"Hitchins L, Fletcher F, Allen S, Dhoot GK (2013) Role of Sulf1A in Wnt1- and Wnt6-induced growth regulation and myoblast hyper-elongation. FEBS Open Bio 3:30\u201334. doi: 10.1016\/j.fob.2012.11.007","journal-title":"FEBS Open Bio"},{"key":"1425_CR15","doi-asserted-by":"publisher","first-page":"150","DOI":"10.1016\/j.expneurol.2014.10.011","volume":"263","author":"MT Joy","year":"2015","unstructured":"Joy MT, Vrbova G, Dhoot GK, Anderson PN (2015) Sulf1 and Sulf2 expression in the nervous system and its role in limiting neurite outgrowth in vitro. Exp Neurol 263:150\u2013160. doi: 10.1016\/j.expneurol.2014.10.011","journal-title":"Exp Neurol"},{"issue":"2","key":"1425_CR16","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1002\/hep.23322","volume":"51","author":"DC Kroy","year":"2010","unstructured":"Kroy DC, Beraza N, Tschaharganeh DF, Sander LE, Erschfeld S, Giebeler A, Liedtke C, Wasmuth HE, Trautwein C, Streetz KL (2010) Lack of interleukin-6\/glycoprotein 130\/signal transducers and activators of transcription-3 signaling in hepatocytes predisposes to liver steatosis and injury in mice. Hepatology 51(2):463\u2013473. doi: 10.1002\/hep.23322","journal-title":"Hepatology"},{"issue":"22","key":"1425_CR17","doi-asserted-by":"publisher","first-page":"11549","DOI":"10.1128\/JVI.01946-15","volume":"89","author":"YC Kwon","year":"2015","unstructured":"Kwon YC, Bose SK, Steele R, Meyer K, Di Bisceglie AM, Ray RB, Ray R (2015) Promotion of cancer stem-like cell properties in hepatitis C virus-infected hepatocytes. J Virol 89(22):11549\u201311556. doi: 10.1128\/JVI.01946-15","journal-title":"J Virol"},{"issue":"25","key":"1425_CR18","doi-asserted-by":"publisher","first-page":"23107","DOI":"10.1074\/jbc.M302203200","volume":"278","author":"J Lai","year":"2003","unstructured":"Lai J, Chien J, Staub J, Avula R, Greene EL, Matthews TA, Smith DI, Kaufmann SH, Roberts LR, Shridhar V (2003) Loss of HSulf-1 up-regulates heparin-binding growth factor signaling in cancer. J Biol Chem 278(25):23107\u201323117. doi: 10.1074\/jbc.M302203200","journal-title":"J Biol Chem"},{"issue":"7","key":"1425_CR19","doi-asserted-by":"publisher","first-page":"2130","DOI":"10.1053\/j.gastro.2006.02.056","volume":"130","author":"JP Lai","year":"2006","unstructured":"Lai JP, Yu C, Moser CD, Aderca I, Han T, Garvey TD, Murphy LM, Garrity-Park MM, Shridhar V, Adjei AA, Roberts LR (2006) SULF1 inhibits tumor growth and potentiates the effects of histone deacetylase inhibitors in hepatocellular carcinoma. Gastroenterology 130(7):2130\u20132144. doi: 10.1053\/j.gastro.2006.02.056","journal-title":"Gastroenterology"},{"issue":"1\u20134","key":"1425_CR20","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1007\/s12029-009-9058-y","volume":"39","author":"JP Lai","year":"2008","unstructured":"Lai JP, Sandhu DS, Shire AM, Roberts LR (2008a) The tumor suppressor function of human sulfatase 1 (SULF1) in carcinogenesis. J Gastrointest Cancer 39(1\u20134):149\u2013158. doi: 10.1007\/s12029-009-9058-y","journal-title":"J Gastrointest Cancer"},{"issue":"6","key":"1425_CR21","doi-asserted-by":"publisher","first-page":"803","DOI":"10.2217\/14796694.4.6.803","volume":"4","author":"JP Lai","year":"2008","unstructured":"Lai JP, Thompson JR, Sandhu DS, Roberts LR (2008b) Heparin-degrading sulfatases in hepatocellular carcinoma: roles in pathogenesis and therapy targets. Future Oncol 4(6):803\u2013814. doi: 10.2217\/14796694.4.6.803","journal-title":"Future Oncol"},{"issue":"5","key":"1425_CR22","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1038\/onc.2009.365","volume":"29","author":"H Lemjabbar-Alaoui","year":"2010","unstructured":"Lemjabbar-Alaoui H, van Zante A, Singer MS, Xue Q, Wang YQ, Tsay D, He B, Jablons DM, Rosen SD (2010) Sulf-2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene 29(5):635\u2013646. doi: 10.1038\/onc.2009.365","journal-title":"Oncogene"},{"key":"1425_CR23","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1042\/bss0690047","volume":"69","author":"CL Merry","year":"2002","unstructured":"Merry CL, Gallagher JT (2002) New insights into heparan sulphate biosynthesis from the study of mutant mice. Biochem Soc Symp 69:47\u201357","journal-title":"Biochem Soc Symp"},{"issue":"5","key":"1425_CR24","doi-asserted-by":"publisher","first-page":"1092","DOI":"10.1158\/1535-7163.MCT-11-0705","volume":"11","author":"M Meyers-Needham","year":"2012","unstructured":"Meyers-Needham M, Lewis JA, Gencer S, Sentelle RD, Saddoughi SA, Clarke CJ, Hannun YA, Norell H, da Palma TM, Nishimura M, Kraveka JM, Khavandgar Z, Murshed M, Cevik MO, Ogretmen B (2012) Off-target function of the Sonic hedgehog inhibitor cyclopamine in mediating apoptosis via nitric oxide-dependent neutral sphingomyelinase 2\/ceramide induction. Mol Cancer Ther 11(5):1092\u20131102. doi: 10.1158\/1535-7163.MCT-11-0705","journal-title":"Mol Cancer Ther"},{"issue":"51","key":"1425_CR25","doi-asserted-by":"publisher","first-page":"49175","DOI":"10.1074\/jbc.M205131200","volume":"277","author":"M Morimoto-Tomita","year":"2002","unstructured":"Morimoto-Tomita M, Uchimura K, Werb Z, Hemmerich S, Rosen SD (2002) Cloning and characterization of two extracellular heparin-degrading endosulfatases in mice and humans. J Biol Chem 277(51):49175\u201349185. doi: 10.1074\/jbc.M205131200","journal-title":"J Biol Chem"},{"issue":"4","key":"1425_CR26","doi-asserted-by":"publisher","first-page":"e392","DOI":"10.1371\/journal.pone.0000392","volume":"2","author":"R Nawroth","year":"2007","unstructured":"Nawroth R, van Zante A, Cervantes S, McManus M, Hebrok M, Rosen SD (2007) Extracellular sulfatases, elements of the Wnt signaling pathway, positively regulate growth and tumorigenicity of human pancreatic cancer cells. PLoS One 2(4):e392. doi: 10.1371\/journal.pone.0000392","journal-title":"PLoS One"},{"issue":"9","key":"1425_CR27","doi-asserted-by":"publisher","first-page":"935","DOI":"10.1517\/14728222.2010.504718","volume":"14","author":"SD Rosen","year":"2010","unstructured":"Rosen SD, Lemjabbar-Alaoui H (2010) Sulf-2: an extracellular modulator of cell signaling and a cancer target candidate. Expert Opin Ther Targets 14(9):935\u2013949. doi: 10.1517\/14728222.2010.504718","journal-title":"Expert Opin Ther Targets"},{"issue":"16","key":"1425_CR28","doi-asserted-by":"publisher","first-page":"2752","DOI":"10.1016\/j.yexcr.2009.06.029","volume":"315","author":"AP Sahota","year":"2009","unstructured":"Sahota AP, Dhoot GK (2009) A novel SULF1 splice variant inhibits Wnt signalling but enhances angiogenesis by opposing SULF1 activity. Exp Cell Res 315(16):2752\u20132764. doi: 10.1016\/j.yexcr.2009.06.029","journal-title":"Exp Cell Res"},{"issue":"6","key":"1425_CR29","doi-asserted-by":"crossref","first-page":"1759","DOI":"10.1002\/hep.21896","volume":"46","author":"A Schulze","year":"2007","unstructured":"Schulze A, Gripon P, Urban S (2007) Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology 46(6):1759\u20131768","journal-title":"Hepatology"},{"issue":"1","key":"1425_CR30","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/S0092-8674(00)80058-6","volume":"99","author":"D Shukla","year":"1999","unstructured":"Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko J, Cohen GH, Eisenberg RJ, Rosenberg RD, Spear PG (1999) A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99(1):13\u201322","journal-title":"Cell"},{"issue":"33","key":"1425_CR31","doi-asserted-by":"publisher","first-page":"11630","DOI":"10.3748\/wjg.v20.i33.11630","volume":"20","author":"M Tarocchi","year":"2014","unstructured":"Tarocchi M, Polvani S, Marroncini G, Galli A (2014) Molecular mechanism of hepatitis B virus-induced hepatocarcinogenesis. World J Gastroenterol 20(33):11630\u201311640. doi: 10.3748\/wjg.v20.i33.11630","journal-title":"World J Gastroenterol"},{"issue":"5","key":"1425_CR32","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1369\/jhc.2010.955161","volume":"58","author":"P T\u00e1trai","year":"2010","unstructured":"T\u00e1trai P, Egedi K, Somor\u00e1cz A, van Kuppevelt TH, Ten Dam G, Lyon M, Deakin JA, Kiss A, Schaff Z et al (2010) Quantitative and qualitative alterations of heparan sulfate in fibrogenic liver diseases and hepatocellular cancer. J Histochem Cytochem 58(5):429\u2013441. doi: 10.1369\/jhc.2010.955161","journal-title":"J Histochem Cytochem"},{"issue":"1","key":"1425_CR33","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1186\/s12967-015-0683-x","volume":"13","author":"JWY Tuo","year":"2015","unstructured":"Tuo JWY, Cheng R, Li Y, Chen M, Qiu F, Qian H, Shen D, Penalva R, Xu H, Ma JX, Chan CC (2015) Wnt signaling in age-related macular degeneration: human macular tissue and mouse model. J Transl Med 13(1):330\u2013342. doi: 10.1186\/s12967-015-0683-x","journal-title":"J Transl Med"},{"key":"1425_CR34","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1186\/1471-2091-7-2","volume":"7","author":"K Uchimura","year":"2006","unstructured":"Uchimura K, Morimoto-Tomita M, Bistrup A, Li J, Lyon M, Gallagher J, Werb Z, Rosen SD (2006) HSulf-2, an extracellular endoglucosamine-6-sulfatase, selectively mobilizes heparin-bound growth factors and chemokines: effects on VEGF, FGF-1, and SDF-1. BMC Biochem 7:2. doi: 10.1186\/1471-2091-7-2","journal-title":"BMC Biochem"},{"issue":"14","key":"1425_CR35","doi-asserted-by":"publisher","first-page":"4833","DOI":"10.1073\/pnas.0401028101","volume":"101","author":"S Wang","year":"2004","unstructured":"Wang S, Ai X, Freeman SD, Pownall ME, Lu Q, Kessler DS, Emerson CP Jr (2004) QSulf1, a heparan sulfate 6-O-endosulfatase, inhibits fibroblast growth factor signaling in mesoderm induction and angiogenesis. Proc Natl Acad Sci USA 101(14):4833\u20134838. doi: 10.1073\/pnas.0401028101","journal-title":"Proc Natl Acad Sci USA"},{"issue":"2","key":"1425_CR36","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1016\/j.jhep.2012.03.029","volume":"57","author":"S Wang","year":"2012","unstructured":"Wang S, Jiang W, Chen X, Zhang C, Li H, Hou W, Liu Z, McNutt MA, Lu F, Gang L (2012) Alpha-fetoprotein acts as a novel signal molecule and mediates transcription of Fn14 in human hepatocellular carcinoma. J Hepatol 57(2):322\u2013329. doi: 10.1016\/j.jhep.2012.03.029","journal-title":"J Hepatol"},{"issue":"13","key":"1425_CR37","doi-asserted-by":"crossref","first-page":"5029","DOI":"10.18632\/oncotarget.2078","volume":"5","author":"G Xu","year":"2014","unstructured":"Xu G, Ji W, Su Y, Xu Y, Yan Y, Shen S, Li X, Sun B, Qian H, Chen L, Fu X, Wu M, Su C (2014) Sulfatase 1 (hSulf-1) reverses basic fibroblast growth factor-stimulated signaling and inhibits growth of hepatocellular carcinoma in animal model. Oncotarget 5(13):5029\u20135039","journal-title":"Oncotarget"},{"issue":"7","key":"1425_CR38","doi-asserted-by":"publisher","first-page":"3846","DOI":"10.1128\/JVI.03647-14","volume":"89","author":"Y Xu","year":"2015","unstructured":"Xu Y, Martinez P, S\u00e9ron K, Luo G, Allain F, Dubuisson J, Belouzard S (2015) Characterization of hepatitis C virus interaction with heparan sulfate proteoglycans. J Virol 89(7):3846\u20133858. doi: 10.1128\/JVI.03647-14","journal-title":"J Virol"},{"issue":"1","key":"1425_CR39","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s00418-015-1365-8","volume":"145","author":"G Zaman","year":"2016","unstructured":"Zaman G, Staines K, Farquharson C, Newton PT, Dudhia J, Chenu C, Pitsillides A, Dhoot GK (2016) Expression of Sulf1 and Sulf2 in cartilage, bone and endochondral fracture healing. Histochem Cell Biol 145(1):67\u201379","journal-title":"Histochem Cell Biol"}],"container-title":["Histochemistry and Cell Biology"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00418-016-1425-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00418-016-1425-8\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00418-016-1425-8","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,5,28]],"date-time":"2019-05-28T15:58:38Z","timestamp":1559059118000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00418-016-1425-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,3,25]]},"references-count":39,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2016,7]]}},"alternative-id":["1425"],"URL":"https:\/\/doi.org\/10.1007\/s00418-016-1425-8","relation":{},"ISSN":["0948-6143","1432-119X"],"issn-type":[{"value":"0948-6143","type":"print"},{"value":"1432-119X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,3,25]]}}}