{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T09:18:39Z","timestamp":1791278319708,"version":"4.1.0"},"reference-count":65,"publisher":"The Royal Society","issue":"3","license":[{"start":{"date-parts":[[2016,3,1]],"date-time":"2016-03-01T00:00:00Z","timestamp":1456790400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"funder":[{"DOI":"10.13039\/100010648","name":"Cancer and Polio Research Fund","doi-asserted-by":"crossref","award":["CPRF"],"award-info":[{"award-number":["CPRF"]}],"id":[{"id":"10.13039\/100010648","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000265","name":"Medical Research Council","doi-asserted-by":"publisher","award":["MR\/K015931\/1"],"award-info":[{"award-number":["MR\/K015931\/1"]}],"id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000357","name":"North West Cancer Research","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000357","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000272","name":"National Institute for Health Research","doi-asserted-by":"publisher","award":["NIHR Liverpool Pancreas Biomedical Research Unit"],"award-info":[{"award-number":["NIHR Liverpool Pancreas Biomedical Research Unit"]}],"id":[{"id":"10.13039\/501100000272","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":["Open Biol."],"published-print":{"date-parts":[[2016,3]]},"abstract":"<jats:p>The interaction of a large number of extracellular proteins with heparan sulfate (HS) regulates their transport and effector functions, but the degree of molecular specificity underlying protein\u2013polysaccharide binding is still debated. The 15 paracrine fibroblast growth factors (FGFs) are one of the paradigms for this interaction. Here, we measure the binding preferences of six FGFs (FGF3, FGF4, FGF6, FGF10, FGF17, FGF20) for a library of modified heparins, representing structures in HS, and model glycosaminoglycans, using differential scanning fluorimetry. This is complemented by the identification of the lysine residues in the primary and secondary binding sites of the FGFs by a selective labelling approach. Pooling these data with previous sets provides good coverage of the FGF phylogenetic tree, deduced from amino acid sequence alignment. This demonstrates that the selectivity of the FGFs for binding structures in sulfated polysaccharides and the pattern of secondary binding sites on the surface of FGFs follow the phylogenetic relationship of the FGFs, and so are likely to be the result of the natural selection pressures that led to the expansion of the FGF family in the course of the evolution of more complex animal body plans.<\/jats:p>","DOI":"10.1098\/rsob.150275","type":"journal-article","created":{"date-parts":[[2016,3,30]],"date-time":"2016-03-30T18:27:30Z","timestamp":1459362450000},"page":"150275","update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":67,"title":["Heparin binding preference and structures in the fibroblast growth factor family parallel their evolutionary diversification"],"prefix":"10.1098","volume":"6","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5594-4434","authenticated-orcid":false,"given":"Yong","family":"Li","sequence":"first","affiliation":[{"name":"Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8602-9629","authenticated-orcid":false,"given":"Changye","family":"Sun","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9365-5433","authenticated-orcid":false,"given":"Edwin A.","family":"Yates","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chao","family":"Jiang","sequence":"additional","affiliation":[{"name":"School of Pharmaceutical Science, Wenzhou Medical University, Chashan University Park, Wenzhou 325035, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark C.","family":"Wilkinson","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4875-4293","authenticated-orcid":false,"given":"David G.","family":"Fernig","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool L69 7ZB, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2016,3]]},"reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M111.228114"},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.2741\/3007"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-biochem-060713-035314"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1111\/iep.12135"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.1038\/246355a0"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1646484"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(91)90512-W"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001361"},{"key":"e_1_3_5_10_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi00430a047"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.84.8.2292"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1039\/c2mb25019e"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1590\/S0001-37652009000300007"},{"key":"e_1_3_5_14_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.01522"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1042\/bj3470069"},{"key":"e_1_3_5_16_2","first-page":"S67","article-title":"Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated?","volume":"100","author":"Rosenberg RD","year":"1997","journal-title":"J. Clin. Invest."},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.sbi.2003.08.002"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M401774200"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2013.00385"},{"key":"e_1_3_5_20_2","first-page":"298147","article-title":"Evolution of the FGF gene family","volume":"2012","author":"Oulion S","year":"2012","journal-title":"Int. J. Evol. Biol."},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.274.8.5236"},{"key":"e_1_3_5_22_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1003068"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ydbio.2010.11.008"},{"key":"e_1_3_5_24_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0008-6215(00)81050-2"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M504338200"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.1002\/anie.200300640"},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1039\/c3md00048f"},{"key":"e_1_3_5_28_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-894X(99)00155-9"},{"key":"e_1_3_5_29_2","doi-asserted-by":"publisher","DOI":"10.1038\/18877"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1021\/bi011000u"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200604035"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M112.398826"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1111\/febs.12201"},{"key":"e_1_3_5_34_2","doi-asserted-by":"publisher","DOI":"10.1021\/ac100188x"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1074\/mcp.M900031-MCP200"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0008-6215(96)90611-4"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.1093\/glycob\/cwm062"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.1060"},{"key":"e_1_3_5_39_2","doi-asserted-by":"publisher","DOI":"10.1021\/mp060097h"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.2174\/138920109789069297"},{"key":"e_1_3_5_41_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.carres.2003.12.023"},{"key":"e_1_3_5_42_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btm404"},{"key":"e_1_3_5_43_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/sys062"},{"key":"e_1_3_5_44_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0436500100"},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.7717\/peerj.461"},{"key":"e_1_3_5_46_2","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.21.17.5946-5957.2001"},{"key":"e_1_3_5_47_2","doi-asserted-by":"publisher","DOI":"10.1101\/gad.1365406"},{"key":"e_1_3_5_48_2","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.01780-08"},{"key":"e_1_3_5_49_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.85.7.2324"},{"key":"e_1_3_5_50_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.150046"},{"key":"e_1_3_5_51_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M601252200"},{"key":"e_1_3_5_52_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.271.25.15292"},{"key":"e_1_3_5_53_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.275.4.2269"},{"key":"e_1_3_5_54_2","doi-asserted-by":"publisher","DOI":"10.1590\/S0001-37652005000400007"},{"key":"e_1_3_5_55_2","doi-asserted-by":"publisher","DOI":"10.1039\/c0ob00246a"},{"key":"e_1_3_5_56_2","doi-asserted-by":"publisher","DOI":"10.1093\/glycob\/cwn103"},{"key":"e_1_3_5_57_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.271.5252.1116"},{"key":"e_1_3_5_58_2","doi-asserted-by":"publisher","DOI":"10.1101\/gad.12.12.1894"},{"key":"e_1_3_5_59_2","doi-asserted-by":"crossref","first-page":"23 906","DOI":"10.1016\/S0021-9258(20)80471-2","article-title":"Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4","volume":"268","author":"Guimond S","year":"1993","journal-title":"J. Biol. Chem"},{"key":"e_1_3_5_60_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M100379200"},{"key":"e_1_3_5_61_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.150277"},{"key":"e_1_3_5_62_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.01051"},{"key":"e_1_3_5_63_2","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a002493"},{"key":"e_1_3_5_64_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1228456"},{"key":"e_1_3_5_65_2","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.273.13.7303"},{"key":"e_1_3_5_66_2","doi-asserted-by":"publisher","DOI":"10.1006\/bbrc.2000.2872"}],"container-title":["Open Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rsob.150275","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rsob.150275","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rsob.150275","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,21]],"date-time":"2021-02-21T04:52:12Z","timestamp":1613883132000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/doi\/10.1098\/rsob.150275"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,3]]},"references-count":65,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2016,3]]}},"alternative-id":["10.1098\/rsob.150275"],"URL":"https:\/\/doi.org\/10.1098\/rsob.150275","relation":{},"ISSN":["2046-2441"],"issn-type":[{"value":"2046-2441","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,3]]},"assertion":[{"value":"2015-12-21","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2016-03-02","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2016-03-01","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}