{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T14:52:19Z","timestamp":1786978339490,"version":"build-2736575974"},"reference-count":45,"publisher":"Wiley","issue":"12","license":[{"start":{"date-parts":[[2018,10,16]],"date-time":"2018-10-16T00:00:00Z","timestamp":1539648000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["GM101644"],"award-info":[{"award-number":["GM101644"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["GM118161"],"award-info":[{"award-number":["GM118161"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Protein Science"],"published-print":{"date-parts":[[2018,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    The folding of predominantly \u03b2\u2010sheet proteins is complicated by the presence of a large number of non\u2010local interactions in their native states, which increase the ruggedness of their folding energy landscapes. However, forming non\u2010local contacts early in folding or even in the unfolded state can smooth the energy landscape and facilitate productive folding. We report that several sequence regions of a \u03b2\u2010barrel protein, cellular retinoic acid\u2010binding protein 1 (CRABP1), populate native\u2010like secondary structure to a significant extent in the denatured state in 8 M urea. In addition, we provide evidence for both local and non\u2010local interactions in the denatured state of CRABP1. NMR chemical shift perturbations (CSPs) under denaturing conditions upon substitution of single residues by mutation support the presence of several non\u2010local interactions in topologically key sites, arguing that the denatured state is conformationally restricted and contains topological information for the native fold. Among the most striking non\u2010local interactions are those between the N\u2010 and C\u2010terminal regions, which are involved in closure of the native \u03b2\u2010barrel. In addition, CSPs support the presence of two features in the denatured state: a major hydrophobic cluster involving residues from various parts of the sequence and a native\u2010like interaction similar to one identified in previous studies as forming early in folding (Budyak et al.,\n                    <jats:italic>Structure<\/jats:italic>\n                    21, 476 [2013]). Taken together, our data support a model in which transient structures involving nonlocal interactions prime early folding interactions in CRABP1, determine its barrel topology, and may protect this predominantly \u03b2\u2010sheet protein against aggregation.\n                  <\/jats:p>","DOI":"10.1002\/pro.3516","type":"journal-article","created":{"date-parts":[[2018,9,25]],"date-time":"2018-09-25T12:31:20Z","timestamp":1537878680000},"page":"2062-2072","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Local and non\u2010local topological information in the denatured state ensemble of a \u03b2\u2010barrel protein"],"prefix":"10.1002","volume":"27","author":[{"given":"Abhay K.","family":"Thakur","sequence":"first","affiliation":[{"name":"Departments of Biochemistry &amp; Molecular Biology and Chemistry University of Massachusetts Amherst  Amherst Massachusetts, 01003"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenli","family":"Meng","sequence":"additional","affiliation":[{"name":"Departments of Biochemistry &amp; Molecular Biology and Chemistry University of Massachusetts Amherst  Amherst Massachusetts, 01003"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5706-115X","authenticated-orcid":false,"given":"Lila M.","family":"Gierasch","sequence":"additional","affiliation":[{"name":"Departments of Biochemistry &amp; Molecular Biology and Chemistry University of Massachusetts Amherst  Amherst Massachusetts, 01003"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2018,10,16]]},"reference":[{"key":"e_1_2_6_2_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.bi.60.070191.004051"},{"key":"e_1_2_6_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2014.02.020"},{"key":"e_1_2_6_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.sbi.2007.01.002"},{"key":"e_1_2_6_5_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2017.07.022"},{"key":"e_1_2_6_6_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0607097104"},{"key":"e_1_2_6_7_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0601395103"},{"key":"e_1_2_6_8_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0403643101"},{"key":"e_1_2_6_9_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1704692114"},{"key":"e_1_2_6_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.str.2013.01.013"},{"key":"e_1_2_6_11_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1607193113"},{"key":"e_1_2_6_12_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1216979110"},{"key":"e_1_2_6_13_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1003004107"},{"key":"e_1_2_6_14_1","doi-asserted-by":"publisher","DOI":"10.1038\/nsb1197-883"},{"key":"e_1_2_6_15_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi3001825"},{"key":"e_1_2_6_16_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi00167a017"},{"key":"e_1_2_6_17_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi4013462"},{"key":"e_1_2_6_18_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1067680"},{"key":"e_1_2_6_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1359-0278(97)00030-8"},{"key":"e_1_2_6_20_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi034304k"},{"key":"e_1_2_6_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0167-4838(99)00247-2"},{"key":"e_1_2_6_22_1","doi-asserted-by":"publisher","DOI":"10.1002\/pro.5560050613"},{"key":"e_1_2_6_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.sbi.2011.09.002"},{"key":"e_1_2_6_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/0022-2836(94)90064-7"},{"key":"e_1_2_6_25_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi991765q"},{"key":"e_1_2_6_26_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1523410"},{"key":"e_1_2_6_27_1","doi-asserted-by":"publisher","DOI":"10.1002\/pro.5560041218"},{"key":"e_1_2_6_28_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1060438"},{"key":"e_1_2_6_29_1","doi-asserted-by":"publisher","DOI":"10.1021\/ja067522k"},{"key":"e_1_2_6_30_1","doi-asserted-by":"publisher","DOI":"10.1002\/pro.370"},{"key":"e_1_2_6_31_1","doi-asserted-by":"publisher","DOI":"10.1110\/ps.04805204"},{"key":"e_1_2_6_32_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi020381o"},{"key":"e_1_2_6_33_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0930122100"},{"key":"e_1_2_6_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2006.12.005"},{"key":"e_1_2_6_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1359-0278(98)00053-4"},{"key":"e_1_2_6_36_1","first-page":"188","article-title":"Early long\u2010range contacts in the folding of intracellular lipid\u2010binding proteins favor native beta\u2010barrel closure and disfavor aggregation","volume":"21","author":"Budyak I","year":"2012","journal-title":"Protein Sci"},{"key":"e_1_2_6_37_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi034304k"},{"key":"e_1_2_6_38_1","doi-asserted-by":"publisher","DOI":"10.1038\/nprot.2006.101"},{"key":"e_1_2_6_39_1","doi-asserted-by":"publisher","DOI":"10.1002\/anie.201100370"},{"key":"e_1_2_6_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pnmrs.2011.02.002"},{"key":"e_1_2_6_41_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10858-007-9197-z"},{"key":"e_1_2_6_42_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pnmrs.2010.07.004"},{"key":"e_1_2_6_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pnmrs.2013.02.001"},{"key":"e_1_2_6_44_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/bts172"},{"key":"e_1_2_6_45_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10858-010-9433-9"},{"key":"e_1_2_6_46_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0702112104"}],"container-title":["Protein Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fpro.3516","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/pro.3516","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,15]],"date-time":"2023-09-15T19:44:19Z","timestamp":1694807059000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/pro.3516"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,10,16]]},"references-count":45,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2018,12]]}},"alternative-id":["10.1002\/pro.3516"],"URL":"https:\/\/doi.org\/10.1002\/pro.3516","archive":["Portico"],"relation":{},"ISSN":["0961-8368","1469-896X"],"issn-type":[{"value":"0961-8368","type":"print"},{"value":"1469-896X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,10,16]]},"assertion":[{"value":"2018-08-03","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-09-19","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-10-16","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}