{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T23:16:43Z","timestamp":1790551003782,"version":"4.1.0"},"reference-count":40,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T00:00:00Z","timestamp":1545177600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Leukemia"],"published-print":{"date-parts":[[2019,3]]},"DOI":"10.1038\/s41375-018-0306-7","type":"journal-article","created":{"date-parts":[[2018,12,19]],"date-time":"2018-12-19T08:36:18Z","timestamp":1545208578000},"page":"653-661","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":37,"title":["Wnt5a causes ROR1 to complex and activate cortactin to enhance migration of chronic lymphocytic leukemia cells"],"prefix":"10.1038","volume":"33","author":[{"given":"Md Kamrul","family":"Hasan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Rassenti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"suffix":"II","given":"George F.","family":"Widhopf","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jian","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas J.","family":"Kipps","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,12,19]]},"reference":[{"key":"306_CR1","doi-asserted-by":"crossref","first-page":"26181","DOI":"10.1016\/S0021-9258(18)35733-8","volume":"267","author":"P Masiakowski","year":"1992","unstructured":"Masiakowski P, Carroll RD. A novel family of cell surface receptors with tyrosine kinase-like domain. J Biol Chem. 1992;267:26181\u201390.","journal-title":"J Biol Chem"},{"key":"306_CR2","doi-asserted-by":"publisher","first-page":"7109","DOI":"10.1073\/pnas.90.15.7109","volume":"90","author":"C Wilson","year":"1993","unstructured":"Wilson C, Goberdhan DC, Steller H. Dror, a potential neurotrophic receptor gene, encodes a Drosophila homolog of the vertebrate Ror family of Trk-related receptor tyrosine kinases. Proc Natl Acad Sci USA. 1993;90:7109\u201313.","journal-title":"Proc Natl Acad Sci USA"},{"key":"306_CR3","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1038\/23722","volume":"400","author":"WC Forrester","year":"1999","unstructured":"Forrester WC, Dell M, Perens E, Garriga GA. C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature. 1999;400:881\u20135.","journal-title":"Nature"},{"key":"306_CR4","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1007\/s00429-004-0381-6","volume":"207","author":"M Rodriguez-Niedenfuhr","year":"2004","unstructured":"Rodriguez-Niedenfuhr M, Prols F, Christ B. Expression and regulation of ROR-1 during early avian limb development. Anat Embryol (Berl). 2004;207:495\u2013502.","journal-title":"Anat Embryol (Berl)"},{"key":"306_CR5","doi-asserted-by":"publisher","first-page":"1390","DOI":"10.1016\/j.leukres.2011.06.021","volume":"35","author":"HE Broome","year":"2011","unstructured":"Broome HE, Rassenti LZ, Wang HY, Meyer LM, Kipps TJ. ROR1 is expressed on hematogones (non-neoplastic human B-lymphocyte precursors) and a minority of precursor-B acute lymphoblastic leukemia. Leuk Res. 2011;35:1390\u20134.","journal-title":"Leuk Res"},{"key":"306_CR6","doi-asserted-by":"publisher","first-page":"3047","DOI":"10.1073\/pnas.0712148105","volume":"105","author":"T Fukuda","year":"2008","unstructured":"Fukuda T, Chen L, Endo T, Tang L, Lu D, Castro JE, et al. Antisera induced by infusions of autologous Ad-CD154-leukemia B cells identify ROR1 as an oncofetal antigen and receptor for Wnt5a. Proc Natl Acad Sci USA. 2008;105:3047\u201352.","journal-title":"Proc Natl Acad Sci USA"},{"key":"306_CR7","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1158\/1078-0432.CCR-07-1823","volume":"14","author":"S Baskar","year":"2008","unstructured":"Baskar S, Kwong KY, Hofer T, Levy JM, Kennedy MG, Lee E, et al. Unique cell surface expression of receptor tyrosine kinase ROR1 in human B-cell chronic lymphocytic leukemia. Clin Cancer Res. 2008;14:396\u2013404.","journal-title":"Clin Cancer Res"},{"key":"306_CR8","doi-asserted-by":"publisher","first-page":"1190","DOI":"10.1002\/ijc.23587","volume":"123","author":"AH Daneshmanesh","year":"2008","unstructured":"Daneshmanesh AH, Mikaelsson E, Jeddi-Tehrani M, Bayat AA, Ghods R, Ostadkarampour M, et al. Ror1, a cell surface receptor tyrosine kinase is expressed in chronic lymphocytic leukemia and may serve as a putative target for therapy. Int J Cancer. 2008;123:1190\u20135.","journal-title":"Int J Cancer"},{"key":"306_CR9","doi-asserted-by":"publisher","first-page":"793","DOI":"10.1073\/pnas.1308374111","volume":"111","author":"GF Widhopf 2nd","year":"2014","unstructured":"Widhopf GF 2nd, Cui B, Ghia EM, Chen L, Messer K, Shen Z, et al. ROR1 can interact with TCL1 and enhance leukemogenesis in Emu-TCL1 transgenic mice. Proc Natl Acad Sci USA. 2014;111:793\u20138.","journal-title":"Proc Natl Acad Sci USA"},{"issue":"25","key":"306_CR10","doi-asserted-by":"publisher","first-page":"2931","DOI":"10.1182\/blood-2016-04-712562","volume":"128","author":"Bing Cui","year":"2016","unstructured":"Cui B, Ghia EM, Chen L, Rassenti LZ, DeBoever C, Widhopf GF 2nd, et al. High-level ROR1 associates with accelerated disease-progression in chronic lymphocytic leukemia. Blood. 2016;128:2931\u201340.","journal-title":"Blood"},{"key":"306_CR11","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1126\/science.1151250","volume":"320","author":"ES Witze","year":"2008","unstructured":"Witze ES, Litman ES, Argast GM, Moon RT, Ahn NG. Wnt5a control of cell polarity and directional movement by polarized redistribution of adhesion receptors. Science. 2008;320:365\u20139.","journal-title":"Science"},{"issue":"2","key":"306_CR12","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1172\/JCI83535","volume":"126","author":"Jian Yu","year":"2015","unstructured":"Yu J, Chen L, Cui B, Widhopf GF 2nd, Shen Z, Wu R, et al. Wnt5a induces ROR1\/ROR2 hetero oligomerization to enhance leukemia chemotaxis and proliferation. J Clin Invest. 2016; 126:585\u201398.","journal-title":"Journal of Clinical Investigation"},{"issue":"Pt 7","key":"306_CR13","doi-asserted-by":"publisher","first-page":"1621","DOI":"10.1242\/jcs.093781","volume":"125","author":"SM MacGrath","year":"2012","unstructured":"MacGrath SM, Koleske AJ. Cortactin in cell migration and cancer at a glance. J Cell Sci. 2012;125(Pt 7):1621\u20136.","journal-title":"J Cell Sci"},{"issue":"Pt 1","key":"306_CR14","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1242\/jcs.01586","volume":"118","author":"JR Kowalski","year":"2005","unstructured":"Kowalski JR, Egile C, Gil S, Snapper SB, Li R, Thomas SM. Cortactin regulates cell migration through activation of N-WASP. J Cell Sci. 2005;118(Pt 1):79\u201387.","journal-title":"J Cell Sci"},{"key":"306_CR15","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1038\/onc.2008.388","volume":"28","author":"Y Zhang","year":"2009","unstructured":"Zhang Y, Zhang M, Dong H, Yong S, Li X, Olashaw N, et al. Deacetylation of cortactin by SIRT1 promotes cell migration. Oncogene. 2009;28:445\u201360.","journal-title":"Oncogene"},{"key":"306_CR16","doi-asserted-by":"publisher","first-page":"3110","DOI":"10.1073\/pnas.92.8.3110","volume":"92","author":"K Alexandropoulos","year":"1995","unstructured":"Alexandropoulos K, Cheng G, Baltimore D. Proline-rich sequences that bind to Src homology 3 domains with individual specificities. Proc Natl Acad Sci USA. 1995;92:3110\u20134.","journal-title":"Proc Natl Acad Sci USA"},{"key":"306_CR17","doi-asserted-by":"publisher","first-page":"5627","DOI":"10.1128\/MCB.15.10.5627","volume":"15","author":"Z Weng","year":"1995","unstructured":"Weng Z, Rickles RJ, Feng S, Richard S, Shaw AS, Schreiber SL, et al. Structure-function analysis of SH3 domains: SH3 binding specificity altered by single amino acid substitutions. Mol Cell Biol. 1995;15:5627\u201334.","journal-title":"Mol Cell Biol"},{"issue":"Pt 1","key":"306_CR18","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1042\/BJ20040737","volume":"382","author":"RJ Daly","year":"2004","unstructured":"Daly RJ. Cortactin signalling and dynamic actin networks. Biochem J. 2004;382(Pt 1):13\u201325.","journal-title":"Biochem J"},{"key":"306_CR19","doi-asserted-by":"publisher","first-page":"1069","DOI":"10.3324\/haematol.2013.090183","volume":"99","author":"C Gattazzo","year":"2014","unstructured":"Gattazzo C, Martini V, Frezzato F, Trimarco V, Tibaldi E, Castelli M, et al. Cortactin, another player in the Lyn signaling pathway, is over-expressed and alternatively spliced in leukemic cells from patients with B-cell chronic lymphocytic leukemia. Haematologica. 2014;99:1069\u201377.","journal-title":"Haematologica"},{"key":"306_CR20","doi-asserted-by":"publisher","first-page":"2067","DOI":"10.1038\/sj.leu.2404744","volume":"21","author":"M Muzio","year":"2007","unstructured":"Muzio M, Scielzo C, Frenquelli M, Bachi A, De Palma M, Alessio M, et al. HS1 complexes with cytoskeleton adapters in normal and malignant chronic lymphocytic leukemia B cells. Leukemia. 2007;21:2067\u201370.","journal-title":"Leukemia"},{"key":"306_CR21","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1111\/bjh.14642","volume":"178","author":"V Martini","year":"2017","unstructured":"Martini V, Gattazzo C, Frezzato F, Trimarco V, Pizzi M, Chiodin G, et al. Cortactin, a Lyn substrate, is a checkpoint molecule at the intersection of BCR and CXCR4 signalling pathway in chronic lymphocytic leukaemia cells. Br J Haematol. 2017;178:81\u201393.","journal-title":"Br J Haematol"},{"key":"306_CR22","doi-asserted-by":"publisher","first-page":"2931","DOI":"10.1182\/blood-2016-04-712562","volume":"128","author":"B Cui","year":"2016","unstructured":"Cui B, Ghia EM, Chen L, Rassenti LZ, DeBoever C, Widhopf GF 2nd, et al. High-level ROR1 associates with accelerated disease progression in chronic lymphocytic leukemia. Blood. 2016;128:2931\u201340.","journal-title":"Blood"},{"issue":"12","key":"306_CR23","doi-asserted-by":"publisher","first-page":"2615","DOI":"10.1038\/leu.2017.133","volume":"31","author":"M K Hasan","year":"2017","unstructured":"Hasan MK, Yu J, Chen L, Cui B, Widhopf II GF, Rassenti L, et al. Wnt5a induces ROR1 to complex with HS1 to enhance migration of chronic lymphocytic leukemia cells. Leukemia. 2017;31:2615\u201322.","journal-title":"Leukemia"},{"key":"306_CR24","doi-asserted-by":"publisher","first-page":"971","DOI":"10.1182\/blood-2012-08-447813","volume":"121","author":"JF Fecteau","year":"2013","unstructured":"Fecteau JF, Messmer D, Zhang S, Cui B, Chen L, Kipps TJ. Impact of oxygen concentration on growth of mesenchymal stromal cells from the marrow of patients with chronic lymphocytic leukemia. Blood. 2013;121:971\u20134.","journal-title":"Blood"},{"key":"306_CR25","doi-asserted-by":"publisher","first-page":"61","DOI":"10.2741\/s251","volume":"4","author":"JF Fecteau","year":"2012","unstructured":"Fecteau JF, Kipps TJ. Structure and function of the hematopoietic cancer niche: focus on chronic lymphocytic leukemia. Front Biosci (Sched). 2012;4:61\u201373.","journal-title":"Front Biosci (Sched)"},{"key":"306_CR26","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/S0145-2126(98)00154-4","volume":"23","author":"A Stacchini","year":"1999","unstructured":"Stacchini A, Aragno M, Vallario A, Alfarano A, Circosta P, Gottardi D, et al. MEC1 and MEC2: two new cell lines derived from B-chronic lymphocytic leukaemia in prolymphocytoid transformation. Leuk Res. 1999;23:127\u201336.","journal-title":"Leuk Res"},{"key":"306_CR27","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1038\/nchembio.481","volume":"7","author":"JA Paolo Di","year":"2011","unstructured":"Di Paolo JA, Huang T, Balazs M, Barbosa J, Barck KH, Bravo BJ, et al. Specific Btk inhibition suppresses B cell- and myeloid cell-mediated arthritis. Nat Chem Biol. 2011;7:41\u201350.","journal-title":"Nat Chem Biol"},{"issue":"6","key":"306_CR28","doi-asserted-by":"publisher","first-page":"1333","DOI":"10.1038\/leu.2016.368","volume":"31","author":"J Yu","year":"2016","unstructured":"Yu J, Chen L, Cui B, Wu C, Choi MY, Chen Y, et al. Cirmtuzumab inhibits Wnt5a-induced Rac1-activation in chronic lymphocytic leukemia treated with ibrutinib. Leukemia. 2017;31:1333\u201339.","journal-title":"Leukemia"},{"key":"306_CR29","doi-asserted-by":"publisher","first-page":"4294","DOI":"10.1091\/mbc.e04-12-1076","volume":"16","author":"K Kurokawa","year":"2005","unstructured":"Kurokawa K, Matsuda M. Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol Biol Cell. 2005;16:4294\u2013303.","journal-title":"Mol Biol Cell"},{"key":"306_CR30","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1002\/cm.20296","volume":"65","author":"AG Ammer","year":"2008","unstructured":"Ammer AG, Weed SA. Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskelet. 2008;65:687\u2013707.","journal-title":"Cell Motil Cytoskelet"},{"key":"306_CR31","doi-asserted-by":"publisher","first-page":"384","DOI":"10.1016\/S0960-9822(03)00107-6","volume":"13","author":"AW Kinley","year":"2003","unstructured":"Kinley AW, Weed SA, Weaver AM, Karginov AV, Bissonette E, Cooper JA, et al. Cortactin interacts with WIP in regulating Arp2\/3 activation and membrane protrusion. Curr Biol. 2003;13:384\u201393.","journal-title":"Curr Biol"},{"key":"306_CR32","doi-asserted-by":"publisher","first-page":"6418","DOI":"10.1038\/sj.onc.1204783","volume":"20","author":"SA Weed","year":"2001","unstructured":"Weed SA, Parsons JT. Cortactin: coupling membrane dynamics to cortical actin assembly. Oncogene. 2001;20:6418\u201334.","journal-title":"Oncogene"},{"key":"306_CR33","doi-asserted-by":"publisher","first-page":"5836","DOI":"10.1074\/jbc.M410713200","volume":"280","author":"SJ Kempiak","year":"2005","unstructured":"Kempiak SJ, Yamaguchi H, Sarmiento C, Sidani M, Ghosh M, Eddy RJ, et al. A neural Wiskott-Aldrich Syndrome protein-mediated pathway for localized activation of actin polymerization that is regulated by cortactin. J Biol Chem. 2005;280:5836\u201342.","journal-title":"J Biol Chem"},{"key":"306_CR34","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1083\/jcb.151.1.29","volume":"151","author":"SA Weed","year":"2000","unstructured":"Weed SA, Karginov AV, Schafer DA, Weaver AM, Kinley AW, Cooper JA, et al. Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2\/3 complex. J Cell Biol. 2000;151:29\u201340.","journal-title":"J Cell Biol"},{"key":"306_CR35","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1016\/S0960-9822(01)00098-7","volume":"11","author":"AM Weaver","year":"2001","unstructured":"Weaver AM, Karginov AV, Kinley AW, Weed SA, Li Y, Parsons JT, et al. Cortactin promotes and stabilizes Arp2\/3-induced actin filament network formation. Curr Biol. 2001;11:370\u20134.","journal-title":"Curr Biol"},{"key":"306_CR36","doi-asserted-by":"publisher","first-page":"1721","DOI":"10.1084\/jem.20101920","volume":"208","author":"M Schnoor","year":"2011","unstructured":"Schnoor M, Lai FP, Zarbock A, Klaver R, Polaschegg C, Schulte D, et al. Cortactin deficiency is associated with reduced neutrophil recruitment but increased vascular permeability in vivo. J Exp Med. 2011;208:1721\u201335.","journal-title":"J Exp Med"},{"key":"306_CR37","doi-asserted-by":"publisher","first-page":"1276","DOI":"10.1016\/j.cub.2005.06.043","volume":"15","author":"NS Bryce","year":"2005","unstructured":"Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, Weaver AM. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol. 2005;15:1276\u201385.","journal-title":"Curr Biol"},{"key":"306_CR38","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1083\/jcb.200402073","volume":"166","author":"L Bougneres","year":"2004","unstructured":"Bougneres L, Girardin SE, Weed SA, Karginov AV, Olivo-Marin JC, Parsons JT, et al. Cortactin and Crk cooperate to trigger actin polymerization during Shigella invasion of epithelial cells. J Cell Biol. 2004;166:225\u201335.","journal-title":"J Cell Biol"},{"issue":"Suppl","key":"306_CR39","doi-asserted-by":"publisher","first-page":"S167","DOI":"10.1016\/j.clml.2015.02.010","volume":"15","author":"MY Choi","year":"2015","unstructured":"Choi MY, Widhopf GF 2nd, Wu CC, Cui B, Lao F, Sadarangani A, et al. Pre-clinical specificity and safety of UC-961, a first-in-class monoclonal antibody targeting ROR1. Clin Lymphoma Myeloma Leuk. 2015;15 Suppl:S167\u20139. https:\/\/doi.org\/10.1016\/j.clml.2015.02.010 , PMID: 26297272, or PMCID: PMC4548279.","journal-title":"Clin Lymphoma Myeloma Leuk"},{"key":"306_CR40","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1016\/j.stem.2018.05.018","volume":"22","author":"MY Choi","year":"2018","unstructured":"Choi MY, Widhopf GF 2nd, Ghia EM, Kidwell RL, Hasan MK, Yu J, et al. Phase I trial: cirmtuzumab inhibits ROR1 signaling and stemness signatures in patients with chronic lymphocytic leukemia. Cell Stem Cell. 2018;22:951\u20139 e953.","journal-title":"Cell Stem Cell"}],"container-title":["Leukemia"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/s41375-018-0306-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41375-018-0306-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/s41375-018-0306-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,20]],"date-time":"2023-05-20T21:36:13Z","timestamp":1684618573000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41375-018-0306-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,12,19]]},"references-count":40,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2019,3]]}},"alternative-id":["306"],"URL":"https:\/\/doi.org\/10.1038\/s41375-018-0306-7","relation":{},"ISSN":["0887-6924","1476-5551"],"issn-type":[{"value":"0887-6924","type":"print"},{"value":"1476-5551","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,12,19]]},"assertion":[{"value":"14 April 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 September 2018","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 November 2018","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 December 2018","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"The authors declare that they have no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}