{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T13:50:23Z","timestamp":1790689823580,"version":"4.1.0"},"reference-count":80,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T00:00:00Z","timestamp":1672704000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"},{"start":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T00:00:00Z","timestamp":1672704000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["TRR 130 project P02"],"award-info":[{"award-number":["TRR 130 project P02"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["SFB 944\/Z"],"award-info":[{"award-number":["SFB 944\/Z"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["INST 190\/182\u20101"],"award-info":[{"award-number":["INST 190\/182\u20101"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["PI 405\/14\u20101"],"award-info":[{"award-number":["PI 405\/14\u20101"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["CIBSS\u2010EXC\u20102189"],"award-info":[{"award-number":["CIBSS\u2010EXC\u20102189"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"name":"HHS \u00a6 National Institutes of Health","award":["AI145656"],"award-info":[{"award-number":["AI145656"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["EMBO J"],"published-print":{"date-parts":[[2023,2,15]]},"DOI":"10.15252\/embj.2022112030","type":"journal-article","created":{"date-parts":[[2023,1,3]],"date-time":"2023-01-03T03:57:50Z","timestamp":1672718270000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":39,"title":["Plasma membrane topography governs the 3D dynamic localization of IgM B cell antigen receptor clusters"],"prefix":"10.1038","volume":"42","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0959-0812","authenticated-orcid":false,"given":"Deniz","family":"Saltukoglu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9823-0581","authenticated-orcid":false,"given":"Bugra","family":"\u00d6zdemir","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2396-2627","authenticated-orcid":false,"given":"Michael","family":"Holtmannsp\u00f6tter","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5496-6711","authenticated-orcid":false,"given":"Ralf","family":"Reski","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2143-2270","authenticated-orcid":false,"given":"Jacob","family":"Piehler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6872-6567","authenticated-orcid":false,"given":"Rainer","family":"Kurre","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1025-7198","authenticated-orcid":false,"given":"Michael","family":"Reth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,1,3]]},"reference":[{"key":"BFEMBJ2022112030_CR1","doi-asserted-by":"crossref","first-page":"7","DOI":"10.4161\/sgtp.28580","volume":"5","author":"P Aspenstr\u00f6m","year":"2014","unstructured":"Aspenstr\u00f6m P (2014) BAR domain proteins regulate rho GTPase signaling. Small GTPases 5: 7","journal-title":"Small GTPases"},{"key":"BFEMBJ2022112030_CR2","doi-asserted-by":"crossref","first-page":"2406","DOI":"10.1091\/mbc.e13-05-0271","volume":"24","author":"AN Becalska","year":"2013","unstructured":"Becalska AN, Kelley CF, Berciu C, Stanishneva\u2010Konovalova TB, Fu X, Wang S, Sokolova OS, Nicastro D, Rodal AA (2013) Formation of membrane ridges and scallops by the F\u2010BAR protein nervous wreck. Mol Biol Cell 24: 2406\u20132418","journal-title":"Mol Biol Cell"},{"key":"BFEMBJ2022112030_CR3","doi-asserted-by":"crossref","first-page":"5231","DOI":"10.1073\/pnas.1621512114","volume":"114","author":"M Becker","year":"2017","unstructured":"Becker M, Hobeika E, Jumaa H, Reth M, Maity PC (2017) CXCR4 signaling and function require the expression of the IgD\u2010class B\u2010cell antigen receptor. Proc Natl Acad Sci U S A 114: 5231\u20135236","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBJ2022112030_CR4","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1038\/ncb3251","volume":"17","author":"WM Bement","year":"2015","unstructured":"Bement WM, Leda M, Moe AM, Kita AM, Larson ME, Golding AE, Pfeuti C, Su K\u2010C, Miller AL, Goryachev AB et\u00a0al (2015) Activator\u2010inhibitor coupling between rho signalling and Actin assembly makes the cell cortex an excitable medium. Nat Cell Biol 17: 1471\u20131483","journal-title":"Nat Cell Biol"},{"key":"BFEMBJ2022112030_CR5","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1172\/JCI120572","volume":"129","author":"A Bouafia","year":"2019","unstructured":"Bouafia A, Lofek S, Bruneau J, Chentout L, Lamrini H, Trinquand A, Deau M\u2010C, Heurtier L, Meignin V, Picard C et\u00a0al (2019) Loss of ARHGEF1 causes a human primary antibody deficiency. J Clin Invest 129: 1047\u20131060","journal-title":"J Clin Invest"},{"key":"BFEMBJ2022112030_CR6","volume":"356","author":"E Cai","year":"2017","unstructured":"Cai E, Marchuk K, Beemiller P, Beppler C, Rubashkin MG, Weaver VM, G\u00e9rard A, Liu T\u2010L, Chen B\u2010C, Betzig E et\u00a0al (2017) Visualizing dynamic microvillar search and stabilization during ligand detection by T cells. Science 356: eaal318","journal-title":"Science"},{"key":"BFEMBJ2022112030_CR7","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1016\/j.immuni.2007.06.007","volume":"27","author":"YR Carrasco","year":"2007","unstructured":"Carrasco YR, Batista FD (2007) B cells acquire particulate antigen in a macrophage\u2010rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 27: 160\u2013171","journal-title":"Immunity"},{"key":"BFEMBJ2022112030_CR8","volume":"346","author":"B\u2010C Chen","year":"2014","unstructured":"Chen B\u2010C, Legant WR, Wang K, Shao L, Milkie DE, Davidson MW, Janetopoulos C, Wu XS, Hammer JA 3rd, Liu Z et\u00a0al (2014) Lattice light\u2010sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346: 1257998","journal-title":"Science"},{"key":"BFEMBJ2022112030_CR9","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1038\/ni1542","volume":"9","author":"G Cinamon","year":"2008","unstructured":"Cinamon G, Zachariah MA, Lam OM, Foss FW Jr, Cyster JG (2008) Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat Immunol 9: 54\u201362","journal-title":"Nat Immunol"},{"key":"BFEMBJ2022112030_CR10","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1038\/ni.1946","volume":"11","author":"JG Cyster","year":"2010","unstructured":"Cyster JG (2010) B cell follicles and antigen encounters of the third kind. Nat Immunol 11: 989\u2013996","journal-title":"Nat Immunol"},{"key":"BFEMBJ2022112030_CR11","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1038\/s41592-019-0539-z","volume":"16","author":"MK Driscoll","year":"2019","unstructured":"Driscoll MK, Welf ES, Jamieson AR, Dean KM, Isogai T, Fiolka R, Danuser G (2019) Robust and automated detection of subcellular morphological motifs in 3D microscopy images. Nat Methods 16: 1037\u20131044","journal-title":"Nat Methods"},{"key":"BFEMBJ2022112030_CR12","doi-asserted-by":"crossref","first-page":"14002","DOI":"10.1073\/pnas.1817255116","volume":"116","author":"RA Fernandes","year":"2019","unstructured":"Fernandes RA, Ganzinger KA, Tzou JC, J\u00f6nsson P, Lee SF, Palayret M, Santos AM, Carr AR, Ponjavic A, Chang VT et\u00a0al (2019) A cell topography\u2010based mechanism for ligand discrimination by the T cell receptor. Proc Natl Acad Sci U S A 116: 14002\u201314010","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBJ2022112030_CR13","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1002\/jemt.1070280404","volume":"28","author":"E Fern\u00e1ndez\u2010Segura","year":"1994","unstructured":"Fern\u00e1ndez\u2010Segura E, Garc\u00eda JM, L\u00f3pez\u2010Esc\u00e1mez JA, Campos A (1994) Surface expression and distribution of fc receptor III (CD16 molecule) on human natural killer cells and polymorphonuclear neutrophils. Microsc Res Tech 28: 277\u2013285","journal-title":"Microsc Res Tech"},{"key":"BFEMBJ2022112030_CR14","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1038\/s42003-022-03152-y","volume":"5","author":"C Franke","year":"2022","unstructured":"Franke C, Chum T, Kv\u00ed\u010dalov\u00e1 Z, Glatzov\u00e1 D, Gentsch GJ, Rodriguez A, Helmerich DA, Herdly L, Mavila H, Frank O et\u00a0al (2022) Approach to map nanotopography of cell surface receptors. Commun Biol 5: 218","journal-title":"Commun Biol"},{"key":"BFEMBJ2022112030_CR15","doi-asserted-by":"crossref","first-page":"1429","DOI":"10.1016\/j.cub.2009.07.058","volume":"19","author":"R Fricke","year":"2009","unstructured":"Fricke R, Gohl C, Dharmalingam E, Grevelh\u00f6rster A, Zahedi B, Harden N, Kessels M, Qualmann B, Bogdan S (2009) Drosophila Cip4\/Toca\u20101 integrates membrane trafficking and Actin dynamics through WASP and SCAR\/WAVE. Curr Biol 19: 1429\u20131437","journal-title":"Curr Biol"},{"key":"BFEMBJ2022112030_CR16","doi-asserted-by":"crossref","first-page":"4002","DOI":"10.1016\/j.bpj.2021.08.014","volume":"120","author":"S Ghosh","year":"2021","unstructured":"Ghosh S, Feigelson SW, Montresor A, Shimoni E, Roncato F, Legler DF, Laudanna C, Haran G, Alon R (2021) CCR7 signalosomes are preassembled on tips of lymphocyte microvilli in proximity to LFA\u20101. Biophys J 120: 4002\u20134012","journal-title":"Biophys J"},{"key":"BFEMBJ2022112030_CR17","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1083\/jcb.200407058","volume":"169","author":"T Golub","year":"2005","unstructured":"Golub T, Caroni P (2005) PI(4,5)P2\u2010dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 169: 151\u2013165","journal-title":"J Cell Biol"},{"key":"BFEMBJ2022112030_CR18","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1146\/annurev-immunol-031210-101255","volume":"29","author":"SF Gonzalez","year":"2011","unstructured":"Gonzalez SF, Degn SE, Pitcher LA, Woodruff M, Heesters BA, Carroll MC (2011) Trafficking of B cell antigen in lymph nodes. Annu Rev Immunol 29: 215\u2013233","journal-title":"Annu Rev Immunol"},{"key":"BFEMBJ2022112030_CR19","doi-asserted-by":"crossref","first-page":"2911","DOI":"10.1021\/pr800016a","volume":"7","author":"J\u2010J Hao","year":"2008","unstructured":"Hao J\u2010J, Wang G, Pisitkun T, Patino\u2010Lopez G, Nagashima K, Knepper MA, Shen R\u2010F, Shaw S (2008) Enrichment of distinct microfilament\u2010associated and GTP\u2010binding\u2010proteins in membrane\/microvilli fractions from lymphoid cells. J Proteome Res 7: 2911\u20132927","journal-title":"J Proteome Res"},{"key":"BFEMBJ2022112030_CR20","volume":"37","author":"X He","year":"2018","unstructured":"He X, Kl\u00e4sener K, Iype JM, Becker M, Maity PC, Cavallari M, Nielsen PJ, Yang J, Reth M (2018) Continuous signaling of CD79b and CD19 is required for the fitness of Burkitt lymphoma B cells. EMBO J 37: e97980","journal-title":"EMBO J"},{"key":"BFEMBJ2022112030_CR21","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.cell.2004.06.027","volume":"118","author":"H\u2010YH Ho","year":"2004","unstructured":"Ho H\u2010YH, Rohatgi R, Lebensohn AM, Ma L, Li J, Gygi SP, Kirschner MW (2004) Toca\u20101 mediates Cdc42\u2010dependent Actin nucleation by activating the N\u2010WASP\u2010WIP complex. Cell 118: 203\u2013216","journal-title":"Cell"},{"key":"BFEMBJ2022112030_CR22","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1038\/s41592-020-01008-z","volume":"18","author":"F Isensee","year":"2021","unstructured":"Isensee F, Jaeger PF, Kohl SAA, Petersen J, Maier\u2010Hein KH (2021) nnU\u2010net: a self\u2010configuring method for deep learning\u2010based biomedical image segmentation. Nat Methods 18: 203\u2013211","journal-title":"Nat Methods"},{"key":"BFEMBJ2022112030_CR23","doi-asserted-by":"crossref","first-page":"1705","DOI":"10.1109\/TVCG.2015.2446493","volume":"22","author":"T Jerman","year":"2016","unstructured":"Jerman T, Pernu\u0161 F, Likar B, \u0160piclin \u017d (2016a) Blob enhancement and visualization for improved intracranial aneurysm detection. IEEE Trans Vis Comput Graph 22: 1705\u20131717","journal-title":"IEEE Trans Vis Comput Graph"},{"key":"BFEMBJ2022112030_CR24","doi-asserted-by":"crossref","first-page":"2107","DOI":"10.1109\/TMI.2016.2550102","volume":"35","author":"T Jerman","year":"2016","unstructured":"Jerman T, Pernus F, Likar B, Spiclin Z (2016b) Enhancement of vascular structures in 3D and 2D angiographic images. IEEE Trans Med Imaging 35: 2107\u20132118","journal-title":"IEEE Trans Med Imaging"},{"key":"BFEMBJ2022112030_CR25","doi-asserted-by":"crossref","first-page":"E5916","DOI":"10.1073\/pnas.1604894113","volume":"113","author":"Y Jung","year":"2016","unstructured":"Jung Y, Riven I, Feigelson SW, Kartvelishvily E, Tohya K, Miyasaka M, Alon R, Haran G (2016) Three\u2010dimensional localization of T\u2010cell receptors in relation to microvilli using a combination of superresolution microscopies. Proc Natl Acad Sci U S A 113: E5916\u2013E5924","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBJ2022112030_CR26","doi-asserted-by":"crossref","first-page":"3872","DOI":"10.1038\/s41467-021-23792-8","volume":"12","author":"Y Jung","year":"2021","unstructured":"Jung Y, Wen L, Altman A, Ley K (2021) CD45 pre\u2010exclusion from the tips of T cell microvilli prior to antigen recognition. Nat Commun 12: 3872","journal-title":"Nat Commun"},{"key":"BFEMBJ2022112030_CR27","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1038\/nature06287","volume":"450","author":"T Junt","year":"2007","unstructured":"Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, Boes M, Fink K, Henrickson SE, Shayakhmetov DM, Di Paolo NC et\u00a0al (2007) Subcapsular sinus macrophages in lymph nodes clear lymph\u2010borne viruses and present them to antiviral B cells. Nature 450: 110\u2013114","journal-title":"Nature"},{"key":"BFEMBJ2022112030_CR28","doi-asserted-by":"crossref","DOI":"10.1080\/19420889.2014.1000703","volume":"8","author":"CF Kelley","year":"2015","unstructured":"Kelley CF, Becalska AN, Berciu C, Nicastro D, Rodal AA (2015) Assembly of Actin filaments and microtubules in Nwk F\u2010BAR\u2010induced membrane deformations. Commun Integr Biol 8: e1000703","journal-title":"Commun Integr Biol"},{"key":"BFEMBJ2022112030_CR29","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/j.celrep.2018.06.051","volume":"24","author":"SJ Keppler","year":"2018","unstructured":"Keppler SJ, Burbage M, Gasparrini F, Hartjes L, Aggarwal S, Massaad MJ, Geha RS, Bruckbauer A, Batista FD (2018) The lack of WIP binding to Actin results in impaired B cell migration and altered humoral immune responses. Cell Rep 24: 619\u2013629","journal-title":"Cell Rep"},{"key":"BFEMBJ2022112030_CR30","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.02069","volume":"3","author":"K Kl\u00e4sener","year":"2014","unstructured":"Kl\u00e4sener K, Maity PC, Hobeika E, Yang J, Reth M (2014) B cell activation involves nanoscale receptor reorganizations and inside\u2010out signaling by Syk. Elife 3: e02069","journal-title":"Elife"},{"key":"BFEMBJ2022112030_CR31","doi-asserted-by":"crossref","first-page":"1481","DOI":"10.1103\/RevModPhys.66.1481","volume":"66","author":"AJ Koch","year":"1994","unstructured":"Koch AJ, Meinhardt H (1994) Biological pattern formation: from basic mechanisms to complex structures. Rev Mod Phys 66: 1481\u20131507","journal-title":"Rev Mod Phys"},{"key":"BFEMBJ2022112030_CR32","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1016\/0262-8856(92)90076-F","volume":"10","author":"JJ Koenderink","year":"1992","unstructured":"Koenderink JJ, van Doorn AJ (1992) Surface shape and curvature scales. Image Vis Comput 10: 557\u2013564","journal-title":"Image Vis Comput"},{"key":"BFEMBJ2022112030_CR33","doi-asserted-by":"crossref","first-page":"45","DOI":"10.4161\/sgtp.18960","volume":"3","author":"B\u2010J de Kreuk","year":"2012","unstructured":"de Kreuk B\u2010J, Hordijk PL (2012) Control of rho GTPase function by BAR\u2010domains. Small GTPases 3: 45\u201352","journal-title":"Small GTPases"},{"key":"BFEMBJ2022112030_CR34","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1038\/nri.2017.133","volume":"18","author":"M Kuka","year":"2018","unstructured":"Kuka M, Iannacone M (2018) Viral subversion of B cell responses within secondary lymphoid organs. Nat Rev Immunol 18: 255\u2013265","journal-title":"Nat Rev Immunol"},{"key":"BFEMBJ2022112030_CR35","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1084\/jem.20110896","volume":"209","author":"G Lanzi","year":"2012","unstructured":"Lanzi G, Moratto D, Vairo D, Masneri S, Delmonte O, Paganini T, Parolini S, Tabellini G, Mazza C, Savoldi G et\u00a0al (2012) A novel primary human immunodeficiency due to deficiency in the WASP\u2010interacting protein WIP. J Exp Med 209: 29\u201334","journal-title":"J Exp Med"},{"key":"BFEMBJ2022112030_CR36","first-page":"462","volume":"56","author":"TC Lee","year":"1994","unstructured":"Lee TC, Kashyap RL, Chu CN (1994) Building skeleton models via 3\u2010D medial surface axis thinning algorithms. CVGIP: Graph Model Image Process 56: 462\u2013478","journal-title":"CVGIP: Graph Model Image Process"},{"key":"BFEMBJ2022112030_CR37","first-page":"713","volume":"17","author":"P\u2010S Liao","year":"2001","unstructured":"Liao P\u2010S, Chen T\u2010S, Chung P\u2010C (2001) A fast algorithm for multilevel thresholding. J Inf Sci Eng 17: 713\u2013727","journal-title":"J Inf Sci Eng"},{"key":"BFEMBJ2022112030_CR38","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1038\/ni.1832","volume":"11","author":"BF Lillemeier","year":"2010","unstructured":"Lillemeier BF, M\u00f6rtelmaier MA, Forstner MB, Huppa JB, Groves JT, Davis MM (2010) TCR and Lat are expressed on separate protein islands on T cell membranes and concatenate during activation. Nat Immunol 11: 90\u201396","journal-title":"Nat Immunol"},{"key":"BFEMBJ2022112030_CR39","doi-asserted-by":"crossref","DOI":"10.1126\/scisignal.2005887","volume":"8","author":"PC Maity","year":"2015","unstructured":"Maity PC, Blount A, Jumaa H, Ronneberger O, Lillemeier BF, Reth M (2015) B cell antigen receptors of the IgM and IgD classes are clustered in different protein islands that are altered during B cell activation. Sci Signal 8: ra93","journal-title":"Sci Signal"},{"key":"BFEMBJ2022112030_CR40","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1182\/blood-2004-02-0437","volume":"104","author":"S Majstoravich","year":"2004","unstructured":"Majstoravich S, Zhang J, Nicholson\u2010Dykstra S, Linder S, Friedrich W, Siminovitch KA, Higgs HN (2004) Lymphocyte microvilli are dynamic, actin\u2010dependent structures that do not require Wiskott\u2010Aldrich syndrome protein (WASp) for their morphology. Blood 104: 1396\u20131403","journal-title":"Blood"},{"key":"BFEMBJ2022112030_CR41","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/j.immuni.2012.11.019","volume":"38","author":"PK Mattila","year":"2013","unstructured":"Mattila PK, Feest C, Depoil D, Treanor B, Montaner B, Otipoby KL, Carter R, Justement LB, Bruckbauer A, Batista FD (2013) The actin and tetraspanin networks organize receptor nanoclusters to regulate B cell receptor\u2010mediated signaling. Immunity 38: 461\u2013474","journal-title":"Immunity"},{"key":"BFEMBJ2022112030_CR42","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1083\/jcb.201504137","volume":"212","author":"PK Mattila","year":"2016","unstructured":"Mattila PK, Batista FD, Treanor B (2016) Dynamics of the actin cytoskeleton mediates receptor cross talk: an emerging concept in tuning receptor signaling. J Cell Biol 212: 267\u2013280","journal-title":"J Cell Biol"},{"key":"BFEMBJ2022112030_CR43","doi-asserted-by":"crossref","first-page":"1977","DOI":"10.1080\/15384101.2016.1190893","volume":"15","author":"NA McDonald","year":"2016","unstructured":"McDonald NA, Gould KL (2016) Linking up at the BAR: oligomerization and F\u2010BAR protein function. Cell Cycle 15: 1977\u20131985","journal-title":"Cell Cycle"},{"key":"BFEMBJ2022112030_CR44","doi-asserted-by":"crossref","DOI":"10.1083\/jcb.202203017","volume":"221","author":"A Michaud","year":"2022","unstructured":"Michaud A, Leda M, Swider ZT, Kim S, He J, Landino J, Valley JR, Huisken J, Goryachev AB, von Dassow G et\u00a0al (2022) A versatile cortical pattern\u2010forming circuit based on rho, F\u2010actin, Ect2, and RGA\u20103\/4. J Cell Biol 221: e202203017","journal-title":"J Cell Biol"},{"key":"BFEMBJ2022112030_CR45","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1038\/35047107","volume":"408","author":"H Miki","year":"2000","unstructured":"Miki H, Yamaguchi H, Suetsugu S, Takenawa T (2000) IRSp53 is an essential intermediate between Rac and WAVE in the regulation of membrane ruffling. Nature 408: 732\u2013735","journal-title":"Nature"},{"key":"BFEMBJ2022112030_CR46","doi-asserted-by":"crossref","first-page":"1594","DOI":"10.1016\/j.jaci.2013.01.042","volume":"131","author":"D Moshous","year":"2013","unstructured":"Moshous D, Martin E, Carpentier W, Lim A, Callebaut I, Canioni D, Hauck F, Majewski J, Schwartzentruber J, Nitschke P et\u00a0al (2013) Whole\u2010exome sequencing identifies Coronin\u20101A deficiency in 3 siblings with immunodeficiency and EBV\u2010associated B\u2010cell lymphoproliferation. J Allergy Clin Immunol 131: 1594\u20131603","journal-title":"J Allergy Clin Immunol"},{"key":"BFEMBJ2022112030_CR47","volume-title":"An introduction to digital image processing","author":"W Niblack","year":"1985","unstructured":"Niblack W (1985) An introduction to digital image processing. K\u00f8benhavn: Strandberg Publishing Company"},{"key":"BFEMBJ2022112030_CR48","doi-asserted-by":"crossref","DOI":"10.1038\/ncomms10969","volume":"7","author":"D Obino","year":"2016","unstructured":"Obino D, Farina F, Malbec O, S\u00e1ez PJ, Maurin M, Gaillard J, Dingli F, Loew D, Gautreau A, Yuseff M\u2010I et\u00a0al (2016) Actin nucleation at the centrosome controls lymphocyte polarity. Nat Commun 7: 10969","journal-title":"Nat Commun"},{"key":"BFEMBJ2022112030_CR49","doi-asserted-by":"crossref","first-page":"2187","DOI":"10.3389\/fimmu.2020.02187","volume":"11","author":"R Orbach","year":"2020","unstructured":"Orbach R, Su X (2020) Surfing on membrane waves: microvilli, curved membranes, and immune signaling. Front Immunol 11: 2187","journal-title":"Front Immunol"},{"key":"BFEMBJ2022112030_CR50","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1109\/TSMC.1979.4310076","volume":"9","author":"N Otsu","year":"1979","unstructured":"Otsu N (1979) A threshold selection method from gray\u2010level histograms. IEEE Trans Syst Man Cybern 9: 62\u201366","journal-title":"IEEE Trans Syst Man Cybern"},{"key":"BFEMBJ2022112030_CR51","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1038\/ni1494","volume":"8","author":"TG Phan","year":"2007","unstructured":"Phan TG, Grigorova I, Okada T, Cyster JG (2007) Subcapsular encounter and complement\u2010dependent transport of immune complexes by lymph node B cells. Nat Immunol 8: 992\u20131000","journal-title":"Nat Immunol"},{"key":"BFEMBJ2022112030_CR52","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.78330","volume":"11","author":"J Pineau","year":"2022","unstructured":"Pineau J, Pinon L, Mesdjian O, Fattaccioli J, Lennon Dum\u00e9nil A\u2010M, Pierobon P (2022) Microtubules restrict F\u2010Actin polymerization to the immune synapse via GEF\u2010H1 to maintain polarity in lymphocytes. Elife 11: e78330","journal-title":"Elife"},{"key":"BFEMBJ2022112030_CR53","doi-asserted-by":"crossref","first-page":"1672","DOI":"10.1126\/science.1125703","volume":"312","author":"H Qi","year":"2006","unstructured":"Qi H, Egen JG, Huang AYC, Germain RN (2006) Extrafollicular activation of lymph node B cells by antigen\u2010bearing dendritic cells. Science 312: 1672\u20131676","journal-title":"Science"},{"key":"BFEMBJ2022112030_CR54","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1038\/s41467-020-14335-8","volume":"11","author":"I Rey\u2010Suarez","year":"2020","unstructured":"Rey\u2010Suarez I, Wheatley BA, Koo P, Bhanja A, Shu Z, Mochrie S, Song W, Shroff H, Upadhyaya A (2020) WASP family proteins regulate the mobility of the B cell receptor during signaling activation. Nat Commun 11: 439","journal-title":"Nat Commun"},{"key":"BFEMBJ2022112030_CR55","first-page":"E1604","volume":"112","author":"K\u2010H Roh","year":"2015","unstructured":"Roh K\u2010H, Lillemeier BF, Wang F, Davis MM (2015) The coreceptor CD4 is expressed in distinct nanoclusters and does not colocalize with T\u2010cell receptor and active protein tyrosine kinase p56lck. Proc Natl Acad Sci U S A 112: E1604\u2013E1613","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBJ2022112030_CR56","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1093\/intimm\/dxn110","volume":"20","author":"R Roozendaal","year":"2008","unstructured":"Roozendaal R, Mebius RE, Kraal G (2008) The conduit system of the lymph node. Int Immunol 20: 1483\u20131487","journal-title":"Int Immunol"},{"key":"BFEMBJ2022112030_CR57","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.immuni.2008.12.014","volume":"30","author":"R Roozendaal","year":"2009","unstructured":"Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, Mebius RE, von Andrian UH, Carroll MC (2009) Conduits mediate transport of low\u2010molecular\u2010weight antigen to lymph node follicles. Immunity 30: 264\u2013276","journal-title":"Immunity"},{"key":"BFEMBJ2022112030_CR58","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1016\/j.devcel.2015.04.014","volume":"33","author":"J Saarikangas","year":"2015","unstructured":"Saarikangas J, Kourdougli N, Senju Y, Chazal G, Segerstr\u00e5le M, Minkeviciene R, Kuurne J, Mattila PK, Garrett L, H\u00f6lter SM et\u00a0al (2015) MIM\u2010induced membrane bending promotes dendritic spine initiation. Dev Cell 33: 644\u2013659","journal-title":"Dev Cell"},{"key":"BFEMBJ2022112030_CR59","first-page":"2411","volume":"126","author":"W Saengsawang","year":"2013","unstructured":"Saengsawang W, Taylor KL, Lumbard DC, Mitok K, Price A, Pietila L, Gomez TM, Dent EW (2013) CIP4 Coordinates with phospholipids and Actin\u2010associated proteins to localize to the protruding edge and produce Actin ribs and veils. J Cell Sci 126: 2411\u20132423","journal-title":"J Cell Sci"},{"key":"BFEMBJ2022112030_CR60","doi-asserted-by":"crossref","first-page":"3686","DOI":"10.4049\/jimmunol.1102594","volume":"188","author":"PT Sage","year":"2012","unstructured":"Sage PT, Varghese LM, Martinelli R, Sciuto TE, Kamei M, Dvorak AM, Springer TA, Sharpe AH, Carman CV (2012) Antigen recognition is facilitated by invadosome\u2010like protrusions formed by memory\/effector T cells. J Immunol 188: 3686\u20133699","journal-title":"J Immunol"},{"key":"BFEMBJ2022112030_CR61","doi-asserted-by":"crossref","first-page":"133","DOI":"10.21512\/emacsjournal.v2i3.6737","volume":"2","author":"YC Sanjaya","year":"2020","unstructured":"Sanjaya YC, Gunawan AAS, Irwansyah E (2020) Semantic segmentation for aerial images: a literature review. EMACS J 2: 133\u2013139","journal-title":"EMACS J"},{"key":"BFEMBJ2022112030_CR62","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/S1361-8415(98)80009-1","volume":"2","author":"Y Sato","year":"1998","unstructured":"Sato Y, Nakajima S, Shiraga N, Atsumi H, Yoshida S, Koller T, Gerig G, Kikinis R (1998) Three\u2010dimensional multi\u2010scale line filter for segmentation and visualization of curvilinear structures in medical images. Med Image Anal 2: 143\u2013168","journal-title":"Med Image Anal"},{"key":"BFEMBJ2022112030_CR63","doi-asserted-by":"crossref","first-page":"905","DOI":"10.1016\/j.immuni.2011.06.001","volume":"34","author":"T Schnyder","year":"2011","unstructured":"Schnyder T, Castello A, Feest C, Harwood NE, Oellerich T, Urlaub H, Engelke M, Wienands J, Bruckbauer A, Batista FD (2011) B cell receptor\u2010mediated antigen gathering requires ubiquitin ligase Cbl and adaptors Grb2 and Dok\u20103 to recruit dynein to the signaling microcluster. Immunity 34: 905\u2013918","journal-title":"Immunity"},{"key":"BFEMBJ2022112030_CR64","doi-asserted-by":"crossref","first-page":"1246","DOI":"10.1021\/acscentsci.7b00392","volume":"3","author":"M Simunovic","year":"2017","unstructured":"Simunovic M, \u0160ari\u0107 A, Henderson JM, Lee KYC, Voth GA (2017) Long\u2010range organization of membrane\u2010curving proteins. ACS Cent Sci 3: 1246\u20131253","journal-title":"ACS Cent Sci"},{"key":"BFEMBJ2022112030_CR65","unstructured":"Sofroniew N, Lambert T, Evans K, Nunez\u2010Iglesias J, Bokota G, Pe\u00f1a\u2010Castellanos G, Winston P, Yamauchi K, Bussonnier M, Pop DD et\u00a0al (2021) napari\/napari: 0.4.12rc1. Zenodohttps:\/\/doi.org\/10.5281\/zenodo.5586292"},{"key":"BFEMBJ2022112030_CR66","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.tcb.2012.01.001","volume":"22","author":"S Suetsugu","year":"2012","unstructured":"Suetsugu S, Gautreau A (2012) Synergistic BAR\u2010NPF interactions in actin\u2010driven membrane remodeling. Trends Cell Biol 22: 141\u2013150","journal-title":"Trends Cell Biol"},{"key":"BFEMBJ2022112030_CR67","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1152\/physrev.00040.2013","volume":"94","author":"S Suetsugu","year":"2014","unstructured":"Suetsugu S, Kurisu S, Takenawa T (2014) Dynamic shaping of cellular membranes by phospholipids and membrane\u2010deforming proteins. Physiol Rev 94: 1219\u20131248","journal-title":"Physiol Rev"},{"key":"BFEMBJ2022112030_CR68","volume":"10","author":"T Sugiyama","year":"2015","unstructured":"Sugiyama T, Pramanik MK, Yumura S (2015) Microtubule\u2010mediated inositol lipid signaling plays critical roles in regulation of Blebbing. PLoS One 10: e0137032","journal-title":"PLoS One"},{"key":"BFEMBJ2022112030_CR80","doi-asserted-by":"crossref","first-page":"1450","DOI":"10.21105\/joss.01450","volume":"4","author":"C Sullivan","year":"2019","unstructured":"Sullivan C, Kaszynski A (2019) PyVista: 3D plotting and mesh analysis through a streamlined interface for the Visualization Toolkit (VTK). J Open Source Softw 4: 1450","journal-title":"J Open Source Softw"},{"key":"BFEMBJ2022112030_CR69","doi-asserted-by":"crossref","first-page":"1485","DOI":"10.1084\/jem.20090209","volume":"206","author":"K Suzuki","year":"2009","unstructured":"Suzuki K, Grigorova I, Phan TG, Kelly LM, Cyster JG (2009) Visualizing B cell capture of cognate antigen from follicular dendritic cells. J Exp Med 206: 1485\u20131493","journal-title":"J Exp Med"},{"key":"BFEMBJ2022112030_CR70","first-page":"132","volume":"1","author":"AJ Thrasher","year":"2009","unstructured":"Thrasher AJ (2009) New insights into the biology of Wiskott\u2010Aldrich syndrome (WAS). ASH Educ Prog Book 1: 132\u2013138","journal-title":"ASH Educ Prog Book"},{"key":"BFEMBJ2022112030_CR71","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1038\/nri.2017.67","volume":"17","author":"P Tolar","year":"2017","unstructured":"Tolar P (2017) Cytoskeletal control of B cell responses to antigens. Nat Rev Immunol 17: 621\u2013634","journal-title":"Nat Rev Immunol"},{"key":"BFEMBJ2022112030_CR72","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.immuni.2009.12.005","volume":"32","author":"B Treanor","year":"2010","unstructured":"Treanor B, Depoil D, Gonzalez\u2010Granja A, Barral P, Weber M, Dushek O, Bruckbauer A, Batista FD (2010) The membrane skeleton controls diffusion dynamics and signaling through the B cell receptor. Immunity 32: 187\u2013199","journal-title":"Immunity"},{"key":"BFEMBJ2022112030_CR73","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1037\/0033-295X.84.4.327","volume":"84","author":"A Tversky","year":"1977","unstructured":"Tversky A (1977) Features of similarity. Psychol Rev 84: 327\u2013352","journal-title":"Psychol Rev"},{"key":"BFEMBJ2022112030_CR74","doi-asserted-by":"crossref","unstructured":"Weems AD, Welf ES, Driscoll MK, Mazloom\u2010Farsibaf H, Chang B\u2010J, Weiss BG, Chi J, Dean KM, Fiolka R, Danuser G (2021) Blebs promote cell survival by assembling oncogenic signaling hubs. bioRxivhttps:\/\/doi.org\/10.1101\/2021.04.23.441200 [PREPRINT]","DOI":"10.1101\/2021.04.23.441200"},{"key":"BFEMBJ2022112030_CR75","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1038\/s41467-017-02469-1","volume":"9","author":"Z Wu","year":"2018","unstructured":"Wu Z, Su M, Tong C, Wu M, Liu J (2018) Membrane shape\u2010mediated wave propagation of cortical protein dynamics. Nat Commun 9: 136","journal-title":"Nat Commun"},{"key":"BFEMBJ2022112030_CR76","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.4049\/jimmunol.161.3.1313","volume":"161","author":"M Wykes","year":"1998","unstructured":"Wykes M, Pombo A, Jenkins C, MacPherson GG (1998) Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T\u2010dependent response. J Immunol 161: 1313\u20131319","journal-title":"J Immunol"},{"key":"BFEMBJ2022112030_CR77","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1038\/nchembio.2000","volume":"12","author":"D Xiong","year":"2016","unstructured":"Xiong D, Xiao S, Guo S, Lin Q, Nakatsu F, Wu M (2016) Frequency and amplitude control of cortical oscillations by phosphoinositide waves. Nat Chem Biol 12: 159\u2013166","journal-title":"Nat Chem Biol"},{"key":"BFEMBJ2022112030_CR78","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1016\/j.celrep.2013.08.024","volume":"4","author":"H Zhao","year":"2013","unstructured":"Zhao H, Michelot A, Koskela EV, Tkach V, Stamou D, Drubin DG, Lappalainen P (2013) Membrane\u2010sculpting BAR domains generate stable lipid microdomains. Cell Rep 4: 1213\u20131223","journal-title":"Cell Rep"},{"key":"BFEMBJ2022112030_CR79","volume":"64","author":"J Zhao","year":"2019","unstructured":"Zhao J, Ai D, Yang Y, Song H, Huang Y, Wang Y, Yang J (2019) Deep feature regression (DFR) for 3D vessel segmentation. Phys Med Biol 64: 115006","journal-title":"Phys Med Biol"}],"container-title":["The EMBO Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.15252\/embj.2022112030.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.15252\/embj.2022112030","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.15252\/embj.2022112030\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.embopress.org\/doi\/pdf\/10.15252\/embj.2022112030","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.15252\/embj.2022112030.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T20:34:30Z","timestamp":1779309270000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.15252\/embj.2022112030"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,3]]},"references-count":80,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2023,2,15]]}},"alternative-id":["BFEMBJ2022112030"],"URL":"https:\/\/doi.org\/10.15252\/embj.2022112030","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.04.29.489661","asserted-by":"object"}]},"ISSN":["0261-4189","1460-2075"],"issn-type":[{"value":"0261-4189","type":"print"},{"value":"1460-2075","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,1,3]]},"assertion":[{"value":"1 July 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 December 2022","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 December 2022","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 January 2023","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"EMBJ2022112030"}}