{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T22:50:17Z","timestamp":1778885417476,"version":"3.51.4"},"reference-count":105,"publisher":"Wiley","issue":"9","license":[{"start":{"date-parts":[[2018,10,18]],"date-time":"2018-10-18T00:00:00Z","timestamp":1539820800000},"content-version":"vor","delay-in-days":47,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000052","name":"NIH Office of the Director","doi-asserted-by":"publisher","award":["DP2 CA186571"],"award-info":[{"award-number":["DP2 CA186571"]}],"id":[{"id":"10.13039\/100000052","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Protein Science"],"published-print":{"date-parts":[[2018,9]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The beta pore\u2010forming proteins (\u03b2\u2010PFPs) are a large class of polypeptides that are produced by all Kingdoms of life to contribute to their species' own survival. Pore assembly is a sophisticated multi\u2010step process that includes receptor\/membrane recognition and oligomerization events, and is ensued by large\u2010scale structural rearrangements, which facilitate maturation of a prepore into a functional membrane spanning pore. A full understanding of pore formation, assembly, and maturation has traditionally been hindered by a lack of structural data; particularly for assemblies representing differing conformations of functional pores. However, recent advancements in cryo\u2010electron microscopy (cryo\u2010EM) techniques have provided the opportunity to delineate the structures of such flexible complexes, and in different states, to near\u2010atomic resolution. In this review, we place a particular emphasis on the use of cryo\u2010EM to uncover the mechanistic details including architecture, activation, and maturation for some of the prominent members of this family.<\/jats:p>","DOI":"10.1002\/pro.3454","type":"journal-article","created":{"date-parts":[[2018,8,22]],"date-time":"2018-08-22T15:32:17Z","timestamp":1534951937000},"page":"1544-1556","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Advances in structure determination by cryo\u2010EM to unravel membrane\u2010spanning pore formation"],"prefix":"10.1002","volume":"27","author":[{"given":"Harry","family":"Scott","sequence":"first","affiliation":[{"name":"Department of Pharmacology Case Western Reserve University  Cleveland Ohio 44106"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei","family":"Huang","sequence":"additional","affiliation":[{"name":"Department of Pharmacology Case Western Reserve University  Cleveland Ohio 44106"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"James G.","family":"Bann","sequence":"additional","affiliation":[{"name":"Department of Chemistry Wichita State University  Wichita Kansas 67260"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Derek J.","family":"Taylor","sequence":"additional","affiliation":[{"name":"Department of Pharmacology Case Western Reserve University  Cleveland Ohio 44106"},{"name":"Department of Biochemistry Case Western Reserve University  Cleveland Ohio 44106"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2018,10,18]]},"reference":[{"key":"e_1_2_5_2_1","doi-asserted-by":"publisher","DOI":"10.1038\/nri911"},{"key":"e_1_2_5_3_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-642-56508-3"},{"key":"e_1_2_5_4_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.273.9.5300"},{"key":"e_1_2_5_5_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M708747200"},{"key":"e_1_2_5_6_1","doi-asserted-by":"publisher","DOI":"10.1529\/biophysj.108.129981"},{"key":"e_1_2_5_7_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-5793(00)01744-0"},{"key":"e_1_2_5_8_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0431098100"},{"key":"e_1_2_5_9_1","doi-asserted-by":"publisher","DOI":"10.1152\/ajpcell.00582.2004"},{"key":"e_1_2_5_10_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.89.21.10277"},{"key":"e_1_2_5_11_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.273.49.32656"},{"key":"e_1_2_5_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbiomolbio.2004.01.009"},{"key":"e_1_2_5_13_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.3769"},{"key":"e_1_2_5_14_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature.2017.22738"},{"key":"e_1_2_5_15_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2818.1981.tb02483.x"},{"key":"e_1_2_5_16_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0033583500004297"},{"key":"e_1_2_5_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jsb.2012.02.003"},{"key":"e_1_2_5_18_1","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.2472"},{"key":"e_1_2_5_19_1","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.03665"},{"key":"e_1_2_5_20_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro.2015.3"},{"key":"e_1_2_5_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.chom.2012.08.005"},{"key":"e_1_2_5_22_1","first-page":"1483","article-title":"Cytolysis by H\u20102\u2010specific T killer cells","volume":"157","author":"Dennert G","year":"1983","journal-title":"Assembly of tubular complexes on target membranes. J Exp Med"},{"key":"e_1_2_5_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0021-9258(17)42872-9"},{"key":"e_1_2_5_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/0092-8674(86)90007-3"},{"key":"e_1_2_5_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2005.02.033"},{"key":"e_1_2_5_26_1","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.04247"},{"key":"e_1_2_5_27_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1002049"},{"key":"e_1_2_5_28_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature14247"},{"key":"e_1_2_5_29_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms11293"},{"key":"e_1_2_5_30_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms12062"},{"key":"e_1_2_5_31_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02931271"},{"key":"e_1_2_5_32_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-007-7434-y"},{"key":"e_1_2_5_33_1","first-page":"823","article-title":"Structural insights into the membrane\u2010anchoring mechanism of a cholesterol\u2010dependent cytolysin","volume":"9","author":"Ramachandran R","year":"2002","journal-title":"Nat Struct Biol"},{"key":"e_1_2_5_34_1","doi-asserted-by":"publisher","DOI":"10.1097\/QCO.0b013e328012c5f1"},{"key":"e_1_2_5_35_1","doi-asserted-by":"publisher","DOI":"10.1097\/00000441-200207000-00008"},{"key":"e_1_2_5_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2005.11.030"},{"key":"e_1_2_5_37_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.mam.2009.06.003"},{"key":"e_1_2_5_38_1","doi-asserted-by":"crossref","first-page":"11099","DOI":"10.1016\/S0021-9258(18)60433-8","article-title":"Internalization and processing of Bacillus anthracis lethal toxin by toxin\u2010sensitive and \u2010resistant cells","volume":"264","author":"Singh Y","year":"1989","journal-title":"J Biol Chem"},{"key":"e_1_2_5_39_1","doi-asserted-by":"publisher","DOI":"10.1038\/322831a0"},{"key":"e_1_2_5_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-291X(02)00547-8"},{"key":"e_1_2_5_41_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-94-017-8881-6_14"},{"key":"e_1_2_5_42_1","doi-asserted-by":"publisher","DOI":"10.1093\/pcp\/pci095"},{"key":"e_1_2_5_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.dci.2005.09.002"},{"key":"e_1_2_5_44_1","doi-asserted-by":"publisher","DOI":"10.1084\/jem.167.4.1459"},{"key":"e_1_2_5_45_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1998.00750.x"},{"key":"e_1_2_5_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbamem.2011.07.036"},{"key":"e_1_2_5_47_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M115.656769"},{"key":"e_1_2_5_48_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2015.00262"},{"key":"e_1_2_5_49_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2015.00257"},{"key":"e_1_2_5_50_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro1824"},{"key":"e_1_2_5_51_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2012.02.003"},{"key":"e_1_2_5_52_1","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.1998.2167"},{"key":"e_1_2_5_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0092-8674(00)80251-2"},{"key":"e_1_2_5_54_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1462-5822.2008.01191.x"},{"key":"e_1_2_5_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tibs.2014.09.002"},{"key":"e_1_2_5_56_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms10587"},{"key":"e_1_2_5_57_1","doi-asserted-by":"publisher","DOI":"10.1038\/srep13293"},{"key":"e_1_2_5_58_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2016.03.002"},{"key":"e_1_2_5_59_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms10588"},{"key":"e_1_2_5_60_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature09518"},{"key":"e_1_2_5_61_1","doi-asserted-by":"crossref","unstructured":"CooperEL Kauschke E Cossarizza A (2001)Annelid humoral immunity: Cell lysis in Earthworms. In: Beck G Sugumaran M Cooper EL Eds. Phylogenetic Perspectives on the Vertebrate Immune System. Advances in Experimental Medicine and Biology Vol. 484. Boston MA: Springer pp169\u2013183.","DOI":"10.1007\/978-1-4615-1291-2_15"},{"key":"e_1_2_5_62_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.str.2012.06.011"},{"key":"e_1_2_5_63_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms11598"},{"key":"e_1_2_5_64_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi049561j"},{"key":"e_1_2_5_65_1","doi-asserted-by":"publisher","DOI":"10.1080\/09687860600995540"},{"key":"e_1_2_5_66_1","doi-asserted-by":"publisher","DOI":"10.1038\/n35101999"},{"key":"e_1_2_5_67_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1462-5822.2000.00052.x"},{"key":"e_1_2_5_68_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature02763"},{"key":"e_1_2_5_69_1","doi-asserted-by":"crossref","first-page":"5012","DOI":"10.1016\/S0021-9258(18)89172-4","article-title":"Crystallization of the protective antigen protein of Bacillus anthracis","volume":"260","author":"Allured VS","year":"1985","journal-title":"J Biol Chem"},{"key":"e_1_2_5_70_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2009.07.037"},{"key":"e_1_2_5_71_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2010.04.041"},{"key":"e_1_2_5_72_1","doi-asserted-by":"publisher","DOI":"10.1016\/0378-1119(88)90501-X"},{"key":"e_1_2_5_73_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2958.1994.tb00500.x"},{"key":"e_1_2_5_74_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.280.5364.734"},{"key":"e_1_2_5_75_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-2958.1998.00953.x"},{"key":"e_1_2_5_76_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0010019"},{"key":"e_1_2_5_77_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1113380"},{"key":"e_1_2_5_78_1","doi-asserted-by":"publisher","DOI":"10.1063\/1.4816467"},{"key":"e_1_2_5_79_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0405405101"},{"key":"e_1_2_5_80_1","doi-asserted-by":"publisher","DOI":"10.1002\/pro.752"},{"key":"e_1_2_5_81_1","doi-asserted-by":"publisher","DOI":"10.1002\/pro.2136"},{"key":"e_1_2_5_82_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2436299100"},{"key":"e_1_2_5_83_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M008309200"},{"key":"e_1_2_5_84_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/15.4.327"},{"key":"e_1_2_5_85_1","doi-asserted-by":"publisher","DOI":"10.1038\/nchembio.1312"},{"key":"e_1_2_5_86_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0020349"},{"key":"e_1_2_5_87_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0925-4439(00)00029-6"},{"key":"e_1_2_5_88_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-5793(01)02491-7"},{"key":"e_1_2_5_89_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-5793(01)02486-3"},{"key":"e_1_2_5_90_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1359-0278(96)00018-1"},{"key":"e_1_2_5_91_1","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1128\/jb.163.1.336-340.1985","article-title":"Activation of the hole\u2010forming toxin aerolysin by extracellular processing","volume":"163","author":"Howard SP","year":"1985","journal-title":"J Bacteriol"},{"key":"e_1_2_5_92_1","doi-asserted-by":"publisher","DOI":"10.1021\/bi00151a026"},{"key":"e_1_2_5_93_1","doi-asserted-by":"publisher","DOI":"10.1038\/367292a0"},{"key":"e_1_2_5_94_1","unstructured":"LepplaSH(1991)The anthrax toxin complex. In: Alouf EJ Freer JH (Eds.) Sourcebook of bacterial protein toxins New York: Academic Press pp277\u2013302."},{"key":"e_1_2_5_95_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.0020056"},{"key":"e_1_2_5_96_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M115.646109"},{"key":"e_1_2_5_97_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.mib.2004.12.005"},{"key":"e_1_2_5_98_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.M402676200"},{"key":"e_1_2_5_99_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biochi.2013.06.012"},{"key":"e_1_2_5_100_1","doi-asserted-by":"publisher","DOI":"10.1046\/j.1432-1033.2002.03338.x"},{"key":"e_1_2_5_101_1","doi-asserted-by":"publisher","DOI":"10.1074\/jbc.274.32.22604"},{"key":"e_1_2_5_102_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0014-5793(02)02274-3"},{"key":"e_1_2_5_103_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/bts152"},{"key":"e_1_2_5_104_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature13603"},{"key":"e_1_2_5_105_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.str.2016.09.014"},{"key":"e_1_2_5_106_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2016.05.040"}],"container-title":["Protein Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fpro.3454","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/pro.3454","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,14]],"date-time":"2023-09-14T18:06:36Z","timestamp":1694714796000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/pro.3454"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,9]]},"references-count":105,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2018,9]]}},"alternative-id":["10.1002\/pro.3454"],"URL":"https:\/\/doi.org\/10.1002\/pro.3454","archive":["Portico"],"relation":{},"ISSN":["0961-8368","1469-896X"],"issn-type":[{"value":"0961-8368","type":"print"},{"value":"1469-896X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,9]]},"assertion":[{"value":"2018-04-28","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-06-11","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-10-18","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}