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It is also an essential process for the bottom-up creation of novel molecular architectures and devices for synthetic biology. However, the complexity of protein\u2013protein interaction surfaces makes it challenging to mimic natural assembly processes in artificial systems. Indeed, many successful computationally designed protein assemblies are prescreened for \u201cdesignability\u201d, limiting the choice of components. Here, we report a simple and pragmatic strategy to assemble chosen multisubunit proteins into more complex structures. A coiled-coil domain appended to one face of the pentameric cholera toxin B-subunit (CTB) enabled the ordered assembly of tubular supra-molecular complexes. Analysis of a tubular structure determined by X-ray crystallography has revealed a hierarchical assembly process that displays features reminiscent of the polymorphic assembly of polyomavirus proteins. The approach provides a simple and straightforward method to direct the assembly of protein building blocks which present either termini on a single face of an oligomer. This scaffolding approach can be used to generate bespoke supramolecular assemblies of functional proteins. Additionally, structural resolution of the scaffolded assemblies highlight \u201cnative-state\u201d forced protein\u2013protein interfaces, which may prove useful as starting conformations for future computational design.<\/jats:p>","DOI":"10.1021\/jacs.8b11480","type":"journal-article","created":{"date-parts":[[2019,3,11]],"date-time":"2019-03-11T18:50:51Z","timestamp":1552330251000},"page":"5211-5219","source":"Crossref","is-referenced-by-count":26,"title":["Directed\nAssembly of Homopentameric Cholera Toxin\nB-Subunit Proteins into Higher-Order Structures Using Coiled-Coil\nAppendages"],"prefix":"10.1021","volume":"141","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4784-103X","authenticated-orcid":true,"given":"James F.","family":"Ross","sequence":"first","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gemma C.","family":"Wildsmith","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Johnson","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel L.","family":"Hurdiss","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristian","family":"Hollingsworth","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebecca F.","family":"Thompson","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Majid","family":"Mosayebi","sequence":"additional","affiliation":[{"name":"University of Bristol , , ,","place":["Bristol, United Kingdom, BS8 1TW"]},{"name":"University of Bristol , , ,","place":["Bristol, United Kingdom, BS8 1TQ"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chi H.","family":"Trinh","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4891-2768","authenticated-orcid":true,"given":"Emanuele","family":"Paci","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arwen R.","family":"Pearson","sequence":"additional","affiliation":[{"name":"Universita\u0308t Hamburg , , ,","place":["Hamburg, Germany, D-22761"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3574-4686","authenticated-orcid":true,"given":"Michael E.","family":"Webb","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7352-0360","authenticated-orcid":true,"given":"W. Bruce","family":"Turnbull","sequence":"additional","affiliation":[{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]},{"name":"University of Leeds , , ,","place":["Leeds, United Kingdom, LS2 9JT"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2019,3,11]]},"reference":[{"issue":"1","key":"2026090305111593500_cit1","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1146\/annurev-biochem-060614-034142","article-title":"Structure, Dynamics, Assembly, and Evolution of Protein\nComplexes","volume":"84","author":"Marsh","year":"2015","journal-title":"Annu. Rev. Biochem."},{"issue":"5","key":"2026090305111593500_cit2","doi-asserted-by":"publisher","first-page":"874","DOI":"10.1016\/j.devcel.2012.10.011","article-title":"Building Complexity:\nInsights into Self-Organized Assembly\nof Microtubule-Based Architectures","volume":"23","author":"Subramanian","year":"2012","journal-title":"Dev. Cell"},{"issue":"1\u20132","key":"2026090305111593500_cit3","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.abb.2012.10.015","article-title":"Assembly,\nStability and Dynamics of Virus Capsids","volume":"531","author":"Mateu","year":"2013","journal-title":"Arch.\nBiochem. Biophys."},{"issue":"2","key":"2026090305111593500_cit4","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1111\/mmi.13117","article-title":"Bacterial\nMicrocompartments: Widespread\nProkaryotic Organelles for Isolation and Optimization of Metabolic\nPathways","volume":"98","author":"Bobik","year":"2015","journal-title":"Mol. Microbiol."},{"issue":"5","key":"2026090305111593500_cit5","doi-asserted-by":"publisher","first-page":"277","DOI":"10.1038\/nrmicro.2018.10","article-title":"Bacterial\nMicrocompartments","volume":"16","author":"Kerfeld","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"issue":"1","key":"2026090305111593500_cit6","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1021\/cb700249v","article-title":"Peptide and Protein\nBuilding Blocks for Synthetic Biology: From Programming Biomolecules\nto Self-Organized Biomolecular Systems","volume":"3","author":"Bromley","year":"2008","journal-title":"ACS\nChem. Biol."},{"key":"2026090305111593500_cit7","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.jbiotec.2012.09.002","article-title":"Bacterial Microcompartments\nMoving into a Synthetic Biological World","volume":"163","author":"Frank","year":"2013","journal-title":"J.\nBiotechnol."},{"issue":"4","key":"2026090305111593500_cit8","doi-asserted-by":"publisher","first-page":"1653","DOI":"10.1021\/cr400011b","article-title":"Ferritin:\nA Versatile Building Block for Bionanotechnology","volume":"115","author":"Jutz","year":"2015","journal-title":"Chem. Rev."},{"key":"2026090305111593500_cit9","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1016\/j.sbi.2016.07.003","article-title":"The Design of Symmetric Protein Nanomaterials Comes\nof Age in Theory and Practice","volume":"39","author":"Yeates","year":"2016","journal-title":"Curr. Opin. Struct.\nBiol."},{"key":"2026090305111593500_cit10","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.cbpa.2017.06.020","article-title":"Advances in Design of Protein Folds\nand Assemblies","volume":"40","author":"Ljubetic\u030c","year":"2017","journal-title":"Curr. Opin. Chem. Biol."},{"issue":"1","key":"2026090305111593500_cit11","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1146\/annurev-biophys-070816-033928","article-title":"Geometric\nPrinciples for Designing Highly Symmetric Self-Assembling Protein\nNanomaterials","volume":"46","author":"Yeates","year":"2017","journal-title":"Annu. Rev. Biophys."},{"key":"2026090305111593500_cit12","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.copbio.2017.01.001","article-title":"Design and Construction\nof Self-Assembling Supramolecular Protein\nComplexes Using Artificial and Fusion Proteins as Nanoscale Building\nBlocks","volume":"46","author":"Kobayashi","year":"2017","journal-title":"Curr. Opin. Biotechnol."},{"issue":"2","key":"2026090305111593500_cit13","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1007\/s12551-017-0376-1","article-title":"Hierarchical\nDesign of Artificial Proteins and Complexes toward Synthetic Structural\nBiology","volume":"10","author":"Arai","year":"2018","journal-title":"Biophys. Rev."},{"key":"2026090305111593500_cit14","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1038\/350631a0","article-title":"Synthesis from DNA\nof a Molecule with the Connectivity\nof a Cube","volume":"350","author":"Chen","year":"1991","journal-title":"Nature"},{"issue":"6111","key":"2026090305111593500_cit15","doi-asserted-by":"publisher","first-page":"1177","DOI":"10.1126\/science.1227268","article-title":"Three-Dimensional\nStructures Self-Assembled from DNA\nBricks","volume":"338","author":"Yin","year":"2012","journal-title":"Science"},{"issue":"6","key":"2026090305111593500_cit16","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1021\/sb300028q","article-title":"A Basis\nSet of de Novo\nCoiled-Coil Peptide Oligomers for Rational Protein Design and Synthetic\nBiology","volume":"1","author":"Fletcher","year":"2012","journal-title":"ACS Synth. Biol."},{"issue":"6132","key":"2026090305111593500_cit17","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1126\/science.1233936","article-title":"Self-Assembling\nCages\nfrom Coiled-Coil Peptide Modules","volume":"340","author":"Fletcher","year":"2013","journal-title":"Science"},{"issue":"6","key":"2026090305111593500_cit18","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1038\/nchembio.1248","article-title":"Design of a Single-Chain Polypeptide\nTetrahedron Assembled from Coiled-Coil Segments","volume":"9","author":"Gradis\u030car","year":"2013","journal-title":"Nat. Chem. Biol."},{"issue":"2","key":"2026090305111593500_cit19","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1016\/j.str.2014.12.008","article-title":"Structural\nPlasticity of Helical Nanotubes Based on Coiled-Coil Assemblies","volume":"23","author":"Egelman","year":"2015","journal-title":"Structure"},{"issue":"24","key":"2026090305111593500_cit20","doi-asserted-by":"publisher","first-page":"8102","DOI":"10.1021\/jacs.7b03890","article-title":"X-Ray Crystallographic\nStructure of a Giant Double-Walled Peptide Nanotube Formed by a Macrocyclic\n\u03b2-Sheet Containing A\u03b216\u201322","volume":"139","author":"Chen","year":"2017","journal-title":"J. Am. Chem. Soc."},{"issue":"6208","key":"2026090305111593500_cit21","doi-asserted-by":"publisher","first-page":"485","DOI":"10.1126\/science.1257452","article-title":"Computational\nDesign of Water-Soluble\n\u03b1-Helical Barrels","volume":"346","author":"Thomson","year":"2014","journal-title":"Science"},{"issue":"11","key":"2026090305111593500_cit22","doi-asserted-by":"publisher","first-page":"1094","DOI":"10.1038\/nbt.3994","article-title":"Design of Coiled-Coil Protein-Origami Cages That Self-Assemble in\nVitro and in Vivo","volume":"35","author":"Ljubetic\u030c","year":"2017","journal-title":"Nat. Biotechnol."},{"key":"2026090305111593500_cit23","doi-asserted-by":"publisher","first-page":"14663","DOI":"10.1038\/ncomms14663","article-title":"Structure\nand Assembly of Scalable Porous Protein Cages","volume":"8","author":"Sasaki","year":"2017","journal-title":"Nat. Commun."},{"issue":"2","key":"2026090305111593500_cit24","doi-asserted-by":"publisher","first-page":"558","DOI":"10.1021\/jacs.7b10513","article-title":"Diversification\nof Protein Cage Structure\nUsing Circularly Permuted Subunits","volume":"140","author":"Azuma","year":"2018","journal-title":"J. Am. Chem.\nSoc."},{"issue":"7503","key":"2026090305111593500_cit25","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1038\/nature13404","article-title":"Accurate Design of\nCo-Assembling Multi-Component Protein Nanomaterials","volume":"510","author":"King","year":"2014","journal-title":"Nature"},{"issue":"18","key":"2026090305111593500_cit26","doi-asserted-by":"publisher","first-page":"2077","DOI":"10.1002\/smll.200900667","article-title":"A Self-Assembled\nProtein Nanotube with High Aspect Ratio","volume":"5","author":"Miranda","year":"2009","journal-title":"Small"},{"key":"2026090305111593500_cit27","doi-asserted-by":"publisher","first-page":"1046","DOI":"10.1039\/C8SC04167A","article-title":"Construction of Supramolecular\nNanotubes from Protein Crystals","volume":"10","author":"Nguyen","year":"2019","journal-title":"Chem. Sci."},{"issue":"7610","key":"2026090305111593500_cit28","doi-asserted-by":"publisher","first-page":"136","DOI":"10.1038\/nature18010","article-title":"Design of a Hyperstable\n60-Subunit Protein\nIcosahedron","volume":"535","author":"Hsia","year":"2016","journal-title":"Nature"},{"issue":"6297","key":"2026090305111593500_cit29","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1126\/science.aaf8818","article-title":"Accurate Design of Megadalton-Scale\nTwo-Component Icosahedral Protein Complexes","volume":"353","author":"Bale","year":"2016","journal-title":"Science"},{"issue":"10","key":"2026090305111593500_cit30","doi-asserted-by":"publisher","first-page":"3433","DOI":"10.1039\/C7CS00818J","article-title":"Protein Cage Assembly across Multiple\nLength Scales","volume":"47","author":"Aumiller","year":"2018","journal-title":"Chem. Soc. Rev."},{"issue":"5","key":"2026090305111593500_cit31","doi-asserted-by":"publisher","first-page":"2217","DOI":"10.1073\/pnas.041614998","article-title":"Nanohedra: Using Symmetry to Design\nSelf Assembling Protein Cages, Layers, Crystals, and Filaments","volume":"98","author":"Padilla","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"issue":"12","key":"2026090305111593500_cit32","doi-asserted-by":"publisher","first-page":"1065","DOI":"10.1038\/nchem.2107","article-title":"Structure\nof a Designed Protein Cage That Self-Assembles into a Highly Porous\nCube","volume":"6","author":"Lai","year":"2014","journal-title":"Nat. Chem."},{"issue":"6017","key":"2026090305111593500_cit33","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1126\/science.1199081","article-title":"Directed Evolution of a Protein Container","volume":"331","author":"Wo\u0308rsdo\u0308rfer","year":"2011","journal-title":"Science"},{"issue":"5","key":"2026090305111593500_cit34","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1021\/acs.biochem.7b01000","article-title":"A Structure-Based\nAssembly Screen of Protein Cage Libraries\nin Living Cells: Experimentally Repacking a Protein-Protein Interface\nto Recover Cage Formation in an Assembly-Frustrated Mutant","volume":"57","author":"Cornell","year":"2018","journal-title":"Biochemistry"},{"issue":"6","key":"2026090305111593500_cit35","doi-asserted-by":"publisher","first-page":"1004","DOI":"10.1039\/c1ra00282a","article-title":"Evaluation\nof\na Symmetry-Based Strategy for Assembling Protein Complexes","volume":"1","author":"Patterson","year":"2011","journal-title":"RSC Adv."},{"issue":"2","key":"2026090305111593500_cit36","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1002\/pro.2405","article-title":"Characterization\nof a Highly Flexible Self-Assembling\nProtein System Designed to Form Nanocages","volume":"23","author":"Patterson","year":"2014","journal-title":"Protein\nSci."},{"issue":"31","key":"2026090305111593500_cit37","doi-asserted-by":"publisher","first-page":"8681","DOI":"10.1073\/pnas.1606013113","article-title":"Flexible, Symmetry-Directed Approach to Assembling\nProtein Cages","volume":"113","author":"Sciore","year":"2016","journal-title":"Proc. Natl. Acad. Sci. U. S.\nA."},{"issue":"19","key":"2026090305111593500_cit38","doi-asserted-by":"publisher","first-page":"1888","DOI":"10.1002\/cbic.201700406","article-title":"Symmetry-Directed\nSelf-Assembly of a Tetrahedral Protein Cage Mediated by de Novo-Designed\nCoiled Coils","volume":"18","author":"Badieyan","year":"2017","journal-title":"ChemBioChem"},{"issue":"2","key":"2026090305111593500_cit39","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1039\/C7ME00012J","article-title":"Evaluation\nof: De Novo -Designed Coiled Coils as off-the-Shelf Components for\nProtein Assembly","volume":"2","author":"Cristie-David","year":"2017","journal-title":"Mol. Syst. Des. Eng."},{"issue":"2","key":"2026090305111593500_cit40","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1080\/09687680410001663267","article-title":"Cholera Toxin: A Paradigm for Multi-Functional Engagement\nof Cellular Mechanisms (Review)","volume":"21","author":"De Haan","year":"2004","journal-title":"Mol. Membr.\nBiol."},{"issue":"6","key":"2026090305111593500_cit41","doi-asserted-by":"publisher","first-page":"3627","DOI":"10.1128\/IAI.73.6.3627-3635.2005","article-title":"Characterization\nof Fluorescent Chimeras\nof Cholera Toxin and Escherichia Coli Heat-Labile Enterotoxins Produced\nby Use of the Twin Arginine Translocation System","volume":"73","author":"Tinker","year":"2005","journal-title":"Infect. Immun."},{"issue":"4","key":"2026090305111593500_cit42","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1002\/jgm.524","article-title":"Ctb Targeted\nNon-Viral CDNA Delivery Enhances Transgene Expression in Neurons","volume":"6","author":"Barrett","year":"2004","journal-title":"J. Gene Med."},{"issue":"5","key":"2026090305111593500_cit43","doi-asserted-by":"publisher","first-page":"1043","DOI":"10.1006\/jmbi.1998.2076","article-title":"The 1.25 \u00c5 Resolution Refinement of the Cholera\nToxin B-Pentamer: Evidence of Peptide Backbone Strain at the Receptor-Binding\nSite","volume":"282","author":"Merritt","year":"1998","journal-title":"J. Mol. Biol."},{"issue":"5","key":"2026090305111593500_cit44","doi-asserted-by":"publisher","first-page":"887","DOI":"10.1016\/S0006-3495(89)82735-3","article-title":"Polymorphism\nin the Assembly of Polyomavirus\nCapsid Protein VP1","volume":"56","author":"Salunke","year":"1989","journal-title":"Biophys. J."},{"issue":"7","key":"2026090305111593500_cit45","doi-asserted-by":"publisher","first-page":"1899","DOI":"10.1099\/vir.0.19067-0","article-title":"Simian Virus 40 VP1\nCapsid Protein Forms Polymorphic Assemblies in Vitro","volume":"84","author":"Kanesashi","year":"2003","journal-title":"J. Gen. Virol."},{"key":"2026090305111593500_cit46","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/0022-2836(69)90465-3","article-title":"The Structure of Viruses\nof the Papilloma-Polyoma Type V. Tubular\nVariants Built of Pentamers","volume":"40","author":"Kiselev","year":"1969","journal-title":"J. Mol. Biol."},{"issue":"4","key":"2026090305111593500_cit47","doi-asserted-by":"publisher","first-page":"432","DOI":"10.1016\/j.sbi.2012.03.002","article-title":"New Currency for\nOld Rope: From Coiled-Coil Assemblies to \u03b1-Helical Barrels","volume":"22","author":"Woolfson","year":"2012","journal-title":"Curr. Opin. Struct. Biol."},{"issue":"9","key":"2026090305111593500_cit48","doi-asserted-by":"publisher","first-page":"903","DOI":"10.1002\/bies.201600062","article-title":"Coiled-Coils: The\nLong and Short of It","volume":"38","author":"Truebestein","year":"2016","journal-title":"BioEssays"},{"issue":"5","key":"2026090305111593500_cit49","doi-asserted-by":"publisher","first-page":"1427","DOI":"10.1006\/jmbi.2001.4545","article-title":"SOCKET: A Program\nfor Identifying and Analysing Coiled-Coil\nMotifs within Protein Structures","volume":"307","author":"Walshaw","year":"2001","journal-title":"J. Mol. Biol."},{"issue":"8","key":"2026090305111593500_cit50","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1107\/S0365110X53001964","article-title":"The\nPacking of \u03b1-Helices: Simple Coiled-Coils","volume":"6","author":"Crick","year":"1953","journal-title":"Acta Crystallogr."},{"issue":"24","key":"2026090305111593500_cit51","doi-asserted-by":"publisher","first-page":"8229","DOI":"10.1021\/jacs.7b01690","article-title":"Modulation\nof Coiled-Coil Dimer Stability through Surface Residues While Preserving\nPairing Specificity","volume":"139","author":"Drobnak","year":"2017","journal-title":"J. Am. Chem. 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