1932

Abstract

Emerging protein design strategies are enabling the creation of diverse, self-assembling supramolecular structures with precision on the atomic scale. The design possibilities include various types of architectures: finite cages or shells, essentially unbounded two-dimensional and three-dimensional arrays (i.e., crystals), and linear or tubular filaments. In nature, structures of those types are generally symmetric, and, accordingly, symmetry provides a powerful guide for developing new design approaches. Recent design studies have produced numerous protein assemblies in close agreement with geometric specifications. For certain design approaches, a complete list of allowable symmetry combinations that can be used for construction has been articulated, opening a path to a rich diversity of geometrically defined protein materials. Future challenges include improving and elaborating on current strategies and endowing designed protein nanomaterials with properties useful in nanomedicine and material science applications.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070816-033928
2017-05-22
2024-06-24
Loading full text...

Full text loading...

/deliver/fulltext/biophys/46/1/annurev-biophys-070816-033928.html?itemId=/content/journals/10.1146/annurev-biophys-070816-033928&mimeType=html&fmt=ahah

Literature Cited

  1. Atwell S, Ridgway JB, Wells JA, Carter P. 1.  1997. Stable heterodimers from remodeling the domain interface of a homodimer using a phage display library. J. Mol. Biol. 270:26–35 [Google Scholar]
  2. Bale JB, Gonen S, Liu Y, Sheffler W, Ellis D. 2.  et al. 2016. Accurate design of megadalton-scale two-component icosahedral protein complexes. Science 353:389–94 [Google Scholar]
  3. Bale JB, Park RU, Liu Y, Gonen S, Gonen T. 3.  et al. 2015. Structure of a designed tetrahedral protein assembly variant engineered to have improved soluble expression. Protein Sci 24:1695–701 [Google Scholar]
  4. Berger O, Gazit E. 4.  2017. Molecular self-assembly using peptide nucleic acids. Pept. Sci. 108:e22930 [Google Scholar]
  5. Boyle AL, Bromley EHC, Bartlett GJ, Sessions RB, Sharp TH. 5.  et al. 2012. Squaring the circle in peptide assembly: from fibers to discrete nanostructures by de novo design. J. Am. Chem. Soc. 134:15457–67 [Google Scholar]
  6. Boyle AL, Woolfson DN. 6.  2011. De novo designed peptides for biological applications. Chem. Soc. Rev. 40:4295–306 [Google Scholar]
  7. Brodin JD, Ambroggio XI, Tang C, Parent KN, Baker TS, Tezcan FA. 7.  2012. Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays. Nat. Chem. 4:375–82 [Google Scholar]
  8. Brodin JD, Auyeung E, Mirkin CA. 8.  2015. DNA-mediated engineering of multicomponent enzyme crystals. PNAS 112:4564–69 [Google Scholar]
  9. Champion CI, Kickhoefer VA, Liu G, Moniz RJ, Freed AS. 9.  et al. 2009. A vault nanoparticle vaccine induces protective mucosal immunity. PLOS ONE 4:e5409 [Google Scholar]
  10. Cheetham AK, Rao CNR, Feller RK. 10.  2006. Structural diversity and chemical trends in hybrid inorganic–organic framework materials. Chem. Commun. 2006:4780–95 [Google Scholar]
  11. Chiu E, Coulibaly F, Metcalf P. 11.  2012. Insect virus polyhedra, infectious protein crystals that contain virus particles. Curr. Opin. Struct. Biol. 22:234–40 [Google Scholar]
  12. Ciengshin T, Sha R, Seeman NC. 12.  2011. Automatic molecular weaving prototyped by using single-stranded DNA. Angew. Chem. Int. Ed. 50:4419–22 [Google Scholar]
  13. Correia BE, Bates JT, Loomis RJ, Baneyx G, Carrico C. 13.  et al. 2014. Proof of principle for epitope-focused vaccine design. Nature 507:201–6 [Google Scholar]
  14. Crick FH, Watson JD. 14.  1956. Structure of small viruses. Nature 177:473–75 [Google Scholar]
  15. Dahiyat BI, Mayo SL. 15.  1997. De novo protein design: fully automated sequence selection. Science 278:82–87 [Google Scholar]
  16. Dantas G, Kuhlman B, Callender D, Wong M, Baker D. 16.  2003. A large scale test of computational protein design: folding and stability of nine completely redesigned globular proteins. J. Mol. Biol. 332:449–60 [Google Scholar]
  17. Dietz H, Douglas SM, Shih WM. 17.  2009. Folding DNA into twisted and curved nanoscale shapes. Science 325:725–30 [Google Scholar]
  18. DiMaio F, Leaver-Fay A, Bradley P, Baker D, André I. 18.  2011. Modeling symmetric macromolecular structures in Rosetta3. PLOS ONE 6:e20450 [Google Scholar]
  19. Doll TAPF, Dey R, Burkhard P. 19.  2015. Design and optimization of peptide nanoparticles. J. Nanobiotechnol. 13:73 [Google Scholar]
  20. Doll TAPF, Raman S, Dey R, Burkhard P. 20.  2013. Nanoscale assemblies and their biomedical applications. J. R. Soc. Interface 10:20120740 [Google Scholar]
  21. Dotan N, Arad D, Frolow F, Freeman A. 21.  1999. Self-assembly of a tetrahedral lectin into predesigned diamondlike protein crystals. Angew. Chem. Int. Ed. 38:2363–66 [Google Scholar]
  22. Doye JP, Poon WCK. 22.  2006. Protein crystallization in vivo. Curr. Opin. Colloid Interface Sci. 11:40–46 [Google Scholar]
  23. Dryden KA, Crowley CS, Tanaka S, Yeates TO, Yeager M. 23.  2009. Two-dimensional crystals of carboxysome shell proteins recapitulate the hexagonal packing of three-dimensional crystals. Protein Sci 18:2629–35 [Google Scholar]
  24. Fletcher JM, Harniman RL, Barnes FRH, Boyle AL, Collins A. 24.  et al. 2013. Self-assembling cages from coiled-coil peptide modules. Science 340:595–99 [Google Scholar]
  25. Furukawa H, Cordova KE, O'Keeffe M, Yaghi OM. 25.  2013. The chemistry and applications of metal-organic frameworks. Science 341:1230444 [Google Scholar]
  26. Ghadiri MR, Granja JR, Milligan RA, McRee DE, Khazanovich N. 26.  1993. Self-assembling organic nanotubes based on a cyclic peptide architecture. Nature 366:324–27 [Google Scholar]
  27. Glover DJ, Giger L, Kim SS, Naik RR, Clark DS. 27.  2016. Geometrical assembly of ultrastable protein templates for nanomaterials. Nat. Commun. 7:11771 [Google Scholar]
  28. Gonen S, DiMaio F, Gonen T, Baker D. 28.  2015. Design of ordered two-dimensional arrays mediated by noncovalent protein-protein interfaces. Science 348:1365–68 [Google Scholar]
  29. Goodman CM, Choi S, Shandler S, DeGrado WF. 29.  2007. Foldamers as versatile frameworks for the design and evolution of function. Nat. Chem. Biol. 3:252–62 [Google Scholar]
  30. Goodsell DS, Olson AJ. 30.  2000. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29:105–53 [Google Scholar]
  31. Gopalan RD, Del Borgo MP, Mechler AI, Perlmutter P, Aguilar MI. 31.  2015. Geometrically precise building blocks: the self-assembly of beta-peptides. Chem. Biol. 22:1417–23 [Google Scholar]
  32. Grabow WW, Jaeger L. 32.  2014. RNA self-assembly and RNA nanotechnology. Acc. Chem. Res. 47:1871–80 [Google Scholar]
  33. Gradisar H, Bozic S, Doles T, Vengust D, Hafner-Bratkovic I. 33.  et al. 2013. Design of a single-chain polypeptide tetrahedron assembled from coiled-coil segments. Nat. Chem. Biol. 9:362–66 [Google Scholar]
  34. Gradišar H, Božič S, Doles T, Vengust D, Hafner-Bratkovič I. 34.  et al. 2013. Design of a single-chain polypeptide tetrahedron assembled from coiled-coil segments. Nat. Chem. Biol. 9:362–66 [Google Scholar]
  35. Grigoryan G, Kim YH, Acharya R, Axelrod K, Jain RM. 35.  et al. 2011. Computational design of virus-like protein assemblies on carbon nanotube surfaces. Science 332:1071–76 [Google Scholar]
  36. Hahn T. 36.  2005. International Tables for Crystallography, Volume A: Space Group Symmetry Dordrecht, Neth.: Springer [Google Scholar]
  37. Hecht MH. 37.  1994. De novo design of beta-sheet proteins. PNAS 91:8729–30 [Google Scholar]
  38. Horne WS, Gellman SH. 38.  2008. Foldamers with heterogeneous backbones. Acc. Chem. Res. 41:1399–408 [Google Scholar]
  39. Huang P-S, Oberdorfer G, Xu C, Pei XY, Nannenga BL. 39.  et al. 2014. High thermodynamic stability of parametrically designed helical bundles. Science 346:481–85 [Google Scholar]
  40. Jennings GT, Bachmann MF. 40.  2008. The coming of age of virus-like particle vaccines. Biol. Chem. 389:521–36 [Google Scholar]
  41. Jeong WH, Lee H, Song DH, Eom J-H, Kim SC. 41.  et al. 2016. Connecting two proteins using a fusion alpha helix stabilized by a chemical cross linker. Nat. Commun. 7:11031 [Google Scholar]
  42. Joh NH, Wang T, Bhate MP, Acharya R, Wu Y. 42.  et al. 2014. De novo design of a transmembrane Zn2+-transporting four-helix bundle. Science 346:1520–24 [Google Scholar]
  43. Ke Y, Ong LL, Shih WM, Yin P. 43.  2012. Three-dimensional structures self-assembled from DNA bricks. Science 338:1177–83 [Google Scholar]
  44. Kim K-H, Ko D-K, Kim Y-T, Kim NH, Paul J. 44.  et al. 2016. Protein-directed self-assembly of a fullerene crystal. Nat. Commun. 7:11429 [Google Scholar]
  45. King NP, Bale JB, Sheffler W, McNamara DE, Gonen S. 45.  et al. 2014. Accurate design of co-assembling multi-component protein nanomaterials. Nature 510:103–8 [Google Scholar]
  46. King NP, Jacobitz AW, Sawaya MR, Goldschmidt L, Yeates TO. 46.  2010. Structure and folding of a designed knotted protein. PNAS 107:20732–37 [Google Scholar]
  47. King NP, Sheffler W, Sawaya MR, Vollmar BS, Sumida JP. 47.  et al. 2012. Computational design of self-assembling protein nanomaterials with atomic level accuracy. Science 336:1171–74 [Google Scholar]
  48. Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, Baker D. 48.  2003. Design of a novel globular protein fold with atomic-level accuracy. Science 302:1364–68 [Google Scholar]
  49. Lai Y-T, Cascio D, Yeates TO. 49.  2012. Structure of a 16-nm cage designed by using protein oligomers. Science 336:1129 [Google Scholar]
  50. Lai Y-T, Hura GL, Dyer KN, Tang HY, Tainer JA, Yeates TO. 50.  2016. Designing and defining dynamic protein cage nanoassemblies in solution. Sci. Adv. 2:e1501855 [Google Scholar]
  51. Lai Y-T, Jiang L, Chen W, Yeates TO. 51.  2015. On the predictability of the orientation of protein domains joined by a spanning alpha-helical linker. Protein Eng. Des. Sel. 28:491–99 [Google Scholar]
  52. Lai Y-T, King NP, Yeates TO. 52.  2012. Principles for designing ordered protein assemblies. Trends Cell Biol 22:653–61 [Google Scholar]
  53. Lai Y-T, Reading E, Hura GL, Tsai K-L, Laganowsky A. 53.  et al. 2014. Structure of a designed protein cage that self-assembles into a highly porous cube. Nat. Chem. 6:1065–71 [Google Scholar]
  54. Lai Y-T, Tsai K-L, Sawaya MR, Asturias FJ, Yeates TO. 54.  2013. Structure and flexibility of nanoscale protein cages designed by symmetric self-assembly. J. Am. Chem. Soc. 135:7738–43 [Google Scholar]
  55. Lanci CJ, MacDermaid CM, Kang S-g, Acharya R, North B. 55.  et al. 2012. Computational design of a protein crystal. PNAS 109:7304–9 [Google Scholar]
  56. Li H, Zhang K, Pi F, Guo S, Shlyakhtenko L. 56.  et al. 2016. Controllable self-assembly of RNA tetrahedrons with precise shape and size for cancer targeting. Adv. Mater. 28:7501–7 [Google Scholar]
  57. López-Sagaseta J, Malito E, Rappuoli R, Bottomley MJ. 57.  2015. Self-assembling protein nanoparticles in the design of vaccines. Comput. Struct. Biotechnol. J. 14:58–68 [Google Scholar]
  58. Ludwig C, Wagner R. 58.  2007. Virus-like particles—universal molecular toolboxes. Curr. Opin. Biotechnol. 18:537–45 [Google Scholar]
  59. Maham A, Tang Z, Wu H, Wang J, Lin Y. 59.  2009. Protein-based nanomedicine platforms for drug delivery. Small 5:1706–21 [Google Scholar]
  60. Marsh JA, Teichmann SA. 60.  2015. Structure, dynamics, assembly, and evolution of protein complexes. Annu. Rev. Biochem. 84:551–75 [Google Scholar]
  61. Martinek TA, Fulop F. 61.  2012. Peptidic foldamers: ramping up diversity. Chem. Soc. Rev. 41:687–702 [Google Scholar]
  62. Marvin DA, Symmons MF, Straus SK. 62.  2014. Structure and assembly of filamentous bacteriophages. Prog. Biophys. Mol. Biol. 114:80–122 [Google Scholar]
  63. Matthaei JF, DiMaio F, Richards JJ, Pozzo LD, Baker D, Baneyx F. 63.  2015. Designing two-dimensional protein arrays through fusion of multimers and interface mutations. Nano Lett 15:5235–39 [Google Scholar]
  64. Maxwell JC. 64.  1864. On the calculation of the equilibrium and stiffness of frames. Phil. Mag. 27:294–99 [Google Scholar]
  65. Mou Y, Yu J-Y, Wannier TM, Guo C-L, Mayo SL. 65.  2015. Computational design of co-assembling protein-DNA nanowires. Nature 525:230–33 [Google Scholar]
  66. Nogales E, Zhang R. 66.  2016. Visualizing microtubule structural transitions and interactions with associated proteins. Curr. Opin. Struct. Biol. 37:90–96 [Google Scholar]
  67. Ogihara NL, Ghirlanda G, Bryson JW, Gingery M, DeGrado WF, Eisenberg D. 67.  2001. Design of three-dimensional domain-swapped dimers and fibrous oligomers. PNAS 98:1404–9 [Google Scholar]
  68. Ohayon YP, Sha R, Flint O, Chandrasekaran AR, Abdallah HO. 68.  et al. 2015. Topological linkage of DNA tiles bonded by paranemic cohesion. ACS Nano 9:10296–303 [Google Scholar]
  69. Ohno H, Osada E, Saito H. 69.  2015. Design, assembly, and evaluation of RNA-protein nanostructures. Methods Mol. Biol. 1297:197–211 [Google Scholar]
  70. Padilla JE, Colovos C, Yeates TO. 70.  2001. Nanohedra: using symmetry to design self assembling protein cages, layers, crystals, and filaments. PNAS 98:2217–21 [Google Scholar]
  71. Padilla JE, Liu W, Seeman NC. 71.  2012. Hierarchical self assembly of patterns from the Robinson tilings: DNA tile design in an enhanced tile assembly model. Nat. Comput. 11:323–38 [Google Scholar]
  72. Pandya MJ, Spooner GM, Sunde M, Thorpe JR, Rodger A, Woolfson DN. 72.  2000. Sticky-end assembly of a designed peptide fiber provides insight into protein fibrillogenesis. Biochemistry 39:8728–34 [Google Scholar]
  73. Parlea L, Bindewald E, Sharan R, Bartlett N, Moriarty D. 73.  et al. 2016. Ring Catalog: A resource for designing self-assembling RNA nanostructures. Methods 103:128–37 [Google Scholar]
  74. Patterson DP, Schwarz B, El-Boubbou K, van der Oost J, Prevelige PE, Douglas T. 74.  2012. Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid. Soft Matter 8:10158–66 [Google Scholar]
  75. Pavone V, Zhang S-Q, Merlino A, Lombardi A, Wu Y, DeGrado WF. 75.  2014. Crystal structure of an amphiphilic foldamer reveals a 48-mer assembly comprising a hollow truncated octahedron. Nat. Commun. 5:3581 [Google Scholar]
  76. Ringler P, Schulz GE. 76.  2003. Self-assembly of proteins into designed networks. Science 302:106–9 [Google Scholar]
  77. Robertson EJ, Battigelli A, Proulx C, Mannige RV, Haxton TK. 77.  et al. 2016. Design, synthesis, assembly, and engineering of peptoid nanosheets. Acc. Chem. Res. 49:379–89 [Google Scholar]
  78. Rothemund PW. 78.  2006. Folding DNA to create nanoscale shapes and patterns. Nature 440:297–302 [Google Scholar]
  79. Ryadnov MG, Woolfson DN. 79.  2003. Introducing branches into a self-assembling peptide fiber. Angew. Chem. Int. Ed. 42:3021–23 [Google Scholar]
  80. Salgado EN, Ambroggio XI, Brodin JD, Lewis RA, Kuhlman B, Tezcan FA. 80.  2010. Metal templated design of protein interfaces. PNAS 107:1827–32 [Google Scholar]
  81. Sayre TC, Lee TM, King NP, Yeates TO. 81.  2011. Protein stabilization in a highly knotted protein polymer. Protein Eng. Des. Sel. 24:627–30 [Google Scholar]
  82. Schuster B, Sleytr UB. 82.  2013. Nanotechnology with S-layer proteins. Methods Mol. Biol. 996:153–75 [Google Scholar]
  83. Sciore A, Su M, Koldewey P, Eschweiler JD, Diffley KA. 83.  et al. 2016. Flexible, symmetry-directed approach to assembling protein cages. PNAS 113:8681–86 [Google Scholar]
  84. Seeman NC. 84.  1982. Nucleic acid junctions and lattices. J. Theor. Biol. 99:237–47 [Google Scholar]
  85. Seeman NC. 85.  2010. Nanomaterials based on DNA. Annu. Rev. Biochem. 79:65–87 [Google Scholar]
  86. Senechal M. 86.  1988. Color symmetry. Comput. Math. Appl. 16:545–53 [Google Scholar]
  87. Severcan I, Geary C, Chworos A, Voss N, Jacovetty E, Jaeger L. 87.  2010. A polyhedron made of tRNAs. Nat. Chem. 2:772–79 [Google Scholar]
  88. Shih WM, Quispe JD, Joyce GF. 88.  2004. A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 427:618–21 [Google Scholar]
  89. Sinclair JC, Davies KM, Vénien-Bryan C, Noble MEM. 89.  2011. Generation of protein lattices by fusing proteins with matching rotational symmetry. Nat. Nanotechnol. 6:558–62 [Google Scholar]
  90. Sleytr UB, Schuster B, Egelseer E-M, Pum D. 90.  2014. S-layers: principles and applications. FEMS Microbiol. Rev. 38:823–64 [Google Scholar]
  91. Sliepen K, Ozorowski G, Burger JA, van Montfort T, Stunnenberg M. 91.  et al. 2015. Presenting native-like HIV-1 envelope trimers on ferritin nanoparticles improves their immunogenicity. Retrovirology 12:82 [Google Scholar]
  92. Sontz PA, Bailey JB, Ahn S, Tezcan FA. 92.  2015. A metal organic framework with spherical protein nodes: rational chemical design of 3D protein crystals. J. Am. Chem. Soc. 137:11598–601 [Google Scholar]
  93. Suzuki Y, Cardone G, Restrepo D, Zavattieri PD, Baker TS, Tezcan FA. 93.  2016. Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals. Nature 533:369–73 [Google Scholar]
  94. Thomas F, Burgess NC, Thomson AR, Woolfson DN. 94.  2016. Controlling the assembly of coiled-coil peptide nanotubes. Angew. Chem. Int. Ed. 55:987–91 [Google Scholar]
  95. Thomson AR, Wood CW, Burton AJ, Bartlett GJ, Sessions RB. 95.  et al. 2014. Computational design of water-soluble alpha-helical barrels. Science 346:485–88 [Google Scholar]
  96. Uchida M, Klem MT, Allen M, Suci P, Flenniken M. 96.  et al. 2007. Biological containers: protein cagesas multifunctional nanoplatforms. Adv. Mater. 19:1025–42 [Google Scholar]
  97. Wang H, Du SM, Seeman NC. 97.  1993. Tight single-stranded DNA knots. J. Biomol. Struct. Dyn. 10:853–63 [Google Scholar]
  98. Winfree E, Liu F, Wenzler LA, Seeman NC. 98.  1998. Design and self-assembly of two-dimensional DNA crystals. Nature 394:539–44 [Google Scholar]
  99. Wörsdörfer B, Woycechowsky KJ, Hilvert D. 99.  2011. Directed evolution of a protein container. Science 331:589–92 [Google Scholar]
  100. Yan H, Park SH, Finkelstein G, Reif JH, LaBean TH. 100.  2003. DNA-templated self-assembly of protein arrays and highly conductive nanowires. Science 301:1882–84 [Google Scholar]
  101. Yeates TO, Liu Y, Laniado J. 101.  2016. The design of symmetric protein nanomaterials comes of age in theory and practice. Curr. Opin. Struct. Biol. 39:134–43 [Google Scholar]
  102. Zhang F, Nangreave J, Liu Y, Yan H. 102.  2014. Structural DNA nanotechnology: state of the art and future perspective. J. Am. Chem. Soc. 136:11198–211 [Google Scholar]
  103. Zhang HV, Polzer F, Haider MJ, Tian Y, Villegas JA. 103.  et al. 2016. Computationally designed peptides for self-assembly of nanostructured lattices. Sci. Adv. 2:e1600307 [Google Scholar]
  104. Zheng J, Birktoft JJ, Chen Y, Wang T, Sha R. 104.  et al. 2009. From molecular to macroscopic via the rational design of a self-assembled 3D DNA crystal. Nature 461:74–77 [Google Scholar]
/content/journals/10.1146/annurev-biophys-070816-033928
Loading
/content/journals/10.1146/annurev-biophys-070816-033928
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error