Advertisement

Designed Protein Origami

  • Igor Drobnak
  • Ajasja Ljubetič
  • Helena Gradišar
  • Tomaž Pisanski
  • Roman JeralaEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 940)

Abstract

Proteins are highly perfected natural molecular machines, owing their properties to the complex tertiary structures with precise spatial positioning of different functional groups that have been honed through millennia of evolutionary selection. The prospects of designing new molecular machines and structural scaffolds beyond the limits of natural proteins make design of new protein folds a very attractive prospect. However, de novo design of new protein folds based on optimization of multiple cooperative interactions is very demanding. As a new alternative approach to design new protein folds unseen in nature, folds can be designed as a mathematical graph, by the self-assembly of interacting polypeptide modules within the single chain. Orthogonal coiled-coil dimers seem like an ideal building module due to their shape, adjustable length, and above all their designability. Similar to the approach of DNA nanotechnology, where complex tertiary structures are designed from complementary nucleotide segments, a polypeptide chain composed of a precisely specified sequence of coiled-coil forming segments can be designed to self-assemble into polyhedral scaffolds. This modular approach encompasses long-range interactions that define complex tertiary structures. We envision that by expansion of the toolkit of building blocks and design strategies of the folding pathways protein origami technology will be able to construct diverse molecular machines.

Keywords

Protein origami Protein design Coiled-coil Building blocks Protein assemblies Modular topological folds Oligomerization domains 

References

  1. 1.
    Turoverov KK, Kuznetsova IM, Uversky VN (2010) The protein kingdom extended: ordered and intrinsically disordered proteins, their folding, supramolecular complex formation, and aggregation. Prog Biophys Mol Biol 102:73–84. doi: 10.1016/j.pbiomolbio.2010.01.003 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Fersht AR (2008) From the first protein structures to our current knowledge of protein folding: delights and scepticisms. Nat Rev Mol Cell Biol 9:650–654. doi: 10.1038/nrm2446 CrossRefPubMedGoogle Scholar
  3. 3.
    Dill KA, MacCallum JL (2012) The protein-folding problem, 50 years on. Science (80-) 338:1042–1046. doi: 10.1126/science.1219021
  4. 4.
    Dill KA, Ozkan SB, Shell MS, Weikl TR (2008) The protein folding problem. Annu Rev Biophys 37:289–316. doi: 10.1146/annurev.biophys.37.092707.153558 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Chandler D (2005) Interfaces and the driving force of hydrophobic assembly. Nature 437:640–647. doi: 10.1038/nature04162 CrossRefPubMedGoogle Scholar
  6. 6.
    Berne BJ, Weeks JD, Zhou R (2009) Dewetting and hydrophobic interaction in physical and biological systems. Annu Rev Phys Chem 60:85–103. doi: 10.1146/annurev.physchem.58.032806.104445 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Pauling L, Corey RB, Branson HR (1951) The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci U S A 37:205–211CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ramakrishnan C, Ramachandran GN (1965) Stereochemical criteria for polypeptide and protein chain conformations. Biophys J 5:909–933. doi: 10.1016/S0006-3495(65)86759-5 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kumar S, Nussinov R (2002) Close-range electrostatic interactions in proteins. ChemBioChem 3:604–617.doi: 10.1002/1439-7633(20020703)3:7<604::AID-CBIC604>3.0.CO;2-X CrossRefPubMedGoogle Scholar
  10. 10.
    Makhatadze GI, Privalov PL (1995) Energetics of protein structure. Adv Protein Chem 47:307–425CrossRefPubMedGoogle Scholar
  11. 11.
    Murphy KP (2001) Stabilization of protein structure. Methods Mol Biol 168:1–16. doi: 10.1385/1-59259-193-0:001 PubMedGoogle Scholar
  12. 12.
    Baldwin RL (2007) Energetics of protein folding. J Mol Biol 371:283–301. doi:http://dx.doi.org/10.1016/j.jmb.2007.05.078
  13. 13.
    Guo W, Shea J-E, Berry RS (2006) The physics of the interactions governing folding and association of proteins. Ann NY Acad Sci 1066:34–53. doi: 10.1196/annals.1363.025 CrossRefGoogle Scholar
  14. 14.
    Berman HM, Westbrook J, Feng Z et al (2000) The protein data bank. Nucleic Acids Res 28:235–242. doi: 10.1093/nar/28.1.235 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sindelar CV, Hendsch ZS, Tidor B (1998) Effects of salt bridges on protein structure and design. Protein Sci 7:1898–1914. doi: 10.1002/pro.5560070906 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Sinha N, Smith-Gill SJ (2002) Electrostatics in protein binding and function. Curr Protein Pept Sci 3:601–614CrossRefPubMedGoogle Scholar
  17. 17.
    Plaxco KW, Simons KT, Baker D (1998) Contact order, transition state placement and the refolding rates of single domain proteins. J Mol Biol 277:985–994. doi:http://dx.doi.org/ 10.1006/jmbi.1998.1645
  18. 18.
    Ivankov DN, Garbuzynskiy SO, Alm E et al (2003) Contact order revisited: influence of protein size on the folding rate. Protein Sci 12:2057–2062. doi: 10.1110/ps.0302503 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Robertson AD, Murphy KP (1997) Protein structure and the energetics of protein stability. Chem Rev 97:1251–1267CrossRefPubMedGoogle Scholar
  20. 20.
    Ghosh K, Dill KA (2009) Computing protein stabilities from their chain lengths. Proc Natl Acad Sci U S A 106:10649–10654. doi: 10.1073/pnas.0903995106 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Božič S, Doles T, Gradišar H, Jerala R (2013) New designed protein assemblies. Curr Opin Chem Biol 17:940–945. doi: 10.1016/j.cbpa.2013.10.014 CrossRefPubMedGoogle Scholar
  22. 22.
    King NP, Lai Y-T (2013) Practical approaches to designing novel protein assemblies. Curr Opin Struct Biol 23:632–638. doi: 10.1016/j.sbi.2013.06.002 CrossRefPubMedGoogle Scholar
  23. 23.
    Salgado EN, Ambroggio XI, Brodin JD et al (2010) Metal templated design of protein interfaces. Proc Natl Acad Sci 107:1827–1832. doi: 10.1073/pnas.0906852107 CrossRefPubMedGoogle Scholar
  24. 24.
    Huard DJE, Kane KM, Tezcan FA (2013) Re-engineering protein interfaces yields copper-inducible ferritin cage assembly. Nat Chem Biol 9:169–176. doi: 10.1038/nchembio.1163 CrossRefPubMedGoogle Scholar
  25. 25.
    Brodin JD, Ambroggio XI, Tang C et al (2012) Metal-directed, chemically tunable assembly of one-, two- and three-dimensional crystalline protein arrays. Nat Chem 4:375–382. doi: 10.1038/nchem.1290 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Anzini P, Xu C, Hughes S et al (2013) Controlling self-assembly of a peptide-based material via metal-Ion induced registry shift. J Am Chem Soc 135:10278–10281. doi: 10.1021/ja404677c CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Fletcher JM, Harniman RL, Barnes FRH, et al (2013) Self-assembling cages from coiled-coil peptide modules. Science (80-) 340:595–599. doi: 10.1126/science.1233936
  28. 28.
    Padilla JE, Colovos C, Yeates TO (2001) Nanohedra: using symmetry to design self assembling protein cages, layers, crystals, and filaments. Proc Natl Acad Sci 98:2217–2221. doi: 10.1073/pnas.041614998 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Lai Y-T, Tsai K-L, Sawaya MR et al (2013) Structure and flexibility of nanoscale protein cages designed by symmetric self-assembly. J Am Chem Soc 135:7738–7743. doi: 10.1021/ja402277f CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Sinclair JC, Davies KM, Vénien-Bryan C, Noble MEM (2011) Generation of protein lattices by fusing proteins with matching rotational symmetry. Nat Nanotechnol 6:558–562. doi: 10.1038/nnano.2011.122 CrossRefPubMedGoogle Scholar
  31. 31.
    King NP, Sheffler W, Sawaya MR et al (2012) Computational design of self-assembling protein nanomaterials with atomic level accuracy. Science (80-) 336:1171–1174. doi: 10.1126/science.1219364
  32. 32.
    Leaver-Fay A, Tyka M, Lewis SM et al (2011) Rosetta3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol 487:545–574. doi: 10.1016/B978-0-12-381270-4.00019-6 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    King NP, Bale JB, Sheffler W et al (2014) Accurate design of co-assembling multi-component protein nanomaterials. Nature 510:103–108. doi: 10.1038/nature13404 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Hsia Y, Bale JB, Gonen S et al (2016) Design of a hyperstable 60-subunit protein icosahedron. Nature 535:136–139. doi: 10.1038/nature18010 CrossRefPubMedGoogle Scholar
  35. 35.
    Lanci CJ, MacDermaid CM, Kang S et al (2012) Computational design of a protein crystal. Proc Natl Acad Sci 109:7304–7309. doi: 10.1073/pnas.1112595109 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Barrick D, Ferreiro DU, Komives EA (2008) Folding landscapes of ankyrin repeat proteins: experiments meet theory. Curr Opin Struct Biol 18:27–34. doi: 10.1016/j.sbi.2007.12.004 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Cortajarena AL, Mochrie SGJ, Regan L (2011) Modulating repeat protein stability: the effect of individual helix stability on the collective behavior of the ensemble. Prot Sci 20:1042–1047. doi: 10.1002/pro.638 CrossRefGoogle Scholar
  38. 38.
    Parmeggiani F, Huang P-S, Vorobiev S et al (2015) A general computational approach for repeat protein design. J Mol Biol 427:563–575. doi: 10.1016/j.jmb.2014.11.005 CrossRefPubMedGoogle Scholar
  39. 39.
    De la Paz ML, Goldie K, Zurdo J et al (2002) De novo designed peptide-based amyloid fibrils. Proc Natl Acad Sci U S A 99:16052–16057. doi: 10.1073/pnas.252340199 CrossRefGoogle Scholar
  40. 40.
    Haines LA, Rajagopal K, Ozbas B et al (2005) Light-activated hydrogel formation via the triggered folding and self-assembly of a designed peptide. J Am Chem Soc 127:17025–17029. doi: 10.1021/ja054719o CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Yanlian Y, Ulung K, Xiumei W et al (2009) Designer self-assembling peptide nanomaterials. Nano Today 4:193–210. doi: 10.1016/j.nantod.2009.02.009 CrossRefGoogle Scholar
  42. 42.
    Saaem I, LaBean TH (2013) Overview of DNA origami for molecular self-assembly. WIREs Nanomed Nanobiotechnol 5:150–162. doi: 10.1002/wnan.1204 CrossRefGoogle Scholar
  43. 43.
    Walshaw J, Woolfson DN (2001) SOCKET: a program for identifying and analysing coiled-coil motifs within protein structures. J Mol Biol 307:1427–1450. doi: 10.1006/jmbi.2001.4545 CrossRefPubMedGoogle Scholar
  44. 44.
    Crick FHC (1953) The packing of α-helices: simple coiled-coils. Acta Crystallogr 6:689–697. doi: 10.1107/S0365110X53001964 CrossRefGoogle Scholar
  45. 45.
    Pauling L, Corey RB (1953) Compound helical configurations of polypeptide chains: structure of proteins of the α-keratin type. Nature 171:59–61. doi: 10.1038/171059a0 CrossRefPubMedGoogle Scholar
  46. 46.
    Lupas A (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21:375–382. doi: 10.1016/S0968-0004(96)10052-9 CrossRefPubMedGoogle Scholar
  47. 47.
    Burkhard P, Stetefeld J, Strelkov SV (2001) Coiled coils: a highly versatile protein folding motif. Trends Cell Biol 11:82–88. doi: 10.1016/S0962-8924(00)01898-5 CrossRefPubMedGoogle Scholar
  48. 48.
    Lupas AN, Gruber M (2005) The structure of α-helical coiled coils. In: Parry DAD, John MS (eds). Academic Press, San Diego, CA, pp 37–38Google Scholar
  49. 49.
    Gruber M, Lupas AN (2003) Historical review: another 50th anniversary – new periodicities in coiled coils. Trends Biochem Sci 28:679–685. doi: 10.1016/j.tibs.2003.10.008 CrossRefPubMedGoogle Scholar
  50. 50.
    Rose A, Schraegle SJ, Stahlberg EA, Meier I (2005) Coiled-coil protein composition of 22 proteomes – differences and common themes in subcellular infrastructure and traffic control. BMC Evol Biol 5:66. doi: 10.1186/1471-2148-5-66 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Rose A, Meier I (2004) Scaffolds, levers, rods and springs: diverse cellular functions of long coiled-coil proteins. Cell Mol Life Sci C 61:1996–2009. doi: 10.1007/s00018-004-4039-6 Google Scholar
  52. 52.
    Esteban MR, Giovinazzo G, de la Hera A, Goday C (1998) PUMA1: a novel protein that associates with the centrosomes, spindle and centromeres in the nematode parascaris. J Cell Sci 111:723–735PubMedGoogle Scholar
  53. 53.
    O’Shea EK, Klemm JD, Kim PS, Alber T (1991) X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science (80-) 254:539–544Google Scholar
  54. 54.
    Steinmetz MO, Jelesarov I, Matousek WM et al (2007) Molecular basis of coiled-coil formation. Proc Natl Acad Sci 104:7062–7067. doi: 10.1073/pnas.0700321104 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Grigoryan G, Reinke AW, Keating AE (2009) Design of protein-interaction specificity gives selective bZIP-binding peptides. Nature 458:859–864. doi: 10.1038/nature07885 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Grigoryan G, Keating AE (2008) Structural specificity in coiled-coil interactions. Curr Opin Struct Biol 18:477–483. doi: 10.1016/j.sbi.2008.04.008 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:347–353. doi: 10.1038/26412 CrossRefPubMedGoogle Scholar
  58. 58.
    Bullough PA, Hughson FM, Skehel JJ, Wiley DC (1994) Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371:37–43. doi: 10.1038/371037a0
  59. 59.
    Dutta K, Alexandrov A, Huang H, Pascal SM (2001) pH-induced folding of an apoptotic coiled coil. Protein Sci 10:2531–2540CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Liang W, Warrick HM, Spudich JA (1999) A structural model for phosphorylation control of dictyostelium myosin II thick filament assembly. J Cell Biol 147:1039–1048. doi: 10.1083/jcb.147.5.1039 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Farah CS, Reinach FC (1999) Regulatory properties of recombinant tropomyosins containing 5-hydroxytryptophan: Ca2 + -binding to troponin results in a conformational change in a region of tropomyosin outside the troponin binding site. Biochemistry 38:10543–10551. doi: 10.1021/bi982813u CrossRefPubMedGoogle Scholar
  62. 62.
    Woolfson DN (2005) The design of coiled-coil structures and assemblies. In: Parry DAD, John MS (eds). Academic Press, San Diego, CA, pp 79–112Google Scholar
  63. 63.
    Hodges RS, Saund AK, Chong PC et al (1981) Synthetic model for two-stranded alpha-helical coiled-coils. Design, synthesis, and characterization of an 86-residue analog of tropomyosin. J Biol Chem 256:1214–1224PubMedGoogle Scholar
  64. 64.
    O’Shea EK, Lumb KJ, Kim PS (1993) Peptide “Velcro”: design of a heterodimeric coiled coil. Curr Biol 3:658–667. doi: 10.1016/0960-9822(93)90063-T CrossRefPubMedGoogle Scholar
  65. 65.
    Oakley MG, Kim PS (1998) A buried polar interaction can direct the relative orientation of helices in a coiled coil. Biochemistry 37:12603–12610. doi: 10.1021/bi981269m CrossRefPubMedGoogle Scholar
  66. 66.
    Harbury PB, Zhang T, Kim PS, Alber T (1993) A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262:1401–1407CrossRefPubMedGoogle Scholar
  67. 67.
    Nautiyal S, Woolfson DN, King DS, Alber T (1995) A designed heterotrimeric coiled coil. Biochemistry 34:11645–11651. doi: 10.1021/bi00037a001 CrossRefPubMedGoogle Scholar
  68. 68.
    Fairman R, Chao HG, Lavoie TB et al (1996) Design of heterotetrameric coiled coils: evidence for increased stabilization by Glu(−)-Lys(+) ion pair interactions. Biochemistry 35:2824–2829. doi: 10.1021/bi952784c CrossRefPubMedGoogle Scholar
  69. 69.
    Liu J, Zheng Q, Deng Y et al (2006) A seven-helix coiled coil. Proc Natl Acad Sci U S A 103:15457–15462. doi: 10.1073/pnas.0604871103 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Testa OD, Moutevelis E, Woolfson DN (2009) CC+: a relational database of coiled-coil structures. Nucleic Acids Res 37:D315–D322. doi: 10.1093/nar/gkn675 CrossRefPubMedGoogle Scholar
  71. 71.
    Moutevelis E, Woolfson DN (2009) A periodic table of coiled-coil protein structures. J Mol Biol 385:726–732. doi: 10.1016/j.jmb.2008.11.028 CrossRefPubMedGoogle Scholar
  72. 71.
    Naik RR, Kirkpatrick SM, Stone MO (2001) The thermostability of an alpha-helical coiled-coil protein and its potential use in sensor applications. Biosens Bioelectron 16:1051–1057. doi: 10.1016/j.ijfoodmicro.2010.12.030 CrossRefPubMedGoogle Scholar
  73. 72.
    Sharma VA, Logan J, King DS et al (1998) Sequence-based design of a peptide probe for the APC tumor suppressor protein. Curr Biol 8:823–830. doi: 10.1016/S0960-9822(98)70324-0 CrossRefPubMedGoogle Scholar
  74. 73.
    Reinke AW, Grant RA, Keating AE (2010) A synthetic coiled-coil interactome provides heterospecific modules for molecular engineering. J Am Chem Soc 132:6025–6031. doi: 10.1021/ja907617a CrossRefPubMedPubMedCentralGoogle Scholar
  75. 74.
    Havranek JJ, Harbury PB (2003) Automated design of specificity in molecular recognition. Nat Struct Mol Biol 10:45–52. doi: 10.1038/nsb877 CrossRefGoogle Scholar
  76. 75.
    Bromley EHC, Sessions RB, Thomson AR, Woolfson DN (2008) Designed α-helical tectons for constructing multicomponent synthetic biological systems. J Am Chem Soc 131:928–930. doi: 10.1021/ja804231a CrossRefGoogle Scholar
  77. 76.
    Gradišar H, Jerala R (2011) De novo design of orthogonal peptide pairs forming parallel coiled-coil heterodimers. J Pept Sci 17:100–106. doi: 10.1002/psc.1331 CrossRefPubMedGoogle Scholar
  78. 77.
    Negron C, Keating AE (2014) A set of computationally designed orthogonal antiparallel homodimers that expands the synthetic coiled-coil toolkit. J Am Chem Soc 136:16544–16556. doi: 10.1021/ja507847t CrossRefPubMedPubMedCentralGoogle Scholar
  79. 78.
    Armstrong CT, Vincent TL, Green PJ, Woolfson DN (2011) SCORER 2.0: an algorithm for distinguishing parallel dimeric and trimeric coiled-coil sequences. Bioinformatics 27:1908–1914. doi: 10.1093/bioinformatics/btr299 CrossRefPubMedGoogle Scholar
  80. 79.
    Mahrenholz CC, Abfalter IG, Bodenhofer U et al (2011) Complex networks govern coiled-coil oligomerization – predicting and profiling by means of a machine learning approach. Mol Cell Proteomics 10:M110.004994. doi: 10.1074/mcp.M110.004994 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 80.
    Li C, Wang X-F, Chen Z et al (2015) Computational characterization of parallel dimeric and trimeric coiled-coils using effective amino acid indices. Mol Biosyst 11:354–360. doi: 10.1039/C4MB00569D CrossRefPubMedGoogle Scholar
  82. 81.
    Trigg J, Gutwin K, Keating AE, Berger B (2011) Multicoil2: predicting coiled coils and their oligomerization states from sequence in the twilight zone. PLoS One 6:e23519. doi: 10.1371/journal.pone.0023519 CrossRefPubMedPubMedCentralGoogle Scholar
  83. 82.
    Vincent TL, Green PJ, Woolfson DN (2013) LOGICOIL—multi-state prediction of coiled-coil oligomeric state. Bioinformatics 29:69–76. doi: 10.1093/bioinformatics/bts648 CrossRefPubMedGoogle Scholar
  84. 83.
    Hagemann UB, Mason JM, Müller KM, Arndt KM (2008) Selectional and mutational scope of peptides sequestering the Jun–Fos coiled-coil domain. J Mol Biol 381:73–88. doi: 10.1016/j.jmb.2008.04.030 CrossRefPubMedGoogle Scholar
  85. 85.
    Sowdhamini R, Alva V, Syamala Devi D (2008) COILCHECK: an interactive server for the analysis of interface regions in coiled coils. Protein Pept Lett 15:33–38. doi: 10.2174/092986608783330314 CrossRefPubMedGoogle Scholar
  86. 86.
    Wood CW, Bruning M, Ibarra AÁ et al (2014) CCBuilder: an interactive web-based tool for building, designing and assessing coiled-coil protein assemblies. Bioinformatics 30:3029–3035. doi: 10.1093/bioinformatics/btu502 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Strelkov SV, Burkhard P (2002) Analysis of α-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J Struct Biol 137:54–64. doi: 10.1006/jsbi.2002.4454 CrossRefPubMedGoogle Scholar
  88. 88.
    Grigoryan G, DeGrado WF (2011) Probing designability via a generalized model of helical bundle geometry. J Mol Biol 405:1079–1100. doi: 10.1016/j.jmb.2010.08.058 CrossRefPubMedGoogle Scholar
  89. 89.
    Gurnon DG, Whitaker JA, Oakley MG (2003) Design and characterization of a homodimeric antiparallel coiled coil. J Am Chem Soc 125:7518–7519. doi: 10.1021/ja0357590 CrossRefPubMedGoogle Scholar
  90. 90.
    Taylor CM, Keating AE (2005) Orientation and oligomerization specificity of the Bcr coiled-coil oligomerization domain†. Biochemistry 44:16246–16256. doi: 10.1021/bi051493t CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Gradišar H, Božič S, Doles T et al (2013) Design of a single-chain polypeptide tetrahedron assembled from coiled-coil segments. Nat Chem Biol 9:362–366. doi: 10.1038/nchembio.1248 CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Fijavž G, Pisanski T, Rus J (2015) Strong traces model of self-assembly polypeptide structures. MATCH Commun Math Comput Chem 71:199–212Google Scholar
  93. 93.
    Kočar V, Schreck JS, Čeru S, Gradišar H, Bašić N, Pisanski T, Doye JP, Jerala R (2016) Design principles for rapid folding of knotted DNA nanostructures. Nat Commun 7:10803. doi: 10.1038/ncomms10803 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Rothemund PWK (2006) Folding DNA to create nanoscale shapes and patterns. Nature 440:297–302. doi: 10.1038/nature04586 CrossRefPubMedGoogle Scholar
  95. 95.
    Ke Y, Ong LL, Shih WM, Yin P (2012) Three-dimensional structures self-assembled from DNA bricks. Science 338:1177–1183. doi: 10.1126/science.1227268 CrossRefPubMedGoogle Scholar
  96. 96.
    Zhang DY, Winfree E (2009) Control of DNA strand displacement kinetics using toehold exchange. J Am Chem Soc 131:17303–17314. doi: 10.1021/ja906987s CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Igor Drobnak
    • 1
  • Ajasja Ljubetič
    • 1
  • Helena Gradišar
    • 2
    • 1
  • Tomaž Pisanski
    • 3
    • 4
  • Roman Jerala
    • 2
    • 1
    Email author
  1. 1.Laboratory of BiotechnologyNational Institute of ChemistryLjubljanaSlovenia
  2. 2.EN-FIST Centre of ExcellenceLjubljanaSlovenia
  3. 3.Faculty of Mathematics and PhysicsUniversity of LjubljanaLjubljanaSlovenia
  4. 4.University of PrimorskaKoperSlovenia

Personalised recommendations