The Structure and Topology of α-Helical Coiled Coils

  • Andrei N. LupasEmail author
  • Jens Bassler
  • Stanislaw Dunin-Horkawicz
Part of the Subcellular Biochemistry book series (SCBI, volume 82)


α-Helical coiled coils constitute one of the most diverse folds yet described. They range in length over two orders of magnitude; they form rods, segmented ropes, barrels, funnels, sheets, spirals, and rings, which encompass anywhere from two to more than 20 helices in parallel or antiparallel orientation; they assume different helix crossing angles, degrees of supercoiling, and packing geometries. This structural diversity supports a wide range of biological functions, allowing them to form mechanically rigid structures, provide levers for molecular motors, project domains across large distances, mediate oligomerization, transduce conformational changes and facilitate the transport of other molecules. Unlike almost any other protein fold known to us, their structure can be computed from parametric equations, making them an ideal model system for rational protein design. Here we outline the principles by which coiled coils are structured, review the determinants of their folding and stability, and present an overview of their diverse architectures.


Leucine Zipper Coiled Coil Heptad Repeat Hydrophilic Residue Antiparallel Orientation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Akey DL, Malashkevich VN, Kim PS (2001) Buried polar residues in coiled-coil interfaces. Biochemistry 40:6352–6360PubMedCrossRefGoogle Scholar
  2. Alfadhli A, Steel E, Finlay L, Bächinger HP, Barklis E (2002) Hantavirus nucleocapsid protein coiled-coil domains. J Biol Chem 277:27103–27108PubMedCrossRefGoogle Scholar
  3. Araya E, Berthier C, Kim E, Yeung T, Wang X, Helfman DM (2002) Regulation of coiled-coil assembly in tropomyosins. J Struct Biol 137:176–183PubMedCrossRefGoogle Scholar
  4. Armstrong CT, Boyle AL, Bromley EH, Mahmoud ZN, Smith L, Thomson AR, Woolfson DN (2009) Rational design of peptide-based building blocks for nanoscience and synthetic biology. Faraday Discuss 143:305–317PubMedCrossRefGoogle Scholar
  5. Armstrong CT, Vincent TL, Green PJ, Woolfson DN (2011) SCORER 2.0: an algorithm for distinguishing parallel dimeric and trimeric coiled-coil sequences. Bioinformatics 27:1908–1914PubMedCrossRefGoogle Scholar
  6. Astbury, W. T. (1938). The fourth Spiers memorial lecture. X-ray adventures among the proteins. Transactions of the Faraday Society 34, 378–388.Google Scholar
  7. Astbury WT (1946) X-ray studies of nucleic acids. Sym Soc Exp Biol (1):66–76Google Scholar
  8. Bassler J, Alvarez BH, Hartmann MD, Lupas AN (2015) A domain dictionary of trimeric autotransporter adhesins. Int J Med Microbiol 305:265–275PubMedCrossRefGoogle Scholar
  9. Berger B, Wilson DB, Wolf E, Tonchev T, Milla M, Kim PS (1995) Predicting coiled coils by use of pairwise residue correlations. Proc Natl Acad Sci 92:8259–8263PubMedPubMedCentralCrossRefGoogle Scholar
  10. Boguski MS, Elshourbagy N, Taylor JM, Gordon JI (1985) Comparative analysis of repeated sequences in rat apolipoproteins AI, A-IV, and E. Proc Natl Acad Sci 82:992–996PubMedPubMedCentralCrossRefGoogle Scholar
  11. Braun V, Bosch V (1972) Repetitive sequences in the murein-lipoprotein of the cell wall of Escherichia coli. Proc Natl Acad Sci 69:970–974PubMedPubMedCentralCrossRefGoogle Scholar
  12. Burkhard P, Stetefeld J, Strelkov SV (2001) Coiled coils: a highly versatile protein folding motif. Trends Cell Biol 11:82–88PubMedCrossRefGoogle Scholar
  13. Burton AJ, Thomas F, Agnew C, Hudson KL, Halford SE, Brady RL, Woolfson DN (2013) Accessibility, reactivity, and selectivity of side chains within a channel of de novo peptide assembly. J Am Chem Soc 135:12524–12527PubMedCrossRefGoogle Scholar
  14. Chothia C, Levitt M, Richardson D (1977) Structure of proteins: packing of α-helices and pleated sheets. Proc Natl Acad Sci 74:4130–4134PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chothia C, Levitt M, Richardson D (1981) Helix to helix packing in proteins. J Mol Biol 145:215–250PubMedCrossRefGoogle Scholar
  16. Ciani B, Bjelic S, Honnappa S, Jawhari H, Jaussi R, Payapilly A, Jowitt T, Steinmetz MO, Kammerer RA (2010) Molecular basis of coiled-coil oligomerization-state specificity. Proc Natl Acad Sci 107:19850–19855PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cohen C (1998) Why fibrous proteins are romantic. J Struct Biol 122:3–16PubMedCrossRefGoogle Scholar
  18. Cohen C, Parry DAD (1986) α-helical coiled coils - a widespread motif in proteins. Trends Biochem Sci 11:245–248CrossRefGoogle Scholar
  19. Cohen C, Parry DAD (1990) α-helical coiled coils and bundles: how to design an α-helical protein. Proteins 7:1–15PubMedCrossRefGoogle Scholar
  20. Cohen C, Parry DAD (1994) Alpha-Helical Coiled Coils-More Facts and Better Predictions. Science 263:488–489PubMedCrossRefGoogle Scholar
  21. Crick FHC (1952) Is α-keratin a coiled coil? Nature 170:882–883PubMedCrossRefGoogle Scholar
  22. Crick FHC (1953a) The Fourier transform of a coiled-coil. Acta Crystallogr 6:685–689CrossRefGoogle Scholar
  23. Crick FHC (1953b) The packing of α-helices: simple coiled-coils. Acta Crystallogr 6:689–697CrossRefGoogle Scholar
  24. Delorenzi M, Speed T (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18:617–625PubMedCrossRefGoogle Scholar
  25. Deng Y, Liu J, Zheng Q, Eliezer D, Kallenbach NR, Lu M (2006) Antiparallel four-stranded coiled coil specified by a 3-3-1 hydrophobic heptad repeat. Structure 14:247–255PubMedCrossRefGoogle Scholar
  26. Deng Y, Liu J, Zheng Q, Li Q, Kallenbach NR, Lu M (2008) A Heterospecific Leucine Zipper Tetramer. Chem Biol 15:908–919PubMedCrossRefGoogle Scholar
  27. Dosztányi Z, Csizmok V, Tompa P, Simon I (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21:3433–3434PubMedCrossRefGoogle Scholar
  28. Dunin-Horkawicz S, Lupas AN (2010a) Measuring the conformational space of square four-helical bundles with the program samCC. J Struct Biol 170:226–235PubMedCrossRefGoogle Scholar
  29. Dunin-Horkawicz S, Lupas AN (2010b) Comprehensive analysis of HAMP domains: implications for transmembrane signal transduction. J Mol Biol 397:1156–1174PubMedCrossRefGoogle Scholar
  30. Egelman EH, Xu C, DiMaio F, Magnotti E, Modlin C, Yu X, Wright E, Baker D, Conticello VP (2015) Structural plasticity of helical nanotubes based on coiled-coil assemblies. Structure 23:280–289PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ferris HU, Dunin-Horkawicz S, Mondéjar LG, Hulko M, Hantke K, Martin J, Schultz JE, Zeth K, Lupas AN, Coles M (2011) The mechanisms of HAMP-mediated signaling in transmembrane receptors. Structure 19:378–385PubMedCrossRefGoogle Scholar
  32. Ferris HU, Dunin-Horkawicz S, Hornig N, Hulko M, Martin J, Schultz JE, Zeth K, Lupas AN, Coles M (2012) Mechanism of regulation of receptor histidine kinases. Structure 20:56–66PubMedCrossRefGoogle Scholar
  33. Ferris HU, Zeth K, Hulko M, Dunin-Horkawicz S, Lupas AN (2014) Axial helix rotation as a mechanism for signal regulation inferred from the crystallographic analysis of the E. coli serine chemoreceptor. J Struct Biol 186:349–356PubMedCrossRefGoogle Scholar
  34. Frank S, Lustig A, Schulthess T, Engel J, Kammerer RA (2000) A distinct seven-residue trigger sequence is indispensable for proper coiled-coil formation of the human macrophage scavenger receptor oligomerization domain. J Biol Chem 275:11672–11677PubMedCrossRefGoogle Scholar
  35. Gernert KM, Surles MC, Labean TH, Richardson JS, Richardson DC (1995) The Alacoil: a very tight, antiparallel coiled-coil of helices. Protein Sci 4:2252–2260PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gonzalez L Jr, Woolfson DN, Alber T (1996) Buried polar residues and structural specificity in the GCN4 leucine zipper. Nat Struct Mol Biol 3:1011–1018CrossRefGoogle Scholar
  37. Grigoryan G, DeGrado WF (2011) Probing designability via a generalized model of helical bundle geometry. J Mol Biol 405:1079–1100PubMedCrossRefGoogle Scholar
  38. Gruber M, Lupas AN (2003) Historical review: another 50th anniversary - new periodicities in coiled coils. Trends Biochem Sci 28:679–685PubMedCrossRefGoogle Scholar
  39. Gruber M, Söding J, Lupas AN (2006) Comparative analysis of coiled-coil prediction methods. J Struct Biol 155:140–145PubMedCrossRefGoogle Scholar
  40. 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 262:1401–1407PubMedCrossRefGoogle Scholar
  41. Harbury PB, Kim P, Alber T (1994) Crystal structure of an isoleucine-zipper trimer. Nature 371:80–83PubMedCrossRefGoogle Scholar
  42. Hartmann MD (2017) Functional and structural roles of coiled coils. Fibrous proteins: structures and mechanisms. Springer, DordrechtGoogle Scholar
  43. Hartmann MD, Ridderbusch O, Zeth K, Albrecht R, Testa O, Woolfson DN, Sauer G, Dunin-Horkawicz S, Lupas AN, Alvarez BH (2009) A coiled-coil motif that sequesters ions to the hydrophobic core. Proc Natl Acad Sci 106:16950–16955PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hartmann MD, Mendler CT, Bassler J, Karamichali I, Ridderbusch O, Lupas AN, Hernandez Alvarez B (2016) α/β coiled coils. eLife 5:e11861PubMedPubMedCentralGoogle Scholar
  45. Hicks MR, Walshaw J, Woolfson DN (2002) Investigating the tolerance of coiled-coil peptides to nonheptad sequence inserts. J Struct Biol 137:73–81PubMedCrossRefGoogle Scholar
  46. Holton J, Alber T (2004) Automated protein crystal structure determination using ELVES. Proc Natl Acad Sci 101:1537–1542PubMedPubMedCentralCrossRefGoogle Scholar
  47. Huang PS, Oberdorfer G, Xu C, Pei XY, Nannenga BL, Rogers JM, DiMaio F, Gonen T, Luisi B, Baker D (2014) High thermodynamic stability of parametrically designed helical bundles. Science 346:481–485PubMedPubMedCentralCrossRefGoogle Scholar
  48. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, Schultz A, Martin J, Schultz JE, Lupas AN, Coles M (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929–940PubMedCrossRefGoogle Scholar
  49. Joh NH, Wang T, Bhate MP, Acharya R, Wu Y, Grabe M, Hong M, Grigoryan G, DeGrado WF (2014) De novo design of a transmembrane Zn2+-transporting four-helix bundle. Science 346:1520–1524PubMedPubMedCentralCrossRefGoogle Scholar
  50. Judson HF (1979) The eighth day of creation. Simon & Schuster, New YorkGoogle Scholar
  51. Kammerer RA, Schulthess T, Landwehr R, Lustig A, Engel J, Aebi U, Steinmetz MO (1998) An autonomous folding unit mediates the assembly of two-stranded coiled coils. Proc Natl Acad Sci 95:13419–13424PubMedPubMedCentralCrossRefGoogle Scholar
  52. Keating AE, Malashkevich VN, Tidor B, Kim PS (2001) Side-chain repacking calculations for predicting structures and stabilities of heterodimeric coiled coils. Proc Natl Acad Sci 98:14825–14830PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kendrew JC, Bodo G, Dintzis HM, Parrish RG, Wyckoff H, Phillips DC (1958) A three-dimensional model of the myoglobin molecule obtained by x-ray analysis. Nature 181:662–666PubMedCrossRefGoogle Scholar
  54. Koretke KK, Szczesny P, Gruber M, Lupas AN (2006) Model structure of the prototypical non-fimbrial adhesin YadA of Yersinia enterocolitica. J Struct Biol 155:154–161PubMedCrossRefGoogle Scholar
  55. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914–919PubMedCrossRefGoogle Scholar
  56. Landschulz WH, Johnson PF, McKnight SL (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240:1759–1764PubMedCrossRefGoogle Scholar
  57. Lee DL, Lavigne P, Hodges RS (2001) Are trigger sequences essential in the folding of two-stranded α-helical coiled-coils? J Mol Biol 306:539–553PubMedCrossRefGoogle Scholar
  58. Liu J, Yong W, Deng Y, Kallenbach NR, Lu M (2004) Atomic structure of a tryptophan-zipper pentamer. Proc Natl Acad Sci 101:16156–16161PubMedPubMedCentralCrossRefGoogle Scholar
  59. Liu J, Zheng Q, Deng Y, Kallenbach NR, Lu M (2006a) Conformational transition between four and five-stranded phenylalanine zippers determined by a local packing interaction. J Mol Biol 361:168–179PubMedCrossRefGoogle Scholar
  60. Liu J, Deng Y, Zheng Q, Cheng CS, Kallenbach NR, Lu M (2006b) A parallel coiled-coil tetramer with offset helices. Biochemistry 45:15224–15231PubMedCrossRefGoogle Scholar
  61. Liu J, Zheng Q, Deng Y, Cheng CS, Kallenbach NR, Lu M (2006c) A seven-helix coiled coil. Proc Natl Acad Sci 103:15457–15462PubMedPubMedCentralCrossRefGoogle Scholar
  62. Liu J, Zheng Q, Deng Y, Qunnu L, Kallenbach NR, Lu M (2007) Conformational specificity of the lac repressor coiled-coil tetramerization domain. Biochemistry 46:14951–14959PubMedCrossRefGoogle Scholar
  63. Lupas A (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21:375–382PubMedCrossRefGoogle Scholar
  64. Lupas AN, Gruber M (2005) The structure of α-helical coiled coils. Adv Protein Chem 70:37–78PubMedCrossRefGoogle Scholar
  65. Lupas A, Van Dyke S, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164PubMedCrossRefGoogle Scholar
  66. Mahrenholz CC, Abfalter IG, Bodenhofer U, Volkmer R, Hochreiter S (2011) Complex networks govern coiled-coil oligomerization–predicting and profiling by means of a machine learning approach. Mol Cell Proteomics 10:M110–004994PubMedPubMedCentralCrossRefGoogle Scholar
  67. Malashkevich VN, Kammerer RA, Efimov VP, Schulthess T, Engel J (1996) The crystal structure of a five-stranded coiled coil in COMP: a prototype ion channel? Science 274:761–765PubMedCrossRefGoogle Scholar
  68. Mason JM, Arndt KM (2004) Coiled coil domains: stability, specificity, and biological implications. Chembiochem 5:170–176PubMedCrossRefGoogle Scholar
  69. McDonnell AV, Jiang T, Keating AE, Berger B (2006) Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics 22:356–358PubMedCrossRefGoogle Scholar
  70. McKay DB, Steitz T (1981) Structure of catabolite gene activator protein at 2.9 Å resolution suggests binding to left-handed B-DNA. Nature 290:744–749PubMedCrossRefGoogle Scholar
  71. McLachlan AD, Stewart M (1975) Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. J Mol Biol 98:293–304PubMedCrossRefGoogle Scholar
  72. McLachlan AD, Stewart M (1976) The 14-fold periodicity in α-tropomyosin and the interaction with actin. J Mol Biol 103:271–298PubMedCrossRefGoogle Scholar
  73. Mittl PRE, Deillon C, Sargent D, Liu N, Klauser S, Thomas RM, Gutte B, Grütter MG (2000) The retro-GCN4 leucine zipper sequence forms a stable three-dimensional structure. Proc Natl Acad Sci 97:2562–2566PubMedPubMedCentralCrossRefGoogle Scholar
  74. Mondéjar LG, Lupas A, Schultz A, Schultz JE (2012) HAMP domain-mediated signal transduction probed with a mycobacterial adenylyl cyclases as a reporter. J Biol Chem 287:1022–1031Google Scholar
  75. Nilges M, Brünger AT (1991) Automated modeling of coiled coils: application to the GCN4 dimerization region. Protein Eng 4:649–659PubMedCrossRefGoogle Scholar
  76. Offer G, Hicks MR, Woolfson DN (2002) Generalized Crick equations for modeling noncanonical coiled coils. J Struct Biol 137:41–53Google Scholar
  77. 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 254:539–544PubMedCrossRefGoogle Scholar
  78. Parry DAD (1975) Analysis of the primary sequence of α-tropomyosin from rabbit skeletal muscle. J Mol Biol 98:519–535PubMedCrossRefGoogle Scholar
  79. Parry DAD (1982) Coiled-coils in α-helix-containing proteins: analysis of the residue types within the heptad repeat and the use of these data in the prediction of coiled-coils in other proteins. Biosci Rep 2:1017–1024PubMedCrossRefGoogle Scholar
  80. Parry DAD, Crewther WG, Fraser RD, MacRae TP (1977) Structure of α-keratin: structural implication of the amino acid sequences of the type I and type II chain segments. J Mol Biol 113:449–454PubMedCrossRefGoogle Scholar
  81. Parry DAD, Fraser RB, Squire JM (2008) Fifty years of coiled-coils and α-helical bundles: A close relationship between sequence and structure. J Struct Biol 163:258–269PubMedCrossRefGoogle Scholar
  82. Pauling L, Corey RB (1950) Two hydrogen-bonded spiral configurations of the polypeptide chain. J Am Chem Soc 72:534CrossRefGoogle Scholar
  83. Pauling L, Corey RB (1953) Compound helical configurations of polypeptide chains: structure of proteins of the α-keratin type. Nature 171:59–61PubMedCrossRefGoogle Scholar
  84. Pauling L, Corey RB, Branson HR (1951) The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci 37:205–211PubMedPubMedCentralCrossRefGoogle Scholar
  85. Peters J, Nitsch M, Kuhlmorgen B, Golbik R, Lupas A, Kellermann J, Engelhardt H, Pfander JP, Müller S, Goldie K, Engel A, Stetter K-O, Baumeister W (1995) Tetrabrachion: a filamentous archaebacterial surface protein assembly of unusual structure and extreme stability. J Mol Biol 245:385–401PubMedCrossRefGoogle Scholar
  86. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman I, Sussman JL (2005) FoldIndex©: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21:3435–3438PubMedCrossRefGoogle Scholar
  87. Simpson AA, Tao Y, Leiman PG, Badasso MO, He Y, Jardine PJ, Olson NH, Morais MC, Grimes S, Anderson DL, Baker TS (2000) Structure of the bacteriophage ϕ29 DNA packaging motor. Nature 408(6813):745–750PubMedPubMedCentralCrossRefGoogle Scholar
  88. Solan A, Ratia K, Fairman R (2002) Exploring the role of alanine in the structure of the Lac repressor tetramerization domain, a ferritin-like Alacoil. J Mol Biol 317:601–612PubMedCrossRefGoogle Scholar
  89. Steinmetz MO, Stock A, Schulthess T, Landwehr R, Lustig A, Faix J, Gerisch G, Aebi U, Kammerer RA (1998) A distinct 14 residue site triggers coiled-coil formation in cortexillin I. EMBO J 17:1883–1891PubMedPubMedCentralCrossRefGoogle Scholar
  90. Stone D, Sodek J, Johnson P, Smillie LB (1975) Tropomyosin: correlation of amino acid sequence and structure. FEBS Proc 31:125–136Google Scholar
  91. 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 137:54–64PubMedCrossRefGoogle Scholar
  92. Symmons MF, Bokma E, Koronakis E, Hughes C, Koronakis V (2009) The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci 106:7173–7178PubMedPubMedCentralCrossRefGoogle Scholar
  93. Szczepaniak K, Lach G, Bujnicki JM, Dunin-Horkawicz S (2014) Designability landscape reveals sequence features that define axial helix rotation in four-helical homo-oligomeric antiparallel coiled-coil structures. J Struct Biol 188:123–133PubMedCrossRefGoogle Scholar
  94. Szczesny P, Lupas A (2008) Domain annotation of trimeric autotransporter adhesins—daTAA. Bioinformatics 24:1251–1256PubMedPubMedCentralCrossRefGoogle Scholar
  95. Testa OD, Moutevelis E, Woolfson DN (2009) CC+: a relational database of coiled-coil structures. Nucleic Acids Res 37:D315–D322PubMedCrossRefGoogle Scholar
  96. Thomson AR, Wood CW, Burton AJ, Bartlett GJ, Sessions RB, Brady RL, Woolfson DN (2014) Computational design of water-soluble α-helical barrels. Science 346:485–488PubMedCrossRefGoogle Scholar
  97. 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:e23519PubMedPubMedCentralCrossRefGoogle Scholar
  98. Trybus KM, Freyzon Y, Faust LZ, Sweeney HL (1997) Spare the rod, spoil the regulation: necessity for a myosin rod. Proc Natl Acad Sci 94:48–52PubMedPubMedCentralCrossRefGoogle Scholar
  99. Vincent TL, Green PJ, Woolfson DN (2013) LOGICOIL—multi-state prediction of coiled-coil oligomeric state. Bioinformatics 29:69–76PubMedCrossRefGoogle Scholar
  100. Walshaw J, Woolfson DN (2001) SOCKET: a program for identifying and analysing coiled-coil motifs within protein structures. J Mol Biol 307:1427–1450PubMedCrossRefGoogle Scholar
  101. Walshaw J, Woolfson DN (2003) Extended knobs-into-holes packing in classical and complex coiled-coil assemblies. J Struct Biol 144:349–361PubMedCrossRefGoogle Scholar
  102. Walshaw J, Shipway JM, Woolfson DN (2001) Guidelines for the assembly of novel coiled-coil structures: α-sheets and α-cylinders. Biochem Soc Symp 68:111–123CrossRefGoogle Scholar
  103. Whitby FG, Phillips GN (2000) Crystal structure of tropomyosin at 7 Ångstroms resolution. Proteins 38:49–59PubMedCrossRefGoogle Scholar
  104. Wilson IA, Skehel JJ, Wiley DC (1981) Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution. Nature 289:366–373PubMedCrossRefGoogle Scholar
  105. Wolf E, Kim PS, Berger B (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci 6:1179–1189PubMedPubMedCentralCrossRefGoogle Scholar
  106. Wood CW, Bruning M, Ibarra AÁ, Bartlett GJ, Thomson AR, Sessions RB, Brady RL, Woolfson DN (2014) CCBuilder: an interactive web-based tool for building, designing and assessing coiled-coil protein assemblies. Bioinformatics 30:3029–3035PubMedPubMedCentralCrossRefGoogle Scholar
  107. Woolfson DN (2005) The design of coiled-coil structures and assemblies. Adv Protein Chem 70:79–112PubMedCrossRefGoogle Scholar
  108. Woolfson DN (2017) Coiled-coil design: updated and upgraded. Fibrous proteins: structures and mechanisms. Springer, DordrechtGoogle Scholar
  109. Woolfson DN, Alber T (1995) Predicting oligomerization states of coiled coils. Protein Sci 4:1596–1607PubMedPubMedCentralCrossRefGoogle Scholar
  110. Woolfson DN, Bartlett GJ, Bruning M, Thomson AR (2012) New currency for old rope: from coiled-coil assemblies to α-helical barrels. Curr Opin Struct Biol 22:432–441PubMedCrossRefGoogle Scholar
  111. Wu KC, Bryan JT, Morasso MI, Jang S-I, Lee J-H, Yang J-M, Marekov LN, Parry DAD, Steinert PM (2000) Coiled-coil trigger motifs in the 1B and 2B rod domain segments are required for the stability of keratin intermediate filaments. Mol Biol Cell 11:3539–3558PubMedPubMedCentralCrossRefGoogle Scholar
  112. Yadav MK, Leman LJ, Price DJ, Brooks CL 3rd, Stout CD, Ghadiri MR (2006) Coiled coils at the edge of configurational heterogeneity. Structural analyses of parallel and antiparallel homotetrameric coiled coils reveal configurational sensitivity to a single solvent-exposed amino acid substitution. Biochemistry 45:4463–4473PubMedPubMedCentralCrossRefGoogle Scholar
  113. Yang Z, Kollman JM, Pandi L, Doolittle RF (2001) Crystal structure of native chicken fibrinogen at 2.7 Å resolution. Biochemistry 40:12515–12523PubMedCrossRefGoogle Scholar
  114. Zaytsev DV, Xie F, Mukherjee M, Bludin A, Demeler B, Breece RM, Tierney DL, Ogawa MY (2010) Nanometer to millimeter scale peptide-porphyrin materials. Biomacromolecules 11:2602–2609PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Andrei N. Lupas
    • 1
    Email author
  • Jens Bassler
    • 1
  • Stanislaw Dunin-Horkawicz
    • 2
  1. 1.Department of Protein EvolutionMax Planck Institute for Developmental BiologyTübingenGermany
  2. 2.Structural Bioinformatics Laboratory, Centre of New TechnologiesUniversity of WarsawWarsawPoland

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