2ccf Citations

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 4463-73 (2006)
Related entries: 1w5h, 1w5j, 1w5k, 1w5l, 2cce, 2ccn

Cited: 45 times
EuropePMC logo PMID: 16584182


A detailed understanding of the mechanisms by which particular amino acid sequences can give rise to more than one folded structure, such as for proteins that undergo large conformational changes or misfolding, is a long-standing objective of protein chemistry. Here, we describe the crystal structures of a single coiled-coil peptide in distinct parallel and antiparallel tetrameric configurations and further describe the parallel or antiparallel crystal structures of several related peptide sequences; the antiparallel tetrameric assemblies represent the first crystal structures of GCN4-derived peptides exhibiting such a configuration. Intriguingly, substitution of a single solvent-exposed residue enabled the parallel coiled-coil tetramer GCN4-pLI to populate the antiparallel configuration, suggesting that the two configurations are close enough in energy for subtle sequence changes to have important structural consequences. We present a structural analysis of the small changes to the helix register and side-chain conformations that accommodate the two configurations and have supplemented these results using solution studies and a molecular dynamics energetic analysis using a replica exchange methodology. Considering the previous examples of structural nonspecificity in coiled-coil peptides, the findings reported here not only emphasize the predisposition of the coiled-coil motif to adopt multiple configurations but also call attention to the associated risk that observed crytstal structures may not represent the only (or even the major) species present in solution.

Articles - 2ccf mentioned but not cited (3)

  1. 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. Yadav MK, Leman LJ, Price DJ, Brooks CL, Stout CD, Ghadiri MR. Biochemistry 45 4463-4473 (2006)
  2. Targeted proteolysis of plectin isoform 1a accounts for hemidesmosome dysfunction in mice mimicking the dominant skin blistering disease EBS-Ogna. Walko G, Vukasinovic N, Gross K, Fischer I, Sibitz S, Fuchs P, Reipert S, Jungwirth U, Berger W, Salzer U, Carugo O, Castañón MJ, Wiche G. PLoS Genet. 7 e1002396 (2011)
  3. An alpha/beta-peptide helix bundle with a pure beta3-amino acid core and a distinctive quaternary structure. Giuliano MW, Horne WS, Gellman SH. J. Am. Chem. Soc. 131 9860-9861 (2009)

Reviews citing this publication (3)

  1. Coiled Coils - A Model System for the 21st Century. Lupas AN, Bassler J. Trends Biochem. Sci. 42 130-140 (2017)
  2. Exploring biomolecular energy landscapes. Joseph JA, Röder K, Chakraborty D, Mantell RG, Wales DJ. Chem. Commun. (Camb.) 53 6974-6988 (2017)
  3. The Structure and Topology of α-Helical Coiled Coils. Lupas AN, Bassler J, Dunin-Horkawicz S. Subcell Biochem 82 95-129 (2017)

Articles citing this publication (39)

  1. The HAMP domain structure implies helix rotation in transmembrane signaling. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, Schultz A, Martin J, Schultz JE, Lupas AN, Coles M. Cell 126 929-940 (2006)
  2. A seven-helix coiled coil. Liu J, Zheng Q, Deng Y, Cheng CS, Kallenbach NR, Lu M. Proc. Natl. Acad. Sci. U.S.A. 103 15457-15462 (2006)
  3. Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Albanesi D, Martín M, Trajtenberg F, Mansilla MC, Haouz A, Alzari PM, de Mendoza D, Buschiazzo A. Proc. Natl. Acad. Sci. U.S.A. 106 16185-16190 (2009)
  4. X-ray crystal structure of a TRPM assembly domain reveals an antiparallel four-stranded coiled-coil. Fujiwara Y, Minor DL. J. Mol. Biol. 383 854-870 (2008)
  5. The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. Inforzato A, Baldock C, Jowitt TA, Holmes DF, Lindstedt R, Marcellini M, Rivieccio V, Briggs DC, Kadler KE, Verdoliva A, Bottazzi B, Mantovani A, Salvatori G, Day AJ. J. Biol. Chem. 285 17681-17692 (2010)
  6. A role of the transient receptor potential domain of vanilloid receptor I in channel gating. García-Sanz N, Valente P, Gomis A, Fernández-Carvajal A, Fernández-Ballester G, Viana F, Belmonte C, Ferrer-Montiel A. J. Neurosci. 27 11641-11650 (2007)
  7. Identifying important structural characteristics of arsenic resistance proteins by using designed three-stranded coiled coils. Touw DS, Nordman CE, Stuckey JA, Pecoraro VL. Proc. Natl. Acad. Sci. U.S.A. 104 11969-11974 (2007)
  8. Direct single-molecule observation of a protein living in two opposed native structures. Gambin Y, Schug A, Lemke EA, Lavinder JJ, Ferreon AC, Magliery TJ, Onuchic JN, Deniz AA. Proc. Natl. Acad. Sci. U.S.A. 106 10153-10158 (2009)
  9. Molecular modeling of the full-length human TRPV1 channel in closed and desensitized states. Fernández-Ballester G, Ferrer-Montiel A. J. Membr. Biol. 223 161-172 (2008)
  10. Role of the C-terminal domain in the structure and function of tetrameric sodium channels. Bagnéris C, Decaen PG, Hall BA, Naylor CE, Clapham DE, Kay CW, Wallace BA. Nat Commun 4 2465 (2013)
  11. Structural insights into the molecular mechanisms of cauliflower mosaic virus transmission by its insect vector. Hoh F, Uzest M, Drucker M, Plisson-Chastang C, Bron P, Blanc S, Dumas C. J. Virol. 84 4706-4713 (2010)
  12. The native GCN4 leucine-zipper domain does not uniquely specify a dimeric oligomerization state. Oshaben KM, Salari R, McCaslin DR, Chong LT, Horne WS. Biochemistry 51 9581-9591 (2012)
  13. Artificial Diiron Enzymes with a De Novo Designed Four-Helix Bundle Structure. Chino M, Maglio O, Nastri F, Pavone V, DeGrado WF, Lombardi A. Eur J Inorg Chem 2015 3371-3390 (2015)
  14. Measuring the conformational space of square four-helical bundles with the program samCC. Dunin-Horkawicz S, Lupas AN. J. Struct. Biol. 170 226-235 (2010)
  15. Crystal structure of a trimeric form of the K(V)7.1 (KCNQ1) A-domain tail coiled-coil reveals structural plasticity and context dependent changes in a putative coiled-coil trimerization motif. Xu Q, Minor DL. Protein Sci. 18 2100-2114 (2009)
  16. Conformational transition between four and five-stranded phenylalanine zippers determined by a local packing interaction. Liu J, Zheng Q, Deng Y, Kallenbach NR, Lu M. J. Mol. Biol. 361 168-179 (2006)
  17. Unique features of the anti-parallel, heterodimeric coiled-coil interaction between methyl-cytosine binding domain 2 (MBD2) homologues and GATA zinc finger domain containing 2A (GATAD2A/p66α). Walavalkar NM, Gordon N, Williams DC. J. Biol. Chem. 288 3419-3427 (2013)
  18. Increasing the affinity of selective bZIP-binding peptides through surface residue redesign. Kaplan JB, Reinke AW, Keating AE. Protein Sci. 23 940-953 (2014)
  19. Self-assembly of coiled-coil tetramers in the 1.40 A structure of a leucine-zipper mutant. Deng Y, Zheng Q, Liu J, Cheng CS, Kallenbach NR, Lu M. Protein Sci. 16 323-328 (2007)
  20. Functional and mechanistic analyses of biomimetic aminoacyl transfer reactions in de novo designed coiled coil peptides via rational active site engineering. Leman LJ, Weinberger DA, Huang ZZ, Wilcoxen KM, Ghadiri MR. J. Am. Chem. Soc. 129 2959-2966 (2007)
  21. Molecular dynamics guided study of salt bridge length dependence in both fluorinated and non-fluorinated parallel dimeric coiled-coils. Pendley SS, Yu YB, Cheatham TE. Proteins 74 612-629 (2009)
  22. Computational analysis of residue contributions to coiled-coil topology. Ramos J, Lazaridis T. Protein Sci. 20 1845-1855 (2011)
  23. Computational design and experimental discovery of an antiestrogenic peptide derived from alpha-fetoprotein. Kirschner KN, Lexa KW, Salisburg AM, Alser KA, Joseph L, Andersen TT, Bennett JA, Jacobson HI, Shields GC. J. Am. Chem. Soc. 129 6263-6268 (2007)
  24. Exploring alternate states and oligomerization preferences of coiled-coils by de novo structure modeling. Rämisch S, Lizatović R, André I. Proteins 83 235-247 (2015)
  25. The effects of pK(a) tuning on the thermodynamics and kinetics of folding: design of a solvent-shielded carboxylate pair at the a-position of a coiled-coil. Lau WL, Degrado WF, Roder H. Biophys. J. 99 2299-2308 (2010)
  26. Analysis of the bacterial luciferase mobile loop by replica-exchange molecular dynamics. Campbell ZT, Baldwin TO, Miyashita O. Biophys. J. 99 4012-4019 (2010)
  27. Competition between Coiled-Coil Structures and the Impact on Myosin-10 Bundle Selection. Vavra KC, Xia Y, Rock RS. Biophys. J. 110 2517-2527 (2016)
  28. Predicting the effect of ions on the conformation of the H-NS dimerization domain. Vreede J, Dame RT. Biophys. J. 103 89-98 (2012)
  29. A heterospecific leucine zipper tetramer. Deng Y, Liu J, Zheng Q, Li Q, Kallenbach NR, Lu M. Chem. Biol. 15 908-919 (2008)
  30. De Novo Design of Tetranuclear Transition Metal Clusters Stabilized by Hydrogen-Bonded Networks in Helical Bundles. Zhang SQ, Chino M, Liu L, Tang Y, Hu X, DeGrado WF, Lombardi A. J. Am. Chem. Soc. 140 1294-1304 (2018)
  31. A hamiltonian replica exchange method for building protein-protein interfaces applied to a leucine zipper. Cukier RI. J Chem Phys 134 045104 (2011)
  32. Coiled coils as possible models of protein structure evolution. Gáspári Z, Nyitray L. Biomol Concepts 2 199-210 (2011)
  33. Crystal structure of the central coiled-coil domain from human liprin-β2. Stafford RL, Tang MY, Sawaya MR, Phillips ML, Bowie JU. Biochemistry 50 3807-3815 (2011)
  34. Organic ligand binding by a hydrophobic cavity in a designed tetrameric coiled-coil protein. Mizuno T, Hasegawa C, Tanabe Y, Hamajima K, Muto T, Nishi Y, Oda M, Kobayashi Y, Tanaka T. Chemistry 15 1491-1498 (2009)
  35. Spectroscopic and metal binding properties of a de novo metalloprotein binding a tetrazinc cluster. Chino M, Zhang SQ, Pirro F, Leone L, Maglio O, Lombardi A, DeGrado WF. Biopolymers 109 e23339 (2018)
  36. Structural Basis of TPR-Mediated Oligomerization and Activation of Oncogenic Fusion Kinases. Pal K, Bandyopadhyay A, Zhou XE, Xu Q, Marciano DP, Brunzelle JS, Yerrum S, Griffin PR, Vande Woude G, Melcher K, Xu HE. Structure 25 867-877.e3 (2017)
  37. Effect of helix length on the stability of the Lac repressor antiparallel coiled coil. Little W, Robblee JP, Dahlberg CL, Kokona B, Fairman R. Biopolymers 104 395-404 (2015)
  38. New tetrameric forms of the rotavirus NSP4 with antiparallel helices. Kumar S, Ramappa R, Pamidimukkala K, Rao CD, Suguna K. Arch. Virol. 163 1531-1547 (2018)
  39. Self-assembly of the bZIP transcription factor ΔFosB. Yin Z, Venkannagari H, Lynch H, Aglyamova G, Bhandari M, Machius M, Nestler EJ, Robison AJ, Rudenko G. Curr Res Struct Biol 2 1-13 (2020)