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Antiparallel four-stranded coiled coil specified by a 3-3-1 hydrophobic heptad repeat.

Deng Y, Liu J, Zheng Q, Eliezer D, Kallenbach NR, Lu M
Structure 14 247-55 (2006)
Cited: 39 times
EuropePMC logo PMID: 16472744

Abstract

Coiled-coil sequences in proteins commonly share a seven-amino acid repeat with nonpolar side chains at the first (a) and fourth (d) positions. We investigate here the role of a 3-3-1 hydrophobic repeat containing nonpolar amino acids at the a, d, and g positions in determining the structures of coiled coils using mutants of the GCN4 leucine zipper dimerization domain. When three charged residues at the g positions in the parental sequence are replaced by nonpolar alanine or valine side chains, stable four-helix structures result. The X-ray crystal structures of the tetramers reveal antiparallel, four-stranded coiled coils in which the a, d, and g side chains interlock in a combination of knobs-into-knobs and knobs-into-holes packing. Interfacial interactions in a coiled coil can therefore be prescribed by hydrophobic-polar patterns beyond the canonical 3-4 heptad repeat. The results suggest that the conserved, charged residues at the g positions in the GCN4 leucine zipper can impart a negative design element to disfavor thermodynamically more stable, antiparallel tetramers.

Reviews - 2b22 mentioned but not cited (1)

  1. The Structure and Topology of α-Helical Coiled Coils. Lupas AN, Bassler J, Dunin-Horkawicz S. Subcell Biochem 82 95-129 (2017)

Articles - 2b22 mentioned but not cited (6)

  1. 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)
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  6. Computational Design of Single-Peptide Nanocages with Nanoparticle Templating. Villegas JA, Sinha NJ, Teramoto N, Von Bargen CD, Pochan DJ, Saven JG. Molecules 27 1237 (2022)


Reviews citing this publication (4)

  1. Fifty years of coiled-coils and alpha-helical bundles: a close relationship between sequence and structure. Parry DA, Fraser RD, Squire JM, Squire JM. J Struct Biol 163 258-269 (2008)
  2. Recent advances in self-assembled peptides: Implications for targeted drug delivery and vaccine engineering. Eskandari S, Guerin T, Toth I, Stephenson RJ. Adv Drug Deliv Rev 110-111 169-187 (2017)
  3. Coiled Coils - A Model System for the 21st Century. Lupas AN, Bassler J. Trends Biochem Sci 42 130-140 (2017)
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Articles citing this publication (28)

  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. 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)
  3. The cytoplasmic coiled-coil mediates cooperative gating temperature sensitivity in the voltage-gated H(+) channel Hv1. Fujiwara Y, Kurokawa T, Takeshita K, Kobayashi M, Okochi Y, Nakagawa A, Okamura Y. Nat Commun 3 816 (2012)
  4. DISC1: Structure, Function, and Therapeutic Potential for Major Mental Illness. Soares DC, Carlyle BC, Bradshaw NJ, Porteous DJ. ACS Chem Neurosci 2 609-632 (2011)
  5. A polycystin-2 (TRPP2) dimerization domain essential for the function of heteromeric polycystin complexes. Giamarchi A, Feng S, Rodat-Despoix L, Xu Y, Bubenshchikova E, Newby LJ, Hao J, Gaudioso C, Crest M, Lupas AN, Honoré E, Williamson MP, Obara T, Ong AC, Delmas P. EMBO J 29 1176-1191 (2010)
  6. Structures and polymorphic interactions of two heptad-repeat regions of the SARS virus S2 protein. Deng Y, Liu J, Zheng Q, Yong W, Lu M. Structure 14 889-899 (2006)
  7. 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)
  8. Computationally designed peptides for self-assembly of nanostructured lattices. Zhang HV, Polzer F, Haider MJ, Tian Y, Villegas JA, Kiick KL, Pochan DJ, Saven JG. Sci Adv 2 e1600307 (2016)
  9. 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)
  10. Cohesin interaction with centromeric minichromosomes shows a multi-complex rod-shaped structure. Surcel A, Koshland D, Ma H, Simpson RT. PLoS One 3 e2453 (2008)
  11. An amino acid packing code for α-helical structure and protein design. Joo H, Chavan AG, Phan J, Day R, Tsai J. J Mol Biol 419 234-254 (2012)
  12. The many types of interhelical ionic interactions in coiled coils - an overview. Meier M, Stetefeld J, Burkhard P. J Struct Biol 170 192-201 (2010)
  13. 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)
  14. 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)
  15. Designability landscape reveals sequence features that define axial helix rotation in four-helical homo-oligomeric antiparallel coiled-coil structures. Szczepaniak K, Lach G, Bujnicki JM, Dunin-Horkawicz S. J Struct Biol 188 123-133 (2014)
  16. Evolutionary patterns in coiled-coils. Surkont J, Pereira-Leal JB. Genome Biol Evol 7 545-556 (2015)
  17. Convergently-evolved structural anomalies in the coiled coil domains of insect silk proteins. Sutherland TD, Trueman HE, Walker AA, Weisman S, Campbell PM, Dong Z, Huson MG, Woodhead AL, Church JS. J Struct Biol 186 402-411 (2014)
  18. Evidence of α-helical coiled coils and β-sheets in hornet silk. Kameda T, Nemoto T, Ogawa T, Tosaka M, Kurata H, Schaper AK. J Struct Biol 185 303-308 (2014)
  19. From peptides to proteins: coiled-coil tetramers to single-chain 4-helix bundles. Naudin EA, Albanese KI, Smith AJ, Mylemans B, Baker EG, Weiner OD, Andrews DM, Tigue N, Savery NJ, Woolfson DN. Chem Sci 13 11330-11340 (2022)
  20. Geometric principles in the assembly of α-helical bundles. Pratap JV, Luisi BF, Calladine CR. Philos Trans A Math Phys Eng Sci 371 20120369 (2013)
  21. Crystal structure of a self-assembling lipopeptide detergent at 1.20 A. Ho DN, Pomroy NC, Cuesta-Seijo JA, Privé GG. Proc Natl Acad Sci U S A 105 12861-12866 (2008)
  22. Specific sequence combinations at parallel and antiparallel helix-helix interfaces. Kurochkina N. J Theor Biol 255 188-198 (2008)
  23. A dimeric proteomimetic prevents SARS-CoV-2 infection by dimerizing the spike protein. Khatri B, Pramanick I, Malladi SK, Rajmani RS, Kumar S, Ghosh P, Sengupta N, Rahisuddin R, Kumar N, Kumaran S, Ringe RP, Varadarajan R, Dutta S, Chatterjee J. Nat Chem Biol 18 1046-1055 (2022)
  24. A possible degree of motional freedom in bacterial chemoreceptor cytoplasmic domains and its potential role in signal transduction. Hu W. Int J Biochem Mol Biol 2 99-110 (2011)
  25. Crystal structure of a super leucine zipper, an extended two-stranded super long coiled coil. Diao J. Protein Sci 19 319-326 (2010)
  26. Role of positions e and g in the fibrous assembly formation of an amphipathic α-helix-forming polypeptide. Takei T, Tsumoto K, Yoshino M, Kojima S, Yazaki K, Ueda T, Takei T, Arisaka F, Miura K. Biopolymers 102 260-272 (2014)
  27. 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)
  28. Lamin Filament Assembly Derived from the Atomic Structure of the Antiparallel Four-Helix Bundle. Ahn J, Jo I, Jeong S, Lee J, Ha NC. Mol Cells 46 309-318 (2023)


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