A switch from parallel to antiparallel strand orientation in a coiled-coil X-ray structure via two core hydrophobic mutations

Malashkevich, Vladimir N.; Higgins, Chelsea D.; Almo, Steven C.; Lai, Jonathan R.

doi:10.1002/bip.22631

A switch from parallel to antiparallel strand orientation in a coiled-coil X-ray structure via two core hydrophobic mutations

Journal Article · Wed May 06 00:00:00 EDT 2015 · Biopolymers

DOI:https://doi.org/10.1002/bip.22631· OSTI ID:1188828

Malashkevich, Vladimir N. ^[1]; Higgins, Chelsea D. ^[1]; Almo, Steven C. ^[1]; Lai, Jonathan R. ^[1]

Albert Einstein College of Medicine, Bronx NY (United States). Dept. of Biochemistry

The coiled-coil is one of the most ubiquitous and well studied protein structural motifs. Significant effort has been devoted to dissecting subtle variations of the typical heptad repeat sequence pattern that can designate larger topological features such as relative α-helical orientation and oligomer size. Here in this paper we report the X-ray structure of a model coiled-coil peptide, HA2-Del-L2seM, which forms an unanticipated core antiparallel dimer with potential sites for discrete higher-order multimerization (trimer or tetramer). In the X-ray structure, a third, partially-ordered α-helix is weakly associated with the antiparallel dimer and analytical ultracentrifugation experiments indicate the peptide forms a well-defined tetramer in solution. The HA2-Del-L2seM sequence is closely related to a parent model peptide, HA2-Del, which we previously reported adopts a parallel trimer; HA2-Del-L2seM differs by only hydrophobic leucine to selenomethione mutations and thus this subtle difference is sufficient to switch both relative α-helical topology and number of α-helices participating in the coiled-coil. Comparison of the X-ray structures of HA2-Del-L2seM (reported here) with the HA2-Del parent (reported previously) reveals novel interactions involving the selenomethionine residues that promote antiparallel coiled-coil configuration and preclude parallel trimer formation. Finally, these novel atomic insights are instructive for understanding subtle features that can affect coiled-coil topology and provide additional information for design of antiparallel coiled-coils.

View Accepted Manuscript (DOE)

Research Organization:: Advanced Photon Source (APS), Argonne National Laboratory (ANL), Argonne, IL (US)

Sponsoring Organization:: US National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1188828

Journal Information:: Biopolymers, Journal Name: Biopolymers Journal Issue: 3 Vol. 104; ISSN 0006-3525

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (36)

Designed protein mimics of the Ebola virus glycoprotein GP2 α-helical bundle: Stability and pH effects Harrison, Joseph S.; Higgins, Chelsea D.; Chandran, Kartik Protein Science, Vol. 20, Issue 9 https://doi.org/10.1002/pro.688	journal	August 2011
Computational analysis of residue contributions to coiled-coil topology: Computational Analysis of Residue Contributions Ramos, Jorge; Lazaridis, Themis Protein Science, Vol. 20, Issue 11 https://doi.org/10.1002/pro.718	journal	September 2011
Predicting helix orientation for coiled-coil dimers Apgar, James R.; Gutwin, Karl N.; Keating, Amy E. Proteins: Structure, Function, and Bioinformatics, Vol. 72, Issue 3 https://doi.org/10.1002/prot.22118	journal	May 2008
Influence of a heptad repeat stutter on the pH-dependent conformational behavior of the central coiled-coil from influenza hemagglutinin HA2: The Heptad Repeat Stutter in Influenza HA2 Higgins, Chelsea D.; Malashkevich, Vladimir N.; Almo, Steven C. Proteins: Structure, Function, and Bioinformatics, Vol. 82, Issue 9 https://doi.org/10.1002/prot.24585	journal	May 2014
A spring-loaded mechanism for the conformational change of influenza hemagglutinin Carr, Chavela M.; Kim, Peter S. Cell, Vol. 73, Issue 4 https://doi.org/10.1016/0092-8674(93)90260-W	journal	May 1993
Peptide ‘Velcro’: Design of a heterodimeric coiled coil O'Shea, Erin K.; Lumb, Kevin J.; Kim, Peter S. Current Biology, Vol. 3, Issue 10, p. 658-667 https://doi.org/10.1016/0960-9822(93)90063-T	journal	October 1993
The Design of Coiled-Coil Structures and Assemblies Woolfson, Derek N. Fibrous Proteins: Coiled-Coils, Collagen and Elastomers, p. 79-112 https://doi.org/10.1016/S0065-3233(05)70004-8	book	January 2005
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques Philo, John S. Analytical Biochemistry, Vol. 354, Issue 2 https://doi.org/10.1016/j.ab.2006.04.053	journal	July 2006
Structural Characterization of the Glycoprotein GP2 Core Domain from the CAS Virus, a Novel Arenavirus-Like Species Koellhoffer, Jayne F.; Dai, Zhou; Malashkevich, Vladimir N. Journal of Molecular Biology, Vol. 426, Issue 7 https://doi.org/10.1016/j.jmb.2013.12.009	journal	April 2014
Designability landscape reveals sequence features that define axial helix rotation in four-helical homo-oligomeric antiparallel coiled-coil structures Szczepaniak, Krzysztof; Lach, Grzegorz; Bujnicki, Janusz M. Journal of Structural Biology, Vol. 188, Issue 2 https://doi.org/10.1016/j.jsb.2014.09.007	journal	November 2014
Structural specificity in coiled-coil interactions Grigoryan, G.; Keating, A. Current Opinion in Structural Biology, Vol. 18, Issue 4 https://doi.org/10.1016/j.sbi.2008.04.008	journal	August 2008
Role of Electrostatic Repulsion in Controlling pH-Dependent Conformational Changes of Viral Fusion Proteins Harrison, Joseph S.; Higgins, Chelsea D.; O’Meara, Matthew J. Structure, Vol. 21, Issue 7 https://doi.org/10.1016/j.str.2013.05.009	journal	July 2013
On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces Gellman, Samuel H. Biochemistry, Vol. 30, Issue 27 https://doi.org/10.1021/bi00241a001	journal	July 1991
Marburg Virus Glycoprotein GP2: pH-Dependent Stability of the Ectodomain α-Helical Bundle Harrison, Joseph S.; Koellhoffer, Jayne F.; Chandran, Kartik Biochemistry, Vol. 51, Issue 12 https://doi.org/10.1021/bi3000353	journal	March 2012
Crystal Structure of the Marburg Virus GP2 Core Domain in Its Postfusion Conformation Koellhoffer, Jayne F.; Malashkevich, Vladimir N.; Harrison, Joseph S. Biochemistry, Vol. 51, Issue 39 https://doi.org/10.1021/bi300976m	journal	September 2012
Design and Characterization of a Heterodimeric Coiled Coil that Forms Exclusively with an Antiparallel Relative Helix Orientation McClain, Diana L.; Woods, Howard L.; Oakley, Martha G. Journal of the American Chemical Society, Vol. 123, Issue 13 https://doi.org/10.1021/ja004099l	journal	April 2001
Design and Characterization of a Homodimeric Antiparallel Coiled Coil Gurnon, Daniel G.; Whitaker, Jennifer A.; Oakley, Martha G. Journal of the American Chemical Society, Vol. 125, Issue 25 https://doi.org/10.1021/ja0357590	journal	June 2003
Strand Orientation by Steric Matching: A Designed Antiparallel Coiled-Coil Trimer Schnarr, Nathan A.; Kennan, Alan J. Journal of the American Chemical Society, Vol. 126, Issue 44 https://doi.org/10.1021/ja047496v	journal	November 2004
Hydrophobic Core Repacking in a Coiled-Coil Dimer via Phage Display: Insights into Plasticity and Specificity at a Protein−Protein Interface Lai, Jonathan R.; Fisk, John D.; Weisblum, Bernard Journal of the American Chemical Society, Vol. 126, Issue 34 https://doi.org/10.1021/ja047710f	journal	September 2004
The d ′-- d -- d ′ Vertical Triad Is Less Discriminating Than the a ′-- a -- a ′ Vertical Triad in the Antiparallel Coiled-Coil Dimer Motif Steinkruger, Jay D.; Bartlett, Gail J.; Hadley, Erik B. Journal of the American Chemical Society, Vol. 134, Issue 5 https://doi.org/10.1021/ja208855x	journal	January 2012
Strong Contributions from Vertical Triads to Helix-Partner Preferences in Parallel Coiled Coils Steinkruger, Jay D.; Bartlett, Gail J.; Woolfson, Derek N. Journal of the American Chemical Society, Vol. 134, Issue 38 https://doi.org/10.1021/ja3063088	journal	September 2012
Structure of influenza haemagglutinin at the pH of membrane fusion Bullough, Per A.; Hughson, Frederick M.; Skehel, John J. Nature, Vol. 371, Issue 6492 https://doi.org/10.1038/371037a0	journal	September 1994
Reptile relationships turn turtle⃛ Lee, Michael S. Y. Nature, Vol. 389, Issue 6648 https://doi.org/10.1038/38422	journal	September 1997
Preferred side-chain constellations at antiparallel coiled-coil interfaces Hadley, E. B.; Testa, O. D.; Woolfson, D. N. Proceedings of the National Academy of Sciences, Vol. 105, Issue 2 https://doi.org/10.1073/pnas.0709068105	journal	January 2008
MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Davis, I. W.; Leaver-Fay, A.; Chen, V. B. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm216	journal	May 2007
The packing of α-helices: simple coiled-coils Crick, F. H. C. Acta Crystallographica, Vol. 6, Issue 8 https://doi.org/10.1107/S0365110X53001964	journal	September 1953
On the treatment of negative intensity observations French, S.; Wilson, K. Acta Crystallographica Section A, Vol. 34, Issue 4 https://doi.org/10.1107/S0567739478001114	journal	July 1978
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Refinement of Macromolecular Structures by the Maximum-Likelihood Method Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3 https://doi.org/10.1107/S0907444996012255	journal	May 1997
Protein Design of an HIV-1 Entry Inhibitor Root, M. J. Science, Vol. 291, Issue 5505 https://doi.org/10.1126/science.1057453	journal	January 2001
Self-Assembling Cages from Coiled-Coil Peptide Modules Fletcher, J. M.; Harniman, R. L.; Barnes, F. R. H. Science, Vol. 340, Issue 6132 https://doi.org/10.1126/science.1233936	journal	April 2013
Characterization of a helical protein designed from first principles Regan, L.; DeGrado, W. F. Science, Vol. 241, Issue 4868, p. 976-978 https://doi.org/10.1126/science.3043666	journal	August 1988
A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants Harbury, P.; Zhang, T; Kim, P. Science, Vol. 262, Issue 5138, p. 1401-1407 https://doi.org/10.1126/science.8248779	journal	November 1993

Cited By (1)

Potent anti-influenza H7 human monoclonal antibody induces separation of hemagglutinin receptor-binding head domains Turner, Hannah L.; Pallesen, Jesper; Lang, Shanshan PLOS Biology, Vol. 17, Issue 2 https://doi.org/10.1371/journal.pbio.3000139	journal	February 2019

Similar Records

Antiparallel Four-Stranded Coiled Coil Specified by a 3-3-1 Hyrdrophobic Heptad Repeat

Journal Article · Sat Dec 31 23:00:00 EST 2005 · Structure · OSTI ID:914012

Self-Assembly of Coiled-coil Tetramers in the 1.40 A Structure of a Leucine-zipper Mutant

Journal Article · Sun Dec 31 23:00:00 EST 2006 · Protein Science · OSTI ID:929879

Conformational Specificity of the Lac Repressor Coiled-Coil Tetramerization Domain

Journal Article · Mon Dec 31 23:00:00 EST 2007 · Biochemistry · OSTI ID:959806

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Coiled-coil
protein folding
protein structure

A switch from parallel to antiparallel strand orientation in a coiled-coil X-ray structure via two core hydrophobic mutations

Citation Formats

References (36)

Cited By (1)

Similar Records

Related Subjects