Structures of single-layer {beta}-sheet proteins evolved from {beta}-hairpin repeats
Abstract
Free-standing single-layer beta-sheets are extremely rare in naturally occurring proteins, even though beta-sheet motifs are ubiquitous. Here we report the crystal structures of three homologous, single-layer, anti-parallel beta-sheet proteins, comprised of three or four twisted beta-hairpin repeats. The structures reveal that, in addition to the hydrogen bond network characteristic of beta-sheets, additional hydrophobic interactions mediated by small clusters of residues adjacent to the turns likely play a significant role in the structural stability and compensate for the lack of a compact hydrophobic core. These structures enabled identification of a family of secreted proteins that are broadly distributed in bacteria from the human gut microbiome and are putatively involved in the metabolism of complex carbohydrates. A conserved surface patch, rich in solvent-exposed tyrosine residues, was identified on the concave surface of the beta-sheet. These new modular single-layer beta-sheet proteins may serve as a new model system for studying folding and design of beta-rich proteins.
- Authors:
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Institutes of Health (NIH)
- OSTI Identifier:
- 1574395
- DOE Contract Number:
- AC02-06CH11357
- Resource Type:
- Journal Article
- Journal Name:
- Protein Science
- Additional Journal Information:
- Journal Volume: 28; Journal Issue: 9
- Country of Publication:
- United States
- Language:
- English
- Subject:
- beta-hairpin repeats; human gut microbiome; protein folding; secreted proteins; single-layer beta-sheet proteins; structural genomics
Citation Formats
Xu, Qingping, Biancalana, Matthew, and Wilson, Ian. Structures of single-layer {beta}-sheet proteins evolved from {beta}-hairpin repeats. United States: N. p., 2019.
Web. doi:10.1002/pro.3683.
Xu, Qingping, Biancalana, Matthew, & Wilson, Ian. Structures of single-layer {beta}-sheet proteins evolved from {beta}-hairpin repeats. United States. doi:10.1002/pro.3683.
Xu, Qingping, Biancalana, Matthew, and Wilson, Ian. Sun .
"Structures of single-layer {beta}-sheet proteins evolved from {beta}-hairpin repeats". United States. doi:10.1002/pro.3683.
@article{osti_1574395,
title = {Structures of single-layer {beta}-sheet proteins evolved from {beta}-hairpin repeats},
author = {Xu, Qingping and Biancalana, Matthew and Wilson, Ian},
abstractNote = {Free-standing single-layer beta-sheets are extremely rare in naturally occurring proteins, even though beta-sheet motifs are ubiquitous. Here we report the crystal structures of three homologous, single-layer, anti-parallel beta-sheet proteins, comprised of three or four twisted beta-hairpin repeats. The structures reveal that, in addition to the hydrogen bond network characteristic of beta-sheets, additional hydrophobic interactions mediated by small clusters of residues adjacent to the turns likely play a significant role in the structural stability and compensate for the lack of a compact hydrophobic core. These structures enabled identification of a family of secreted proteins that are broadly distributed in bacteria from the human gut microbiome and are putatively involved in the metabolism of complex carbohydrates. A conserved surface patch, rich in solvent-exposed tyrosine residues, was identified on the concave surface of the beta-sheet. These new modular single-layer beta-sheet proteins may serve as a new model system for studying folding and design of beta-rich proteins.},
doi = {10.1002/pro.3683},
journal = {Protein Science},
number = 9,
volume = 28,
place = {United States},
year = {2019},
month = {9}
}
Works referenced in this record:
Converging concepts of protein folding in vitro and in vivo
journal, June 2009
- Hartl, F. Ulrich; Hayer-Hartl, Manajit
- Nature Structural & Molecular Biology, Vol. 16, Issue 6
The Protein-Folding Problem, 50 Years On
journal, November 2012
- Dill, K. A.; MacCallum, J. L.
- Science, Vol. 338, Issue 6110
RepeatsDB: a database of tandem repeat protein structures
journal, December 2013
- Di Domenico, Tomás; Potenza, Emilio; Walsh, Ian
- Nucleic Acids Research, Vol. 42, Issue D1
Protein Repeats: Structures, Functions, and Evolution
journal, May 2001
- Andrade, Miguel A.; Perez-Iratxeta, Carolina; Ponting, Chris P.
- Journal of Structural Biology, Vol. 134, Issue 2-3
A recurring theme in protein engineering: the design, stability and folding of repeat proteins
journal, August 2005
- Main, E.; Lowe, A.; Mochrie, S.
- Current Opinion in Structural Biology, Vol. 15, Issue 4
Repeat-protein folding: New insights into origins of cooperativity, stability, and topology
journal, January 2008
- Kloss, Ellen; Courtemanche, Naomi; Barrick, Doug
- Archives of Biochemistry and Biophysics, Vol. 469, Issue 1
Classification of β-hairpin repeat proteins
journal, February 2018
- Roche, Daniel B.; Viet, Phuong Do; Bakulina, Anastasia
- Journal of Structural Biology, Vol. 201, Issue 2
Tryptophan zippers: Stable, monomeric -hairpins
journal, May 2001
- Cochran, A. G.; Skelton, N. J.; Starovasnik, M. A.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 10
10 Residue Folded Peptide Designed by Segment Statistics
journal, August 2004
- Honda, Shinya; Yamasaki, Kazuhiko; Sawada, Yoshito
- Structure, Vol. 12, Issue 8
β-hairpin-forming peptides; models of early stages of protein folding
journal, September 2010
- Lewandowska, Agnieszka; Ołdziej, Stanisław; Liwo, Adam
- Biophysical Chemistry, Vol. 151, Issue 1-2
A stable single-layer β-sheet without a hydrophoe
journal, February 1998
- Pham, Thúy-Nga; Koide, Akiko; Koide, Shohei
- Nature Structural Biology, Vol. 5, Issue 2
Crystal structure of Lyme disease antigen outer surface protein A complexed with an Fab
journal, April 1997
- Li, H.; Dunn, J. J.; Luft, B. J.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 8, p. 3584-3589
Crystal structures of the CPAP/STIL complex reveal its role in centriole assembly and human microcephaly
journal, September 2013
- Cottee, Matthew A.; Muschalik, Nadine; Wong, Yao Liang
- eLife, Vol. 2
Structural Analysis of the G-Box Domain of the Microcephaly Protein CPAP Suggests a Role in Centriole Architecture
journal, November 2013
- Hatzopoulos, Georgios N.; Erat, Michèle C.; Cutts, Erin
- Structure, Vol. 21, Issue 11
The BC component of ABC toxins is an RHS-repeat-containing protein encapsulation device
journal, August 2013
- Busby, Jason N.; Panjikar, Santosh; Landsberg, Michael J.
- Nature, Vol. 501, Issue 7468
The centriolar protein CPAP G-box: an amyloid fibril in a single domain
journal, October 2015
- Cutts, Erin E.; Inglis, Alison; Stansfeld, Phillip J.
- Biochemical Society Transactions, Vol. 43, Issue 5
Topographical and Temporal Diversity of the Human Skin Microbiome
journal, May 2009
- Grice, E. A.; Kong, H. H.; Conlan, S.
- Science, Vol. 324, Issue 5931
Expansion of the Protein Repertoire in Newly Explored Environments: Human Gut Microbiome Specific Protein Families
journal, June 2010
- Ellrott, Kyle; Jaroszewski, Lukasz; Li, Weizhong
- PLoS Computational Biology, Vol. 6, Issue 6
Structural genomics of the Thermotoga maritima proteome implemented in a high-throughput structure determination pipeline
journal, August 2002
- Lesley, S. A.; Kuhn, P.; Godzik, A.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 18
Identification, classification, and analysis of beta-bulges in proteins
journal, October 1993
- Chan, A. W. Edith; Hutchinson, E. Gail; Harris, Daniel
- Protein Science, Vol. 2, Issue 10
Searching protein structure databases with DaliLite v.3
journal, September 2008
- Holm, L.; Kaariainen, S.; Rosenstrom, P.
- Bioinformatics, Vol. 24, Issue 23
The crystal structure of mouse VDAC1 at 2.3 A resolution reveals mechanistic insights into metabolite gating
journal, November 2008
- Ujwal, R.; Cascio, D.; Colletier, J. -P.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 46
Atomic-resolution crystal structure of Borrelia burgdorferi outer surface protein A via surface engineering
journal, August 2006
- Makabe, Koki; Tereshko, Valentina; Gawlak, Grzegorz
- Protein Science, Vol. 15, Issue 8
Role of Tryptophan−Tryptophan Interactions in Trpzip β-Hairpin Formation, Structure, and Stability
journal, November 2009
- Wu, Ling; McElheny, Dan; Huang, Rong
- Biochemistry, Vol. 48, Issue 43
A mechanism of covalent substrate binding in the x-ray structure of subunit K of the Escherichia coli dihydroxyacetone kinase
journal, June 2003
- Siebold, Christian; García-Alles, Luis Fernando; Erni, Bernhard
- Proceedings of the National Academy of Sciences, Vol. 100, Issue 14, p. 8188-8192
Hydrophobic Surface Burial Is the Major Stability Determinant of a Flat, Single-layer β-Sheet
journal, April 2007
- Yan, Shude; Gawlak, Grzegorz; Makabe, Koki
- Journal of Molecular Biology, Vol. 368, Issue 1
Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules
journal, February 1998
- Fraczkiewicz, Robert; Braun, Werner
- Journal of Computational Chemistry, Vol. 19, Issue 3
Tryptophan residues: Scarce in proteins but strong stabilizers of β-hairpin peptides
journal, January 2010
- Santiveri, Clara M.; Jiménez, M. Angeles
- Biopolymers, Vol. 94, Issue 6
Bacteroides cellulosilyticus sp. nov., a cellulolytic bacterium from the human gut microbial community
journal, July 2007
- Robert, C.; Chassard, C.; Lawson, P. A.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 7
Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont
journal, March 2005
- Sonnenburg, J. L.
- Science, Vol. 307, Issue 5717
Functional Genomic and Metabolic Studies of the Adaptations of a Prominent Adult Human Gut Symbiont, Bacteroides thetaiotaomicron , to the Suckling Period
journal, September 2006
- Bjursell, Magnus K.; Martens, Eric C.; Gordon, Jeffrey I.
- Journal of Biological Chemistry, Vol. 281, Issue 47
A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates
journal, October 1992
- Reizer, Jonathan; Reizer, Aiala; Saier, Milton H.
- Protein Science, Vol. 1, Issue 10
Carbohydrate-binding modules: fine-tuning polysaccharide recognition
journal, September 2004
- Boraston, Alisdair B.; Bolam, David N.; Gilbert, Harry J.
- Biochemical Journal, Vol. 382, Issue 3
Recent structural studies of carbohydrate-binding modules
journal, November 2006
- Hashimoto, H.
- Cellular and Molecular Life Sciences, Vol. 63, Issue 24
Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007
- Krissinel, Evgeny; Henrick, Kim
- Journal of Molecular Biology, Vol. 372, Issue 3
Natural -sheet proteins use negative design to avoid edge-to-edge aggregation
journal, March 2002
- Richardson, J. S.; Richardson, D. C.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 5
Model systems for β-hairpins and β-sheets
journal, August 2006
- Hughes, Robert M.; Waters, Marcey L.
- Current Opinion in Structural Biology, Vol. 16, Issue 4
Combining the polymerase incomplete primer extension method for cloning and mutagenesis with microscreening to accelerate structural genomics efforts
journal, January 2008
- Klock, Heath E.; Koesema, Eric J.; Knuth, Mark W.
- Proteins: Structure, Function, and Bioinformatics, Vol. 71, Issue 2
Improved Prediction of Signal Peptides: SignalP 3.0
journal, July 2004
- Dyrløv Bendtsen, Jannick; Nielsen, Henrik; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 340, Issue 4, p. 783-795
Atomic Structures of the Human Immunophilin FKBP-12 Complexes with FK506 and Rapamycin
journal, January 1993
- Van Duyne, Gregory D.; Standaert, Robert F.; Karplus, P. Andrew
- Journal of Molecular Biology, Vol. 229, Issue 1
An approach to rapid protein crystallization using nanodroplets
journal, March 2002
- Santarsiero, B. D.; Yegian, D. T.; Lee, C. C.
- Journal of Applied Crystallography, Vol. 35, Issue 2
An automated system to mount cryo-cooled protein crystals on a synchrotron beamline, using compact sample cassettes and a small-scale robot
journal, November 2002
- Cohen, Aina E.; Ellis, Paul J.; Miller, Mitchell D.
- Journal of Applied Crystallography, Vol. 35, Issue 6
A short history of SHELX
journal, December 2007
- Sheldrick, George M.
- Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122
The Buccaneer software for automated model building. 1. Tracing protein chains
journal, August 2006
- Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9
Coot model-building tools for molecular graphics
journal, November 2004
- Emsley, Paul; Cowtan, Kevin
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
REFMAC 5 for the refinement of macromolecular crystal structures
journal, March 2011
- Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit
journal, February 2013
- Pronk, Sander; Páll, Szilárd; Schulz, Roland
- Bioinformatics, Vol. 29, Issue 7
ProDy: Protein Dynamics Inferred from Theory and Experiments
journal, April 2011
- Bakan, A.; Meireles, L. M.; Bahar, I.
- Bioinformatics, Vol. 27, Issue 11, p. 1575-1577
PROMOTIF-A program to identify and analyze structural motifs in proteins
journal, February 1996
- Hutchinson, E. Gail; Thornton, Janet M.
- Protein Science, Vol. 5, Issue 2
Matt: Local Flexibility Aids Protein Multiple Structure Alignment
journal, January 2008
- Menke, Matthew; Berger, Bonnie; Cowen, Lenore
- PLoS Computational Biology, Vol. 4, Issue 1
TM-align: a protein structure alignment algorithm based on the TM-score
journal, April 2005
- Zhang, Y.
- Nucleic Acids Research, Vol. 33, Issue 7
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
TeXshade: shading and labeling of multiple sequence alignments using LaTeX2e
journal, February 2000
- Beitz, E.
- Bioinformatics, Vol. 16, Issue 2
Recognition of spatial motifs in protein structures 1 1Edited by J. Thornton
journal, January 1999
- Kleywegt, Gerard J.
- Journal of Molecular Biology, Vol. 285, Issue 4
PISCES: a protein sequence culling server
journal, August 2003
- Wang, G.; Dunbrack, R. L.
- Bioinformatics, Vol. 19, Issue 12