Cooperative allostery and structural dynamics of streptavidin at cryogenic- and ambient-temperature

Ayan, Esra; Yuksel, Busra; Destan, Ebru; Ertem, Fatma Betul; Yildirim, Gunseli; Eren, Meryem; Yefanov, Oleksandr M.; Barty, Anton; Tolstikova, Alexandra; Ketawala, Gihan K.; Botha, Sabine; Dao, E. Han; Hayes, Brandon; Liang, Mengning; Seaberg, Matthew H.; Hunter, Mark S.; Batyuk, Alexander; Mariani, Valerio; Su, Zhen; Poitevin, Frederic; Yoon, Chun Hong; Kupitz, Christopher; Cohen, Aina; Doukov, Tzanko; Sierra, Raymond G.; Dağ, Çağdaş; DeMirci, Hasan

doi:10.1038/s42003-021-02903-7

Title: Cooperative allostery and structural dynamics of streptavidin at cryogenic- and ambient-temperature

Journal Article · 20 January 2022 · Communications Biology

DOI: https://doi.org/10.1038/s42003-021-02903-7 · OSTI ID:1831492

Ayan, Esra ^[1];

^[2]; Destan, Ebru ^[2]; Ertem, Fatma Betul ^[2]; Yildirim, Gunseli ^[2];

^[2]; Yefanov, Oleksandr M. ^[3]; Barty, Anton ^[3]; Tolstikova, Alexandra ^[3]; Ketawala, Gihan K. ^[4]; Botha, Sabine ^[4]; Dao, E. Han ^[5]; Hayes, Brandon ^[6]; Liang, Mengning ^[6];

^[6];

^[6]; Batyuk, Alexander ^[6]; Mariani, Valerio ^[6]; Su, Zhen ^[7]; Poitevin, Frederic ^[6] more »

Koc University, Istanbul (Turkey); Stanford PULSE Institute
Koc University, Istanbul (Turkey)
Deutsches Elektronen-Synchrotron (DESY), Hamburg (Germany)
Arizona State Univ., Tempe, AZ (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS) ; Stanford Univ., CA (United States)
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Koc University, Istanbul (Turkey) ; SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)

Multimeric protein assemblies are abundant in nature. Streptavidin is an attractive protein that provides a paradigm system to investigate the intra- and intermolecular interactions of multimeric protein complexes. Also, it offers a versatile tool for biotechnological applications. Here, we present two apo-streptavidin structures, the first one is an ambient temperature Serial Femtosecond X-ray crystal (Apo-SFX) structure at 1.7 Å resolution and the second one is a cryogenic crystal structure (Apo-Cryo) at 1.1 Å resolution. These structures are mostly in agreement with previous structural data. Combined with computational analysis, these structures provide invaluable information about structural dynamics of apo streptavidin. Collectively, these data further reveal a novel cooperative allostery of streptavidin which binds to substrate via water molecules that provide a polar interaction network and mimics the substrate biotin which displays one of the strongest affinities found in nature.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Lab., Menlo Park, CA (United States). Photon Ultrafast Laser Science and Engineering Inst. (PULSE)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1831492

Journal Information:: Communications Biology, Journal Name: Communications Biology Journal Issue: 1 Vol. 5; ISSN 2399-3642

Publisher:: Springer NatureCopyright Statement

Country of Publication:: United States

Language:: English

References (61)

Determination of protein-protein interactions by matrix-assisted laser desorption/ionization mass spectrometry Farmer, Terry B.; Caprioli, Richard M. Journal of Mass Spectrometry, Vol. 33, Issue 8 https://doi.org/10.1002/(SICI)1096-9888(199808)33:8<697::AID-JMS711>3.0.CO;2-H	journal	August 1998
Structural studies of the streptavidin binding loop: Streptavidin binding loop Stenkamp, Ronald E.; Trong, Isolde Le; Klumb, Lisa Protein Science, Vol. 6, Issue 6 https://doi.org/10.1002/pro.5560060604	journal	June 1997
Engineering monomeric streptavidin and its ligands with infinite affinity in binding but reversibility in interaction Wu, Sau-Ching; Ng, Kenneth K. -S.; Wong, Sui-Lam Proteins: Structure, Function, and Bioinformatics, Vol. 77, Issue 2 https://doi.org/10.1002/prot.22446	journal	November 2009
Absolute and relative binding free energy calculations of the interaction of biotin and its analogs with streptavidin using molecular dynamics/free energy perturbation approaches Miyamoto, Shuichi; Kollman, Peter A. Proteins: Structure, Function, and Genetics, Vol. 16, Issue 3 https://doi.org/10.1002/prot.340160303	journal	July 1993
Streptavidin–biotin technology: improvements and innovations in chemical and biological applications Dundas, Christopher M.; Demonte, Daniel; Park, Sheldon Applied Microbiology and Biotechnology, Vol. 97, Issue 21 https://doi.org/10.1007/s00253-013-5232-z	journal	September 2013
Flexibility of a biotinylated ligand in artificial metalloenzymes based on streptavidin—an insight from molecular dynamics simulations with classical and ab initio force fields Panek, Jarosław J.; Ward, Thomas R.; Jezierska-Mazzarello, Aneta Journal of Computer-Aided Molecular Design, Vol. 24, Issue 9 https://doi.org/10.1007/s10822-010-9369-x	journal	June 2010
Protein-protein interactions: A review of protein dimer structures Jones, Susan; Thornton, Janet M. Progress in Biophysics and Molecular Biology, Vol. 63, Issue 1 https://doi.org/10.1016/0079-6107(94)00008-W	journal	January 1995
Rapid estimation of avidin and streptavidin by fluorescence quenching or fluorescence polarization Kada, Gerald; Kaiser, Karl; Falk, Heinz Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1427, Issue 1 https://doi.org/10.1016/S0304-4165(98)00177-9	journal	March 1999
Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential Bahar, Ivet; Atilgan, Ali Rana; Erman, Burak Folding and Design, Vol. 2, Issue 3 https://doi.org/10.1016/S1359-0278(97)00024-2	journal	June 1997
Streptavidin cooperative allosterism upon binding biotin observed by differential changes in intrinsic fluorescence Waner, Mark J.; Hiznay, James M.; Mustovich, Anthony T. Biochemistry and Biophysics Reports, Vol. 17 https://doi.org/10.1016/j.bbrep.2018.12.011	journal	March 2019
Love–Hate ligands for high resolution analysis of strain in ultra-stable protein/small molecule interaction Fairhead, Michael; Shen, Di; Chan, Louis K. M. Bioorganic & Medicinal Chemistry, Vol. 22, Issue 19 https://doi.org/10.1016/j.bmc.2014.07.029	journal	October 2014
Crystallographic Analysis of a Full-length Streptavidin with Its C-terminal Polypeptide Bound in the Biotin Binding Site Le Trong, Isolde; Humbert, Nicolas; Ward, Thomas R. Journal of Molecular Biology, Vol. 356, Issue 3 https://doi.org/10.1016/j.jmb.2005.11.086	journal	February 2006
Plug-and-Play Pairing via Defined Divalent Streptavidins Fairhead, Michael; Krndija, Denis; Lowe, Ed D. Journal of Molecular Biology, Vol. 426, Issue 1 https://doi.org/10.1016/j.jmb.2013.09.016	journal	January 2014
Coarse-grained normal mode analysis in structural biology Bahar, Ivet; Rader, Aj Current Opinion in Structural Biology, Vol. 15, Issue 5 https://doi.org/10.1016/j.sbi.2005.08.007	journal	October 2005
Time-resolved structural studies at synchrotrons and X-ray free electron lasers: opportunities and challenges Neutze, Richard; Moffat, Keith Current Opinion in Structural Biology, Vol. 22, Issue 5 https://doi.org/10.1016/j.sbi.2012.08.006	journal	October 2012
Macromolecular room temperature crystallography Fischer, Marcus Quarterly Reviews of Biophysics, Vol. 54 https://doi.org/10.1017/S0033583520000128	journal	January 2021
A Streptavidin Binding Site Mutation Yields an Unexpected Result: An Ionized Asp128 Residue Is Not Essential for Strong Biotin Binding Baugh, Loren; Le Trong, Isolde; Stayton, Patrick S. Biochemistry, Vol. 55, Issue 37 https://doi.org/10.1021/acs.biochem.6b00698	journal	September 2016
Impact of Silane Monolayers on the Adsorption of Streptavidin on Silica and Its Subsequent Interactions with Biotin: Molecular Dynamics and Steered Molecular Dynamics Simulations Lecot, Solène; Chevolot, Yann; Phaner-Goutorbe, Magali The Journal of Physical Chemistry B, Vol. 124, Issue 31 https://doi.org/10.1021/acs.jpcb.0c04382	journal	July 2020
A Streptavidin Mutant Useful for Directed Immobilization on Solid Surfaces Reznik, Gabriel O.; Vajda, Sandor; Cantor, Charles R. Bioconjugate Chemistry, Vol. 12, Issue 6 https://doi.org/10.1021/bc015507t	journal	September 2001
Engineered Streptavidin Monomer and Dimer with Improved Stability and Function Lim, Kok Hong; Huang, Heng; Pralle, Arnd Biochemistry, Vol. 50, Issue 40 https://doi.org/10.1021/bi2010366	journal	September 2011
The Origins of Femtomolar Protein−Ligand Binding: Hydrogen-Bond Cooperativity and Desolvation Energetics in the Biotin−(Strept)Avidin Binding Site DeChancie, Jason; Houk, K. N. Journal of the American Chemical Society, Vol. 129, Issue 17 https://doi.org/10.1021/ja066950n	journal	May 2007
Crystal structure of human cytochrome P450 2C9 with bound warfarin Williams, Pamela A.; Cosme, Jose; Ward, Alison Nature, Vol. 424, Issue 6947 https://doi.org/10.1038/nature01862	journal	July 2003
Selenium single-wavelength anomalous diffraction de novo phasing using an X-ray-free electron laser Hunter, Mark S.; Yoon, Chun Hong; DeMirci, Hasan Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13388	journal	November 2016
Concentric-flow electrokinetic injector enables serial crystallography of ribosome and photosystem II Sierra, Raymond G.; Gati, Cornelius; Laksmono, Hartawan Nature Methods, Vol. 13, Issue 1 https://doi.org/10.1038/nmeth.3667	journal	November 2015
Allosteric coupling between α-rings of the 20S proteasome Yu, Zanlin; Yu, Yadong; Wang, Feng Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18415-7	journal	September 2020
The origin of the cooperativity in the streptavidin-biotin system: A computational investigation through molecular dynamics simulations Liu, Fengjiao; Zhang, John Z. H.; Mei, Ye Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep27190	journal	June 2016
The Crystal Structure of Monovalent Streptavidin Zhang, Min; Biswas, Sangita; Deng, Wenbin Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35915	journal	December 2016
Temperature artifacts in protein structures bias ligand-binding predictions Bradford, Shanshan Y. C.; El Khoury, Léa; Ge, Yunhui Chemical Science, Vol. 12, Issue 34 https://doi.org/10.1039/D1SC02751D	journal	January 2021
Entropic effect and residue specific entropic contribution to the cooperativity in streptavidin–biotin binding Cong, Yalong; Huang, Kaifang; Li, Yuchen Nanoscale, Vol. 12, Issue 13 https://doi.org/10.1039/c9nr08380d	journal	January 2020
How the biotin–streptavidin interaction was made even stronger: investigation via crystallography and a chimaeric tetramer Chivers, Claire E.; Koner, Apurba L.; Lowe, Edward D. Biochemical Journal, Vol. 435, Issue 1 https://doi.org/10.1042/BJ20101593	journal	March 2011
Accessing protein conformational ensembles using room-temperature X-ray crystallography Fraser, J. S.; van den Bedem, H.; Samelson, A. J. Proceedings of the National Academy of Sciences, Vol. 108, Issue 39 https://doi.org/10.1073/pnas.1111325108	journal	September 2011
Crystal structure of core streptavidin determined from multiwavelength anomalous diffraction of synchrotron radiation. Hendrickson, W. A.; Pahler, A.; Smith, J. L. Proceedings of the National Academy of Sciences, Vol. 86, Issue 7 https://doi.org/10.1073/pnas.86.7.2190	journal	April 1989
What determines the strength of noncovalent association of ligands to proteins in aqueous solution? Miyamoto, S.; Kollman, P. A. Proceedings of the National Academy of Sciences, Vol. 90, Issue 18 https://doi.org/10.1073/pnas.90.18.8402	journal	September 1993
Engineering subunit association of multisubunit proteins: A dimeric streptavidin Sano, T.; Vajda, S.; Smith, C. L. Proceedings of the National Academy of Sciences, Vol. 94, Issue 12 https://doi.org/10.1073/pnas.94.12.6153	journal	June 1997
Recombinant Core Streptavidins Sano, Takeshi; Pandori, Mark W.; Chen, Xiaomin Journal of Biological Chemistry, Vol. 270, Issue 47 https://doi.org/10.1074/jbc.270.47.28204	journal	November 1995
Interaction of Biotin with Streptavidin González, Martín; Bagatolli, Luis A.; Echabe, Izaskun Journal of Biological Chemistry, Vol. 272, Issue 17 https://doi.org/10.1074/jbc.272.17.11288	journal	April 1997
Ligand Exchange between Proteins Pazy, Yael; Kulik, Tikva; Bayer, Edward A. Journal of Biological Chemistry, Vol. 277, Issue 34 https://doi.org/10.1074/jbc.M202874200	journal	August 2002
ProDy: Protein Dynamics Inferred from Theory and Experiments Bakan, A.; Meireles, L. M.; Bahar, I. Bioinformatics, Vol. 27, Issue 11, p. 1575-1577 https://doi.org/10.1093/bioinformatics/btr168	journal	April 2011
Vibrational Dynamics of Folded Proteins: Significance of Slow and Fast Motions in Relation to Function and Stability Bahar, Ivet; Atilgan, Ali Rana; Demirel, Melik C. Physical Review Letters, Vol. 80, Issue 12 https://doi.org/10.1103/PhysRevLett.80.2733	journal	March 1998
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
CrystFEL : a software suite for snapshot serial crystallography White, Thomas A.; Kirian, Richard A.; Martin, Andrew V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812002312	journal	March 2012
Indexing in single-crystal diffractometry with an obstinate list of reflections Duisenberg, A. J. M. Journal of Applied Crystallography, Vol. 25, Issue 2 https://doi.org/10.1107/S0021889891010634	journal	April 1992
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Validation of crystallographic models containing TLS or other descriptions of anisotropy Zucker, Frank; Champ, P. Christoph; Merritt, Ethan A. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 8 https://doi.org/10.1107/S0907444910020421	journal	July 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
Streptavidin and its biotin complex at atomic resolution Le Trong, Isolde; Wang, Zhizhi; Hyre, David E. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 9 https://doi.org/10.1107/S0907444911027806	journal	August 2011
Autoindexing diffraction images with iMosflm Powell, Harold R.; Johnson, Owen; Leslie, Andrew G. W. Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444912048524	journal	June 2013
Cheetah : software for high-throughput reduction and analysis of serial femtosecond X-ray diffraction data Barty, Anton; Kirian, Richard A.; Maia, Filipe R. N. C. Journal of Applied Crystallography, Vol. 47, Issue 3 https://doi.org/10.1107/S1600576714007626	journal	May 2014
Linac Coherent Light Source data analysis using psana Damiani, D.; Dubrovin, M.; Gaponenko, I. Journal of Applied Crystallography, Vol. 49, Issue 2 https://doi.org/10.1107/S1600576716004349	journal	March 2016
Recent developments in CrystFEL White, Thomas A.; Mariani, Valerio; Brehm, Wolfgang Journal of Applied Crystallography, Vol. 49, Issue 2 https://doi.org/10.1107/S1600576716004751	journal	March 2016
OnDA : online data analysis and feedback for serial X-ray imaging Mariani, Valerio; Morgan, Andrew; Yoon, Chun Hong Journal of Applied Crystallography, Vol. 49, Issue 3 https://doi.org/10.1107/S1600576716007469	journal	May 2016
The Macromolecular Femtosecond Crystallography Instrument at the Linac Coherent Light Source Sierra, Raymond G.; Batyuk, Alexander; Sun, Zhibin Journal of Synchrotron Radiation, Vol. 26, Issue 2 https://doi.org/10.1107/S1600577519001577	journal	February 2019
The ePix10k 2-megapixel hard X-ray detector at LCLS van Driel, Tim Brandt; Nelson, Silke; Armenta, Rebecca Journal of Synchrotron Radiation, Vol. 27, Issue 3 https://doi.org/10.1107/S1600577520004257	journal	April 2020
XGANDALF – extended gradient descent algorithm for lattice finding Gevorkov, Yaroslav; Yefanov, Oleksandr; Barty, Anton Acta Crystallographica Section A Foundations and Advances, Vol. 75, Issue 5 https://doi.org/10.1107/S2053273319010593	journal	August 2019
Processing serial crystallography data with CrystFEL : a step-by-step guide White, Thomas A. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/S205979831801238X	journal	January 2019
Cooperative hydrogen bond interactions in the streptavidin-biotin system Hyre, D. E. Protein Science, Vol. 15, Issue 3 https://doi.org/10.1110/ps.051970306	journal	February 2006
Biotin-Binding Proteins in the Defense of Mushrooms against Predators and Parasites Bleuler-Martinez, Silvia; Schmieder, Stefanie; Aebi, Markus Applied and Environmental Microbiology, Vol. 78, Issue 23 https://doi.org/10.1128/AEM.02286-12	journal	December 2012
Quaternary Structure of Proteins Klotz, I. M.; Langebman, N. R.; Dahnall, D. W. Annual Review of Biochemistry, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.bi.39.070170.000325	journal	June 1970
Data systems for the Linac coherent light source Thayer, J.; Damiani, D.; Ford, C. Advanced Structural and Chemical Imaging, Vol. 3, Issue 1 https://doi.org/10.1186/s40679-016-0037-7	journal	January 2017

Similar Records

Streptavidin and its biotin complex at atomic resolution

Journal Article · 2011 · Acta Crystallographica. Section D: Biological Crystallography · OSTI ID:22351242

Le Trong, Isolde; Wang, Zhizhi; Hyre, David E.; +2 more

Spore-displayed streptavidin: A live diagnostic tool in biotechnology

Journal Article · 2005 · Biochemical and Biophysical Research Communications · OSTI ID:20709207

Kim, June-Hyung; Lee, Chang-Soo; Kim, Byung-Gee

A novel approach to make homogeneous protease-stable monovalent streptavidin

Journal Article · 2015 · Biochemical and Biophysical Research Communications · OSTI ID:1232691

Zhang, M.; Shao, J; Xiao, J.; +2 more

Related Subjects

60 APPLIED LIFE SCIENCES
Serial Femtosecond X-ray Crystallography

Title: Cooperative allostery and structural dynamics of streptavidin at cryogenic- and ambient-temperature

Citation Formats

References (61)

Similar Records

Related Subjects