Design of an expression system to enhance MBP-mediated crystallization

Jin, Tengchuan; Chuenchor, Watchalee; Jiang, Jiansheng; Cheng, Jinbo; Li, Yajuan; Fang, Kang; Huang, Mo; Smith, Patrick; Xiao, Tsan Sam

doi:10.1038/srep40991

Title: Design of an expression system to enhance MBP-mediated crystallization

Journal Article · Mon Jan 23 00:00:00 EST 2017 · Scientific Reports

DOI:https://doi.org/10.1038/srep40991· OSTI ID:1357647

Jin, Tengchuan ^[1]; Chuenchor, Watchalee ^[2]; Jiang, Jiansheng ^[2]; Cheng, Jinbo ^[3]; Li, Yajuan ^[3]; Fang, Kang ^[3]; Huang, Mo ^[2]; Smith, Patrick ^[2]; Xiao, Tsan Sam ^[4]

Univ. of Science and Technology of China, Hefei (China); National Inst. of Health (NIH), Bethesda, MD (United States)
National Inst. of Health (NIH), Bethesda, MD (United States)
Univ. of Science and Technology of China, Hefei (China)
Case Western Reserve Univ., Cleveland, OH (United States)

Crystallization chaperones have been used to facilitate the crystallization of challenging proteins. Even though the maltose-binding protein (MBP) is one of the most commonly used crystallization chaperones, the design of optimal expression constructs for crystallization of MBP fusion proteins remains a challenge. To increase the success rate of MBP-facilitated crystallization, a series of expression vectors have been designed with either a short flexible linker or a set of rigid helical linkers. Seven death domain superfamily members were tested for crystallization with this set of vectors, six of which had never been crystallized before. All of the seven targets were crystallized, and their structures were determined using at least one of the vectors. Our successful crystallization of all of the targets demonstrates the validity of our approach and expands the arsenal of the crystallization chaperone toolkit, which may be applicable to crystallization of other difficult protein targets, as well as to other crystallization chaperones.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Cancer Inst.; National Inst. of General Medical Sciences; China Postdoctoral Science Foundation

Grant/Contract Number:: AC02-98CH10886; Y1-CO-1020; Y1-GM-1104; 2015M582007

OSTI ID:: 1357647

Journal Information:: Scientific Reports, Vol. 7, Issue 1; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 41 works

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References (59)

Bax Crystal Structures Reveal How BH3 Domains Activate Bax and Nucleate Its Oligomerization to Induce Apoptosis Czabotar, Peter E.; Westphal, Dana; Dewson, Grant Cell, Vol. 152, Issue 3 https://doi.org/10.1016/j.cell.2012.12.031	journal	January 2013
The Fas–FADD death domain complex structure unravels signalling by receptor clustering Scott, Fiona L.; Stec, Boguslaw; Pop, Cristina Nature, Vol. 457, Issue 7232 https://doi.org/10.1038/nature07606	journal	December 2008
New surface contacts formed upon reductive lysine methylation: Improving the probability of protein crystallization: Lysine Methylation Sledz, Pawel; Zheng, Heping; Murzyn, Krzysztof Protein Science, Vol. 19, Issue 7 https://doi.org/10.1002/pro.420	journal	May 2010
Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1 Qin, Hongxu; Srinivasula, Srinivasa M.; Wu, Geng Nature, Vol. 399, Issue 6736 https://doi.org/10.1038/21124	journal	June 1999
Crystal structure of human T cell leukemia virus type 1 gp21 ectodomain crystallized as a maltose-binding protein chimera reveals structural evolution of retroviral transmembrane proteins Kobe, B.; Center, R. J.; Kemp, B. E. Proceedings of the National Academy of Sciences, Vol. 96, Issue 8 https://doi.org/10.1073/pnas.96.8.4319	journal	April 1999
A Maltose-Binding Protein Fusion Construct Yields a Robust Crystallography Platform for MCL1 Clifton, Matthew C.; Dranow, David M.; Leed, Alison PLOS ONE, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pone.0125010	journal	April 2015
Crystal structure of human IPS-1/MAVS/VISA/Cardif caspase activation recruitment domain Potter, Jane A.; Randall, Richard E.; Taylor, Garry L. BMC Structural Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1472-6807-8-11	journal	January 2008
It's all in the crystals… Derewenda, Zygmunt S. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911007797	journal	March 2011
Mass spectrometry guided in situ proteolysis to obtain crystals for X-ray structure determination Gheyi, Tarun; Rodgers, Logan; Romero, Richard Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 10 https://doi.org/10.1016/j.jasms.2010.06.015	journal	October 2010
Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused Kapust, Rachel B.; Waugh, David S. Protein Science, Vol. 8, Issue 8, p. 1668-1674 https://doi.org/10.1110/ps.8.8.1668	journal	January 1999
Fusion Partner Toolchest for the Stabilization and Crystallization of G Protein-Coupled Receptors Chun, Eugene; Thompson, Aaron A.; Liu, Wei Structure, Vol. 20, Issue 6 https://doi.org/10.1016/j.str.2012.04.010	journal	June 2012
Structural Basis for Allosteric Regulation of GPCRs by Sodium Ions Liu, W.; Chun, E.; Thompson, A. A. Science, Vol. 337, Issue 6091 https://doi.org/10.1126/science.1219218	journal	July 2012
Structural insights for engineering binding proteins based on non-antibody scaffolds Gilbreth, Ryan N.; Koide, Shohei Current Opinion in Structural Biology, Vol. 22, Issue 4 https://doi.org/10.1016/j.sbi.2012.06.001	journal	August 2012
GPCR Engineering Yields High-Resolution Structural Insights into 2-Adrenergic Receptor Function Rosenbaum, D. M.; Cherezov, V.; Hanson, M. A. Science, Vol. 318, Issue 5854 https://doi.org/10.1126/science.1150609	journal	October 2007
Use of a fusion protein to obtain crystals suitable for X-ray analysis: Crystallization of a GST-fused protein containing the DNA-binding domain of DNA replication-related element-binding factor, DREF Kuge, Munekazu; Fujii, Yoshifumi; Shimizu, Toshiyuki Protein Science, Vol. 6, Issue 8 https://doi.org/10.1002/pro.5560060822	journal	August 1997
Structure of the human smoothened receptor bound to an antitumour agent Wang, Chong; Wu, Huixian; Katritch, Vsevolod Nature, Vol. 497, Issue 7449 https://doi.org/10.1038/nature12167	journal	May 2013
Easy mammalian expression and crystallography of maltose-binding protein-fused human proteins Bokhove, Marcel; Sadat Al Hosseini, Hamed; Saito, Takako Journal of Structural Biology, Vol. 194, Issue 1 https://doi.org/10.1016/j.jsb.2016.01.016	journal	April 2016
The Ability to Enhance the Solubility of Its Fusion Partners Is an Intrinsic Property of Maltose-Binding Protein but Their Folding Is Either Spontaneous or Chaperone-Mediated Raran-Kurussi, Sreejith; Waugh, David S. PLoS ONE, Vol. 7, Issue 11 https://doi.org/10.1371/journal.pone.0049589	journal	November 2012
Crystal structure of peroxisomal targeting signal-2 bound to its receptor complex Pex7p–Pex21p Pan, Dongqing; Nakatsu, Toru; Kato, Hiroaki Nature Structural & Molecular Biology, Vol. 20, Issue 8 https://doi.org/10.1038/nsmb.2618	journal	June 2013
The Fas–FADD death domain complex structure reveals the basis of DISC assembly and disease mutations Wang, Liwei; Yang, Jin Kuk; Kabaleeswaran, Venkataraman Nature Structural & Molecular Biology, Vol. 17, Issue 11 https://doi.org/10.1038/nsmb.1920	journal	October 2010
Thioredoxin as a fusion tag for carrier‐driven crystallization Corsini, Lorenzo; Hothorn, Michael; Scheffzek, Klaus Protein Science, Vol. 17, Issue 12 https://doi.org/10.1110/ps.037564.108	journal	December 2008
Helical assembly in the MyD88–IRAK4–IRAK2 complex in TLR/IL-1R signalling Lin, Su-Chang; Lo, Yu-Chih; Wu, Hao Nature, Vol. 465, Issue 7300 https://doi.org/10.1038/nature09121	journal	May 2010
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Toward rational protein crystallization: A Web server for the design of crystallizable protein variants Goldschmidt, Lukasz; Cooper, David R.; Derewenda, Zygmunt S. Protein Science, Vol. 16, Issue 8 https://doi.org/10.1110/ps.072914007	journal	August 2007
N-Terminal T4 Lysozyme Fusion Facilitates Crystallization of a G Protein Coupled Receptor Zou, Yaozhong; Weis, William I.; Kobilka, Brian K. PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0046039	journal	October 2012
Crystallization of a trimeric human T cell leukemia virus type 1 gp21 ectodomain fragment as a chimera with maltose-binding protein Center, Rob J.; Kobe, Bostjan; Wilson, Kirilee A. Protein Science, Vol. 7, Issue 7 https://doi.org/10.1002/pro.5560070715	journal	July 1998
An approach to crystallizing proteins by metal-mediated synthetic symmetrization Laganowsky, Arthur; Zhao, Minglei; Soriaga, Angela B. Protein Science, Vol. 20, Issue 11 https://doi.org/10.1002/pro.727	journal	September 2011
Crystal Structure of the Maltose Transporter in a Pretranslocation Intermediate State Oldham, M. L.; Chen, J. Science, Vol. 332, Issue 6034 https://doi.org/10.1126/science.1200767	journal	May 2011
Solution structure of the tumor necrosis factor receptor-1 death domain Sukits, Steven F.; Lin, Lih-Ling; Hsu, Sang Journal of Molecular Biology, Vol. 310, Issue 4 https://doi.org/10.1006/jmbi.2001.4790	journal	July 2001
Processive Steps in the Reverse Direction Require Uncoupling of the Lead Head Lever Arm of Myosin VI Ménétrey, Julie; Isabet, Tatiana; Ropars, Virginie Molecular Cell, Vol. 48, Issue 1 https://doi.org/10.1016/j.molcel.2012.07.034	journal	October 2012
In situ proteolysis for protein crystallization and structure determination Dong, Aiping; Xu, Xiaohui; Edwards, Aled M. Nature Methods, Vol. 4, Issue 12 https://doi.org/10.1038/nmeth1118	journal	November 2007
Chapter 16 Tagging for Protein Expression Malhotra, Arun; Burgess, Richard R.; Deutscher, Murray P. Guide to Protein Purification, 2nd Edition, Vol. 463, p. 239-258 https://doi.org/10.1016/S0076-6879(09)63016-0	book	January 2009
Structure of the NLRP1 caspase recruitment domain suggests potential mechanisms for its association with procaspase-1: 2.0 Å Crystal Structure of the NLRP1 CARD Jin, Tengchuan; Curry, James; Smith, Patrick Proteins: Structure, Function, and Bioinformatics, Vol. 81, Issue 7 https://doi.org/10.1002/prot.24287	journal	April 2013
Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems Terpe, K. Applied Microbiology and Biotechnology, Vol. 60, Issue 5, p. 523-533 https://doi.org/10.1007/s00253-002-1158-6	journal	January 2003
Enhanced Crystallizability by Protein Engineering Approaches: A General Overview Ruggiero, Alessia; Smaldone, Giovanni; Squeglia, Flavia Protein & Peptide Letters, Vol. 19, Issue 7 https://doi.org/10.2174/092986612800793172	journal	May 2012
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
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
Polymer-driven crystallization Nauli, Sehat; Farr, Saman; Lee, Yueh-Jung Protein Science, Vol. 16, Issue 11 https://doi.org/10.1110/ps.073074207	journal	November 2007
The death-fold superfamily of homotypic interaction motifs Kersse, Kristof; Verspurten, Jelle; Berghe, Tom Vanden Trends in Biochemical Sciences, Vol. 36, Issue 10 https://doi.org/10.1016/j.tibs.2011.06.006	journal	October 2011
Structure-function analyses of the human SIX1–EYA2 complex reveal insights into metastasis and BOR syndrome Patrick, Aaron N.; Cabrera, Joshua H.; Smith, Anna L. Nature Structural & Molecular Biology, Vol. 20, Issue 4 https://doi.org/10.1038/nsmb.2505	journal	February 2013
Basis for a ubiquitin-like protein thioester switch toggling E1–E2 affinity Huang, Danny T.; Hunt, Harold W.; Zhuang, Min Nature, Vol. 445, Issue 7126 https://doi.org/10.1038/nature05490	journal	January 2007
A graphical user interface to the CCP 4 program suite Potterton, Elizabeth; Briggs, Peter; Turkenburg, Maria Acta Crystallographica Section D Biological Crystallography, Vol. 59, Issue 7 https://doi.org/10.1107/S0907444903008126	journal	June 2003
New concepts and aids to facilitate crystallization Bukowska, Magdalena A.; Grütter, Markus G. Current Opinion in Structural Biology, Vol. 23, Issue 3 https://doi.org/10.1016/j.sbi.2013.03.003	journal	June 2013
Crystal structure of a dominant B-cell epitope from the pres2 region of hepatitis B virus in the form of an inserted peptide segment in maltodextrin-binding protein Saul, F. A.; Normand, B. Vulliez-le; Lema, F. Journal of Molecular Biology, Vol. 280, Issue 2 https://doi.org/10.1006/jmbi.1998.1866	journal	July 1998
Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana Ullah, Hemayet; Scappini, Erica Louise; Moon, Andrea Florence Protein Science, Vol. 17, Issue 10 https://doi.org/10.1110/ps.035121.108	journal	October 2008
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
Combining in-situ proteolysis and microseed matrix screening to promote crystallization of PrPc-nanobody complexes Abskharon, R. N. N.; Soror, S. H.; Pardon, E. Protein Engineering Design and Selection, Vol. 24, Issue 9 https://doi.org/10.1093/protein/gzr017	journal	May 2011
Crystal structures of MBP fusion proteins: Structures of MBP Fusion Proteins Waugh, David S. Protein Science, Vol. 25, Issue 3 https://doi.org/10.1002/pro.2863	journal	January 2016
Lysine Methylation as a Routine Rescue Strategy for Protein Crystallization Walter, Thomas S.; Meier, Christoph; Assenberg, Rene Structure, Vol. 14, Issue 11 https://doi.org/10.1016/j.str.2006.09.005	journal	November 2006
Death Domain Assembly Mechanism Revealed by Crystal Structure of the Oligomeric PIDDosome Core Complex Park, Hyun Ho; Logette, Emmanuelle; Raunser, Stefan Cell, Vol. 128, Issue 3 https://doi.org/10.1016/j.cell.2007.01.019	journal	February 2007
Molecular recognition of parathyroid hormone by its G protein-coupled receptor Pioszak, Augen A.; Xu, H. Eric Proceedings of the National Academy of Sciences, Vol. 105, Issue 13 https://doi.org/10.1073/pnas.0801027105	journal	March 2008
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
A synergistic approach to protein crystallization: Combination of a fixed-arm carrier with surface entropy reduction Moon, Andrea F.; Mueller, Geoffrey A.; Zhong, Xuejun Protein Science https://doi.org/10.1002/pro.368	journal	January 2010
[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
The ability to enhance the solubility of its fusion partners is an intrinsic property of maltose-binding protein but their folding is either spontaneous or chaperone-mediated Raran-Kurussi, Sreejith; Waugh, David S. Plos One, Vol. 7, Issue 11, e49589 https://doi.org/10.3410/f.717968797.793468506	journal	November 2012
Crystallization and improvement of crystal quality for X-ray diffraction of maltooligosyl trehalose synthase by reductive methylation of lysine residues Kobayashi, Masanori; Kubota, Michio; Matsuura, Yoshiki Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 4 https://doi.org/10.1107/s0907444999002115	journal	April 1999
The structure of the CARD8 caspase-recruitment domain suggests its association with the FIIND domain and procaspases through adjacent surfaces Jin, Tengchuan; Huang, Mo; Smith, Patrick Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 69, Issue 5 https://doi.org/10.1107/s1744309113010075	journal	April 2013
Structure of the caspase-recruitment domain from a zebrafish guanylate-binding protein Jin, Tengchuan; Huang, Mo; Smith, Patrick Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 69, Issue 8 https://doi.org/10.1107/s1744309113015558	journal	July 2013
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010

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