Enhancing protein stability with extended disulfide bonds

Liu, Tao; Wang, Yan; Luo, Xiaozhou; Li, Jack; Reed, Sean A.; Xiao, Han; Young, Travis S.; Schultz, Peter G.

doi:10.1073/pnas.1605363113

Title: Enhancing protein stability with extended disulfide bonds

Journal Article · Mon May 09 00:00:00 UTC 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1605363113 · OSTI ID:1252319

Liu, Tao ^[1]; Wang, Yan ^[1]; Luo, Xiaozhou ^[1]; Li, Jack ^[1]; Reed, Sean A. ^[1]; Xiao, Han ^[1]; Young, Travis S. ^[2]; Schultz, Peter G. ^[3]

Department of Chemistry and The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA 92037,
California Institute for Biomedical Research , La Jolla, CA 92037
Department of Chemistry and The Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA 92037,, California Institute for Biomedical Research , La Jolla, CA 92037

Significance This work describes a facile system for incorporating noncanonical amino acids containing long side-chain thiols using an expanded genetic code. These amino acids begin to overcome the distance and geometric constraints of the cysteine disulfide and can pair with cysteines to cross-link more remote sites in proteins. To demonstrate this notion, we constructed a library of random β-lactamase mutants containing these noncanonical amino acids and grew them at nonpermissive temperatures. We identified a mutant enzyme that is cross-linked by one such extended disulfide bond that has significantly enhanced thermal stability. This study suggests that an expanded set of amino acid building blocks can provide novel solutions to evolutionary challenges.

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Research Organization:: Scripps Research Inst., La Jolla, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0011787

OSTI ID:: 1252319

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 21 Vol. 113; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (36)

Site-Specific Incorporation of ε-N-Crotonyllysine into Histones Kim, Chan Hyuk; Kang, Mingchao; Kim, Hak Joong Angewandte Chemie International Edition, Vol. 51, Issue 29 https://doi.org/10.1002/anie.201203349	journal	June 2012
Proximity-Enabled Protein Crosslinking through Genetically Encoding Haloalkane Unnatural Amino Acids Xiang, Zheng; Lacey, Vanessa K.; Ren, Haiyan Angewandte Chemie International Edition, Vol. 53, Issue 8 https://doi.org/10.1002/anie.201308794	journal	January 2014
Development of thermostable Candida antarctica lipase B through novel in silico design of disulfide bridge Le, Quang Anh Tuan; Joo, Jeong Chan; Yoo, Young Je Biotechnology and Bioengineering, Vol. 109, Issue 4 https://doi.org/10.1002/bit.24371	journal	November 2011
Enhancing thermostability of a Rhizomucor miehei lipase by engineering a disulfide bond and displaying on the yeast cell surface Han, Zhen-lin; Han, Shuang-yan; Zheng, Sui-ping Applied Microbiology and Biotechnology, Vol. 85, Issue 1 https://doi.org/10.1007/s00253-009-2067-8	journal	June 2009
Enhancing the Thermostability of a Cold-Active Lipase from Penicillium cyclopium by In Silico Design of a Disulfide Bridge Tan, Zhongbiao; Li, Jianfang; Wu, Minchen Applied Biochemistry and Biotechnology, Vol. 173, Issue 7 https://doi.org/10.1007/s12010-014-0962-7	journal	May 2014
Disulphide bridges in globular proteins Thornton, J. M. Journal of Molecular Biology, Vol. 151, Issue 2 https://doi.org/10.1016/0022-2836(81)90515-5	journal	September 1981
Evolution of an Antibiotic Resistance Enzyme Constrained by Stability and Activity Trade-offs Wang, Xiaojun; Minasov, George; Shoichet, Brian K. Journal of Molecular Biology, Vol. 320, Issue 1 https://doi.org/10.1016/S0022-2836(02)00400-X	journal	June 2002
Disulfide bonds as switches for protein function Hogg, Philip J. Trends in Biochemical Sciences, Vol. 28, Issue 4 https://doi.org/10.1016/S0968-0004(03)00057-4	journal	April 2003
Disulfide bond isomerization in prokaryotes Gleiter, Stefan; Bardwell, James C. A. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1783, Issue 4 https://doi.org/10.1016/j.bbamcr.2008.02.009	journal	April 2008
Mechanism of stabilization of Bacillus circulans xylanase upon the introduction of disulfide bonds Davoodi, Jamshid; Wakarchuk, Waren W.; Carey, Paul R. Biophysical Chemistry, Vol. 125, Issue 2-3 https://doi.org/10.1016/j.bpc.2006.10.006	journal	February 2007
Protein disulfide engineering Dombkowski, Alan A.; Sultana, Kazi Zakia; Craig, Douglas B. FEBS Letters, Vol. 588, Issue 2 https://doi.org/10.1016/j.febslet.2013.11.024	journal	November 2013
Engineering a de novo internal disulfide bridge to improve the thermal stability of xylanase from Bacillus stearothermophilus No. 236 Jeong, Mi-Young; Kim, Sanguk; Yun, Cheol-Won Journal of Biotechnology, Vol. 127, Issue 2 https://doi.org/10.1016/j.jbiotec.2006.07.005	journal	January 2007
Multiple Global Suppressors of Protein Stability Defects Facilitate the Evolution of Extended-Spectrum TEM β-Lactamases Brown, Nicholas G.; Pennington, Jeanine M.; Huang, Wanzhi Journal of Molecular Biology, Vol. 404, Issue 5 https://doi.org/10.1016/j.jmb.2010.10.008	journal	December 2010
Site-directed mutagenesis of an Aspergillus niger xylanase B and its expression, purification and enzymatic characterization in Pichia pastoris Chen, Xingzhou; Xu, Shunqing; Zhu, Maosheng Process Biochemistry, Vol. 45, Issue 1 https://doi.org/10.1016/j.procbio.2009.08.009	journal	January 2010
New Water-Soluble Phosphines as Reductants of Peptide and Protein Disulfide Bonds: Reactivity and Membrane Permeability ^† Cline, Daniel J.; Redding, Sarah E.; Brohawn, Stephen G. Biochemistry, Vol. 43, Issue 48 https://doi.org/10.1021/bi048329a	journal	December 2004
Structural Perturbation and Compensation by Directed Evolution at Physiological Temperature Leads to Thermostabilization of β-Lactamase ^† Hecky, Jochen; Müller, Kristian M. Biochemistry, Vol. 44, Issue 38 https://doi.org/10.1021/bi0501885	journal	September 2005
Genetically Encoding an Electrophilic Amino Acid for Protein Stapling and Covalent Binding to Native Receptors Chen, Xiao-Hua; Xiang, Zheng; Hu, Ying S. ACS Chemical Biology, Vol. 9, Issue 9 https://doi.org/10.1021/cb500453a	journal	July 2014
Genetic Incorporation of ε- N -2-Hydroxyisobutyryl-lysine into Recombinant Histones Xiao, Han; Xuan, Weimin; Shao, Sida ACS Chemical Biology, Vol. 10, Issue 7 https://doi.org/10.1021/cb501055h	journal	April 2015
Improving Trichoderma reesei Cel7B Thermostability by Targeting the Weak Spots Zhang, Shujun; Wang, Yefei; Song, Xiangfei Journal of Chemical Information and Modeling, Vol. 54, Issue 10 https://doi.org/10.1021/ci500339v	journal	September 2014
A Genetically Encoded aza-Michael Acceptor for Covalent Cross-Linking of Protein–Receptor Complexes Furman, Jennifer L.; Kang, Mingchao; Choi, Seihyun Journal of the American Chemical Society, Vol. 136, Issue 23 https://doi.org/10.1021/ja502851h	journal	May 2014
Addicting diverse bacteria to a noncanonical amino acid Tack, Drew S.; Ellefson, Jared W.; Thyer, Ross Nature Chemical Biology, Vol. 12, Issue 3 https://doi.org/10.1038/nchembio.2002	journal	January 2016
Adding an unnatural covalent bond to proteins through proximity-enhanced bioreactivity Xiang, Zheng; Ren, Haiyan; Hu, Ying S. Nature Methods, Vol. 10, Issue 9 https://doi.org/10.1038/nmeth.2595	journal	August 2013
The human protein disulphide isomerase family: substrate interactions and functional properties Ellgaard, Lars; Ruddock, Lloyd W. EMBO reports, Vol. 6, Issue 1 https://doi.org/10.1038/sj.embor.7400311	journal	January 2005
Designing logical codon reassignment – Expanding the chemistry in biology Dumas, Anaëlle; Lercher, Lukas; Spicer, Christopher D. Chemical Science, Vol. 6, Issue 1 https://doi.org/10.1039/C4SC01534G	journal	January 2015
Evolution of cyclic peptide protease inhibitors Young, T. S.; Young, D. D.; Ahmad, I. Proceedings of the National Academy of Sciences, Vol. 108, Issue 27 https://doi.org/10.1073/pnas.1108045108	journal	June 2011
Exploring the potential impact of an expanded genetic code on protein function Xiao, Han; Nasertorabi, Fariborz; Choi, Sei-hyun Proceedings of the National Academy of Sciences, Vol. 112, Issue 22 https://doi.org/10.1073/pnas.1507741112	journal	May 2015
Disulfide Bond Dihedral Angles from Raman Spectroscopy Van Wart, H. E.; Lewis, A.; Scheraga, H. A. Proceedings of the National Academy of Sciences, Vol. 70, Issue 9 https://doi.org/10.1073/pnas.70.9.2619	journal	September 1973
Stabilization of phage T4 lysozyme by engineered disulfide bonds Matsumura, M.; Becktel, W. J.; Levitt, M. Proceedings of the National Academy of Sciences, Vol. 86, Issue 17 https://doi.org/10.1073/pnas.86.17.6562	journal	September 1989
Disulfide Bond Acquisition through Eukaryotic Protein Evolution Wong, Jason W. H.; Ho, Simon Y. W.; Hogg, Philip J. Molecular Biology and Evolution, Vol. 28, Issue 1 https://doi.org/10.1093/molbev/msq194	journal	July 2010
MODIP revisited: re-evaluation and refinement of an automated procedure for modeling of disulfide bonds in proteins Dani, Vardhan S.; Ramakrishnan, C.; Varadarajan, Raghavan Protein Engineering, Design and Selection, Vol. 16, Issue 3 https://doi.org/10.1093/proeng/gzg024	journal	March 2003
TEM1 β-lactamase structure solved by molecular replacement and refined structure of the S235A mutant Fonzé, E.; Charlier, P.; To'th, Y. Acta Crystallographica Section D Biological Crystallography, Vol. 51, Issue 5 https://doi.org/10.1107/S0907444994014496	journal	September 1995
Disulfide Bonding in Protein Biophysics Fass, Deborah Annual Review of Biophysics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-biophys-050511-102321	journal	June 2012
Adding New Chemistries to the Genetic Code Liu, Chang C.; Schultz, Peter G. Annual Review of Biochemistry, Vol. 79, Issue 1, p. 413-444 https://doi.org/10.1146/annurev.biochem.052308.105824	journal	June 2010
Disulfide by Design 2.0: a web-based tool for disulfide engineering in proteins Craig, Douglas B.; Dombkowski, Alan A. BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-346	journal	December 2013
Engineering a Disulfide Bond in the Lid Hinge Region of Rhizopus chinensis Lipase: Increased Thermostability and Altered Acyl Chain Length Specificity Yu, Xiao-Wei; Tan, Nian-Jiang; Xiao, Rong PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0046388	journal	October 2012
Contribution of Disulfide Bridges to the Thermostability of a Type A Feruloyl Esterase from Aspergillus usamii Yin, Xin; Hu, Die; Li, Jian-Fang PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0126864	journal	May 2015

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59 BASIC BIOLOGICAL SCIENCES
evolutionary advantage
extended disulfide bonds
noncanonical amino acids
thermostability
β-lactamase

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