journal article Open Access Sep 25, 2018

Thermophilic Proteins as Versatile Scaffolds for Protein Engineering

Microorganisms Vol. 6 No. 4 pp. 97 · MDPI AG
View at Publisher Save 10.3390/microorganisms6040097
Abstract
Literature from the past two decades has outlined the existence of a trade-off between protein stability and function. This trade-off creates a unique challenge for protein engineers who seek to introduce new functionality to proteins. These engineers must carefully balance the mutation-mediated creation and/or optimization of function with the destabilizing effect of those mutations. Subsequent research has shown that protein stability is positively correlated with “evolvability” or the ability to support mutations which bestow new functionality on the protein. Since the ultimate goal of protein engineering is to create and/or optimize a protein’s function, highly stable proteins are preferred as potential scaffolds for protein engineering. This review focuses on the application potential for thermophilic proteins as scaffolds for protein engineering. The relatively high inherent thermostability of these proteins grants them a great deal of mutational robustness, making them promising scaffolds for various protein engineering applications. Comparative studies on the evolvability of thermophilic and mesophilic proteins have strongly supported the argument that thermophilic proteins are more evolvable than mesophilic proteins. These findings indicate that thermophilic proteins may represent the scaffold of choice for protein engineering in the future.
Topics

No keywords indexed for this article. Browse by subject →

References
42
[1]
Rubingh "Protein engineering from a bioindustrial point of view" Curr. Opin. Biotechnol. (1997) 10.1016/s0958-1669(97)80062-6
[2]
A relationship between protein stability and protein function.

B K Shoichet, W A Baase, R Kuroki et al.

Proceedings of the National Academy of Sciences 1995 10.1073/pnas.92.2.452
[3]
Effect of active site residues in barnase on activity and stability

Elizabeth M. Meiering, Luis Serrano, Alan R. Fersht

Journal of Molecular Biology 1992 10.1016/0022-2836(92)90387-y
[4]
Why are proteins so robust to site mutations?

Darin M Taverna, Richard A Goldstein

Journal of Molecular Biology 2002 10.1006/jmbi.2001.5226
[5]
Protein stability promotes evolvability

Jesse D. Bloom, Sy T. Labthavikul, Christopher R. Otey et al.

Proceedings of the National Academy of Sciences 2006 10.1073/pnas.0510098103
[6]
Evolution of an Antibiotic Resistance Enzyme Constrained by Stability and Activity Trade-offs

Xiaojun Wang, George Minasov, Brian K. Shoichet

Journal of Molecular Biology 2002 10.1016/s0022-2836(02)00400-x
[7]
Liang "Apparent Tradeoff of Higher Activity in MMP-12 for Enhanced Stability and Flexibility in MMP-3" Biophys. J. (2010) 10.1016/j.bpj.2010.04.002
[8]
How Protein Stability and New Functions Trade Off

Nobuhiko Tokuriki, François Stricher, Luis Serrano et al.

PLOS Computational Biology 2008 10.1371/journal.pcbi.1000002
[9]
Genetic Constraints on Protein Evolution

Manel Camps, Asael Herman, Ern Loh et al.

Critical Reviews in Biochemistry and Molecular Bio... 2007 10.1080/10409230701597642
[10]
Mittenhall "Exploring the interplay of stability and function in protein evolution" BioEssays (2010) 10.1002/bies.201000038
[11]
Robustness and evolvability in the functional anatomy of a PER-ARNT-SIM (PAS) domain

Andrew F. Philip, Masato Kumauchi, Wouter D. Hoff

Proceedings of the National Academy of Sciences 2010 10.1073/pnas.1004823107
[12]
Taylor, T.J., and Vaisman, I.I. (2000). Discrimination of thermophilic and mesophilic proteins. BMC Struct. Biol., 10. 10.1186/1472-6807-10-s1-s5
[13]
Kim, H., Kim, S., Jung, Y., Han, J., Yun, J.H., Chang, I., and Lee, W. (2016). Probing the folding-unfolding transition of a thermophilic protein. MTH1880. PLoS ONE, 11. 10.1371/journal.pone.0145853
[14]
Ota "The direction of protein evolution is destined by the stability" Biochimie (2018) 10.1016/j.biochi.2018.05.006
[15]
Yang, H., Zhang, Y., Li, X., Bai, Y., Xia, W., Ma, R., Juo, H., Shi, P., and Yao, B. (2018). Impact of disulfide bonds on the folding and refolding capability of a novel thermostable GH45 cellulase. Appl. Microbiol. Biotechnol. 10.1007/s00253-018-9256-2
[17]
Hydrophobic environment is a key factor for the stability of thermophilic proteins

M. Michael Gromiha, Manish C. Pathak, Kadhirvel Saraboji et al.

Proteins: Structure, Function, and Bioinformatics 2013 10.1002/prot.24232
[18]
Takano "Evolvability of thermophilic proteins from archaea and bacteria" Biochemistry (2013) 10.1021/bi400652c
[19]
Structural differences between thermophilic and mesophilic membrane proteins

Alejandro D. Meruelo, Seong Kyu Han, Sanguk Kim et al.

Protein Science 2012 10.1002/pro.2157
[20]
Glyakina "Different packing of external residues can explain differences in the thermostability of proteins from thermophilic and mesophilic organisms" Bioinformatics (2007) 10.1093/bioinformatics/btm345
[21]
Contribution of main chain and side chain atoms and their locations to the stability of thermophilic proteins

Dharma Rao Tompa, K. Saraboji

Journal of Molecular Graphics and Modelling 2016 10.1016/j.jmgm.2016.01.001
[22]
Widespread Disulfide Bonding in Proteins from Thermophilic Archaea

Julien Jorda, Todd O. Yeates

Archaea 2011 10.1155/2011/409156
[23]
Ladenstein "Reconsideration of an early dogma, saying “there is no evidence for disulfide bonds in proteins from archaea”" Extremophiles (2008) 10.1007/s00792-007-0076-z
[24]
Georlette "Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic, and thermophilic DNA ligases" J. Biol. Chem. (2003) 10.1074/jbc.m305142200
[25]
Okada, J., Okamoto, T., Mukaiyama, A., Tadokoro, T., You, D.J., Chon, H., Koga, Y., Takano, K., and Kanaya, S. (2010). Evolution and thermodynamics of the slow unfolding of hyperstable monomeric proteins. BMC Evol. Biol., 10. 10.1186/1471-2148-10-207
[26]
Luke "Thermodyamic stability and folding of proteins from hyperthermophilic organisms" FEBS J. (2007) 10.1111/j.1742-4658.2007.05955.x
[27]
Collins "Activity, stability and flexibility in glycosidases adapted to extreme thermal environments" J. Mol. Biol. (2003) 10.1016/s0022-2836(03)00287-0
[28]
Pica "Shedding light on the extra thermal stability of thermophilic proteins" Biopolymers (2016) 10.1002/bip.22923
[29]
Wintrode "Protein dynamics in a family of laboratory evolved thermophilic enzymes" J. Mol. Biol. (2003) 10.1016/s0022-2836(03)00147-5
[30]
Entropic Stabilization of Proteins and Its Proteomic Consequences

Igor N Berezovsky, William W Chen, Paul J Choi

PLOS Computational Biology 10.1371/journal.pcbi.0010047
[31]
Intense Neutral Drifts Yield Robust and Evolvable Consensus Proteins

Shimon Bershtein, Korina Goldin, Dan S. Tawfik

Journal of Molecular Biology 2008 10.1016/j.jmb.2008.04.024
[32]
Chaperonin overexpression promotes genetic variation and enzyme evolution

Nobuhiko Tokuriki, Dan S. Tawfik

Nature 2009 10.1038/nature08009
[33]
Aledo "Thermodynamic Stability Explains the Differential Evolutionary Dynamics of Cytochrome b and COX I in Mammals" J. Mol. Evol. (2012) 10.1007/s00239-012-9489-0
[34]
Takahasi "A highly stable D-amino oxidase of the thermophilic bacterium rubrobacter xylanophilus" Appl. Environ. Microbiol. (2014) 10.1128/aem.02193-14
[35]
Remy "Cloncal selection and in vivo quantitation of protein interactions with protein-fragment complementation assays" Proc. Natl. Acad. Sci. USA (1999) 10.1073/pnas.96.10.5394
[36]
Nguyen "Thermostability promotes the cooperative function of split adenylate kinases" Protein Eng. Des. Sel. (2008) 10.1093/protein/gzn005
[37]
Nguyen "Mesophilic and hyperthermophilic adenylate kinases differ in their tolerance to random fragmentation" J. Mol. Biol. (2011) 10.1016/j.jmb.2010.11.057
[38]
Kim "Enzyme stabilization by domain insertion into a thermophilic protein" Protein Eng. Des. Sel. (2009) 10.1093/protein/gzp044
[39]
Pierre "Stability of a guest protein depends on stability of a host protein in insertional fusion" Biotechnol. Bioeng. (2011) 10.1002/bit.23039
[40]
Pierre "Molecular determinants for protein stabilization by insertional fusion to a thermophilic host protein" Chembiochem (2015) 10.1002/cbic.201500310
[41]
Shah "Stabilization of bacillus circulans xylanase by combinatorial insertional fusion to a thermophilic host protein" Protein Eng. Des. Sel. (2017)
[42]
Shah "Laboratory evolution of bacillus circulans xylanase inserted into pyrococcus furiosus maltodextrin-binding protein for increased xylanase activity and thermal stability toward alkaline pH" Appl. Biochem. Biotechnol. (2018) 10.1007/s12010-017-2619-9
Metrics
49
Citations
42
References
Details
Published
Sep 25, 2018
Vol/Issue
6(4)
Pages
97
License
View
Funding
National Science Foundation Award: CBET-1134247
Cite This Article
Anthony J. Finch (2018). Thermophilic Proteins as Versatile Scaffolds for Protein Engineering. Microorganisms, 6(4), 97. https://doi.org/10.3390/microorganisms6040097
Related

You May Also Like