Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Review Article

Protein Engineering, a Robust Tool to Engineer Novel Functions in Protein

Author(s): Nancy, Sudarshan Singh Lakhawat, Sanjeev Chandel, Sunil Kumar Jaswal and Pushpender Kumar Sharma*

Volume 30, Issue 7, 2023

Published on: 14 June, 2023

Page: [541 - 551] Pages: 11

DOI: 10.2174/0929866530666230519122612

Price: $65

Abstract

Designing effective diagnostics, biotherapeutics, and biocatalysts are a few interesting potential outcomes of protein engineering. Despite being just a few decades old, the discipline of de novo protein designing has provided a foundation for remarkable outcomes in the pharmaceuticals and enzyme industries. The technologies that will have the biggest impact on current protein therapeutics include engineered natural protein variants, Fc fusion protein, and antibody engineering. Furthermore, designing protein scaffolds can be used in developing next-generation antibodies and in transplanting active sites in the enzyme. The article highlights the important tools and techniques used in protein engineering and their application in the engineering of enzymes and therapeutic proteins. This review further sheds light on the engineering of superoxide dismutase, an enzyme responsible for catalyzing the conversion of superoxide radicals to oxygen and hydrogen peroxide by catalyzing a redox reaction at the metal center while concurrently oxidizing and reducing superoxide free radicals.

Graphical Abstract

[1]
Woolfson, D.N. A brief history of de novo protein design: Minimal, rational, and computational. J. Mol. Biol., 2021, 433(20), 167160.
[http://dx.doi.org/10.1016/j.jmb.2021.167160] [PMID: 34298061]
[2]
Carter, P.J. Introduction to current and future protein therapeutics: A protein engineering perspective. Exp. Cell Res., 2011, 317(9), 1261-1269.
[http://dx.doi.org/10.1016/j.yexcr.2011.02.013] [PMID: 21371474]
[3]
Huang, J.; Zhao, P.; Jin, X.; Wang, Y.; Yuan, H.; Zhu, X. Enzymatic biofuel cells based on protein engineering: Recent advances and future prospects. Biomater. Sci., 2020, 8(19), 5230-5240.
[http://dx.doi.org/10.1039/D0BM00925C] [PMID: 32845259]
[4]
Smoak, M.M.; Mikos, A.G. Advances in biomaterials for skeletal muscle engineering and obstacles still to overcome. Mater. Today Bio, 2020, 7, 100069.
[http://dx.doi.org/10.1016/j.mtbio.2020.100069] [PMID: 32695987]
[5]
Voutilainen, S.; Heinonen, M.; Andberg, M.; Jokinen, E.; Maaheimo, H.; Pääkkönen, J.; Hakulinen, N.; Rouvinen, J.; Lähdesmäki, H.; Kaski, S.; Rousu, J.; Penttilä, M.; Koivula, A. Substrate specificity of 2-deoxy-D-ribose 5-phosphate aldolase (DERA) assessed by different protein engineering and machine learning methods. Appl. Microbiol. Biotechnol., 2020, 104(24), 10515-10529.
[http://dx.doi.org/10.1007/s00253-020-10960-x] [PMID: 33147349]
[6]
Zeuner, B.; Teze, D.; Muschiol, J.; Meyer, A.S. Synthesis of human milk oligosaccharides: Protein engineering strategies for improved enzymatic transglycosylation. Molecules, 2019, 24(11), 2033.
[http://dx.doi.org/10.3390/molecules24112033] [PMID: 31141914]
[7]
Bernal, C.; Rodríguez, K.; Martínez, R. Integrating enzyme immobilization and protein engineering: An alternative path for the development of novel and improved industrial biocatalysts. Biotechnol. Adv., 2018, 36(5), 1470-1480.
[http://dx.doi.org/10.1016/j.biotechadv.2018.06.002] [PMID: 29894813]
[8]
Qu, G.; Li, A.; Acevedo-Rocha, C.G.; Sun, Z.; Reetz, M.T. The crucial role of methodology development in directed evolution of selective enzymes. Angew. Chem. Int. Ed., 2020, 59(32), 13204-13231.
[http://dx.doi.org/10.1002/anie.201901491] [PMID: 31267627]
[9]
Sinha, R.; Shukla, P. Current trends in protein engineering: Updates and progress. Curr. Protein Pept. Sci., 2019, 20(5), 398-407.
[http://dx.doi.org/10.2174/1389203720666181119120120] [PMID: 30451109]
[10]
Podar, M.; Eads, J.R.; Richardson, T.H. Evolution of a microbial nitrilase gene family: A comparative and environmental genomics study. BMC Evol. Biol., 2005, 5(1), 42.
[http://dx.doi.org/10.1186/1471-2148-5-42] [PMID: 16083508]
[11]
Sugaya, K.; Yasuda, S.; Sato, S.; Sisi, C.; Yamamoto, T.; Umeno, D.; Matsuura, T.; Hayashi, T.; Ogasawara, S.; Kinoshita, M.; Murata, T. A methodology for creating thermostabilized mutants of G‐protein coupled receptors by combining statistical thermodynamics and evolutionary molecular engineering. Protein Sci., 2022, 31(9), e4404.
[http://dx.doi.org/10.1002/pro.4404]
[12]
Rodríguez-Núñez, K.; Bernal, C.; Martínez, R. Immobilized Biocatalyst Engineering: High throughput enzyme immobilization for the integration of biocatalyst improvement strategies. Int. J. Biol. Macromol., 2021, 170, 61-70.
[http://dx.doi.org/10.1016/j.ijbiomac.2020.12.097] [PMID: 33358947]
[13]
Woodley, J.M. Protein engineering of enzymes for process applications. Curr. Opin. Chem. Biol., 2013, 17(2), 310-316.
[http://dx.doi.org/10.1016/j.cbpa.2013.03.017] [PMID: 23562542]
[14]
Madhavan, A.; Arun, K.B.; Binod, P.; Sirohi, R.; Tarafdar, A.; Reshmy, R.; Kumar Awasthi, M.; Sindhu, R. Design of novel enzyme biocatalysts for industrial bioprocess: Harnessing the power of protein engineering, high throughput screening and synthetic biology. Bioresour. Technol., 2021, 325, 124617.
[http://dx.doi.org/10.1016/j.biortech.2020.124617] [PMID: 33450638]
[15]
Galán, A.; Comor, L.; Horvatić, A.; Kuleš, J.; Guillemin, N.; Mrljak, V.; Bhide, M. Library-based display technologies: Where do we stand? Mol. Biosyst., 2016, 12(8), 2342-2358.
[http://dx.doi.org/10.1039/C6MB00219F] [PMID: 27306919]
[16]
Soni, S. Trends in lipase engineering for enhanced biocatalysis. Biotechnol. Appl. Biochem., 2022, 69(1), 265-272.
[http://dx.doi.org/10.1002/bab.2105] [PMID: 33438779]
[17]
Scott, B.M.; Sheffield, W.P. Engineering the serpin α 1 ‐antitrypsin: A diversity of goals and techniques. Protein Sci., 2020, 29(4), 856-871.
[http://dx.doi.org/10.1002/pro.3794] [PMID: 31774589]
[18]
Trovão, M.; Schüler, L.M.; Machado, A.; Bombo, G.; Navalho, S.; Barros, A.; Pereira, H.; Silva, J.; Freitas, F.; Varela, J. Random mutagenesis as a promising tool for microalgal strain improvement towards industrial production. Mar. Drugs, 2022, 20(7), 440.
[http://dx.doi.org/10.3390/md20070440] [PMID: 35877733]
[19]
Karunarathna, N.L.; Patiranage, D.S.R.; Harloff, H.J.; Sashidhar, N.; Jung, C. Genomic background selection to reduce the mutation load after random mutagenesis. Sci. Rep., 2021, 11(1), 19404.
[http://dx.doi.org/10.1038/s41598-021-98934-5] [PMID: 34593904]
[20]
Zeymer, C.; Hilvert, D. Directed evolution of protein catalysts. Annu. Rev. Biochem., 2018, 87(1), 131-157.
[http://dx.doi.org/10.1146/annurev-biochem-062917-012034] [PMID: 29494241]
[21]
Lopez, R.; Chen, Y.J.; Dumas Ang, S.; Yekhanin, S.; Makarychev, K.; Racz, M.Z.; Seelig, G.; Strauss, K.; Ceze, L. DNA assembly for nanopore data storage readout. Nat. Commun., 2019, 10(1), 2933.
[http://dx.doi.org/10.1038/s41467-019-10978-4] [PMID: 31270330]
[22]
Zuo, E.; Sun, Y.; Yuan, T.; He, B.; Zhou, C.; Ying, W.; Liu, J.; Wei, W.; Zeng, R.; Li, Y.; Yang, H. A rationally engineered cytosine base editor retains high on-target activity while reducing both DNA and RNA off-target effects. Nat. Methods, 2020, 17(6), 600-604.
[http://dx.doi.org/10.1038/s41592-020-0832-x] [PMID: 32424272]
[23]
Weinstein, J.A.; Regev, A.; Zhang, F. DNA microscopy: Optics-free spatio-genetic imaging by a stand-alone chemical reaction. Cell, 2019, 178(1), 229-241.e16.
[http://dx.doi.org/10.1016/j.cell.2019.05.019] [PMID: 31230717]
[24]
Guo, J.; Bolduc, B.; Zayed, A.A.; Varsani, A.; Dominguez-Huerta, G.; Delmont, T.O.; Pratama, A.A.; Gazitúa, M.C.; Vik, D.; Sullivan, M.B.; Roux, S. VirSorter2: A multi-classifier, expert-guided approach to detect diverse DNA and RNA viruses. Microbiome, 2021, 9(1), 37.
[http://dx.doi.org/10.1186/s40168-020-00990-y] [PMID: 33522966]
[25]
Jain, P.C.; Varadarajan, R. A rapid, efficient, and economical inverse polymerase chain reaction-based method for generating a site saturation mutant library. Anal. Biochem., 2014, 449, 90-98.
[http://dx.doi.org/10.1016/j.ab.2013.12.002] [PMID: 24333246]
[26]
Fagone, P.; Wright, J.F.; Nathwani, A.C.; Nienhuis, A.W.; Davidoff, A.M.; Gray, J.T. Systemic errors in quantitative polymerase chain reaction titration of self-complementary adeno-associated viral vectors and improved alternative methods. Hum. Gene Ther. Methods, 2012, 23(1), 1-7.
[http://dx.doi.org/10.1089/hgtb.2011.104] [PMID: 22428975]
[27]
Corman, V.M.; Eckerle, I.; Bleicker, T.; Zaki, A.; Landt, O.; Eschbach-Bludau, M.; van Boheemen, S.; Gopal, R.; Ballhause, M.; Bestebroer, T.M.; Muth, D.; Müller, M.A.; Drexler, J.F.; Zambon, M.; Osterhaus, A.D.; Fouchier, R.M.; Drosten, C. Detection of a novel human coronavirus by real-time reverse-transcription polymerase chain reaction. Euro Surveill., 2012, 17(39), 20285.
[http://dx.doi.org/10.2807/ese.17.39.20285-en] [PMID: 23041020]
[28]
Brittain-Long, R.; Andersson, L.M.; Olofsson, S.; Lindh, M.; Westin, J. Seasonal variations of 15 respiratory agents illustrated by the application of a multiplex polymerase chain reaction assay. Scand. J. Infect. Dis., 2012, 44(1), 9-17.
[http://dx.doi.org/10.3109/00365548.2011.598876] [PMID: 21867470]
[29]
Motohashi, K. A simple and efficient seamless DNA cloning method using SLiCE from Escherichia coli laboratory strains and its application to SLiP site-directed mutagenesis. BMC Biotechnol., 2015, 15(1), 47.
[http://dx.doi.org/10.1186/s12896-015-0162-8] [PMID: 26037246]
[30]
Hayakijkosol, O.; Jaroenram, W.; Owens, L.; Elliman, J. Reverse transcription polymerase chain reaction (RT-PCR) detection for Australian Cherax reovirus from redclaw crayfish (Cherax quadricarinatus). Aquaculture, 2021, 530, 735881.
[http://dx.doi.org/10.1016/j.aquaculture.2020.735881]
[31]
Yang, H.; Swartz, A.M.; Park, H.J.; Srivastava, P.; Ellis-Guardiola, K.; Upp, D.M.; Lee, G.; Belsare, K.; Gu, Y.; Zhang, C.; Moellering, R.E.; Lewis, J.C. Evolving artificial metalloenzymes via random mutagenesis. Nat. Chem., 2018, 10(3), 318-324.
[http://dx.doi.org/10.1038/nchem.2927] [PMID: 29461523]
[32]
Li, A.; Qu, G.; Sun, Z.; Reetz, M.T. Statistical analysis of the benefits of focused saturation mutagenesis in directed evolution based on reduced amino acid alphabets. ACS Catal., 2019, 9(9), 7769-7778.
[http://dx.doi.org/10.1021/acscatal.9b02548]
[33]
Cozens, C.; Pinheiro, V.B. Darwin Assembly: Fast, efficient, multi-site bespoke mutagenesis. Nucleic Acids Res., 2018, 46(8), e51-e51.
[http://dx.doi.org/10.1093/nar/gky067] [PMID: 29409059]
[34]
Wang, H.; Bian, X.; Xia, L.; Ding, X.; Müller, R.; Zhang, Y.; Fu, J.; Stewart, A.F. Improved seamless mutagenesis by recombineering using ccdB for counterselection. Nucleic Acids Res., 2014, 42(5), e37-e37.
[http://dx.doi.org/10.1093/nar/gkt1339] [PMID: 24369425]
[35]
Pacher, M.; Puchta, H. From classical mutagenesis to nuclease‐based breeding–directing natural DNA repair for a natural end‐product. The Plant J., 2017, 90(4), 819-833.
[http://dx.doi.org/10.1111/tpj.13469]
[36]
Song, J.; Yang, Q.; Lv, F.; Liu, L.; Wang, S. Visual detection of DNA mutation using multicolor fluorescent coding. ACS Appl. Mater. Interfaces, 2012, 4(6), 2885-2890.
[http://dx.doi.org/10.1021/am300830r] [PMID: 22698148]
[37]
Yang, W.; Han, L.; Mandlaa, M.; Zhang, H.; Zhang, Z.; Xu, H. A plate method for rapid screening of Ketogulonicigenium vulgare mutants for enhanced 2-keto- l -gulonic acid production. Braz. J. Microbiol., 2017, 48(3), 397-402.
[http://dx.doi.org/10.1016/j.bjm.2017.02.002] [PMID: 28292630]
[38]
de Carlos Cáceres, I.; Porto, D.A.; Gallotta, I.; Santonicola, P.; Rodríguez-Cordero, J.; Di Schiavi, E.; Lu, H. Automated screening of C. elegans neurodegeneration mutants enabled by microfluidics and image analysis algorithms. Integr. Biol., 2018, 10(9), 539-548.
[http://dx.doi.org/10.1039/C8IB00091C] [PMID: 30116818]
[39]
Fürst, M.J.L.J.; Martin, C.; Lončar, N.; Fraaije, M.W. Experimental protocols for generating focused mutant libraries and screening for thermostable proteins. Methods Enzymol., 2018, 608, 151-187.
[40]
Salazar, O; Sun, L Evaluating a screen and analysis of mutant libraries. Methods Mol Biol., 2003, 230, 85-97.
[http://dx.doi.org/10.1385/1-59259-396-8:85]
[41]
Czajkowsky, D.M.; Hu, J.; Shao, Z.; Pleass, R.J. Fc‐fusion proteins: New developments and future perspectives. EMBO Mol. Med., 2012, 4(10), 1015-1028.
[http://dx.doi.org/10.1002/emmm.201201379] [PMID: 22837174]
[42]
Beck, A.; Reichert, J.M. Therapeutic Fc-fusion proteins and peptides as successful alternatives to antibodies. MAbs., 2011, 3(5), 415-416.
[http://dx.doi.org/10.4161/mabs.3.5.17334]
[43]
Benjamin, W.U.; Sun, Y.N. Pharmacokinetics of Peptide-Fc fusion proteins. J. Pharm. Sci., 2014, 103(1), 53-64.
[http://dx.doi.org/10.1002/jps.23783] [PMID: 24285510]
[44]
Mihara, M.; Komachiya, M.; Arai, A.; Kawahara, Y.; Okubo, Y.; Yamakura, F.; Hirooka, Y. Preference for threonine over serine near the active site metal of superoxide dismutase in Porphyromonas gingivalis: Effect of Gly 155 to Ser mutation. J Matsumoto Dent Univ Soc., 2021, 46(2), 59-69.
[45]
Lua, W.H.; Ling, W.L.; Yeo, J.Y.; Poh, J.J.; Lane, D.P.; Gan, S.K.E. The effects of antibody engineering CH and CL in Trastuzumab and Pertuzumab recombinant models: Impact on antibody production and antigen-binding. Sci. Rep., 2018, 8(1), 1-9.
[PMID: 29311619]
[46]
Sulea, T.; Rohani, N.; Baardsnes, J.; Corbeil, C.R.; Deprez, C.; Cepero-Donates, Y.; Robert, A.; Schrag, J.D.; Parat, M.; Duchesne, M. Structure-based engineering of pH-dependent antibody binding for selective targeting of solid-tumor microenvironment. MAbs., 2020, 12(1), 1682866.
[http://dx.doi.org/10.1080/19420862.2019.1682866]
[47]
Nelson, A.L. Antibody fragments: Hope and hype. MAbs., 2010, 2(1), 77-83.
[48]
Wong, S.L.; Ye, R.; Nathoo, S. Engineering and production of streptokinase in a Bacillus subtilis expression-secretion system. Appl. Environ. Microbiol., 1994, 60(2), 517-523.
[http://dx.doi.org/10.1128/aem.60.2.517-523.1994] [PMID: 8135514]
[49]
Stuebner, K.; Boschke, E.; Wolf, K.H.; Langer, J. Kinetic analysis and modelling of streptokinase fermentation. Acta Biotechnol., 1991, 11(5), 467-477.
[http://dx.doi.org/10.1002/abio.370110511]
[50]
Aslanabadi, N.; Safaie, N.; Talebi, F.; Dousti, S.; Entezari-Maleki, T. The streptokinase therapy complications and its associated risk factors in patients with acute ST elevation myocardial infarction. Iran. J. Pharm. Res., 2018, 17(Suppl.), 53-63.
[PMID: 29796029]
[51]
Gera, S.; Sant, D.; Haider, S.; Korkmaz, F.; Kuo, T.C.; Mathew, M.; Perez-Pena, H.; Xie, H.; Chen, H.; Batista, R.; Ma, K.; Cheng, Z.; Hadelia, E.; Robinson, C.; Macdonald, A.; Miyashita, S.; Williams, A.; Jebian, G.; Miyashita, H.; Gumerova, A.; Ievleva, K.; Smith, P.; He, J.; Ryu, V.; DeMambro, V.; Quinn, M.A.; Meseck, M.; Kim, S.M.; Kumar, T.R.; Iqbal, J.; New, M.I.; Lizneva, D.; Rosen, C.J.; Hsueh, A.J.; Yuen, T.; Zaidi, M. First-in-class humanized FSH blocking antibody targets bone and fat. Proc. Natl. Acad. Sci. USA, 2020, 117(46), 28971-28979.
[http://dx.doi.org/10.1073/pnas.2014588117] [PMID: 33127753]
[52]
Lin, L.; Hu, K. Tissue plasminogen activator: Side effects and signaling. J. Drug Res., 2014, 1(1), 1001.
[PMID: 25879083]
[53]
Semba, C.P.; Sugimoto, K.; Razavi, M.K. Alteplase and tenecteplase: Applications in the peripheral circulation. Tech. Vasc. Interv. Radiol., 2001, 4(2), 99-106.
[http://dx.doi.org/10.1016/S1089-2516(01)90003-4] [PMID: 11981795]
[54]
Liu, M.; White, B.F.; Praveen, P.; Li, W.; Lin, F.; Wu, H.; Li, R.; Delaine, C.; Forbes, B.E.; Wade, J.D.; Hossain, M.A. Engineering of a biologically active insulin dimer. J. Med. Chem., 2021, 64(23), 17448-17454.
[http://dx.doi.org/10.1021/acs.jmedchem.1c01594] [PMID: 34797669]
[55]
Kim, Y.G.; Baltabekova, A.Z.; Zhiyenbay, E.E.; Aksambayeva, A.S.; Shagyrova, Z.S.; Khannanov, R.; Ramanculov, E.M.; Shustov, A.V. Recombinant Vaccinia virus-coded interferon inhibitor B18R: Expression, refolding and a use in a mammalian expression system with a RNA-vector. PLoS One, 2017, 12(12), e0189308.
[http://dx.doi.org/10.1371/journal.pone.0189308] [PMID: 29216299]
[56]
Liu, L.; Yu, H.; Huang, X.; Tan, H.; Li, S.; Luo, Y.; Zhang, L.; Jiang, S.; Jia, H.; Xiong, Y.; Zhang, R.; Huang, Y.; Chu, C.C.; Tian, W. A novel engineered VEGF blocker with an excellent pharmacokinetic profile and robust anti-tumor activity. BMC Cancer, 2015, 15(1), 170.
[http://dx.doi.org/10.1186/s12885-015-1140-1] [PMID: 25881012]
[57]
Leonard, J.P.; Rosenblatt, J.D.; Bartlett, N.L.; Gopal, A.; Younes, A.; Fisher, D.; Foss, F.; Forero, A.; Bernstein, S.; Cheson, B. A Phase II study of SGN-30 (anti-CD30 mAb) in Hodgkin lymphoma or systemic anaplastic large cell lymphoma. Br J Haematol., 2004, 146(2), 171-9.
[58]
Saqr, A.; Vakili, M.R.; Huang, Y.H.; Lai, R.; Lavasanifar, A. Development of Traceable Rituximab-Modified PEO-Polyester Micelles by Postinsertion of PEG-phospholipids for Targeting of B-cell Lymphoma. ACS Omega, 2019, 4(20), 18867-18879.
[http://dx.doi.org/10.1021/acsomega.9b02910] [PMID: 31737848]
[59]
Burke, T.J.; Segrin, C. Examining diet- and exercise-related communication in romantic relationships: Associations with health behaviors. Health Commun., 2014, 29(9), 877-887.
[http://dx.doi.org/10.1080/10410236.2013.811625] [PMID: 24295060]
[60]
Zhou, Q.; Chen, V.; Shannon, C.P.; Wei, X.S.; Xiang, X.; Wang, X.; Wang, Z.H.; Tebbutt, S.J.; Kollmann, T.R.; Fish, E.N. Interferon-α2b treatment for COVID-19. Front. Immunol., 2020, 11, 1061.
[http://dx.doi.org/10.3389/fimmu.2020.01061] [PMID: 32574262]
[61]
Asmana Ningrum, R. Human interferon alpha-2b: A therapeutic protein for cancer treatment. Scientifica, 2014, 2014, 970315.
[http://dx.doi.org/10.1155/2014/970315]
[62]
Gebauer, M.; Skerra, A. Engineered protein scaffolds as next-generation therapeutics. Annu. Rev. Pharmacol. Toxicol., 2020, 60(1), 391-415.
[http://dx.doi.org/10.1146/annurev-pharmtox-010818-021118] [PMID: 31914898]
[63]
Liu, Z.; Cao, S.; Liu, M.; Kang, W.; Xia, J. Self-assembled multienzyme nanostructures on synthetic protein scaffolds. ACS Nano, 2019, 13(10), 11343-11352.
[http://dx.doi.org/10.1021/acsnano.9b04554] [PMID: 31498583]
[64]
Singh, R.; Tiwari, M.; Singh, R.; Lee, J.K. From protein engineering to immobilization: Promising strategies for the upgrade of industrial enzymes. Int. J. Mol. Sci., 2013, 14(1), 1232-1277.
[http://dx.doi.org/10.3390/ijms14011232] [PMID: 23306150]
[65]
Hirokawa, K.; Ichiyanagi, A.; Kajiyama, N. Enhancement of thermostability of fungal deglycating enzymes by directed evolution. Appl. Microbiol. Biotechnol., 2008, 78(5), 775-781.
[http://dx.doi.org/10.1007/s00253-008-1363-z] [PMID: 18246344]
[66]
Bradley, R.; Braybrooke, J.; Gray, R.; Hills, R.; Liu, Z.; Peto, R.; Davies, L.; Dodwell, D.; McGale, P.; Pan, H.; Taylor, C.; Anderson, S.; Gelber, R.; Gianni, L.; Jacot, W.; Joensuu, H.; Moreno-Aspitia, A.; Piccart, M.; Press, M.; Romond, E.; Slamon, D.; Suman, V.; Berry, R.; Boddington, C.; Clarke, M.; Davies, C.; Duane, F.; Evans, V.; Gay, J.; Gettins, L.; Godwin, J.; James, S.; Liu, H.; MacKinnon, E.; Mannu, G.; McHugh, T.; Morris, P.; Read, S.; Straiton, E.; Wang, Y.; Crown, J.; de Azambuja, E.; Delaloge, S.; Fung, H.; Geyer, C.; Spielmann, M.; Valagussa, P.; Albain, K.; Anderson, S.; Arriagada, R.; Bartlett, J.; Bergsten-Nordström, E.; Bliss, J.; Brain, E.; Carey, L.; Coleman, R.; Cuzick, J.; Davidson, N.; Del Mastro, L.; Di Leo, A.; Dignam, J.; Dowsett, M.; Ejlertsen, B.; Francis, P.; Gnant, M.; Goetz, M.; Goodwin, P.; Halpin-Murphy, P.; Hayes, D.; Hill, C.; Jagsi, R.; Janni, W.; Loibl, S.; Mamounas, E.P.; Martín, M.; Mukai, H.; Nekljudova, V.; Norton, L.; Ohashi, Y.; Pierce, L.; Poortmans, P.; Raina, V.; Rea, D.; Regan, M.; Robertson, J.; Rutgers, E.; Spanic, T.; Sparano, J.; Steger, G.; Tang, G.; Toi, M.; Tutt, A.; Viale, G.; Wang, X.; Whelan, T.; Wilcken, N.; Wolmark, N.; Cameron, D.; Bergh, J.; Pritchard, K.I.; Swain, S.M. Trastuzumab for early-stage, HER2-positive breast cancer: A meta-analysis of 13 864 women in seven randomised trials. Lancet Oncol., 2021, 22(8), 1139-1150.
[http://dx.doi.org/10.1016/S1470-2045(21)00288-6] [PMID: 34339645]
[67]
Guo, Z.; Murphy, L.; Stein, V.; Johnston, W.A.; Alcala-Perez, S.; Alexandrov, K. Engineered PQQ-glucose dehydrogenase as a universal biosensor platform. J. Am. Chem. Soc., 2016, 138(32), 10108-10111.
[http://dx.doi.org/10.1021/jacs.6b06342] [PMID: 27463000]
[68]
Xie, W.; Bülow, L.; Xie, B. Pyrroloquinoline quinone glucose dehydrogenase adopted in thermometric analysis for enhancement of glucose determination. J. Therm. Anal. Calorim., 2018, 134(3), 1913-1919.
[http://dx.doi.org/10.1007/s10973-018-7273-0]
[69]
Kumar, A.; Dutt, S.; Bagler, G.; Ahuja, P.S.; Kumar, S. Engineering a thermo-stable superoxide dismutase functional at sub-zero to >50°C, which also tolerates autoclaving. Sci. Rep., 2012, 2(1), 387.
[http://dx.doi.org/10.1038/srep00387]
[70]
Chen, Y.; Toth, E.A.; Ruan, B.; Choi, E.J.; Simmerman, R.; Chen, Y.; He, Y.; Wang, R.; Godoy-Ruiz, R.; King, H.; Custer, G.; Travis Gallagher, D.; Rozak, D.A.; Solomon, M.; Muro, S.; Weber, D.J.; Orban, J.; Fuerst, T.R.; Bryan, P.N. Engineering subtilisin proteases that specifically degrade active RAS. Commun. Biol., 2021, 4(1), 299.
[http://dx.doi.org/10.1038/s42003-021-01818-7] [PMID: 33674772]
[71]
Li, M.; Guo, S.; Li, X.; Wang, Q.; Zhu, L.; Yin, C.; Wang, W. Engineering a highly thermostable and stress tolerant superoxide dismutase by N-terminal modification and metal incorporation. Biotechnol. Bioprocess Eng., 2017, 22(6), 725-733.
[http://dx.doi.org/10.1007/s12257-017-0243-8]
[72]
Wu, T.; Huang, S.; Yang, H.; Ye, N.; Tong, L.; Chen, G.; Zhou, Q.; Ouyang, G. Bimetal biomimetic engineering utilizing metal–organic frameworks for superoxide dismutase mimic. ACS Materials Letters, 2022, 4(4), 751-757.
[http://dx.doi.org/10.1021/acsmaterialslett.2c00075]
[73]
Zhang, Y.; Wu, Y.Q.; Xu, N.; Zhao, Q.; Yu, H.L.; Xu, J.H. Engineering of cyclohexanone monooxygenase for the enantioselective synthesis of (S)-omeprazole. ACS Sustain. Chem.& Eng., 2019, 7(7), 7218-7226.
[http://dx.doi.org/10.1021/acssuschemeng.9b00224]
[74]
van Beek, H.L.; Romero, E.; Fraaije, M.W. Engineering cyclohexanone monooxygenase for the production of methyl propanoate. ACS Chem. Biol., 2017, 12(1), 291-299.
[http://dx.doi.org/10.1021/acschembio.6b00965] [PMID: 27935281]
[75]
Heine, T.; Tucker, K.; Okonkwo, N.; Assefa, B.; Conrad, C.; Scholtissek, A.; Schlömann, M.; Gassner, G.; Tischler, D. Engineering styrene monooxygenase for biocatalysis: Reductase-epoxidase fusion proteins. Appl. Biochem. Biotechnol., 2017, 181(4), 1590-1610.
[http://dx.doi.org/10.1007/s12010-016-2304-4] [PMID: 27830466]
[76]
Gong, X.M.; Qin, Z.; Li, F.L.; Zeng, B.B.; Zheng, G.W.; Xu, J.H. Development of an engineered ketoreductase with simultaneously improved thermostability and activity for making a bulky atorvastatin precursor. ACS Catal., 2019, 9(1), 147-153.
[http://dx.doi.org/10.1021/acscatal.8b03382]
[77]
Barski, O.A.; Tipparaju, S.M.; Bhatnagar, A. The aldo-keto reductase superfamily and its role in drug metabolism and detoxification. Drug Metab. Rev., 2008, 40(4), 553-624.
[http://dx.doi.org/10.1080/03602530802431439] [PMID: 18949601]
[78]
Qin, F.; Qin, B.; Mori, T.; Wang, Y.; Meng, L.; Zhang, X.; Jia, X.; Abe, I.; You, S. Engineering of Candida glabrata ketoreductase 1 for asymmetric reduction of α-halo ketones. ACS Catal., 2016, 6(9), 6135-6140.
[http://dx.doi.org/10.1021/acscatal.6b01552]
[79]
Xie, X.; Ban, X.; Gu, Z.; Li, C.; Hong, Y.; Cheng, L.; Li, Z. Structure-based engineering of a maltooligosaccharide-forming amylase to enhance product specificity. J. Agric. Food Chem., 2020, 68(3), 838-844.
[http://dx.doi.org/10.1021/acs.jafc.9b07234] [PMID: 31896254]
[80]
Park, J.; Kim, J. Secretion of the iron containing superoxide dismutase of Streptomyces subrutilus P5. Misaengmul Hakhoe Chi, 2015, 51(2), 108-114.
[http://dx.doi.org/10.7845/kjm.2015.5019]
[81]
Wang, Y.; Branicky, R.; Noë, A.; Hekimi, S. Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. J. Cell Biol., 2018, 217(6), 1915-1928.
[http://dx.doi.org/10.1083/jcb.201708007] [PMID: 29669742]
[82]
Che, M.; Wang, R.; Li, X.; Wang, H.Y.; Zheng, X.F.S. Expanding roles of superoxide dismutases in cell regulation and cancer. Drug Discov. Today, 2016, 21(1), 143-149.
[http://dx.doi.org/10.1016/j.drudis.2015.10.001] [PMID: 26475962]
[83]
Bresciani, G.; da Cruz, I.B.M.; González-Gallego, J. Manganese superoxide dismutase and oxidative stress modulation. Adv. Clin. Chem., 2015, 68, 87-130.
[http://dx.doi.org/10.1016/bs.acc.2014.11.001] [PMID: 25858870]
[84]
Beyer, W.; Imlay, J.; Fridovich, I. Superoxide Dismutases. Prog. Nucleic Acid Res. Mol. Biol., 1991, 40, 221-253.
[http://dx.doi.org/10.1016/S0079-6603(08)60843-0] [PMID: 1851570]
[85]
Okado-Matsumoto, A.; Fridovich, I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J. Biol. Chem., 2001, 276(42), 38388-38393.
[http://dx.doi.org/10.1074/jbc.M105395200] [PMID: 11507097]
[86]
Mondola, P.; Damiano, S.; Sasso, A.; Santillo, M. The Cu, Zn superoxide dismutase: Not only a dismutase enzyme. Front. Physiol., 2016, 7, 594.
[http://dx.doi.org/10.3389/fphys.2016.00594] [PMID: 27965593]
[87]
Rosa, A.C.; Corsi, D.; Cavi, N.; Bruni, N.; Dosio, F. Superoxide dismutase administration: A review of proposed human uses. Molecules, 2021, 26(7), 1844.
[http://dx.doi.org/10.3390/molecules26071844] [PMID: 33805942]
[88]
Houmani, H.; Rodríguez-Ruiz, M.; Palma, J.M.; Abdelly, C.; Corpas, F.J. Modulation of superoxide dismutase (SOD) isozymes by organ development and high long-term salinity in the halophyte Cakile maritima. Protoplasma, 2016, 253(3), 885-894.
[http://dx.doi.org/10.1007/s00709-015-0850-1] [PMID: 26159565]
[89]
Zhou, Y; Hu, L; Wu, H; Jiang, L; Liu, S Genome-wide identification and transcriptional expression analysis of cucumber superoxide dismutase (SOD) family in response to various abiotic stresses. Int J Genomics., 2017, 2017(9), 7243973.
[90]
Gabbianelli, R.; Battistoni, A.; Polticelli, F.; Meier, B.; Schmidt, M.; Rotilio, G.; Desideri, A. Effect of Lys175 mutation on structure function properties of Propionibacterium shermanii superoxide dismutase. Protein Eng. Des. Sel., 1997, 10(9), 1067-1070.
[http://dx.doi.org/10.1093/protein/10.9.1067] [PMID: 9464571]
[91]
Bonetta, R.; Hunter, G.J.; Trinh, C.H.; Borowski, T.; Fenech, A.G.; Kulp, M.; Tabares, L.C.; Un, S.; Hunter, T. Substitution of histidine 30 by asparagine in manganese superoxide dismutase alters biophysical properties and supports proliferation in a K562 leukemia cell line. Eur. Biophys. J., 2021, 50(3-4), 571-585.
[http://dx.doi.org/10.1007/s00249-021-01544-2] [PMID: 34021366]
[92]
Kumar, S.; Bhardwaj, V.K.; Guleria, S.; Purohit, R.; Kumar, S. Improving the catalytic efficiency and dimeric stability of Cu,Zn superoxide dismutase by combining structure-guided consensus approach with site-directed mutagenesis. Biochim. Biophys. Acta Bioenerg., 2022, 1863(1), 148505.
[http://dx.doi.org/10.1016/j.bbabio.2021.148505] [PMID: 34626596]
[93]
Liu, J.; Wei, B.; Che, C.; Gong, Z.; Jiang, Y.; Si, M.; Zhang, J.; Yang, G. Enhanced stability of manganese superoxide dismutase by amino acid replacement designed via molecular dynamics simulation. Int. J. Biol. Macromol., 2019, 128, 297-303.
[http://dx.doi.org/10.1016/j.ijbiomac.2019.01.126] [PMID: 30685308]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy