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Research Article

Understanding the basis of thermostability for enzyme “Nanoluc” towards designing industry-competent engineered variants

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Received 26 Oct 2023, Accepted 12 Feb 2024, Published online: 28 Feb 2024

References

  • Alhumaydhi, F. A., Aljasir, M. A., Aljohani, A. S., Alsagaby, S. A., Alwashmi, A. S., Shahwan, M., Hassan, M. I., Islam, A., & Shamsi, A. (2021). Probing the interaction of memantine, an important Alzheimer’s drug, with human serum albumin: In silico and in vitro approach. Journal of Molecular Liquids, 340, 116888. https://doi.org/10.1016/j.molliq.2021.116888
  • Bateman, A. (2019). UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47, D506–D515.
  • Behera, K., Wani, F. A., Bhat, A. R., Juneja, S., Banjare, M. K., Pandey, S., & Patel, R. (2021). Behavior of lysozyme within ionic liquid-in-water microemulsions. Journal of Molecular Liquids, 326, 115350. https://doi.org/10.1016/j.molliq.2021.115350
  • Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., & Hermans, J. (1981). Interaction Models for Water in Relation to Protein Hydration. Intermolecular Forces: proceedings of the Fourteenth Jerusalem Symposium on Quantum Chemistry and Biochemistry Held in Jerusalem, April 331–342.
  • Berman, H., Henrick, K., & Nakamura, H. (2003). Announcing the worldwide Protein Data Bank. Nature Structural Biology, 10(12), 980–980. https://doi.org/10.1038/nsb1203-980
  • Bharatiy, S. K., Hazra, M., Paul, M., Mohapatra, S., Samantaray, D., Dubey, R. C., Sanyal, S., Datta, S., & Hazra, S. (2016). In silico designing of an industrially sustainable carbonic anhydrase using molecular dynamics simulation. ACS Omega, 1(6), 1081–1103. https://doi.org/10.1021/acsomega.6b00041
  • Bhattacharya, S., Junghare, V., Pandey, N. K., Ghosh, D., Patra, H., & Hazra, S. (2020). An insight into the complete biophysical and biochemical characterization of novel class A beta-lactamase (Bla1) from Bacillus anthracis. International Journal of Biological Macromolecules, 145, 510–526. https://doi.org/10.1016/j.ijbiomac.2019.12.136
  • Borders, C. L., Broadwater, J. A., Bekeny, P. A., Salmon, J. E., Lee, A. S., Eldridge, A. M., & Pett, V. B. (1994). A structural role for arginine in proteins: multiple hydrogen bonds to backbone carbonyl oxygens. Protein Science : a Publication of the Protein Society, 3(4), 541–548. https://doi.org/10.1002/pro.5560030402 8003972
  • Boyle, R. (1666). New experiments concerning the relation between light and air (in shining wood and fish;) made by the honourable Robert Boyle, and by him addressed from Oxford to the publisher, and so communicated to the Royal Society. Philosophical Transactions of the Royal Society of London, 2(31), 581–600.
  • Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. Journal of Chemical Physics, 126, 14101.
  • Darden, T., Perera, L., Li, L., & Pedersen, L. (1999). New tricks for modelers from the crystallography toolkit: The particle mesh Ewald algorithm and its use in nucleic acid simulations. Structure (London, England: 1993), 7(3), R55–R60. https://doi.org/10.1016/s0969-2126(99)80033-1
  • Dixon, A. S., Schwinn, M. K., Hall, M. P., Zimmerman, K., Otto, P., Lubben, T. H., Butler, B. L., Binkowski, B. F., Machleidt, T., Kirkland, T. A., Wood, M. G., Eggers, C. T., Encell, L. P., & Wood, K. V. (2016). NanoLuc complementation reporter optimized for accurate measurement of protein interactions in cells. ACS Chemical Biology, 11(2), 400–408. https://doi.org/10.1021/acschembio.5b00753
  • Durham, E., Dorr, B., Woetzel, N., Staritzbichler, R., & Meiler, J. (2009). Solvent accessible surface area approximations for rapid and accurate protein structure prediction. Journal of Molecular Modeling, 15(9), 1093–1108. https://doi.org/10.1007/s00894-009-0454-9
  • Fanaei Kahrani, Z., Emamzadeh, R., Nazari, M., & Rasa, S. M. M. (2017). Molecular basis of thermostability enhancement of Renilla luciferase at higher temperatures by insertion of a disulfide bridge into the structure. Biochimica et Biophysica Acta. Proteins and Proteomics, 1865(2), 252–259. https://doi.org/10.1016/j.bbapap.2016.11.004
  • Ferruz, N., Schmidt, S., & Höcker, B. (2021). ProteinTools: A toolkit to analyze protein structures. Nucleic Acids Research, 49(W1), W559–W566. https://doi.org/10.1093/nar/gkab375
  • Gallivan, J. P., & Dougherty, D. A. (1999). Cation-π interactions in structural biology. Proceedings of the National Academy of Sciences of the United States of America, 96(17), 9459–9464. https://doi.org/10.1073/pnas.96.17.9459
  • Gibbons, A. E., Luker, K. E., & Luker, G. D. (2018). Dual reporter bioluminescence imaging with NanoLuc and firefly luciferase. Methods in Molecular Biology (Clifton, N.J.), 1790, 41–50. https://doi.org/10.1007/978-1-4939-7860-1_4
  • Haghdoust, F., Molakarimi, M., Mirshahi, M., & Sajedi, R. H. (2021). Engineering aequorin to improve thermostability through rigidifying flexible sites. J Mol Struct,.1240, 130575. https://doi.org/10.1016/j.molstruc.2021.130575
  • Hall, M. P., Unch, J., Binkowski, B. F., Valley, M. P., Butler, B. L., Wood, M. G., Otto, P., Zimmerman, K., Vidugiris, G., Machleidt, T., Robers, M. B., Benink, H. A., Eggers, C. T., Slater, M. R., Meisenheimer, P. L., Klaubert, D. H., Fan, F., Encell, L. P., & Wood, K. V. (2012). Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. ACS Chemical Biology, 7(11), 1848–1857. https://doi.org/10.1021/cb3002478
  • Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12<1463::AID-JCC4>3.3.CO;2-L
  • Indari, O., Sk, M. F., Jakhmola, S., Jonniya, N. A., Jha, H. C., & Kar, P. (2022). Decoding the host–parasite protein interactions involved in cerebral malaria through glares of molecular dynamics simulations. The Journal of Physical Chemistry B, 126(2), 387–402. https://doi.org/10.1021/acs.jpcb.1c07850
  • Inouye, S., & Sasaki, S. (2007). Overexpression, purification and characterization of the catalytic component of Oplophorus luciferase in the deep-sea shrimp, Oplophorus gracilirostris. Protein Expression and Purification, 56(2), 261–268. https://doi.org/10.1016/j.pep.2007.08.002 17900925
  • Inouye, S., Watanabe, K., Nakamura, H., & Shimomura, O. (2000). Secretional luciferase of the luminous shrimp Oplophorus gracilirostris: CDNA cloning of a novel imidazopyrazinone luciferase. FEBS Letters, 481(1), 19–25. https://doi.org/10.1016/s0014-5793(00)01963-3
  • Kalyan, G., Junghare, V., Bhattacharya, S., & Hazra, S. (2021). Understanding structure-based dynamic interactions of antihypertensive peptides extracted from food sources. Journal of Biomolecular Structure & Dynamics, 39(2), 635–649. https://doi.org/10.1080/07391102.2020.1715836
  • Karimzadeh, S., Moradi, M., & Hosseinkhani, S. (2012). Delicate balance of electrostatic interactions and disulfide bridges in thermostability of firefly luciferase. International Journal of Biological Macromolecules, 51(5), 837–844. https://doi.org/10.1016/j.ijbiomac.2012.06.028
  • Kitchen, D. B., Reed, L. H., & Levy, R. M. (1992). Molecular dynamics simulation of solvated protein at high pressure. Biochemistry, 31(41), 10083–10093. https://doi.org/10.1021/bi00156a031
  • Koksharov, M. I., & Ugarova, N. N. (2011). Thermostabilization of firefly luciferase by in vivo directed evolution. Protein Engineering, Design & Selection: PEDS, 24(11), 835–844. https://doi.org/10.1093/protein/gzr044
  • Kumar, S., Seth, D., & Deshpande, P. A. (2021). Molecular dynamics simulations identify the regions of compromised thermostability in SazCA. Proteins: Structure, Function and Bioinformatics, 89(4), 375–388. https://doi.org/10.1002/prot.26022
  • Kumari, M., Dohare, N., Maurya, N., Dohare, R., & Patel, R. (2017). Effect of 1-methyl-3-octyleimmidazolium chloride on the stability and activity of lysozyme: A spectroscopic and molecular dynamics studies. Journal of Biomolecular Structure & Dynamics, 35(9), 2016–2030. https://doi.org/10.1080/07391102.2016.1204946
  • Li, L., Liao, H., Yang, Y., Gong, J., Liu, J., Jiang, Z., Zhu, Y., Xiao, A., & Ni, H. (2018). Improving the thermostability by introduction of arginines on the surface of α-L-rhamnosidase (r-Rha1) from Aspergillus niger. International Journal of Biological Macromolecules, 112, 14–21. https://doi.org/10.1016/j.ijbiomac.2018.01.078
  • Lindahl, E., Hess, B., & van der Spoel, D. (2001). GROMACS 3.0: A package for molecular simulation and trajectory analysis. Journal of Molecular Modeling, 7(8), 306–317. https://doi.org/10.1007/s008940100045
  • Lindorff‐Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J. L., Dror, R. O., & Shaw, D. E. (2010). Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins, 78(8), 1950–1958. https://doi.org/10.1002/prot.22711
  • Matsutani, M., Hirakawa, H., Nishikura, M., Soemphol, W., Ali, I. A. I., Yakushi, T., & Matsushita, K. (2011). Increased number of Arginine-based salt bridges contributes to the thermotolerance of thermotolerant acetic acid bacteria, Acetobacter tropicalis SKU1100. Biochemical and Biophysical Research Communications, 409(1), 120–124. https://doi.org/10.1016/j.bbrc.2011.04.126
  • Maurya, J. K., Mir, M. U. H., Singh, U. K., Maurya, N., Dohare, N., Patel, S., Ali, A., & Patel, R. (2015). Molecular investigation of the interaction between ionic liquid type gemini surfactant and lysozyme: A spectroscopic and computational approach. Biopolymers, 103(7), 406–415. https://doi.org/10.1002/bip.22647
  • Narang, S. S., Goyal, D., & Goyal, B. (2020). Inhibition of Alzheimer’s amyloid-β42 peptide aggregation by a bi-functional bis-tryptoline triazole: Key insights from molecular dynamics simulations. Journal of Biomolecular Structure & Dynamics, 38(6), 1598–1611. https://doi.org/10.1080/07391102.2019.1614093
  • Parra-Cruz, R., Jäger, C. M., Lau, P. L., Gomes, R. L., & Pordea, A. (2018). Rational design of thermostable carbonic anhydrase mutants using molecular dynamics simulations. The Journal of Physical Chemistry. B, 122(36), 8526–8536. https://doi.org/10.1021/acs.jpcb.8b05926
  • Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
  • Paul, M., Hazra, M., Barman, A., & Hazra, S. (2014). Comparative molecular dynamics simulation studies for determining factors contributing to the thermostability of chemotaxis protein ‘cheY. Journal of Biomolecular Structure & Dynamics, 32(6), 928–949. https://doi.org/10.1080/07391102.2013.799438
  • Purmonen, M., Valjakka, J., Takkinen, K., Laitinen, T., & Rouvinen, J. (2007). Molecular dynamics studies on the thermostability of family 11 xylanases. Protein Engineering, Design & Selection: PEDS, 20(11), 551–559. https://doi.org/10.1093/protein/gzm056
  • Salameh, J. W., Kumar, S., Rivera-Cruz, C. M., & Figueiredo, M. L. (2022). A second-generation Nanoluc-IL27 fusion cytokine for targeted-gene-therapy applications. Bioengineering (Basel, Switzerland), 9(2), 77. https://doi.org/10.3390/bioengineering9020077
  • Schaub, F. X., Reza, M. S., Flaveny, C. A., Li, W., Musicant, A. M., Hoxha, S., Guo, M., Cleveland, J. L., & Amelio, A. L. (2015). Fluorophore-NanoLuc BRET reporters enable sensitive in vivo optical imaging and flow cytometry for monitoring tumorigenesis. Cancer Research, 75(23), 5023–5033. https://doi.org/10.1158/0008-5472.CAN-14-3538
  • Schwede, T., Kopp, J., Guex, N., & Peitsch, M. C. (2003). SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Research, 31(13), 3381–3385. https://doi.org/10.1093/nar/gkg520
  • Sharma, T., Dohare, N., Kumari, M., Singh, U. K., Khan, A. B., Borse, M. S., & Patel, R. (2017). Comparative effect of cationic gemini surfactant and its monomeric counterpart on the conformational stability and activity of lysozyme. RSC Advances, 7(27), 16763–16776. https://doi.org/10.1039/C7RA00172J
  • Tenda, K., van Gerven, B., Arts, R., Hiruta, Y., Merkx, M., & Citterio, D. (2018). Paper-based antibody detection devices using bioluminescent BRET-switching sensor proteins. Angewandte Chemie (International ed. in English), 57(47), 15369–15373. https://doi.org/10.1002/anie.201808070
  • Tisi, L. C., White, P. J., Squirrell, D. J., Murphy, M. J., Lowe, C. R., & Murray, J. A. H. (2002). Development of a thermostable firefly luciferase. Anal Chim Acta, 457(1), 115–123. https://doi.org/10.1016/S0003-2670(01)01496-9
  • Weber, W., Hünenberger, P. H., & Andrew McCammon, J. (2000). Molecular dynamics simulations of a polyalanine octapeptide under Ewald boundary conditions: Influence of artificial periodicity on peptide conformation. Journal of Physical Chemistry B, 104(15), 3668–3675. https://doi.org/10.1021/jp9937757
  • Xu, Q., Si, M., Zhang, Z., Li, Z., Jiang, L., & Huang, H. (2018). Rational side-chain amino acid substitution in firefly luciferase for improved thermostability. Applied Biochemistry and Microbiology, 54(6), 584–590. https://doi.org/10.1134/S0003683819010204

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