297
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

pH modulates the role of SP6 RNA polymerase in transcription process: an in silico study

ORCID Icon & ORCID Icon
Pages 11763-11780 | Received 14 Oct 2022, Accepted 22 Dec 2022, Published online: 29 Jan 2023

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindah, E. (2015). Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
  • Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389
  • Amadei, A., Linssen, A. B. M., & Berendsen, H. J. C. (1993). Essential dynamics of proteins. Proteins: Structure, Function, and Bioinformatics, 17, 412–425. https://doi.org/10.1002/prot.340170408
  • Batys, P., Morga, M., Bonarek, P., & Sammalkorpi, M. (2020). pH-induced changes in polypeptide conformation: Force-field comparison with experimental validation. Journal of Physical Chemistry B, 124, 2961–2972. https://doi.org/10.1021/acs.jpcb.0c01475
  • Berendsen, H. J. C., Postma, J. P. M., Van Gunsteren, W. F., Dinola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. Journal of Chemical Physics, 81, 3684–3690. https://doi.org/10.1063/1.448118
  • Bloom, K., van den Berg, F., & Arbuthnot, P. (2021). Self-amplifying RNA vaccines for infectious diseases. Gene Therapy, 28(3–4), 117–129. https://doi.org/10.1038/s41434-020-00204-y
  • Borkotoky, S., Meena, C. K., Bhalerao, G. M., & Murali, A. (2017). An in-silico glimpse into the pH dependent structural changes of T7 RNA polymerase: A protein with simplicity. Scientific Reports, 7, 6290. https://doi.org/10.1038/s41598-017-06586-1
  • Borkotoky, S., Meena, C. K., & Murali, A. (2016). Interaction analysis of T7 RNA polymerase with heparin and its low molecular weight derivatives – An in silico approach. Bioinformatics and Biology Insights, 10, 155–166. https://doi.org/10.4137/BBI.S40427
  • Borkotoky, S., & Murali, A. (2017). A computational assessment of pH-dependent differential interaction of T7 lysozyme with T7 RNA polymerase. BMC Structural Biology. 17, 7. https://doi.org/10.1186/s12900-017-0077-9
  • Brown, J. E., Klement, J. F., & Mcallister, W. T. (1986). Sequences of three promoters for the bacteriophage SP6 RNA polymerase. Nucleic Acids Research, 14(8), 3521–3526. https://doi.org/10.1093/nar/14.8.3521
  • Burkoff, N. S., Várnai, C., Wells, S. A., & Wild, D. L. (2012). Exploring the energy landscapes of protein folding simulations with Bayesian computation. Biophysical Journal, 102(4), 878–886. https://doi.org/10.1016/j.bpj.2011.12.053
  • Butler, E. T., & Chamberlin, M. J. (1982). Bacteriophage SP6-specific RNA polymerase. I. Isolation and characterization of the enzyme. The Journal of Biological Chemistry, 257(10), 5772–5778. https://doi.org/10.1016/s0021-9258(19)83846-2
  • Caffrey, M., & Lavie, A. (2021). pH-dependent mechanisms of influenza infection mediated by hemagglutinin. Frontiers in Molecular Biosciences, 8, 777095–777096. https://doi.org/10.3389/fmolb.2021.777095
  • Cheetham, G. M., Jeruzalmi, D., & Steitz, T. A. (1999). Structural basis for initiation of transcription from an RNA polymerase-promoter complex. Nature, 399(6731), 80–83. https://doi.org/10.1038/19999
  • Cheetham, G. M., & Steitz, T. A. (2000). Insights into transcription: Structure and function of single-subunit DNA-dependent RNA polymerases. Current Opinion in Structural Biology, 10(1), 117–123. https://doi.org/10.1016/S0959-440X(99)00058-5
  • Cheng, W.-F., Hung, C.-F., Chai, C.-Y., Hsu, K.-F., He, L., Ling, M., & Wu, T.-C. (2001). Enhancement of Sindbis virus self-replicating RNA vaccine potency by linkage of herpes simplex virus type 1 VP22 protein to antigen. Journal of Virology, 75(5), 2368–2376. https://doi.org/10.1128/jvi.75.5.2368-2376.2001
  • Clark, J. R., & March, J. B. (2004). Bacterial viruses as human vaccines? Expert Review of Vaccines, 3(4), 463–476. https://doi.org/10.1586/14760584.3.4.463
  • CLC Sequence Viewer. (n.d.).
  • Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of non-bonded atomic interactions. Protein Science, 2, 1511–1519. https://doi.org/10.1002/pro.5560020916
  • Cramer, P. (2002). Common structural features of nucleic acid polymerases. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 24(8), 724–729. https://doi.org/10.1002/bies.10127
  • Cunningham, P. R., Weitzmann, C. J., & Ofengand, J. (1991). SP6 RNA polymerase stutters when initiating from an AAA… sequence. Nucleic Acids Research, 19, 4669–4673. https://doi.org/10.1093/nar/19.17.4669
  • Davidson, E. A., Meyer, A. J., Ellefson, J. W., Levy, M., & Ellington, A. D. (2012). An in vitro autogene. ACS Synthetic Biology, 1, 190–196. https://doi.org/10.1021/sb3000113
  • Dedrick, R. M., Guerrero-Bustamante, C. A., Garlena, R. A., Russell, D. A., Ford, K., Harris, K., Gilmour, K. C., Soothill, J., Jacobs-Sera, D., Schooley, R. T., Hatfull, G. F., & Spencer, H. (2019). Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nature Medicine, 25(5), 730–733. https://doi.org/10.1038/s41591-019-0437-z
  • Dobbins, A. T., George, M., Basham, D. A., Ford, M. E., Houtz, J. M., Pedulla, M. L., Lawrence, J. G., Hatfull, G. F., & Hendrix, R. W. (2004). Complete genomic sequence of the virulent Salmonella bacteriophage SP6. Journal of Bacteriology, 186(7), 1933–1944. https://doi.org/10.1128/JB.186.7.1933
  • Durniak, K. J., Bailey, S., & Steitz, T. A. (2008). The structure of a transcribing T7 RNA polymerase in transition from initiation to elongation. Science (New York, N.Y.), 322(5901), 553–557. https://doi.org/10.1126/science.1163433
  • Eisenberg, D., Lüthy, R., & Bowie, J. U. (1997). VERIFY3D: Assessment of protein models with three-dimensional profiles. Methods in Enzymology, 277, 396–404. https://doi.org/10.1016/S0076-6879(97)77022-8
  • Fiser, A., & Sali, A. (2003). ModLoop: Automated modeling of loops in protein structures. Bioinformatics, 19, 2500–2501. https://doi.org/10.1093/bioinformatics/btg362
  • Furfaro, L. L., Payne, M. S., & Chang, B. J. (2018). bacteriophage therapy: Clinical trials and regulatory hurdles. Frontiers in Cellular and Infection Microbiology, 8, 376. https://doi.org/10.3389/fcimb.2018.00376
  • Geourjon, C., & Deléage, G. (1995). Sopma: Significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Bioinformatics, 11, 681–684. https://doi.org/10.1093/bioinformatics/11.6.681
  • Gordon, J. C., Myers, J. B., Folta, T., Shoja, V., Heath, L. S., & Onufriev, A. (2005). H++: A server for estimating pKas and adding missing hydrogens to macromolecules. Nucleic Acids Research, 33, W368–W371. https://doi.org/10.1093/nar/gki464
  • Hamzeh-Mivehroud, M., Moghaddas-Sani, H., Rahbar-Shahrouziasl, M., & Dastmalchi, S. (2015). Identifying key interactions stabilizing DOF zinc finger-DNA complexes using in silico approaches. Journal of Theoretical Biology, 382, 150–159. https://doi.org/10.1016/j.jtbi.2015.06.013
  • Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
  • Iacovelli, F., Idili, A., Benincasa, A., Mariottini, D., Ottaviani, A., Falconi, M., Ricci, F., & Desideri, A. (2017). Simulative and experimental characterization of a pH-dependent clamp-like DNA triple-helix nanoswitch. Journal of the American Chemical Society, 139(15), 5321–5329. https://doi.org/10.1021/jacs.6b11470
  • Jácome, R., Becerra, A., De León, S. P., & Lazcano, A. (2015). Structural analysis of monomeric RNA- dependent polymerases: Evolutionary and therapeutic implications. PLoS One. 10, 1–26. https://doi.org/10.1371/journal.pone.0139001
  • Jepson, C. D., & March, J. B. (2004). Bacteriophage lambda is a highly stable DNA vaccine delivery vehicle. Vaccine, 22(19), 2413–2419. https://doi.org/10.1016/j.vaccine.2003.11.065
  • Jeruzalmi, D., & Steitz, T. A. (1998). Structure of T7 RNA polymerase complexed to the transcriptional inhibitor T7 lysozyme. EMBO Journal, 17, 4101–4113. https://doi.org/10.1093/emboj/17.14.4101
  • Jorgensen, E. D., Durbin, R. K., Risman, S. S., & McAllister, W. T. (1991). Specific contacts between the bacteriophage T3, T7, and SP6 RNA polymerases and their promoters. The Journal of Biological Chemistry, 266(1), 645–651. https://doi.org/10.1016/s0021-9258(18)52483-2
  • Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., Bridgland, A., Meyer, C., Kohl, S. A. A., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873), 583–589. https://doi.org/10.1038/s41586-021-03819-2
  • Kennedy, W. P., Momand, J. R., & Yin, Y. W. (2007). Mechanism for de novo RNA synthesis and initiating nucleotide specificity by T7 RNA polymerase. Journal of Molecular Biology, 370, 256–268. https://doi.org/10.1016/j.jmb.2007.03.041
  • Kots, E., Shore, D. M., & Weinstein, H. (2021). Simulation of pH-dependent conformational transitions in membrane proteins: The CLC-ec1 Cl−/H + antiporter. Molecules, 26, 6956. https://doi.org/10.3390/molecules26226956
  • Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
  • Kumari, R., Kumar, R., & Lynn, A, Open Source Drug Discovery Consortium (2014). G-mmpbsa—A GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
  • Kwon, Y., Tang, K., Cantor, C., Köster, H., & Kang, C. (2001). DNA sequencing and genotyping by transcriptional synthesis of chain-terminated RNA ladders and MALDI-TOF mass spectrometry. Nucleic acids Research, 29(3), E11. https://doi.org/10.1093/nar/29.3.e11
  • Laskowski, R. A., Macarthur, M. W., & Thornton, J. M. (2012). PROCHECK: Validation of protein‐structure coordinates. International tables for crystallography (pp. 684–687). Wiley. https://doi.org/10.1107/97809553602060000882
  • Liu, W. Y., Wang, Y., Sun, Y. H., Wang, Y., Wang, Y. P., Chen, S. P., & Zhu, Z. Y. (2005). Efficient RNA interference in zebrafish embryos using siRNA synthesized with SP6 RNA polymerase. Development, Growth & Differentiation, 47(5), 323–331. https://doi.org/10.1111/j.1440-169X.2005.00807.x
  • Luscombe, N. M., Laskowski, R. A., & Thornton, J. M. (1997). NUCPLOT: A program to generate schematic diagrams of protein-nucleic acid interactions. Nucleic Acids Research, 25(24), 4940–4945. https://doi.org/10.1093/nar/25.24.4940
  • Ma, S., Henderson, J. A., & Shen, J. (2021). Exploring the pH-dependent structure-dynamics-function relationship of human renin. Journal of Chemical Information and Modeling, 61(1), 400–407. https://doi.org/10.1021/acs.jcim.0c01201
  • Maruggi, G., Zhang, C., Li, J., Ulmer, J. B., & Yu, D. (2019). mRNA as a transformative technology for vaccine development to control infectious diseases. Molecular Therapy: The Journal of the American Society of Gene Therapy, 27(4), 757–772. https://doi.org/10.1016/j.ymthe.2019.01.020
  • Molenaar, T. J. M., Michon, I., De Haas, S. A. M., Van Berkel, T. J. C., Kuiper, J., & Biessen, E. A. L. (2002). Uptake and processing of modified bacteriophage M13 in mice: Implications for phage display. Virology, 293(1), 182–191. https://doi.org/10.1006/viro.2001.1254
  • Mulvey, M. C., Lemmon, M., Rotter, S., Lees, J., Einck, L., & Nacy, C. A. (2015). Optimization of a nucleic acid-based reporter system to detect Mycobacterium tuberculosis antibiotic sensitivity. Antimicrobial Agents and Chemotherapy, 59(1), 407–413. https://doi.org/10.1128/AAC.03135-14
  • Mulvey, M. C., Sacksteder, K. A., Einck, L., & Nacy, C. A. (2012). Generation of a novel nucleic acid-based reporter system to detect phenotypic susceptibility to antibiotics in Mycobacterium tuberculosis. MBio, 3, 00312. https://doi.org/10.1128/mBio.00312-11
  • NCBI Resource Coordinators (2018). Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 46, D8–D13. https://doi.org/10.1093/nar/gkx1095
  • Pandey, B., Grover, A., & Sharma, P. (2018). Molecular dynamics simulations revealed structural differences among WRKY domain-DNA interaction in barley (Hordeum vulgare). BMC Genomics, 19, 132. https://doi.org/10.1186/s12864-018-4506-3
  • Pardi, N., Hogan, M. J., Porter, F. W., & Weissman, D. (2018). mRNA vaccines—A new era in vaccinology. Nature Reviews. Drug Discovery, 17(4), 261–279. https://doi.org/10.1038/nrd.2017.243
  • Petersen, H. G. (1995). Accuracy and efficiency of the particle mesh Ewald method. Journal of Chemical Physics, 103, 3668–3679. https://doi.org/10.1063/1.470043
  • Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera – A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. https://doi.org/10.1002/jcc.20084
  • Putra, R. D., & Lyrawati, D. (2020). Interactions between Bacteriophages and Eukaryotic cells. Scientifica, 2020, 3589316. https://doi.org/10.1155/2020/3589316
  • Sagawa, H., Ohshima, A., & Kato, I. (1996). A tightly regulated expression system in Escherichia coli with SP6 RNA polymerase. Gene, 168(1), 37–41. https://doi.org/10.1016/0378-1119(95)00644-3
  • Scholl, D., Adhya, S., & Merril, C. R. (2002). Bacteriophage SP6 is closely related to phages K1-5, K5, and K1E but encodes a tail protein very similar to that of the distantly related P22. Journal of Bacteriology, 184(10), 2833–2836. https://doi.org/10.1128/JB.184.10.2833-2836.2002
  • Scholl, D., Kieleczawa, J., Kemp, P., Rush, J., Richardson, C. C., Merril, C., Adhya, S., & Molineux, I. J. (2004). Genomic analysis of bacteriophages SP6 and K1-5, an estranged subgroup of the T7 supergroup. Journal of Molecular Biology, 335(5), 1151–1171. https://doi.org/10.1016/j.jmb.2003.11.035
  • Shkoporov, A. N., & Hill, C. (2019). Bacteriophages of the human gut: The “known unknown” of the microbiome. Cell Host & Microbe, 25(2), 195–209. https://doi.org/10.1016/j.chom.2019.01.017
  • Sousa, R., Chung, Y. J., McAllister, W. T., Wang, B. C., & Lafer, E. M. (1990). Single crystals of a chimeric T7/T3 RNA polymerase with T3 promoter specificity and a nonprocessive T7 RNAP mutant. Journal of Biological Chemistry, 265, 21430–21432. https://doi.org/10.1016/S0021-9258(18)45755-9
  • Sousa, R., Chung, Y. J., Rose, J. P., & Wang, B. C. (1993). Crystal structure of bacteriophage T7 RNA polymerase at 3.3 Å resolution. Nature, 364(6438), 593–599. https://doi.org/10.1038/364593a0
  • Sousa, R., Chung, Y. J., Wang, B. C., & Lafer, E. M. (1992). Single crystals of a chimeric T7/T3 RNA polymerase with T3 promoter specificity. Journal of Crystal Growth, 122, 366–374. https://doi.org/10.1016/0022-0248(92)90271-J
  • Sousa, R., & Mukherjee, S. (2003). T7 RNA polymerase. Progress in Nucleic Acid Research and Molecular Biology, 73, 1–41. https://doi.org/10.1016/S0079-6603(03)01001-8
  • Summers, W. C. (2001). Bacteriophage therapy. Annual Review of Microbiology, 55(1), 437–451. https://doi.org/10.1146/annurev.micro.55.1.437
  • Tahirov, T. H., Temiakov, D., Anikin, M., Patlan, V., McAllister, W. T., Vassylyev, D. G., & Yokoyama, S. (2002). Structure of a T7 RNA polymerase elongation complex at 2.9 Å resolution. Nature, 420(6911), 43–50. https://doi.org/10.1038/nature01129
  • Taylor, D. R., & Mathews, M. B. (1993). Transcription by SP6 RNA polymerase exhibits an ATP dependence that is influenced by promoter topology. Nucleic Acids Research, 8, 1927–1933. https://doi.org/10.1093/nar/21.8.1927
  • The UniProt Consortium. (2019) UniProt: A worldwide hub of protein knowledge. Nucleic Acids Research, 47, D506–D515. https://doi.org/10.1093/nar/gky1049
  • Tunitskaya, V. L., & Kochetkov, S. N. (2002). Structural-functional analysis of bacteriophage T7 RNA polymerase. Biochemistry. Biokhimiia, 67(10), 1124–1135. https://doi.org/10.1023/a:1020911223250
  • Ul Haq, I., Chaudhry, W. N., Akhtar, M. N., Andleeb, S., & Qadri, I. (2012). Bacteriophages and their implications on future biotechnology: A review. Virology Journal, 9, 9. https://doi.org/10.1186/1743-422X-9-9
  • van Dijk, M., & Bonvin, A. (2009). 3D-DART: A DNA structure modelling server. Nucleic Acids Research, 37, 235–239. https://doi.org/10.1093/nar/gkp287
  • Van Zundert, G. C. P., Rodrigues, J., Trellet, M., Schmitz, C., Kastritis, P. L., Karaca, E., Melquiond, A. S. J., Van Dijk, M., De Vries, S. J., & Bonvin, A. (2016). The HADDOCK2.2 web server: User-friendly integrative modeling of biomolecular complexes. Journal of Molecular Biology, 428(4), 720–725. https://doi.org/10.1016/j.jmb.2015.09.014
  • Waseem, R., Shamsi, A., Shahbaz, M., Khan, T., Kazim, S. N., Ahmad, F., Hassan, M. I., & Islam, A. (2021). Effect of pH on the structure and stability of Irisin, a multifunctional protein: Multispectroscopic and molecular dynamics simulation approach. Journal of Molecular Structure, 1252, 132–141. https://doi.org/10.1016/j.molstruc.2021.132141
  • Webb, B., & Sali, A. (2016). Comparative protein structure modeling using MODELLER. Current protocols in Bioinformatics, 54, 5.6.1–5.6.37. https://doi.org/10.1002/cpbi.3
  • Wittebole, X., De Roock, S., & Opal, S. M. (2014). A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence, 5(1), 226–235. https://doi.org/10.4161/viru.25991
  • Wu, Y., Tepper, H. L., & Voth, G. A. (2006). Flexible simple point-charge water model with improved liquid-state properties. The Journal of Chemical Physics, 124(2), 024503. https://doi.org/10.1063/1.2136877
  • Xu, S., Yang, K., Li, R., & Zhang, L. (2020). mRNA vaccine era—Mechanisms, drug platform and clinical prospection. International Journal of Molecular Sciences, 21, 6582. https://doi.org/10.3390/ijms21186582
  • Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2014). The I-TASSER suite: Protein structure and function prediction. Nature Methods, 12, 7–8. https://doi.org/10.1038/nmeth.3213
  • Yang, B., Zhu, Y., Wang, Y., & Chen, G. (2011). Interaction identification of Zif268 and TATAZF proteins with GC-/AT-rich DNA sequence: A theoretical study. Journal of Computational Chemistry, 32(3), 416–428. https://doi.org/10.1002/jcc.21630
  • Yin, Y. W., & Steitz, T. A. (2004). The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell, 116(3), 393–404. https://doi.org/10.1016/S00928674(04)00120-5
  • Ying, H., Zaks, T. Z., Wang, R. F., Irvine, K. R., Kammula, U. S., Marincola, F. M., Leitner, W. W., & Restifo, N. P. (1999). Cancer therapy using a self-replicating RNA vaccine. Nature Medicine, 5(7), 823–827. https://doi.org/10.1038/10548
  • Zgarbová, M., Šponer, J., Otyepka, M., Cheatham, T. E., 3rd, Galindo-Murillo, R., & Jurečka, P. (2015). Refinement of the sugar-phosphate backbone torsion beta for AMBER force fields improves the description of Z- and B-DNA. Journal of Chemical Theory and Computation, 11(12), 5723–5736. https://doi.org/10.1021/acs.jctc.5b00716
  • Zhou, W., & Doetsch, P. W. (1993). Effects of abasic sites and DNA single-strand breaks on prokaryotic RNA polymerases. Proceedings of the National Academy of Sciences of the United States of America, 14, 6601–6605. https://doi.org/10.1073/pnas.90.14.6601

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.