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Research Article

Decoding the structural integrity and multifunctional role of Era protein in the survival of Mycobacterium tuberculosis H37Rv

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Received 27 Jan 2023, Accepted 15 Jan 2024, Published online: 06 Feb 2024

References

  • Albericio, F. (2004). Developments in peptide and amide synthesis. Current Opinion in Chemical Biology, 8(3), 211–221. https://doi.org/10.1016/j.cbpa.2004.03.002
  • Allué-Guardia, A., García, J. I., & Torrelles, J. B. (2021). Evolution of drug-resistant Mycobacterium tuberculosis strains and their adaptation to the human lung environment. Frontiers in Microbiology, 12, 612675. https://www.frontiersin.org/articles/10.3389/fmicb.2021.612675/full
  • Bourne, H. R., Sanders, D. A., & McCormick, F. (1990). The GTPase superfamily: A conserved switch for diverse cell functions. Nature, 348(6297), 125–132. https://doi.org/10.1038/348125a0
  • Bourne, H. R., Sanders, D. A., & McCormick, F. (1991). The GTPase superfamily: Conserved structure and molecular mechanism. Nature, 349(6305), 117–127. https://doi.org/10.1038/349117a0
  • Britton, B. A., & Lupski, J. R. (1997). Isolation and characterization of suppressors of two Escherichia coli dnaG mutations, dnaG2903 and parB. Genetics, 145(4), 867–875. https://doi.org/10.1093/genetics/145.4.867
  • Britton, R. A., Powell, B. S., Court, D. L., & Lupski, J. R. (1997). Characterization of mutations affecting the Escherichia coli essential GTPase era that suppress two temperature-sensitive dnaG alleles. Journal of Bacteriology, 179(14), 4575–4582. https://doi.org/10.1128/jb.179.14.4575-4582.1997
  • Britton, R. A., Powell, B. S., Dasgupta, S., Sun, Q., Margolin, W., Lupski, J. R., & Court, D. L. (1998). Cell cycle arrest in Era GTPase mutants: A potential growth rate-regulated checkpoint in Escherichia coli. Molecular Microbiology, 27(4), 739–750. https://doi.org/10.1046/j.1365-2958.1998.00719.x
  • Castro, R. A. D., Ross, A., Kamwela, L., Reinhard, M., Loiseau, C., Feldmann, J., Borrell, S., Trauner, A., & Gagneux, S. (2020). The genetic background modulates the evolution of fluoroquinolone-resistance in Mycobacterium tuberculosis. Molecular Biology and Evolution, 37(1), 195–207. https://doi.org/10.1093/molbev/msz214
  • Chen, X., Court, D. L., & Ji, X. (1999). Crystal structure of ERA: A GTPase-dependent cell cycle regulator containing an RNA binding motif. Proceedings of the National Academy of Sciences of the United States of America, 96(15), 8396–8401. https://doi.org/10.1073/pnas.96.15.8396
  • Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., III, Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., … Barrell, B. G. (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature, 396(6707), 190–190. https://doi.org/10.1038/24206
  • Dallakyan, S., & Olson, A. J. (2015). Small-molecule library screening by docking with PyRx. Chemical biology (pp. 243–250). Humana Press. https://doi.org/10.1007/978-1-4939-2269-7_19
  • de Castro, E., Sigrist, C. J. A., Gattiker, A., Bulliard, V., Langendijk-Genevaux, P. S., Gasteiger, E., Bairoch, A., & Hulo, N. (2006). ScanProsite: Detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Research, 34, W362–W365. https://doi.org/10.1093/nar/gkl124
  • Dever, T. E., Glynias, M. J., & Merrick, W. C. (1987). GTP-binding domain: Three consensus sequence elements with distinct spacing. Proceedings of the National Academy of Sciences of the United States of America, 84(7), 1814–1818. https://doi.org/10.1073/pnas.84.7.1814
  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340
  • Eldholm, V., & Balloux, F. (2016). Antimicrobial resistance in Mycobacterium tuberculosis: The odd one out. Trends in Microbiology, 24(8), 637–648. https://doi.org/10.1016/j.tim.2016.03.007
  • Eswar, N., Eramian, D., Webb, B., Shen, M. Y., & Sali, A. (2008). Protein structure modeling with MODELLER. Structural proteomics. Methods in Molecular Biology, 426, 145–159. https://doi.org/10.1007/978-1-60327-058-8_8
  • Farazi, T. A., Waksman, G., & Gordon, J. I. (2001). The biology and enzymology of proteinN-myristoylation* 210. The Journal of Biological Chemistry, 276(43), 39501–39504. https://doi.org/10.1074/jbc.R100042200
  • Fiser, A., & Sali, A. (2003). Modeller: Generation and refinement of homology-based protein structure models. Methods in Enzymology, 374, 461–491. https://doi.org/10.1016/S0076-6879(03)74020-8
  • Folkman, L., Stantic, B., Sattar, A., & Zhou, Y. (2016). EASE-MM: Sequence-based prediction of mutation-induced stability changes with feature-based multiple models. Journal of Molecular Biology, 428(6), 1394–1405. https://doi.org/10.1016/j.jmb.2016.01.012
  • Garg, A., & Gupta, D. (2008). VirulentPred: A SVM based prediction method for virulent proteins in bacterial pathogens. BMC Bioinformatics, 9(1), 62. https://doi.org/10.1186/1471-2105-9-62
  • Garg, V. K., Avashthi, H., Tiwari, A., Jain, A. P., Ramkete, P. W., Kayastha, A. M., & Singh, V. K. (2016). MFPPI–multi FASTA ProtParam interface. Bioinformation, 12(2), 74–77. https://doi.org/10.6026/97320630012074
  • Global Tuberculosis Report, World Health Organization. (2021). https://www.who.int/publications/digital/global-tuberculosis-report-2021
  • Gollop, N., & March, P. E. (1991). A GTP-binding protein (Era) has an essential role in growth rate and cell cycle control in Escherichia coli. Journal of Bacteriology, 173(7), 2265–2270. https://doi.org/10.1128/jb.173.7.2265-2270.1991
  • Gray, J. L., von Delft, F., & Brennan, P. E. (2020). Targeting the small GTPase superfamily through their regulatory proteins. Angewandte Chemie (International ed. in English), 59(16), 6342–6366. https://doi.org/10.1002/anie.201900585
  • Guruprasad, K., Reddy, B. V., & Pandit, M. W. (1990). Correlation between stability of a protein and its dipeptide composition: A novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Engineering, 4(2), 155–161. https://doi.org/10.1093/protein/4.2.155
  • Heo, L., Park, H., & Seok, C. (2013). GalaxyRefine: Protein structure refinement driven by side-chain repacking. Nucleic Acids Research, 41, W384–W388. https://doi.org/10.1093/nar/gkt458
  • Kalbitzer, H. R., & Spoerner, M. (2013). State 1(T) (2013) inhibitors of activated Ras. In F. Tamanoi (Ed.), Inhibitors of the ras superfamily G-proteins, part A (Vol. 33, pp. 69–94). Elsevier Inc. https://doi.org/10.1016/B978-0-12-416749-0.00004-X
  • Kapopoulou, A., Lew, J. M., & Cole, S. T. (2011). The MycoBrowser portal: A comprehensive and manually annotated resource for mycobacterial genomes. Tuberculosis (Edinburgh, Scotland), 91(1), 8–13. https://doi.org/10.1016/j.tube.2010.09.006
  • Kaziro, Y., Itoh, H., Kozasa, T., Nakafuku, M., & Satoh, T. (1991). Structure and function of signal-transducing GTP-binding proteins. Annual Review of Biochemistry, 60(1), 349–400. https://doi.org/10.1146/annurev.bi.60.070191.002025
  • Kuhn, M., Mering, C. V., Campillos, M., Jensen, L. J., & Bork, P. (2007). STITCH: Interaction networks of chemicals and proteins. Nucleic Acids Research, 36, D684–D688. https://doi.org/10.1093/nar/gkm795
  • Kyte, J., & Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology, 157(1), 105–132. https://doi.org/10.1016/0022-2836(82)90515-0
  • Kirchhausen, T., Macia, E., & Pelish, H. E. (2008). Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis. Methods in Enzymology, 438, 77–93. https://doi.org/10.1016/S0076-6879(07)38006-3
  • Lew, J. M., Kapopoulou, A., Jones, L. M., & Cole, S. T. (2011). TubercuList–10 years after. Tuberculosis (Edinburgh, Scotland), 91(1), 1–7. https://doi.org/10.1016/j.tube.2010.09.008
  • Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., & Kirchhausen, T. (2006). Dynasore, a cell-permeable inhibitor of dynamin. Developmental Cell, 10(6), 839–850. https://doi.org/10.1016/j.devcel.2006.04.002
  • Mann, C. M., Muppirala, U. K., & Dobbs, D. (2017). Computational prediction of RNA-protein interactions. Promoter Associated RNA. Humana Press, New York, NY. Methods in Molecular Biology, 1543, 169–185. https://doi.org/10.1007/978-1-4939-6716-2_8
  • March, P. E., Lerner, C. G., Ahnn, J., Cui, X., & Inouye, M. (1988). The Escherichia coli Ras-like protein (Era) has GTPase activity and is essential for cell growth. Oncogene, 2(6), 539–544. https://pubmed.ncbi.nlm.nih.gov/2838786/
  • McGuffin, L. J., Bryson, K., & Jones, D. T. (2000). The PSIPRED protein structure prediction server. Bioinformatics (Oxford, England), 16(4), 404–405. https://doi.org/10.1093/bioinformatics/16.4.404
  • McLaughlin, S., & Aderem, A. (1995). The myristoyl-electrostatic switch: A modulator of reversible protein-membrane interactions. Trends in Biochemical Sciences, 20(7), 272–276. https://doi.org/10.1016/S0968-0004(00)89042-8
  • Meena, L., & Rajni, S. (2010). Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv.The FEBS Journal, 277(11), 2416–2427. https://doi.org/10.1111/j.1742-4658.2010.07666.x
  • Meena, L. S., Chopra, P., Bedwal, R. S., & Singh, Y. (2008). Cloning and characterization of GTP-binding proteins of Mycobacterium tuberculosis H37Rv. Enzyme and Microbial Technology, 42(2), 138–144. https://doi.org/10.1016/j.enzmictec.2007.08.008
  • Musco, G., Stier, G., Joseph, C., Castiglione Morelli, M. A., Nilges, M., Gibson, T. J., & Pastore, A. (1996). Three-dimensional structure and stability of the KH domain: Molecular insights into the fragile X syndrome. Cell, 85(2), 237–245. https://doi.org/10.1016/S0092-8674(00)81100-9
  • Murphy, N. P., Mott, H. R., & Owen, D. (2021). Progress in the therapeutic inhibition of Cdc42 signalling. Biochemical Society Transactions, 49(3), 1443–1456. https://doi.org/10.1042/BST20210112
  • Paduch, M., Jeleń, F., & Otlewski, J. (2001). Structure of small G proteins and their regulators. Acta Biochimica Polonica, 48(4), 829–850. https://doi.org/10.18388/abp.2001_3850
  • Patni, K., Agarwal, P., Kumar, A., & Meena, L. S. (2021). Computational evaluation of anticipated PE_PGRS39 protein involvement in host–pathogen interplay and its integration into vaccine development. 3 Biotech, 11(4), 204. https://doi.org/10.1007/s13205-021-02746-3
  • Polakis, P., & McCormick, F. (1993). Structural requirements for the interaction of p21ras with GAP, exchange factors, and its biological effector target. Journal of Biological Chemistry, 268(13), 9157–9160. https://doi.org/10.1016/S0021-9258(18)98325-0
  • Preeti, P., Meena, S., & Meena, L. S. (2021). Comprehensive analysis of GTP cyclohydrolase I activity in Mycobacterium tuberculosis H37Rv via in silico studies. Biotechnology and Applied Biochemistry, 68(4), 756–768. https://doi.org/10.1002/bab.1988
  • Prieto-Dominguez, N., Parnell, C., & Teng, Y. (2019). Drugging the small GTPase pathways in cancer treatment: Promises and challenges. Cells, 8(3), 255. https://doi.org/10.3390/cells8030255
  • Pruitt, K. D., Tatusova, T., & Maglott, D. R. (2007). NCBI reference sequences (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Research, 35, D61–D65. https://doi.org/10.1093/nar/gkr1178
  • Rodrigues, C. H. M., Pires, D., & Ascher, D. B. (2018). DynaMut: Predicting the impact of mutations on protein conformation, flexibility and stability. Nucleic Acids Research, 46(W1), W350–W355. https://doi.org/10.1093/nar/gky300
  • Rosenberg, E. M., Jr, Jian, X., Soubias, O., Yoon, H.-Y., Yadav, M. P., Hammoudeh, S., Pallikkuth, S., Akpan, I., Chen, P. W., Maity, T. K., Jenkins, L. M., Yohe, M. E., Byrd, R. A., & Randazzo, P. A. (2023). The small molecule inhibitor NAV-2729 has a complex target profile including multiple ADP-ribosylation factor regulatory proteins. Journal of Biological Chemistry, 299(3), 102992. https://doi.org/10.1016/j.jbc.2023.102992
  • 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, M. R., Barat, C., Wilson, D. N., Booth, T. M., Kawazoe, M., Hori-Takemoto, C., Shirouzu, M., Yokoyama, S., Fucini, P., & Agrawal, R. K. (2005). Interaction of Era with the 30S ribosomal subunit: Implications for 30S subunit assembly. Molecular Cell, 18(3), 319–329. https://doi.org/10.1016/j.molcel.2005.03.028
  • Shashi, B. P., & Srinivasan, N. (2003). Survey for g-proteins in the prokaryotic genomes: Prediction of functional roles based on classification. Proteins, 52(4), 585–597. https://doi.org/10.1002/prot.10420
  • Shimamoto, T., & Inouye, M. (1996). Mutational analysis of Era, an essential GTP-binding protein of Escherichia coli. FEMS Microbiology Letters, 136(1), 57–62. https://doi.org/10.1111/j.1574-6968.1996.tb08025.x
  • Sood, P., Lerner, C. G., Shimamoto, T., Lu, Q., & Inouye, M. (1994). Characterization of the autophosphorylation of Era, an essential Escherichia coli GTPase. Molecular Microbiology, 12(2), 201–208. https://doi.org/10.1111/j.1365-2958.1994.tb01009.x
  • Stephen, R. S. (1997). G protein mechanisms: Insights from structural analysis. Annual Review of Biochemistry, 66(1), 639–678. https://doi.org/10.1146/annurev.biochem.66.1.639
  • Tu, C., Zhou, X., Tarasov, S. G., Tropea, J. E., Austin, B. P., Waugh, D. S., Court, D. L., & Ji, X. (2011). The Era GTPase recognizes the GAUCACCUCC sequence and binds helix 45 near the 3′ end of 16S rRNA. Proceedings of the National Academy of Sciences of the United States of America, 108(25), 10156–10161. https://doi.org/10.1073/pnas.1017679108
  • Tu, C., Zhou, X., Tropea, J. E., Austin, B. P., Waugh, D. S., Court, D. L., & Ji, X. (2009). Structure of ERA in complex with the 3′ end of 16S rRNA: Implications for ribosome biogenesis. Proceedings of the National Academy of Sciences of the United States of America, 106(35), 14843–14848. https://doi.org/10.1073/pnas.0904032106
  • Uchiumi, T., Ohgaki, K., Yagi, M., Aoki, Y., Sakai, A., Matsumoto, S., & Kang, D. (2010). ERAL1 is associated with mitochondrial ribosome and elimination of ERAL1 leads to mitochondrial dysfunction and growth retardation. Nucleic Acids Research, 38(16), 5554–5568. https://doi.org/10.1093/nar/gkq305
  • UniProt Consortium. (2015). UniProt: A hub for protein information. Nucleic Acids Research. 43, D204–D212. https://doi.org/10.1093/nar/gku989
  • Wang, S., Li, W., Liu, S., & Xu, J. (2016). RaptorX-Property: A web server for protein structure property prediction. Nucleic Acids Research, 44(W1), W430–W435. https://doi.org/10.1093/nar/gkw306
  • Wang, W., Fang, G., & Rudolph, J. (2012). Ras inhibition via direct Ras binding–is there a path forward? Bioorganic & Medicinal Chemistry Letters, 22(18), 5766–5776. https://doi.org/10.1016/j.bmcl.2012.07.082
  • Wuichet, K., & Søgaard-Andersen, L. (2015). Evolution and diversity of the Ras superfamily of small GTPases in prokaryotes. Genome Biology and Evolution, 7(1), 57–70. https://doi.org/10.1093/gbe/evu264
  • Xue, B., Dunbrack, R. L., Williams, R. W., Dunker, A. K., & Uversky, V. N. (2010). PONDR-FIT: A meta-predictor of intrinsically disordered amino acids. Biochimica et Biophysica Acta, 1804(4), 996–1010. https://doi.org/10.1016/j.bbapap.2010.01.011
  • Yan, Y., Zhang, D., Zhou, P., Li, B., & Huang, S. Y. (2017). HDOCK: A web server for protein–protein and protein–DNA/RNA docking based on a hybrid strategy. Nucleic Acids Research, 45(W1), W365–W373. https://doi.org/10.1038/s41596-020-0312-x
  • Yang, J., & Zhang, Y. (2015). I-TASSER server: New development for protein structure and function predictions. Nucleic Acids Research, 43(W1), W174–W181. https://doi.org/10.1093/nar/gkv342
  • Yang, J. F., Wang, F., Chen, Y. Z., Hao, G. F., & Yang, G. F. (2020). LARMD: Integration of bioinformatic resources to profile ligand-driven protein dynamics with a case on the activation of estrogen receptor. Briefings in Bioinformatics, 21(6), 2206–2218. https://doi.org/10.1093/bib/bbz141
  • Yu, C. S., Cheng, C. W., Su, W. C., Chang, K. C., Huang, S. W., Hwang, J. K., & Lu, C. H. (2014). CELLO2GO: A web server for protein sub cellular localization prediction with functional gene ontology annotation. PLoS One, 9(6), e99368. https://doi.org/10.1371/journal.pone.0099368
  • Zhao, G., Meier, T. I., Peery, R. B., Matsushima, P., & Skatrud, P. L. (1999). Biochemical and molecular analyses of the C-terminal domain of Era GTPase from Streptococcus pneumoniae. Microbiology (Reading, England), 145 (Pt 4)(4), 791–800. https://doi.org/10.1099/13500872-145-4-791

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