Comparative Analysis of Inhibitor Binding to Peroxiredoxins from Candidatus Liberibacter asiaticus and Its Host Citrus sinensis.
Circular dichroism
Differential scanning calorimetry
Inhibitor molecules
Molecular dynamics simulations
Peroxiredoxins
Surface plasmon resonance
Journal
Applied biochemistry and biotechnology
ISSN: 1559-0291
Titre abrégé: Appl Biochem Biotechnol
Pays: United States
ID NLM: 8208561
Informations de publication
Date de publication:
29 Dec 2023
29 Dec 2023
Historique:
accepted:
09
12
2023
medline:
2
1
2024
pubmed:
2
1
2024
entrez:
29
12
2023
Statut:
aheadofprint
Résumé
The peroxiredoxins (Prxs), potential drug targets, constitute an important class of antioxidant enzymes present in both pathogen and their host. The comparative binding potential of inhibitors to Prxs from pathogen and host could be an important step in drug development against pathogens. Huanglongbing (HLB) is a most devastating disease of citrus caused by Candidatus Liberibacter asiaticus (CLa). In this study, the binding of conoidin-A (conoidin) and celastrol inhibitor molecules to peroxiredoxin of bacterioferritin comigratory protein family from CLa (CLaBCP) and its host plant peroxiredoxin from Citrus sinensis (CsPrx) was assessed. The CLaBCP has a lower specific activity than CsPrx and is efficiently inhibited by conoidin and celastrol molecules. The biophysical studies showed conformational changes and significant thermal stability of CLaBCP in the presence of inhibitor molecules as compared to CsPrx. The surface plasmon resonance (SPR) studies revealed that the conoidin and celastrol inhibitor molecules have a strong binding affinity (K
Identifiants
pubmed: 38157153
doi: 10.1007/s12010-023-04798-y
pii: 10.1007/s12010-023-04798-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Department of Biotechnology, Ministry of Science and Technology, India
ID : BT/PR9877/BRB/10/1274/2014
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Jagoueix, S., Bove, J. M., & Garnier, M. (1994). The phloem-limited bacterium of greening disease of citrus is a member of the alpha subdivision of the Proteobacteria. International Journal of Systematic and Evolutionary Microbiology, 44(3), 379–386. https://doi.org/10.1099/00207713-44-3-379
doi: 10.1099/00207713-44-3-379
Bove, J. M. (2006). Huanglongbing: A destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology, 7–37. https://www.jstor.org/stable/41998278
Halbert, S. E., & Manjunath, K. L. (2004). Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: A literature review and assessment of risk in Florida. The Florida Entomologist, 87(3), 330–353. https://doi.org/10.1653/0015-4040(2004)
doi: 10.1653/0015-4040(2004)
Texeira, D., Ayres, J., Kitajima, E., Danet, L., Jagoueix-Eveillard, S., Saillard, C., & Bove, J. (2005). First report of a huanglongbing-like disease of citrus in Sao Paulo State, Brazil, and association of a new Liberibacter species, “Candidatus Liberibacter americanus”, with the disease. Plant Disease, 89(1), 107–107. https://doi.org/10.1094/PD-89-0107A
doi: 10.1094/PD-89-0107A
pubmed: 30795297
Duan, J., Li, X., Zhang, J., Cheng, B., Liu, S., Li, H., Zhou, Q., & Chen, W. (2021). Cocktail therapy of fosthiazate and cupric-ammonium complex for citrus huanglongbing. Frontiers in Plant Science, 12, 643971. https://doi.org/10.3389/fpls.2021.643971
doi: 10.3389/fpls.2021.643971
pubmed: 33868341
pmcid: 8044827
Ghosh, D. K., Motghare, M., & Gowda, S. (2018). Citrus greening: Overview of the most severe disease of citrus. Journal of Advanced Agricultural Technologies, 2(1), 83–100. http://isasat.org/Vol-ii,issue-i/AARJ_2_1_13_Ghosh.pdf
Fones, H., & Preston, G. M. (2012). Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. FEMS Microbiology Letters, 327(1), 1–8. https://doi.org/10.1111/j.1574-6968.2011.02449.x
doi: 10.1111/j.1574-6968.2011.02449.x
pubmed: 22092667
Nita, M., & Grzybowski, A. (2016). The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxidative Medicine and Cellular Longevity, 3164734. https://doi.org/10.1155/2016/3164734
Dumanovic, J., Nepovimova, E., Natić, M., Kuča, K., & Jaćević, V. (2021). The significance of reactive oxygen species and antioxidant defense system in plants: A concise overview. Frontiers in Plant Science, 11, 552969. https://doi.org/10.3389/fpls.2020.552969
doi: 10.3389/fpls.2020.552969
pubmed: 33488637
pmcid: 7815643
Hasanuzzaman, M., Bhuyan, M., Zulfiqar, F., Raza, A., Mohsin, S. M., Mahmud, J. A., Fujita, M., & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants (Basel, Switzerland), 9(8), 681. https://doi.org/10.3390/antiox9080681
doi: 10.3390/antiox9080681
pubmed: 32751256
Neumann, C. A., & Fang, Q. (2007). Are Prxs tumor suppressors? Current Opinion in Pharmacology, 7(4), 375–380. https://doi.org/10.1016/j.coph.2007.04.007
doi: 10.1016/j.coph.2007.04.007
pubmed: 17616437
Rhee, S. G., Kang, S. W., Chang, T. S., Jeong, W., & Kim, K. (2001). Prx, a novel family of peroxidases. IUBMB Life, 52(1–2), 35–41. https://doi.org/10.1080/15216540252774748
doi: 10.1080/15216540252774748
pubmed: 11795591
Rhee, S. G. (2016). Overview on Prx. Molecules and Cells, 39(1), 1–5. https://doi.org/10.14348/molcells.2016.2368
doi: 10.14348/molcells.2016.2368
pubmed: 26831451
pmcid: 4749868
Portillo-Ledesma, S., Randall, L. M., Parsonage, D., Dalla Rizza, J., Karplus, P. A., Poole, L. B., Denicola, A., & Ferrer-Sueta, G. (2018). Differential kinetics of two-cysteine peroxiredoxin disulfide formation reveal a novel model for peroxide sensing. Biochem, 57(24), 3416–3424. https://doi.org/10.1021/acs.biochem.8b00188
doi: 10.1021/acs.biochem.8b00188
Dalla Rizza, J., Randall, L. M., Santos, J., Ferrer-Sueta, G., & Denicola, A. (2019). Differential parameters between cytosolic 2-Cys peroxiredoxins, PRDX1 and PRDX2. Protein Science, 28(1), 191–201. https://doi.org/10.1002/pro.3520
doi: 10.1002/pro.3520
pubmed: 30284335
Gupta, D. N., Dalal, V., Savita, B. K., Alam, M. S., Singh, A., Gubyad, M., Ghosh, D. K., Kumar, P. & Sharma, A. K. (2022). Biochemical characterization and structure-based in silico screening of potent inhibitor molecules against the 1 Cys peroxiredoxin of bacterioferritin comigratory protein family from Candidatus Liberibacter asiaticus, Journal of Biomolecular Structure and Dynamics, 1–13, Advance online publication. https://doi.org/10.1080/07391102.2022.2096118
Nelson, K. J., Knutson, S. T., Soito, L., Klomsiri, C., Poole, L. B., & Fetrow, J. S. (2011). Analysis of the peroxiredoxin family: Using active-site structure and sequence information for global classification and residue analysis. Proteins, 79(3), 947–964. https://doi.org/10.1002/prot.22936
doi: 10.1002/prot.22936
pubmed: 21287625
Hall, A., Nelson, K., Poole, L. B., & Karplus, P. A. (2011). Structure-based insights into the catalytic power and conformational dexterity of peroxiredoxins. Antioxidants & Redox Signaling, 15(3), 795–815. https://doi.org/10.1089/ars.2010.3624
doi: 10.1089/ars.2010.3624
Auf dem Keller, U., Kümin, A., Braun, S., & Werner, S. (2006). Reactive oxygen species and their detoxification in healing skin wounds. Journal of Investigative Dermatology Symposium Proceedings, 11(1), 106–111. https://doi.org/10.1038/sj.jidsymp.5650001
doi: 10.1038/sj.jidsymp.5650001
pubmed: 17069017
Kinnula, V. L., Soini, Y., Kvist-Mäkelä, K., Savolainen, E. R., & Koistinen, P. (2002). Antioxidant defense mechanisms in human neutrophils. Antioxidants & Redox Signaling, 4(1), 27–34. https://doi.org/10.1089/152308602753625825
doi: 10.1089/152308602753625825
Gupta, D. N., Rani, R., Kokane, A. D., Ghosh, D. K., Tomar, S., & Sharma, A. K. (2022). Characterization of a cytoplasmic 2-Cys peroxiredoxin from Citrus sinensis and its potential role in protection from oxidative damage and wound healing. International Journal of Biological Macromolecules, 209(Pt A), 1088–1099. https://doi.org/10.1016/j.ijbiomac.2022.04.086
doi: 10.1016/j.ijbiomac.2022.04.086
pubmed: 35452700
Wink, M. (2015). Modes of Action of herbal medicines and plant secondary metabolites. Medicines (Basel, Switzerland), 2(3), 251–286. https://doi.org/10.3390/medicines2030251
doi: 10.3390/medicines2030251
pubmed: 28930211
pmcid: 5456217
Haraldsen, J. D., Liu, G., Botting, C. H., Walton, J. G., Storm, J., Phalen, T. J., Kwok, L. Y., Soldati-Favre, D., Heintz, N. H., Müller, S., Westwood, N. J., & Ward, G. E. (2009). Identification of conoidin A as a covalent inhibitor of peroxiredoxin II. Organic & Biomolecular Chemistry, 7, 3040–3048. https://doi.org/10.1039/B901735F
doi: 10.1039/B901735F
Nguyen, J. B., Pool, C. D., Wong, C. Y., Treger, R. S., Williams, D. L., Cappello, M., Lea, W. A., Simeonov, A., Vermeire, J. J., & Modis, Y. (2013). Peroxiredoxin-1 from the human hookworm Ancylostoma ceylanicum forms a stable oxidized decamer and is covalently inhibited by conoidin A. Chemistry & Biology, 20(8), 991–1001. https://doi.org/10.1016/j.chembiol.2013.06.011
doi: 10.1016/j.chembiol.2013.06.011
Liu, Z., Ma, L., & Zhou, G. B. (2011). The main anticancer bullets of the Chinese medicinal herb, thunder god vine. Molecules (Basel, Switzerland), 16(6), 5283–5297. https://doi.org/10.3390/molecules16065283
doi: 10.3390/molecules16065283
pubmed: 21701438
Chen, X., Zhao, Y., Luo, W., Chen, S., Lin, F., Zhang, X., Fan, S., Shen, X., Wang, Y., & Liang, G. (2020). Celastrol induces ROS-mediated apoptosis via directly targeting peroxiredoxin-2 in gastric cancer cells. Theranostics, 10(22), 10290–10308. https://doi.org/10.7150/thno.46728
doi: 10.7150/thno.46728
pubmed: 32929349
pmcid: 7481428
Singh, A., Kumar, N., Tomar, P., Bhose, S., Ghosh, D. K., Roy, P., & Sharma, A. K. (2017). Characterization of a bacterioferritin comigratory protein family 1-Cys peroxiredoxin from Candidatus Liberibacter asiaticus. Protoplasma, 254(4), 1675–1691. https://doi.org/10.1007/s00709-016-1062-z
doi: 10.1007/s00709-016-1062-z
pubmed: 27987036
Savita, B. K., Dalal, V., Choudhary, S., Gupta, D. N., Das, N., Tomar, S., Kumar, P., Roy, P., & Sharma, A. K. (2021). Characterization of recombinant pumpkin 2S albumin and mutation studies to unravel potential DNA/RNA binding site. Biochemical and Biophysical Research Communications, 580, 28–34. https://doi.org/10.1016/j.bbrc.2021.09.076
doi: 10.1016/j.bbrc.2021.09.076
pubmed: 34610489
Thurman, R. G., Ley, H. G., & Scholz, R. (1972). Hepatic microsomal ethanol oxidation. Hydrogen peroxide formation and the role of catalase. European Journal of Biochemistry., 25(3), 420–430. https://doi.org/10.1111/j.1432-1033.1972.tb01711.x
doi: 10.1111/j.1432-1033.1972.tb01711.x
pubmed: 4402915
Sharma, S., Gupta, D. N., Kushwah, A. S., Sharma, A. K., & Prasad, R. (2023). Identification and characterization of the Cyamopsis tetragonoloba transcription factor MYC (CtMYC) under drought stress. Gene, 882, 147654. https://doi.org/10.1016/j.gene.2023.147654
doi: 10.1016/j.gene.2023.147654
pubmed: 37479095
Kumar, V., Sharma, A., Pratap, S., & Kumar, P. (2018). Biochemical and biophysical characterization of 1,4-naphthoquinone as a dual inhibitor of two key enzymes of type II fatty acid biosynthesis from Moraxella catarrhalis. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, 1866(11), 1131–1142. https://doi.org/10.1016/j.bbapap.2018.08.008
doi: 10.1016/j.bbapap.2018.08.008
pubmed: 30282611
Verma, P., Kar, B., Varshney, R., Roy, P., & Sharma, A. K. (2017). Characterization of AICAR transformylase/IMP cyclohydrolase (ATIC) from Staphylococcus lugdunensis. FEBS Letters, 24, 4233–4261. https://doi.org/10.1111/febs.14303
doi: 10.1111/febs.14303
Kumar, P., Kesari, P., Kokane, S., Ghosh, D. K., Kumar, P., & Sharma, A. K. (2019). Crystal structures of a putative periplasmic cystine-binding protein from Candidatus Liberibacter asiaticus: Insights into an adapted mechanism of ligand binding. FEBS Letters, 286(17), 3450–3472. https://doi.org/10.1111/febs.14921
doi: 10.1111/febs.14921
Gunnarsson, A., Stubbs, C. J., Rawlins, P. B., Taylor-Newman, E., Lee, W. C., Geschwindner, S., Hytönen, V., Holdgate, G., Jha, R., & Dahl, G. (2021). Regenerable biosensors for small-molecule kinetic characterization using SPR. SLAS Discovery, 26(5), 730–739. https://doi.org/10.1177/2472555220975358
doi: 10.1177/2472555220975358
pubmed: 33289457
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., Ballard, A. J., Cowie, A., Romera-Paredes, B., Nikolov, S., Jain, R., Adler, J., Back, T., … Hassabis, D. (2021). Highly accurate protein structure prediction with AlphaFold. Nature, 596(7873): 583–589. https://doi.org/10.1038/s41586-021-03819-2
Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
doi: 10.1002/jcc.21256
pubmed: 19399780
pmcid: 2760638
Saini, G., Dalal, V., Gupta, D. N., Sharma, N., Kumar, P., & Sharma, A. K. (2021). A molecular docking and dynamic approach to screen inhibitors against ZnuA1 of Candidatus Liberibacter asiaticus. Molecular Simulation, 47(6), 510–525. https://doi.org/10.1080/08927022.2021.1888948
doi: 10.1080/08927022.2021.1888948
Gupta, D. N., Dalal, V., Savita, B. K., Dhankhar, P., Ghosh, D. K., Kumar, P., & Sharma, A. K. (2021). In-silico screening and identification of potential inhibitors against 2Cys peroxiredoxin of Candidatus Liberibacter asiaticus, Journal of Biomolecular Structure and Dynamics, 1–15. https://doi.org/10.1080/07391102.2021.1916597
Alam, M. S., Sharma, M., Kumar, R., Das, J., Rode, S., Kumar, P., Prasad, R., & Sharma, A. K. (2022). In-silico identification of potential phytochemical inhibitors targeting farnesyl diphosphate synthase of cotton bollworm (Helicoverpa armigera). Journal of Biomolecular Structure and Dynamics, 1–10, Advance online publication. https://doi.org/10.1080/07391102.2022.2025904
Skolnick, J., Gao, M., Zhou, H., & Singh, S. (2021). AlphaFold 2: Why it works and its implications for understanding the relationships of protein sequence, structure, and function. Journal of Chemical Information and Modeling, 61(10), 4827–4831. https://doi.org/10.1021/acs.jcim.1c01114
doi: 10.1021/acs.jcim.1c01114
pubmed: 34586808
pmcid: 8592092
David, A., Islam, S., Tankhilevich, E., & Sternberg, M. (2022). The AlphaFold database of protein structures: A biologist’s guide. Journal of Molecular Biology, 434(2), 167336. https://doi.org/10.1016/j.jmb.2021.167336
doi: 10.1016/j.jmb.2021.167336
pubmed: 34757056
pmcid: 8783046
Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31(4), 671–690. https://doi.org/10.1002/jcc.21367
doi: 10.1002/jcc.21367
pubmed: 19575467
pmcid: 2888302
Vanommeslaeghe, K., & MacKerell, A. D. (2012). Automation of the CHARMM General Force Field (CGenFF) I: Bond perception and atom typing. Journal of Chemical Information and Modeling, 52(12), 3144–3154. https://doi.org/10.1021/ci300363c
doi: 10.1021/ci300363c
pubmed: 23146088
pmcid: 3528824
Berendsen, H. J., Postma, J. V., Van Gunsteren, W. F., DiNola, A., & Haak, J. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
doi: 10.1063/1.448118
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
doi: 10.1063/1.328693
Siligardi, G., Hussain, R., Patching, S. G., & Phillips-Jones, M. K. (2014). Ligand- and drug-binding studies of membrane proteins revealed through circular dichroism spectroscopy. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1838(1 Pt A), 34–42. https://doi.org/10.1016/j.bbamem.2013.06.019
doi: 10.1016/j.bbamem.2013.06.019
pubmed: 23811229
Ali, S. S., Zia, M. K., Siddiqui, T., Ahsan, H., & Khan, F. H. (2020). Bilirubin binding affects the structure and function of alpha-2-macroglobulin. Journal of Immunoassay & Immunochemistry, 41(5), 841–851. https://doi.org/10.1080/15321819.2020.1783290
doi: 10.1080/15321819.2020.1783290
Matveeva, E. G., Morisseau, C., Goodrow, M. H., Mullin, C., & Hammock, B. D. (2009). Tryptophan fluorescence quenching by enzyme inhibitors as a tool for enzyme active site structure investigation: Epoxide hydrolase. Current Pharmaceutical Biotechnology, 10(6), 589–599. https://doi.org/10.2174/138920109789069260
doi: 10.2174/138920109789069260
pubmed: 19619123
pmcid: 2861369
Sedov, I., Nikiforova, A., & Khaibrakhmanova, D. (2020). Evaluation of the binding properties of drugs to albumin from DSC thermograms. International Journal of Pharmaceutics, 583, 119362. https://doi.org/10.1016/j.ijpharm.2020.119362
doi: 10.1016/j.ijpharm.2020.119362
pubmed: 32334069
Linkuvienė, V., Zubrienė, A., & Matulis, D. (2022). Intrinsic affinity of protein-ligand binding by differential scanning calorimetry. Biochim. Biophys. Acta - Proteins Proteom., 1870(9), 140830. https://doi.org/10.1016/j.bbapap.2022.140830
doi: 10.1016/j.bbapap.2022.140830
pubmed: 35934299
Lonare, S., Sharma, M., Dalal, V., Gubyad, M., Kumar, P., Gupta, Deena Nath, Pareek, A., Tomar, S., Kumar Ghosh, D., Kumar, P., & Kumar Sharma, A. (2023). Identification and evaluation of potential inhibitor molecules against TcyA from Candidatus Liberibacter asiaticus. Journal of Structural Biology, 215(3), 107992. https://doi.org/10.1016/j.jsb.2023.107992
doi: 10.1016/j.jsb.2023.107992
pubmed: 37394197