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Research Article

The Amaryllidaceae alkaloid, montanine, is a potential inhibitor of the Trypanosoma cruzi trans-sialidase enzyme

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Received 11 Jul 2023, Accepted 10 Aug 2023, Published online: 23 Oct 2023

References

  • Akakpo, L., Gasu, E. N., Mensah, J. O., & Borquaye, L. S. (2023). Oplodiol and nitidine as potential inhibitors of Plasmodium falciparum dihydrofolate reductase: Insights from a computational study. Journal of Biomolecular Structure & Dynamics, 0(0), 1–15. https://doi.org/10.1080/07391102.2023.2212815
  • Aldasoro, E., Posada, E., Requena-Méndez, A., Calvo-Cano, A., Serret, N., Casellas, A., Sanz, S., Soy, D., Pinazo, J., & Gascon, J. (2018). What to expect and when: Benznidazole toxicity in chronic Chagas’ disease treatment. The Journal of Antimicrobial Chemotherapy, 73(4), 1060–1067. https://doi.org/10.1093/jac/dkx516
  • Amaya, M. F., Watts, A. G., Damager, I., Wehenkel, A., Nguyen, T., Buschiazzo, A., Paris, G., Frasch, A. C., Withers, S. G., & Alzari, P. M. (2004). Structural insights into the catalytic mechanism of Trypanosoma cruzi trans-sialidase. Structure (London, England: 1993), 12(5), 775–784. https://doi.org/10.1016/j.str.2004.02.036
  • Amusengeri, A., Tata, R. B., & Bishop, Ö. T. (2020). Understanding the pyrimethamine drug resistance mechanism via combined molecular dynamics and dynamic residue network analysis. Molecules (Basel, Switzerland), 25(4), 904. https://doi.org/10.3390/molecules25040904
  • Basile, L., Jansá, J. M., Carlier, Y., Salamanca, D. D., Angheben, A., Bartoloni, A., Seixas, J., Van Gool, T., Cañavate, C., Flores-Chávez, M., Jackson, Y., Chiodini, P. L., Albajar-Viñas, P., & Working Group On Chagas Disease, C. (2011). Chagas disease in European countries: The challenge of a surveillance system. Eurosurveillance, 16(37), 3. https://doi.org/10.2807/ese.16.37.19968-en
  • Boakye, A., Gasu, E. N., Mensah, J. O., & Borquaye, L. S. (2023). Computational studies on potential small molecule inhibitors of Leishmania pteridine reductase 1. Journal of Biomolecular Structure & Dynamics, 0(0), 1–14. https://doi.org/10.1080/07391102.2023.2166119
  • Borquaye, L. S., Gasu, E. N., Ampomah, G. B., Kyei, L. K., Amarh, M. A., Mensah, C. N., Nartey, D., Commodore, M., Adomako, A. K., Acheampong, P., Mensah, J. O., Mormor, D. B., & Aboagye, C. I. (2020). Alkaloids from Cryptolepis sanguinolenta as potential inhibitors of SARS-CoV-2 viral proteins: An in silico study. BioMed Research International, 2020, 5324560–5324514. https://doi.org/10.1155/2020/5324560
  • Buschiazzo, A., Amaya, M. F., Cremona, M. L., Frasch, A. C., & Alzari, P. M. (2002). The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Molecular Cell, 10(4), 757–768. https://doi.org/10.1016/S1097-2765(02)00680-9
  • Campetella, O. E., Uttaro, A. D., Parodi, A. J., & Frasch, A. C. C. (1994). A recombinant Trypanosoma cruzi trans-sialidase lacking the amino acid repeats retains the enzymatic activity. Molecular and Biochemical Parasitology, 64(2), 337–340. https://doi.org/10.1016/0166-6851(94)00036-0
  • Damager, I., Buchini, S., Amaya, M. F., Buschiazzo, A., Alzari, P., Frasch, A. C., Watts, A., & Withers, S. G. (2008). Kinetic and mechanistic analysis of Trypanosoma cruzi trans-sialidase reveals a classical ping-pong mechanism with acid/base catalysis. Biochemistry, 47(11), 3507–3512. https://doi.org/10.1021/bi7024832
  • De Lederkremer, R. M., Giorgi, M. E., & Agusti, R. (2022). trans -Sialylation: A strategy used to incorporate sialic acid into oligosaccharides. RSC Chemical Biology, 3(2), 121–139. https://doi.org/10.1039/d1cb00176k
  • Demir, Ö., & Roitberg, A. E. (2009). Modulation of catalytic function by differential plasticity of the active site: Case study of Trypanosoma cruzi trans-sialidase and Trypanosoma rangeli sialidase. Biochemistry, 48(15), 3398–3406. https://doi.org/10.1021/bi802230y
  • Forli, S., Huey, R., Pique, M. E., Sanner, M., Goodsell, D. S., & Arthur, J. (2016). Computational protein-ligand docking and virtual drug screening with the AutoDock suite. Nature Protocols, 11(5), 905–919. https://doi.org/10.1038/nprot.2016.051.Computational
  • Gaskell, A., Crennell, S., & Taylor, G. (1995). The three domains of a bacterial sialidase: A (3-propeller, an immunoglobulin module and a galactose-binding jelly-roll. Structure, 15(11):1197–205.
  • Hall, B. S., & Wilkinson, S. R. (2012). Activation of benznidazole by trypanosomal type I nitroreductases results in glyoxal formation. Antimicrobial Agents and Chemotherapy, 56(1), 115–123. https://doi.org/10.1128/AAC.05135-11
  • Irigoín, F., Cibils, L., Comini, M. A., Wilkinson, S. R., Flohé, L., & Radi, R. (2008). Insights into the redox biology of Trypanosoma cruzi: Trypanothione metabolism and oxidant detoxification. Free Radical Biology & Medicine, 45(6), 733–742. https://doi.org/10.1016/j.freeradbiomed.2008.05.028
  • Kashif, M., Moreno-Herrera, A., Villalobos-Rocha, J. C., Nogueda-Torres, B., Pérez-Villanueva, J., Rodríguez-Villar, K., Medina-Franco, J. L., De Andrade, P., Carvalho, I., & Rivera, G. (2017). Benzoic acid derivatives with trypanocidal activity: Enzymatic analysis and molecular docking studies toward trans-sialidase. Molecules (Basel, Switzerland), 22(11), 1863. https://doi.org/10.3390/molecules22111863
  • Kashif, M., Chacón-Vargas, K. F., López-Cedillo, J. C., Nogueda-Torres, B., Paz-González, A. D., Ramírez-Moreno, E., Agusti, R., Uhrig, M. L., Reyes-Arellano, A., Peralta-Cruz, J., Ashfaq, M., & Rivera, G. (2018). Synthesis, molecular docking and biological evaluation of novel phthaloyl derivatives of 3-amino-3-aryl propionic acids as inhibitors of Trypanosoma cruzi trans-sialidase. European Journal of Medicinal Chemistry, 156, 252–268. https://doi.org/10.1016/j.ejmech.2018.07.005
  • Kumari, R., Kumar, R., & Lynn, A. (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
  • Kutzner, C., Páll, S., Fechner, M., Esztermann, A., de Groot, B. L., & Grubmüller, H. (2019). More bang for your buck: Improved use of GPU nodes for GROMACS 2018. Journal of Computational Chemistry, 40(27), 2418–2431. https://doi.org/10.1002/jcc.26011
  • Kyei, L. K., Gasu, E. N., Ampomah, G. B., Mensah, J. O., & Borquaye, L. S. (2022). An in silico study of the interactions of alkaloids from Cryptolepis sanguinolenta with Plasmodium falciparum dihydrofolate reductase and dihydroorotate dehydrogenase. Journal of Chemistry, 2022, e5314179–26. https://doi.org/10.1155/2022/5314179
  • Machado, F. S., Dutra, W. O., Esper, L., Gollob, K. J., Teixeira, M. M., Factor, S. M., Weiss, L. M., Nagajyothi, F., Tanowitz, H. B., & Garg, N. J. (2012). Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Seminars in Immunopathology, 34(6), 753–770. https://doi.org/10.1007/s00281-012-0351-7
  • Martínez-Peinado, N., Cortes-Serra, N., Tallini, L. R., Pinazo, M. J., Gascon, J., Bastida, J., & Alonso-Padilla, J. (2021). Amaryllidaceae plants: A potential natural resource for the treatment of Chagas disease. Parasites & Vectors, 14(1), 337. https://doi.org/10.1186/s13071-021-04837-9
  • Martinez-Peinado, N., Cortes-Serra, N., Torras-Claveria, L., Pinazo, M. J., Gascon, J., Bastida, J., & Alonso-Padilla, J. (2020). Amaryllidaceae alkaloids with anti-Trypanosoma cruzi activity. Parasites & Vectors, 13(1), 299. https://doi.org/10.1186/s13071-020-04171-6
  • Mensah, J. O., Ampomah, G. B., Gasu, E. N., Adomako, A. K., Menkah, E. S., & Borquaye, L. S. (2022). Allosteric modulation of the main protease (MPro) of SARS-CoV-2 by casticin—Insights from molecular dynamics simulations. Chemistry Africa, 5(5), 1305–1320. https://doi.org/10.1007/s42250-022-00411-7
  • Mensah, J. O., Boakye, A., Manu, P., Nketia, P. B., Gasu, E. N., Asiamah, I., & Borquaye, L. S. (2023). Computational studies provide a molecular basis for the quorum sensing inhibitory action of compounds from Dioon spinulosum dyer ex Eichler. ChemistrySelect, 8(1), e202203773. https://doi.org/10.1002/slct.202203773
  • Mitchell, F. L., Miles, S. M., Neres, J., Bichenkova, E. V., & Bryce, R. A. (2010). Tryptophan as a molecular shovel in the glycosyl transfer activity of Trypanosoma cruzi trans-sialidase. Biophysical Journal, 98(9), L38–40. https://doi.org/10.1016/j.bpj.2010.01.006
  • Mitchell, F. L., Neres, J., Ramraj, A., Raju, R. K., Hillier, I. H., Vincent, M. A., & Bryce, R. A. (2013). Insights into the activity and specificity of Trypanosoma cruzi trans -Sialidase from molecular dynamics simulations. Biochemistry, 52(21), 3740–3751. https://doi.org/10.1021/bi301112p
  • Moncayo, Á., & Silveira, A. C. (2017). Current epidemiological trends of Chagas disease in Latin America and future challenges: Epidemiology, surveillance, and health policies. American Trypanosomiasis Chagas Disease: One Hundred Years of Research: Second Edition, 104(May), 59–88. https://doi.org/10.1016/B978-0-12-801029-7.00004-6
  • Nardy, A. F. F. R., Freire-de-Lima, C. G., Pérez, A. R., & Morrot, A. (2016). Role of Trypanosoma cruzi Trans-sialidase on the escape from host immune surveillance. Frontiers in Microbiology, 7(MAR), 348. https://doi.org/10.3389/fmicb.2016.00348
  • Nesmelova, I. V., Ermakova, E., Daragan, V. A., Pang, M., Menéndez, M., Lagartera, L., Solís, D., Baum, L. G., Mayo, K. H., & Carolina, N. (2010). Lactose binding to galectin-1 modulates structural dynamics, increases conformational entropy, and occurs with apparent negative cooperativity. Journal of Molecular Biology, 397(5), 1209–1230. https://doi.org/10.1016/j.jmb.2010.02.033
  • Oliveira, I. A., Freire-de-Lima, L., Penha, L. L., Dias, W. B., Todeschini, A. R. (2014). Trypanosoma cruzi Trans-Sialidase: Structural Features and Biological Implications. In Santos, A., Branquinha, M., d’Avila-Levy, C., Kneipp, L., Sodré, C. (Eds.), Proteins and Proteomics of Leishmania and Trypanosoma. Subcellular Biochemistry (vol. 74). Dordrecht: Springer. https://doi.org/10.1007/978-94-007-7305-9_8
  • Paris, G., Cremona, M. L., Amaya, M. F., Buschiazzo, A., Giambiagi, S., Frasch, A. C. C., & Alzari, P. M. (2001). Probing molecular function of trypanosomal sialidases: Single point mutations can change substrate specificity and increase hydrolytic activity. In Glycobiology, 11 (4), 305–311. https://doi.org/10.1093/glycob/11.4.305
  • Pérez-Molina, J. A., & Molina, I. (2018). Chagas disease. The Lancet. 391, (10115), 82–94. https://doi.org/10.1016/S0140-6736(17)31612-4
  • Pollevick, G. D., Affranchino, J. L., Frasch, A. C. C., Snchez, D. O., Frasch, C. A. C. C., In, I. D., Campomar, F., & Aires, B. (1991). The complete sequence of a shed acute-phase antigen of Trypanosoma cruzi the American parasite Trypanosoma cruzi has a number of molecules able to elicit an antibody response in the infected host [1]. Molecular and Biochemical Parasitology, 47(2), 247–250. https://doi.org/10.1016/0166-6851(91)90185-9
  • Presley, C. C., Krai, P., Dalal, S., Su, Q., Cassera, M., Goetz, M., & Kingston, D. G. I. (2016). New potently bioactive alkaloids from Crinum erubescens. Bioorganic & Medicinal Chemistry, 24(21), 5418–5422. https://doi.org/10.1016/j.bmc.2016.08.058
  • Requena-Méndez, A., Aldasoro, E., de Lazzari, E., Sicuri, E., Brown, M., Moore, D. A. J., Gascon, J., & Muñoz, J. (2015). Prevalence of chagas disease in Latin-American migrants living in Europe: A systematic review and meta-analysis. PLoS Neglected Tropical Diseases, 9(2), e0003540. https://doi.org/10.1371/journal.pntd.0003540
  • Roggentin, P., Rothe, B., Kaper, J. B., Galen, J., Vlmr, L. E. R., Schauer, R., I., B., Kiel, D., & Germany, W. (1989). Conserved sequences in bacterial and viral sialidases. Glycoconjugate Journal, 6(3), 349–353. https://doi.org/10.1007/BF01047853
  • Schenkman, B. S., Carvalho, L. P. D., & Nussenzweig, V. (1992). Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes. Journal of Experimental Medicine, 175(February), 567–575.
  • Tallini, L. R., Andrade, J. P. d., Kaiser, M., Viladomat, F., Nair, J. J., Zuanazzi, J. A. S., & Bastida, J. (2017). Alkaloid constituents of the amaryllidaceae plant Amaryllis belladonna L. Molecules (Basel, Switzerland), 22(9), 1437. https://doi.org/10.3390/molecules22091437
  • Taylor, G. (1996). Sialidases: Structures, biological significance and therapeutic potential. Current Opinion in Structural Biology, 6(6), 830–837. https://doi.org/10.1016/s0959-440x(96)80014-5
  • Tian, W., Chen, C., Lei, X., Zhao, J., & Liang, J. (2018). CASTp 3.0: Computed atlas of surface topography of proteins. Nucleic Acids Research, 46(W1), W363–W367. https://doi.org/10.1093/nar/gky473
  • Xu, Y., Wang, S., Hu, Q., Gao, S., Ma, X., Zhang, W., Shen, Y., Chen, F., Lai, L., & Pei, J. (2018). CavityPlus: A web server for protein cavity detection with pharmacophore modelling, allosteric site identification and covalent ligand binding ability prediction. Nucleic Acids Research, 46(W1), W374–W379. https://doi.org/10.1093/nar/gky380

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