125
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Identification of starvation-mimetic bioactive phytocomponent from Withania somnifera using in-silico molecular modelling and flow cytometry-based analysis for the management of malaria

, , , , , , , & show all
Pages 528-549 | Received 15 Feb 2023, Accepted 15 Mar 2023, Published online: 23 Apr 2023

References

  • Ahmad Fuad, F. A., & Ogu Salim, N. (2022). Analogues of oxamate, pyruvate, and lactate as potential inhibitors of Plasmodium knowlesi lactate dehydrogenase identified using virtual screening and verified via inhibition assays. Processes, 10(11), 2443. https://doi.org/10.3390/pr10112443
  • Alqahtani, M. S., Kazi, M., Alsenaidy, M. A., & Ahmad, M. Z. (2021). Advances in oral drug delivery. Frontiers in Pharmacology, 12, 618411. https://doi.org/10.3389/fphar.2021.618411
  • Ascenzi, P., Fanali, G., Fasano, M., Pallottini, V., & Trezza, V. (2014). Clinical relevance of drug binding to plasma proteins. Journal of Molecular Structure, 1077, 4–13. https://doi.org/10.1016/j.molstruc.2013.09.053
  • Cameron, A., Read, J., Tranter, R., Winter, V. J., Sessions, R. B., Brady, R. L., Vivas, L., Easton, A., Kendrick, H., Croft, S. L., Barros, D., Lavandera, J. L., Martin, J. J., Risco, F., García-Ochoa, S., Gamo, F. J., Sanz, L., Leon, L., Ruiz, J. R., … Gómez de las Heras, F. (2004). Identification and activity of a series of azole-based compounds with lactate dehydrogenase-directed anti-malarial activity. The Journal of Biological Chemistry, 279(30), 31429–31439. https://doi.org/10.1074/jbc.M402433200
  • Chakraborti, S. K., De, B. K., & Bandyopadhyay, T. (1974). Variations in the antitumour constituents of Withania somnifera Dunal. Experientia, 30(8), 852–853. https://doi.org/10.1007/BF01938320
  • Chen, Y., Rosenkranz, C., Hirte, S., & Kirchmair, J. (2022). Ring systems in natural products: Structural diversity, physicochemical properties, and coverage by synthetic compounds. Natural Product Reports, 39(8), 1544–1556. https://doi.org/10.1039/d2np00001f
  • Dey, A., Chatterjee, S., & Kumar, V. (2018). Triethylene glycol-like effects of Ashwagandha (Withania somnifera (L.) Dunal) root extract devoid of withanolides in stressed mice. Ayu, 39(4), 230–238. https://doi.org/10.4103/ayu.AYU_219_16
  • Evans, B. C., Nelson, C. E., Yu, S. S., Beavers, K. R., Kim, A. J., Li, H., Nelson, H. M., Giorgio, T. D., & Duvall, C. L. (2013). Ex vivo red blood cell hemolysis assay for the evaluation of pH-responsive endosomolytic agents for cytosolic delivery of biomacromolecular drugs. Journal of Visualized Experiments, 9(73), e50166.
  • Genheden, S., & Ryde, U. (2015). The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opinion on Drug Discovery, 10(5), 449–461. https://doi.org/10.1517/17460441.2015.1032936
  • Gupta, S. K., Jadhav, S., Gohil, D., Panigrahi, G. C., Kaushal, R. K., Gandhi, K., Patil, A., Chavan, P., & Gota, V. (2022). Safety, toxicity and pharmacokinetic assessment of oral Withaferin-A in mice. Toxicology Reports, 9, 1204–1212. https://doi.org/10.1016/j.toxrep.2022.05.012
  • Hapuarachchi, S. V., Cobbold, S. A., Shafik, S. H., Dennis, A. S., McConville, M. J., Martin, R. E., Kirk, K., & Lehane, A. M. (2017). The malaria parasite’s lactate transporter PfFNT is the target of antiplasmodial compounds identified in whole cell phenotypic screens. PLoS Pathogens, 13(2), e1006180. https://doi.org/10.1371/journal.ppat.1006180
  • Heikham, K. D., Gupta, A., Kumar, A., Singh, C., Saxena, J., Srivastava, K., Puri, S. K., Dwivedi, A. K., Habib, S., & Misra, A. (2015). Preferential targeting of human erythrocytes infected with the malaria parasite Plasmodium falciparum via hexose transporter surface proteins. International Journal of Pharmaceutics, 483(1–2), 57–62. https://doi.org/10.1016/j.ijpharm.2015.02.011
  • Heitmeier, M. R., Hresko, R. C., Edwards, R. L., Prinsen, M. J., Ilagan, M. X. G., Odom John, A. R., & Hruz, P. W. (2019). Identification of druggable small molecule antagonists of the Plasmodium falciparum hexose transporter PfHT and assessment of ligand access to the glucose permeation pathway via FLAG-mediated protein engineering. PloS One, 14(5), e0216457. https://doi.org/10.1371/journal.pone.0216457
  • Huang, J., Yuan, Y., Zhao, N., Pu, D., Tang, Q., Zhang, S., Luo, S., Yang, X., Wang, N., Xiao, Y., Zhang, T., Liu, Z., Sakata-Kato, T., Jiang, X., Kato, N., Yan, N., & Yin, H. (2021). Orthosteric-allosteric dual inhibitors of PfHT1 as selective antimalarial agents. Proceedings of the National Academy of Sciences, 118(3), e2017749118. https://doi.org/10.1073/pnas.2017749118
  • Islam, M. M., Rohman, M. A., Gurung, A. B., Bhattacharjee, A., Aguan, K., & Mitra, S. (2018). Correlation of cholinergic drug induced quenching of acetylcholinesterase bound thioflavin-T fluorescence with their inhibition activity. Spectrochimica Acta. Part A, Molecular and Biomolecular Spectroscopy, 189, 250–257. https://doi.org/10.1016/j.saa.2017.08.009
  • Ivanova, L., Tammiku-Taul, J., García-Sosa, A. T., Sidorova, Y., Saarma, M., & Karelson, M. (2018). Molecular dynamics simulations of the interactions between glial cell line-derived neurotrophic factor family receptor GFRα1 and small-molecule ligands. ACS Omega, 3(9), 11407–11414. https://doi.org/10.1021/acsomega.8b01524
  • Jiang, X. (2022). An overview of the Plasmodium falciparum hexose transporter and its therapeutic interventions. Proteins, 90(10), 1766–1778. https://doi.org/10.1002/prot.26351
  • Jiang, X., Yuan, Y., Huang, J., Zhang, S., Luo, S., Wang, N., Pu, D., Zhao, N., Tang, Q., Hirata, K., Yang, X., Jiao, Y., Sakata-Kato, T., Wu, J.-W., Yan, C., Kato, N., Yin, H., & Yan, N. (2020). Structural basis for blocking sugar uptake into the malaria parasite Plasmodium falciparum. Cell, 183(1), 258–268. https://doi.org/10.1016/j.cell.2020.08.015
  • Joshi, N., Hada, R., Gupta, S., Khan, J., Dobrowolski, J., Dhar, P. K., Kumar, N., & Singh, S. (2022). Highly potent anti-malarial activity of benzopyrano (4, 3-b) benzopyran derivatives and in silico interaction analysis with putative target Plasmodium falciparum lactate dehydrogenase. Journal of Biomolecular Structure & Dynamics, 40(11), 5159–5174. https://doi.org/10.1080/07391102.2020.1868336
  • Kalita, J., Chetia, D., & Rudrapal, M. (2020). Design, synthesis, antimalarial activity and docking study of 7-chloro-4- (2-(substituted benzylidene)hydrazineyl)quinolines. Medicinal Chemistry (Shariqah (United Arab Emirates)), 16(7), 928–937. https://doi.org/10.2174/1573406415666190806154722
  • Kasschau, M. R., Byam-Smith, M. P., Gentry, D. S., & Watson, F. N. (1995). Influence of pH and temperature on hemolysis by adult Schistosoma mansoni membranes. The Journal of Experimental Zoology, 271(4), 315–322. https://doi.org/10.1002/jez.1402710409
  • Ko, D. H., Won, D., Jeong, T. D., Lee, W., Chun, S., & Min, W. K. (2015). Comparison of red blood cell hemolysis using plasma and serum separation tubes for outpatient specimens. Annals of Laboratory Medicine, 35(2), 194–197. https://doi.org/10.3343/alm.2015.35.2.194
  • Kraft, T. E., Armstrong, C., Heitmeier, M. R., Odom, A. R., & Hruz, P. W. (2015). The glucose transporter PfHT1 is an antimalarial target of the HIV protease inhibitor lopinavir. Antimicrobial Agents and Chemotherapy, 59(10), 6203–6209. https://doi.org/10.1128/AAC.00899-15
  • Kulkeaw, K., Ketprasit, N., Tungtrongchitr, A., & Palasuwan, D. (2020). A simple monochromatic flow cytometric assay for assessment of intraerythrocytic development of Plasmodium falciparum. Malaria Journal, 19(1), 13. https://doi.org/10.1186/s12936-020-03156-1
  • Kumar, B., Kalvala, A., Chu, S., Rosen, S., Forman, S. J., Marcucci, G., Chen, C.-C., & Pullarkat, V. (2017). Antileukemic activity and cellular effects of the antimalarial agent artesunate in acute myeloid leukemia. Leukemia Research, 59, 124–135. https://doi.org/10.1016/j.leukres.2017.05.007
  • Kyakulaga, A. H. (2019). Therapeutic potential of Withaferin A against non-small cell lung cancer. University of Louisville.
  • Lawson, A. D., MacCoss, M., & Heer, J. P. (2017). Importance of rigidity in designing small molecule drugs to tackle protein–protein interactions (PPIs) through stabilization of desired conformers: Miniperspective. Journal of Medicinal Chemistry, 61(10), 4283–4289. https://doi.org/10.1021/acs.jmedchem.7b01120
  • Manoharan, S., Panjamurthy, K., Pugalendi, P., Balakrishnan, S., Rajalingam, K., Vellaichamy, J., & Alias, L. (2009). Protective role of Withaferin-A on red blood cell integrity during 7, 12-dimethylbenz [a] anthracene induced oral carcinogenesis. African Journal of Traditional, Complementary and Alternative Medicines, 6(1).
  • Meireles, P., Sales‐Dias, J., Andrade, C. M., Mello‐Vieira, J., Mancio‐Silva, L., Simas, J. P., Staines, H. M., & Prudêncio, M. (2017). GLUT1‐mediated glucose uptake plays a crucial role during Plasmodium hepatic infection. Cellular Microbiology, 19(2), e12646. https://doi.org/10.1111/cmi.12646
  • Mesdaghinia, A., Pourpak, Z., Naddafi, K., Nodehi, R. N., Alizadeh, Z., Rezaei, S., Mohammadi, A., & Faraji, M. (2019). An in vitro method to evaluate hemolysis of human red blood cells (RBCs) treated by airborne particulate matter (PM10). MethodsX, 6, 156–161. https://doi.org/10.1016/j.mex.2019.01.001
  • Miao, J., & Cui, L. (2011). Rapid isolation of single malaria parasite-infected red blood cells by cell sorting. Nature Protocols, 6(2), 140–146. https://doi.org/10.1038/nprot.2010.185
  • Moradi, M., Golmohammadi, R., Najafi, A., Moosazadeh Moghaddam, M., Fasihi-Ramandi, M., & Mirnejad, R. (2022). A contemporary review on the important role of in silico approaches for managing different aspects of COVID-19 crisis. Informatics in Medicine Unlocked, 28, 100862. https://doi.org/10.1016/j.imu.2022.100862
  • Muttaqin, S. S., & Maji, J. S. (2018). Screening of oxamic acid similar 3D structures as candidate inhibitor Plasmodium falciparum L-lactate dehydrogenase of malaria through molecular docking. In 2018 1st International Conference on Bioinformatics, Biotechnology, and Biomedical Engineering-Bioinformatics and Biomedical Engineering (pp. 1–6). IEEE.
  • Ortiz, D., Guiguemde, W. A., Johnson, A., Elya, C., Anderson, J., Clark, J., Connelly, M., Yang, L., Min, J., Sato, Y., Guy, R. K., & Landfear, S. M. (2015). Identification of selective inhibitors of the Plasmodium falciparum hexose transporter PfHT by screening focused libraries of anti-malarial compounds. PloS One, 10(4), e0123598. https://doi.org/10.1371/journal.pone.0123598
  • Owoloye, A. J., Ligali, F. C., Enejoh, O. A., Musa, A. Z., Aina, O., Idowu, E. T., & Oyebola, K. M. (2022). Molecular docking, simulation and binding free energy analysis of small molecules as Pf HT1 inhibitors. PloS One, 17(8), e0268269. https://doi.org/10.1371/journal.pone.0268269
  • Palmer, C. S., Anzinger, J. J., Butterfield, T. R., McCune, J. M., & Crowe, S. M. (2016). A simple flow cytometric method to measure glucose uptake and glucose transporter expression for monocyte subpopulations in whole blood. Journal of Visualized Experiments. 12(114), e54255.
  • Parikh, S., Gut, J., Istvan, E., Goldberg, D. E., Havlir, D. V., & Rosenthal, P. J. (2005). Antimalarial activity of human immunodeficiency virus type 1 protease inhibitors. Antimicrobial Agents and Chemotherapy, 49(7), 2983–2985. https://doi.org/10.1128/AAC.49.7.2983-2985.2005
  • Penna-Coutinho, J., Cortopassi, W. A., Oliveira, A. A., França, T. C., & Krettli, A. U. (2011). Antimalarial activity of potential inhibitors of Plasmodium falciparum lactate dehydrogenase enzyme selected by docking studies. PloS One, 6(7), e21237. https://doi.org/10.1371/journal.pone.0021237
  • Possemiers, H., Vandermosten, L., & Van den Steen, P. E. (2021). Etiology of lactic acidosis in malaria. PLoS Pathogens, 17(1), e1009122. https://doi.org/10.1371/journal.ppat.1009122
  • Pradhan, D., Biswasroy, P., Sahu, D. K., Ghosh, G., & Rath, G. (2022). Isolation and structure elucidation of a steroidal moiety from Withania somnifera and in silico evaluation of antimalarial efficacy against artemisinin resistance Plasmodium falciparum kelch 13 protein. Journal of Biomolecular Structure and Dynamics, 14, 1–14. https://doi.org/10.1080/07391102.2022.2077448
  • Ram, N., Peak, S. L., Perez, A. R., & Jinwal, U. K. (2021). Implications of Withaferin A in neurological disorders. Neural Regeneration Research, 16(2), 304–305. https://doi.org/10.4103/1673-5374.290894
  • Ramachandran, B., Kesavan, S., & Rajkumar, T. (2016). Molecular modeling and docking of small molecule inhibitors against NEK2. Bioinformation, 12(2), 62–68. https://doi.org/10.6026/97320630012062
  • Roth, E. Jr (1990). Plasmodium falciparum carbohydrate metabolism: A connection between host cell and parasite. Blood Cells, 16(2–3), 453–460. discussion 461–456.
  • Rudrapal, M., Chetia, D., & Singh, V. (2017). Novel series of 1,2,4-trioxane derivatives as antimalarial agents. Journal of Enzyme Inhibition and Medicinal Chemistry, 32(1), 1159–1173. https://doi.org/10.1080/14756366.2017.1363742
  • Rudrapal, M., Issahaku, A. R., Agoni, C., Bendale, A. R., Nagar, A., Soliman, M. E. S., & Lokwani, D. (2022). In silico screening of phytopolyphenolics for the identification of bioactive compounds as novel protease inhibitors effective against SARS-CoV-2. Journal of Biomolecular Structure & Dynamics, 40(20), 10437–10453. https://doi.org/10.1080/07391102.2021.1944909
  • Saleem, S., Muhammad, G., Hussain, M. A., Altaf, M., & Bukhari, S. N. A. (2020). Withania somnifera L. insights into the phytochemical profile, therapeutic potential, clinical trials, and future prospective. Iranian Journal of Basic Medical Sciences, 23, 1501–1526.
  • Shah, H. S., Nasrullah, U., Zaib, S., Usman, F., Khan, A., Gohar, U. F., Uddin, J., Khan, I., & Al-Harrasi, A. (2021). Preparation, characterization, and pharmacological investigation of Withaferin-A loaded nanosponges for cancer therapy; in vitro, in vivo and molecular docking studies. Molecules, 26(22), 6990. https://doi.org/10.3390/molecules26226990
  • Shivapurkar, R., Hingamire, T., Kulkarni, A. S., Rajamohanan, P. R., Reddy, D. S., & Shanmugam, D. (2018). Evaluating antimalarial efficacy by tracking glycolysis in Plasmodium falciparum using NMR spectroscopy. Scientific Reports, 8(1), 18076. https://doi.org/10.1038/s41598-018-36197-3
  • Skinner, J. (2018). Statistics for immunologists. Current Protocols in Immunology, 122, 54.
  • Slavic, K., Krishna, S., Derbyshire, E. T., & Staines, H. M. (2011). Plasmodial sugar transporters as anti-malarial drug targets and comparisons with other protozoa. Malaria Journal, 10, 165. https://doi.org/10.1186/1475-2875-10-165
  • Temre, M. K., Kumar, A., & Singh, S. M. (2022). An appraisal of the current status of inhibition of glucose transporters as an emerging antineoplastic approach: Promising potential of new pan-GLUT inhibitors. Frontiers in Pharmacology, 13. https://doi.org/10.3389/fphar.2022.1035510
  • Thaiparambil, J. T., Bender, L., Ganesh, T., Kline, E., Patel, P., Liu, Y., Tighiouart, M., Vertino, P. M., Harvey, R. D., Garcia, A., & Marcus, A. I. (2011). Withaferin A inhibits breast cancer invasion and metastasis at sub‐cytotoxic doses by inducing vimentin disassembly and serine 56 phosphorylation. International Journal of Cancer, 129(11), 2744–2755. https://doi.org/10.1002/ijc.25938
  • Thien, H. V., Kager, P. A., & Sauerwein, H. P. (2006). Hypoglycemia in falciparum malaria: Is fasting an unrecognized and insufficiently emphasized risk factor? Trends in Parasitology, 22(9), 410–415. https://doi.org/10.1016/j.pt.2006.06.014
  • Van Herck, S., Hassannia, B., Louage, B., Compostizo, R. P., De Coen, R., Berghe, W. V., Berghe, T. V., & De Geest, B. G. (2019). Water-soluble Withaferin A polymer prodrugs via a drug-functionalized RAFT CTA approach. European Polymer Journal, 110, 313–318. https://doi.org/10.1016/j.eurpolymj.2018.11.043
  • Woodrow, C. J., Burchmore, R. J., & Krishna, S. (2000). Hexose permeation pathways in Plasmodium falciparum infected erythrocytes. Proceedings of the National Academy of Sciences of the United States of America, 97(18), 9931–9936. https://doi.org/10.1073/pnas.170153097
  • Xiong, G., Wu, Z., Yi, J., Fu, L., Yang, Z., Hsieh, C., Yin, M., Zeng, X., Wu, C., Lu, A., Chen, X., Hou, T., & Cao, D. (2021). ADMETlab 2.0: An integrated online platform for accurate and comprehensive predictions of ADMET properties. Nucleic Acids Research, 49(W1), W5–w14. https://doi.org/10.1093/nar/gkab255
  • Yang, H., Zhang, M. Z., Sun, H. W., Chai, Y. T., Li, X., Jiang, Q., & Hou, J. (2021). A novel microcrystalline BAY-876 formulation achieves long-acting antitumor activity against aerobic glycolysis and proliferation of hepatocellular carcinoma. Frontiers in Oncology, 11, 783194. https://doi.org/10.3389/fonc.2021.783194
  • Zakaria, N. H., Hassan, N., & Wai, L. (2020). Molecular docking study of the interactions between plasmodium falciparum lactate dehydrogenase and 4-aminoquinoline hybrids. Sains Malaysiana, 49(8), 1905–1913. https://doi.org/10.17576/jsm-2020-4908-12
  • Zothantluanga, J. H., Abdalla, M., Rudrapal, M., Tian, Q., Chetia, D., & Li, J. (2022). Computational investigations for identification of bioactive molecules from Baccaurea ramiflora and Bergenia ciliata as inhibitors of SARS-CoV-2 Mpro. Polycyclic Aromatic Compounds, 26, 1–29. https://doi.org/10.1080/10406638.2022.2046613
  • Zügner, E., Yang, H.-C., Kotzbeck, P., Boulgaropoulos, B., Sourij, H., Hagvall, S., Elmore, C. S., Esterline, R., Moosmang, S., Oscarsson, J., Pieber, T. R., Peng, X.-R., & Magnes, C. (2022). Differential in vitro effects of SGLT2 inhibitors on mitochondrial oxidative phosphorylation, glucose uptake and cell metabolism. International Journal of Molecular Sciences, 23(14), 7966. https://doi.org/10.3390/ijms23147966

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.