Screening of traditional medicinal plant extracts and compounds identifies a potent anti-leishmanial diarylheptanoid from Siphonochilus aethiopicus

References

• Ajibesin, K. K., Ekpo, B. A., Bala, D. N., Essien, E. E., & Adesanya, S. A. (2008). Ethnobotanical survey of Akwa Ibom State of Nigeria. Journal of Ethnopharmacology, 115(3), 387–408. https://doi.org/10.1016/j.jep.2007.10.021
   PubMed Web of Science ®Google Scholar
• Amos, B., Aurrecoechea, C., Barba, M., Barreto, A., Basenko, E. Y., Bażant, W., Belnap, R., Blevins, A. S., Böhme, U., Brestelli, J., Brunk, B. P., Caddick, M., Callan, D., Campbell, L., Christensen, M. B., Christophides, G. K., Crouch, K., Davis, K., DeBarry, J., … Zheng, J. (2022). VEuPathDB: The eukaryotic pathogen, vector and host bioinformatics resource center. Nucleic Acids Research, 50(D1), D898–D911. https://doi.org/10.1093/nar/gkab929
   PubMed Web of Science ®Google Scholar
• Anand, U., Jacobo-Herrera, N., Altemimi, A., & Lakhssassi, N. (2019). A comprehensive review on medicinal plants as antimicrobial therapeutics: Potential avenues of biocompatible drug discovery. In Metabolites, 9(11), 258. https://doi.org/10.3390/metabo9110258
   PubMed Web of Science ®Google Scholar
• Benchokroun, Y., Couprie, J., & Larsen, A. K. (1995). Aurintricarboxylic acid, a putative inhibitor of apoptosis, is a potent inhibitor of DNA topoisomerase II in vitro and in Chinese hamster fibrosarcoma cells. Biochemical Pharmacology, 49(3), 305–313. https://doi.org/10.1016/0006-2952(94)00465-X
   PubMed Web of Science ®Google Scholar
• Bero, J., Hannaert, V., Chataigné, G., Hérent, M. F., & Quetin-Leclercq, J. (2011). In vitro antitrypanosomal and anti activity of plants used in Benin in traditional medicine and bio-guided fractionation of the most active extract. Journal of Ethnopharmacology, 137(2), 998–1002. https://doi.org/10.1016/j.jep.2011.07.022
   PubMed Web of Science ®Google Scholar
• Bruschi, F., & Gradoni, L. (2018). The leishmaniases: Old neglected tropical diseases. In The leishmaniases: Old neglected tropical diseases. https://doi.org/10.1007/978-3-319-72386-0
   Google Scholar
• Calla-Magarinos, J., Giménez, A., Troye-Blomberg, M., & Fernández, C. (2009). An alkaloid extract of evanta, traditionally used as anti-leishmania agent in Bolivia, inhibits cellular proliferation and interferon-γ production in polyclonally activated cells. Scandinavian Journal of Immunology, 69(3), 251–258. https://doi.org/10.1111/j.1365-3083.2008.02219.x
   PubMed Web of Science ®Google Scholar
• Catchpoole, D. R., & Stewart, B. W. (1994). Inhibition of topoisomerase II by aurintricarboxylic acid: Implications for mechanisms of apoptosis. Anticancer Research, 14(3 A), 853–856.
   PubMedGoogle Scholar
• Chen, C. W., Chao, Y., Chang, Y. H., Hsu, M. J., & Lin, W. W. (2002). Inhibition of cytokine-induced JAK-STAT signalling pathways by an endonuclease inhibitor aurintricarboxylic acid. British Journal of Pharmacology, 137(7), 1011–1020. https://doi.org/10.1038/sj.bjp.0704955
   PubMed Web of Science ®Google Scholar
• Clancy, R. M., & Abramson, S. B. (1995). Nitric oxide: A novel mediator of inflammation. Proceedings of the Society for Experimental Biology and Medicine, 210(2), 93-101. https://doi.org/10.3181/00379727-210-43927AA
   Google Scholar
• Cragg, G. M., & Newman, D. J. (2013). Natural products: A continuing source of novel drug leads. Biochimica et Biophysica Acta (BBA) - General Subjects, 1830(6), 3670–3695. https://doi.org/10.1016/j.bbagen.2013.02.008
   PubMed Web of Science ®Google Scholar
• Dangi, P., Jain, R., Mamidala, R., Sharma, V., Agarwal, S., Bathula, C., Thirumalachary, M., Sen, S., & Singh, S. (2019). Natural product inspired novel indole based chiral Scaffold kills human malaria parasites via ionic imbalance mediated cell death. Scientific Reports, 9(1), 17785. https://doi.org/10.1038/s41598-019-54339-z
   Google Scholar
• De Menezes, J. P. B., Guedes, C. E. S., De Oliveira Almeida Petersen, A. L., Fraga, D. B. M., & Veras, P. S. T. (2015). Advances in development of new treatment for leishmaniasis. BioMed Research International, 2015, 815023. https://doi.org/10.1155/2015/815023
   PubMed Web of Science ®Google Scholar
• Delano, W. L. (2002). The PyMOL Molecular Graphics System. Schrodinger. https://pymol.org/2/
   Google Scholar
• Dey, S., Mukherjee, D., Chakraborty, S., Mallick, S., Dutta, A., Ghosh, J., Swapana, N., Maiti, S., Ghorai, N., Singh, C. B., & Pal, C. (2015). Protective effect of Croton caudatus Geisel leaf extract against experimental visceral leishmaniasis induces proinflammatory cytokines in vitro and in vivo. Experimental Parasitology, 151-152, 84–95. https://doi.org/10.1016/j.exppara.2015.01.012
   PubMed Web of Science ®Google Scholar
• Ezenyi, I. C., Verma, V., Singh, S., Okhale, S. E., & Adzu, B. (2020). Ethnopharmacology-aided antiplasmodial evaluation of six selected plants used for malaria treatment in Nigeria. Journal of Ethnopharmacology, 254, 112694. https://doi.org/10.1016/j.jep.2020.112694
   PubMed Web of Science ®Google Scholar
• Gestaut, D., Roh, S. H., Ma, B., Pintilie, G., Joachimiak, L. A., Leitner, A., Walzthoeni, T., Aebersold, R., Chiu, W., & Frydman, J. (2019). The Chaperonin TRiC/CCT Associates with prefoldin through a conserved electrostatic interface essential for cellular proteostasis. Cell, 177(3), 751–765.e15. https://doi.org/10.1016/j.cell.2019.03.012
   PubMed Web of Science ®Google Scholar
• Goldman-Pinkovich, A., Kannan, S., Nitzan-Koren, R., Puri, M., Pawar, H., Bar-Avraham, Y., McDonald, J., Sur, A., Zhang, W. W., Matlashewski, G., Madhubala, R., Michaeli, S., Myler, P. J., & Zilberstein, D. (2020). Sensing host arginine is essential for leishmania parasites’ intracellular development. mBio, 11(5), e02023-20. https://doi.org/10.1128/mBio.02023-20
   PubMed Web of Science ®Google Scholar
• Gordon, S. (2003). Alternative activation of macrophages. Nature Reviews Immunology, 3(1), 23–35. https://doi.org/10.1038/nri978
   PubMed Web of Science ®Google Scholar
• Gravitz, L. (2011). Chemoprevention: First line of defence. Nature, 471(7339), S5–S7. https://doi.org/10.1038/471S5a
   PubMed Web of Science ®Google Scholar
• Grochowski, D. M., Locatelli, M., Granica, S., Cacciagrano, F., & Tomczyk, M. (2018). A review on the dietary flavonoid tiliroside. Comprehensive Reviews in Food Science and Food Safety, 17(5), 1395–1421. https://doi.org/10.1111/1541-4337.12389
   PubMed Web of Science ®Google Scholar
• Gutiérrez-Rebolledo, G. A., Drier-Jonas, S., & Jiménez-Arellanes, M. A. (2017). Natural compounds and extracts from Mexican medicinal plants with anti-leishmaniasis activity: An update. Asian Pacific Journal of Tropical Medicine, 10(12), 1105–1110. https://doi.org/10.1016/j.apjtm.2017.10.016
   PubMed Web of Science ®Google Scholar
• Igoli, N. P., Al-Tannak, N. F., Ezenyi, I. C., Gray, A. I., & Igoli, J. O. (2021). Antiplasmodial activity of a novel diarylheptanoid from Siphonochilus aethiopicus. Natural Product Research, 35(24), 5588–5595. https://doi.org/10.1080/14786419.2020.1799358
   PubMed Web of Science ®Google Scholar
• Iyamah, P. C., & Idu, M. (2015). Ethnomedicinal survey of plants used in the treatment of malaria in Southern Nigeria. Journal of Ethnopharmacology, 173, 287–302. https://doi.org/10.1016/j.jep.2015.07.008
   PubMed Web of Science ®Google Scholar
• Jain, R., Gupta, S., Munde, M., Pati, S., & Singh, S. (2020). Development of novel anti-malarial from structurally diverse library of molecules, targeting plant-like CDPK1, a multistage growth regulator of P. falciparum. Biochemical Journal, 477(10), 1951–1970. https://doi.org/10.1042/BCJ20200045
   PubMed Web of Science ®Google Scholar
• Jia, J., Zhu, F., Ma, X., Cao, Z., Cao, Z. W., Li, Y., Li, Y. X., & Chen, Y. Z. (2009). Mechanisms of drug combinations: Interaction and network perspectives. Nature Reviews. Drug Discovery, 8(2), 111–128. https://doi.org/10.1038/nrd2683
   PubMed Web of Science ®Google Scholar
• Kostka, S. L., Knop, J., Konur, A., Udey, M. C., & Von Stebut, E. (2006). Distinct roles for IL-1 receptor type I signaling in early versus established Leishmania major infections. Journal of Investigative Dermatology, 126(7), 1582–1589. https://doi.org/10.1038/sj.jid.5700309
   PubMed Web of Science ®Google Scholar
• Kropf, P., Fuentes, J. M., Fähnrich, E., Arpa, L., Herath, S., Weber, V., Soler, G., Celada, A., Modolell, M., & Müller, I. (2005). Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. The FASEB Journal, 19(8), 1000–1002. https://doi.org/10.1096/fj.04-3416fje
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Liu, B., Gao, H. M., Wang, J. Y., Jeohn, G. H., Cooper, C. L., & Hong, J. S. (2002). Role of nitric oxide in inflammation-mediated neurodegeneration. Annals of the New York Academy of Sciences, 962(1), 318–331. https://doi.org/10.1111/j.1749-6632.2002.tb04077.x
   PubMed Web of Science ®Google Scholar
• McCune, S. A., Foe, L. G., Kemp, R. G., & Jurin, R. R. (1989). Aurintricarboxylic acid is a potent inhibitor of phosphofructokinase. The Biochemical Journal, 259(3), 925–927. https://doi.org/10.1042/bj2590925
   PubMed Web of Science ®Google Scholar
• Muhammed, M. T., & Aki-Yalcin, E. (2019). Homology modeling in drug discovery: Overview, current applications, and future perspectives. Chemical Biology & Drug Design, 93(1), 12–20. https://doi.org/10.1111/cbdd.13388
   PubMed Web of Science ®Google Scholar
• Mushtaq, S., Abbasi, B. H., Uzair, B., & Abbasi, R. (2018). Natural products as reservoirs of novel therapeutic agents. EXCLI Journal, 17, 420–451. https://doi.org/10.17179/excli2018-1174
   PubMed Web of Science ®Google Scholar
• Nandan, D., Camargo de Oliveira, C., Moeenrezakhanlou, A., Lopez, M., Silverman, J. M., Subek, J., & Reiner, N. E. (2012). Myeloid cell IL-10 production in response to leishmania involves inactivation of glycogen synthase kinase-3β downstream of phosphatidylinositol-3 kinase. The Journal of Immunology, 188(1), 367–378. https://doi.org/10.4049/jimmunol.1100076
   PubMed Web of Science ®Google Scholar
• Ogbole, O. O., Segun, P. A., & Fasinu, P. S. (2018). Antimicrobial and antiprotozoal activities of twenty-four Nigerian medicinal plant extracts. South African Journal of Botany, 117, 240–246. https://doi.org/10.1016/j.sajb.2018.05.028
   Web of Science ®Google Scholar
• Ohashi, M., Amoa-Bosompem, M., Kwofie, K. D., Agyapong, J., Adegle, R., Sakyiamah, M. M., Ayertey, F., Owusu, K. B.-A., Tuffour, I., Atchoglo, P., Tung, N. H., Uto, T., Aboagye, F., Appiah, A. A., Appiah-Opong, R., Nyarko, A. K., Anyan, W. K., Ayi, I., Boakye, D. A., … Ohta, N. (2018). In vitro antiprotozoan activity and mechanisms of action of selected Ghanaian medicinal plants against Trypanosoma, Leishmania, and Plasmodium parasites. Phytotherapy Research: PTR, 32(8), 1617–1630. https://doi.org/10.1002/ptr.6093
   PubMed Web of Science ®Google Scholar
• Oliveira, C. F., Manzoni-De-Almeida, D., Mello, P. S., Natale, C. C., Santiago, H. D. C., Miranda, L. D. S., Ferraz, F. O., Dos Santos, L. M., Teixeira, M. M., Arantes, R. M. E., & Vieira, L. Q. (2012). Characterization of chronic cutaneous lesions from TNF-receptor-1-deficient mice infected by Leishmania major. Clinical & Developmental Immunology, 2012, 865708. https://doi.org/10.1155/2012/865708
   PubMedGoogle Scholar
• Oryan. (2015). Plant-derived compounds in treatment of leishmaniasis. Iran J Vet Res, 16(1), 1-19.
   Google Scholar
• Osorio, Y., Travi, B. L., Renslo, A. R., Peniche, A. G., & Melby, P. C. (2011). Identification of small molecule lead compounds for visceral leishmaniasis using a novel ex vivo splenic explant model system. PLoS Neglected Tropical Diseases, 5(2), e962. https://doi.org/10.1371/journal.pntd.0000962
   PubMed Web of Science ®Google Scholar
• Otun, K. O., Onikosi, D. B., Ajiboye, A. T., & Jimoh, A. A. (2015). Chemical composition, antioxidant and antimicrobial potentials of Icacina trichantha oliv. leaf extracts. Research Journal of Phytochemistry, 9(4), 161–174. https://doi.org/10.3923/rjphyto.2015.161.174
   Google Scholar
• Pacher, P., Beckman, J. S., & Liaudet, L. (2007). Nitric oxide and peroxynitrite in health and disease. In Physiological Reviews, 87(1), 315–424. https://doi.org/10.1152/physrev.00029.2006
   PubMed Web of Science ®Google Scholar
• Pawar, H., Puri, M., Weinberger, R. F., Madhubala, R., & Zilberstein, D. (2019). The arginine sensing and transport binding sites are distinct in the human pathogen Leishmania. PLoS Neglected Tropical Diseases, 13(4), e0007304. https://doi.org/10.1371/journal.pntd.0007304
   PubMed Web of Science ®Google Scholar
• Ramachandran, G. N., & Sasisekharan, V. (1968). Conformation of polypeptides and proteins. Advances in Protein Chemistry, 23(C), 283–438. https://doi.org/10.1016/S0065-3233(08)60402-7
   PubMedGoogle Scholar
• Rodrigues, I. A., Mazotto, A. M., Cardoso, V., Alves, R. L., Amaral, A. C. F., Silva, J. R. D. A., Pinheiro, A. S., & Vermelho, A. B. (2015). Natural products: Insights into leishmaniasis inflammatory response. Mediators of Inflammation, 2015, 835910. https://doi.org/10.1155/2015/835910
   PubMed Web of Science ®Google Scholar
• Rodríguez, N. E., & Wilson, M. E. (2014). Eosinophils and mast cells in leishmaniasis. Immunologic Research, 59 (1–3), 129–141. https://doi.org/10.1007/s12026-014-8536-x
   PubMed Web of Science ®Google Scholar
• Rui, H., Xu, J., Mehta, S., Fang, H., Williams, J., Dong, F., & Grimley, P. M. (1998). Activation of the Jak2-Stat5 signaling pathway in Nb2 lymphoma cells by an anti-apoptotic agent, aurintricarboxylic acid. The Journal of Biological Chemistry, 273(1), 28–32. https://doi.org/10.1074/jbc.273.1.28
   PubMed Web of Science ®Google Scholar
• Sacks, D., & Noben-Trauth, N. (2002). The immunology of susceptibility and resistance to Leishmania major in mice. Nature Reviews Immunology, 2(11), 845–858. https://doi.org/10.1038/nri933
   PubMed Web of Science ®Google Scholar
• Salvador, M. J., Sartori, F. T., Sacilotto, A. C. B. C., Pral, E. M. F., Alfieri, S. C., & Vichnewski, W. (2009). Bioactivity of flavonoids isolated from Lychnophora markgravii against Leishmania amazonensis amastigotes. Zeitschrift Für Naturforschung C, 64(7-8), 509–512. https://doi.org/10.1515/znc-2009-7-807
   PubMed Web of Science ®Google Scholar
• Saraiva, M., & O’Garra, A. (2010). The regulation of IL-10 production by immune cells. Nature Reviews Immunology, 10(3), 170–181. https://doi.org/10.1038/nri2711
   PubMed Web of Science ®Google Scholar
• Schmidt, B. H., Osheroff, N., & Berger, J. M. (2012). Structure of a topoisomerase II-DNA-nucleotide complex reveals a new control mechanism for ATPase activity. Nature Structural & Molecular Biology, 19(11), 1147–1154. https://doi.org/10.1038/nsmb.2388
   PubMed Web of Science ®Google Scholar
• Simoben, C. V., Ntie-Kang, F., Akone, S. H., & Sippl, W. (2018). Compounds from African medicinal plants with activities against selected parasitic diseases: Schistosomiasis, trypanosomiasis and leishmaniasis. Natural Products and Bioprospecting, 8(3), 151–169. https://doi.org/10.1007/s13659-018-0165-y
   PubMed Web of Science ®Google Scholar
• Simons, L. A. (2002). Additive effect of plant sterol-ester margarine and cerivastatin in lowering low-density lipoprotein cholesterol in primary hypercholesterolemia. The American Journal of Cardiology, 90(7), 737–740. https://doi.org/10.1016/S0002-9149(02)02600-0
   PubMed Web of Science ®Google Scholar
• Singh, O. P., Singh, B., Chakravarty, J., & Sundar, S. (2016). Current challenges in treatment options for visceral leishmaniasis in India: A public health perspective. In Infectious Diseases of Poverty, 5, 19. https://doi.org/10.1186/s40249-016-0112-2
   Web of Science ®Google Scholar
• Singhal, J., Madan, E., Chaurasiya, A., Srivastava, P., Singh, N., Kaushik, S., Kahlon, A. K., Maurya, M. K., Marothia, M., Joshi, P., Ranganathan, A., & Singh, S. (2022). Host SUMOylation pathway negatively regulates protective immune responses and promotes leishmania donovani survival. Frontiers in Cellular and Infection Microbiology, 12, 878136. https://doi.org/10.3389/fcimb.2022.878136
   PubMed Web of Science ®Google Scholar
• Srivastava, A., Garg, S., Jain, R., Ayana, R., Kaushik, H., Garg, L., Pati, S., & Singh, S. (2019). Identification and functional characterization of a bacterial homologue of Zeta toxin in Leishmania donovani. FEBS Letters, 593(11), 1223-1235. https://doi.org/10.1002/1873-3468.13429
   Web of Science ®Google Scholar
• Tariq, A., Adnan, M., Amber, R., Pan, K., Mussarat, S., & Shinwari, Z. K. (2016). Ethnomedicines and anti-parasitic activities of Pakistani medicinal plants against Plasmodia and Leishmania parasites. Annals of Clinical Microbiology and Antimicrobials, 15 (1), 52. https://doi.org/10.1186/s12941-016-0170-0
   Google Scholar
• Tripathi, P., Tripathi, P., Kashyap, L., & Singh, V. (2007). The role of nitric oxide in inflammatory reactions. FEMS Immunology & Medical Microbiology, 51(3), 443–452. https://doi.org/10.1111/j.1574-695X.2007.00329.x
   PubMed Web of Science ®Google Scholar
• Trott, O., & Olson, A. J. (2010). AutoDock vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc
   PubMed Web of Science ®Google Scholar
• Tsi, C. J., Chao, Y., Chen, C. W., & Lin, W. W. (2002). Aurintricarboxylic acid protects against cell death caused by lipopolysaccharide in macrophages by decreasing inducible nitric-oxide synthase induction via IκB kinase, extracellular signal-regulated kinase, and p38 mitogen-activated protein kinase inhibit. Molecular Pharmacology, 62(1), 90–101. https://doi.org/10.1124/mol.62.1.90
   PubMed Web of Science ®Google Scholar
• Ullah, N., Nadhman, A., Siddiq, S., Mehwish, S., Islam, A., Jafri, L., & Hamayun, M. (2016). Plants as anti agents: Current scenario. Phytotherapy Research: PTR, 30(12), 1905–1925. https://doi.org/10.1002/ptr.5710
   PubMed Web of Science ®Google Scholar
• von Stebut, E., Ehrchen, J. M., Belkaid, Y., Kostka, S. L., Mölle, K., Knop, J., Sunderkötter, C., & Udey, M. C. (2003). Interleukin 1α promotes TH1 differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. Journal of Experimental Medicine, 198(2), 191–199. https://doi.org/10.1084/jem.20030159
   PubMed Web of Science ®Google Scholar
• Wang, Y., Xiao, J., Suzek, T. O., Zhang, J., Wang, J., Zhou, Z., Han, L., Karapetyan, K., Dracheva, S., Shoemaker, B. A., Bolton, E., Gindulyte, A., & Bryant, S. H. (2012). PubChem’s BioAssay database. Nucleic Acids Research, 40(Database issue), D400–12. https://doi.org/10.1093/nar/gkr1132
   PubMed Web of Science ®Google Scholar
• Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., Beer, T. A. P., De, Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. https://doi.org/10.1093/nar/gky427
   PubMed Web of Science ®Google Scholar
• World Health Organization, & Pan American Health Organization. (2019). Leishmaniases: Epidemiological report of the Americas. Report Leishmaniases, (7).
   Google Scholar
• Xu, D., & Zhang, Y. (2011). Improving the physical realism and structural accuracy of protein models by a two-step atomic-level energy minimization. Biophysical Journal, 101(10), 2525–2534. https://doi.org/10.1016/j.bpj.2011.10.024
   PubMed Web of Science ®Google Scholar
• Yadav, P., Ayana, R., Garg, S., Jain, R., Sah, R., Joshi, N., Pati, S., & Singh, S. (2019). Plasmodium palmitoylation machinery engineered in E. coli for high-throughput screening of palmitoyl acyl-transferase inhibitors. FEBS Open Bio, 9(2), 248–264. https://doi.org/10.1002/2211-5463.12564
   PubMed Web of Science ®Google Scholar