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Computational life sciences, Bioinformatics and System Biology

Advances in schistosomiasis drug discovery based on natural products.

, , , &
Pages 608-623 | Received 16 May 2021, Accepted 12 May 2022, Published online: 27 May 2022

References

  • Abd El Wahab WM, El-Badry AA, Mahmoud SS, El-Badry YA, El-Badry MA, Hamdy DA. 2021. Ginger (Zingiber officinale)-derived nanoparticles in Schistosoma mansoni infected mice: hepatoprotective and enhancer of etiological treatment. PLoS Negl Trop Dis. 15(5):e0009423.
  • Abe EM, Tambo E, Xue J, Xu J, Ekpo UF, Rollinson D, Yang K, Li SZ, Zhou XN. 2020. Approaches in scaling up schistosomiasis intervention towards transmission elimination in Africa: leveraging from the Chinese experience and lessons. Acta Trop. 208(July 2018):105379–105379. doi:10.1016/j.actatropica.2020.105379.
  • Adekiya TA, Kondiah PP, Choonara YE, Kumar P, Pillay V. 2020. A review of nanotechnology for targeted anti-schistosomal therapy. Frontiers in Bioengineering and BiotechUhnology. 8:2296–4185.
  • Akachukwu I, Olubiyi OO, Kosisochukwu A, John MC, Justina NN. 2017. Structure-Based study of Natural products with anti-Schistosoma activity. Curr Comput-Aided Drug Des. 13(2):91–100. doi:10.2174/1573409913666170119114859.
  • Aleixo de Carvalho LSG, de Moraes RB, Silva Pinto J, de Faria Pinto PL, Pereira P, dos S O, Da Silva Filho AA. 2015. Schistosomicidal activity and docking of Schistosoma mansoni ATPDase 1 with licoflavone B isolated from glycyrrhizainflata (fabaceae). Exp Parasitol. 159:207–214. doi:10.1016/j.exppara.2015.09.015.
  • Aly HF, Mantawy MM. 2013. Efficiency of ginger (Zingiber officinale) against Schistosoma mansoni infection during host-parasite association. Parasitol Int. 62(4):380–389.
  • Ammar AI, Afifi AF, Essa A, Galal-Khallaf A, Mokhtar MM, Shehab-Eldeen S, Rady AA. 2020. Cucurbita pepo seed Oil induces microsatellite instability and tegumental damage to Schistosoma mansoni immature and adult worms In vitro. Infect Drug Resist. 13:3469–3484.
  • Aula OP, McManus DP, Jones MK, Gordon CA. 2021. Schistosomiasis with a focus on Africa. Tropical Medicine and Infectious Disease. 6(3):109–109.
  • Banegas-Luna A-J, Cerón-Carrasco JP, Pérez-Sánchez H. 2018. A review of ligand-based virtual screening web tools and screening algorithms in large molecular databases in the age of big data. Future Med Chem. 10(22):2641–2658. doi:10.4155/fmc-2018-0076.
  • Batool M, Ahmad B, Choi S. 2019. A structure-based drug discovery paradigm. Int J Mol Sci. 20(11):2783–2783. doi:10.3390/ijms20112783.
  • Bender A, Cortes-Ciriano I. 2019. Artificial intelligence in drug discovery: what is realistic, what are illusions? part 2: a discussion of chemical and biological data. Drug Discovery Today Elseiver. 26(2):511–524. doi:10.1016/j.drudis.2020.11.037.
  • Bergquist R, Utzinger J, Keiser J. 2017. Controlling schistosomiasis with praziquantel: How much longer without a viable alternative? Infect Dis Poverty. 6(1):1–10. doi:10.1186/s40249-017-0286-2.
  • Beshay EVN, Rady AA, Afifi AF, Mohamed AH. 2019. Schistosomicidal, antifibrotic and antioxidant effects of Cucurbita pepo L. seed oil and praziquantel combined treatment for Schistosoma mansoni infection in a mouse model. J Helminthol. 93(3):286–294. doi:10.1017/S0022149X18000317.
  • Bultum LE, Woyessa AM, Lee D. 2019. ETM-DB: Integrated Ethiopian traditional herbal medicine and phytochemicals database. BMC Complement Altern Med. 19(1):212–212. doi:10.1186/s12906-019-2634-1.
  • Caffrey CR, El-Sakkary N, Mäder P, Krieg R, Becker K, Schlitzer M, Drewry DH, Vennerstrom JL, Grevelding CG. 2019. Drug discovery and development for schistosomiasis. Neglected Tropical Diseases: Drug Discovery and Development. 12:187–225. doi:10.1002/9783527808656.ch8.
  • Cheuka PM, Mayoka G, Mutai P, Chibale K. 2017. The role of natural products in drug discovery and development against neglected tropical diseases. Molecules. 22(1):58–58. doi:10.3390/molecules22010058.
  • Chisango TJ, Ndlovu B, Vengesai A, Nhidza AF, Sibanda EP, Zhou D, … Mduluza T. 2019. Benefits of annual chemotherapeutic control of schistosomiasis on the development of protective immunity. BMC Infect Dis. 19(1):1–9.
  • Cock IE, Selesho MI, Van Vuuren SF. 2018. A review of the traditional use of southern African medicinal plants for the treatment of selected parasite infections affecting humans. J Ethnopharmacol. 220:250–264.
  • Cragg GM, Newman DJ. 2013. Natural products: a continuing source of novel drug leads. Biochimica et Biophysica Acta (BBA)-General Subjects. 1830(6):3670–3695.
  • De Rycker M, Baragaña B, Duce SL, Gilbert IH. 2018. Challenges and recent progress in drug discovery for tropical diseases. Nature. 559(7715):498–506. doi:10.1038/s41586-018-0327-4.
  • Dkhil MA, Khalil MF, Diab MS, Bauomy AA, Santourlidis S, Al-Shaebi EM, Al-Quraishy S. 2019. Evaluation of nanoselenium and nanogold activities against murine intestinal schistosomiasis. Saudi J Biol Sci. 26(7):1468–1472.
  • Duarte Galhardo de Albuquerque RD, Mahomoodally MF, Lobine D, Suroowan S, Rengasamy KR. 2020. Botanical products in the treatment and control of schistosomiasis: recent studies and distribution of active plant resources according to affected regions. Biology (Basel). 9(8):223–223. doi:10.3390/biology9080223.
  • Durojaye OA, Nwanguma BC, Joshua PE, Ogidigo JO, Cosmas S, Asomadu RO, Obeta JN. 2019. Evaluation of 6-gingerol and its modified analogues as therapeutic candidates against Schistosoma mansoni phosphofructokinase. VacciMonitor. 28(1):38–47.
  • Eissa MM, El-Azzouni MZ, El-Khordagui LK, Abdel Bary A, El-Moslemany RM, Abdel Salam SA. 2020. Single oral fixed-dose praziquantel-miltefosine nanocombination for effective control of experimental schistosomiasis mansoni. Parasites and Vectors. 13(1):1–12. doi:10.1186/s13071-020-04346-1.
  • El-derbawy1 MM, El WAEMS, Kholy1 IRB, S HS. 2019. A study of the potential therapeutic effect of ginger (Zingiber officinale) loaded nanoparticles on murine schistosomiasis mansoni. J Egypt Soc Parasitol. 49(1):123–128.
  • El-Faham MH, Eissa MM, Igetei JE, Amer EI, Liddell S, El-Azzouni MZ, Doenhoff MJ. 2017. Treatment of Schistosoma mansoni with miltefosine in vitro enhances serological recognition of defined worm surface antigens. PLoS Negl Trop Dis. 11(8):1–26. doi:10.1371/journal.pntd.0005853.
  • El-Nour A, Mohamed F, Fadladdin Y. 2021. Anti-schistosomal activity of Zingiber officinale, piper nigrum, and coriandrum sativum aqueous plant extracts on hamsters infected with Schistosoma mansoni. J Parasitol Res. 2021.
  • El-Sameih MA, Hassan FA, Abed GH, Omar HEDM. 2017. Role Of ginger in the Treatment of Schistosoma mansoni infection a histopathological studies. Alexandria Journal of Veterinary Sciences. 52(1):198–204.
  • Elujoba AA, Odeleye OM, Ogunyemi CM. 2005. Review traditional medicine development for medical and dental primary health care Delivery system in the orthodox medicine, as currently made available today in Nigeria (as in most African countries), so long as every nook and corner of our rural popu. African Ethnomedicines Network. 2:46–61.
  • Eweas AF, Allam G, Abuelsaad AS, ALGhamdi AH, Maghrabi IA. 2013. Design, synthesis, anti-schistosomal activity and molecular docking of novel 8-hydroxyquinoline-5-sufonyl 1, 4-diazepine derivatives. Bioorg Chem. 46:17–25.
  • Fadladdin YAJ. 2021. Antischistosomal activity of Origanum majorana, Ziziphus spina-christi, and salvia fruticosa plant extracts on hamster infected with Schistosoma haematobium. BioMed Res Int. 2021.
  • Ferreira LG, Oliva G, Andricopulo AD. 2018. From medicinal Chemistry to human health: Current approaches to drug discovery for Cancer and Neglected Tropical diseases. Anais da Academia Brasileira de Ciensias. 90:645–661.
  • Fuss A, Mazigo HD, Mueller A. 2020. Malacological survey to identify transmission sites for intestinal schistosomiasis on ijinga island, mwanza, north-western Tanzania. Acta Trop. 203(April 2019):105289–105289. doi:10.1016/j.actatropica.2019.105289.
  • Gemma S, Federico S, Brogi S, Brindisi M, Butini S, Campiani G. 2019. Dealing with schistosomiasis: Current drug discovery strategies. In Annual Reports in Medicinal Chemistry (1st ed., Vol. 53). Elsevier Inc. https://doi.org/10.1016/bs.armc.2019.06.002.
  • Ghosh S, Das AK, Sarkar P, Sil PC. 2019. Oxidative stress in schistosomiasis, echinococcosis, and trypanosomiasis: a therapeutic approach. In: Discovery and development of therapeutics from Natural products against Neglected Tropical diseases. Kolkata: Elsevier; p. 219–239.
  • Gönnert R, Andrews P. 1977. Praziquantel, a new broad-spectrum anti-schistosomal agent. ZeitschriftFür Parasitenkunde. 52(2):129–150. doi:10.1007/BF00389899.
  • Gouveia MJ, Brindley PJ, Gärtner F, Costa JM, Vale N. 2018. Drug repurposing for schistosomiasis: combinations of drugs or biomolecules. Pharmaceuticals. 11(1):15–15.
  • Gruessner BM, Cornet-Vernet L, Desrosiers MR, Lutgen P, Towler MJ, Weathers PJ. 2019. It is not just artemisinin: Artemisia sp. for treating diseases including malaria and schistosomiasis. Phytochem Rev. 18(6):1509–1527.
  • Guerra RA, Silva MP, Silva TC, Salvadori MC, Teixeira FS, De Oliveira RN, Rocha JA, Pinto PLS, De Moraes J. 2019. In vitro and in vivo studies of spironolactone as an anti-schistosomal drug capable of clinical repurposing. Antimicrob Agents Chemother. 63(3):1–11. doi:10.1128/AAC.01722-18.
  • Guidi A, Lalli C, Gimmelli R, Nizi E, Andreini M, Gennari N, Saccoccia F, Harper S, Bresciani A, Ruberti G. 2017. Discovery by organism-based high-throughput screening of new multi-stage compounds affecting Schistosoma mansoni viability, egg formation and production. PLoS Negl Trop Dis. 11(10):e0005994–e0005994. doi:10.1371/journal.pntd.0005994.
  • Guidi A, Lalli C, Perlas E, Bolasco G, Nibbio M, Monteagudo E, Bresciani A, Ruberti G. 2016. Discovery and Characterisation of novel anti-schistosomal properties of the anti-anginal drug, perhexiline and Its impact on Schistosoma mansoni male and female reproductive systems. PLoS Negl Trop Dis. 10(8):1–22. doi:10.1371/journal.pntd.0004928.
  • Hatherley R, Brown DK, Musyoka TM, Penkler DL, Faya N, Lobb KA, Tastan Bishop Ö. 2015. SANCDB: A South African natural compound database. J Cheminform. 7(1):29–29. doi:10.1186/s13321-015-0080-8.
  • Hernandez HW, Soeung M, Zorn KM, Ashoura N, Mottin M, Andrade CH, Caffrey CR, de Siqueira-Neto JL, Ekins S. 2019. High-Throughput and Computational repurposing for Neglected diseases. Pharm Res. 36(2):27–27. doi:10.1007/s11095-018-2558-3.
  • Herrera Acevedo C, Scotti L, Feitosa Alves M, Formiga Melo Diniz MDF, Scotti MT. 2017. Computer-aided drug design using sesquiterpene lactones as sources of new structures with potential activity against infectious neglected diseases. Molecules. 22(1):79–79.
  • Kang N, Shen W, Gao H, Feng Y, Zhu W, Yang S, Liu Y, Xu Q, Yu D. 2018. Anti-schistosomal properties of hederacolchiside a1 isolated from Pulsatilla chinensis. Molecules. 23(6):1–16. doi:10.3390/molecules23061431.
  • Kefalidou AA, Nations U, Affairs S. 2016. Brief for GSDR – 2016 Update Sustainable drug development for Neglected Tropical Diseases. 1–6.
  • Kiriiri GK, Njogu PM, Mwangi AN. 2020. Exploring different approaches to improve the success of drug discovery and development projects: a review. Futur J Pharm Sci. 6:27–27. doi:10.1186/s43094-020-00047-9.
  • Kuhn I, Kellenberger E, Said-Hassane F, Villa P, Rognan D, Lobstein A, Haiech J, Hibert M, Schuber F, Muller-Steffner H. 2010. Identification by high-throughput screening of inhibitors of Schistosoma mansoni NAD+ catabolizing enzyme. Bioorg Med Chem. 18(22):7900–7910. doi:10.1016/j.bmc.2010.09.041.
  • Kumar D. 2017. Software and web resources for computer-aided molecular software and web resources for computer-aided molecular modelling and drug discovery. March 2016. https://doi.org/10.1201/b19853-3.
  • Lago EM, Silva MP, Queiroz TG, Mazloum SF, Rodrigues VC, Carnaúba PU, Pinto PL, Rocha JA, Ferreira LLG, Andricopulo AD, de Moraes J. 2019. Phenotypic screening of nonsteroidal anti-inflammatory drugs identified mefenamic acid as a drug for the treatment of schistosomiasis. EBioMedicine. 43:370–379. doi:10.1016/j.ebiom.2019.04.029.
  • Length F. 2017. Determination of bioactive constituents of Rauwolfia vomitoria afzel(asofeyeje) roots using gas chromatography-mass spectrometry (GC-MS) and Fourier transform infrared spectrometry (FT-IR). African Journal of Pharmacy and Pharmacology. 11(2):25–31. doi:10.5897/AJPP2016.4712.
  • Lesser B. 2021. The Origin and Mechanism of Consuming and Administering Medicine. Dual diagnosis. orghttps://dualdiagnosis.org/drug-addiction/evolution-administering-consuming-drugs/.
  • Lin X, Li X, Lin X. 2020. A review on applications of Computational methods in drug screening and design. Molecules. 25(6):1375–1375. doi:10.3390/molecules25061375.
  • Liu Y-X, Wu W, Liang Y-J, Jie Z-L, Wang H, Wang W, Huang Y-X. 2014. New uses for old drugs: The tale of artemisinin derivatives in the elimination of schistosomiasis japonica in China. Molecules. 19:15058–15074.
  • Lombardo FC, Pasche V, Panic G, Endriss Y, Keiser J. 2019. Life cycle maintenance and drug-sensitivity assays for early drug discovery in Schistosoma mansoni. Nat Protoc. 14(2):461–481.
  • Macalino SJY, Gosu V, Hong S, Choi S. 2015. Role of computer-aided drug design in modern drug discovery. Arch Pharmacal Res. 38(9):1686–1701.
  • Mafud AC, Silva MP, Monteiro DC, Oliveira MF, Resende JG, Coelho ML, … de Moraes J. 2016. Structural parameters, molecular properties, and biological evaluation of some terpenes targeting Schistosoma mansoni parasite. Chem-Biol Interact. 244:129–139.
  • Marxer M, Ingram K, Keiser J. 2012. Development of an in vitro drug screening assay using Schistosoma haematobium schistosomula. Parasit Vectors. 5(1):1–8.
  • Mbereko A, Chimbari MJ, Manyangadze T, Mukaratirwa S. 2020. Knowledge and perceptions of schistosomiasis, a water-borne disease, in two semi-arid rural areas of South Africa (ndumo) and Zimbabwe (ntalale). Food and Waterborne Parasitology. 21:e00091–e00091.
  • Melo-Filho CC, Dantas RF, Braga RC, Neves BJ, Senger MR, Valente WCG, Rezende-Neto JM, Chaves WT, Muratov EN, Paveley RA, et al. 2016. QSAR-Driven Discovery of novel chemical scaffolds active against Schistosoma mansoni. Journal of Chemical Information and Modelling. 56(7):1357–1372. doi:10.1021/acs.jcim.6b00055.
  • Mokbel KEDM, Baiuomy IR, Sabry AEHA, Mohammed MM, El-Dardiry MA. 2020. In vivo assessment of the antischistosomal activity of curcumin loaded nanoparticles versus praziquantel in the treatment of Schistosoma mansoni. Sci Rep. 10(1):1–9.
  • Mølgaard P, Nielsen SB, Rasmussen DE, Drummond RB, Makaza N, Andreassen J. 2001. Anthelmintic screening of Zimbabwean plants traditionally used against schistosomiasis. J Ethnopharmacol. 74(3):257–264.
  • Moon S, Bermudez J, ‘t Hoen E. 2012. Innovation and access to medicines for neglected populations: could a treaty address a broken pharmaceutical R&D system? PLoS Med. 9(5):e1001218–e1001218. doi:10.1371/journal.pmed.1001218.
  • Moreira-Filho JT, Silva AC, Dantas RF, Gomes BF, Neto LRS, Brandao-Neto J, … Andrade CH. 2021. Schistosomiasis drug discovery in the Era of automation and Artificial intelligence. Front Immunol. 12:642383–642383.
  • Mortier J, Rakers C, Bermudez M, Murgueitio MS, Riniker S, Wolber G. 2015. The impact of molecular dynamics on drug design applications for the characterization of ligand-macromolecule complexes. Drug Discov Today. 20:20686–20702.
  • Mostafa OMS, Eid RA. 2011. Anti-schistosomal activity of ginger (Zingiber officinale) against Schistosoma mansoni harboured in C57 mice. 395–403. https://doi.org/10.1007/s00436-011-2267-x.
  • Mtemeli FL, Walter I, Tinago T, Shoko R. 2021. An assessment of the molluscicidal potential of Cucurbita maxima seed extracts on biomphalaria pfeifferi and bulinus globosus snails. All Life. 14(1):244–255. DOI: 10.1080/26895293.2021.1901788.
  • Ndamba J, Nyazema N, Makaza N, Anderson C, Kaondera KC. 1994. Traditional herbal remedies used for the treatment of urinary schistosomiasis in Zimbabwe. J Ethnopharmacol. 42(2):125–132.
  • Neves BJ, Andrade CH, Cravo PVL. 2015. Natural products as leads in schistosome drug discovery. Molecules. 20(2):1872–1903. doi:10.3390/molecules20021872.
  • Neves BJ, Braga RC, Melo-Filho CC, Moreira-Filho JT, Muratov EN, Andrade CH. 2018. QSAR-based virtual screening: Advances and applications in drug discovery. Front Pharmacol. 9(NOV):1–7. doi:10.3389/fphar.2018.01275.
  • Neves BJ, Dantas RF, Senger MR, Melo-Filho CC, Valente WCG, de Almeida ACM, Rezende-Neto JM, Lima EFC, Paveley R, Furnham N, et al. 2016a. Discovery of New anti-schistosomal hits by integration of QSAR-based virtual screening and high content screening. J Med Chem. 59(15):7075–7088. doi:10.1021/acs.jmedchem.5b02038.
  • Neves BJ, Muratov E, Machado RB, Andrade CH, Cravo PV. 2016b. Modern approaches to accelerate the discovery of new anti-schistosomal drugs. Expert Opin Drug Discovery. 11(6):557–567. doi:10.1080/17460441.2016.1178230.
  • Ngangoue MO, Ngameni B, Ambassa P, Chi GF, Wamba BEN, Ombito JO, … Ngadjui BT. 2020. A phenanthridine-6(5H)-one derivative and a lanostane-type triterpene with antibacterial properties from Anonidium mannii (oliv). engl. & diels (annonaceae). Nat Prod Res. 0(0):1–10. doi:10.1080/14786419.2020.1758094.
  • Ntie-Kang F, Telukunta KK, Döring K, Simoben CV, Moumbock AAF, Malange YI, Njume LE, Yong JN, Sippl W, Günther S. 2017. NANPDB: A resource for Natural products from Northern African sources. J Nat Prod. 80(7): 2067–2076. doi:10.1021/acs.jnatprod.7b00283.
  • Nunes R, Campos P, Pinto R, Mioduski J, Santos R, Justus B, Padilha de Paula F, Klein T, Boscardin P, Corrêa S, et al. 2021. The promising antischistosomal activity of oleic acid-loaded polymeric nanocapsules for oral administration. Journal of Drug Delivery Science and Technology. 63:102429–102429. doi:10.1016/j.jddst.2021.102429.
  • Nunes RR, Costa MdS, Santos BdR, Fonseca ALd, Ferreira LS, Chagas RCR, Silva AMd, Varotti FdP, Taranto AG. 2016. Successful application of virtual screening and molecular dynamics simulations against antimalarial molecular targets. Memórias Do Instituto Oswaldo Cruz. 111(12):721–730. doi:10.1590/0074-02760160207.
  • Onasanya A, Bengtson M, Oladepo O, Engelen JV, Diehl JC, Author C. 2021. Rethinking the top-down approach to schistosomiasis control and elimination in sub-Saharan Africa. 9(February), 1–12. doi:10.3389/fpubh.2021.622809.
  • Otarigho B. 2019. Structural, functional and docking analysis against Schistosoma mansoni dihydroorotate dehydrogenase for potential chemotherapeutic drugs. F1000Res. 8:651–651. doi:10.12688/f1000research.18904.1.
  • Oyeyemi OT, de Jesus Jeremias W, Grenfell RFQ. 2020. Schistosomiasis in Nigeria: gleaning from the past to improve current efforts towards control. One Health. 11:10013–100183. doi:10.1016/j.onehlt.2020.100183.
  • Panic G, Duthaler U, Speich B, Keiser J. 2014. Repurposing drugs for the treatment and control of helminth infections. Int J Parasitol 4:185–200.
  • Pasche V, Laleu B, Keiser J. 2019. Early antischistosomal leads identified from in vitro and in vivo screening of the Medicines for Malaria Venture pathogen Box. ACS Infect Dis. 5(1):102–110. doi:10.1021/acsinfecdis.8b00220.
  • Pereira C, Saye M, Reigada C, Silber A, Labadie G, Miranda M, & Valera-Vera E. 2020. Computational approaches for drug discovery against trypanosomatid-caused diseases. Parasitology. 147(6):611–633. doi:10.1017/S0031182020000207.
  • Prieto-Martínez FD, López-López E, Juárez-Mercado KE, Medina-Franco JL. 2019. Computational drug design methods—current and future perspectives. In: In silico drug design. Veracruz: Academic Press; p. 19–44.
  • Roquini DB, Cogo RM, Mengarda AC, Mazloum SF, Morais CS, Xavier RP, Salvadori MC, Teixeira FS, Ferreira LE, Pinto PL, et al. 2019. Promethazine exhibits antiparasitic properties In vitro and reduces worm burden, Egg production, hepatomegaly, and splenomegaly in a schistosomiasis animal model daniel. American Society for Microbiology. 63(12):1–10.
  • Sanderson L, Bartlett A, Whitfield P. 2002. In vitro and in vivo studies on the bioactivity of a ginger (Zingiber officinale) extract towards adult schistosomes and their egg production. J Helminthol. 76(3):241–247. doi:10.1079/JOH2002116.
  • Schultz MD, Dadali T, Jacques SA, Muller-Steffner H, Foote JB, Sorci L, … Lund FE. 2020. Inhibition of the NAD salvage pathway in schistosomes impairs metabolism, reproduction, and parasite survival. PLoS Pathog. 16(5):e1008539–e1008539.
  • Selvaraj C, Chandra I, Kumar Singh S. 2021. Artifcial intelligence and machine learning approaches for drug design: challenges and opportunities for the pharmaceutical industries. Mol Diversity. doi:10.1007/s11030-021-10326-z.
  • Shelar DB, Shirote PJ. 2011. Natural product in drug discovery: back to future. Biomedical & Pharmacology Journal. 4(1):141–141.
  • Singh R, Pandey PN. 2015. Molecular docking and molecular dynamics study on SmHDAC1 to identify potential lead compounds against schistosomiasis. Mol Biol Rep. 42(3):689–698.
  • Sorokina M, Steinbeck C. 2020. Review on natural products databases: where to find data in 2020. J Cheminform. 12(1):1–51.
  • Sparg SG, Van Staden J, Jäger AK. 2000. Efficiency of traditionally used South African plants against schistosomiasis. J Ethnopharmacol. 73(1-2):209–214.
  • Stein EM, Machado LP, Roffato HK, Miyasato PA, Nakano E, Colepicolo P, Andreguetti DX. 2015. Antischistosomal activity from Brazilian marine algae. Revista Brasileira de Farmacognosia. 25:663–667.
  • Stein EM, Tajú SG, Miyasato PA, de Freitas RP, Tallarico LDF, Dos Santos GS, … Nakano E. 2021. The prospective use of Brazilian marine macroalgae in schistosomiasis control. Mar Drugs. 19(5):234–234.
  • Süntar I. 2020. Importance of ethnopharmacological studies in drug discovery: role of medicinal plants. Phytochem Rev. 19(5):1199–1209. doi:10.1007/s11101-019-09629-9.
  • Tavares NC, de Aguiar PHN, Gava SG, Oliveira G, Mourão MM. 2016. Schistosomiasis: setting routes for drug discovery. Special Topics in Drug Discovery. Chapter 5:116–24. doi:10.5772/65386.
  • Tekwu EM, Bosompem KM, Anyan WK, Appiah-Opong R, Owusu KBA, Tettey MD, … Nyarko AK. 2017. In vitro assessment of Anthelmintic activities of Rauwolfia vomitoria (apocynaceae) stem bark and roots against parasitic stages of Schistosoma mansoni and cytotoxic study. J Parasitol Res. 2017:2090–0023. doi:10.1155/2017/2583969.
  • Thomas CM, Timson DJ. 2020. The mechanism of action of praziquantel: can new drugs exploit similar mechanisms? Curr Med Chem. 27(5):676–696.
  • Torini JR, Romanello L, Batista FAH, Serrão VHB, Faheem M, Zeraik AE, … Pereira HDM. 2018. The molecular structure of Schistosoma mansoni PNP isoform 2 provides insights into the nucleoside selectivity of PNPs. PloS one. 13(9):e0203532–e0203532.
  • ToussiMatchi JL, TchamoNoungoue D, Kuhn I, Boissier J, Tchouankeu JC, Nothisen M, Wagner A. 2020. Manniindole, an indole derivative from the roots of Anonidium mannii and combined antischistosomal and enzymatic activities. Nat Prod Res. 0(0):1–9. doi:10.1080/14786419.2020.1824227.
  • Tung C. 2014. Public Databases of Plant Natural Products for Computational Drug Discovery. 191–196.
  • Wang L, Ding J, Pan L, Cao D, Jiang H, Ding X. 2019. Artificial intelligence facilitates drug design in the big data era. Chemom Intell Lab Syst. 194:article 103850–103850.
  • Weng HB, Chen HX, Wang MW. 2018. Innovation in neglected tropical disease drug discovery and development. Infect Dis Poverty. 7(1):1–9.
  • Wilson GL, Lill MA. 2011. Integrating structure-based and ligand-based approaches for computational drug design. Future Med. Chem. 3(6):735–750.
  • Xiao S, Chollet J, Utzinger J, Matile H, Mei J, Tanner M. 2001. Artemether administered together with haemin damages schistosomes in vitro. Trans R Soc Trop Med Hyg 95:67–71.
  • Xu X, Huang M, Zou X. 2018. Docking-based inverse virtual screening: methods, applications, and challenges. Biophys Rep. 4:1–16. doi:10.1007/s41048-017-0045-8.
  • Yousif F, Hifnawy MS, Soliman G, Boulos L, Labib T, Mahmoud S, … El-Menshawi BS. 2007. Large-scale in vitro. screening of Egyptian native and cultivated plants for schistosomicidal activity. Pharm Biol. 45(6):501–510.
  • Zorn KM, Sun S, Mcconnon CL, Ma K, Chen EK, Foil DH, Lane TR, Liu LJ, El-Sakkary N, Skinner DE, et al. 2021. A machine learning strategy for drug discovery identifies anti-schistosomal small molecules. ACS Infect Dis. 7(2):406–420. doi:10.1021/acsinfecdis.0c00754.