Constituents of the ripe fruits of Nauclea latifolia Sm. (Rubiaceae) and their antileishmanial activities

Trends in Phytochemical Research

دوره 6، شماره 4، اسفند 2022، صفحه 292-300   

نوع مقاله: Original Article

شناسه دیجیتال (DOI): 10.30495/tpr.2022.1966060.1275

نویسندگان

Argan Kelly Nkwenti Wonkam^{1، 2}؛ Cyrille Armel Ngansop Njanpa³؛ Joël E.T. Ateba^{* 4}؛ Yannick S.F. Fongang⁵؛ Angelbert Fusi Awantu^{* 6}؛ J.J.K. Bankeu⁶؛ Jean Rodolph Chouna⁷؛ Fabrice F. Boyom³؛ Norbert Sewald⁸؛ Bruno Ndjakou Lenta^{* 1}

¹Department of Chemistry, Higher Teacher Training College, University of Yaoundé 1, P.O. Box 47, Yaoundé, Cameroon

²Department of Organic Chemistry, Faculty of Science, University of Yaoundé 1, P.O. Box 812, Yaoundé, Cameroon

³Department of Biochemistry, Faculty of Science, University of Yaoundé 1, P.O. Box 812, Yaoundé, Cameroon

⁴Department of Process Engineering, National Higher Polytechnic School, University of Douala, P.O. Box 2701, Douala, Cameroon

⁵Department of Chemistry, Higher Teacher Training College, University of Maroua, P.O. Box 55, Maroua, Cameroon

⁶Department of Chemistry, Faculty of Science, The University of Bamenda, P.O. Box 39, Bambili, Cameroon

⁷Department of Chemistry, Faculty of Science, University of Dschang, P.O. Box 67, Dschang, Cameroon

⁸Organic and Bioorganic Chemistry, Faculty of Chemistry, Bielefeld University, D-33501, Bielefeld, Germany

چکیده

The MeOH extract of the ripe fruits of Nauclea latifolia Sm. (Rubiaceae) showed potent antileishmanial activity in vitro during preliminary screening (IC50 = 2.20 µg/mL) against Leishmania donovani 1S (MHOM/SD/62/1S) promastigotes. Three of the four fractions of this extract showed moderate to good activities (7.06 ≤ IC50 ≤ 91.21 µg/mL) on the same strain. The purification of the fractions through CC yielded fifteen compounds whose structures were established based on their MS and NMR data. All the isolated compounds were assessed for their antileishmanial activity against L. donovani and for their cytotoxicity towards Raw 264.7 macrophage cells. 2,6-Dimethoxybenzoquinone (1) and hederagenin (6) showed good antileishmanial activity with IC50 values of 9.94 and 19.3 µM, respectively. Compound 1 was not selective, while compound 6 displayed a good selectivity towards raw 264.7 macrophage cells (SI > 7.82). These results indicate that the extract from N. latifolia fruits could be considered as a source of leishmaniacidal agents.

کلیدواژه‌ها

Cytotoxicity؛ Leishmaniasis؛ Nauclea latifolia؛ Ripe fruits؛ Rubiaceae

مراجع

Abreu, P., Pereira, A., 2001. New indole alkaloids from Sarcocephalus latifolius. Nat. Prod. Res. 5, 43-48.
Adeniran, O.I., Abimbade, S.F., 2015. Characterization of compounds from leaf extracts of tree spinach-Cnidoscolus aconitifolius (Miller) I. M. Johnston. Int. J. Sci. Res. Chem. Eng. 1, 82-86.
Agrawal, P.K., 1992. NMR spectroscopy in the structural elucidation of oligosaccharides and glycosides. Phytochemistry 31, 3307-3330.
Ahua, K.M., Ioset, J.R., Ioset, K.N., Diallo, D., Mauël, J., Hostettmann, K., 2007. Antileishmanial activities associated with plants used in the Malian traditional medicine. J. Ethnopharmacol. 10, 99-104.
Akhoundi, M., Kuhls, K., Cannet, A., Votypka, J., Marty, P., Delaunay, P., 2016. A historical overview of the classification, evolution, and dispersion of Leishmania parasites and sandflies. PLoS Negl. Trop. Dis. 10, e0004349.
Bankeu, K.J.J., Kagho, K.D.U., Fongang, F.S.Y., Toghueo, K.R.M., Mba’ning, B.M., Feuya, T.G.R., Fekam, B.F., Tchouankeu, J.C., Ngouela, S.A., Sewald, N., Lenta, N.B., Ali, M.S., 2019. Constituents from Nauclea latifolia with anti-Haemophilus influenzae type b inhibitory activities. J. Nat. Prod. 82, 2580-2585.
Bapela, M.J., Kaiser, M., Meyer, J.J.M., 2017. Antileishmanial activity of selected South African plant species. S. Afr. J. Bot. 108, 342-345.
Bianco, A., Venditti, A., Foddai, S., Toniolo, C., Nicoletti, M., 2014. A new problem. Contamination of botanicals by phthalates. Rapid detection tests. Nat. Prod. Rep. 28, 134-137.
Boucherle, B., Haudecoeur, R., Ferreira, Q.E., De Waard, M., Wolfender, J.-L., Robins, R.J.,  Boumendjel, A., 2016. Nauclea latifolia: biological activity and alkaloid phytochemistry of a West African tree. Nat. Prod. Rep. 33, 1034-1043.
Bremer, B., Eriksson, T., 2009. Time tree of Rubiaceae: Phylogeny and dating the family, subfamilies and tribes. Int. J. Plant Sci. 170, 766-793.
Caesar, L.K., Cech, N.B., 2019. Synergy and antagonism in natural product extracts: when 1+1 does not equal 2. Nat. Prod. Rep. 36, 869-888.
Croft, S.L., Coombs, G.H., 2003. Leishmaniasis-current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol. 19, 502-508.
De Sena, P.V.S., De Oliveira, C.B.S., Fumagalli, F., Da Silva, E.F., Da Silva, N.B., De Andrade-Neto, V.F., 2016. Cytotoxicity, hemolysis and in vivo acute toxicity of 2-hydroxy-3-anilino-1,4-naphthoquinone derivatives. Toxicol. Rep. 3, 756-762.
Eder, B., Walmir, S.G., Lidihone, H., Caroline, T., Fernanda, R.G., 2008. Bioactive pentacyclic triterpenes from the stems of Combretum laxum. Molecules 13, 2717-2728.
Fadipe, A.L., 2014a. Some fatty acid esters of the ripe fruits of Nauclea latifolia (family Rubiaceae). Int. J. Pharm. Chem. Res. 4, 783-788.
Fadipe, A.L., 2014c. Isolation and characterization of di-(1-hexen-5-yl) phthalate and monoethyl phthalate from the ethyl acetate extract of unripe fruits of Nauclea latifolia. Int. J. Biol. Pharm. Allied Sci. 3, 776-784.
Fadipe, A.L., Haruna, K., Mohammed I., 2014b. Antibacterial activity of 1,2-benzenedicarboxylic acid, dioctyl ester isolated from the ethyl acetate soluble sub-portion of the unripe fruits of Nauclea latifolia. Int. J. Pure Appl. Biosci. 2, 223-230.
Fadipe, A.L., Haruna, K., Mohammed, I., Usman, P.U., 2015. Some volatile constituents of the unripe fruits of Nauclea latifolia (Family: Rubiaceae). J. Med. Plants Stud. 3, 1-4.
Gidado, A., Ameh, D.A., Atawodi, S.E., 2005. Effect of Nauclea latifolia leaves aqueous extracts on bloods glucose levels of normal and alloxan-induced diabetic rats. Afr. J. Biotechnol. 4, 91-93.
Goijman, G., Turrens, F., Marini-Bettolo, B., Stoppani, O., 1984. Inhibition of growth and macromolecular biosynthesis in Trypanosoma cruzi by natural products. Effects of miconidine and tingenone. J. Herb. Med. Pharmacol. 44, 361-370.
Habib, M.R., Nikkon, F., Rahman, M., Haque, M.E., Karim, M.R., 2007. Isolation of stigmasterol and β-sitosterol from methanolic extract of root bark of Calotropis gigantea (Linn). Pak. J. Biol. Sci. 10, 4174-4176.
Haudecoeur, R., Peuchmaur, M., Peres, B., Rome, M., Taiwe, G.S., Boumendjel, A., Boucherle B., 2018. Traditional uses, phytochemistry and pharmacological properties of African Nauclea latifolia species: A review. J. Ethnopharmacol. 212, 106-136.
Hotellier, F., Delaveau, P., 1975. Naucléfine et Nauclétine deux nouveaux alcaloïdes de type indoloquinolizidine isolés de Nauclea latifolia. Phytochemistry 14, 1407-1409.
Igoli, J.O., Tsenongo, S.N., Tor-Anyiin, T.A., 2011. A Survey of anti-venomous, toxic and other plants used in some parts of Tivland, Nigeria. Int. J. Appl. Res. Med. Aromat. Plants 1, 240-244.
Isah, M.B., Ibrahim, M.A., Mohammed, A., Aliyu, A.B., Masola, B., Coetzer, H.T.T., 2016. Systematic review of pentacyclic triterpenes and their derivatives as chemotherapeutic agents against tropical parasitic diseases. Parasitology 143, 1219-1231.
James, O., Ugbede, H.H., 2011. Hypocholesterolemic effects of Nauclea latifolia (Smith) fruits studied in albino rats. Int. J. Trop. Dis. Health 1, 11-21.
Jian-Juan, L.I., Jie, Y., Fang, L., Yin-Tao, Q.I., Yan-Qing, L.I.U., Yun, S., Wang, Q., 2012. Chemical constituents from the stems of Celastrus orbiculatus. Chin. J. Nat. Med. 10, 279-283.
Kanchanapoom, T., Picheansoonthon, C., Kasai, R., Yamasaki, K., 2001. New glucosides from Thai medicinal plant Balanophora Iatisepala. J. Nat. Med. 55, 213-216.
Khanjani, J. S., Farazmand, A., Amin, M., Doroodgar, A., Shirzadi, M., Razavi, M., 2015. Methanolic extract’s activity of Artemisia absinthium, Vitex agnus-castus and Phytolaca Americana against Leishmania major in vitro and in vivo. Int. J. Health Sci. 2, 69-74.
Kostalova, D., Hrochova, V., Suchy, V., Budesinsky, M., Ubik, K., 1992. Two pyrrole acids from Berberis koreana. Phytochemistry 31, 3669-3670.
Kuete, V., Sandjo, L.P., Mbaveng, A.T., Seukep, J.A., Ngadjui, B.T., Efferth, T., 2015. Cytotoxicity of selected Cameroonian medicinal plants and Nauclea pobeguinii towards multi-factorial drug-resistant cancer cells. BMC Complement. Altern. Med. 15, 1-6.
Lenta, B.N., Ngamgwe, R.F., Kamdem, L.M., Ngatchou, J., Tantangmo, F., Antheaume, C., Ngouela, S., Tsamo, E., Sewald, N., 2015. Compounds from Diospyros canaliculata (Ebenaceae) and their antiparasitic activities. Int. Res. J. Pure Appl. Chem. 6, 56-65.
Lenta, B.N., Vonthron-Sénécheau, C., Weniger, B., Devkota, K.P., Ngoupayo, J., Kaiser M., Naz, Q., Choudhary, M.I., Tsamo, E., Sewald, N., 2007. Leishmanicidal and cholinesterase inhibiting activities of phenolic compounds from Allanblackia monticola and Symphonia globulifera. Molecules 12, 1548-1557.
Lima, T. C., Souza, R.J., Santos, A.D., Moraes, M.H., Biondo, N.E., Barison, A.,  Steindel, M., Biavatti, M.W., 2015. Evaluation of leishmanicidal and trypanocidal activities of phenolic compounds from Calea uniflora Less. Nat. Prod. Res. 30, 551-557.
Liu, Y.P., Ju, P.K., Long, J.T., Lai, L., Zhao, W.H., Zhang, C., Zhang, Z.J., Fu, Y.H., 2018. Cytotoxic indole alkaloids from Nauclea orientalis. Nat. Prod. Res. 32, 2922-2927.
Mahato, S.B., Kundu, A., 1994. 13C NMR spectra of pentacyclic triterpenoids-a compilation and some salient features. Phytochemistry 37, 1517-1575.
Mai, S.Y., Li, Y.H., Zhang, X.G., Wang, Y.R., Zhang, J.Q., Jia, A., 2021. A new indole alkaloid with HUVEC proliferation activities from Nauclea officinalis. Nat. Prod. Res. 35, 3049-3055.
Mohammadhosseini, M., Venditti, A., Frezza, C., Serafini, M., Bianco, A., Mahdavi, B., 2021. The genus Haplophyllum Juss.: Phytochemistry and bioactivities—A review. Molecules 26, 4664.
Mishina, V., Krishna, S., Haynes, K., Meade, C., 2007. Artemisinins inhibit Trypanosoma cruzi and Trypanosoma brucei rhodesiense in vitro growth. Antimicrob. Agents Chemother. 51, 1852-1854.
Mosmann, T., 1993. Rapid colorimetric assay for cellular growth and survival application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
Nahar, L., Sarker, S.D., 2021. ‘Gandho badali’ (Paederia foetida L.): Horrendous smell, but tremendous medicinal value. Trends Phytochem. Res. 5, 166-167.
Ngnokam, D., Ayafor, J.F., Connolly, J.D., Nuzillard, J.M., 2003. Nauclefolinine: a new alkaloid from the roots of Nauclea latifolia. Bull. Chem. Soc. Ethiop. 17, 173-176.
Nkouayeb, B.M.N., Azebaze, A.G.B., Tabekoueng, G.B., Tsopgni, W.D.T., Lenta, B.N., Frese, M, Sewald, N., Vardamides, J.C., 2020. Chemical Constituents of Nauclea vanderguchtii. Nat. Prod. Sci. 26, 144-150.
Sattar, A.F., Ahmed, F., Ahmed, N., Sattar, A.S., Malghani, A.K.M., Choudarhy, I.M., 2012. A doubled blind, randomized, clinical trial on the antileishmanial activity of a Morinda citrifolia (Noni) stem extract and its major constituents. Nat. Prod. Commun. 7, 195-440.
Shigemori, H., Kagata, T., Ishiyama, H., Morah, F., Ohsaki, A., Kobayashi, J., 2003. Naucleamides A-E, new monoterpene indole alkaloids from Nauclea latifolia. Chem. Pharm. Bull. 51, 58-61.
Singh, N., Mishra, B.B., Bajpai, S., Singh, R.K., Tiwari, V.K., 2014. Natural product based leads to fight against leishmaniasis. Bioorg. Med. Chem. 22, 18-45.
Siqueira-Neto, J.L., Song, O.-R., Oh, H., Sohn, J.-H., Yang, G., Nam, J., Jang, J., Cechetto, J., Lee, C.B., Moon, S., Genovesio, A., Chatelai, E., Christophe, T., Freitas-Junior, L.H., 2010. Antileishmanial high-throughput drug screening reveals drug candidates with new scaffolds. PLOS Negl. Trop. Dis. 4, e675.
Sorensen, J.L., 2010. The isolation of citric acid derivatives from Aspergillus niger. FEMS Microbiol. Lett. 306, 123-124.
Sun, J.S., Tsuang, Y.H., Huang, W.C., Chen, L.T., Hang, Y.S., Lu, F.J., 1997. Menadione-induced cytotoxicity to rat osteoblasts. Cell. Mol. Life Sci. 53, 967-976.
Taiwe, G.S., Ngo Bum, E., Talla, E., Dimo, T., Dawe, A., Sinniger, V., 2014. Nauclea latifolia smith (Rubiaceae) exerts antinociceptive effects in neuropathic pain induced by chronic constriction injury of the sciatic nerve. J. Ethnopharmacol. 151, 445-451.
Thiemann, T., 2021. Isolation of Phthalates and Terephthalates from Plant Material - Natural Products or Contaminants? Open Chem. J. 8, 1-36.
Venditti, A., Frezza, C., Riccardelli, M., Foddai, S., Nicoletti, M., Serafini, M., Bianco, A. 2015. Unusual molecular pattern in Ajugoideae subfamily: the case of Ajuga genevensis L. from Dolomites. Nat. Prod. Res. 30, 1098-1102.
Venditti, A., 2018. What is and what should never be: artifacts, improbable phytochemicals, contaminants and natural products. Nat. Prod. Res., 1-18.
Wandji, J., Tillequin, F., Mulholland, D.A., Shirri, J.C., Tsabang, N., Seguin, E., Verite, P., Libot, F., Fomum, Z.T., 2003. Pentacyclic triterpenoid and saponins from Gambeya boukokoensis. Phytochemistry 64, 845-849.
WHO. World Health Report, 2000. Special programme for Research and Training in Tropical Disease (TDR). Natural products for parasitic diseases. TDR News.
Wonkam, A.K.N., Ngansop, C.A.N., Wouamba, S.C.N., Jouda, J.B., Happi, G.M., Boyom, F.F., Sewald, N., Lenta, B.N., 2020. Rothmanniamide and other constituents from the leaves of Rothmannia hispida (K. Schum.) Fagerl. (Rubiaceae) and their chemophenetic significance. Biochem. Syst. Ecol. 93, 104137.
Xiaoling, L., Shihai, X., Kai, Y., Shuhao, G., Xiangchao Z., 2004. Isolation and identification of the secondary metabolites from Hydroclathrus clathratus. Zhongyaocai 27, 254-256.