Login Register Cart 0
Generic placeholder image

Current Topics in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1568-0266
ISSN (Online): 1873-4294

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Absolute Configuration and Antileishmanial Activity of (–)-Cyclocolorenone Isolated from Duguetia lanceolata (Annonaceae)

Author(s): Jackson Monteiro, Luiz Felipe D. Passero, Jéssica A. Jesus, Márcia D. Laurenti, João H. G. Lago, Marisi G. Soares, Andrea N. L. Batista, João M. Batista* and Patricia Sartorelli*

Volume 22, Issue 19, 2022

Published on: 27 July, 2022

Page: [1626 - 1633] Pages: 8

DOI: 10.2174/1568026622666220707095718

Price: $65

Abstract

Background: The fractionation of the n-hexane phase of the EtOH extract from the leaves of Duguetia lanceolata (Annonaceae) led to the identification of the sesquiterpene (–)-cyclocolorenone.

Objectives: Chemical characterization, including determination of the absolute stereochemistry, and in vitro evaluation of antileishmanial activity of the sesquiterpene (–)-cyclocolorenone, isolated from D. lanceolata, were carried out.

Methods: (–)-Cyclocolorenone was isolated from D. lanceolata leaves using different chromatographic steps and its structure was defined by analysis of NMR and ESI-HRMS data. Additionally, the absolute configuration of (–)-cyclocolorenone was ambiguously assigned by means of vibrational circular dichroism (VCD). Antileishmanial activity of (–)-cyclocolorenone was evaluated on promastigote and amastigote forms of Leishmania (Leishmania) amazonensis. The integrity of the cell membrane of L. (L.) amazonensis was analyzed using the SYTOX green probe.

Results: (–)-(1R,6S,7R,10R)-Cyclocolorenone displayed activity against promastigotes and amastigotes forms of L. (L.) amazonensis with IC50 of 4.54 and 28.44 µM, respectively. Furthermore, this compound was non-toxic in J774 macrophage cells (CC50 > 458.71 µM) with a selectivity index > 100 (promastigotes) and > 32.2 (amastigotes). Additionally, (–)-cyclocolorenone was observed to target the parasite cell membrane.

Conclusion: Obtained data suggested that (–)-cyclocolorenone, in which absolute configuration was determined, can be considered as a scaffold for the development of new drugs for the treatment of leishmaniasis.

Keywords: Duguetia lanceolata, (–)-Cyclocolorenone, VCD, Antileishmanial activity, Cell membrane, Macrophage cells.

« Previous
Graphical Abstract

[1]
Pérez, E.G.; Cassels, B.K. Alkaloids from the genus duguetia. In: Alkaloids: Chemistry and Biology; Elsevier, 2010; p. 68.
[http://dx.doi.org/10.1016/S1099-4831(10)06803-3]
[2]
Fosberg, F.R.; Schultes, R.E.; Raffauf, R.F. The healing forest: Medicinal and toxic plants of the northwest amazonia. Taxon, 1991, 40(1), 40.
[http://dx.doi.org/10.2307/1222960]
[3]
Muhammad, I.; Dunbar, D.C.; Takamatsu, S.; Walker, L.A.; Clark, A.M. Antimalarial, cytotoxic, and antifungal alkaloids from Duguetia hadrantha. J. Nat. Prod., 2001, 64(5), 559-562.
[http://dx.doi.org/10.1021/np000436s] [PMID: 11374943]
[4]
Fechine, I.M.; Navarro, V.R.; da-Cunha, E.V.L.; Silva, M.S.; Guilherme, S.; Maia, J.; Barbosa-Filho, J.M. Alkaloids and volatile constituents from Duguetia flagellaris. Biochem. Syst. Ecol., 2002, 30(3), 267-269.
[5]
Carollo, C.A.; de Siqueira, J.M.; Garcez, W.S.; Diniz, R.; Fernandes, N.G. N-nitrosoanonaine and N-nitrosoxylopine, aporphine alkaloids from Duguetia furfuracea. J. Nat. Prod., 2006, 69(8), 1222-1224.
[http://dx.doi.org/10.1021/np0600191] [PMID: 16933882]
[6]
Lúcio, A.S.S.C.; Almeida, J.R.G. da S.; da-Cunha, E.V.L.; Tavares, J.F.; Barbosa Filho, J.M Chapter five-alkaloids of the Annonaceae: Occurrence and a compilation of their biological activities;Elsevier; , 2015, 74, pp. 233-409.
[7]
Leboeuf, M.; Cavé, A.; Bhaumik, P.K.; Mukherjee, B.; Mukherjee, R. The phytochemistry of the annonaceae. Phytochemistry, 1982, 21, 2783-2813.
[8]
Cavé, A.; Leboeuf, M.; Waterman, P.G. The aporphinoid alkaloids of the annonaceae. In: Alkaloids: Chemical and Biological Perspectives; John Wiley: New York, 1987; 5, pp. 134-270.
[9]
Padoan Gonçalves, G.L.; de Cássia Domingues, V.; do Prado Ribeiro, L.; Fernandes, J.B. de Fátima das Graças Fernandes, M.; Rossi Forim, M.; Vendramim, J.D. Compounds from Duguetia Lanceolata St.- Hil. (Annonaceae) bioactive against Zabrotes subfasciatus (Boheman) (Coleoptera: Chrysomelidae: Bruchinae). Ind. Crops Prod., 2017, 97, 360-367.
[10]
Santos, D.Y.A.C.; Salatino, M.L.F. Foliar flavonoids of Annonaceae from Brazil: Taxonomic significance. Phytochemistry, 2000, 55(6), 567-573.
[http://dx.doi.org/10.1016/S0031-9422(00)00227-2] [PMID: 11130666]
[11]
Attiq, A.; Jalil, J.; Husain, K. Annonaceae: Breaking the wall of inflammation. Front. Pharmacol., 2017, 8, 752.
[http://dx.doi.org/10.3389/fphar.2017.00752] [PMID: 29104539]
[12]
Parra, J.; De Ford, C.; Murillo, R. Phytochemical study of endemic costa rican annonaceae species Annona pittieri and Cymbopetalum costaricense. J. Chil. Chem. Soc., 2021, 66(1), 66.
[http://dx.doi.org/10.4067/S0717-97072021000105047]
[13]
Brastianos, H.C.; Sturgeon, C.M.; Roberge, M.; Andersen, R.J. Inhibition of the G2 DNA damage checkpoint by oliveroline isolated from Duguetia odorata. J. Nat. Prod., 2007, 70(2), 287-288.
[http://dx.doi.org/10.1021/np060285e] [PMID: 17315964]
[14]
Matos, M.F.C.; Leite, L.I.S.P.; Brustolim, D.; de Siqueira, J.M.; Carollo, C.A.; Hellmann, A.R.; Pereira, N.F.G.; da Silva, D.B. Antineoplastic activity of selected constituents of Duguetia glabriuscula. Fitoterapia, 2006, 77(3), 227-229.
[http://dx.doi.org/10.1016/j.fitote.2006.01.013] [PMID: 16563660]
[15]
Mesquita, M.L.; Desrivot, J.; Bories, C.; Fournet, A.; Paula, J.E.; Grellier, P.; Espindola, L.S. Antileishmanial and trypanocidal activity of Brazilian Cerrado plants. Mem. Inst. Oswaldo Cruz, 2005, 100(7), 783-787.
[http://dx.doi.org/10.1590/S0074-02762005000700019] [PMID: 16419337]
[16]
Isernhagen, I. Floristic listing of tree and shrub species in mato grosso: A starting point for ecological restoration projects / ingo isernhagen Sinop: Embrapa Agrossilvipastoril, 2015.
[17]
Maas, P.; Lobão, A.; Rainer, H. Annonaceae in List of Brazilian Flora Species., Available from: http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB110319
[18]
Fischer, D.C.H.; de Amorim Gualda, N.C.; Bachiega, D.; Carvalho, C.S.; Lupo, F.N.; Bonotto, S.V.; Alves, M. de O.; Yogi, A.; Santi, S.M.; Avila, P.E.; Kirchgatter, K.; Moreno, P.R.H. In vitro screening for antiplasmodial activity of isoquinoline alkaloids from Brazilian plant species. Acta Trop., 2004, 92(3), 261-266.
[http://dx.doi.org/10.1016/j.actatropica.2004.08.009] [PMID: 15533296]
[19]
Sousa, O.V.; Del-Vechio-Vieira, G.; Amaral, M.P.H.; Pinho, J.J.R.G.; Yamamoto, C.H.; Alves, M.S. Antinociceptive and anti-inflammatory effects of the ethanolic extract of the leaves of Duguetia lanceolata St.-Hil. (Annonaceae). Lat. Am. J. Pharm., 2008, 2008, 27.
[20]
Sousa, O.V.; Soares Júnior, D.T.; Del-Vechio, G.; Mattosinhos, R.G.; Gattass, C.R.; Kaplan, M.A.C. Antinociceptive and anti-inflammatory activities of Duguetia lanceolata St. Hil. Annonaceae. Rev. Bras. Farmacogn., 2004, 14, 398-402.
[21]
Sousa, O.V.; Del-Vechio-Vieira, G.; Alves, M.S.; Araújo, A.A.L.; Pinto, M.A.O.; Amaral, M.P.H.; Rodarte, M.P.; Kaplan, M.A.C. Chemical composition and biological activities of the essential oils from Duguetia lanceolata St. Hil. barks. Molecules, 2012, 17(9), 11056-11066.
[http://dx.doi.org/10.3390/molecules170911056] [PMID: 22976469]
[22]
Tempone, A.G.; Borborema, S.E.; de Andrade, H.F., Jr; de Amorim Gualda, N.C.; Yogi, A.; Carvalho, C.S.; Bachiega, D.; Lupo, F.N.; Bonotto, S.V.; Fischer, D.C.H. Antiprotozoal activity of Brazilian plant extracts from isoquinoline alkaloid-producing families. Phytomedicine, 2005, 12(5), 382-390.
[http://dx.doi.org/10.1016/j.phymed.2003.10.007] [PMID: 15957374]
[23]
Dantas, E.; Monteiro, J.; de Medeiros, L.; Romanelli, M.; Amaral, M.; Tempone, A.; Lago, J.H.; Soares, M.; Sartorelli, P. Dereplication of Aporphine Alkaloids by UHPLC-HR-ESI-MS/MS and NMR from Duguetia lanceolata St.-Hil (Annonaceae) and antiparasitic activity evaluation. J. Braz. Chem. Soc., 2020, 31, 1908-1916.
[http://dx.doi.org/10.21577/0103-5053.20200089]
[24]
Neves, D.P.M.; de Linardi, A.L.; Vitor, P.M. Human parasitology. Athena, 11th ed; Elsevier, 2005, pp. 1-494.
[25]
Sandoval Pacheco, C.M.; Araujo Flores, G.V.; Gonzalez, K.; De Castro Gomes, C.M.; Passero, L.F.D.; Tomokane, T.Y.; Sosa-Ochoa, W.; Zúniga, C.; Calzada, J.; Saldaña, A.; Corbett, C.E.P.; Silveira, F.T.; Laurenti, M.D. Macrophage polarization in the skin lesion caused by neotropical species of Leishmania. Sp. J. Immunol. Res., 2021, 2021, 5596876.
[http://dx.doi.org/10.1155/2021/5596876]
[26]
Atta, -ur-Rahman S.; Atia-tul-Wahab; Iqbal Choudhary, M. Discovery of leishmanicidal agents from medicinal plants. Proc. Pure Appl. Chem., 2008, 80, 1783-1790.
[27]
Caldas, L.A.; Yoshinaga, M.L.; Ferreira, M.J.P.; Lago, J.H.G.; de Souza, A.B.; Laurenti, M.D.; Passero, L.F.D.; Sartorelli, P. Antileishmanial activity and ultrastructural changes of sesquiterpene lactones isolated from Calea pinnatifida (Asteraceae). Bioorg. Chem., 2019, 83, 348-353.
[http://dx.doi.org/10.1016/j.bioorg.2018.10.059] [PMID: 30399466]
[28]
Dos Santos, A.L.; Amaral, M.; Hasegawa, F.R.; Lago, J.H.G.; Tempone, A.G.; Sartorelli, P. (–)-T-Cadinol-a sesquiterpene isolated from casearia sylvestris (salicaceae)-displayed in vitro activity and causes hyperpolarization of the membrane potential of trypanosoma cruzi. Front. Pharmacol., 2021, 12, 734127.
[http://dx.doi.org/10.3389/fphar.2021.734127] [PMID: 34803682]
[29]
De Jesus, J.A.; Laurenti, M.D.; Antonangelo, L.; Faria, C.S.; Lago, J.H.G.; Passero, L.F.D. Related pentacyclic triterpenes have immunomodulatory activity in chronic experimental visceral leishmaniasis. J. Immunol. Res., 2021, 2021, 6671287.
[http://dx.doi.org/10.1155/2021/6671287]
[30]
Frisch, M.J.; Trucks, G.W.; Schlegel, H.B.; Scuseria, G.E.; Robb, M.A.; Cheeseman, J.R.; Scalmani, G.; Barone, V.; Petersson, G.A.; Nakatsuji, H.; Li, X.; Caricato, M.; Marenich, A.V.; Bloino, J.; Janesko, B.G.; Gomperts, R.; Mennucci, B.; Hratchian, H.P.; Ortiz, J.V.; Izmaylov, A.F.; Sonnenberg, J.L.; Williams Ding, F.; Lipparini, F.; Egidi, F.; Goings, J.; Peng, B.; Petrone, A.; Henderson, T.; Ranasinghe, D.; Zakrzewski, V.G.; Gao, J.; Rega, N.; Zheng, G.; Liang, W.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Throssell, K.; Montgomery, J.A.; Peralta, J.E.; Ogliaro, F.; Bearpark, M.J.; Heyd, J.J.; Brothers, E.N.; Kudin, K.N.; Staroverov, V.N.; Keith, T.A.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.P.; Burant, J.C.; Iyengar, S.S.; Tomasi, J.; Cossi, M.; Millam, J.M.; Klene, M.; Adamo, C.; Cammi, R.; Ochterski, J.W.; Martin, R.L.; Morokuma, K.; Farkas, O.; Foresman, J.B.; Fox, D.J. Gaussian09 Revision A.02; Gaussian, Inc.: Wallingford, CT, 2009.
[31]
Wu, C.L.; Chen, C.L. Oxygenated sesquitterpenes from the liverwort bazzania tridens. Phytochemistry, 1992, 31(12), 31.
[http://dx.doi.org/10.1016/0031-9422(92)80445-K]
[32]
la Torre Fabiola, V.D.; Ralf, K.; Gabriel, B.; Victor Ermilo, A.A.; Martha, M.G.; Mirbella, C.F.; Rocio, B.A. Anti-inflammatory and immunomodulatory effects of Critonia aromatisans leaves: Downregulation of pro-inflammatory cytokines. J. Ethnopharmacol., 2016, 190, 174-182.
[http://dx.doi.org/10.1016/j.jep.2016.06.006] [PMID: 27282666]
[33]
Ishii, T.; Shinjo, Y.; Miyagi, M.; Matsuura, H.; Abe, T.; Kikuchi, N.; Suzuki, M. Investigation of insect repellent activity of cyclocolorenone obtained from the red alga Laurencia intricata. Rec. Nat. Prod., 2019, 13, 81-84.
[34]
Corbett, R.E.; Speden, R.N. 743. The volatile oil of Pseudowintera colorata. Part II. The structure of cyclocolorenone. J. Chem. Soc., 1958, 3710.
[http://dx.doi.org/10.1039/jr9580003710]
[35]
Ingwalson, P.F. Part I. Total Synthesis of (-) -Cyclocolorenone; Part II. Total Synthesis of (±)-a-Vetispirene; Georgia Institute of Technolog: School of Chemistry and Biochemistry Theses and Dissertations, 1973.
[36]
Jacyno, J.M.; Cutler, H.G.; Montemurro, N.; Bates, A.D. Phytotoxic and antimicrobial properties of cyclocolorenone from Magnolia grandiflora L. J. Agric. Food Chem., 1991, 39(6), 39.
[http://dx.doi.org/10.1021/jf00006a036]
[37]
Büchi, G.; Kauffman, J.M.; Loewenthal, H.J.E. Synthesis of 1-epicyclocolorenone and stereochemistry of cyclocolorenone1. J. Am. Chem. Soc., 1966, 88, 3403-3408.
[38]
Matsuo, A.; Nakayama, M.; Sato, S.; Nakamoto, T.; Uto, S.; Hayashi, S. (–)-Maalioxide and (+)-cyclocolorenone, enantiomeric sesquiterpenoids from the liverwort, Plagiochila acanthophylla Subsp. Japonica. Experientia, 1974, 30, 321-322.
[39]
Křepinský, J.; Herout, V. Plant Substances. XVIII. Isolation of terpenic compounds from Solidago Canadensis L. Collect. Czech. Chem. Commun., 1962, 27, 2459-2462.
[40]
Batista, A.N.L.; Angrisani, B.R.P.; Lima, M.E.D.; da Silva, S.M.P.; Schettini, V.H.; Chagas, H.A.; dos Santos, F.M., Jr; Batista, J.M., Jr; Valverde, A.L. Absolute configuration reassignment of natural products: An overview of the last decade. J. Braz. Chem. Soc., 2021, 32, 79.
[http://dx.doi.org/10.21577/0103-5053.20210079]
[41]
Batista, J.M., Jr; Blanch, E.W.; Bolzani, V.S. Recent advances in the use of vibrational chiroptical spectroscopic methods for stereochemical characterization of natural products. Nat. Prod. Rep., 2015, 32(9), 1280-1302.
[http://dx.doi.org/10.1039/C5NP00027K] [PMID: 26140548]
[42]
Polavarapu, P.L.; Santoro, E. Vibrational optical activity for structural characterization of natural products. Nat. Prod. Rep., 2020, 37(12), 1661-1699.
[http://dx.doi.org/10.1039/D0NP00025F] [PMID: 32608433]
[43]
Cerda-García-Rojas, C.M.; Catalán, C.A.N.; Muro, A.C.; Joseph-Nathan, P. Vibrational circular dichroism of Africanane and Lippifoliane sesquiterpenes from Lippia integrifolia. J. Nat. Prod., 2008, 71(6), 967-971.
[http://dx.doi.org/10.1021/np8000927] [PMID: 18500843]
[44]
Matsuda, H.; Pongpiriyadacha, Y.; Morikawa, T.; Kashima, Y.; Nakano, K.; Yoshikawa, M. Protective effects of polygodial and related compounds on ethanol-induced gastric mucosal lesions in rats: Structural requirements and mode of action. Bioorg. Med. Chem. Lett., 2002, 12(3), 477-482.
[http://dx.doi.org/10.1016/S0960-894X(01)00781-8] [PMID: 11814823]
[45]
Mikhailova, N.S.; Konovalova, O.A.; Zakharov, P.I.; Rybalko, K.S. Isolation of cyclocolorenone from the essential oil of Ledum palustre. Chem. Nat. Compd., 1978, 14, 201302105029.
[46]
Asakawa, Y.; Toyota, M.; Uemoto, M.; Aratani, T. Sesquiterpenes of six Porella Species (Hepaticae). Phytochemistry, 1976, 15, 1929-1931.
[47]
Asakawa, Y.; Toyota, M.; von Konrat, M.; Braggins, J.E. Volatile components of selected species of the liverwort genera Frullania and Schusterella (Frullaniaceae) from New Zealand, Australia and South America: A chemosystematic approach. Phytochemistry, 2003, 62(3), 439-452.
[http://dx.doi.org/10.1016/S0031-9422(02)00542-3] [PMID: 12620357]
[48]
Nagashima, F.; Momosaki, S.; Watanabe, Y.; Takaoka, S.; Huneck, S.; Asakawa, Y. Sesquiterpenoids from the Liverworts Bazzania trilobata and Porella canariensis. Phytochemistry, 1996, 42(5), 42.
[http://dx.doi.org/10.1016/0031-9422(96)00105-7]
[49]
Chan-Bacab, M.J.; Peña-Rodríguez, L.M. Plant natural products with leishmanicidal activity. Nat. Prod. Rep., 2001, 18(6), 674-688.
[http://dx.doi.org/10.1039/b100455g] [PMID: 11820764]
[50]
Salem, M.M.; Werbovetz, K.A. Natural products from plants as drug candidates and lead compounds against leishmaniasis and trypanosomiasis. Curr. Med. Chem., 2006, 13(21), 2571-2598.
[http://dx.doi.org/10.2174/092986706778201611] [PMID: 17017912]
[51]
Deshpande, R.G.; Khan, M.B.; Genco, C.A. Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis. Infect. Immun., 1998, 66(11), 5337-5343.
[http://dx.doi.org/10.1128/IAI.66.11.5337-5343.1998] [PMID: 9784541]
[52]
Araujo, C.A.C.; Alegrio, L.V.; Gomes, D.C.F.; Lima, M.E.F.; Gomes-Cardoso, L.; Leon, L.L. Studies on the effectiveness of diarylheptanoids derivatives against Leishmania amazonensis. Mem. Inst. Oswaldo Cruz, 1999, 94(6), 791-794.
[http://dx.doi.org/10.1590/S0074-02761999000600015] [PMID: 10585657]
[53]
Martins, M.M.; de Aquino, F.J.T.; de Oliveira, A.; do Nascimento, E.A.; Chang, R.; Borges, M.S.; de Melo, G.B.; da Silva, C.V.; Machado, F.C.; de Morais, S.A.L. Chemical composition, antimicrobial and antiprotozoal activity of essential oils from Vernonia brasiliana (Less) Druce (Asteraceae). J. Essential Oil-Bear. Plants, 2015, 18, 561-569.
[54]
Bermejo, B.P.; Abad, M.J.; Díaz, A.M.; Villaescusa, L.; González, M.A.; Silván, A.M. Sesquiterpenes from Jasonia glutinosa: In vitro anti-inflammatory activity. Biol. Pharm. Bull., 2002, 25, 1-4.
[55]
Puri, A.; Saxena, R.; Saxena, R.P.; Saxena, K.C.; Srivastava, V.; Tandon, J.S. Immunostimulant activity of Nyctanthes arbor-tristis L. J. Ethnopharmacol., 1994, 42(1), 31-37.
[http://dx.doi.org/10.1016/0378-8741(94)90020-5] [PMID: 8046941]

Rights & Permissions Print Cite
Article Metrics
53
1
World Chagas Disease
© 2024 Bentham Science Publishers | Privacy Policy