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Acta Parasitologica

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Volume 60, Issue 1


Effect of structurally related flavonoids from Zuccagnia punctata Cav. on Caenorhabditis elegans

Romina E. D’Almeida / María R. Alberto
  • Corresponding author
  • INQUINOA (CONICET) San Lorenzo 1469. 4000. San Miguel de Tucumán, Argentina
  • Facultad de Ciencias Naturales e Instituto Miguel Lillo Universidad Nacional de Tucumán, San Lorenzo 1469. 4000. San Miguel de Tucumán, Argentina
  • Cátedra de Fitoquímica, Facultad de Bioquímica, Química y Farmacia Ayacucho 471. 4000. San Miguel de Tucumán, Argentina
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  • Other articles by this author:
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/ Phillip Morgan
  • Department of Anesthesiology, University of Washington and Children’s Research Institute, Seattle, WA 9810, USA
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/ Margaret Sedensky
  • Department of Anesthesiology, University of Washington and Children’s Research Institute, Seattle, WA 9810, USA
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/ María I. Isla
  • INQUINOA (CONICET) San Lorenzo 1469. 4000. San Miguel de Tucumán, Argentina
  • Facultad de Ciencias Naturales e Instituto Miguel Lillo Universidad Nacional de Tucumán, San Lorenzo 1469. 4000. San Miguel de Tucumán, Argentina
  • Cátedra de Fitoquímica, Facultad de Bioquímica, Química y Farmacia Ayacucho 471. 4000. San Miguel de Tucumán, Argentina;
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2014-12-30 | DOI: https://doi.org/10.1515/ap-2015-0023


Zuccagnia punctata Cav. (Fabaceae), commonly called jarilla macho or pus-pus, is being used in traditional medicine as an antiseptic, anti-inflammatory and to relieve muscle and bone pain. The aim of this work was to study the anthelmintic effects of three structurally related flavonoids present in aerial parts of Z. punctata Cav. The biological activity of the flavonoids 7-hydroxyflavanone (HF), 3,7-dihydroxyflavone (DHF) and 2´,4´-dihydroxychalcone (DHC) was examined in the free-living nematode Caenorhabditis elegans. Our results showed that among the assayed flavonoids, only DHC showed an anthelmintic effect and alteration of egg hatching and larval development processes in C. elegans. DHC was able to kill 50% of adult nematodes at a concentration of 17 μg/mL. The effect on larval development was observed after 48 h in the presence of 25 and 50 μg/mL DHC, where 33.4 and 73.4% of nematodes remained in the L3 stage or younger. New therapeutic drugs with good efficacy against drug-resistant nematodes are urgently needed. Therefore, DHC, a natural compound present in Z. punctata, is proposed as a potential anthelmintic drug.

Keywords: 7-hydroxyflavanone; 3,7-dihydroxyflavone; 2´,4´-dihydroxychalcone; anthelmintic effect; Caenorhabditis elegans


  • Aceves J., Erlij D., Martinez-Maranon R. 1970. The mechanism of the paralyzing action of tetramisole on Ascaris somatic muscle. British Journal Pharmacology, 38, 602-607. DOI: 10.1111/j.1476-5381.1970.tb10601.x CrossrefGoogle Scholar

  • Aguero M.B., Gonzalez M., Lima B., Svetaz L., Sanchez M., Zacchino S., Feresin G., Schmeda-Hirschmann G., Palermo J., Wunderlin D., Tapia A. 2010. Argentinean propolis from Zuccagnia punctata Cav. (Caesalpinieae) Exudates: Phytochemical characterization and antifungal activity. Journal of Agricultural and Food Chemistry, 58, 194-201. DOI: 10.1021/jf902991t PubMedCrossrefGoogle Scholar

  • Artal-Sanz M., de Jong L., Tavernarakis N. 2006. Caenorhabditis elegans: A versatile platform for drug discovery. Biotechnology Journal, 1, 1405-1418. DOI: 10.1002/biot.200600176CrossrefGoogle Scholar

  • Attar S., O’Brien Z., Alhaddad H., Golden M.L., Calderon-Urrea A. 2011. Ferrocenyl chalcones versus organic chalcones: A comparative study of their nematocidal activity. Bioorganic and Medicinal Chemistry, 19, 2055-2073. DOI: 10.1016/ j.bmc.2011.01.048CrossrefGoogle Scholar

  • Avery L., Shtonda B.B. 2003. Food transport in the Caenorhabditis elegans pharynx. The Journal of Experimental Biology, 206, 2441-2457. DOI: 10.1242/jeb.00433CrossrefGoogle Scholar

  • Bull K., Cook A., Hopper N.A., Harder A., Holden-Dye L., Walker R.J. 2007. Effects of the novel anthelmintic emodepside on the locomotion, egg-laying behaviour and development of Caenorhabditis elegans. International Journal for Parasitology, 37, 627-636. DOI : 10.1016/j.ijpara.2006.10.013CrossrefGoogle Scholar

  • Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics, 77, 71-94. DOI: 10.1895/wormbook.1.101.1CrossrefPubMedGoogle Scholar

  • Chieli E., Romiti N., Zampini I.C., Garrido G., Isla M.I. 2012. Effects of Zuccagnia punctata extracts and their flavonoids on the function and expression of ABCB1/P-glycoprotein multidrug transporter. Journal of Ethnopharmacology 144, 797-801. DOI: 10.1016/j.jep.2012.10.012CrossrefGoogle Scholar

  • Collins J.J., Evason K., Kornfeld K. 2006. Pharmacology of delayed aging and extended lifespan of Caenorhabditis elegans. Experimental Gerontology, 41, 1032-1039. DOI:10.1016/ j.exger.2006.06.038PubMedCrossrefGoogle Scholar

  • Cox G.N., Kusch M., Edgar R.S. 1981. Cuticle of Caenorhabditis elegans: its isolation and partial characterization. The Journal of Cell Biology, 90, 7-17. DOI: 10.1083/jcb.90.1CrossrefGoogle Scholar

  • Daglia M. 2012. Polyphenols as antimicrobial agents. Current Opinion in Biotechnology, 23, 174-181. DOI: 10.1016/j.copbio. 2011.08.007 PubMedCrossrefGoogle Scholar

  • de la Rocha N., Maria A.O., Gianello J.C., Pelzer L. 2003. Cytoprotective effects of chalcones from Zuccagnia punctata and melatonin on gastroduodenal tract in rats. Pharmacology Research, 48, 97-99. DOI: 10.1016/S1043-6618(03)00063-X CrossrefGoogle Scholar

  • de Mello T.F.P., Bitencourt H.R., Pedroso R.B., Aristides S.M.A., Lonardoni M.V.C., Silveira T.G.V. 2014. Leishmanicidal activity of synthetic chalcones in Leishmania (Viannia) braziliensis. Experimental Parasitology, 136, 27-34. DOI: 10.1016/j.exppara.2013.11.003CrossrefGoogle Scholar

  • Franks C.J., Pemberton D., Vinogradova I., Cook A., Walker J.R., Holden L. 2002. Ionic basis of the resting membrane potential and action potential in the pharyngeal muscle of Caenorhabditis elegans. Journal of Neurophysiology, 87, 954-961. DOI: 10.1152/jn.00233.2001CrossrefGoogle Scholar

  • Gandhi S., Santelli J., Mitchell D.H., Stiles J., Sanadi D. 1980. A simple method for maintaining large, aging populations of Caenorhabditis elegans. Mechanism of Ageing and Development 12, 137-150. DOI:10.1016/0047-6374(80)90090-1CrossrefGoogle Scholar

  • Geary T.G., Thompson D.P. 2001. Caenorhabditis elegans: how good a model for veterinary parasites? Veterinary Parasitology 101, 371-386. DOI: 10.1016/S0304-4017(01)00562-3CrossrefGoogle Scholar

  • Gonzalez J.A., Estevez-Braun A.J. 1998. Effect of (E)-Chalcone on Potato-Cyst Nematodes (Globodera pallida and G. rostochiensis). Journal of Agricultural and Food Chemistry, 46, 1163-1165. DOI: 10.1021/jf9706686CrossrefGoogle Scholar

  • Grunz G., Haas K., Soukup S., Klingenspor M., Kulling S.E., Daniel H., Spanier B. 2012. Structural features and bioavailability of four flavonoids and their implications for lifespan-extending and antioxidant actions in Caenorhabditis elegans. Mechanism of Ageing and Development, 133, 1-10. DOI: 10.1016/j.mad.2011.11.005CrossrefGoogle Scholar

  • Holden-Dye L., Walker R.J. 2007. Anthelmintic drugs, WormBook, ed. The C. elegans Research Community, WormBook. DOI: 10.1895/wormbook.1.143.1CrossrefGoogle Scholar

  • Horton D.A., Bourne G.T., Smythe M.L. 2003. The combinatorial synthesis of bicyclic privileged structures or privileged substructures. Chemical Reviews, 103, 893-930. DOI: 10.1021/cr020033s CrossrefGoogle Scholar

  • Iglesias J., Medina I., Pazos M. 2014. Galloylation and polymerization: role of structure to antioxidant activity of polyphenols in lipid systems. In: (Eds. Watson R.R., Preedy V.R., Zibadi S.). Polyphenols in Human Health and Disease. Elsevier, 323-338. DOI: 10.1016/B978-0-12-398456-2.00025-6CrossrefGoogle Scholar

  • Jospin M., Jacquemond V., Mariol M.C., Segalat L., Allard B. 2002. The L-type voltage-dependent Ca2+ channel EGL-19 controls body wall muscle function in Caenorhabditis elegans. The Journal of Cell Biology, 159, 337-348. DOI: 10.1083/ jcb.200203055Google Scholar

  • Kampkotter A., Gombitang Nkwonkam C., Zurawski R.F., Timpel C., Chovolou Y., Watjen W., Kahl R. 2007. Effects of the flavonoids kaempferol and fisetin on thermotolerance, oxidative stress and FoxO transcription factor DAF-16 in the model organism Caenorhabditis elegans. Archives of Toxicology, 81, 849-858. DOI: 10.1007/s00204-007-0215-4CrossrefGoogle Scholar

  • Katiki L.M., Ferreira J.F.S., Zajac A.M., Masler C., Lindsay D.S., Chagas A.C.S., Amarante A.F.T. 2011. Caenorhabditis elegans as a model to screen plant extracts and compounds as natural anthelmintics for veterinary use. Veterinary Parasitology, 182, 264-268. DOI: 10.1016/j.vetpar.2011.05.020CrossrefGoogle Scholar

  • Kelly E.H., Anthony R.T., Dennis J.B. 2002. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. Journal of Nutritional Biochemistry, 13, 572-584. DOI: 10. 1016/S0955-2863(02)00208-5CrossrefGoogle Scholar

  • Klekota J., Roth F.P. 2008. Chemical substructures that enrich for biological activity. Bioinformatics, 24, 2518-2525. DOI: 10. 1093/bioinformatics/btn479CrossrefPubMedGoogle Scholar

  • Kwok T.C.Y., Ricker N., Fraser R., Burns A., Stanley E.F., McCourt P., Cutler S.R., Roy P.J. 2006. A small-molecule screen in Caenorhabditis elegans yields a new calcium channel antagonist. Nature, 441, 91-95. DOI: 10.1038/nature04657CrossrefGoogle Scholar

  • Laliberte R., Campbell D., Brauderlein F. 1967. Anthelmintic activities of chalcones and related compounds. Canadian Journal of Pharmaceutical Sciences, 2, 37-43Google Scholar

  • Lamoral-Theys D., Pottier L., Dufrasne F., Neve J., Dubois J., Kornienko A., Kiss R., Ingrassia L. 2010. Natural polyphenols that display anticancer properties through inhibition of kinase activity. Current Medicinal Chemistry, 17, 812-25. DOI: 10.2174/092986710790712183CrossrefGoogle Scholar

  • Lee Y.U., Kawasaki I., Lim Y., Oh W.S., Paik Y.K., Shim Y.H. 2008. Inhibition of developmental processes by flavone in Caenorhabditis elegans and its application to the pinewood nematode, Bursaphelenchus xylophilus. Molecular Cells, 26, 171-174. DOI: 10.1007/s11418-007-0220-1CrossrefPubMedGoogle Scholar

  • Lindblom T.H., Dodd A.K. 2006. Xenobiotic detoxification in the nematode Caenorhabditis elegans. Journal of Experimental Zoology Part A: Comparative Experimental Biology, 305, 720-730. DOI: 10.1002/jez.a.324CrossrefGoogle Scholar

  • Liu M.,Wilairat P., Croft S.L., Tan A.L.C., Go M.L. 2003. Structure- activity relationships of antileishmanial and antimalarial chalcones. Bioorganic and Medicinal Chemistry, 11, 2729-2738. DOI: 10.1016/j.ejmech.2009.09.012CrossrefGoogle Scholar

  • Loa J., Chow P., Zhang K. 2009. Studies of structure-activity relationship on plant polyphenol-induced suppression of human liver cancer cells. Cancer Chemotherapy and Pharmacology, 63, 1007-1016. DOI: 10.1007/s00280-008-0802-y CrossrefGoogle Scholar

  • Menaa F., Menaa A., Treton J. 2014. Polyphenols against Skin Aging. In: (Eds. Watson R.R., Preedy V.R. and Zibadi S.). Polyphenols in Human Health and Disease. Elsevier, 819-830. DOI: 10.1016/B978-0-12-398456-2.00063-3CrossrefGoogle Scholar

  • Moran Vieyra F., Zampini I., Ordonez R., Isla M.I., Boggetti H., De Rosso V., Mercadante A., Alvarez R., Borsarelli C. 2009. Singlet oxygen quenching and radical scavenging capacities of structurally related flavonoids present in Zuccagnia punctata Cav. Free Radical Research, 43, 553-564. DOI: 10.1080/ 10715760902912264CrossrefGoogle Scholar

  • Morris M., Zhang S. 2006. Flavonoid-drug interactions. Effects of flavonoids on ABC transporters. Life Science, 78, 2116-2130. DOI: 10.1016/j.lfs.2005.12.003CrossrefGoogle Scholar

  • Ndjonkaa D., Abladama E.D., Djafsiaa B., Ajonina-Ekotia I., Achukwia M.D., Liebaua E. 2013. Anthelmintic activity of phenolic acids from the axlewood tree Anogeissus leiocarpus on the filarial nematode Onchocerca ochengi and drug-resistant strains of the free-living nematode Caenorhabditis elegans. Journal of Helminthology, 1-8. DOI: 10.1017/S0022149X 1300045X CrossrefGoogle Scholar

  • Nijveldt R.J., van Nood E., van Hoorn D.E., Boelens P.G., van Norren K., van Leeuwen P.A. 2001. Flavonoids: a review of probable mechanisms of action and potential applications. The American Journal of Clinical Nutrition, 74, 418-25Google Scholar

  • Nowakowska Z. 2007. A review of anti-infective and anti-inflammatory chalcones. European Journal of Medicinal Chemistry, 42, 125-137. DOI: 10.1016/j.ejmech.2006.09.019PubMedCrossrefGoogle Scholar

  • Pederiva R., Giordano O. 1984. 3,7-Dihydroxy-8-methoxyflavone from Zuccagnia punctata. Phytochemistry, 23, 1340-1341. DOI: 10.1016/S0031-9422(00)80459-8CrossrefGoogle Scholar

  • Ratera E.L., Ratera M.O. (Ed.) 1980. Plantas de la Flora Argentina Empleadas en Medicina Popular. Hemisferio Sur, Press. Buenos Aires, Argentina, 98-189 pp.Google Scholar

  • Rice-Evans C.A., Miller N.J., Paganga G. 1996. Structure/antioxidant activity relationshis of flavonoids and phenolic compounds. Free Radical Biology and Medine, 20, 933-956. DOI:10.1016/0891-5849(95)02227-9CrossrefGoogle Scholar

  • Ross J.A., Kasum C.M. 2002. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annual Review of Nutrition, 22, 19-34. DOI: 10.1146/annurev.nutr.22.111401.144957CrossrefPubMedGoogle Scholar

  • Shenvi S., Kumar K., Hatti K.S., Rijesh K., Diwakar L., Reddy G. 2013. Synthesis, anticancer and antioxidant activities of 2,4,5- trimethoxy chalcones and analogues from asaronaldehyde: Structure-activity relationship. European Journal of Medicinal Chemistry, 62, 435-442. DOI: 10.1016/j.ejmech.2013. 01.018CrossrefGoogle Scholar

  • Skantar A.M., Agama K., Meyer S.L.F., Carta L.K., Vinyard B.T. 2005. Effects of geldanamycin on hatching and juvenile motility in Caenorhabditis elegans and Heterodera glycines. Journal of Chemical Ecology, 31, 2481-2491. DOI: 10.1007/ s10886-005-7114-z CrossrefGoogle Scholar

  • Strayer A., Wu Z., Christen Y., Link C.D., Luo Y. 2003. Expression of the small heat-shock protein Hsp-16-2 in Caenorhabditis elegans is suppressed by Ginkgo biloba extract EGb 761.Google Scholar

  • The FASEB Journal, 17, 2305-2307. DOI: 10.1096/fj.03-0376fje Svetaz L., Tapia A., Lopez S., Furlan R., Petenatti E., Pioli R., Schmeda-Hirschmann G., Zacchino S. 2004. Antifungal chalcones and new caffeic acid esters from Zuccagnia punctata acting against soybean infecting fungi. Journal of Agricultural and Food Chemistry, 52, 3297-3300. DOI: 10.1021/ jf035213x CrossrefGoogle Scholar

  • Thompson D.P., Klein R.D., Geary T.G. 1996. Prospects for rational approaches to anthelmintic discovery. Parasitology, 113 (Suppl), S217-S238. DOI: 10.1017/S0031182000077994CrossrefGoogle Scholar

  • Toursarkissian M. (Ed.) 1980. Plantas Medicinales de la Argentina. Sus nombres botanicos, vulgares, usos y distribucion geografica. Hemisferio Sur SA, Buenos Aires, Argentina Williams C.A., Grayer R.J. 2004. Anthocyanins and other flavonoids. Natural Product Reports, 21, 539-573. DOI: 10.1039/b3 11404j CrossrefGoogle Scholar

  • Wilson M.A., Shukitt-Hale B., Kalt W., Ingram D.K., Joseph J.A., Wolkow C.A. 2006. Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans. Aging Cell 5, 59-68. DOI: 10.1111/j.1474-9726.2006.00192.x CrossrefPubMedGoogle Scholar

  • Wink M., Abbas S. 2013. Epigallocatechin Gallate (EGCG) from green tea (Camellia sinensis) and other natural products mediate stress resistance and slow down aging processes in Caenorhabditis elegans. In: (Ed. Preedy, V.R.). Tea in Health and Disease Prevention. Elsevier, 1105-1115. DOI: 10.1016/ B978-0-12-384937-3.00093-8CrossrefGoogle Scholar

  • Young-Ah Y., Hojung K., Yoongho L., Yhong-Hee S. 2006. Relationships between the larval growth inhibition of Caenorhabditis elegans by apigenin derivatives and their structures. Archives of Pharmacal Research 29, 582-586. DOI: 10.1007/ BF02969269CrossrefGoogle Scholar

  • Zampini I.C., Vattuone M., Isla M.I. 2005. Antibacterial activity against antibiotic-resistant Gram negative human pathogenic bacteria of hydroxychalcone isolated from Zuccagnia punctata Cav. Journal of Ethnopharmacology, 102, 450-456. DOI: 10.1016/j.jep.2005.07.005 CrossrefGoogle Scholar

  • Zampini I.C., Villarini M., Moretti M., Dominici L., Isla M.I. 2008. Evaluation of genotoxic and antigenotoxic effects of hydroalcoholic extracts of Zuccagnia punctata. Cav. Journal of Ethnopharmacology 115, 330-335. DOI: 10.1016/j.jep. 2007.10.007CrossrefGoogle Scholar

  • Zampini I.C., Villena J., Salva S., Herrera M., Isla M.I., Alvarez S. 2012. Potentiality of standardized extract and isolated flavonoids from Zuccagnia punctata for the treatment of respiratory infections by Streptococcus pneumoniae: In vitro and in vivo studies. Journal of Ethnopharmacology 140, 287-292. DOI: 10.1016/j.jep.2012.01.019 CrossrefGoogle Scholar

About the article

Received: 2014-04-30

Revised: 2014-10-17

Accepted: 2014-10-22

Published Online: 2014-12-30

Published in Print: 2014-03-01

Citation Information: Acta Parasitologica, Volume 60, Issue 1, Pages 164–172, ISSN (Online) 1896-1851, DOI: https://doi.org/10.1515/ap-2015-0023.

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