Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter December 30, 2014

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

  • Romina E. D’Almeida , María R. Alberto EMAIL logo , Phillip Morgan , Margaret Sedensky and María I. Isla
From the journal Acta Parasitologica

Abstract

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.

References

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 Search in Google 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 Search in Google 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.200600176Search in Google 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.2011.01.048Search in Google 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.00433Search in Google 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.2006.10.013Search in Google Scholar

Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics, 77, 71-94. DOI: 10.1895/wormbook.1.101.1Search in Google 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.2012.10.012Search in Google 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.2006.06.038Search in Google 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.90.1Search in Google Scholar

Daglia M. 2012. Polyphenols as antimicrobial agents. Current Opinion in Biotechnology, 23, 174-181. DOI: 10.1016/j.copbio. 2011.08.007 Search in Google 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 Search in Google 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.2013.11.003Search in Google 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.00233.2001Search in Google 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)90090-1Search in Google 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)00562-3Search in Google 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/jf9706686Search in Google 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.2011.11.005Search in Google Scholar

Holden-Dye L., Walker R.J. 2007. Anthelmintic drugs, WormBook, ed. The C. elegans Research Community, WormBook. DOI: 10.1895/wormbook.1.143.1Search in Google 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 Search in Google 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/B978-0-12-398456-2.00025-6Search in Google 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.200203055Search in Google 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/s00204-007-0215-4Search in Google 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.2011.05.020Search in Google 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)00208-5Search in Google Scholar

Klekota J., Roth F.P. 2008. Chemical substructures that enrich for biological activity. Bioinformatics, 24, 2518-2525. DOI: 10. 1093/bioinformatics/btn479Search in Google 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/nature04657Search in Google Scholar

Laliberte R., Campbell D., Brauderlein F. 1967. Anthelmintic activities of chalcones and related compounds. Canadian Journal of Pharmaceutical Sciences, 2, 37-43Search in Google 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: 10.2174/092986710790712183Search in Google 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/s11418-007-0220-1Search in Google 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.324Search in Google 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.2009.09.012Search in Google 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 Search in Google 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/B978-0-12-398456-2.00063-3Search in Google 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/ 10715760902912264Search in Google 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.2005.12.003Search in Google 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 Search in Google 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, 418-25Search in Google 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.2006.09.019Search in Google Scholar

Pederiva R., Giordano O. 1984. 3,7-Dihydroxy-8-methoxyflavone from Zuccagnia punctata. Phytochemistry, 23, 1340-1341. DOI: 10.1016/S0031-9422(00)80459-8Search in Google 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.Search in 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)02227-9Search in Google 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.22.111401.144957Search in Google 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. 01.018Search in Google 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 Search in Google 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.Search in 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 Search in Google 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/S0031182000077994Search in Google 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 Search in Google 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 Search in Google 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/ B978-0-12-384937-3.00093-8Search in Google 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/ BF02969269Search in Google 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 Search in Google 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. 2007.10.007Search in Google 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 Search in Google Scholar

Received: 2014-4-30
Revised: 2014-10-17
Accepted: 2014-10-22
Published Online: 2014-12-30
Published in Print: 2014-3-1

© 2015

Downloaded on 28.3.2024 from https://www.degruyter.com/document/doi/10.1515/ap-2015-0023/html
Scroll to top button