Anticancer potential of selected Fallopia Adans species

Olaru,Octavian  Tudorel; Venables,Luanne; van de Venter,Maryna; Nitulescu,George  Mihai; Margina,Denisa; Spandidos,Demetrios  A.; Tsatsakis,Aristidis  M.

doi:10.3892/ol.2015.3453

Anticancer potential of selected Fallopia Adans species

Authors:
- Octavian Tudorel Olaru
- Luanne Venables
- Maryna van de Venter
- George Mihai Nitulescu
- Denisa Margina
- Demetrios A. Spandidos
- Aristidis M. Tsatsakis
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Affiliations: Faculty of Pharmacy, ‘Carol Davila’ University of Medicine and Pharmacy, Bucharest 020956, Romania, Department of Biochemistry and Microbiology, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa, Department of Clinical Virology, School of Medicine, University of Crete, Heraklion 71003, Greece, Department of Forensic Sciences and Toxicology, Faculty of Medicine, University of Crete, Heraklion 71003, Greece
Published online on: July 2, 2015 https://doi.org/10.3892/ol.2015.3453
Pages: 1323-1332
Copyright: © Olaru et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The aim of the present study was to determine the anticancer potential of three species belonging to the Fallopia genus (Polygonaceae): Fallopia convolvulus (F. convolvulus, Fallopia dumetorum (F. dumetorum) and Fallopia aubertii (F. aubertii). For this purpose, crude extracts were obtained and characterized for their phenolic and flavonoid total content and examined for their anticancer activity on three tumor cell lines: breast cancer (MCF7), colon carcinoma (Caco-2) and cervical cancer (HeLa) cells. The cytotoxic potential of the three species was assessed by MTT assay, cell cycle analysis and by the evaluation of mitochondrial membrane potential (MMP). The acute toxicity of the extracts was evaluated using one in vitro cell model (Vero cells, an African Green monkey kidney cell line) and two invertebrate in vivo models (Daphnia magna and Artemia salina). The highest total phenolic and flavonoid content was found in the F. aubertii flower extracts. The cytotoxic effects of the extracts from F. aubertii and F. convolvulus on all three cell lines were examined at concentrations ranging from 3 to 300 µg/ml. G2/M cell cycle arrest was induced by all the extracts, and a significant increase in the subG1 cell population was observed. The hydroethanolic extract from the flowers of F. aubertii induced cell apoptosis more rapidly than the other extracts. The MMP indicates the involvement of the mitochondria in the induction of apoptosis. A positive correlation between the total phenolic content of the extracts and the IC50 values against the HeLa cells was also noted. None of the extracts exhibited significantly toxic effects. Considering the antitumor potential of F. aubertii and F. convolvulus, these two species may represent a good source of plant extracts with anticancer properties.

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1	Ridge CA, McErlean AM and Ginsberg MS: Epidemiology of lung cancer. Semin Intervent Radiol. 30:93–98. 2013. View Article : Google Scholar : PubMed/NCBI
2	Baili P, Hoekstra-Weebers J, Van Hoof E, Bartsch HH, Travado L, Garami M, Di Salvo F, Micheli A and Veerus PEUROCHIP-3 Working group on Cancer Rehabilitation: Cancer rehabilitation indicators for Europe. Eur J Cancer. 49:1356–1364. 2013. View Article : Google Scholar : PubMed/NCBI
3	Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D and Bray F: Cancer incidence and mortality patterns in Europe: Estimates for 40 countries in 2012. Eur J Cancer. 49:1374–1403. 2013. View Article : Google Scholar : PubMed/NCBI
4	Orlikova B and Diederich M: Power from the garden: Plant compounds as inhibitors of the hallmarks of cancer. Curr Med Chem. 19:2061–2087. 2012. View Article : Google Scholar : PubMed/NCBI
5	Gordaliza M: Natural products as leads to anticancer drugs. Clin Transl Oncol. 9:767–776. 2007. View Article : Google Scholar : PubMed/NCBI
6	Karikas GA: Anticancer and chemopreventing natural products: Some biochemical and therapeutic aspects. J BUON. 15:627–638. 2010.PubMed/NCBI
7	Tan G, Gyllenhaal C and Soejarto DD: Biodiversity as a source of anticancer drugs. Curr Drug Targets. 7:265–277. 2006. View Article : Google Scholar : PubMed/NCBI
8	Singh M, Kaur M and Silakari O: Flavones: An important scaffold for medicinal chemistry. Eur J Med Chem. 84:206–239. 2014. View Article : Google Scholar : PubMed/NCBI
9	Wu B, Zhang Q, Shen W and Zhu J: Anti-proliferative and chemosensitizing effects of luteolin on human gastric cancer AGS cell line. Mol Cell Biochem. 313:125–132. 2008. View Article : Google Scholar : PubMed/NCBI
10	Sak K: Cytotoxicity of dietary flavonoids on different human cancer types. Pharmacogn Rev. 8:122–146. 2014. View Article : Google Scholar : PubMed/NCBI
11	Patil JR, Chidambara Murthy KN, Jayaprakasha GK, Chetti MB and Patil BS: Bioactive compounds from Mexican lime (Citrus aurantifolia) juice induce apoptosis in human pancreatic cells. J Agric Food Chem. 57:10933–10942. 2009. View Article : Google Scholar : PubMed/NCBI
12	Russo P, Del Bufalo A and Cesario A: Flavonoids acting on DNA topoisomerases: Recent advances and future perspectives in cancer therapy. Curr Med Chem. 19:5287–5293. 2012. View Article : Google Scholar : PubMed/NCBI
13	Tu SH, Ho CT, Liu MF, Huang CS, Chang HW, Chang CH, Wu CH and Ho YS: Luteolin sensitises drug-resistant human breast cancer cells to tamoxifen via the inhibition of cyclin E2 expression. Food Chem. 141:1553–1561. 2013. View Article : Google Scholar : PubMed/NCBI
14	Kuntz S, Wenzel U and Daniel H: Comparative analysis of the effects of flavonoids on proliferation, cytotoxicity, and apoptosis in human colon cancer cell lines. Eur J Nutr. 38:133–142. 1999. View Article : Google Scholar : PubMed/NCBI
15	Mojzis J, Varinska L, Mojzisova G, Kostova I and Mirossay L: Antiangiogenic effects of flavonoids and chalcones. Pharmacol Res. 57:259–265. 2008. View Article : Google Scholar : PubMed/NCBI
16	Hou D-X and Kumamoto T: Flavonoids as protein kinase inhibitors for cancer chemoprevention: Direct binding and molecular modeling. Antioxid Redox Signal. 13:691–719. 2010. View Article : Google Scholar : PubMed/NCBI
17	Syed DN, Adhami VM, Khan MI and Mukhtar H: Inhibition of Akt/mTOR signaling by the dietary flavonoid fisetin. Anticancer Agents Med Chem. 13:995–1001. 2013. View Article : Google Scholar : PubMed/NCBI
18	Kong D, Zhang Y, Yamori T, Duan H and Jin M: Inhibitory activity of flavonoids against class I phosphatidylinositol 3-kinase isoforms. Molecules. 16:5159–5167. 2011. View Article : Google Scholar : PubMed/NCBI
19	Dai J and Mumper RJ: Plant phenolics: Extraction, analysis and their antioxidant and anticancer properties. Molecules. 15:7313–7352. 2010. View Article : Google Scholar : PubMed/NCBI
20	Dolečková I, Rárová L, Grúz J, Vondrusová M, Strnad M and Kryštof V: Antiproliferative and antiangiogenic effects of flavone eupatorin, an active constituent of chloroform extract of Orthosiphon stamineus leaves. Fitoterapia. 83:1000–1007. 2012. View Article : Google Scholar : PubMed/NCBI
21	Kitdamrongtham W, Manosroi A, Akazawa H, Gidado A, Stienrut P, Manosroi W, Lohcharoenkal W, Akihisa T and Manosroi J: Potent anti-cervical cancer activity: Synergistic effects of Thai medicinal plants in recipe N040 selected from the MANOSROI III database. J Ethnopharmacol. 149:288–296. 2013. View Article : Google Scholar : PubMed/NCBI
22	Holub J: Fallopia Adans. 1763 instead of Bilderdykia Dum. 1827. Folia Geobot Phytotaxon. 6:171–177. 1971.
23	Haraldson K: Anatomy and taxonomy in Polygonaceae subfam. Polygonoideae Meisn. emend. Jaretzky. Symb. Bot Upsal. 22:1–95. 1978.
24	Decraene LP and Akeroyd JR: Generic limits in Polygonum L. and related genera (Polygonaceae) on the basis of floral characters. J Linn Soc. 98:321–371. 1988. View Article : Google Scholar
25	Nielsen H and Steinar H: Fallopia Adans. Flora Nordica. Vol. 1: Lycopodiaceae to PolygonaceaeJonsell B: Bergius Foundation; Stockholm: pp. 273–278. 2000
26	Song J, Yao H, Li Y, Li X, Lin Y, Liu C, Han J, Xie C and Chen S: Authentication of the family Polygonaceae in Chinese pharmacopoeia by DNA barcoding technique. J Ethnopharmacol. 124:434–439. 2009. View Article : Google Scholar : PubMed/NCBI
27	Tiébré MS, Bizoux JP, Hardy OJ, Bailey JP and Mahy G: Hybridization and morphogenetic variation in the invasive alien Fallopia (Polygonaceae) complex in Belgium. Am J Bot. 94:1900–1910. 2007. View Article : Google Scholar : PubMed/NCBI
28	Kim M, Hee Park J and Park CC: Flavonoid chemistry of Fallopia section Fallopia (Polygonaceae). Biochem Syst Ecol. 28:433–441. 2000. View Article : Google Scholar : PubMed/NCBI
29	Kim MH, Park JH, Won H and Park CW: Flavonoid chemistry and chromosome numbers of Fallopia section Pleuropterus (Polygonaceae). Can J Bot. 78:1136–1143. 2000. View Article : Google Scholar
30	Smolarz HD: Comparative study on the free flavonoid aglycones in herbs of different species of Polygonum L. Acta Pol Pharm. 59:145–148. 2002.PubMed/NCBI
31	Zhang CF, Chen J, Zhao LQ, Zhang D, Zhang M and Wang ZT: Three new flavonoids from the active extract of Fallopia convolvulus. J Asian Nat Prod Res. 13:136–142. 2011. View Article : Google Scholar : PubMed/NCBI
32	Olaru OT, Anghel AI, Istudor V, Ancuceanu RV and Dinu M: Contributions to the pharmacognostical and phytobiological study of Fallopia aubertii (L. Henry) Holub. (Polygonaceae). Farmacia. 61:991–999. 2013.
33	Zhao YM, Qi HY and Shi YP: Several chromones from the stems of Polygonum aubertii Henry. J Asian Nat Prod Res. 12:623–628. 2010. View Article : Google Scholar : PubMed/NCBI
34	González M, Guzmán B, Rudyk R, Romano E and Molina MA: Spectrophotometric determination of phenolic compounds in propolis. Lat Am J Pharm. 22:243–248. 2003.
35	Chang CC, Yang MH, Wen HM and Chern JC: Estimation of total flavonoid content in propolis by two complementary colometric methods. J Food Drug Anal. 10:178–182. 2002.
36	Bazylko A, Parzonko A, Jez W, Osińska E and Kiss AK: Inhibition of ROS production, photoprotection, and total phenolic, flavonoids and ascorbic acid content of fresh herb juice and extracts from the leaves and flowers of Tropaeolum majus. Ind Crops Prod. 55:19–24. 2014. View Article : Google Scholar
37	Meyer BN, Ferrigni NR, Putnam JE, Jacobsen LB, Nichols DE and McLaughlin JL: Brine shrimp: A convenient general bioassay for active plant constituents. Planta Med. 45:31–34. 1982. View Article : Google Scholar
38	Fan W, Cui M, Liu H, Wang C, Shi Z, Tan C and Yang X: Nano-TiO₂ enhances the toxicity of copper in natural water to Daphnia magna. Environ Pollut. 159:729–734. 2011. View Article : Google Scholar : PubMed/NCBI
39	Nitulescu GM, Draghici C and Olaru OT: New potential antitumor pyrazole derivatives: Synthesis and cytotoxic evaluation. Int J Mol Sci. 14:21805–21818. 2013. View Article : Google Scholar : PubMed/NCBI
40	Gong Y, Liu X, He WH, Xu HG, Yuan F and Gao YX: Investigation into the antioxidant activity and chemical composition of alcoholic extracts from defatted marigold (Tagetes erecta L.) residue. Fitoterapia. 83:481–489. 2012. View Article : Google Scholar : PubMed/NCBI
41	Ghitescu RE, Volf I, Carausu C, Bühlmann AM, Gilca IA and Popa VI: Optimization of ultrasound-assisted extraction of polyphenols from spruce wood bark. Ultrason Sonochem. 22:535–541. 2015. View Article : Google Scholar : PubMed/NCBI
42	Olaru OT, Ancuceanu RV, Anghel AI and Dinu M: Șeremet OC and Istudor V: Botanical investigation of Fallopia dumetorum (L.) Holub (Polygonaceae) and qualitative and quantitative assessment of its polyphenolic compounds. Acta Med Marisiensis. 60:67–71. 2014.
43	Olaru OT, Anghel AI, Istudor V and Olaru II: The qualitative and quantitative determination of the phenolic compounds in Polygonum convolvulus L. species, Polygonaceae family. Acta Med Marisiensis. 59:162–164. 2013.
44	Sultana B, Anwar F and Ashraf M: Effect of extraction solvent/technique on the antioxidant activity of selected medicinal plant extracts. Molecules. 14:2167–2180. 2009. View Article : Google Scholar : PubMed/NCBI
45	Sahpazidou D, Geromichalos GD, Stagos D, Apostolou A, Haroutounian SA, Tsatsakis AM, Tzanakakis GN, Hayes AW and Kouretas D: Anticarcinogenic activity of polyphenolic extracts from grape stems against breast, colon, renal and thyroid cancer cells. Toxicol Lett. 230:218–224. 2014. View Article : Google Scholar : PubMed/NCBI
46	Sun T, Chen QY, Wu LJ, Yao XM and Sun XJ: Antitumor and antimetastatic activities of grape skin polyphenols in a murine model of breast cancer. Food Chem Toxicol. 50:3462–3467. 2012. View Article : Google Scholar : PubMed/NCBI
47	Busino L, Chiesa M, Draetta GF and Donzelli M: Cdc25A phosphatase: Combinatorial phosphorylation, ubiquitylation and proteolysis. Oncogene. 23:2050–2056. 2004. View Article : Google Scholar : PubMed/NCBI
48	Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD Jr and Chen LB: Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc Natl Acad Sci USA. 88:3671–3675. 1991. View Article : Google Scholar : PubMed/NCBI
49	Saelens X, Festjens N, Vande Walle L, van Gurp M, van Loo G and Vandenabeele P: Toxic proteins released from mitochondria in cell death. Oncogene. 23:2861–2874. 2004. View Article : Google Scholar : PubMed/NCBI
50	Guilhermino L, Diamantino T, Silva MC and Soares AM: Acute toxicity test with Daphnia magna: An alternative to mammals in the prescreening of chemical toxicity? Ecotoxicol Environ Saf. 46:357–362. 2000. View Article : Google Scholar : PubMed/NCBI
51	Hartl M and Humpf HU: Toxicity assessment of fumonisins using the brine shrimp (Artemia salina) bioassay. Food Chem Toxicol. 38:1097–1102. 2000. View Article : Google Scholar : PubMed/NCBI
52	Logarto Parra A, Silva Yhebra R, Guerra Sardiñas I and Iglesias Buela L: Comparative study of the assay of Artemia salina L. and the estimate of the medium lethal dose (LD50 value) in mice, to determine oral acute toxicity of plant extracts. Phytomedicine. 8:395–400. 2001. View Article : Google Scholar : PubMed/NCBI