Synergy and other interactions between polymethoxyflavones from citrus byproducts

Molecules

Volumn 20, Issue 11, 2015, Pages 20079-20106

  García, Benito F ^a   Torres, Ascensión ^a   Macías, Francisco A ^a  

^a UNIVERSITY OF CÁDIZ   (Spain)

Author keywords

Citrus by products; Coleoptiles; DPPH; Flavonoids; Isobolography; Synergism

Indexed keywords

FLAVONE DERIVATIVE; PLANT EXTRACT; SCAVENGER;

CHEMICAL STRUCTURE; CHEMISTRY; CITRUS; DRUG INTERACTION; DRUG POTENTIATION; ISOLATION AND PURIFICATION;

CITRUS; DRUG INTERACTIONS; DRUG SYNERGISM; FLAVONES; FREE RADICAL SCAVENGERS; MOLECULAR STRUCTURE; PLANT EXTRACTS;

EID: 84949962458     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules201119677     Document Type: Article

References (80)

1. Tatum, J.H.; Berry, R.E. Six new flavonoids from Citrus. Phytochemistry 1972, 11, 2283-2288. [Cross Ref]
2. Nogata, Y.; Sakamoto, K.; Shiratsuchi, H.; Ishii, T.; Yano, M.; Ohta, H. Flavonid Composition of Fruit Tissues of Citrus Species. Biosci. Biotechnol. Biochem. 2006, 70, 178-192. [Cross Ref] [Pub Med]
3. Bennett, R.D.; Miyake, M.; Ozaki, Y.; Hasegawa, S. Limonoid glucosides in Citrus aurantium. Phytochemistry 1991, 30, 3803-3805. [Cross Ref]
4. Anagnostopoulou, M.A.; Kefalas, P.; Kokklalou, E.; Assimopoulou, A.N.; Papageorgiou, V.P. Analysis of antioxidant compounds in sweet orange peel by HPLC-diode array detection-electrospray ionization mass spectrometry. Biomed. Chromatogr. 2005, 19, 138-148. [Cross Ref] [Pub Med]
5. Li, S.; Pan, M.-H.; Lai, C.-S.; Lo, C.-Y.; Dushenkov, S.; Ho, C.-T. Isolation and syntheses of polymethoxyflavones and hydroxylated polymetoxyflanones as inhibitor of HL-60 cell lines. Bioorg. Med. Chem. 2007, 15, 3381-3389. [Cross Ref] [Pub Med]
6. Hirata, T.; Fujii, M.; Akita, K.; Yanaka, N.; Ogawa, K.; Kuroyanagi, M.; Hongo, D. Identification and physiological evaluation of the components from Citrus fruits as potential drugs for anti-corpulence and anticancer. Bioorg. Med. Chem. 2009, 17, 25-28. [Cross Ref] [Pub Med]
7. Li, S.; Sang, S.; Pan, M.-H.; Lai, C.-S.; Lo, C.-Y.; Yang, C.S. Anti-inflammatory property of the urinary metabolites of nobiletin in mouse. Bioorg. Med. Chem. Lett. 2007, 17, 5177-5181. [Cross Ref] [Pub Med]
8. Ho, S.-C.; Lin, C.-C. Investigation of Heat Treating Conditions for Enhancing the Anti-inflammatory Activity of Citrus Fruits (Citrus reticulata) Peels. J. Agric. Food Chem. 2008, 56, 7976-7982. [Cross Ref] [Pub Med]
9. Xu, G.H.; Chen, J.C.; Liu, D.H.; Zhang, Y.H.; Jiang, P.; Ye, X.Q. Minerals, phenolics compounds, and antioxidant capacity of citrus peel extract by hot water. J. Food Sci. 2008, 73, 11-18. [Cross Ref] [Pub Med]
10. Jun, Y.L.W.; Rosemary, L.; Walzem, E.G.; Miller, L.M.; Pike, B.S. Antioxidant Activity of Citrus Limoids, Flavonoids and Coumarins. J. Agric. Food Chem. 2005, 53, 2009-2014.
11. Okuno, Y.; Miyazawa, M. Microbial O-demethylation of sinensetin and antimutagenic activity of the metabolite. J. Chem. Technol. Biotechnol. 2006, 81, 29-33. [Cross Ref]
12. Miyazawa, M.; Okuno, Y.; Fukuyama, M.; Nakamura, S.-I.; Kosaka, H. Antimutagenic Activity of Polimethoxyflavonoids from Citrus aurantium. J. Agric. Food Chem. 1999, 47, 5239-5244. [Cross Ref] [Pub Med]
13. Río, J.A.D.; Gómez, P.; Baidez, A.G.; Arcas, M.C.; Botía, J.M.; Ortuño, A. Changes in the Levels of Polymethoxyflavones and Flavanones as Part of the Defense Mechanism of Citrus sinensis (Cv. Valencia Late) Fruits against Phytophthora citrophthora. J. Agric. Food Chem. 2004, 52, 1913-1917. [Pub Med]
14. Río, J.A.D.; Arcas, M.C.; Benavente-García, O.; Ortuño, A. Citrus Polymethoxylated Flavones Can Confer Resistance against Phytophora citrophthora, Penicillium digitatum, and Geotrichum Species. J. Agric. Food Chem. 1998, 46, 4423-4428.
15. Lam, K.H.; Alex, D.; Lam, I.K.; Tsui, S.K.W.; Yang, Z.F.; Lee, S.M.Y. Nobiletin, a Polymethoxylated Flavonoid from Citrus, Shows Anti-Angiogenic Activity in a Zebrafish in vivo Model and HUVEC in Vitro model. J. Cell Biochem. 2011, 112, 3313-3321. [Cross Ref] [Pub Med]
16. Murakami, A.; Nakamura, Y.; Ohto, Y.; Yano, M.; Koshiba, T.; Koshimizu, K. Suppressive effects of citrus fruits on free radical generation and nobiletin, and anti-inflammatory polymethoxyflavonoid. Bio Factors 2000, 12, 187-192. [Cross Ref] [Pub Med]
17. Pan, M.-H.; Chen, W.-J.; Lin-Shiau, S.-Y.; Ho, C.-T.; Lin, J.-K. Tangeretin induces cell-cycle G1 arrest through inhibting cyclin-dependent kinases 2 and 4 activities as well as elevating Cdk inhibiting p21 and p27 in human colorectal carcinoma cells. Carcinogenesis 2002, 23, 1677-1687. [Cross Ref] [Pub Med]
18. Chen, K.-H.; Weng, M.-H.; Lin, J.-K. Tangeretin suppresses Il-1b-induced cyclooxygenase (COX)-2 expression through inhibition of p38 MAPK, JNK, and AKT activation in human lung carcinoma cells. Biochem. Pharmacol 2007, 73, 215-227. [Cross Ref] [Pub Med]
19. Lam, I.K.; Alex, D.; Wang, Y.-H.; Liu, P.; Liu, A.-L.; Du, G.-H.; Yuen Lee, S.M. In vitro an in vivo structure and activity relationship analysis of polymethoxylated flavonoids: Identifying sinensetin as a novel antiangiogenesis agent. Mol. Nutr. Food Res. 2012, 56, 945-956. [Cross Ref] [Pub Med]
20. Shin, H.-S.; Kang, S.-I.; Yoon, S.-A.; Ko, H.-C.; Kim, S.-J. Sinensetin Attenuates LPS-Induced inflammation by Regulating the Protein Level of IkB-A. Biosci. Biotechnol. Biochem. 2012, 76, 847-849. [Cross Ref] [Pub Med]
21. Junio, H.A.; Sy-Cordero, A.A.; Ettefagh, K.A.; Burns, J.T.; Micko, K.T.; Graf, T.N. Synergy-Directed Fractionation of Botanical Medicines: A case study with Goldenseal (Hydrastis canadensis). J. Nat. Prod. 2011, 74, 1621-1629. [Cross Ref] [Pub Med]
22. Wagner, H. Synergy research: Approaching a new generation of phytopharmaceuticals. Fitoterapia. 2011, 82, 34-37. [Cross Ref] [Pub Med]
23. Williamson, E.M. Synergy and other interactions in phytomedicines. Phytomedicine 2001, 8, 401-409. [Cross Ref] [Pub Med]
24. So, F.I.; Guthrie, N.; Chambers, A.F.; Moussa, M.; Caroll, K.K. Inhibition of human breast caner cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr. Cancer. 1996, 26, 167-181. [Cross Ref] [Pub Med]
25. Itoh, T.; Ohguchi, K.; Iinuma, M.; Nozawa, Y.; Akao, Y. Inhibitory effects of polymethoxy flavones isolated from Citrus reticulate on degranulation in rat basophilic leukemia RBL-2H3: Enhanced inhibition by their combination. Bioorg. Med. Chem. 2008, 16, 7592-7598. [Cross Ref] [Pub Med]
26. Akao, Y.; Itoh, T.; Ohguchi, K.; Iinuma, M.; Nozawa, Y. Interactive effects of polymethoxy flavones from Citrus on cell growth inhibition in human neoroblastoma SH-SY5Y cells. Bioorg. Med. Chem. 2008, 16, 2803-2810. [Cross Ref] [Pub Med]
27. Ko, H-C.; Jang, M-G.; Kang, C-H.; Lee, N-H.; Kang, S.; Lee, S-R.; Park, D-B.; Kim, S-J.; Kim, S-J. Preparation of a polymethoxyflavone-rich fraction (PRF) of Citrus sunki Hort. ex Tanaka and its antiproliferative effects. Food Chem. 2010, 123, 484-488. [Cross Ref]
28. Guo, S.; Qiu, P.; Xu, G.; Wu, X.; Dong, P.; Yang, G. Synergistic Anti-inflammatory Effects of Nobiletin and Sulforphane in Lipooplysaccharide-Stimulated RAW 264.7 Cells. J. Agric. Food Chem. 2012, 60, 2157-2164. [Cross Ref] [Pub Med]
29. Harasstani, O.A.; Moin, S.; Tham, C.L.; Liew, C.Y.; Ismail, N.; Rajajendram, R. Flavonoid combinations cause synergistic inhibition of proinflammatory mediator secretion from lipopolysaccharide induced RAW 264.7 cells. Inflamm. Res. 2010, 59, 711-721. [Cross Ref] [Pub Med]
30. Uesato, S.; Yamashita, H.; Maeda, R.; Hirata, Y.; Yamamoto, M.; Matsue, S. Synergistic antitumor effect of a combination of Paclitaxel and Carboplatin with Nobiletin from Citrus depressa on Non-small-Cel lung cancer cell lines. Planta Med. 2014, 80, 452-457. [Pub Med]
31. Bocco, A.; Cuvelier, M.-E.; Richard, H.; Berset, C. Antioxidant Activity and Phenolic Composition of Citrus Peel and Seed Extracts. J. Agric. Food Chem. 1998, 46, 2123-2129. [Cross Ref]
32. Benavente-García, O.J.C.; Marin, F.R.; Ortuño, A.; del Río, J.A. Uses and Properties of Citrus Flavonoids. J. Agric. Food Chem. 1997, 45, 4505-4515.
33. Yang, X.; Kang, S.-M.; Jeon, B.-T.; Kim, Y.-D.; Ha, J.-H.; Kim, Y.-T. Isolation and identification of an antioxidant flavonoid compound from citrus-processing by-product. J. Sci. Food Agric. 2011, 91, 1925-1927. [Cross Ref] [Pub Med]
34. Senevirathne, M.; Jeon, Y.-J.; Ha, J.-H.; Kim, S.-H. Effective drying of citrus by-product by high speed drying: A novel drying technique and their antioxidant activity. J. Food Eng. 2009, 92, 157-163. [Cross Ref]
35. Cutler, H.G. A fresh look at the wheat coleoptile bioassay. In Proceedings of the 11th Annual Meeting of the Plant Growth Regulator Society of America, Boston, MA, USA, 29 July-1 August 1984; Cutler, H.G., Ed.; pp. 1-9.
36. Cutler, S.J.; Hoagland, R.E.; Cutler, H.G. Evaluation of selected pharmaceuticals as potencial herbicides: Brindging the gap between agrochemicals and pharmaceuticals. In Allelopathy in Ecological Agriculture and Forestry, Proceedings of the III International Congress, Dharwad, Karantaka, India, 18-21 August 1998; Narwal, S.S., Hoagland, R.E., Dilday, M.J., Reigosa, M.J., Eds.; Springer: Dordrecht, The Netherlands, 2000; pp. 129-137.
37. Jacyno, J.M.; Cutler, H.G. Detection of herbicidal properties: Scope, and limitations of the etiolated wheat coleoptiles biossay. PGRSA Q. 1993, 21, 15-24.
38. Li, S.; Lo, C.-Y.; Ho, C.-T. Hydroxilated Polymethoxyflavones and Methylated Flavonoids in Sweet Orange (Citrus sinensis) Peel. J. Agric. Food Chem. 2006, 54, 4176-4185. [Cross Ref] [Pub Med]
39. Han, S.; Kim, H.M.; Lee, J.M.; Mok, S.-Y.; Lee, S. Isolation and Identification of Polymethoxyflavones from the Hybrid Citrus, Hallabong. J. Agric. Food Chem. 2010, 58, 9488-9491. [Cross Ref] [Pub Med]
40. Akkal, S.; Benayache, F.; Bentamene, A.; Medjroubi, K.; Seguin, E.; Tillequin, F. Flavonoid aglycones from Centaure napifolia. Chem. Nat. Compd. 2003, 39, 219-220. [Cross Ref]
41. Breksalll, A.P.; Dragull, K.; Wong, R.Y. Isolation and identification of the first C-17 limonin epimer, epilimonin. J. Agric. Food Chem. 2008, 56, 5595-5598. [Cross Ref] [Pub Med]
42. Green, I.R.; October, N. Role of the methoxy group in product formation via TICL4 promoted 4-phenyldioxolane isomerizations. Arkivoc 2010, 2, 71-96.
43. Kleiman, R.; Plattner, R.D.; Weisleder, D. Antigermination activity of phenylpropenoids from the genus Pimpinella. J. Nat. Prod. 1988, 51, 249-256. [Cross Ref]
44. Zou, K.; Tong, W.-Y.Y.; Liang, H.; Cui, J.-R.; Tu, G.-Z.; Zhao, Y.-Y. Diastereoisomeric saponins from Albizia julibrissin. Carbohydr. Res. 2005, 340, 1329-1334. [Cross Ref] [Pub Med]
45. Marwah, R.G.; Fatope, M.O.; Deadman, M.L.; Al-Maqbali, Y.M.; Husband, J. Musanahol: A new aureonitol-related metabolite from a Chaetomium sp. Tetrahedron 2007, 63, 8174-8180. [Cross Ref]
46. Naidu, S.V.; Gupta, P.; Kumar, P. Enantioselective symtheses of (-)-pinellic acid, α- and β-dimorphecolic acid. Tetrahedron 2007, 63, 7624-7633. [Cross Ref]
47. Iacazio, G. Easy access to various natural keto polyunsaturated fatty acids and their corresponding racemic alcohols. Chem. Phys. Lipids 2003, 125, 115-121. [Cross Ref]
48. Weber, B.; Hartmann, B.; Stöckigt, D.; Schreiber, K.; Roloff, M.; Bertram, H.-J. Liquid Chromatography/Mass Spectrometry and Liquid Chromatography/Nuclear Magnetic Resonance as Complementary Analytical Techniques for Unambiguous Identification of Polymethoxylated Flavones in Residues from Molecular Distillation of Orange Peel Oils. J. Agric. Food Chem. 2006, 54, 274-278. [Cross Ref] [Pub Med]
49. Mohamed, T.K. Chemical constituents and antioxidant activity of Citrus paradisis (Star-ruby Red Grapefruit) and Citrus sinensis (Blood Sweet Orange) Egyptian cultivars. Asian J. Chem. 2004, 16, 1753-1764.
50. Manners, G.D.; Breksa, A.P., III. Identifying citrus limonoid aglycones by HPLC-EI/MS and HPLC-APCI/MS techniques. Phytochem. Anal. 2004, 15, 372-381. [Cross Ref] [Pub Med]
51. Nakagawa, H.; Duan, H.; Takaishi, Y. Limonoids from Citrus sudachi. Chem. Pharm. Bull. 2001, 49, 649-651. [Cross Ref] [Pub Med]
52. Kirbaslar, S.I.; Kirbaslar, F.G. Composition of Turkish Mandarin and Bergamot Leaf Oils. J. Essent. Oil Res. 2006, 18, 318-327. [Cross Ref]
53. Ferhat, M.A.; Meklati, B.Y.; Chemat, F. Comparison of different isolation methods of esential oil from Citrus fruits: Cold pressing, hydrodistillation and microwave "dry" distillation. Flavour Fragr. J. 2007, 22, 494-504. [Cross Ref]
54. Matin, R.; Reichling, J. NIH-Shift during biosynthesis of epoxy-pseudoisoegugenol.(2-methylbutyrate) in tissue cultures of Pimpinella Anisum. Phytochemistry 1992, 31, 511-514. [Cross Ref]
55. Reichling, J.; Martin, R.; Kemmerer, B. Biosynthesis of pseudoisogenol-derivatives in liquid tissue cultures of Pimpinella anisum. Plant Cell. Tiss. Organ Cult. 1995, 43, 131-136. [Cross Ref]
56. Chin, Y-W.; Chai, H-B.; Keller, W.J.; Kinghorn, A.D. Lignans and Other Constituents of the Fruit of Euterpe oleracea (Açai) with Antioxidant and Cytoprotective Activities. J. Agric. Food Chem. 2008, 56, 7759-7764.
57. Smith, C.R., Jr.; Wilson, T.L.; Melvin, E.H.; Wolff, I.A. Dimorphecolic acid a Unique Hydroxydienoid Fatty Acid. J. Am. Chem. Soc. 1960, 82, 1417-1421. [Cross Ref]
58. Wu, Z.; Robinson, D.S. High-Performance Liquid Chromatographic Analysis of the Products of Linolic Acid Oxidation Catalyzed by Pea (Pisum sativum) Seed Lipoxygenases. J. Agric. Food Chem. 1995, 43, 337-342. [Cross Ref]
59. Macías, F.A.; Simonet, A.M.; Pacheco, P.C.; Barrero, A.F.; Cabrera, E; Jiménez-González, D. Natural and Synthetic Podolactones with Potential Use as Natural Herbicide Models. J. Agric. Food Chem. 2000, 48, 3003-3007.
60. Kang, P.; Kim, K.Y.; Lee, H.S.; Min, S.S.; Seol, G.H. Anti-inflammatory effects of anethole in lipopolysaccharide-induced acute lung injury in mice. Life Sci. 2013, 93, 955-961. [Cross Ref] [Pub Med]
61. Librán, C.M.; Moro, A.; Zalacain, A.; Molina, A.; Carmona, M.; Berruga, M.I. Potential aplication for aromatic plant extracts to prevent cheese blowing. World J. Microbiol. Biotechnol. 2013, 29, 1179-1188. [Cross Ref] [Pub Med]
62. Kuklev, D.V.; Christie, W.W.; Durand, T.; Rossi, J.C.; Vidal, J.P.; Kasyanov, S.P. Synthesis of keto- and hydroxydienoic compounds from linoleic acid. Chem. Phys. Lipids 1997, 85, 125-134. [Cross Ref]
63. Anagnostopoulou, M.A.; Kefalas, P.; Papageorgiou, V.P.; Assimopoulou, A.N.; Boskou, D. Radical scavenging activity of various extracts and fractions of sweet orange peel (Citrus sinensis). Food Chem. 2006, 94, 19-25. [Cross Ref]
64. Wu, Z.; Li, H.; Yang, Y.; Zhan, Y.; Tu, D. Variation in the components and antioxidant activity of Citrus medica L. var. sarcodactylis essential oils at different stages of madurity. Ind. Crops Prod. 2013, 46, 311-316. [Cross Ref]
65. Barreca, D.; Belloco, D.; Caristi, C.; Leuzzi, U.; Gattuso, G. Flavonoid profile and radical-scavenging activity of Mediterranean sweet lemon (Citrus limetta Risso) juice. Food Chem. 2011, 129, 417-422. [Cross Ref]
66. Freeman, B.L.; Eggett, D.L.; Parker, T.L. Synergistic and Antagonistic Interactions of Phenolics Compounds Found in Navel Oranges. J. Food Sci. 2010, 75, 570-576. [Cross Ref] [Pub Med]
67. Parker, T.L.; Miller, S.A.; Myers, L.E.; Miguez, F.E.; Engeseth, N.J. Evaluation of Synergistic Antioxidant Potential of Complex Mixtures Using Oxygen Radical Absorbance Capacity (ORAC) and Electron Paramagnetic Resonance (EPR). J. Agric. Food Chem. 2010, 58, 209-217. [Cross Ref] [Pub Med]
68. Scherer, R.; Godoy, H.T. Antioxidant activity index (AAI) by the 2,2-diphenyl-1-picrylhydrazyl method. Food Chem. 2009, 112, 654-658. [Cross Ref]
69. Amic, D.; Davidovic-Amic, D.; Beslo, D.; Rastija, V.; Lucic, B.; Trinajstic, N. SAR and QSAR of the antioxidant activity of flavonoids. Curr. Med. Chem. 2007, 14, 827-845. [Cross Ref] [Pub Med]
70. Tallarida, R.J. Drug Synergism: Its Detection and Applications. J. Pharmacol. Exp. Ther. 2001, 298, 865-872. [Pub Med]
71. Cedergreen, N.; Kudsk, P.; Mathiassen, S.K.; Sorensen, H.; Streibig, J.C. Reproducibility of Binary-Mixture Toxicity Studies. Environ. Toxicol. Chem. 2007, 26, 149-156. [Cross Ref] [Pub Med]
72. Berenbaum, M.C. What is Synergy? Pharmacol. Rev. 1989, 41, 93-141. [Pub Med]
73. Caccioni, D.R.L.; Guizzardi, M.; Biondi, D.M.; Renda, A.; Ruberto, G. Relationship between volatile components of citrus fruit essential oils and antimicrobial action on Penicillium digitatum and Penicillium italicum. Int. J. Food. Microbiol. 1998, 43, 73-79. [Cross Ref]
74. Stange, R.R.; Midland, S.L.; Sims, J.J.; McCollum, T.G. Differential effects of citrus peel extracts on growth of Penicillium digitatum, P. italicum, and P. expansum. Physiol. Mol. Plant. Pathol. 2002, 61, 303-311. [Cross Ref]
75. Hancock, C.R.; Barlow, H.W.; Lacey, H.J. The east malling coleoptile straight growth test method. J. Exp. Bot. 1961, 12, 401-408. [Cross Ref]
76. Nitsch, J.P.; Nitsch, C. Studies on the growth of coleoptile and first internode sections. A new, sensitive, straight-growth test for auxins. Plant. Physiol. 1956, 31, 94-111. [Cross Ref] [Pub Med]
77. Martín Andrés, A.; Luna del Castillo, J.D. Bioestadistica para las Ciencias de la Salud; Norma: Madrid, Spain, 1990; p. 22.
78. Mishra, K.; Ojha, H.; Chaudhury, N.K. Estimation of antiradical properties of antioxidants using DPPH assay: A critival review and results. Food. Chem. 2012, 130, 1036-1043. [Cross Ref]
79. Tallarida, R.J. Drug Synergism and Dose-Effect Data Analysis, 1st ed.; Chapman & Hall/CRC Press: Boca Raton, FL, USA, 2000; pp. 1-247.
80. Tallarida, R.J. The interaction index: A measure of drug synergism. Pain 2002, 98, 163-168. [Cross Ref]