Antioxidant, pro-oxidant and other biological activities of sesquiterpenes

Current Topics in Medicinal Chemistry

Volumn 14, Issue 22, 2014, Pages 2478-2494

  Bártíková, Hana ^a   Hanušová, Veronika ^a   Skálová, Lenka ^a   Ambrož, Martin ^a   Boušová, Iva ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Antioxidant; Cancer; Chemoprevention; Inflammation; Pro oxidant; Sesquiterpene

Indexed keywords

ALANTOLACTONE; ALPHA HYDROXYL 3BETA ANGELOYLCINNAMOLIDE; ARTEMISININ; BETA ELEMENE; BISABOLOL; CARYOPHYLLENE; CATALASE; FARNESOL; FURANODIENE; GERMACRANOLIDE DERIVATIVE; GLUTATHIONE TRANSFERASE; GUAIAZULENE; HUMULENE; IROFULVEN; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE; PARTHENOLIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; QUERCETIN; REACTIVE OXYGEN METABOLITE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SESQUITERPENE; SESQUITERPENE DERIVATIVE; SESQUITERPENE LACTONE; SUPEROXIDE DISMUTASE; TAMOXIFEN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ZEDERONE; ZERUMBONE; ANTIOXIDANT;

ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; BIOLOGICAL ACTIVITY; BIOTRANSFORMATION; CELL CYCLE REGULATION; CHELATION; DOWN REGULATION; DRUG BIOAVAILABILITY; DRUG ELIMINATION; DRUG HALF LIFE; DRUG METABOLISM; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; HUMAN; MAXIMUM PLASMA CONCENTRATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION;

ANTIOXIDANTS; MOLECULAR STRUCTURE; OXIDATION-REDUCTION; SESQUITERPENES;

EID: 84921839155     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026614666141203120833     Document Type: Article

References (158)

1. Huang, M.; Lu, J.-J.; Huang, M.-Q.; Bao, J.-L.; Chen, X.-P.; Wang, Y.-T. Terpenoids: natural products for cancer therapy. Exp. Opin. Invest. Drugs, 2012, 21(12), 1801-1818.
2. Cheng, A.-X.; Lou, Y.-G.; Mao, Y.-B.; Lu, S.; Wang, L.-J.; Chen, X.-Y. Plant terpenoids: Biosynthesis and ecological functions. J. Integr. Plant Biol., 2007, 49(2), 179-186.
3. Lange, B.M.; Ahkami, A. Metabolic engineering of plant monoterpenes, sesquiterpenes and diterpenes-current status and future opportunities. Plant Biotechnol. J., 2013, 11(2), 169-196.
4. Slamenova, D.; Horvathova, E. Cytotoxic, anti-carcinogenic and antioxidant properties of the most frequent plant volatiles. Neoplasma, 2013, 60(4), 343-354.
5. Nagegowda, D.A. Plant volatile terpenoid metabolism: Biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett., 2010, 584(14), 2965-2973.
6. Chen, F.; Tholl, D.; Bohlmann, J.; Pichersky, E. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J., 2011, 66(1), 212-229.
7. Oldfield, E. Targeting Isoprenoid Biosynthesis for Drug Discovery: Bench to Bedside. Accounts Chem. Res., 2010, 43(9), 1216-1226.
8. Merfort, I. Perspectives on Sesquiterpene Lactones in Inflammation and Cancer. Cur. Drug Targets, 2011, 12(11), 1560-1573.
9. Sampath, C.; Haug, K.; Thanei, S.; Hamburger, M.; Derendorf, H.; Frye, R.; Butterweck, V. Pharmacokinetics of Valerenic Acid in Rats after Intravenous and Oral Administrations. Planta Med., 2012, 78(6), 575-581.
10. Pei, L.; Liu, S.; Zheng, J.; Chen, X. A sensitive method for determination of furanodiene in rat plasma using liquid chromatography/ tandem mass spectrometry and its application to a pharmacokinetic study. Biomed. Chromatogr., 2012, 26(7), 826-832.
11. Chaves, J.S.; Leal, P.C.; Pianowisky, L.; Calixto, J.B. Pharmacokinetics and Tissue Distribution of the Sesquiterpene alpha- Humulene in Mice. Planta Med., 2008, 74(14), 1678-1683.
12. Liu, H.; Yang, G.; Tang, Y.; Cao, D.; Qi, T.; Qi, Y.; Fan, G. Physicochemical characterization and pharmacokinetics evaluation of beta- caryophyllene/beta-cyclodextrin inclusion complex. Int. J. Pharmaceut., 2013, 450(1-2), 304-310.
13. Zhang, F.; Gong, X.; Xiao, B.; Zhang, C.; Wang, Z. Pharmacokinetics and tissue distribution of a bioactive sesquiterpenoid from Polygonum jucundum following oral and intravenous administrations to rats. J. Pharm. Biomed. Anal., 2013, 83, 135-140.
14. Wang, K.; Li, Z.; Chen, Y.R.; Su, C.Y. The pharmacokinetics of a novel anti-tumor agent, beta-elemene, in Sprague-Dawley rats. Biopharm. Drug Dispos., 2005, 26(7), 301-307.
15. Thomas, J.P.; Arzoomanian, R.; Alberti, D.; Feierabend, C.; Binger, K.; Tutsch, K.D.; Steele, T.; Marnocha, R.; Smith, C.; Smith, S.; MacDonald, J.; Wilding, G.; Bailey, H. Phase I clinical and pharmacokinetic trial of irofulven. Cancer Chemoth. Pharm., 2001, 48(6), 467-472.
16. Ishida, T. Biotransformation of terpenoids by mammals, microorganisms, and plant-cultured cells. Chem. Biodivers., 2005, 2(5), 569-590.
17. Lee, Y.-P.; Hsu, F.-L.; Kang, J.-J.; Chen, C.-K.; Lee, S.-S. Metabolism of (2S)-Pterosin A: Identification of the Phase I and Phase II Metabolites in Rat Urine. Drug Metab. Dispos., 2012, 40(8), 1566- 1574.
18. Pimkaew, P.; Kublbeck, J.; Petsalo, A.; Jukka, J.; Suksamrarn, A.; Juvonen, R.; Auriola, S.; Piyachaturawat, P.; Honkakoski, P. Interactions of sesquiterpenes zederone and germacrone with the human cytochrome P450 system. Toxicol. In vitro, 2013, 27(6), 2005- 2012.
19. Pimkaew, P.; Suksen, K.; Somkid, K.; Chokchaisiri, R.; Jariyawat, S.; Chuncharunee, A.; Suksamrarn, A.; Piyachaturawat, P. Zederone, a Sesquiterpene from Curcuma elata Roxb, is Hepatotoxic in Mice. Int. J. Toxicol., 2013, 32(6), 454-462.
20. Lou, Y.; Zhang, H.; He, H.; Peng, K.; Kang, N.; Wei, X.; Li, X.; Chen, L.; Yao, X.; Qiu, F. Isolation and Identification of Phase 1 Metabolites of Curcumol in Rats. Drug Metab. Dispos., 2010, 38(11), 2014-2022.
21. Grace, J.M.; Aguilar, A.J.; Trotman, K.M.; Brewer, T.G. Metabolism of beta-arteether to dihydroqinghaosu by human liver microsomes and recombinant cytochrome P450. Drug Metab. Dispos., 1998, 26(4), 313-317.
22. Bamba, Y.; Yun, Y.S.; Kunugi, A.; Inoue, H. Compounds isolated from Curcuma aromatica Salisb. inhibit human P450 enzymes. J. Nat. Med., 2011, 65(3-4), 583-587.
23. th ed.; Oxford University Press: Oxford, 2007.
24. Dinkova-Kostova, A.T.; Talalay, P. Direct and indirect antioxidant properties of inducers of cytoprotective proteins. Mol. Nutr. Food Res., 2008, 52, S128-S138.
25. Amorati, R.; Foti, M.C.; Valgimigli, L. Antioxidant Activity of Essential Oils. J. Agr. Food Chem., 2013, 61(46), 10835-10847.
26. Bozin, B.; Mlmica-Dukic, N.; Samojlik, I.; Jovin, E. Antimicrobial and antioxidant properties of rosemary and sage (Rosmarinus officinalis L. and Salvia officinalis L., lamiaceae) essential oils. J. Agr. Food Chem., 2007, 55(19), 7879-7885.
27. Viuda-Martos, M.; Navajas, Y.R.; Zapata, E.S.; Fernandez-Lopez, J.; Perez-Alvarez, J.A. Antioxidant activity of essential oils of five spice plants widely used in a Mediterranean diet. Flavour Frag. J., 2010, 25(1), 13-19.
28. Bentayeb, K.; Vera, P.; Rubio, C.; Nerin, C. The additive properties of Oxygen Radical Absorbance Capacity (ORAC) assay: The case of essential oils. Food Chem., 2014, 148, 204-208.
29. Karakaya, S.; El, S.N.; Karagozlu, N.; Sahin, S. Antioxidant and Antimicrobial Activities of Essential Oils Obtained from Oregano (Origanum vulgare ssp hirtum) by Using Different Extraction Methods. J. Med. Food, 2011, 14(6), 645-652.
30. Wu, C.Q.; Chen, F.; Wang, X.; Kim, H.J.; He, G.Q.; Haley-Zitlin, V.; Huang, G. Antioxidant constituents in feverfew (Tanacetum parthenium) extract and their chromatographic quantification. Food Chem., 2006, 96(2), 220-227.
31. Hancianu, M.; Cioanca, O.; Mihasan, M.; Hritcu, L. Neuroprotective effects of inhaled lavender oil on scopolamine-induced dementia via anti-oxidative activities in rats. Phytomedicine, 2013, 20(5), 446-452.
32. Manjamalai, A.; Grace, V.M.B. Antioxidant Activity of Essential Oils from Wedelia chinensis (Osbeck) in vitro and in vivo Lung Cancer Bearing C57BL/6 Mice. Asian Pac. J. Cancer P., 2012, 13(7), 3065-3071.
33. Nakamura, Y.; Yoshida, C.; Murakami, A.; Ohigashi, H.; Osawa, T.; Uchida, K. Zerumbone, a tropical ginger sesquiterpene, activates phase II drug metabolizing enzymes. FEBS Lett., 2004, 572(1-3), 245-250.
34. Lee, W.L.; Huang, J.Y.; Shyur, L.F. Phytoagents for cancer management: regulation of nucleic acid oxidation, ROS, and related mechanisms. Oxid. Med. Cell. Longev., 2013, 2013, 925804, 22 pages.
35. Wang, X.; Beckham, T.H.; Morris, J.C.; Chen, F.; Gangemi, J.D. Bioactivities of gossypol, 6-methoxygossypol, and 6,6 '- dimethoxygossypol. J. Agr. Food Chem., 2008, 56(12), 4393-4398.
36. Vinholes, J.; Goncalves, P.; Martel, F.; Coimbra, M.A.; Rocha, S.M. Assessment of the antioxidant and antiproliferative effects of sesquiterpenic compounds in in vitro Caco-2 cell models. Food Chem., 2014, 156, 204-211.
37. van Zyl, R.L.; Seatlholo, S.T.; van Vuuren, S.F.; Viljoen, A.M. The biological activities of 20 nature identical essential oil constituents. J. Essent. Oil Res., 2006, 18, 129-133.
38. Gomez-Vidales, V.; Granados-Oliveros, G.; Nieto-Camacho, A.; Reyes-Solis, M.; Jimenez-Estrada, M. Cacalol and cacalol acetate as photoproducers of singlet oxygen and as free radical scavengers, evaluated by EPR spectroscopy and TBARS. Rsc. Adv., 2014, 4(3), 1371-1377.
39. Erasto, P.; Grierson, D.S.; Afolayan, A.J. Antioxidant constituents in Vernonia amygdalina leaves. Pharm. Biol., 2007, 45(3), 195- 199.
40. Shin, J.W.; Ohnishi, K.; Murakami, A.; Lee, J.S.; Kundu, J.K.; Na, H.K.; Ohigashi, H.; Surh, Y.J. Zerumbone Induces Heme Oxygenase- 1 Expression in Mouse Skin and Cultured Murine Epidermal Cells through Activation of Nrf2. Cancer Prev. Res., 2011, 4(6), 860-870.
41. Murakami, A.; Takahashi, D.; Kinoshita, T.; Koshimizu, K.; Kim, H.W.; Yoshihiro, A.; Nakamura, Y.; Jiwajinda, S.; Terao, J.; Ohigashi, H. Zerumbone, a Southeast Asian ginger sesquiterpene, markedly suppresses free radical generation, proinflammatory protein production, and cancer cell proliferation accompanied by apoptosis: the alpha,beta-unsaturated carbonyl group is a prerequisite. Carcinogenesis, 2002, 23(5), 795-802.
42. Calleja, M.A.; Vieites, J.M.; Montero-Meterdez, T.; Torres, M.I.; Faus, M.J.; Gil, A.; Suarez, A. The antioxidant effect of betacaryophyllene protects rat liver from carbon tetrachloride-induced fibrosis by inhibiting hepatic stellate cell activation. Br. J. Nutr., 2013, 109(3), 394-401.
43. Chang, H.J.; Kim, J.M.; Lee, J.C.; Kim, W.K.; Chun, H.S. Protective Effect of beta-Caryophyllene, a Natural Bicyclic Sesquiterpene, Against Cerebral Ischemic Injury. J. Med. Food, 2013, 16(6), 471-480.
44. Jimenez-Estrada, M.; Reyes-Chilpa, R.; Navarro-Ocana, A.; Arrieta- Baez, D. Reactivity of several reactive oxygen species (ROS) with the sesquiterpene cacalol. Nat. Prod. Commun., 2008, 3(4), 479-482.
45. Turkez, H.; Celik, K.; Togar, B. Effects of copaene, a tricyclic sesquiterpene, on human lymphocytes cells in vitro. Cytotechnology, 2013, 66(4):597-603.
46. Laughton, M.J.; Halliwell, B.; Evans, P.J.; Hoult, J.R. Antioxidant and pro-oxidant actions of the plant phenolics quercetin, gossypol and myricetin. Effects on lipid peroxidation, hydroxyl radical generation and bleomycin-dependent damage to DNA. Biochem. Pharmacol., 1989, 38(17), 2859-2865.
47. Rocha, N.F.M.; de Oliveira, G.V.; de Araujo, F.Y.R.; Rios, E.R.V.; Carvalho, A.M.R.; Vasconcelos, L.F.; Macedo, D.S.; Soares, P.M.G.; De Sousa, D.P.; de Sousa, F.C.F. (-)-alpha-Bisabololinduced gastroprotection is associated with reduction in lipid peroxidation, superoxide dismutase activity and neutrophil migration. Eur. J. Pharm. Sci., 2011, 44(4), 455-461.
48. Qamar, W.; Sultana, S. Farnesol ameliorates massive inflammation, oxidative stress and lung injury induced by intratracheal instillation of cigarette smoke extract in rats: an initial step in lung chemoprevention. Chem. Biol. Interact., 2008, 176(2-3), 79-87.
49. Lateef, A.; Rehman, M.U.; Tahir, M.; Khan, R.; Khan, A.Q.; Qamar, W.; Sultana, S. Farnesol protects against intratracheally instilled cigarette smoke extract-induced histological alterations and oxidative stress in prostate of Wistar rats. Toxicol. Intern., 2013, 20(1), 35-42.
50. Chen, B.Y.; Lin, D.P.; Su, K.C.; Chen, Y.L.; Wu, C.Y.; Teng, M.C.; Tsai, Y.T.; Sun, C.Y.; Wang, S.R.; Chang, H.H. Dietary zerumbone prevents against ultraviolet B-induced cataractogenesis in the mouse. Mol. Vis., 2011, 17, 723-730.
51. Berker, K.I.; Guclu, K.; Tor, I.; Demirata, B.; Apak, R. Total Antioxidant Capacity Assay Using Optimized Ferricyanide/Prussian Blue Method. Food Anal. Method., 2010, 3(3), 154-168.
52. Apak, R.; Guclu, K.; Ozyurek, M.; Celik, S.E. Mechanism of antioxidant capacity assays and the CUPRAC (cupric ion reducing antioxidant capacity) assay. Microchim. Acta, 2008, 160(4), 413-419.
53. Ben Sghaier, M.; Skandrani, I.; Nasr, N.; Franca, M.G.D.; Chekir- Ghedira, L.; Ghedira, K. Flavonoids and sesquiterpenes from Tecurium ramosissimum promote antiproliferation of human cancer cells and enhance antioxidant activity: A structure-activity relationship study. Environ. Toxicol. Phar., 2011, 32(3), 336-348.
54. Ding, Y.; Kim, J.A.; Yang, S.Y.; Kim, W.K.; Lee, S.H.; Jang, H.D.; Kim, Y.H. Antioxidative Sesquiterpenes from Artemisia iwayomogi. Bull. Korean Chem. Soc., 2011, 32(9), 3493-3496.
55. Zhang, Y.S.; Gordon, G.B. A strategy for cancer prevention: Stimulation of the Nrf2-ARE signaling pathway. Mol. Cancer Ther., 2004, 3(7), 885-893.
56. Ramos-Gomez, M.; Kwak, M.K.; Dolan, P.M.; Itoh, K.; Yamamoto, M.; Talalay, P.; Kensler, T.W. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc. Natl. Acad. Sci. U. S. A., 2001, 98(6), 3410-3415.
57. Hayes, J.D.; McMahon, M. Molecular basis for the contribution of the antioxidant responsive element to cancer chemoprevention. Cancer Lett., 2001, 174(2), 103-113.
58. McMahon, M.; Itoh, K.; Yamamoto, M.; Chanas, S.A.; Henderson, C.J.; McLellan, L.I.; Wolf, C.R.; Cavin, C.; Hayes, J.D. The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res., 2001, 61(8), 3299-3307.
59. Mandlekar, S.; Hong, J.L.; Kong, A.N. Modulation of metabolic enzymes by dietary phytochemicals: a review of mechanisms underlying beneficial versus unfavorable effects. Curr. Drug Metab., 2006, 7(6), 661-675.
60. Xu, C.J.; Li, C.Y.T.; Kong, A.N.T. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res., 2005, 28(3), 249-268.
61. Tang, C.Y.; Bi, M.J.; Yu, H.M.; Chen, W.; Wang, J.X. Zerumbone protects HEK 293 cells from irradiation-induced DNA damage via activating Keap1/Nrf2/ARE pathway. Afr. J. Pharm. Pharmacol., 2011, 5(20), 2247-2254.
62. Zheng, G.Q.; Kenney, P.M.; Lam, L.K.T. Sesquiterpenes from Clove (Eugenia-Caryophyllata) as Potential Anticarcinogenic Agents. J. Nat. Prod., 1992, 55(7), 999-1003.
63. Umemura, K.; Itoh, T.; Hamada, N.; Fujita, Y.; Akao, Y.; Nozawa, Y.; Matsuura, N.; Iinuma, M.; Ito, M. Preconditioning by sesquiterpene lactone enhances H2O2-induced Nrf2/ARE activation. Biochem. Biophys. Res. Commun., 2008, 368(4), 948-954.
64. Fischedick, J.T.; Standiford, M.; Johnson, D.A.; De Vos, R.C.H.; Todorovic, S.; Banjanac, T.; Verpoorte, R.; Johnson, J.A. Activation of Antioxidant Response Element in Mouse Primary Cortical Cultures with Sesquiterpene Lactones Isolated from Tanacetum parthenium. Planta Med., 2012, 78(16), 1725-1730.
65. Jeong, G.S.; Pae, H.O.; Jeong, S.O.; Kim, Y.C.; Kwon, T.O.; Lee, H.S.; Kim, N.S.; Park, S.D.; Chung, H.T. The alpha-methylenegamma- butyrolactone moiety in dehydrocostus lactone is responsible for cytoprotective heme oxygenase-1 expression through activation of the nuclear factor E2-related factor 2 in HepG2 cells. Eur. J. Pharmacol., 2007, 565(1-3), 37-44.
66. Kim, N.; Hwangbo, C.; Lee, S.; Lee, J.H. Eupatolide Inhibits PDGF-induced Proliferation and Migration of Aortic Smooth Muscle Cells Through ROS-dependent Heme Oxygenase-1 Induction. Phytother. Res., 2013, 27(11), 1700-1707.
67. Herrera, F.; Martin, V.; Rodriguez-Blanco, J.; Garcia-Santos, G.; Antolin, I.; Rodriguez, C. Intracellular redox state regulation by parthenolide. Biochem. Biophys. Res. Commun., 2005, 332(2), 321- 325.
68. Kim, J.H.; Lee, H.J.; Yeon, S.C.; Choi, D.H.; Lee, S.S.; Kang, J.K.; Chae, C.H.; Paik, N.W.; Lee, K.H.; Cho, M.H. Antioxidative effects of 7-hydroxy-3-methoxy-cadalene extracted from Zelkova serrata on 4-(methylinitros amino)-1-(3-pyridyl)-1-butanoneinduced oxidative stress in A/J mice. Phytother. Res., 2004, 18(5), 425-427.
69. Sun, Y.L.; Clair, D.K.S.; Xu, Y.; Crooks, P.A.; Clair, W.H.S. A NADPH Oxidase-Dependent Redox Signaling Pathway Mediates the Selective Radiosensitization Effect of Parthenolide in Prostate Cancer Cells. Cancer Res., 2010, 70(7), 2880-2890.
70. Bohm, F.; Edge, R.; Truscott, G. Interactions of dietary carotenoids with activated (singlet) oxygen and free radicals: potential effects for human health. Mol. Nutr. Food Res., 2012, 56(2), 205-216.
71. Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov., 2009, 8(7), 579-591.
72. Chaturvedi, D. In: Opportunity, Challenge and Scope of Natural Products in Medicinal Chemistry; Tiwari, V.M.; Mishra, B.B., Eds.; Research Signpost: Trivandrum, 2011; pp 313-334.
73. Amorim, M.H.; Gil da Costa, R.M.; Lopes, C.; Bastos, M.M. Sesquiterpene lactones: adverse health effects and toxicity mechanisms. Crit. Rev. Toxicol., 2013, 43(7), 559-579.
74. Barrera, P.; Sulsen, V.P.; Lozano, E.; Rivera, M.; Beer, M.F.; Tonn, C.; Martino, V.S.; Sosa, M.A. Natural Sesquiterpene Lactones Induce Oxidative Stress in Leishmania mexicana. Evid.- Based Complement. Altern. Med., 2013, 2013, 163404, 6 pages.
75. Kovacic, P. Mechanism of drug and toxic actions of gossypol: focus on reactive oxygen species and electron transfer. Curr. Med. Chem., 2003, 10(24), 2711-2718.
76. Prochazkova, D.; Bousova, I.; Wilhelmova, N. Antioxidant and prooxidant properties of flavonoids. Fitoterapia, 2011, 82(4), 513- 523.
77. D'Anneo, A.; Carlisi, D.; Lauricella, M.; Puleio, R.; Martinez, R.; Di Bella, S.; Di Marco, P.; Emanuele, S.; Di Fiore, R.; Guercio, A.; Vento, R.; Tesoriere, G. Parthenolide generates reactive oxygen species and autophagy in MDA-MB231 cells. A soluble parthenolide analogue inhibits tumour growth and metastasis in a xenograft model of breast cancer. Cell Death Dis., 2013, 4, e891, 14 pages.
78. Golenser, J.; Waknine, J.H.; Krugliak, M.; Hunt, N.H.; Grau, G.E. Current perspectives on the mechanism of action of artemisinins. Int. J. Parasitol., 2006, 36(14), 1427-1441.
79. Kijima, Y.; Ogunbunmi, E.; Fleischer, S. Drug action of thapsigargin on the Ca2+ pump protein of sarcoplasmic reticulum. J. Biol. Chem., 1991, 266(34), 22912-22918.
80. Rogers, T.B.; Inesi, G.; Wade, R.; Lederer, W.J. Use of thapsigargin to study Ca2+ homeostasis in cardiac cells. Bioscience Rep., 1995, 15(5), 341-349.
81. Eckstein-Ludwig, U.; Webb, R.J.; Van Goethem, I.D.; East, J.M.; Lee, A.G.; Kimura, M.; O'Neill, P.M.; Bray, P.G.; Ward, S.A.; Krishna, S. Artemisinins target the SERCA of Plasmodium falciparum. Nature, 2003, 424(6951), 957-961.
82. Wen, J.; You, K.R.; Lee, S.Y.; Song, C.H.; Kim, D.G. Oxidative stress-mediated apoptosis. The anticancer effect of the sesquiterpene lactone parthenolide. J. Biol. Chem., 2002, 277(41), 38954- 38964.
83. Machida, K.; Tanaka, T.; Fujita, K.; Taniguchi, M. Farnesolinduced generation of reactive oxygen species via indirect inhibition of the mitochondrial electron transport chain in the yeast Saccharomyces cerevisiae. J. Bacteriol., 1998, 180(17), 4460-4465.
84. Machida, K.; Tanaka, T.; Yano, Y.; Otani, S.; Taniguchi, M. Farnesol- induced growth inhibition in Saccharomyces cerevisiae by a cell cycle mechanism. Microbiology, 1999, 145 (Pt 2), 293-299.
85. Yang, F.; Chen, W.D.; Deng, R.; Li, D.D.; Wu, K.W.; Feng, G.K.; Li, H.J.; Zhu, X.F. Hirsutanol A induces apoptosis and autophagy via reactive oxygen species accumulation in breast cancer MCF-7 cells. J. Pharmacol. Sci., 2012, 119(3), 214-220.
86. Lee, W.L.; Shyur, L.F. Deoxyelephantopin impedes mammary adenocarcinoma cell motility by inhibiting calpain-mediated adhesion dynamics and inducing reactive oxygen species and aggresome formation. Free Radic. Biol. Med., 2012, 52(8), 1423-1436.
87. Kumar, A.; Malik, F.; Bhushan, S.; Sethi, V.K.; Shahi, A.K.; Kaur, J.; Taneja, S.C.; Qazi, G.N.; Singh, J. An essential oil and its major constituent isointermedeol induce apoptosis by increased expression of mitochondrial cytochrome c and apical death receptors in human leukaemia HL-60 cells. Chem. Biol. Interact., 2008, 171(3), 332-347.
88. Cavalieri, E.; Bergamini, C.; Mariotto, S.; Leoni, S.; Perbellini, L.; Darra, E.; Suzuki, H.; Fato, R.; Lenaz, G. Involvement of mitochondrial permeability transition pore opening in alpha-bisabolol induced apoptosis. FEBS J., 2009, 276(15), 3990-4000.
89. Saeidnia, S.; Gohari, A.R.; Haddadi, A. Biogenic trypanocidal sesquiterpenes: lead compounds to design future trypanocidal drugs - a mini review. Daru J. Pharm. Sci., 2013, 21(1), 35, 9 pages.
90. Jodynis-Liebert, J.; Murias, M.; Bloszyk, E. Effect of several sesquiterpene lactones on lipid peroxidation and glutathione level. Planta Med., 1999, 65(4), 320-324.
91. Franco, R.; Panayiotidis, M.I.; Cidlowski, J.A. Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J. Biol. Chem., 2007, 282(42), 30452-30465.
92. Khan, M.; Yi, F.; Rasul, A.; Li, T.; Wang, N.; Gao, H.; Gao, R.; Ma, T. Alantolactone induces apoptosis in glioblastoma cells via GSH depletion, ROS generation, and mitochondrial dysfunction. IUBMB Life, 2012, 64(9), 783-794.
93. Merrill, J.C.; Kim, H.L.; Safe, S.; Murray, C.A.; Hayes, M.A. Role of glutathione in the toxicity of the sesquiterpene lactones hymenoxon and helenalin. J. Toxicol. Environ. Health, 1988, 23(2), 159-169.
94. Robles, M.; Choi, B.H.; Han, B.; Santa Cruz, K.; Kim, R.C. Repininduced neurotoxicity in rodents. Exp. Neurol., 1998, 152(1), 129- 136.
95. Tukov, F.F.; Rimoldi, J.M.; Matthews, J.C. Characterization of the role of glutathione in repin-induced mitochondrial dysfunction, oxidative stress and dopaminergic neurotoxicity in rat pheochromocytoma (PC12) cells. Neurotoxicology, 2004, 25(6), 989-999.
96. Machida, K.; Tanaka, T.; Taniguchi, M. Depletion of glutathione as a cause of the promotive effects of polygodial, a sesquiterpene on the production of reactive oxygen species in Saccharomyces cerevisiae. J. Biosci. Bioeng., 1999, 88(5), 526-530.
97. Legault, J.; Dahl, W.; Debiton, E.; Pichette, A.; Madelmont, J.C. Antitumor activity of balsam fir oil: production of reactive oxygen species induced by alpha-humulene as possible mechanism of action. Planta Med., 2003, 69(5), 402-407.
98. Woerdenbag, H.J.; Lemstra, W.; Malingre, T.M.; Konings, A.W. Enhanced cytostatic activity of the sesquiterpene lactone eupatoriopicrin by glutathione depletion. Br. J. Cancer, 1989, 59(1), 68- 75.
99. Arrick, B.A.; Griffo, W.; Cohn, Z.; Nathan, C. Hydrogen peroxide from cellular metabolism of cystine. A requirement for lysis of murine tumor cells by vernolepin, a glutathione-depleting antineoplastic. J. Clin. Invest., 1985, 76(2), 567-574.
100. Arrick, B.A.; Nathan, C.F.; Cohn, Z.A. Inhibition of glutathione synthesis augments lysis of murine tumor cells by sulfhydrylreactive antineoplastics. J. Clin. Invest., 1983, 71(2), 258-267.
101. Choi, J.H.; Ha, J.; Park, J.H.; Lee, J.Y.; Lee, Y.S.; Park, H.J.; Choi, J.W.; Masuda, Y.; Nakaya, K.; Lee, K.T. Costunolide triggers apoptosis in human leukemia U937 cells by depleting intracellular thiols. Jpn. J. Cancer Res., 2002, 93(12), 1327-1333.
102. Choi, J.H.; Lee, K.T. Costunolide-induced apoptosis in human leukemia cells: involvement of c-jun N-terminal kinase activation. Biol. Pharm. Bull., 2009, 32(10), 1803-1808.
103. Lee, M.G.; Lee, K.T.; Chi, S.G.; Park, J.H. Costunolide induces apoptosis by ROS-mediated mitochondrial permeability transition and cytochrome C release. Biol. Pharm. Bull., 2001, 24(3), 303- 306.
104. Khan, M.; Li, T.; Ahmad Khan, M.K.; Rasul, A.; Nawaz, F.; Sun, M.; Zheng, Y.; Ma, T. Alantolactone induces apoptosis in HepG2 cells through GSH depletion, inhibition of STAT3 activation, and mitochondrial dysfunction. BioMed Res. Int., 2013, 2013, 719858, 11 pages.
105. Jodynis-Liebert, J.; Murias, M.; Bloszyk, E. Effect of sesquiterpene lactones on antioxidant enzymes and some drug-metabolizing enzymes in rat liver and kidney. Planta Med., 2000, 66(3), 199-205.
106. Liu, X.; Pietsch, K.E.; Sturla, S.J. Susceptibility of the antioxidant selenoenyzmes thioredoxin reductase and glutathione peroxidase to alkylation-mediated inhibition by anticancer acylfulvenes. Chem. Res. Toxicol., 2011, 24(5), 726-736.
107. Liu, X.; Sturla, S.J. Profiling patterns of glutathione reductase inhibition by the natural product illudin S and its acylfulvene analogues. Mol. Biosyst., 2009, 5(9), 1013-1024.
108. Schmidt, T.J. Glutathione adducts of helenalin and 11 alpha,13- dihydrohelenalin acetate inhibit glutathione S-transferase from horse liver. Planta Med., 2000, 66(2), 106-109.
109. Bollrath, J.; Greten, F.R. IKK/NF-kappaB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis. EMBO Rep., 2009, 10(12), 1314-1319.
110. Baldwin, A.S., Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol., 1996, 14, 649-683.
111. Karin, M.; Liu, Z.; Zandi, E. AP-1 function and regulation. Curr. Opin. Cell Biol., 1997, 9(2), 240-246.
112. Surh, Y.J. NF-kappa B and Nrf2 as potential chemopreventive targets of some anti-inflammatory and antioxidative phytonutrients with anti-inflammatory and antioxidative activities. Asia Pac. J. Clin. Nutr., 2008, 17, 269-272.
113. Huxford, T.; Ghosh, G. A Structural Guide to Proteins of the NFkappa B Signaling Module. Cold Spring Harbor Perspect. Biol., 2009, 1(3), a000075, 16 pages.
114. Schattner, E.J.; Furman, R.R.; Bernal, A. In: NF-κB/Rel Transcription Factor Family; Liou, H.C., Ed.; Springer, New York, 2006; pp. 134-146.
115. Fernandes, E.S.; Passos, G.F.; Medeiros, R.; da Cunha, F.M.; Ferreira, J.; Campos, M.M.; Pianowski, L.F.; Calixto, J.B. Antiinflammatory effects of compounds alpha-humulene and (-)-transcaryophyllene isolated from the essential oil of Cordia verbenacea. Eur. J. Pharmacol., 2007, 569(3), 228-236.
116. Medeiros, R.; Passos, G.F.; Vitor, C.E.; Koepp, J.; Mazzuco, T.L.; Pianowski, L.F.; Campos, M.M.; Calixto, J.B. Effect of two active compounds obtained from the essential oil of Cordia verbenacea on the acute inflammatory responses elicited by LPS in the rat paw. Br. J. Pharmacol., 2007, 151(5), 618-627.
117. Passos, G.F.; Fernandes, E.S.; da Cunha, F.M.; Ferreira, J.; Pianowski, L.F.; Campos, M.M.; Calixto, J.B. Anti-inflammatory and anti-allergic properties of the essential oil and active compounds from Cordia verbenacea. J. Ethnopharmacol., 2007, 110(2), 323- 333.
118. Rogerio, A.P.; Andrade, E.L.; Leite, D.F.; Figueiredo, C.P.; Calixto, J.B. Preventive and therapeutic anti-inflammatory properties of the sesquiterpene alpha-humulene in experimental airways allergic inflammation. Br. J. Pharmacol., 2009, 158(4), 1074-1087.
119. Horvath, B.; Mukhopadhyay, P.; Kechrid, M.; Patel, V.; Tanchian, G.; Wink, D.A.; Gertsch, J.; Pacher, P. beta-Caryophyllene ameliorates cisplatin-induced nephrotoxicity in a cannabinoid 2 receptordependent manner. Free Radic. Biol. Med., 2012, 52(8), 1325- 1333.
120. Wenhong, D.; Jia, Y.; Weixing, W.; Xiaoyan, C.; Chen, C.; Sheng, X.; Hao, J. Zerumbone attenuates the severity of acute necrotizing pancreatitis and pancreatitis-induced hepatic injury. Mediat. Inflamm., 2012, 2012, 156507, 12 pages.
121. Murakami, A.; Miyamoto, M.; Ohigashi, H. Zerumbone, an antiinflammatory phytochemical, induces expression of proinflammatory cytokine genes in human colon adenocarcinoma cell lines. BioFactors, 2004, 21(1-4), 95-101.
122. Huo, M.; Gao, R.; Jiang, L.; Cui, X.; Duan, L.; Deng, X.; Guan, S.; Wei, J.; Soromou, L.W.; Feng, H.; Chi, G. Suppression of LPSinduced inflammatory responses by gossypol in RAW 264.7 cells and mouse models. Int. Immunopharmacol., 2013, 15(2), 442-449.
123. Sobota, R.; Szwed, M.; Kasza, A.; Bugno, M.; Kordula, T. Parthenolide inhibits activation of signal transducers and activators of transcription (STATs) induced by cytokines of the IL-6 family. Biochem. Biophys. Res. Commun., 2000, 267(1), 329-333.
124. Tsoyi, K.; Jang, H.J.; Lee, Y.S.; Kim, Y.M.; Kim, H.J.; Seo, H.G.; Lee, J.H.; Kwak, J.H.; Lee, D.U.; Chang, K.C. (+)-Nootkatone and (+)-valencene from rhizomes of Cyperus rotundus increase survival rates in septic mice due to heme oxygenase-1 induction. J. Ethnopharmacol., 2011, 137(3), 1311-1317.
125. Erel, S.B.; Karaalp, C.; Bedir, E.; Kaehlig, H.; Glasl, S.; Khan, S.; Krenn, L. Secondary metabolites of Centaurea calolepis and evaluation of cnicin for anti-inflammatory, antioxidant, and cytotoxic activities. Pharm. Biol., 2011, 49(8), 840-849.
126. Kim, S.; Jung, E.; Kim, J.H.; Park, Y.H.; Lee, J.; Park, D. Inhibitory effects of (-)-alpha-bisabolol on LPS-induced inflammatory response in RAW264.7 macrophages. Food Chem. Toxicol., 2011, 49(10), 2580-2585.
127. Tan, W.; Lu, J.; Huang, M.; Li, Y.; Chen, M.; Wu, G.; Gong, J.; Zhong, Z.; Xu, Z.; Dang, Y.; Guo, J.; Chen, X.; Wang, Y. Anticancer natural products isolated from chinese medicinal herbs. Chin. Med., 2011, 6(1), 27, 15 pages.
128. Kim, H.J.; Hawke, N.; Baldwin, A.S. NF-kappaB and IKK as therapeutic targets in cancer. Cell Death Differ., 2006, 13(5), 738- 747.
129. Park, K.R.; Nam, D.; Yun, H.M.; Lee, S.G.; Jang, H.J.; Sethi, G.; Cho, S.K.; Ahn, K.S. beta-Caryophyllene oxide inhibits growth and induces apoptosis through the suppression of PI3K/AKT/ mTOR/S6K1 pathways and ROS-mediated MAPKs activation. Cancer Lett., 2011, 312(2), 178-188.
130. Kim, C.; Cho, S.K.; Kapoor, S.; Kumar, A.; Vali, S.; Abbasi, T.; Kim, S.H.; Sethi, G.; Ahn, K.S. beta-Caryophyllene oxide Inhibits Constitutive and Inducible STAT3 Signaling Pathway Through Induction of the SHP-1 Protein Tyrosine Phosphatase. Mol. Carcinog., 2013, 53(10), 793-806.
131. Kim, C.; Cho, S.K.; Kim, K.D.; Nam, D.; Chung, W.S.; Jang, H.J.; Lee, S.G.; Shim, B.S.; Sethi, G.; Ahn, K.S. beta-Caryophyllene oxide potentiates TNFalpha-induced apoptosis and inhibits invasion through down-modulation of NF-kappaB-regulated gene products. Apoptosis, 2014, 19(4), 708-718.
132. Sain, S.; Naoghare, P.K.; Devi, S.S.; Daiwile, A.; Krishnamurthi, K.; Arrigo, P.; Chakrabarti, T. Beta caryophyllene and caryophyllene oxide, isolated from Aegle marmelos, as the potent antiinflammatory agents against lymphoma and neuroblastoma cells. Antiinflamm. Antiallergy Agents Med. Chem., 2014, 13(1), 45-55.
133. Lan, Y.H.; Wu, Y.C.; Wu, K.W.; Chung, J.G.; Lu, C.C.; Chen, Y.L.; Wu, T.S.; Yang, J.S. Death receptor 5-mediated TNFR family signaling pathways modulate gamma-humulene-induced apoptosis in human colorectal cancer HT29 cells. Oncol. Rep., 2011, 25(2), 419-424.
134. Takada, Y.; Murakami, A.; Aggarwal, B.B. Zerumbone abolishes NF-kappaB and IkappaBalpha kinase activation leading to suppression of antiapoptotic and metastatic gene expression, upregulation of apoptosis, and downregulation of invasion. Oncogene, 2005, 24(46), 6957-6969.
135. Ma, E.; Wang, X.; Li, Y.; Sun, X.; Tai, W.; Li, T.; Guo, T. Induction of apoptosis by furanodiene in HL60 leukemia cells through activation of TNFR1 signaling pathway. Cancer Lett., 2008, 271(1), 158-166.
136. Zhong, Z.F.; Hoi, P.M.; Wu, G.S.; Xu, Z.T.; Tan, W.; Chen, X.P.; Cui, L.; Wu, T.; Wang, Y.T. Anti-angiogenic effect of furanodiene on HUVECs in vitro and on zebrafish in vivo. J. Ethnopharmacol., 2012, 141(2), 721-727.
137. Xu, W.S.; Dang, Y.Y.; Guo, J.J.; Wu, G.S.; Lu, J.J.; Chen, X.P.; Wang, Y.T. Furanodiene induces endoplasmic reticulum stress and presents antiproliferative activities in lung cancer cells. Evid.- Based Complement. Altern. Med., 2012, 2012, 426521, 8 pages.
138. Zhong, Z.F.; Li, Y.B.; Wang, S.P.; Tan, W.; Chen, X.P.; Chen, M.W.; Wang, Y.T. Furanodiene enhances tamoxifen-induced growth inhibitory activity of ERa-positive breast cancer cells in a PPARgamma independent manner. J. Cell. Biochem., 2012, 113(8), 2643-2651.
139. Aggarwal, B.B.; Yuan, W.; Li, S.; Gupta, S.C. Curcumin-free turmeric exhibits anti-inflammatory and anticancer activities: Identification of novel components of turmeric. Mol. Nutr. Food Res., 2013, 57(9), 1529-1542.
140. Zhang, S.; Ong, C.N.; Shen, H.M. Critical roles of intracellular thiols and calcium in parthenolide-induced apoptosis in human colorectal cancer cells. Cancer Lett., 2004, 208(2), 143-153.
141. Mathema, V.B.; Koh, Y.S.; Thakuri, B.C.; Sillanpaa, M. Parthenolide, a sesquiterpene lactone, expresses multiple anti-cancer and anti-inflammatory activities. Inflammation, 2012, 35(2), 560-565.
142. Pajak, B.; Gajkowska, B.; Orzechowski, A. Molecular basis of parthenolide-dependent proapoptotic activity in cancer cells. Folia Histochem. Cytobiol., 2008, 46(2), 129-135.
143. Kim, S.L.; Trang, K.T.; Kim, S.H.; Kim, I.H.; Lee, S.O.; Lee, S.T.; Kim, D.G.; Kim, S.W. Parthenolide suppresses tumor growth in a xenograft model of colorectal cancer cells by inducing mitochondrial dysfunction and apoptosis. Int. J. Oncol., 2012, 41(4), 1547- 1553.
144. Ferrara, N.; Hillan, K.J.; Gerber, H.P.; Novotny, W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov., 2004, 3(5), 391-400.
145. Kim, M.; Miyamoto, S.; Yasui, Y.; Oyama, T.; Murakami, A.; Tanaka, T. Zerumbone, a tropical ginger sesquiterpene, inhibits colon and lung carcinogenesis in mice. Int. J. Cancer, 2009, 124(2), 264-271.
146. Sung, B.; Jhurani, S.; Ahn, K.S.; Mastuo, Y.; Yi, T.; Guha, S.; Liu, M.; Aggarwal, B.B. Zerumbone down-regulates chemokine receptor CXCR4 expression leading to inhibition of CXCL12-induced invasion of breast and pancreatic tumor cells. Cancer Res., 2008, 68(21), 8938-8944.
147. Oka, D.; Nishimura, K.; Shiba, M.; Nakai, Y.; Arai, Y.; Nakayama, M.; Takayama, H.; Inoue, H.; Okuyama, A.; Nonomura, N. Sesquiterpene lactone parthenolide suppresses tumor growth in a xenograft model of renal cell carcinoma by inhibiting the activation of NF-kappaB. Int. J. Cancer, 2007, 120(12), 2576-2581.
148. Moon, D.O.; Choi, Y.H.; Moon, S.K.; Kim, W.J.; Kim, G.Y. Gossypol decreases tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 expression via suppression of NF-kappaB activity. Food Chem. Toxicol., 2011, 49(4), 999-1005.
149. Wakabayashi, H.; Hashiba, K.; Yokoyama, K.; Hashimoto, K.; Kikuchi, H.; Nishikawa, H.; Kurihara, T.; Satoh, K.; Shioda, S.; Saito, S.; Kusano, S.; Nakashima, H.; Motohashi, N.; Sakagami, H. Cytotoxic activity of azulenes against human oral tumor cell lines. Anticancer Res., 2003, 23(6C), 4747-4755.
150. Mo, H.; Peffley, D.; Elson, C. In: Nutritional Oncology; Heber, D.; Blackburn, G.L.; Go, V.L.W.; Milner, J., Eds.; Academic Press: San Diego, 1999; pp. 379-391.
151. Lu, J.J.; Dang, Y.Y.; Huang, M.; Xu, W.S.; Chen, X.P.; Wang, Y.T. Anti-cancer properties of terpenoids isolated from Rhizoma Curcumae--a review. J. Ethnopharmacol., 2012, 143(2), 406-411.
152. Zhong, Z.; Dang, Y.; Yuan, X.; Guo, W.; Li, Y.; Tan, W.; Cui, J.; Lu, J.; Zhang, Q.; Chen, X.; Wang, Y. Furanodiene, a natural product, inhibits breast cancer growth both in vitro and in vivo. Cell. Physiol. Biochem., 2012, 30(3), 778-790.
153. Wiseman, D.A.; Werner, S.R.; Crowell, P.L. Cell cycle arrest by the isoprenoids perillyl alcohol, geraniol, and farnesol is mediated by p21(Cip1) and p27(Kip1) in human pancreatic adenocarcinoma cells. J. Pharmacol. Exp. Ther., 2007, 320(3), 1163-1170.
154. Weng, S.X.; Sui, M.H.; Chen, S.; Wang, J.A.; Xu, G.; Ma, J.; Shan, J.; Fang, L. Parthenolide inhibits proliferation of vascular smooth muscle cells through induction of G0/G1 phase cell cycle arrest. J. Zhejiang Univ. Sci. B, 2009, 10(7), 528-535.
155. Ferreira, F.M.; Palmeira, C.M.; Oliveira, M.M.; Santos, D.; Simoes, A.M.; Rocha, S.M.; Coimbra, M.A.; Peixoto, F. Nerolidol effects on mitochondrial and cellular energetics. Toxicol. In vitro, 2012, 26(2), 189-196.
156. Legault, J.; Pichette, A. Potentiating effect of beta-caryophyllene on anticancer activity of alpha-humulene, isocaryophyllene and paclitaxel. J. Pharm. Pharmacol., 2007, 59(12), 1643-1647.
157. Xu, W.S.; Dang, Y.Y.; Chen, X.P.; Lu, J.J.; Wang, Y.T. Furanodiene presents synergistic anti-proliferative activity with paclitaxel via altering cell cycle and integrin signaling in 95-D lung cancer cells. Phytother. Res., 2014, 28(2), 296-299.
158. Giancotti, F.G. Targeting integrin beta4 for cancer and antiangiogenic therapy. Trends Pharmacol. Sci., 2007, 28(10), 506- 511.