Seaweed extracts and unsaturated fatty acid constituents from the green alga Ulva lactuca as activators of the cytoprotective Nrf2-ARE pathway

Free Radical Biology and Medicine

Volumn 57, Issue , 2013, Pages 141-153

  Wang, Rui ^a   Paul, Valerie J ^b   Luesch, Hendrik ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b SMITHSONIAN MARINE STATION   (United States)

Author keywords

Antioxidant response element; Antioxidants; Cytoprotective enzymes; Edible seaweeds; Fatty acid amides; Free radicals; Glutathione; Keap1; Monounsaturated fatty acids; NQO1; Nrf2; Oxidative stress; Reactive oxygen species; Ulva lactuca

Indexed keywords

9 KETO HEXADEC 7 ENOIC ACID; 9 KETO OCTADEC 7 ENAMIDE; 9 KETO OCTADEC 7 ENOIC ACID; ANTIOXIDANT; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; HEME OXYGENASE 1; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MONOUNSATURATED FATTY ACID; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); THIOREDOXIN REDUCTASE 1; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NRF2; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BRAIN TISSUE; CANCER CELL CULTURE; CELL PROTECTION; CHEMICAL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DRUG ACTIVITY; DRUG BIOAVAILABILITY; ELECTROPHILICITY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG PARENCHYMA; MALE; MASS SPECTROMETRY; MOUSE; NEUROBLASTOMA CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; RNA INTERFERENCE; STOMACH; STRUCTURE ACTIVITY RELATION; UBIQUITINATION; ULVA; WESTERN BLOTTING;

AMINO ACID TRANSPORT SYSTEM Y+; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; ANTIOXIDANTS; CELL LINE, TUMOR; CYTOPROTECTION; FATTY ACIDS, UNSATURATED; GLUTAMATE-CYSTEINE LIGASE; HEK293 CELLS; HEME OXYGENASE-1; HUMANS; MALE; MICE; MICE, TRANSGENIC; NAD(P)H DEHYDROGENASE (QUINONE); NEUROBLASTOMA; NF-E2-RELATED FACTOR 2; PHOSPHATIDYLINOSITOL 3-KINASES; PLANT EXTRACTS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SEAWEED; THIOREDOXIN REDUCTASE 1; TRANSCRIPTION, GENETIC; ULVA;

ALGAE; CHLOROPHYTA; EUKARYOTA; MUS; ULVA LACTUCA;

EID: 84873708928     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.12.019     Document Type: Article

References (64)

1. B. Halliwell Biochemistry of oxidative stress Biochem. Soc. Trans. 35 2007 1147 1150
2. Y. Liu, J.T. Kern, J.R. Walker, J.A. Johnson, P.G. Schultz, and H. Luesch A genomic screen for activators of the antioxidant response element Proc. Natl. Acad. Sci. USA 104 2007 5205 5210 (Pubitemid 47186200)
3. D.D. Zhang Mechanistic studies of the Nrf2-Keap1 signaling pathway Drug Metab. Rev. 38 2006 769 789 (Pubitemid 44903268)
4. M. Kobayashi, and M. Yamamoto Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species Adv. Enzyme Regul 46 2006 113 140 (Pubitemid 44301353)
5. A.T. Dinkova-Kostova, W.D. Holtzclaw, and T.W. Kensler The role of Keap1 in cellular protective responses Chem. Res. Toxicol. 18 2005 1779 1791 (Pubitemid 43023036)
6. E. Balogun, M. Hoque, P. Gong, E. Killeen, C.J. Green, R. Foresti, J. Alam, and R. Motterlini Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element Biochem. J. 371 2003 887 895 (Pubitemid 36578887)
7. H. Hatcher, R. Planalp, J. Cho, F.M. Torti, and S.V. Torti Curcumin: from ancient medicine to current clinical trials Cell Mol. Life Sci. 65 2008 1631 1652
8. P. Langcake, and R.J. Pryce Production of resveratrol by Vitis-vinifera and other members of Vitaceae as a response to infection or injury Physiol. Plant Pathol 9 1976 77 86
9. J.A. Rubiolo, G. Mithieux, and F.V. Vega Resveratrol protects primary rat hepatocytes against oxidative stress damage: activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes Eur. J. Pharmacol 591 2008 66 72
10. F. Levi, C. Pasche, F. Lucchini, R. Ghidoni, M. Ferraroni, and C. La Vecchia Resveratrol and breast cancer risk Eur. J. Cancer Prev. 14 2005 139 142 (Pubitemid 40516975)
11. W. Zhu, W. Qin, K. Zhang, G.E. Rottinghaus, Y.C. Chen, B. Kliethermes, and E.R. Sauter Trans-resveratrol alters mammary promoter hypermethylation in women at increased risk for breast cancer Nutr. Cancer 64 2012 393 400
12. T.W. Kensler, P.A. Egner, A.S. Agyeman, K. Visvanathan, J.D. Groopman, J.G. Chen, T.Y. Chen, J.W. Fahey, and P. Talalay Keap1-Nrf2 signaling: a target for cancer prevention by sulforaphane Top. Curr. Chem. 329 2013 163 177
13. T.W. Kensler, J.G. Chen, P.A. Egner, J.W. Fahey, L.P. Jacobson, K.K. Stephenson, L. Ye, J.L. Coady, J.B. Wang, Y. Wu, Y. Sun, Q.N. Zhang, B.C. Zhang, Y.R. Zhu, G.S. Qian, S.G. Carmella, S.S. Hecht, L. Benning, S.J. Gange, J.D. Groopman, and P. Talalay Effects of glucosinolate-rich broccoli sprouts on urinary levels of aflatoxin-DNA adducts and phenanthrene tetraols in a randomized clinical trial in He Zuo township, Qidong, People's Republic of China Cancer Epidemiol. Biomarkers Prev 14 2005 2605 2613 (Pubitemid 41752722)
14. M.W. Farnham, K.K. Stephenson, and J.W. Fahey Glucoraphanin level in broccoli seed is largely determined by genotype Hortscience 40 2005 50 53 (Pubitemid 40177995)
15. Y. Zhang, P. Talalay, C.G. Cho, and G.H. Posner A major inducer of anticarcinogenic protective enzymes from broccoli: isolation and elucidation of structure Proc. Natl. Acad. Sci. USA 89 1992 2399 2403
16. D.J. Newman, and G.M. Cragg Marine natural products and related compounds in clinical and advanced preclinical trials J. Nat. Prod. 67 2004 1216 1238 (Pubitemid 39145623)
17. R. Montaser, and H. Luesch Marine natural products: a new wave of drugs? Future Med. Chem 3 2011 1475 1489
18. K. Taori, V.J. Paul, and H. Luesch Structure and activity of largazole, a potent antiproliferative agent from the Floridian marine cyanobacterium Symploca sp J. Am. Chem. Soc. 130 2008 1806 1807 (Pubitemid 351238618)
19. J. Hong, and H. Luesch Largazole: from discovery to broad-spectrum therapy Nat. Prod. Rep. 29 2012 449 456
20. Q.Y. Chen, Y. Liu, and H. Luesch Systematic chemical mutagenesis identifies a potent novel apratoxin A/E hybrid with improved in vivo antitumor activity ACS Med. Chem. Lett 2 2011 861 865
21. Y. Hoshiyama, T. Sekine, and T. Sasaba A case-control study of colorectal cancer and its relation to diet, cigarettes, and alcohol consumption in Saitama Prefecture, Japan Tohoku J. Exp. Med. 171 1993 153 165
22. Y. Hoshiyama, and T. Sasaba A case-control study of single and multiple stomach cancers in Saitama Prefecture, Japan Jpn. J. Cancer Res. 83 1992 937 943
23. Y.J. Surh Cancer chemoprevention with dietary phytochemicals Nat. Rev. Cancer 3 2003 768 780
24. X. Yan, Y. Chuda, M. Suzuki, and T. Nagata Fucoxanthin as the major antioxidant in Hijikia fusiformis, a common edible seaweed Biosci. Biotechnol. Biochem. 63 1999 605 607 (Pubitemid 129555518)
25. C.L. Liu, Y.T. Chiu, and M.L. Hu Fucoxanthin enhances HO-1 and NQO1 expression in murine hepatic BNL CL.2 cells through activation of the Nrf2/ARE system partially by its pro-oxidant activity J. Agric. Food Chem 59 2011 11344 11351
26. R. Wang, J.T. Kern, T.L. Goodfriend, D.L. Ball, and H. Luesch Activation of the antioxidant response element by specific oxidized metabolites of linoleic acid Prostaglandins Leukotrienes Essent. Fatty Acids 81 2009 53 59
27. W. Hur, Z. Sun, T. Jiang, D.E. Mason, E.C. Peters, D.D. Zhang, H. Luesch, P.G. Schultz, and N.S. Gray A small-molecule inducer of the antioxidant response element Chem. Biol. 17 2010 537 547
28. J.D. Moehlenkamp, and J.A. Johnson Activation of antioxidant/ electrophile-responsive elements in IMR-32 human neuroblastoma cells Arch. Biochem. Biophys. 363 1999 98 106 (Pubitemid 29394335)
29. S.K. Chanda, S. White, A.P. Orth, R. Reisdorph, L. Miraglia, R.S. Thomas, P. DeJesus, D.E. Mason, Q. Huang, R. Vega, D.H. Yu, C.G. Nelson, B.M. Smith, F.J. Terry, A.S. Linford, Y. Yu, G.W. Chirn, C. Song, M.A. Labow, D. Cohen, F.J. King, E.C. Peters, P.G. Schultz, P.K. Vogt, J.B. Hogenesch, and J.S. Caldwell Genome-scale functional profiling of the mammalian AP-1 signaling pathway Proc. Natl. Acad. Sci. USA 100 2003 12153 12158 (Pubitemid 37271530)
30. D.D. Zhang, and M. Hannink Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress Mol. Cell. Biol 23 2003 8137 8151 (Pubitemid 37377505)
31. D.A. Johnson, G.K. Andrews, W. Xu, and J.A. Johnson Activation of the antioxidant response element in primary cortical neuronal cultures derived from transgenic reporter mice J. Neurochem. 81 2002 1233 1241 (Pubitemid 34809257)
32. A.D. Kraft, D.A. Johnson, and J.A. Johnson Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult J. Neurosci 24 2004 1101 1112 (Pubitemid 38177017)
33. A. Fontana, G. d'Ippolito, A. Cutignano, G. Romano, N. Lamari, A. Massa Gallucci, G. Cimino, A. Miralto, and A. Ianora LOX-induced lipid peroxidation mechanism responsible for the detrimental effect of marine diatoms on zooplankton grazers ChemBioChem 8 2007 1810 1818 (Pubitemid 47612870)
34. B. Wang, and G. Williamson Transcriptional regulation of the human NAD(P)H:quinone oxidoreductase (NQO1) gene by monofunctional inducers Biochim. Biophys. Acta 1307 1996 104 110
35. G. Shen, W.S. Jeong, R. Hu, and A.N. Kong Regulation of Nrf2, NF-kappaB, and AP-1 signaling pathways by chemopreventive agents Antioxid. Redox Signaling 7 2005 1648 1663 (Pubitemid 41767999)
36. S.M. Deneke, and B.L. Fanburg Regulation of cellular glutathione Am. J. Physiol. 257 1989 L163 173
37. J.M. Lee, J.D. Moehlenkamp, J.M. Hanson, and J.A. Johnson Nrf2-dependent activation of the antioxidant responsive element by tert-butylhydroquinone is independent of oxidative stress in IMR-32 human neuroblastoma cells Biochem. Biophys. Res. Commun. 280 2001 286 292 (Pubitemid 32917509)
38. S. Bannai Transport of cystine and cysteine in mammalian cells Biochim. Biophys. Acta 779 1984 289 306 (Pubitemid 14027591)
39. K.A. Jung, and M.K. Kwak The Nrf2 system as a potential target for the development of indirect antioxidants Molecules 15 2010 7266 7291
40. H. Sasaki, H. Sato, K. Kuriyama-Matsumura, K. Sato, K. Maebara, H. Wang, M. Tamba, K. Itoh, M. Yamamoto, and S. Bannai Electrophile response element-mediated induction of the cystine/glutamate exchange transporter gene expression J. Biol. Chem. 277 2002 44765 44771 (Pubitemid 36159069)
41. J. Feng, P. Zhang, X. Chen, and G. He PI3K and ERK/Nrf2 pathways are involved in oleanolic acid-induced heme oxygenase-1 expression in rat vascular smooth muscle cells J. Cell. Biochem 112 2011 1524 1531
42. J.M. Lee, J.M. Hanson, W.A. Chu, and J.A. Johnson Phosphatidylinositol 3-kinase, not extracellular signal-regulated kinase, regulates activation of the antioxidant-responsive element in IMR-32 human neuroblastoma cells J. Biol. Chem. 276 2001 1 20016 2001
43. Y.J. Surh, J.K. Kundu, and H.K. Na Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals Planta Med 74 2008 1526 1539
44. H.K. Na, E.H. Kim, J.H. Jung, H.H. Lee, J.W. Hyun, and Y.J. Surh (-)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells Arch. Biochem. Biophys. 476 2008 171 177
45. L.M. Zipper, and R.T. Mulcahy Erk activation is required for Nrf2 nuclear localization during pyrrolidine dithiocarbamate induction of glutamate cysteine ligase modulatory gene expression in HepG2 cells Toxicol. Sci 73 2003 124 134 (Pubitemid 36609094)
46. M.S. Yates, M. Tauchi, F. Katsuoka, K.C. Flanders, K.T. Liby, T. Honda, G.W. Gribble, D.A. Johnson, J.A. Johnson, N.C. Burton, T.R. Guilarte, M. Yamamoto, M.B. Sporn, and T.W. Kensler Pharmacodynamic characterization of chemopreventive triterpenoids as exceptionally potent inducers of Nrf2-regulated genes Mol. Cancer Ther 6 2007 154 162 (Pubitemid 46206678)
47. T.H. Rushmore, and C.B. Pickett Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene: characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants J. Biol. Chem 265 1990 14648 14653
48. K. Itoh, T. Chiba, S. Takahashi, T. Ishii, K. Igarashi, Y. Katoh, T. Oyake, N. Hayashi, K. Satoh, I. Hatayama, M. Yamamoto, and Y. Nabeshima An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements Biochem. Biophys. Res. Commun. 236 1997 313 322 (Pubitemid 27373291)
49. P. Moi, K. Chan, I. Asunis, A. Cao, and Y.W. Kan Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region Proc. Natl. Acad. Sci. USA 91 1994 9926 9930 (Pubitemid 24311921)
50. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 13 1999 76 86 (Pubitemid 29045117)
51. W.S. Jeong, M. Jun, and A.N. Kong Nrf2: a potential molecular target for cancer chemoprevention by natural compounds Antioxid. Redox Signaling 8 2006 99 106 (Pubitemid 43324535)
52. R.J. Margret, S. Kumaresan, and S. Ravikumar A preliminary study on the anti-inflammatory activity of methanol extract of Ulva lactuca in rat J. Environ. Biol. 30 2009 899 902
53. Y.H. Chiu, Y.L. Chan, T.L. Li, and C.J. Wu Inhibition of Japanese encephalitis virus infection by the sulfated polysaccharide extracts from Ulva lactuca Mar. Biotechnol. (NY) 14 2012 468 478
54. A. Sathivel, H.R. Raghavendran, P. Srinivasan, and T. Devaki Anti-peroxidative and anti-hyperlipidemic nature of Ulva lactuca crude polysaccharide on D-galactosamine induced hepatitis in rats Food Chem. Toxicol 46 2008 3262 3267
55. P. Talalay, M.J. De Long, and H.J. Prochaska Identification of a common chemical signal regulating the induction of enzymes that protect against chemical carcinogenesis Proc. Natl. Acad. Sci. USA 85 1988 8261 8265
56. A.T. Dinkova-Kostova, M.A. Massiah, R.E. Bozak, R.J. Hicks, and P. Talalay Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups Proc. Natl. Acad. Sci. USA 98 2001 3404 3409 (Pubitemid 32220858)
57. C. Craig Kirk-Othmer Encyclopedia of Chemical Technology and Ullmann's Encyclopedia of Industrial Chemistry [Review] Issues Sci. Technol. Librarianship 46 2006 6-6
58. P.C. Calder, J.A. Bond, D.J. Harvey, S. Gordon, and E.A. Newsholme Uptake and incorporation of saturated and unsaturated fatty acids into macrophage lipids and their effect upon macrophage adhesion and phagocytosis Biochem. J. 269 1990 807 814 (Pubitemid 20236095)
59. R.K. Thimmulappa, K.H. Mai, S. Srisuma, T.W. Kensler, M. Yamamoto, and S. Biswal Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray Cancer Res. 62 2002 5196 5203 (Pubitemid 35033454)
60. E. Kansanen, H.K. Jyrkkanen, and A.L. Levonen Activation of stress signaling pathways by electrophilic oxidized and nitrated lipids Free Radic. Biol. Med. 52 2012 973 982
61. C. Kohle, and K.W. Bock Coordinate regulation of phase I and II xenobiotic metabolisms by the Ah receptor and Nrf2 Biochem. Pharmacol 73 2007 1853 1862 (Pubitemid 46677898)
62. W. Miao, L. Hu, P.J. Scrivens, and G. Batist Transcriptional regulation of NF-E2 p45-related factor (NRF2) expression by the aryl hydrocarbon receptor-xenobiotic response element signaling pathway: direct cross-talk between phase I and II drug-metabolizing enzymes J. Biol. Chem 280 2005 20340 20348 (Pubitemid 40776732)
63. L.G. Gillingham, S. Harris-Janz, and P.J. Jones Dietary monounsaturated fatty acids are protective against metabolic syndrome and cardiovascular disease risk factors Lipids 46 2011 209 228
64. M.Y. Abeywardena, and G.S. Patten Role of ω3 long-chain polyunsaturated fatty acids in reducing cardio-metabolic risk factors Endocr. Metab. Immune Disord. Drug Targets 11 2011 232 246