Caffeoylglycolic acid methyl ester, a major constituent of sorghum, exhibits anti-inflammatory activity via the Nrf2/heme oxygenase-1 pathway

RSC Advances

Volumn 5, Issue 23, 2015, Pages 17786-17796

  Choo, Young Yeon ^a   Lee, Suhyun ^a   Nguyen, Phi Hung ^b   Lee, Wanju ^a   Woo, Mi Hee ^b   Min, Byung Sun ^b   Lee, Jeong Hyung ^a  

^a Kangwon National University   (South Korea)

^b Catholic University of Daegu   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ESTERIFICATION; ESTERS; NITRIC OXIDE;

ANTI-INFLAMMATORIES; ANTI-INFLAMMATORY ACTIVITY; ANTI-INFLAMMATORY EFFECTS; INDUCIBLE NITRIC OXIDE SYNTHASE (INOS); INFLAMMATORY DISEASE; INHIBITORY EFFECT; LIPOPOLYSACCHARIDES; NUCLEAR TRANSLOCATIONS;

IMMUNOLOGY;

EID: 84923205489     PISSN: None     EISSN: 20462069     Source Type: Journal    
DOI: 10.1039/c4ra13847c     Document Type: Article

References (50)

1. D. L. Laskin V. R. Sunil C. R. Gardner J. D. Laskin Macrophages and tissue injury: agents of defense or destruction? Annu. Rev. Pharmacol. Toxicol. 2011 51 267 288
2. T. Lawrence D. A. Willoughby D. W. Gilroy Anti-inflammatory lipid mediators and insights into the resolution of inflammation Nat. Rev. Immunol. 2002 2 787 795
3. M. D. Maines N. Panahian The heme oxygenase system and cellular defense mechanisms. Do HO-1 and HO-2 have different functions? Adv. Exp. Med. Biol. 2001 502 249 272
4. N. G. Abraham A. Kappas Pharmacological and clinical aspects heme oxygenase Pharmacol. Rev. 2008 60 79 127
5. D. Morse L. Lin A. M. Choi S. W. Ryter Heme oxygenase-1, a critical arbitrator of cell death pathways in lung injury and disease Free Radical Biol. Med. 2009 47 1 12
6. A. Paine B. Eiz-Vesper R. Blasczyk S. Immenschuh Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential Biochem. Pharmacol. 2010 80 1895 1903
7. L. E. Otterbein L. L. Mantell A. M. Choi Carbon monoxide provides protection against hyperoxic lung injury Am. J. Physiol. 1999 276 L688 L694
8. S. W. Ryter J. Alam A. M. Choi Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications Pharmacol. Rev. 2006 86 583 650
9. D. Morse S. E. Pischke Z. Zhou R. J. Davis R. A. Flavell T. Loop Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1 J. Biol. Chem. 2003 278 36993 36998
10. G. Y. Suh Y. Jin A. K. Yi X. M. Wang A. M. Choi CCAAT/enhancer-binding protein mediates carbon monoxide-induced suppression of cyclooxygenase-2 Am. J. Respir. Cell Mol. Biol. 2006 35 220 226
11. K. Nakahira H. P. Kim X. H. Geng A. Nakao X. Wang N. Murase P. F. Drain X. Wang M. Sasidhar E. G. Nabel T. Takahashi N. W. Lukacs S. W. Ryter K. Morita A. M. Choi Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts J. Exp. Med. 2006 203 2377 2389
12. X. M. Wang H. P. Kim K. Nakahira S. W. Ryter A. M. Choi The heme oxygenase-1/carbon monoxide pathway suppresses TLR4 signaling by regulating the interaction of TLR4 with caveolin-1 J. Immunol. 2009 182 3809 3818
13. R. Furst S. B. Blumenthal A. K. Kiemer S. Zahler A. M. Vollmar Nuclear factor-κB-independent anti-inflammatory action of salicylate in human endothelial cells: induction of heme oxygenase-1 by the c-jun N-terminal kinase/activator protein-1 pathway J. Pharmacol. Exp. Ther. 2006 318 389 394
14. F. Gueler J. K. Park S. Rong T. Kirsch C. Lindschau W. Zheng M. Elger A. Fiebeler D. Fliser F. C. Luft H. Haller Statins attenuate ischemia-reperfusion injury by inducing heme oxygenase-1 in infiltrating macrophages Am. J. Pathol. 2007 170 1192 1199
15. K. S. Helmer J. W. Suliburk D. W. Mercer Ketamine-induced gastroprotection during endotoxemia: role of heme-oxygenase-1 Dig. Dis. Sci. 2006 51 1571 1581
16. H. J. Kwak J. S. Song Z. S. No J. H. Song S. D. Yang H. G. Cheon The inhibitory effects of roflumilast on lipopolysaccharide-induced nitric oxide production in RAW264.7 cells are mediated by hemeoxygenase-1 and its product carbon monoxide Inflammation Res. 2005 54 508 513
17. R. Motterlini R. Foresti Heme oxygenase-1 as a target for drug discovery Antioxid. Redox Signaling 2014 20 1810 1826
18. P. H. Nguyen B. T. Zhao J. H. Lee Y. H. Kim B. S. Min M. H. Woo Isolation of benzoic and cinnamic acid derivatives from the grains of Sorghum bicolor and their inhibition of lipopolysaccharide-induced nitric oxide production in RAW 264.7 cells Food Chem. 2015 168 512 519
19. M. Saleem H. J. Kim C. B Jin Y. S. Lee Antioxidant caffeic acid derivatives from leaves of Parthenocissus tricuspidata Arch. Pharmacal Res. 2004 27 300 304
20. S. U. Lee C. G. Shin C. K. Lee Y. S. Lee Caffeoylglycolic and caffeoylamino acid derivatives, halfmers of l-chicoric acid, as new HIV-1 integrase inhibitors Eur. J. Med. Chem. 2007 42 1309 1315
21. J. Alam D. Stewart C. Touchard S. Boinapally A. M. Choi J. L. Cook Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene J. Biol. Chem. 1999 274 26071 26078
22. J. M. Awika L. W. Rooney Sorghum phytochemicals and their potential impact on human health Phytochemistry 2004 65 1199 1221
23. L. Svensson B. Sekwati-Manang D. L. Lutz A. Schieber M. G. Ganzle Phenolic acids and flavonoids in nonfermented and fermented red sorghum (Sorghum bicolor (L.) Moench) J. Agric. Food Chem. 2010 58 9214 9220
24. K. F. Benson J. L. Beaman B. Ou A. Okubena O. Okubena G. S. Jensen West African Sorghum bicolor leaf sheaths have anti-inflammatory and immune-modulating properties in vitro J. Med. Food 2013 16 230 238
25. A. Burdette P. L. Garner E. P. Mayer J. L. Hargrove D. K. Hartle P. Greenspan Anti-inflammatory activity of select Sorghum (Sorghum bicolor) brans J. Med. Food 2004 13 879 887
26. H. Abuarqoub R. Foresti C. Green R. Motterlini Heme oxygenase-1 mediates the anti-inflammatory actions of 2′-hydroxychalcone in RAW 264.7 murine macrophages Am. J. Physiol.: Cell Physiol. 2006 290 C1092 C1099
27. S. H. Juan T. H. Cheng H. C. Lin Y. L. Chu W. S. Lee Mechanism of concentration-dependent induction of heme oxygenase-1 by resveratrol in human aortic smooth muscle cells Biochem. Pharmacol. 2004 69 41 48
28. S. Lee J. Seo S. Ryoo T. D. Cuong B. S. Min J. H. Lee Malabaricone C inhibits PDGF-induced proliferation and migration of aortic smooth muscle cells through induction of heme oxygenase-1 J. Cell. Biochem. 2012 133 2866 2876
29. R. Motterlini R. Foresti R. Bassi C. J. Green Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress Free Radical Biol. Med. 2000 28 1303 1312
30. J. L. Ríos M. C. Recio J. M. Escandell I. Andújar Inhibition of transcription factors by plant-derived compounds and their implications in inflammation and cancer Curr. Pharm. Des. 2009 15 1212 1237
31. C. Y. Chen J. H. Jang M. H. Li Y. J. Surh Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells Biochem. Biophys. Res. Commun. 2005 331 993 1000
32. H. Y. Hsu L. C. Chu K. F. Hua L. K. Chao Heme oxygenase-1 mediates the anti-inflammatory effect of curcumin within LPS-stimulated human monocytes J. Cell. Physiol. 2008 215 603 612
33. M. C. Jaramillo D. D. Zhang The emerging role of the Nrf2-Keap1 signaling pathway in cancer Genes Dev. 2013 27 2179 2191
34. H. Y. Cho S. P. Reddy S. R. Kleeberger Nrf2 defends the lung from oxidative stress Antioxid. Redox Signaling 2006 8 76 87
35. K. Itoh N. Wakabayashi Y. Katoh T. Ishii K. Igarashi J. D. Engel M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev. 1999 13 76 86
36. L. E. Otterbein F. H. Bach J. Alam M. Soares H. Tao Lu M. Wysk R. J. Davis R. A. Flavell A. M. Choi Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway Nat. Med. 2003 6 422 428
37. D. Martin A. I. Rojo M. Salinas R. Diaz G. Gallardo J. Alam C. M. De Galarreta A. Cuadrado Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/AKT pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol J. Biol. Chem. 2004 279 8919 8929
38. S. Lee J. Seo S. Ryoo T. D. Cuong B. S. Min H. J. Lee Malabaricone C inhibits PDGF-induced proliferation and migration of aortic smooth muscle cells through induction of heme oxygenase-1 J. Cell. Biochem. 2012 113 2866 2876
39. S. Makabe Y. Takahashi H. Watanabe M. Murakami T. Ohba H. Ito Fluvastatin protects vascular smooth muscle cells against oxidative stress through the Nrf2-dependent antioxidant pathway Atherosclerosis 2010 213 377 384
40. C. C. Wu C. W. Hsieh P. H. Lai J. B. Lin Y. C. Liu B. S. Wung Upregulation of endothelial heme oxygenase-1 expression through the activation of the JNK pathway by sublethal concentrations of acrolein Toxicol. Appl. Pharmacol. 2006 214 244 252
41. T. W. Kensler N. Wakabayashi S. Biswal Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway Annu. Rev. Pharmacol. Toxicol. 2007 47 89 116
42. A. Lau N. F. Villeneuve Z. Sun P. K. Wong D. D. Zhang Dual roles of Nrf2 in cancer Pharmacol. Res. 2008 58 262 270
43. G. E. Mann B. Bonacasa T. Ishii R. C. Siow Targeting the redox sensitive Nrf2-Keap1defense pathway in cardiovascular disease: protection afforded by dietary isoflavones Curr. Opin. Pharmacol. 2009 9 139 145
44. A. Alfieri S. Srivastava R. C. Siow M. Modo P. A. Fraser G. E. Mann Targeting the Nrf2-Keap1 antioxidant defense pathway for neurovascular protection in stroke J. Physiol. 2008 589 4125 4136
45. L. H. Kushi K. A. Meyer D. R. Jacobs Cereals, legumes, and chronic disease risk reduction: evidence from epidemiologic studies Am. J. Clin. Nutr. 1999 70 suppl. 451S 458S
46. J. L. Slavin D. Jacobs L. Marquart Grain processing and nutrition Crit. Rev. Food Sci. Nutr. 2000 40 309 326
47. S. J. Van Rensburg Epidemiological and dietary evidence for a specific nutritional predisposition to esophageal cancer J. Natl. Cancer Inst. 1981 67 243 251
48. M. T. Mitjavila J. J. Moreno The effects of polyphenols on oxidative stress and the arachidonic acid cascade. Implications for the prevention/treatment of high prevalence diseases Biochem. Pharmacol. 2012 84 1113 1122
49. D. Kluth A. Banning I. Paur R. Blomhoff R. Brigelius-Flohe Modulation of pregnane X receptor- and electrophile responsive element-mediated gene expression by dietary polyphenolic compounds Free Radical Biol. Med. 2007 42 315 325
50. Z. Ungvari Z. Bagi A. Feher F. A. Recchia W. E. Sonntag K. Pearson R. de Cabo A. Csiszar Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2 Am. J. Physiol.: Heart Circ. Physiol. 2010 299 H18 H24