Antrodia salmonea inhibits TNF-α-induced angiogenesis and atherogenesis in human endothelial cells through the down-regulation of NF-κB and up-regulation of Nrf2 signaling pathways

Journal of Ethnopharmacology

Volumn 151, Issue 1, 2014, Pages 394-406

  Yang, Hsin Ling ^a   Chang, Hebron C ^b   Lin, Shu Wei ^a   Senthil Kumar, K J ^a   Liao, Chun Huei ^a   Wang, Hui Min ^c   Lin, Kai Yuan ^d   Hseu, You Cheng ^a,b  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b ASIA UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d CHI MEI MEDICAL CENTER   (Taiwan)

Author keywords

Antrodia salmonea; EA.hy 926 cells; HO 1; NF B; Nrf2; TNF

Indexed keywords

GAMMA GLUTAMYLCYSTEINE; GELATINASE B; HEME OXYGENASE 1; I KAPPA B; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NF E2; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; ANTIOXIDANT RESPONSIVE ELEMENT; ANTRODIA; ANTRODIA SALMONEA; ARTICLE; ATHEROGENESIS; CELL ADHESION; CELL INVASION; CELL MIGRATION; CELL STRUCTURE; CELL SURFACE; CELL VIABILITY; COLORIMETRY; CONTROLLED STUDY; DNA STRUCTURE; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING; ZYMOGRAPHY;

ANTRODIA SALMONEA;

ANTIOXIDANT RESPONSE ELEMENT; ANTRODIA SALMONEA; ARE; AS; DMEM; DULBECCO'S MODIFIED EAGLE'S MEDIUM; EA.HY 926 CELLS; FBS; FETAL BOVINE SERUM; FITC; FLUORESCEIN ISOTHIOCYANATE; GLUTATHIONE; GSH; HEMEOXYGENASE-1; HO-1; I-ΚB; I-ΚB KINASE-Α; ICAM-1; IKKΑ; INHIBITOR-ΚB; INTERCELLULAR ADHESION MOLECULE-1; MATRIX METALLOPROTEINASE-9; MMP-9; NF-ΚB; NRF2; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; NUCLEAR FACTOR-ΚB; PBS; PHOSPHATE BUFFER SALINE; TNF-Α; TUMOR NECROSIS FACTOR-Α; Γ-GCLC; Γ-GLUTAMYLCYSTEINE SYNTHETASE;

ANTRODIA; ATHEROSCLEROSIS; CELL ADHESION; CELL SURVIVAL; DOWN-REGULATION; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; GLUTAMATE-CYSTEINE LIGASE; HEME OXYGENASE-1; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MATRIX METALLOPROTEINASE 9; NEOVASCULARIZATION, PHYSIOLOGIC; NF-E2-RELATED FACTOR 2; NF-KAPPA B; TUMOR NECROSIS FACTOR-ALPHA; U937 CELLS; UP-REGULATION;

EID: 84891487344     PISSN: 03788741     EISSN: 18727573     Source Type: Journal    
DOI: 10.1016/j.jep.2013.10.052     Document Type: Article

References (54)

1. N.G. Abraham, and A. Kappas Pharmacological and clinical aspects of heme oxygenase Pharmacol. Rev. 60 2008 79 127
2. J. Bauer, M. Margolis, C. Schreiner, C.J. Edgell, J. Azizkhan, E. Lazarowski, and R.L. Juliano In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression, G-proteins, and integrins J. Cell. Physiol. 153 1992 437 449
3. S. Blankenberg, S. Barbaux, and L. Tiret Adhesion molecules and atherosclerosis Atherosclerosis 170 2003 191 203
4. N. Brandes, S. Schmitt, and U. Jakob Thiol-based redox switches in eukaryotic proteins Antioxid. Redox Signal. 11 2009 997 1014
5. X.L. Chen, G. Dodd, S. Thomas, X. Zhang, M.A. Wasserman, B.H. Rovin, and C. Kunsch Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression Am. J. Physiol. Heart Circ. Physiol. 290 2006 H1862 1870
6. R. De Martin, M. Hoeth, R. Hofer-Warbinek, and J.A. Schmid The transcription factor NF-kappa B and the regulation of vascular cell function Arterioscler. Thromb. Vasc. Biol. 20 2000 E83 88
7. E.I. Deryugina, and J.P. Quigley Matrix metalloproteinases and tumor metastasis Cancer Metastasis Rev. 25 2006 9 34
8. D.A. Dickinson, and H.J. Forman Cellular glutathione and thiols metabolism Biochem. Pharmacol. 64 2002 1019 1026
9. E.O. Farombi, and Y.J. Surh Heme oxygenase-1 as a potential therapeutic target for hepatoprotection J. Biochem. Mol. Biol. 39 2006 479 491
10. A.W. Griffioen, and G. Molema Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation Pharmacol. Rev. 52 2000 237 268
11. G.J. Hannon, and J.J. Rossi Unlocking the potential of the human genome with RNA interference Nature 431 2004 371 378
12. F. Hillen, and A.W. Griffioen Tumour vascularization: sprouting angiogenesis and beyond Cancer Metastasis Rev. 26 2007 489 502
13. A. Hoeben, B. Landuyt, M.S. Highley, H. Wildiers, A.T. Van Oosterom, and E.A. De Bruijn Vascular endothelial growth factor and angiogenesis Pharmacol. Rev. 56 2004 549 580
14. Y.C. Hseu, S.C. Chen, W.H. Lin, D.Z. Hung, M.K. Lin, Y.H. Kuo, M.T. Wang, H.J. Cho, L. Wang, and H.L. Yang Toona sinensis (leaf extracts) inhibit vascular endothelial growth factor (VEGF)-induced angiogenesis in vascular endothelial cells J. Ethnopharmacol. 134 2011 111 121
15. Y.C. Hseu, C.W. Chou, K.J. Senthil Kumar, K.T. Fu, H.M. Wang, L.S. Hsu, Y.H. Kuo, C.R. Wu, S.C. Chen, and H.L. Yang Ellagic acid protects human keratinocyte (HaCaT) cells against UVA-induced oxidative stress and apoptosis through the upregulation of the HO-1 and Nrf-2 antioxidant genes Food Chem. Toxicol. 50 2012 1245 1255
16. Y.C. Hseu, C.R. Wu, H.W. Chang, K.J. Kumar, M.K. Lin, C.S. Chen, H.J. Cho, C.Y. Huang, C.Y. Huang, H.Z. Lee, W.T. Hsieh, J.G. Chung, H.M. Wang, and H.L. Yang Inhibitory effects of Physalis angulata on tumor metastasis and angiogenesis J. Ethnopharmacol. 135 2011 762 771
17. Hseu, Y.C., Lee, C.C., Chen, Y.C., Kumar, K.J.S., Chen, C.S., Tsai, C.T., Huang, H.C., Yang, H.L. Antrodia salmonea in submerged culture exhibits antioxidant activity in vitro and protected human erythrocytes and low-density lipoprotein from oxidative modification. Food Chem. Toxicol., in press.
18. G.J. Huang, C.H. Pan, F.C. Liu, T.S. Wu, and C.H. Wu Anti-inflammatory effects of ethanolic extract of Antrodia salmonea in the lipopolysaccharide- stimulated RAW246.7 macrophages and he lambda-carrageenan-induced paw edema model Food Chem. Toxicol. 50 2012 1485 1493
19. H. Kamencic, A. Lyon, P.G. Paterson, and B.H. Juurlink Monochlorobimane fluorometric method to measure tissue glutathione Anal. Biochem. 286 2000 35 37
20. K. Kessenbrock, V. Plaks, and Z. Werb Matrix metalloproteinases: regulators of the tumor microenvironment Cell 141 2010 52 67
21. K.S. Kim, H.M. Choi, Y.A. Lee, I.A. Choi, S.H. Lee, S.J. Hong, H.I. Yang, and M.C. Yoo Expression levels and association of gelatinases MMP-2 and MMP-9 and collagenases MMP-1 and MMP-13 with VEGF in synovial fluid of patients with arthritis Rheumatol. Int. 31 2011 543 547
22. Y.S. Kim, Y. Ahn, M.H. Hong, K.H. Kim, H.W. Park, Y.J. Hong, J.H. Kim, W. Kim, M.H. Jeong, J.G. Cho, J.C. Park, and J.C. Kang Rosuvastatin suppresses the inflammatory responses through inhibition of c-Jun N-terminal kinase and Nuclear Factor-kappaB in endothelial cells J. Cardiovasc. Pharmacol. 49 2007 376 383
23. J.K. Kundu, and Y.J. Surh Breaking the relay in deregulated cellular signal transduction as a rationale for chemoprevention with anti-inflammatory phytochemicals Mutat. Res. 591 2005 123 146
24. L. Lamalice, F. Le Boeuf, and J. Huot Endothelial cell migration during angiogenesis Circ. Res. 100 2007 782 794
25. W. Li, T.O. Khor, C. Xu, G. Shen, W.S. Jeong, S. Yu, and A.N. Kong Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis Biochem. Pharmacol. 76 2008 1485 1489
26. P. Libby Inflammation in atherosclerosis Arterioscler. Thromb. Vasc. Biol. 32 2012 2045 2051
27. G. Liuzzo, G. Giubilato, and M. Pinnelli T cells and cytokines in atherogenesis Lupus 14 2005 732 735
28. V. Lobo, A. Patil, A. Phatak, and N. Chandra Free radicals, antioxidants and functional foods: Impact on human health Pharmacogn. Rev. 4 2010 118 126
29. J. Lu, K. Zhang, S. Nam, R.A. Anderson, R. Jove, and W. Wen Novel angiogenesis inhibitory activity in cinnamon extract blocks VEGFR2 kinase and downstream signaling Carcinogenesis 31 2010 481 488
30. A. Matsuda, K. Orihara, S. Fukuda, H. Fujinaga, K. Matsumoto, and H. Saito Corticosteroid enhances TNF-alpha-mediated leukocyte adhesion to pulmonary microvascular endothelial cells Allergy 63 2008 1610 1616
31. M. Muller, A. Banning, R. Brigelius-Flohe, and A. Kipp Nrf2 target genes are induced under marginal selenium-deficiency Genes Nutr. 5 2010 297 307
32. M.N. Nakatsu, R.C. Sainson, J.N. Aoto, K.L. Taylor, M. Aitkenhead, S. Perez-del-Pulgar, P.M. Carpenter, and C.C. Hughes Angiogenic sprouting and capillary lumen formation modeled by human umbilical vein endothelial cells (HUVEC) in fibrin gels: the role of fibroblasts and Angiopoietin-1 Microvasc. Res. 66 2003 102 112
33. B.A. Narayanan, N.K. Narayanan, L. Davis, and D. Nargi RNA interference-mediated cyclooxygenase-2 inhibition prevents prostate cancer cell growth and induces differentiation: modulation of neuronal protein synaptophysin, cyclin D1, and androgen receptor Mol. Cancer Ther. 5 2006 1117 1125
34. B. Osterud, and E. Bjorklid Role of monocytes in atherogenesis Physiol. Rev. 83 2003 1069 1112
35. H.O. Pae, Y.C. Lee, and H.T. Chung Heme oxygenase-1 and carbon monoxide: emerging therapeutic targets in inflammation and allergy Recent Patents on Inflamm. Allergy Drug Discov. 2 2008 159 165
36. M. Papetti, and I.M. Herman Mechanisms of normal and tumor-derived angiogenesis Am. J. Physiol. Cell Physiol. 282 2002 C947 970
37. S.W. Ryter, L.E. Otterbein, D. Morse, and A.M. Choi Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance Mol. Cell. Biochem. 234-235 2002 249 263
38. M. Sasaki, D. Ostanin, J.W. Elrod, T. Oshima, P. Jordan, M. Itoh, T. Joh, A. Minagar, and J.S. Alexander TNF-alpha-induced endothelial cell adhesion molecule expression is cytochrome P-450 monooxygenase dependent Am. J. Physiol. Cell Physiol. 284 2003 C422 428
39. C.C. Shen, Y.C. Shen, Y.H. Wang, L.C. Lin, M.J. Don, K.T. Liou, W.Y. Wang, Y.C. Hou, and T.T. Chang New lanostanes and naphthoquinones isolated from Antrodia salmonea and their antioxidative burst activity in human leukocytes Planta Med. 72 2006 199 203
40. C.C. Shen, Y.H. Wang, T.T. Chang, L.C. Lin, M.J. Don, Y.C. Hou, K.T. Liou, S. Chang, W.Y. Wang, H.C. Ko, and Y.C. Shen Anti-inflammatory ergostanes from the basidiomata of Antrodia salmonea Planta Med. 73 2007 1208 1213
41. C.C. Shen, C.F. Lin, Y.L. Huang, S.T. Wan, C.C. Chen, S.J. Sheu, Y.C. Lin, and C.C. Chen Bioactive components from the mycelium of Antrodia salmonea J. Chin. Chem. Soc. 55 2008 854 857
42. R.B. Singh, S.A. Mengi, Y.J. Xu, A.S. Arneja, and N.S. Dhalla Pathogenesis of atherosclerosis: a multifactorial process Exp. Clin. Cardiol. 7 2002 40 53
43. M.P. Soares, M.P. Seldon, I.P. Gregoire, T. Vassilevskaia, P.O. Berberat, J. Yu, T.Y. Tsui, and F.H. Bach Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation J. Immunol. 172 2004 3553 3563
44. A.H. Sprague, and R.A. Khalil Inflammatory cytokines in vascular dysfunction and vascular disease Biochem. Pharmacol. 78 2009 539 552
45. Y.J. Surh Cancer chemoprevention with dietary phytochemicals Nat. Rev. Cancer 3 2003 768 780
46. Y.J. Surh, J.K. Kundu, H.K. Na, and J.S. Lee Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals J. Nutr. 135 2005 2993S 3001S
47. T. Takahashi, H. Shimizu, H. Morimatsu, K. Maeshima, K. Inoue, R. Akagi, M. Matsumi, H. Katayama, and K. Morita Heme oxygenase-1 is an essential cytoprotective component in oxidative tissue injury induced by hemorrhagic shock J. Clin. Biochem. Nutr. 44 2009 28 40
48. D.M. Townsend, K.D. Tew, and H. Tapiero The importance of glutathione in human disease Biomed. Pharmacother. 57 2003 145 155
49. Z.T. Tsai, and S.L. Liaw The Use and the Effect of Ganoderma 1985 San Yun Press Taichung, Taiwan
50. Z. Ungvari, Z. Bagi, A. Feher, F.A. Recchia, W.E. Sonntag, K. Pearson, R. de Cabo, and A. Csiszar Resveratrol confers endothelial protection via activation of the antioxidant transcription factor Nrf2 Am. J. Physiol. Heart Circ. Physiol. 299 2010 H18 24
51. M. Ushio-Fukai Redox signaling in angiogenesis: role of NADPH oxidase Cardiovasc. Res. 71 2006 226 235
52. J. Wels, R.N. Kaplan, S. Rafii, and D. Lyden Migratory neighbors and distant invaders: tumor-associated niche cells Genes Dev. 22 2008 559 574
53. D.D. Zhang Mechanistic studies of the Nrf2-Keap1 signaling pathway Drug Metab. Rev. 38 2006 769 789
54. W.J. Zhang, and B. Frei Alpha-lipoic acid inhibits TNF-alpha-induced NF-kappaB activation and adhesion molecule expression in human aortic endothelial cells FASEB J. 15 2001 2423 2432