Honokiol inhibits TNF-α-stimulated NF-κB activation and NF-κB-regulated gene expression through suppression of IKK activation

Biochemical Pharmacology

Volumn 70, Issue 10, 2005, Pages 1443-1457

  Tse, Anfernee Kai Wing ^a   Wan, Chi Keung ^a   Shen, Xiao Ling ^a   Yang, Mengsu ^a   Fong, Wang Fun ^a  

^a CITY UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Cell signaling; Honokiol; I B; IKK; NF B; TNF

Indexed keywords

GELATINASE B; GENE PRODUCT; HONOKIOL; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; LUCIFERASE; MONOCYTE CHEMOTACTIC PROTEIN 1; SYNAPTOTAGMIN; TUMOR NECROSIS FACTOR ALPHA;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; DNA BINDING; ENZYME ACTIVATION; ENZYME ASSAY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; METASTASIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STIMULATION; UPREGULATION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BIPHENYL COMPOUNDS; CELL LINE, TUMOR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENES, REPORTER; HUMANS; I-KAPPA B KINASE; LIGNANS; LIPOPOLYSACCHARIDES; LUCIFERASES; LYMPHOTOXIN-ALPHA; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 26944444312     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2005.08.011     Document Type: Article

References (76)

1. R. Sen, and D. Baltimore Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism Cell 47 1986 921 928
2. A. Garg, and B.B. Aggarwal Nuclear transcription factor-kappaB as a target for cancer drug development Leukemia 16 2002 1053 1068
3. F.R. Greten, L. Eckmann, T.F. Greten, J.M. Park, Z.W. Li, and L.J. Egan IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer Cell 118 2004 285 296
4. E. Pikarsky, R.M. Porat, I. Stein, R. Abramovitch, S. Amit, and S. Kasem NF-kappaB functions as a tumour promoter in inflammation-associated cancer Nature 431 2004 461 466
5. J. Adams The proteasome: a suitable antineoplastic target Nat Rev Cancer 4 2004 349 360
6. A.S. Baldwin Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB J Clin Invest 107 2001 241 246
7. Y. Yamamoto, and R.B. Gaynor Therapeutic potential of inhibition of the NF-kappaB pathway in the treatment of inflammation and cancer J Clin Invest 107 2001 135 142
8. P.K. Farmer, X. He, M.L. Schmitz, J. Rubin, and M.S. Nanes Inhibitory effect of NF-kappaB on 1,25-dihydroxyvitamin D(3) and retinoid X receptor function Am J Physiol Endocrinol Metab 279 2000 E213 E220
9. X. Lu, P. Farmer, J. Rubin, and M.S. Nanes Integration of the NfkappaB p65 subunit into the vitamin D receptor transcriptional complex: identification of p65 domains that inhibit 1,25-dihydroxyvitamin D3-stimulated transcription J Cell Biochem 92 2004 833 848
10. A.S. Baldwin Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights Annu Rev Immunol 14 1996 649 683
11. M. Karin, and Y. Ben-Neriah Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity Annu Rev Immunol 18 2000 621 663
12. X. Bai, F. Cerimele, M. Ushio-Fukai, M. Waqas, P.M. Campbell, and B. Govindarajan Honokiol, a small molecular weight natural product, inhibits angiogenesis in vitro and tumor growth in vivo J Biol Chem 278 2003 35501 35507
13. H. Nagase, K. Ikeda, and Y. Sakai Inhibitory effect of magnolol and honokiol from Magnolia obovata on human fibrosarcoma HT-1080. Invasiveness in vitro Planta Med 67 2001 705 708
14. T. Hirano, M. Gotoh, and K. Oka Natural flavonoids and lignans are potent cytostatic agents against human leukemic HL-60 cells Life Sci 55 1994 1061 1069
15. H. Hibasami, Y. Achiwa, H. Katsuzaki, K. Imai, K. Yoshioka, and K. Nakanishi Honokiol induces apoptosis in human lymphoid leukemia Molt 4B cells Int J Mol Med 2 1998 671 673
16. T.E. Battle, J. Arbiser, and D.A. Frank The natural product honokiol induces caspase-dependent apoptosis in B-cell chronic lymphocytic leukemia (B-CLL) cells Blood 106 2005 690 697
17. Ishitsuka K, Hideshima T, Hamasaki M, Raje N, Kumar S, Hideshima H, et al. Honokiol overcomes conventional drug resistance in human multiple myeloma by induction of caspase-dependent and independent apoptosis. Blood 2005; in press.
18. S.E. Yang, M.T. Hsieh, T.H. Tsai, and S.L. Hsu Down-modulation of Bcl-XL, release of cytochrome c and sequential activation of caspases during honokiol-induced apoptosis in human squamous lung cancer CH27 cells Biochem Pharmacol 63 2002 1641 1651
19. F. Chen, T. Wang, Y.F. Wu, Y. Gu, X.L. Xu, and S. Zheng Honokiol: a potent chemotherapy candidate for human colorectal carcinoma World J Gastroenterol 10 2004 3459 3463
20. T. Wang, F. Chen, Z. Chen, Y.F. Wu, X.L. Xu, and S. Zheng Honokiol induces apoptosis through p53-independent pathway in human colorectal cell line RKO World J Gastroenterol 10 2004 2205 2208
21. Z.L. Kong, S.C. Tzeng, and Y.C. Liu Cytotoxic neolignans: an SAR study Bioorg Med Chem Lett 15 2005 163 166
22. E.J. Park, Y.Z. Zhao, Y.H. Kim, B.H. Lee, and D.H. Sohn Honokiol induces apoptosis via cytochrome c release and caspase activation in activated rat hepatic stellate cells in vitro Planta Med 71 2005 82 84
23. W.F. Fong, A.K. Tse, K.H. Poon, and C. Wang Magnolol and honokiol enhance HL-60 human leukemia cell differentiation induced by 1,25-dihydroxyvitamin D3 and retinoic acid Int J Biochem Cell Biol 37 2005 427 441
24. M.M. Chaturvedi, A. Mukhopadhyay, and B.B. Aggarwal Assay for redox-sensitive transcription factor Methods Enzymol 319 2000 585 602
25. S. Sun, J. Elwood, and W.C. Greene Both amino- and carboxyl-terminal sequences within I kappa B alpha regulate its inducible degradation Mol Cell Biol 16 1996 1058 1065
26. F. Mercurio, H. Zhu, B.W. Murray, A. Shevchenko, B.L. Bennett, and J. Li IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation Science 278 1997 860 866
27. A.J. McGahon, S.J. Martin, R.P. Bissonnette, A. Mahboubi, Y. Shi, and R.J. Mogil The end of the (cell) line: methods for the study of apoptosis in vitro Methods Cell Biol 46 1995 153 185
28. M.S. Hayden, and S. Ghosh Signaling to NF-kappaB Genes Dev 18 2004 2195 2224
29. H.P. Hohmann, R. Remy, B. Poschl, and A.P. van Loon Tumor necrosis factors-alpha and -beta bind to the same two types of tumor necrosis factor receptors and maximally activate the transcription factor NF-kappa B at low receptor occupancy and within minutes after receptor binding J Biol Chem 265 1990 15183 15188
30. M.M. Chaturvedi, R. LaPushin, and B.B. Aggarwal Tumor necrosis factor and lymphotoxin. Qualitative and quantitative differences in the mediation of early and late cellular response J Biol Chem 269 1994 14575 14583
31. M. Higuchi, and B.B. Aggarwal Modulation of two forms of tumor necrosis factor receptors and their cellular response by soluble receptors and their monoclonal antibodies J Biol Chem 267 1992 20892 20899
32. K. Natarajan, S. Singh, T.R. Burke Jr., D. Grunberger, and B.B. Aggarwal Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B Proc Natl Acad Sci USA 93 1996 9090 9095
33. V. Haridas, C.J. Arntzen, and J.U. Gutterman Avicins, a family of triterpenoid saponins from Acacia victoriae (Bentham), inhibit activation of nuclear factor-kappaB by inhibiting both its nuclear localization and ability to bind DNA Proc Natl Acad Sci USA 98 2001 11557 11562
34. Y.F. Xia, B.Q. Ye, Y.D. Li, J.G. Wang, X.J. He, and X. Lin Andrographolide attenuates inflammation by inhibition of NF-kappa B activation through covalent modification of reduced cysteine 62 of p50 J Immunol 173 2004 4207 4217
35. T. Henkel, T. Machleidt, I. Alkalay, M. Kronke, Y. Ben-Neriah, and P.A. Baeuerle Rapid proteolysis of I kappa B-alpha is necessary for activation of transcription factor NF-kappa B Nature 365 1993 182 185
36. S.C. Sun, P.A. Ganchi, D.W. Ballard, and W.C. Greene NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway Science 259 1993 1912 1915
37. V.J. Palombella, O.J. Rando, A.L. Goldberg, and T. Maniatis The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B Cell 78 1994 773 785
38. E. Zandi, D.M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation Cell 91 1997 243 252
39. L. Ling, Z. Cao, and D.V. Goeddel NF-kappaB-inducing kinase activates IKK-alpha by phosphorylation of Ser-176 Proc Natl Acad Sci USA 95 1998 3792 3797
40. M.L. Schmitz, and P.A. Baeuerle The p65 subunit is responsible for the strong transcription activating potential of NF-kappa B EMBO J 10 1991 3805 3817
41. L. Vermeulen, G. De Wilde, S. Notebaert, W. Vanden Berghe, and G. Haegeman Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit Biochem Pharmacol 64 2002 963 970
42. S. Shishodia, and B.B. Aggarwal Nuclear factor-kappaB: a friend or a foe in cancer? Biochem Pharmacol 68 2004 1071 1080
43. X. Wang, Y. Wang, Y. Geng, F. Li, and C. Zheng Isolation and purification of honokiol and magnolol from cortex Magnoliae officinalis by high-speed counter-current chromatography J Chromatogr A 1036 2004 171 175
44. S. Mathas, A. Lietz, M. Janz, M. Hinz, F. Jundt, and C. Scheidereit Inhibition of NF-kappaB essentially contributes to arsenic-induced apoptosis Blood 102 2003 1028 1034
45. L.S. Olsen, P.J. Hjarnaa, S. Latini, P.K. Holm, R. Larsson, and E. Bramm Anticancer agent CHS 828 suppresses nuclear factor-kappa B activity in cancer cells through downregulation of IKK activity Int J Cancer 111 2004 198 205
46. J. Yang, and A. Richmond Constitutive IkappaB kinase activity correlates with nuclear factor-kappaB activation in human melanoma cells Cancer Res 61 2001 4901 4909
47. H.J. Son, H.J. Lee, H.S. Yun-Choi, and J.H. Ryu Inhibitors of nitric oxide synthesis and TNF-alpha expression from Magnolia obovata in activated macrophages Planta Med 66 2000 469 471
48. H. Matsuda, T. Kageura, M. Oda, T. Morikawa, Y. Sakamoto, and M. Yoshikawa Effects of constituents from the bark of Magnolia obovata on nitric oxide production in lipopolysaccharide-activated macrophages Chem Pharm Bull (Tokyo) 49 2001 716 720
49. J. Park, J. Lee, E. Jung, Y. Park, K. Kim, and B. Park In vitro antibacterial and anti-inflammatory effects of honokiol and magnolol against Propionibacterium sp Eur J Pharmacol 496 2004 189 195
50. M.A. Altinoz, and R. Korkmaz NF-kappaB, macrophage migration inhibitory factor and cyclooxygenase-inhibitions as likely mechanisms behind the acetaminophen- and NSAID-prevention of the ovarian cancer Neoplasma 51 2004 239 247
51. F. Aoudjit, E.F. Potworowski, T.A. Springer, and Y. St-Pierre Protection from lymphoma cell metastasis in ICAM-1 mutant mice: a posthoming event J Immunol 161 1998 2333 2338
52. T. Itoh, M. Tanioka, H. Matsuda, H. Nishimoto, T. Yoshioka, and R. Suzuki Experimental metastasis is suppressed in MMP-9-deficient mice Clin Exp Metastasis 17 1999 177 181
53. A. Hoffmann, A. Levchenko, M.L. Scott, and D. Baltimore The IkappaB-NF-kappaB signaling module: temporal control and selective gene activation Science 298 2002 1241 1245
54. A. Hoffmann, T.H. Leung, and D. Baltimore Genetic analysis of NF-kappaB/Rel transcription factors defines functional specificities EMBO J 22 2003 5530 5539
55. T.H. Leung, A. Hoffmann, and D. Baltimore One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers Cell 118 2004 453 464
56. A. van de Stolpe, and P.T. van der Saag Intercellular adhesion molecule-1 J Mol Med 74 1996 13 33
57. M. Hayakawa, H. Miyashita, I. Sakamoto, M. Kitagawa, H. Tanaka, and H. Yasuda Evidence that reactive oxygen species do not mediate NF-kappaB activation EMBO J 22 2003 3356 3366
58. R.F. Squires, J. Ai, M.R. Witt, P. Kahnberg, E. Saederup, and O. Sterner Honokiol and magnolol increase the number of [3H] muscimol binding sites three-fold in rat forebrain membranes in vitro using a filtration assay, by allosterically increasing the affinities of low-affinity sites Neurochem Res 24 1999 1593 1602
59. J. Ai, X. Wang, and M. Nielsen Honokiol and magnolol selectively interact with GABAA receptor subtypes in vitro Pharmacology 63 2001 34 41
60. A.A. Beg, and D. Baltimore An essential role for NF-kappaB in preventing TNF-alpha-induced cell death Science 274 1996 782 784
61. D.J. Van Antwerp, S.J. Martin, T. Kafri, D.R. Green, and I.M. Verma Suppression of TNF-alpha-induced apoptosis by NF-kappaB Science 274 1996 787 789
62. C.Y. Wang, M.W. Mayo, and A.S. Baldwin Jr. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kappaB Science 274 1996 784 787
63. H. Hsu, H.B. Shu, M.G. Pan, and D.V. Goeddel TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways Cell 84 1996 299 308
64. Y. Deng, X. Ren, L. Yang, Y. Lin, and X. Wu A JNK-dependent pathway is required for TNFalpha-induced apoptosis Cell 115 2003 61 70
65. G.E. Weitsman, A. Ravid, U.A. Liberman, and R. Koren Vitamin D enhances caspase-dependent and -independent TNFalpha-induced breast cancer cell death: the role of reactive oxygen species and mitochondria Int J Cancer 106 2003 178 186
66. H. Kamata, S. Honda, S. Maeda, L. Chang, H. Hirata, and M. Karin Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases Cell 120 2005 649 661
67. J. Varghese, S. Chattopadhaya, and A. Sarin Inhibition of p38 kinase reveals a TNF-alpha-mediated, caspase-dependent, apoptotic death pathway in a human myelomonocyte cell line J Immunol 166 2001 6570 6577
68. S. Luschen, G. Scherer, S. Ussat, H. Ungefroren, and S. Adam-Klages Inhibition of p38 mitogen-activated protein kinase reduces TNF-induced activation of NF-kappaB, elicits caspase activity, and enhances cytotoxicity Exp Cell Res 293 2004 196 206
69. Y. Nio, J. Zighelboim, J. Berek, and B. Bonavida Cycloheximide-induced modulation of TNF-mediated cytotoxicity in sensitive and resistant ovarian tumor cells Cancer Chemother Pharmacol 26 1990 1 8
70. L. Li, R.M. Thomas, H. Suzuki, J.K. De Brabander, X. Wang, and P.G. Harran A small molecule Smac mimic potentiates TRAIL- and TNFalpha-mediated cell death Science 305 2004 1471 1474
71. T. Hirano, M. Gotoh, and K. Oka Natural flavonoids and lignans are potent cytostatic agents against human leukemic HL-60 cells Life Sci 55 1994 1061 1069
72. J.A. Gustin, O.N. Ozes, H. Akca, R. Pincheira, L.D. Mayo, and Q. Li Cell type-specific expression of the IkappaB kinases determines the significance of phosphatidylinositol 3-kinase/Akt signaling to NF-kappa B activation J Biol Chem 279 2004 1615 1620
73. 2 production as a mechanism for cell type specific inhibition of TNFa-induced, but not IL-1b-induced IKK/NF-kB activation J Biol Chem 280 2005 2912 2923
74. S. Park, D.K. Lee, and C.H. Yang Inhibition of fos-jun-DNA complex formation by dihydroguaiaretic acid and in vitro cytotoxic effects on cancer cells Cancer Lett 127 1998 23 28
75. A.K. Lee, S.H. Sung, Y.C. Kim, and S.G. Kim Inhibition of lipopolysaccharide-inducible nitric oxide synthase, TNF-alpha and COX-2 expression by sauchinone effects on I-kappaBalpha phosphorylation. C/EBP and AP-1 activation Br J Pharmacol 139 2003 11 20
76. M.K. Cho, Y.P. Jang, Y.C. Kim, and S.G. Kim Arctigenin, a phenylpropanoid dibenzylbutyrolactone lignan, inhibits MAP kinases and AP-1 activation via potent MKK inhibition: the role in TNF-alpha inhibition Int Immunopharmacol 4 2004 1419 1429