Inhibitory effects of tert-butylhydroquinone on osteoclast differentiation via up-regulation of heme oxygenase-1 and down-regulation of HMGB1 release and NFATc1 expression

Journal of Applied Toxicology

Volumn 34, Issue 1, 2014, Pages 49-56

  Yamaguchi, Yu ^a   Sakai, Eiko ^a   Sakamoto, Hiroshi ^a   Fumimoto, Reiko ^a   Fukuma, Yutaka ^a   Nishishita, Kazuhisa ^a   Okamoto, Kuniaki ^a   Tsukuba, Takayuki ^a  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

Author keywords

Heme oxygenase 1; High mobility group box1; Nuclear factor of activated T cells cytoplasmic 1; Osteoclasts; tert butylhydroquinone

Indexed keywords

CATHEPSIN K; HEME OXYGENASE 1; HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NUCLEAR FACTOR OF ACTIVATED T CELL CYTOPLASMIC 1; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INDUCTION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

MURINAE;

HEME OXYGENASE-1; HIGH MOBILITY GROUP BOX 1; NUCLEAR FACTOR OF ACTIVATED T CELLS CYTOPLASMIC-1; OSTEOCLASTS; TERT-BUTYLHYDROQUINONE;

ANIMALS; CATHEPSIN K; CELL DIFFERENTIATION; DOWN-REGULATION; HEME OXYGENASE-1; HMGB1 PROTEIN; HYDROQUINONES; MACROPHAGES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MONOCYTES; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84886777392     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.2827     Document Type: Article

References (31)

1. Alamed J, Chaiyasit W, McClements DJ, Decker EA. 2009. Relationships between free radical scavenging and antioxidant activity in foods. J. Agric. Food Chem. 57: 2969-2976.
2. Boyle WJ, Simonet WS, Lacey DL. 2003. Osteoclast differentiation and activation. Nature 423: 337-342.
3. Cheung KL, Yu S, Pan Z, Ma J, Wu TY, Kong AN. 2011. tBHQ-induced HO-1 expression is mediated by calcium through regulation of Nrf2 binding to enhancer and polymerase II to promoter region of HO-1. Chem. Res. Toxicol. 24: 670-676.
4. Darnay BG, Ni J, Moore PA, Aggarwal BB. 1999. Activation of NF-kappaB by RANK requires tumor necrosis factor receptor-associated factor (TRAF) 6 and NF-kappaB-inducing kinase. Identification of a novel TRAF6 interaction motif. J. Biol. Chem. 274: 7724-7731.
5. Delaisse JM, Andersen TL, Engsig MT, Henriksen K, Troen T, Blavier L. 2003. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities. Microsc. Res. Tech. 61: 504-513.
6. Gharavi N, Haggarty S, El-Kadi AO. 2007. Chemoprotective and carcinogenic effects of tert-butylhydroquinone and its metabolites. Curr. Drug Metab. 8: 1-7.
7. Hotokezaka H, Sakai E, Kanaoka K, Saito K, Matsuo K, Kitaura H, Yoshida N, Nakayama K. 2002. U0126 and PD98059, specific inhibitors of MEK, accelerate differentiation of RAW264.7 cells into osteoclast-like cells. J. Biol. Chem. 277: 47366-47372.
8. Hu JP, Nishishita K, Sakai E, Yoshida H, Kato Y, Tsukuba T, Okamoto K. 2008. Berberine inhibits RANKL-induced osteoclast formation and survival through suppressing the NF-kappaB and Akt pathways. Eur. J. Pharmacol. 580: 70-79.
9. Hwang SY, Putney JW, Jr. 2011. Calcium signaling in osteoclasts. Biochim. Biophys. Acta 1813: 979-983.
10. Jin W, Ni H, Dai Y, Wang H, Lu T, Wu J, Jiang J, Liang W. 2010. Effects of tert-butylhydroquinone on intestinal inflammatory response and apoptosis following traumatic brain injury in mice. Mediators Inflamm. 2010: 502564.
11. Kamiya T, Kobayashi Y, Kanaoka K, Nakashima T, Kato Y, Mizuno A, Sakai H. 1998. Fluorescence microscopic demonstration of cathepsin K activity as the major lysosomal cysteine proteinase in osteoclasts. J. Biochem. 123: 752-759.
12. Kensler TW, Wakabayashi N, Biswal S. 2007. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47: 89-116.
13. Keum YS, Han YH, Liew C, Kim JH, Xu C, Yuan X, Shakarjian MP, Chong S, Kong AN. 2006. Induction of heme oxygenase-1 (HO-1) and NAD[P]H: quinone oxidoreductase 1 (NQO1) by a phenolic antioxidant, butylated hydroxyanisole (BHA) and its metabolite, tert-butylhydroquinone (tBHQ) in primary-cultured human and rat hepatocytes. Pharm. Res. 23: 2586-2594.
14. Khodagholi F, Tusi SK. 2011. Stabilization of Nrf2 by tBHQ prevents LPS-induced apoptosis in differentiated PC12 cells. Mol. Cell. Biochem. 354: 97-112.
15. Kim MS, Yang YM, Son A, Tian YS, Lee SI, Kang SW, Muallem S, Shin DM. 2010. RANKL-mediated reactive oxygen species pathway that induces long lasting Ca2+ oscillations essential for osteoclastogenesis. J. Biol. Chem. 285: 6913-6921.
16. Koh K, Cha Y, Kim S, Kim J. 2009. tBHQ inhibits LPS-induced microglial activation via Nrf2-mediated suppression of p38 phosphorylation. Biochem. Biophys. Res. Commun. 380: 449-453.
17. Lee NK, Choi YG, Baik JY, Han SY, Jeong DW, Bae YS, Kim N, Lee SY. 2005. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 106: 852-859.
18. Li HY, Zhong YF, Wu SY, Shi N. 2007. NF-E2 related factor 2 activation and heme oxygenase-1 induction by tert-butylhydroquinone protect against deltamethrin-mediated oxidative stress in PC12 cells. Chem. Res. Toxicol. 20: 1242-1251.
19. Matsumoto M, Sudo T, Saito T, Osada H, Tsujimoto M. 2000. Involvement of p38 mitogen-activated protein kinase signaling pathway in osteoclastogenesis mediated by receptor activator of NF-kappa B ligand (RANKL). J. Biol. Chem. 275: 31155-31161.
20. Rushmore TH, Kong AN. 2002. Pharmacogenomics, regulation and signaling pathways of phase I and II drug metabolizing enzymes. Curr. Drug Metab. 3: 481-490.
21. Sakai E, Shimada-Sugawara M, Nishishita K, Fukuma Y, Naito M, Okamoto K, Nakayama K, Tsukuba T. 2012. Suppression of RANKL-dependent heme oxygenase-1 is required for high mobility group box1 release and osteoclastogenesis. J. Cell. Biochem. 113: 486-498.
22. Song I, Kim JH, Kim K, Jin HM, Youn BU, Kim N. 2009. Regulatory mechanism of NFATc1 in RANKL-induced osteoclast activation. FEBS Lett. 583: 2435-2440.
23. Takayanagi H, Kim S, Koga T, Nishina H, Isshiki M, Yoshida H, Saiura A, Isobe M, Yokochi T, Inoue J, Wagner EF, Mak TW, Kodama T, Taniguchi T. 2002. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell 3: 889-901.
24. Teitelbaum SL. 2000. Bone resorption by osteoclasts. Science 289: 1504-1508.
25. Watanabe T, Kukita T, Kukita A, Wada N, Toh K, Nagata K, Nomiyama H, Iijima T. 2004. Direct stimulation of osteoclastogenesis by MIP-1alpha: evidence obtained from studies using RAW264 cell clone highly responsive to RANKL. J. Endocrinol. 180: 193-201.
26. Xu C, Li CY, Kong AN. 2005. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch. Pharm. Res. 28: 249-268.
27. Yamoah K, Brebene A, Baliram R, Inagaki K, Dolios G, Arabi A, Majeed R, Amano H, Wang R, Yanagisawa R, Abe E. 2008. High-mobility group box proteins modulate tumor necrosis factor-alpha expression in osteoclastogenesis via a novel deoxyribonucleic acid sequence. Mol. Endocrinol. 22: 1141-1153.
28. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, Tomoyasu A, Yano K, Goto M, Murakami A, Tsuda E, Morinaga T, Higashio K, Udagawa N, Takahashi N, Suda T. 1998. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc. Natl. Acad. Sci. U. S. A. 95: 3597-3602.
29. Yu R, Mandlekar S, Lei W, Fahl WE, Tan TH, Kong AN. 2000. p38 mitogen-activated protein kinase negatively regulates the induction of phase II drug-metabolizing enzymes that detoxify carcinogens. J. Biol. Chem. 275: 2322-2327.
30. Zhang YH, Heulsmann A, Tondravi MM, Mukherjee A, Abu-Amer Y. 2001. Tumor necrosis factor-alpha (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways. J. Biol. Chem. 276: 563-568.
31. Zhou Z, Han JY, Xi CX, Xie JX, Feng X, Wang CY, Mei L, Xiong WC. 2008. HMGB1 regulates RANKL-induced osteoclastogenesis in a manner dependent on RAGE. J. Bone Miner. Res. 23: 1084-1096.