Hispidulin attenuates bone resorption and osteoclastogenesis via the RANKL-induced NF-κB and NFATc1 pathways

European Journal of Pharmacology

Volumn 715, Issue 1-3, 2013, Pages 96-104

  Nepal, Manoj ^a   Choi, Hwa Jung ^a   Choi, Bo Yun ^a   Yang, Moon Shik ^a   Chae, Jung Il ^a   Li, Liang ^a   Soh, Yunjo ^a  

^a Chonbuk National University   (South Korea)

Author keywords

Bone resorption; Hispidulin; Osteoclastogenesis; RANKL; CT

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CATHEPSIN K; GELATINASE B; HISPIDULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; OSTEOCLAST DIFFERENTIATION FACTOR; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; DRUG MECHANISM; GENE EXPRESSION; HISTOCHEMISTRY; IN VITRO STUDY; MACROPHAGE; MICRO-COMPUTED TOMOGRAPHY; MONOCYTE; MOUSE; MULTINUCLEAR CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOCLAST ACTIVITY; OSTEOCLASTOGENESIS; OSTEOLYSIS; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

BONE RESORPTION; HISPIDULIN; OSTEOCLASTOGENESIS; RANKL; ΜCT;

ALKALINE PHOSPHATASE; ANIMALS; BONE RESORPTION; CELL LINE; FLAVONES; GENE EXPRESSION REGULATION; LIPOPOLYSACCHARIDES; MICE; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; PROTO-ONCOGENE PROTEINS C-FOS; RANK LIGAND; SIGNAL TRANSDUCTION;

EID: 84885469419     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.06.002     Document Type: Article

References (34)

1. Ang, E.S., Yang, X., Chen, H., Liu, Q., Zheng, M.H., Xu, J., 2011. Naringin abrogates osteoclastogenesis and bone resorption via the inhibition of RANKL-induced NF-kappaB and ERK activation. FEBS Lett. 585, 2755-2762.
2. Ang, E.S., Zhang, P., Steer, J.H., Tan, J.W., Yip, K., Zheng, M.H., Joyce, D.A., Xu, J., 2007. Calcium/calmodulin-dependent kinase activity is required for efficient induction of osteoclast differentiation and bone resorption by receptor activator of nuclear factor kappa B ligand (RANKL). J. Cell. Physiol. 212, 787-795. (Pubitemid 47267548)
3. Bu, S.Y., Lerner, M., Stoecker, B.J., Boldrin, E., Brackett, D.J., Lucas, E.A., Smith, B.J., 2008. Dried plum polyphenols inhibit osteoclastogenesis by downregulating NFATc1 and inflammatory mediators. Calcif. Tissue Int. 82, 475-488.
4. Choi, H.J., Park, Y.R., Nepal, M., Choi, B.Y., Cho, N.P., Choi, S.H., Heo, S.R., Kim, H.S., Yang, M.S., Soh, Y., 2010. Inhibition of osteoclastogenic differentiation by Ikarisoside A in RAW 264.7 cells via JNK and NF-kappaB signaling pathways. Eur. J. Pharmacol. 636, 28-35.
5. Dabaghi-Barbosa, P., Mariante Rocha, A., Franco da Cruz Lima, A., Heleno de Oliveira, B., Benigna Martinelli de Oliveira, M., Gunilla Skare Carnieri, E., Cadena, S.M., Eliane Merlin Rocha, M., 2005. Hispidulin: antioxidant properties and effect on mitochondrial energy metabolism. Free Radical Res. 39, 1305-1315. (Pubitemid 43023795)
6. Deal, C., 2009. Potential new drug targets for osteoporosis. Nat. Clin. Pract. Rheumatol. 5, 20-27.
7. Giannoudis, P., Kanakaris, N., Einhorn, T., 2007. Interaction of bone morphogenetic proteins with cells of the osteoclast lineage: review of the existing evidence. Osteoporosis Int. 18 (12), 1565-1581. (Pubitemid 47620320)
8. Granholm, S., Lundberg, P., Lerner, U.H., 2007. Calcitonin inhibits osteoclast formation in mouse haematopoetic cells independently of transcriptional regulation by receptor activator of NF-{kappa}B and c-Fms. J. Endocrinol. 195, 415-427.
9. He, L., Wu, Y., Lin, L., Wang, J., Wu, Y., Chen, Y., Yi, Z., Liu, M., Pang, X., 2011. Hispidulin, a small flavonoid molecule, suppresses the angiogenesis and growth of human pancreatic cancer by targeting vascular endothelial growth factor receptor 2-mediated PI3K/Akt/mTOR signaling pathway. Cancer Sci. 102, 219-225.
10. Ikeda, F., Matsubara, T., Tsurukai, T., Hata, K., Nishimura, R., Yoneda, T., 2008. JNK/c-Jun signaling mediates an anti-apoptotic effect of RANKL in osteoclasts. J. Bone Miner. Res. 23, 907-914. (Pubitemid 351768809)
11. Karsenty, G., Wagner, E.F., 2002. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell 2, 389-406. (Pubitemid 34436569)
12. Kavvadias, D., Sand, P., Youdim, K.A., Qaiser, M.Z., Rice-Evans, C., Baur, R., Sigel, E., Rausch, W.D., Riederer, P., Schreier, P., 2004. The flavone hispidulin, a benzo-diazepine receptor ligand with positive allosteric properties, traverses the blood-brain barrier and exhibits anticonvulsive effects. Br. J. Pharmacol. 142, 811-820. (Pubitemid 38998095)
13. Kim, J.H., Kim, K., Youn, B.U., Jin, H.M., Kim, J.Y., Moon, J.B., Ko, A., Seo, S.B., Lee, K.Y., Kim, N., 2011. RANKL induces NFATc1 acetylation and stability via histone acetyltransferases during osteoclast differentiation. Biochem. J. 436, 253-262.
14. Koehn, F.E., Carter, G.T., 2005. The evolving role of natural products in drug discovery. Nat. Rev. 4, 206-220. (Pubitemid 40372555)
15. Lee, J.H., Jin, H., Shim, H.E., Kim, H.N., Ha, H., Lee, Z.H., 2010. Epigallocatechin-3-gallate inhibits osteoclastogenesis by down-regulating c-Fos expression and suppressing the nuclear factor-kappaB signal. Mol. Pharmacol. 77, 17-25.
16. Lee, Z.H., Kim, H.H., 2003. Signal transduction by receptor activator of nuclear factor kappa B in osteoclasts. Biochem. Biophys. Res. Commun. 305, 211-214. (Pubitemid 36555454)
17. Lee, Z.H., Kwack, K., Kim, K.K., Lee, S.H., Kim, H.H., 2000. Activation of c-Jun N-terminal kinase and activator protein 1 by receptor activator of nuclear factor kappaB. Mol. Pharmacol. 58, 1536-1545.
18. Leibbrandt, A., Penninger, J.M., 2008. RANK/RANKL: regulators of immune responses and bone physiology. Ann. N. Y. Acad. Sci. 1143, 123-150.
19. Li, J., Vederas, J., 2009. Drug discovery and natural products: end of an era or an endless frontier? Science 325, 161-165.
20. Lin, Y.C., Hung, C.M., Tsai, J.C., Lee, J.C., Chen, Y.L., Wei, C.W., Kao, J.Y., Way, T.D., 2010. Hispidulin potently inhibits human glioblastoma multiforme cells through activation of AMP-activated protein kinase (AMPK). J. Agric. Food Chem. 58, 9511-9517.
21. Lubberts, E., Oppers-Walgreen, B., Pettit, A.R., Van Den Bersselaar, L., Joosten, L.A.B., Goldring, S.R., Gravallese, E.M., Van Den Berg, W.B., 2002. Increase in expression of receptor activator of nuclear factor κB at sites of bone erosion correlates with progression of inflammation in evolving collagen-induced arthritis. Arthritis Rheum. 46, 3055-3064. (Pubitemid 35315901)
22. 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.
23. O'Regan, R.M., Gradishar, W.J., 2001. Selective estrogen-receptor modulators in 2001. Oncology (Williston Park) 15 (9), 1177-1194.
24. Park, C.K., Kim, H.J., Kwak, H.B., Lee, T.H., Bang, M.H., Kim, C.M., Lee, Y., Chung, D.K., Baek, N.I., Kim, J., Lee, Z.H., Kim, H.H., 2007. Inhibitory effects of Stewartia koreana on osteoclast differentiation and bone resorption. Int. Immunophar-macol. 7, 1507-1516. (Pubitemid 47499256)
25. Rejnmark, L., Mosekilde, L., 2011. New and emerging antiresorptive treatments in osteoporosis. Curr. Drug Saf. 6, 75-88.
26. Sugatani, T., Alvarez, U., Hruska, K.A., 2003. PTEN regulates RANKL- and osteopontin-stimulated signal transduction during osteoclast differentiation and cell motility. J. Biol. Chem. 278, 5001-5008. (Pubitemid 36801009)
27. Sundaram, K., Nishimura, R., Senn, J., Youssef, R.F., London, S.D., Reddy, S.V., 2007. RANK ligand signaling modulates the matrix metalloproteinase-9 gene expression during osteoclast differentiation. Exp. Cell Res. 313, 168-178. (Pubitemid 44958461)
28. Takayanagi, H., Kim, S., Koga, T., Nishina, H., Isshiki, M., Yoshida, H., Saiura, A., Isobe, M., Yokochi, T., Inoue, J., Wagner, E.F., Mak, T.W., 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. (Pubitemid 35460788)
29. Takayanagi, H., 2007. The role of NFAT in osteoclast formation. Ann. N. Y. Acad. Sci. 1116, 227-237. (Pubitemid 350274348)
30. Tao, H., Okamoto, M., Nishikawa, M., Yoshikawa, H., Myoui, A., 2011. P38 mitogen-activated protein kinase inhibitor, FR167653, inhibits parathyroid hormone related protein-induced osteoclastogenesis and bone resorption. PloS One 6, e23199.
31. Teitelbaum, S.L., 2000. Bone resorption by osteoclasts. Science 289, 1504-1508.
32. Vaira, S., Johnson, T., Hirbe, A.C., Alhawagri, M., Anwisye, I., Sammut, B., O'Neal, J., Zou, W., Weilbaecher, K.N., Faccio, R., Novack, D.V., 2008. RelB is the NF-kappaB subunit downstream of NIK responsible for osteoclast differentiation. Proc. Natl. Acad. Sci. USA 105, 3897-3902. (Pubitemid 351723496)
33. Viatour, P., Merville, M.P., Bours, V., Chariot, A., 2005. Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem. Sci. 30, 43-52. (Pubitemid 40093740)
34. Yang, J.M., Hung, C.M., Fu, C.N., Lee, J.C., Huang, C.H., Yang, M.H., Lin, C.L., Kao, J.Y., Way, T.D., 2010. Hispidulin sensitizes human ovarian cancer cells to TRAIL-induced apoptosis by AMPK activation leading to Mcl-1 block in translation. J. Agric. Food Chem. 58, 10020-10026.