Tetrandrine prevents bone loss in sciatic-neurectomized mice and inhibits receptor activator of nuclear factor κB ligand-induced osteoclast differentiation

Biological and Pharmaceutical Bulletin

Volumn 35, Issue 10, 2012, Pages 1765-1774

  Takahashi, Tatsuo ^a   Tonami, Yusuke ^a   Tachibana, Mami ^a   Nomura, Masaaki ^a   Shimada, Tsutomu ^b   Aburada, Masaki ^b   Kobayashi, Shinjiro ^a  

^a HOKURIKU UNIVERSITY   (Japan)

^b MUSASHINO UNIVERSITY   (Japan)

Author keywords

Nuclear factor of activated T cell c1; Osteoclast; Osteoporosis; Receptor activator of nuclear factor B ligand; Tetrandrine

Indexed keywords

BISBENZYLISOQUINOLINE ALKALOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOCLAST DIFFERENTIATION FACTOR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TETRANDRINE; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE ATROPHY; BONE MARROW CELL; BONE MASS; CELL LINE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG STRUCTURE; MACROPHAGE; MALE; MONOCULTURE; MOUSE; NEURECTOMY; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOPOROSIS; PLANT ROOT; RECEPTOR BINDING; SCIATIC NERVE; SIGNAL TRANSDUCTION; STEPHANIA TETRANDRA;

ANIMALS; BENZYLISOQUINOLINES; BONE MARROW CELLS; BONE RESORPTION; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; DRUGS, CHINESE HERBAL; MALE; MICE; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; SCIATIC NERVE;

EID: 84867248984     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b12-00445     Document Type: Article

References (67)

1. Karsenty G, Wagner EF. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell, 2, 389-406 (2002).
2. Sambrook P, Cooper C. Osteoporosis. Lancet, 367, 2010-2018 (2006).
3. Zaidi M. Skeletal remodeling in health and disease. Nat. Med., 13, 791-801 (2007).
4. Mohamed SG, Sugiyama E, Shinoda K, Taki H, Hounoki H, Ab-del- Aziz HO, Maruyama M, Kobayashi M, Ogawa H, Miyahara T. Interleukin-10 inhibits RANKL-mediated expression of NFATc1 in part via suppression of c-Fos and c-Jun in RAW264.7 cells and mouse bone marrow cells. Bone, 41, 592-602 (2007).
5. Reddy SV, Hundley JE, Windle JJ, Alcantara O, Linn R, Leach RJ, Boldt DH, Roodman GD. Characterization of the mouse tartrate- resistant acid phosphatase (TRAP) gene promoter. J. Bone Miner. Res., 10, 601-606 (1995).
6. Anusaksathien O, Laplace C, Li X, Ren Y, Peng L, Goldring SR, Galson DL. Tissue-specific and ubiquitous promoters direct the expression of alternatively spliced transcripts from the calcitonin receptor gene. J. Biol. Chem., 276, 22663-22674 (2001).
7. Motyckova G, Weilbaecher KN, Horstmann M, Rieman DJ, Fisher DZ, Fisher DE. Linking osteopetrosis and pycnodysostosis: regulation of cathepsin K expression by the microphthalmia transcription factor family. Proc. Natl. Acad. Sci. U.S.A., 98, 5798-5803 (2001).
8. 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. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev. Cell, 3, 889-901 (2002).
9. Theill LE, Boyle WJ, Penninger JM. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu. Rev. Immunol., 20, 795-823 (2002).
10. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD, Nishikawa S. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature, 345, 442-444 (1990).
11. Lee SE, Woo KM, Kim SY, Kim HM, Kwack K, Lee ZH, Kim HH. The phosphatidylinositol 3-kinase, p38, and extracellular signal-regulated kinase pathways are involved in osteoclast differentiation. Bone, 30, 71-77 (2002).
12. Darnay BG, Haridas V, Ni J, Moore PA, Aggarwal BB. Characterization of the intracellular domain of receptor activator of NF-kappaB (RANK). Interaction with tumor necrosis factor receptor-associated factors and activation of NF-kappaB and c-Jun N-terminal kinase. J. Biol. Chem., 273, 20551-20555 (1998).
13. Darnay BG, Ni J, Moore PA, Aggarwal BB. Activation of NF-κB by RANK requires tumor necrosis factor receptor-associated factor (TRAF) 6 and NF- κB-inducing kinase. Identification of a novel TRAF6 interaction motif. J. Biol. Chem., 274, 7724-7731 (1999).
14. Li J, Sarosi I, Yan XQ, Morony S, Capparelli C, Tan HL, McCabe S, Elliott R, Scully S, Van G, Kaufman S, Juan SC, Sun Y, Tarpley J, Martin L, Christensen K, McCabe J, Kostenuik P, Hsu H, Fletcher F, Dunstan CR, Lacey DL, Boyle WJ. RANK is the intrinsic hematopoietic cell surface receptor that controls osteoclastogenesis and regulation of bone mass and calcium metabolism. Proc. Natl. Acad. Sci. U.S.A., 97, 1566-1571 (2000).
15. Kobayashi N, Kadono Y, Naito A, Matsumoto K, Yamamoto T, Tanaka S, Inoue J. Segregation of TRAF6-mediated signaling pathways clarifies its role in osteoclastogenesis. EMBO J., 20, 1271-1280 (2001).
16. Grigoriadis AE, Wang ZQ, Cecchini MG, Hofstetter W, Felix R, Fleisch HA, Wagner EF. c-Fos: a key regulator of osteoclast- macrophage lineage determination and bone remodeling. Science, 266, 443-448 (1994).
17. Franzoso G, Carlson L, Xing L, Poljak L, Shores EW, Brown KD, Leonardi A, Tran T, Boyce BF, Siebenlist U. Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev., 11, 3482-3496 (1997).
18. Iotsova V, Caamaño J, Loy J, Yang Y, Lewin A, Bravo R. Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nat. Med., 3, 1285-1289 (1997).
19. Yamashita T, Yao Z, Li F, Zhang Q, Badell IR, Schwarz EM, Takeshita S, Wagner EF, Noda M, Matsuo K, Xing L, Boyce BF. NF-kappaB p50 and p52 regulate receptor activator of NF-kappaB ligand (RANKL) and tumor necrosis factor-induced osteoclast precursor differentiation by activating c-Fos and NFATc1. J. Biol. Chem., 282, 18245-18253 (2007).
20. Matsuo K, Galson DL, Zhao C, Peng L, Laplace C, Wang KZ, Bachler MA, Amano H, Aburatani H, Ishikawa H, Wagner EF. Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J. Biol. Chem., 279, 26475-26480 (2004).
21. Jimi E, Aoki K, Saito H, D'Acquisto F, May MJ, Nakamura I, Sudo T, Kojima T, Okamoto F, Fukushima H, Okabe K, Ohya K, Ghosh S. Selective inhibition of NF- κB blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat. Med., 10, 617-624 (2004).
22. Mino T, Sugiyama E, Taki H, Kuroda A, Yamashita N, Maruyama M, Kobayashi M. Interleukin-1alpha and tumor necrosis factor alpha synergistically stimulate prostaglandin E2-dependent production of interleukin-11 in rheumatoid synovial fibroblasts. Arthritis Rheum., 41, 2004-2013 (1998).
23. Coon D, Gulati A, Cowan C, He J. The role of cyclooxygenase-2 (COX-2) in inflammatory bone resorption. J. Endod., 33, 432-436 (2007).
24. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, Suda T. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J. Clin. Invest., 103, 1345-1352 (1999).
25. Anandarajah AP, Schwarz EM. Anti-RANKL therapy for inflammatory bone disorders: Mechanisms and potential clinical applications. J. Cell. Biochem., 97, 226-232 (2006).
26. Han KY, Yang D, Chang EJ, Lee Y, Huang H, Sung SH, Lee ZH, Kim YC, Kim HH. Inhibition of osteoclast differentiation and bone resorption by sauchinone. Biochem. Pharmacol., 74, 911-923 (2007).
27. Li D, Lu H, Li X, Quan Q, Li X, Lu W. Calcium channel blockers in cirrhotic patients with portal hypertension. Chin. Med. J. (Engl.), 108, 803-808 (1995).
28. Kobayashi S, Inaba K, Kimura I, Kimura M. Inhibitory effects of tetrandrine on angiogenesis in adjuvant-induced chronic inflammation and tube formation of vascular endothelial cells. Biol. Pharm. Bull., 21, 346-349 (1998).
29. Kwan CY, Achike FI. Tetrandrine and related bis-benzylisoquinoline alkaloids from medicinal herbs: cardiovascular effects and mechanisms of action. Acta Pharmacol. Sin., 23, 1057-1068 (2002).
30. Lai JH. Immunomodulatory effects and mechanisms of plant alkaloid tetrandrine in autoimmune diseases. Acta Pharmacol. Sin., 23, 1093-1101 (2002).
31. Xie QM, Tang HF, Chen JQ, Bian RL. Pharmacological actions of tetrandrine in inflammatory pulmonary diseases. Acta Pharmacol. Sin., 23, 1107-1113 (2002).
32. Shen YC, Chou CJ, Chiou WF, Chen CF. Anti-inflammatory effects of the partially purified extract of radix Stephaniae tetrandrae: comparative studies of its active principles tetrandrine and fangchinoline on human polymorphonuclear leukocyte functions. Mol. Pharmacol., 60, 1083-1090 (2001).
33. Chen YJ. Potential role of tetrandrine in cancer therapy. Acta Pharmacol. Sin., 23, 1102-1106 (2002).
34. Ho LJ, Juan TY, Chao P, Wu WL, Chang DM, Chang SY, Lai JH. Plant alkaloid tetrandrine downregulates IκBα kinases- IκBα- NF-κB signaling pathway in human peripheral blood T cell. Br. J. Pharmacol., 143, 919-927 (2004).
35. Wu JM, Chen Y, Chen JC, Lin TY, Tseng SH. Tetrandrine induces apoptosis and growth suppression of colon cancer cells in mice. Cancer Lett., 287, 187-195 (2010).
36. Mercurio F, Zhu H, Murray BW, Shevchenko A, Bennett BL, Li J, Young DB, Barbosa M, Mann M, Manning A, Rao A. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science, 278, 860-866 (1997).
37. Zandi E, Rothwarf DM, Delhase M, Hayakawa M, Karin M. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell, 91, 243-252 (1997).
38. Zhang H, Li YY, Wu XZ. Effect of Tetrandrine on LPS-induced NF-kappaB activation in isolated pancreatic acinar cells of rat. World J. Gastroenterol., 12, 4232-4236 (2006).
39. Wu SJ, Ng LT. Tetrandrine inhibits proinflammatory cytokines, iNOS and COX-2 expression in human monocytic cells. Biol. Pharm. Bull., 30, 59-62 (2007).
40. Lin ST, Wang Y, Xue Y, Feng DC, Xu Y, Xu LY. Tetrandrine suppresses LPS-induced astrocyte activation via modulating IKKs-IkappaBalpha-NF-kappaB signaling pathway. Mol. Cell. Biochem., 315, 41-49 (2008).
41. Kikuchi M, Kamimura S, Nomura M, Takahashi T, Hagino N, Kobayashi S. Inhibitory actions of tetrandrine on tumor necrosis factor α-induced NF-κB activation in neovascularization of cultured choroidal explants. Chinese Medicine, 1, 75-83 (2010).
42. Musacchia XJ, Steffen JM, Fell RD. Disuse atrophy of skeletal muscle: animal models. Exerc. Sport Sci. Rev., 16, 61-87 (1988).
43. Bharti AC, Takada Y, Shishodia S, Aggarwal BB. Evidence that receptor activator of nuclear factor (NF)-kappaB ligand can suppress cell proliferation and induce apoptosis through activation of a NF-kappaB-independent and TRAF6-dependent mechanism. J. Biol. Chem., 279, 6065-6076 (2004).
44. Sakai A, Sakata T, Ikeda S, Uchida S, Okazaki R, Norimura T, Hori M, Nakamura T. Intermittent administration of human parathyroid Hormone(1-34) prevents immobilization-related bone loss by regulating bone marrow capacity for bone cells in ddY mice. J. Bone Miner. Res., 14, 1691-1699 (1999).
45. Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat. Rev. Immunol., 7, 292-304 (2007).
46. Soysa NS, Alles N. NF-kappaB functions in osteoclasts. Biochem. Biophys. Res. Commun., 378, 1-5 (2009).
47. Takatsuna H, Asagiri M, Kubota T, Oka K, Osada T, Sugiyama C, Saito H, Aoki K, Ohya K, Takayanagi H, Umezawa K. Inhibition of RANKL-induced osteoclastogenesis by (-)-DHMEQ, a novel NF-kappaB inhibitor, through downregulation of NFATc1. J. Bone Miner. Res., 20, 653-662 (2005).
48. Asagiri M, Sato K, Usami T, Ochi S, Nishina H, Yoshida H, Morita I, Wagner EF, Mak TW, Serfling E, Takayanagi H. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J. Exp. Med., 202, 1261-1269 (2005).
49. Kim Y, Sato K, Asagiri M, Morita I, Soma K, Takayanagi H. Contribution of nuclear factor of activated T cells c1 to the transcriptional control of immunoreceptor osteoclast-associated receptor but not triggering receptor expressed by myeloid cells-2 during osteoclastogenesis. J. Biol. Chem., 280, 32905-32913 (2005).
50. Crotti TN, Flannery M, Walsh NC, Fleming JD, Goldring SR, McHugh KP. NFATc1 regulation of the human beta3 integrin promoter in osteoclast differentiation. Gene, 372, 92-102 (2006).
51. Kuroda Y, Hisatsune C, Nakamura T, Matsuo K, Mikoshiba K. Osteoblasts induce Ca2+ oscillation-independent NFATc1 activation during osteoclastogenesis. Proc. Natl. Acad. Sci. U.S.A., 105, 8643-8648 (2008).
52. Masuyama R, Vriens J, Voets T, Karashima Y, Owsianik G, Vennekens R, Lieben L, Torrekens S, Moermans K, Vanden Bosch A, Bouillon R, Nilius B, Carmeliet G. TRPV4-mediated calcium influx regulates terminal differentiation of osteoclasts. Cell Metab., 8, 257-265 (2008).
53. Kim MS, Yang YM, Son A, Tian YS, Lee SI, Kang SW, Muallem S, Shin DM. RANKL-mediated reactive oxygen species pathway that induces long lasting Ca2+ oscillations essential for osteoclastogenesis. J. Biol. Chem., 285, 6913-6921 (2010).
54. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol., 4, 517-529 (2003).
55. Parekh AB, Putney JW Jr. Store-operated calcium channels. Physiol. Rev., 85, 757-810 (2005).
56. Berridge MJ, Galione A. Cytosolic calcium oscillators. FASEB J., 2, 3074-3082 (1988).
57. Thomas AP, Bird GS, Hajnóczky G, Robb-Gaspers LD, Putney JW Jr. Spatial and temporal aspects of cellular calcium signaling. FASEB J., 10, 1505-1517 (1996).
58. Bird GS, Putney JW Jr. Capacitative calcium entry supports calcium oscillations in human embryonic kidney cells. J. Physiol., 562, 697-706 (2005).
59. Miyauchi A, Hruska KA, Greenfield EM, Duncan R, Alvarez J, Barattolo R, Colucci S, Zambonin-Zallone A, Teitelbaum SL, Teti A. Osteoclast cytosolic calcium, regulated by voltage-gated calcium channels and extracellular calcium, controls podosome assembly and bone resorption. J. Cell Biol., 111, 2543-2552 (1990).
60. Ritchie CK, Maercklein PB, Fitzpatrick LA. Direct effect of calcium channel antagonists on osteoclast function: alterations in bone resorption and intracellular calcium concentrations. Endocrinology, 135, 996-1003 (1994).
61. King VF, Garcia ML, Himmel D, Reuben JP, Lam YK, Pan JX, Han GQ, Kaczorowski GJ. Interaction of tetrandrine with slowly inactivating calcium channels. Characterization of calcium channel modulation by an alkaloid of Chinese medicinal herb origin. J. Biol. Chem., 263, 2238-2244 (1988).
62. Stern PH. The calcineurin-NFAT pathway and bone: intriguing new findings. Mol. Interv., 6, 193-196 (2006).
63. Winslow MM, Pan M, Starbuck M, Gallo EM, Deng L, Karsenty G, Crabtree GR. Calcineurin/NFAT signaling in osteoblasts regulates bone mass. Dev. Cell, 10, 771-782 (2006).
64. Matsumoto M, Kogawa M, Wada S, Takayanagi H, Tsujimoto M, Katayama S, Hisatake K, Nogi Y. Essential role of p38 mito-gen- activated protein kinase in cathepsin K gene expression during osteoclastogenesis through association of NFATc1 and PU.1. J. Biol. Chem., 279, 45969-45979 (2004).
65. Koga T, Matsui Y, Asagiri M, Kodama T, de Crombrugghe B, Nakashima K, Takayanagi H. NFAT and Osterix cooperatively regulate bone formation. Nat. Med., 11, 880-885 (2005).
66. McClung MR, Lewiecki EM, Cohen SB, Bolognese MA, Woodson GC, Moffett AH, Peacock M, Miller PD, Lederman SN, Chesnut CH, Lain D, Kivitz AJ, Holloway DL, Zhang C, Peterson MC, Bekker PJ; AMG 162 Bone Loss Study Group. Denosumab in postmenopausal women with low bone mineral density. N. Engl. J. Med., 354, 821-831 (2006).
67. Kendler DL, Roux C, Benhamou CL, Brown JP, Lillestol M, Siddhanti S, Man HS, San Martin J, Bone HG. Effects of denosumab on bone mineral density and bone turnover in postmenopausal women transitioning from alendronate therapy. J. Bone Miner. Res., 25, 72-81 (2010).