Saurolactam inhibits osteoclast differentiation and stimulates apoptosis of mature osteoclasts

Journal of Cellular Physiology

Volumn 221, Issue 3, 2009, Pages 618-628

  Kim, Myung Hee ^a,b   Ryu, Shi Yong ^a   Choi, Joon Sig ^b   Min, Yong Ki ^a   Kim, Seong Hwan ^a  

^a Korea Research Institute of Chemical Technology   (South Korea)

^b Chungnam National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE B; RAS PROTEIN; SAUROLACTAM; SAURURUS CHINENSIS EXTRACT; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FRA 2; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; ACID PHOSPHATASE; ALKALOID; APOPTOSIS REGULATORY PROTEIN; CASP3 PROTEIN, MOUSE; CASPASE 3; COLONY STIMULATING FACTOR 1; CYTOCHROME C; ISOENZYME; LACTAM; NFATC1 PROTEIN, MOUSE; OSTEOCLAST DIFFERENTIATION FACTOR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; RELA PROTEIN, MOUSE; TARTRATE-RESISTANT ACID PHOSPHATASE; TNFSF11 PROTEIN, MOUSE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL MATURATION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; GENE EXPRESSION; MACROPHAGE; MOUSE; MURINAE; NONHUMAN; ONCOGENE C FOS; ONCOGENE SRC; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SAURURACEAE; TUMOR CELL LINE;

MURINAE;

ACID PHOSPHATASE; ALKALOIDS; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BONE RESORPTION; CASPASE 3; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROMES C; GENE EXPRESSION; ISOENZYMES; LACTAMS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASES; NFATC TRANSCRIPTION FACTORS; OSTEOCLASTS; PHOSPHORYLATION; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; SAURURACEAE; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTOR RELA;

EID: 70449707304     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21892     Document Type: Article

References (61)

1. Akiyama T, Bouillet P, Miyazaki T, Kadono Y, Chikuda H, Chung UI, Fukuda A, Hikita A, Seto H, Okada T, Inaba T, Sanjay A, Baron R, Kawaguchi H, Oda H, Nakamura K, Strasser A, Tanaka S. 2003. Regulation of osteoclast apoptosis by ubiquitylation of proapoptotic BH3- only Bcl-2 family member Bim. EMBO J 22:6653-6664. (Pubitemid 38009611)
2. Angel NZ, Walsh N, Forwood MR, Ostrowski MC, Cassady AI, Hume DA. 2000. Transgenic mice overexpressing tartrate-resistant acid phosphatase exhibit an increased rate of bone turnover. J Bone Miner Res 15:103-110. (Pubitemid 30026937)
3. Armstrong AP, Tometsko ME, Glaccum M, Sutherland CL, Cosman D, Dougall WC. 2002. A RANK/TRAF6-dependent signal transduction pathway is essential for osteoclast cytoskeletal organization and resorptive function. J Biol Chem 277:44347-44356. (Pubitemid 36157870)
4. Asagiri M, Takayanagi H. 2007. The molecular understanding of osteoclast differentiation. Bone 40:251-264.
5. Boyle WJ, Simonet WS, Lacey DL. 2003. Osteoclast differentiation and activation. Nature 423:337-342.
6. Cho HY, Cho CW, Song YS. 2005. Antioxidative and anti-inflammatory effects of Saururus chinensis methanol extract in RAW 264.7 macrophages. J Med Food 8:190-197.
7. Dannemann C, Gratz KW, Riener MO, Zwahlen RA. 2007. Jaw osteonecrosis related to bisphosphonate therapy: A severe secondary disorder. Bone 40:828-834. (Pubitemid 46386541)
8. Delaissé JM, Engsig MT, Everts V, del Carmen Ovejero M, Ferreras M, Lund L, Vu TH, Werb Z, Winding B, Lochter A, Karsdal MA, Troen T, Kirkegaard T, Lenhard T, Heegaard AM, Neff L, Baron R, Foged NT. 2000. Proteinases in bone resorption: Obvious and less obvious roles. Clin Chim Acta 291:223-234. (Pubitemid 30089766)
9. Eferl R, Hoebertz A, Schilling AF, Rath M, Karreth F, Kenner L, Amling M, Wagner EF. 2004. The Fos-related antigen Fra-1 is an activator of bone matrix formation. EMBO J 23:2789-2799. (Pubitemid 39013551)
10. Franzoso G, Carlson L, Xing L, Poljak L, Shores EW, Brown KD, Leonardi A, Tran T, Boyce BF, Siebenlist U. 1997. Requirement for NF-kappaB in osteoclast and B-cell development. Genes Dev 11:3482-3496. (Pubitemid 28023969)
11. Fuller K, Wong B, Fox S, Choi Y, Chambers TJ. 1998. TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts. J Exp Med 188:997-1001. (Pubitemid 28433427)
12. Galibert L, Tometsko ME, Anderson DM, Cosman D, Dougall WC. 1998. The involvement of multiple tumor necrosis factor receptor (TNFR)-associated factors in the signaling mechanisms of receptor activator of NF-kappaB, a member of the TNFR superfamily. J Biol Chem 273:34120-34127. (Pubitemid 129758357)
13. Gelb BD, Shi GP, Chapman HA, Desnick RJ. 1996. Pycnodysostosis, a lysosomal disease caused by cathepsin K deficiency. Science 273:1236-1238.
14. Halleen JM, Raisanen S, Salo JJ, Reddy SV, Roodman GD, Hentunen TA, Lehenkari PP, Kaija H, Vihko P, Vaananen HK. 1999. Intracellular fragmentation of bone resorption products by reactive oxygen species generated by osteoclastic tartrate-resistant acid phosphatase. J Biol Chem 274:22907-22910. (Pubitemid 129529113)
15. Han KY, Yang D, Chang EJ, Lee Y, Huang H, Sung SH, Lee ZH, Kim YC, Kim HH. 2007. Inhibition of osteoclast differentiation and bone resorption by sauchinone. Biochem Pharmacol 74:911-923. (Pubitemid 47212083)
16. Hengartner MO. 2000. The biochemistry of apoptosis. Nature 407:770-776.
17. Hirotani H, Tuohy NA, Woo JT, Stern PH, Clipstone NA. 2004. The calcineurin/nuclear factor of activated T cells signaling pathway regulates osteoclastogenesis in RAW264.7 cells. J Biol Chem 279:13984-13992. (Pubitemid 38468932)
18. Hwang YH, Lee JW, Hahm ER, Jung KC, Lee JH, Park CH, Rhee HS, Ryu JM, Kim HK, Yang CH. 2005. Momordin I, an inhibitor of AP-1, suppressed osteoclastogenesis through inhibition of NF-kappaB and AP-1 and also reduced osteoclast activity and survival. Biochem Biophys Res Commun 337:815-823.
19. Ikeda F, Nishimura R, Matsubara T, Tanaka S, Inoue J, Reddy SV, Hata K, Yamashita K, Hiraga T, Watanabe T, Kukita T, Yoshioka K, Rao A, Yoneda T. 2004. Critical roles of c-Jun signaling in regulation of NFAT family and RANKL-regulated osteoclast differentiation. J Clin Invest 114:475-484. (Pubitemid 39572097)
20. Ishibashi O, Niwa S, Kadoyama K, Inui T. 2006. MMP-9 antisense oligodeoxynucleotide exerts an inhibitory effect on osteoclastic bone resorption by suppressing cell migration. Life Sci 79:1657-1660. (Pubitemid 44344731)
21. Ishida N, Hayashi K, Hoshijima M, Ogawa T, Koga S, Miyatake Y, Kumegawa M, Kimura T, Takeya T. 2002. Large scale gene expression analysis of osteoclastogenesis in vitro and elucidation of NFAT2 as a key regulator. J Biol Chem 277:41147-41156. (Pubitemid 35215706)
22. Ishikawa T, Kamiyama M, Tani-Ishii N, Suzuki H, Ichikawa Y, Hamaguchi Y, Momiyama N, Shimada H. 2001. Inhibition of osteoclast differentiation and bone resorption by cathepsin K antisense oligonucleotides. Mol Carcinog 32:84-91. (Pubitemid 33063186)
23. Jeong JG, Kim YS, Min YK, Kim SH. 2008. Low concentration of 3-carene stimulates the differentiation of mouse osteoblastic MC3T3-E1 subclone 4 cells. Phytother Res 22:18-22.
24. Johnson RS, Spiegelman BM, Papaioannou V. 1992. Pleiotropic effects of a null mutation in the c-fos proto-oncogene. Cell 71:577-586.
25. Kim SR, Sung SH, Kang SY, Koo KA, Kim SH, Ma CJ, Lee HS, Park MJ, Kim YC. 2004. Aristolactam BII of Saururus chinensis attenuates glutamate-induced neurotoxicity in rat cortical cultures probably by inhibiting nitric oxide production. Planta Med 70:391-396.
26. Kim Y, Sato K, Asagiri M, Morita I, Soma K, Takayanagi H. 2005. Contribution of nuclear factorof 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. (Pubitemid 41368340)
27. Kim H, Choi HK, Shin JH, Kim KH, Huh JY, Lee SA, Ko CY, Kim HS, Shin HI, Lee HJ, Jeong D, Kim N, Choi Y, Lee SY. 2009a. Selective inhibition of RANK blocks osteoclast maturation and function and prevents bone loss in mice. J Clin Invest 119:813-825.
28. Kim SN, Kim MH, Kim YS, Ryu SY, Min YK, Kim SH. 2009b. Inhibitory effect of (-)-saucerneol on osteoclast differentiation and bone pit formation. Phytother Res 23:185-191.
29. Koga T, Inui M, Inoue K, Kim S, Suematsu A, Kobayashi E, Iwata T, Ohnishi H, Matozaki T, Kodama T, Taniguchi T, Takayanagi H, Takai T. 2004. Costimulatory signals mediated by the ITAM motif cooperate with RANKL for bone homeostasis. Nature 428:758-763. (Pubitemid 38508286)
30. Lakkakorpi PT, Väänänen HK. 1996. Cytoskeletal changes in osteoclasts during the resorption cycle. Microsc Res Tech 33:171-181.
31. Lee ZH, Kim HH. 2003. Signal transduction by receptor activator of nuclear factor kappa B in osteoclasts. Biochem Biophys Res Commun 305:211-214. (Pubitemid 36555454)
32. Lee WS, Baek YI, Kim JR, Cho KH, Sok DE, Jeong TS. 2004. Antioxidant activities of a new lignan and a neolignan from Saururus chinensis. Bioorg Med Chem Lett 14:5623-5628.
33. Lee E, Haa K, Yook JM, Jin MH, Seo CS, Son KH, Kim HP, Bae KH, Kang SS, Son JK, Chang HW. 2006a. Anti-asthmatic activity of an ethanol extract from Saururus chinensis. Biol Pharm Bull 29:211-215. (Pubitemid 43200885)
34. Lee SH, Rho J, Jeong D, Sul JY, Kim T, Kim N, Kang JS, Miyamoto T, Suda T, Lee SK, Pignolo RJ, Koczon-Jaremko B, Lorenzo J, Choi Y. 2006b. v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat Med 12:1403-1409. (Pubitemid 44924499)
35. -ΔΔCT method. Methods 25:402-408.
36. Lomaga MA, Yeh WC, Sarosi I, Duncan GS, Furlonger C, Ho A, Morony S, Capparelli C, Van G, Kaufman S, van der Heiden A, Itie A, Wakeham A, Khoo W, Sasaki T, Cao Z, Penninger JM, Paige CJ, Lacey DL, Dunstan CR, Boyle WJ, Goeddel DV, Mak TW. 1999. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev 13:1015-1024.
37. Lowe C, Yoneda T, Boyce BF, Chen H, Mundy GR, Soriano P. 1993. Osteopetrosis in Src-deficient mice is due to an autonomous defect of osteoclasts. Proc Natl Acad Sci USA 90:4485-4489. (Pubitemid 23148929)
38. Matsuo K, Owens JM, Tonko M, Elliott C, Chambers TJ, Wagner EF. 2000. Fos11 is a transcriptional target of c-Fos during osteoclast differentiation. Nat Genet 24:184-187. (Pubitemid 30094722)
39. Matsuo K, Galson DL, Zhao C, Peng L, Laplace C, Wang KZ, Bachler MA, Amano H, Aburatani H, Ishikawa H, Wagner EF. 2004. Nuclear factor of activated T-cells (NFAT) rescues osteoclastogenesis in precursors lacking c-Fos. J Biol Chem 279:26475-26480. (Pubitemid 38798801)
40. McHugh KP, Hodivala-Dilke K, Zheng MH, Namba N, Lam J, Novack D, Feng X, Ross FP, Hynes RO, Teitelbaum SL. 2000. Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J Clin Invest 105:433-440. (Pubitemid 30127243)
41. Miyazaki T, Katagiri H, Kanegae Y, Takayanagi H, Sawada Y, Yamamoto A, Pando MP, Asano T, Verma IM, Oda H, Nakamura K, Tanaka S. 2000. Reciprocal role of ERK and NF-kappaB pathways in survival and activation of osteoclasts. J Cell Biol 148:333-342. (Pubitemid 30078245)
42. Morabito N, Crisafulli A, Vergara C, Gaudio A, Lasco A, Frisina N, D'Anna R, Corrado F, Pizzoleo MA, Cincotta M, Altavilla D, Ientile R, Squadrito F. 2002. Effects of genistein and hormone-replacement therapy on bone loss in early postmenopausal women: A randomized double-blind placebo-controlled study. J Bone Miner Res 17:1904-1912.
43. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. 2001. Osteoporosis prevention, diagnosis, and therapy. J Am Med Assoc 285:785-795.
44. Park SY, Lee SH, Choi WH, Koh EM, Seo JH, Ryu SY, Kim YS, Kwon DY, Koh WS. 2007. Immunosuppressive lignans isolated from Saururus chinensis. Planta Med 73:674-678.
45. Rassi CM, Lieberherr M, Chaumaz G, Pointillart A, Cournot G. 2002. Down-regulation of osteoclast differentiation by daidzein via caspase 3. J Bone Miner Res 17:630-638. (Pubitemid 34246638)
46. Reinheckel T, Deussing J, Roth W, Peters C. 2001. Towards specific functions of lysosomal cysteine peptidases: Phenotypes of mice deficient for cathepsin B or cathepsin L. Biol Chem 382:735-741. (Pubitemid 32631710)
47. Reponen P, Sahlberg C, Munaut C, Thesleff I, Tryggvason K. 1994. High expression of 92-kD type IV collagenase (gelatinase B) in the osteoclast lineage during mouse development. J Cell Biol 124:1091-1102. (Pubitemid 24109410)
48. Rozen S, Skaletsky HJ. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics methods and protocols: Methods in molecular biology. Totowa: Humana Press. pp 365-386.
49. Shim KS, Kim SN, Kim MH, Kim YS, Min YK, Kim SH. 2008. Inhibitory effects of Saururus chinensis extracts on osteoclast differentiation. Nat Prod Sci 14:113-117.
50. Song H, Kim YC, Moon A. 2003. Sauchinone, a lignan from Saururus chinensis, inhibits staurosporine-induced apoptosis in C6 rat glioma cells. Biol Pharm Bull 26:1428-1430. (Pubitemid 41685394)
51. Song SY, Lee I, Park C, Lee H, Hahm JC, Kang WK. 2005. Neolignans from Saururus chinensis inhibit PC-3 prostate cancer cell growth via apoptosis and senescence-like mechanisms. Int J Mol Med 16:517-523.
52. Soriano P, Montgomery C, Geske R, Bradley A. 1991. Targeted disruption of the c-src protooncogene leads to osteopetrosis in mice. Cell 64:693-702. (Pubitemid 121001157)
53. Stern PH. 2007. Antiresorptive agents and osteoclast apoptosis. J Cell Biochem 101:1087-1096.
54. 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 for terminal differentiation of osteoclasts. Dev Cell 3:889-901.
55. Tanaka S, Miyazaki T, Fukuda A, Akiyama T, Kadono Y, Wakeyama H, Kono S, Hoshikawa S, Nakamura M, Ohshima Y, Hikita A, Nakamura I, Nakamura K. 2006. Molecular mechanism of the life and death of the osteoclast. Ann N Y Acad Sci 1068:180-186.
56. Tang QY, Kukita T, Ushijima Y, Kukita A, Nagata K, Sandra F, Watanabe T, Toh K, Okuma Y, Kawasaki S, Rasubala L, Teramachi J, Miyamoto I, Wu Z, Iijima T. 2006. Regulation of osteoclastogenesis by Simon extracts composed of caffeic acid and related compounds: Successful suppression of bone destruction accompanied with adjuvant-induced arthritis in rats. Histochem Cell Biol 125:215-225.
57. Wang ZQ, Ovitt C, Grigoriadis AE, Mohle-Steinlein U, Ruther U, Wagner EF. 1992. Bone and haematopoietic defects in mice lacking c-fos. Nature 360:741-745.
58. Wu X, McKenna MA, Feng X, Nagy TR, McDonald JM. 2003. Osteoclast apoptosis: The role of Fas in vivo and in vitro. Endocrinology 144:5545-5555.
59. Wu H, Xu G, Li YP. 2009. Atp6v0d2 is an essential component of the osteoclast-specific proton pump that mediates extracellular acidification in bone resorption. J Bone Miner Res 24:871-885.
60. Yamashita T, Kobayashi Y, Mizoguchi T, Yamaki M, Miura T, Tanaka S, Udagawa N, Takahashi N. 2008. MKK6-p38 MAPK signaling pathway enhances survival but not bone-resorbing activity of osteoclasts. Biochem Biophys Res Commun 365:252-257. (Pubitemid 350137282)
61. Zhao H, Ross FP, Teitelbaum SL. 2005. Unoccupied alpha(v)beta3 integrin regulates osteoclast apoptosis by transmitting a positive death signal. Mol Endocrinol 19:771-780. (Pubitemid 40349447)