Modified salicylanilide and 3-phenyl-2 H -benzo[ e ][1,3]oxazine-2,4(3 H)-dione derivatives as novel inhibitors of osteoclast differentiation and bone resorption

Journal of Medicinal Chemistry

Volumn 57, Issue 19, 2014, Pages 8072-8085

  Chen, Chun Liang ^a,b   Liu, Fei Lan ^c   Lee, Chia Chung ^a,b   Chen, Tsung Chih ^a,b   Ahmed Ali, Ahmed Atef ^b,d   Sytwu, Huey Kang ^b   Chang, Deh Ming ^b,c   Huang, Hsu Shan ^a,b  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^c TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^d INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 OXAZINE DERIVATIVE; 3 (2 FLUORO 4 IODOPHENYL) 2H BENZO[E][1,3]OXAZINE 2,4(3H) DIONE; 3 (4 CHLORO 2 FLUOROPHENYL) 2H BENZO[E][1,3]OXAZINE 2,4(3H) DIONE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N(4 CHLORO 2 FLUOROPHENYL) 2 HYDROXYBENZAMIDE; OSTEOCLAST DIFFERENTIATION FACTOR; SALICYLANILIDE DERIVATIVE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; UNCLASSIFIED DRUG; OXAZINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL NUCLEUS; CELL VIABILITY; CHEMICAL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DOSE RESPONSE; DOWN REGULATION; DRUG SYNTHESIS; MARKER GENE; NONHUMAN; OSTEOCLASTOGENESIS; OSTEOLYSIS; PHARMACOPHORE; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ACTIVITY RELATION; TELOMERIC REPEAT AMPLIFICATION PROTOCOL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; MOUSE; OSTEOCLAST; PREVENTION AND CONTROL; SYNTHESIS;

ANIMALS; BONE RESORPTION; CELL DIFFERENTIATION; CELLS, CULTURED; MICE; OSTEOCLASTS; OXAZINES; RANK LIGAND; SALICYLANILIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84907901196     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm5007897     Document Type: Article

References (49)

1. Goltzman, D. Discoveries, drugs and skeletal disorders Nat. Rev. Drug Discovery 2002, 1, 784-796
2. Boyle, W. J.; Simonet, W. S.; Lacey, D. L. Osteoclast differentiation and activation Nature 2003, 423, 337-342
3. Romas, E.; Gillespie, M. T.; Martin, T. J. Involvement of receptor activator of NFκB ligand and tumor necrosis factor-α in bone destruction in rheumatoid arthritis Bone 2002, 30, 340-246
4. Tanaka, S. Signaling axis in osteoclast biology and therapeutic targeting in the RANKL/RANK/OPG system Am. J. Nephrol. 2007, 27, 466-478
5. Walsh, N. C.; Gravallese, E. M. Bone loss in inflammatory arthritis: Mechanisms and treatment strategies Curr. Opin. Rheumatol. 2004, 16, 419-427
6. Kearns, A. E.; Khosla, S.; Kostenuik, P. J. Receptor activator of nuclear factor κB ligand and osteoprotegerin regulation of bone remodeling in health and disease Endocr. Rev. 2008, 29, 155-192
7. Teitelbaum, S. L. Bone resorption by osteoclasts Science 2000, 289, 1504-1508
8. Suda, T.; Takahashi, N.; Udagawa, N.; Jimi, E.; Gillespie, M. T.; Martin, T. J. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families Endocr. Rev. 1999, 20, 345-357
9. Darnay, B. G.; Haridas, V.; Ni, J.; Moore, P. A.; Aggarwal, B. B. Characterization of the intracellular domain of receptor activator of NF-κB (RANK). Interaction with tumor necrosis factor receptor-associated factors and activation of NF-κB and c-Jun N-terminal kinase J. Biol. Chem. 1998, 273, 20551-20555
10. Kikuta, J.; Ishii, M. Osteoclast migration, differentiation and function: Novel therapeutic targets for rheumatic diseases Rheumatology (Oxford, U. K.) 2013, 52, 226-234
11. Koga, T.; Matsui, Y.; Asagiri, M.; Kodama, T.; de Crombrugghe, B.; Nakashima, K.; Takayanagi, H. NFAT and Osterix cooperatively regulate bone formation Nat. Med. 2005, 11, 880-885
12. 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. Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts Dev. Cell 2002, 3, 889-901
13. 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. 2005, 280, 32905-32913
14. Asagiri, M.; Takayanagi, H. The molecular understanding of osteoclast differentiation Bone 2007, 40, 251-264
15. Yagi, M.; Miyamoto, T.; Sawatani, Y.; Iwamoto, K.; Hosogane, N.; Fujita, N.; Morita, K.; Ninomiya, K.; Suzuki, T.; Miyamoto, K.; Oike, Y.; Takeya, M.; Toyama, Y.; Suda, T. DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells J. Exp. Med. 2005, 202, 345-351
16. Kukita, T.; Wada, N.; Kukita, A.; Kakimoto, T.; Sandra, F.; Toh, K.; Nagata, K.; Iijima, T.; Horiuchi, M.; Matsusaki, H.; Hieshima, K.; Yoshie, O.; Nomiyama, H. RANKL-induced DC-STAMP is essential for osteoclastogenesis J. Exp. Med. 2004, 200, 941-946
17. Grigoriadis, A. E.; Wang, Z. Q.; Cecchini, M. G.; Hofstetter, W.; Felix, R.; Fleisch, H. A.; Wagner, E. F. c-Fos: A key regulator of osteoclast-macrophage lineage determination and bone remodeling Science 1994, 266, 443-448
18. Wada, T.; Nakashima, T.; Hiroshi, N.; Penninger, J. M. RANKL-RANK signaling in osteoclastogenesis and bone disease Trends Mol. Med. 2006, 12, 17-25
19. Watts, N. B. Bisphosphonate treatment of osteoporosis Clin. Geriatr. Med. 2003, 19, 395-414
20. Strampel, W.; Emkey, R.; Civitelli, R. Safety considerations with bisphosphonates for the treatment of osteoporosis Drug Saf. 2007, 30, 755-763
21. Conte, P.; Guarneri, V. Safety of intravenous and oral bisphosphonates and compliance with dosing regimens Oncologist 2004, 9 (Suppl. 4) 28-37
22. Soekanto, A.; Ohya, K.; Ogura, H. The effect of sodium salicylate on the osteoclast-like cell formation and bone resorption in a mouse bone marrow culture Calcif. Tissue Int. 1994, 54, 290-295
23. Tsai, H. Y.; Lin, H. Y.; Fong, Y. C.; Wu, J. B.; Chen, Y. F.; Tsuzuki, M.; Tang, C. H. Paeonol inhibits RANKL-induced osteoclastogenesis by inhibiting ERK, p38 and NF-κB pathway Eur. J. Pharmacol. 2008, 588, 124-133
24. Hsu, Y. C.; Cheng, C. P.; Chang, D. M. Plectranthus amboinicus attenuates inflammatory bone erosion in mice with collagen-induced arthritis by downregulation of RANKL-induced NFATc1 expression J. Rheumatol. 2011, 38, 1844-1857
25. Cheng, C. P.; Huang, H. S.; Hsu, Y. C.; Sheu, M. J.; Chang, D. M. A benzamide-linked small molecule NDMC101 inhibits NFATc1 and NF-κB activity: A potential osteoclastogenesis inhibitor for experimental arthritis J. Clin. Immunol. 2012, 32, 762-777
26. Idris, A. I.; Mrak, E.; Greig, I.; Guidobono, F.; Ralston, S. H.; van't Hof, R. ABD56 causes osteoclast apoptosis by inhibiting the NFκB and ERK pathways Biochem. Biophys. Res. Commun. 2008, 371, 94-98
27. van't Hof, R. J.; Idris, A. I.; Ridge, S. A.; Dunford, J.; Greig, I. R.; Ralston, S. H. Identification of biphenylcarboxylic acid derivatives as a novel class of bone resorption inhibitors J. Bone Miner. Res. 2004, 19, 1651-1660
28. Steffen, J. D.; Coyle, D. L.; Damodaran, K.; Beroza, P.; Jacobson, M. K. Discovery and structure-activity relationships of modified salicylanilides as cell permeable inhibitors of poly(ADP-ribose) glycohydrolase (PARG) J. Med. Chem. 2011, 54, 5403-5413
29. Brown, M. E.; Fitzner, J. N.; Stevens, T.; Chin, W.; Wright, C. D.; Boyce, J. P. Salicylanilides: Selective inhibitors of interleukin-12p40 production Bioorg. Med. Chem. 2008, 16, 8760-8764
30. Liu, F. C.; Huang, H. S.; Huang, C. Y.; Yang, R.; Chang, D. M.; Lai, J. H.; Ho, L. J. A benzamide-linked small molecule HS-Cf inhibits TNF-α-induced interferon regulatory factor-1 in porcine chondrocytes: A potential disease-modifying drug for osteoarthritis therapeutics J. Clin. Immunol. 2011, 31, 1131-1142
31. Coste, E.; Greig, I. R.; Mollat, P.; Rose, L.; Gray, M.; Ralston, S. H.; van't Hof, R. J. Identification of small molecule inhibitors of RANKL and TNF signalling as anti-inflammatory and antiresorptive agents in mice Ann. Rheum. Dis. 2013, 10.1136/annrheumdis-2013-203700
32. Crockett, J. C.; Rogers, M. J.; Coxon, F. P.; Hocking, L. J.; Helfrich, M. H. Bone remodelling at a glance J. Cell Sci. 2011, 124, 991-998
33. Bellows, C. G.; Aubin, J. E.; Heersche, J. N. Initiation and progression of mineralization of bone nodules formed in vitro: The role of alkaline phosphatase and organic phosphate Bone Miner. 1991, 14, 27-40
34. Quarles, L. D.; Yohay, D. A.; Lever, L. W.; Caton, R.; Wenstrup, R. J. Distinct proliferative and differentiated stages of murine MC3T3-E1 cells in culture: An in vitro model of osteoblast development J. Bone Miner. Res. 1992, 7, 683-692
35. Wang, D.; Christensen, K.; Chawla, K.; Xiao, G.; Krebsbach, P. H.; Franceschi, R. T. Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential J. Bone Miner. Res. 1999, 14, 893-903
36. Skala, P.; Machacek, M.; Vejsova, M.; Kubicova, L.; Kunes, J.; Waisser, K. Synthesis and antifungal evaluation of hydroxy-3-phenyl-2 H -1,3-benzoxazine-2,4(3 H)-diones and their thioanalogs J. Heterocycl. Chem. 2009, 46, 873-880
37. Alam, M. I.; Gomes, A. Viper venom-induced inflammation and inhibition of free radical formation by pure compound (2-hydroxy-4-methoxy benzoic acid) isolated and purified from anantamul (Hemidesmus indicus R. BR) root extract Toxicon 1998, 36, 207-215
38. Hayman, A. R.; Jones, S. J.; Boyde, A.; Foster, D.; Colledge, W. H.; Carlton, M. B.; Evans, M. J.; Cox, T. M. Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis Development 1996, 122, 3151-3162
39. Saftig, P.; Hunziker, E.; Everts, V.; Jones, S.; Boyde, A.; Wehmeyer, O.; Suter, A.; von Figura, K. Functions of cathepsin K in bone resorption-Lessons from cathepsin K deficient mice Adv. Exp. Med. Biol. 2000, 477, 293-303
40. Xia, L. H.; Kilb, J.; Wex, H.; Li, Z. Q.; Lipyansky, A.; Breuil, V.; Stein, L.; Palmer, J. T.; Dempster, D. W.; Bromme, D. Localization of rat cathepsin K in osteoclasts and resorption pits: Inhibition of bone resorption and cathepsin K-activity by peptidyl vinyl sulfones Biol. Chem. 1999, 380, 679-687
41. Ishibashi, O.; Niwa, S.; Kadoyama, K.; Inui, T. MMP-9 antisense oligodeoxynucleotide exerts an inhibitory effect on osteoclastic bone resorption by suppressing cell migration Life Sci. 2006, 79, 1657-1660
42. Delaisse, J. M.; Andersen, T. L.; Engsig, M. T.; Henriksen, K.; Troen, T.; Blavier, L. Matrix metalloproteinases (MMP) and cathepsin K contribute differently to osteoclastic activities Microsc. Res. Technol. 2003, 61, 504-513
43. Miyazaki, T.; Katagiri, H.; Kanegae, Y.; Takayanagi, H.; Sawada, Y.; Yamamoto, A.; Pando, M. P.; Asano, T.; Verma, I. M.; Oda, H.; Nakamura, K.; Tanaka, S. Reciprocal role of ERK and NF-κB pathways in survival and activation of osteoclasts J. Cell Biol. 2000, 148, 333-342
44. Shiotani, A.; Takami, M.; Itoh, K.; Shibasaki, Y.; Sasaki, T. Regulation of osteoclast differentiation and function by receptor activator of NFκB ligand and osteoprotegerin Anat. Rec. 2002, 268, 137-146
45. Yamashita, T.; Yao, Z.; Li, F.; Zhang, Q.; Badell, I. R.; Schwarz, E. M.; Takeshita, S.; Wagner, E. F.; Noda, M.; Matsuo, K.; Xing, L.; Boyce, B. F. NF-κB p50 and p52 regulate receptor activator of NF-κB ligand (RANKL) and tumor necrosis factor-induced osteoclast precursor differentiation by activating c-Fos and NFATc1 J. Biol. Chem. 2007, 282, 18245-18253
46. Asagiri, M.; Sato, K.; Usami, T.; Ochi, S.; Nishina, H.; Yoshida, H.; Morita, I.; Wagner, E. F.; Mak, T. W.; Serfling, E.; Takayanagi, H. Autoamplification of NFATc1 expression determines its essential role in bone homeostasis J. Exp. Med. 2005, 202, 1261-1269
47. Ishida, N.; Hayashi, K.; Hoshijima, M.; Ogawa, T.; Koga, S.; Miyatake, Y.; Kumegawa, M.; Kimura, T.; Takeya, T. Large scale gene expression analysis of osteoclastogenesis in vitro and elucidation of NFAT2 as a key regulator J. Biol. Chem. 2002, 277, 41147-41156
48. Zhu, Z. W.; Shi, L.; Ruan, X. M.; Yang, Y.; Li, H. Q.; Xu, S. P.; Zhu, H. L. Synthesis and antiproliferative activities against Hep-G2 of salicylanide derivatives: Potent inhibitors of the epidermal growth factor receptor (EGFR) tyrosine kinase J. Enzyme Inhib. Med. Chem. 2011, 26, 37-45
49. Denizot, F.; Lang, R. Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability J. Immunol. Methods 1986, 89, 271-277