Inhibition of microsomal prostaglandin e synthase-1 by aminothiazoles decreases prostaglandin E2 synthesis in vitro and ameliorates experimental periodontitis in vivo

FASEB Journal

Volumn 27, Issue 6, 2013, Pages 2328-2341

  Kats, Anna ^a   Båge, Tove ^a   Georgsson, Pierre ^a   Jönsson, Jörgen ^a   Quezada, Hernán Concha ^a   Gustafsson, Anders ^a   Jansson, Leif ^b   Lindberg, Claes ^c   Näsström, Karin ^a   Yucel Lindberg, Tülay ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b STOCKHOLM COUNTY COUNCIL   (Sweden)

^c Thurne Teknik AB   (Sweden)

Author keywords

Anti inflammatory; Cyclooxygenase 2; Gingival fibroblasts; Interleukin 1 ; MPGES 1 inhibitor; PGE2

Indexed keywords

2 AMINOTHIAZOLE DERIVATIVE; CELECOXIB; CYCLOOXYGENASE 2; DEXAMETHASONE; INTERLEUKIN 1BETA; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2; TH 644; TH 848; TRICLOSAN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIMICROBIAL ACTIVITY; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG CYTOTOXICITY; IC 50; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OSTEOLYSIS; PERIODONTITIS; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT;

ANTI-INFLAMMATORY; CYCLOOXYGENASE-2; GINGIVAL FIBROBLASTS; INTERLEUKIN-1Β; MPGES-1 INHIBITOR; PGE2;

ANIMALS; CELLS, CULTURED; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; DINOPROSTONE; HUMANS; INTRAMOLECULAR OXIDOREDUCTASES; MICROSOMES; PERIODONTITIS; PROSTAGLANDIN ANTAGONISTS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, SPRAGUE-DAWLEY; THIAZOLES;

RATTUS;

EID: 84878763501     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-214445     Document Type: Article

References (67)

1. Armitage, G. C. (2004) Periodontal diagnoses and classification of periodontal diseases. Periodontol. 2000 34, 9-211
2. Kinney, J. S., Ramseier, C. A., and Giannobile, W. V. (2007) Oral fluid-based biomarkers of alveolar bone loss in periodontitis. Ann. N. Y. Acad. Sci. 1098, 230-2511
3. Page, R. C. (1991) The role of inflammatory mediators in the pathogenesis of periodontal disease. J. Periodontal Res. 26, 230-2422
4. Inada, M., Matsumoto, C., Uematsu, S., Akira, S., and Miyaura, C. (2006) Membrane-bound prostaglandin E synthase-1-mediated prostaglandin E2 production by osteoblast plays a critical role in lipopolysaccharide-induced bone loss associated with inflammation. J. Immunol. 177, 1879-18855
5. Blackwell, K. A., Raisz, L. G., and Pilbeam, C. C. (2010) Prostaglandins in bone: bad cop, good cop? Trends Endocrinol. Metab. 21, 294-3011
6. Wang, M., Song, W. L., Cheng, Y., and Fitzgerald, G. A. (2008) Microsomal prostaglandin E synthase-1 inhibition in cardiovascular inflammatory disease. J. Intern. Med. 263, 500-5055
7. 2 and EP receptors in the pathogenesis of rheumatoid arthritis and as a novel therapeutic strategy. Endocr. Metab. Immune Disord. Drug Targets 6, 383-3944
8. Preshaw, P. M., and Heasman, P. A. (2002) Prostaglandin E2 concentrations in gingival crevicular fluid: observations in untreated chronic periodontitis. J. Clin. Periodontol. 29, 15-200
9. Murakami, M., and Kudo, I. (2004) Recent advances in molecular biology and physiology of the prostaglandin E2-biosynthetic pathway. Prog. Lipid Res. 43, 3-355
10. Jakobsson, P. J., Thoren, S., Morgenstern, R., and Samuelsson, B. (1999) Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc. Natl. Acad. Sci. U. S. A. 96, 7220-72255
11. Tanikawa, N., Ohmiya, Y., Ohkubo, H., Hashimoto, K., Kangawa, K., Kojima, M., Ito, S., and Watanabe, K. (2002) Identification and characterization of a novel type of membraneassociated prostaglandin E synthase. Biochem. Biophys. Res. Commun. 291, 884-8899
12. Tanioka, T., Nakatani, Y., Semmyo, N., Murakami, M., and Kudo, I. (2000) Molecular identification of cytosolic prostaglandin E2 synthase that is functionally coupled with cyclooxygenase- 1 in immediate prostaglandin E2 biosynthesis. J. Biol. Chem. 275, 32775-327822
13. Murakami, M., Naraba, H., Tanioka, T., Semmyo, N., Nakatani, Y., Kojima, F., Ikeda, T., Fueki, M., Ueno, A., Oh, S., and Kudo, I. (2000) Regulation of prostaglandin E2 biosynthesis by inducible membrane-associated prostaglandin E2 synthase that acts in concert with cyclooxygenase-2. J. Biol. Chem. 275, 32783-327922
14. Båge, T., Kats, A., Lopez, B. S., Morgan, G., Nilsson, G., Burt, I., Korotkova, M., Corbett, L., Knox, A. J., Pino, L., Jakobsson, P. J., Modeer, T., and Yucel-Lindberg, T. (2011) Expression of prostaglandin E synthases in periodontitis immunolocalization and cellular regulation. Am. J. Pathol. 178, 1676-16888
15. Gudis, K., Tatsuguchi, A., Wada, K., Futagami, S., Nagata, K., Hiratsuka, T., Shinji, Y., Miyake, K., Tsukui, T., Fukuda, Y., and Sakamoto, C. (2005) Microsomal prostaglandin E synthase (mPGES)-1, mPGES-2 and cytosolic PGES expression in human gastritis and gastric ulcer tissue. Lab. Invest. 85, 225-2366
16. Westman, M., Korotkova, M., af Klint, E., Stark, A., Audoly, L. P., Klareskog, L., Ulfgren, A. K., and Jakobsson, P. J. (2004) Expression of microsomal prostaglandin E synthase 1 in rheumatoid arthritis synovium. Arthritis Rheum. 50, 1774-17800
17. Yucel-Lindberg, T., Hallström, T., Kats, A., Mustafa, M., and Modeer, T. (2004) Induction of microsomal prostaglandin E synthase-1 in human gingival fibroblasts. Inflammation 28, 89-955
18. Mustafa, M., Wondimu, B., Yucel-Lindberg, T., Kats, A., Hallström, T., Jonsson, A. S., and Modeer, T. (2005) Triclosan reduces microsomal prostaglandin E synthase-1 expression in human gingival fibroblasts. J. Clin. Periodontol. 32, 6-111
19. Turini, M. E., and DuBois, R. N. (2002) Cyclooxygenase-2: a therapeutic target. Annu. Rev. Med. 53, 35-577
20. Chen, Y. F., Jobanputra, P., Barton, P., Bryan, S., Fry-Smith, A., Harris, G., and Taylor, R. S. (2008) Cyclooxygenase-2 selective non-steroidal anti-inflammatory drugs (etodolac, meloxicam, celecoxib, rofecoxib, etoricoxib, valdecoxib and lumiracoxib) for osteoarthritis and rheumatoid arthritis: a systematic review and economic evaluation. Health Technol. Assess. 12, 1-278, iiii
21. Anderson, G. D., Keys, K. L., De Ciechi, P. A., and Masferrer, J. L. (2009) Combination therapies that inhibit cyclooxygenase- 2 and leukotriene synthesis prevent disease in murine collagen induced arthritis. Inflamm. Res. 58, 109-1177
22. Koeberle, A., and Werz, O. (2009) Inhibitors of the microsomal prostaglandin E(2) synthase-1 as alternative to non steroidal anti-inflammatory drugs (NSAIDs)-a critical review. Curr. Med. Chem. 16, 4274-42966
23. Ng, S. C., and Chan, F. K. (2010) NSAID-induced gastrointestinal and cardiovascular injury. Curr. Opin. Gastroenterol. 26, 611-6177
24. Sanghi, S., MacLaughlin, E. J., Jewell, C. W., Chaffer, S., Naus, P. J., Watson, L. E., and Dostal, D. E. (2006) Cyclooxygenase-2 inhibitors: a painful lesson. Cardiovasc. Hematol. Disord. Drug Targets 6, 85-1000
25. Cannon, C. P., and Cannon, P. J. (2012) Physiology. COX-2 inhibitors and cardiovascular risk. Science 336, 1386-13877
26. 2 secretion as a determinant of periodontal disease expression. J. Periodontol. 64, 432-4444
27. Pouliot, M., Clish, C. B., Petasis, N. A., Van Dyke, T. E., and Serhan, C. N. (2000) Lipoxin A(4) analogues inhibit leukocyte recruitment to Porphyromonas gingivalis: a role for cyclooxygenase- 2 and lipoxins in periodontal disease. Biochemistry 39, 4761-47688
28. 2 and IL-1 beta in the gingival crevicular fluid of adults with periodontitis: its relationship to alveolar bone loss and disruption by twice daily treatment with ketorolac tromethamine oral rinse. J. Periodontal. Res. 33, 75-822
29. Hasturk, H., Kantarci, A., Goguet-Surmenian, E., Blackwood, A., Andry, C., Serhan, C. N., and Van Dyke, T. E. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 179, 7021-70299
30. Hasturk, H., Kantarci, A., Ohira, T., Arita, M., Ebrahimi, N., Chiang, N., Petasis, N. A., Levy, B. D., Serhan, C. N., and Van Dyke, T. E. (2006) RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J. 20, 401-4033
31. Salvi, G. E., and Lang, N. P. (2005) The effects of non-steroidal anti-inflammatory drugs (selective and non-selective) on the treatment of periodontal diseases. Curr. Pharm. Des. 11, 1757-17699
32. Yen, C. A., Damoulis, P. D., Stark, P. C., Hibberd, P. L., Singh, M., and Papas, A. S. (2008) The effect of a selective cyclooxygenase- 2 inhibitor (celecoxib) on chronic periodontitis. J. Periodontol. 79, 104-1133
33. Blinkhorn, A., Bartold, P. M., Cullinan, M. P., Madden, T. E., Marshall, R. I., Raphael, S. L., and Seymour, G. J. (2009) Is there a role for Triclosan/copolymer toothpaste in the management of periodontal disease? Br. Dent. J. 207, 117-1255
34. Luan, Q., Desta, T., Chehab, L., Sanders, V. J., Plattner, J., and Graves, D. T. (2008) Inhibition of experimental periodontitis by a topical boron-based antimicrobial. J. Dent. Res. 87, 148-1522
35. Mancini, J. A., Blood, K., Guay, J., Gordon, R., Claveau, D., Chan, C. C., and Riendeau, D. (2001) Cloning, expression, and up-regulation of inducible rat prostaglandin e synthase during lipopolysaccharide-induced pyresis and adjuvant-induced arthritis. J. Biol. Chem. 276, 4469-44755
36. Båge, T., Modeer, T., Kawakami, T., Quezada, H. C., and Yucel-Lindberg, T. (2007) Regulation of prostaglandin E synthases: effects of siRNA-mediated inhibition of microsomal prostaglandin E synthase-1. Biochim. Biophys. Acta 1773, 1589-15988
37. Koeberle, A., Northoff, H., and Werz, O. (2009) Curcumin blocks prostaglandin E2 biosynthesis through direct inhibition of the microsomal prostaglandin E2 synthase-1. Mol. Cancer Ther. 8, 2348-23555
38. Moon, Y., Glasgow, W. C., and Eling, T. E. (2005) Curcumin suppresses interleukin 1beta-mediated microsomal prostaglandin E synthase 1 by altering early growth response gene 1 and other signaling pathways. J. Pharmacol. Exp. Ther. 315, 788-7955
39. Guimaraes, M. R., de Aquino, S. G., Coimbra, L. S., Spolidorio, L. C., Kirkwood, K. L., and Rossa, C., Jr. (2012) Curcumin modulates the immune response associated with LPS-induced periodontal disease in rats. Innate Immun. 18, 155-1633
40. Tonetti, M. S., and Chapple, I. L. (2011) Biological approaches to the development of novel periodontal therapies-consensus of the Seventh European Workshop on Periodontology. J. Clin. Periodontol. 38(Suppl. 11), 114-1188
41. Nishikaku, F., and Koga, Y. (1993) Suppression of murine collagen-induced arthritis by treatment with a novel thiazole derivative, SM-8849. Immunopharmacology 25, 65-744
42. Ohno, H., Uemura, Y., Murooka, H., Takanashi, H., Tokieda, T., Ohzeki, Y., Kubo, K., and Serizawa, I. (2008) The orallyactive and selective c-Fms tyrosine kinase inhibitor Ki20227 inhibits disease progression in a collagen-induced arthritis mouse model. Eur. J. Immunol. 38, 283-2911
43. Cho, Y. S., Kim, C. H., Surh, J. H., Kang, N. S., Yoo, S. E., and Cheon, H. G. (2010) Identification of 4-[4-(4-fluoro-phenyl)- thiazol-2-ylamino]-2,6- dimethyl-phenol (KR-33749) as an inhibitor of 5-lipoxygenase with potent antiinflammatory activity. Pharmacology 86, 65-722
44. Moldovan, C. M., Oniga, O., Parvu, A., Tiperciuc, B., Verite, P., Pirnau, A., Crisan, O., Bojita, M., and Pop, R. (2011) Synthesis and anti-inflammatory evaluation of some new acyl-hydrazones bearing 2-aryl-thiazole. Eur. J. Med. Chem. 46, 526-5344
45. Trott, O., and and Olson, A. J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-4611
46. Jegerschold, C., Pawelzik, S. C., Purhonen, P., Bhakat, P., Gheorghe, K. R., Gyobu, N., Mitsuoka, K., Morgenstern, R., Jakobsson, P. J., and Hebert, H. (2008) Structural basis for induced formation of the inflammatory mediator prostaglandin E2. Proc. Natl. Acad. Sci. U. S. A. 105, 11110-111155
47. Yucel-Lindberg, T., Olsson, T., and Kawakami, T. (2006) Signal pathways involved in the regulation of prostaglandin E synthase- 1 in human gingival fibroblasts. Cell. Signal. 18, 2131-21422
48. Friesen, R. W., and Mancini, J. A. (2008) Microsomal prostaglandin E2 synthase-1 (mPGES-1): a novel anti-inflammatory therapeutic target. J. Med. Chem. 51, 4059-40677
49. Båge, T., Lindberg, J., Lundeberg, J., Modeer, T., and Yucel- Lindberg, T. (2010) Signal pathways JNK and NF-kappaB, identified by global gene expression profiling, are involved in regulation of TNFalpha-induced mPGES-1 and COX-2 expression in gingival fibroblasts. BMC Genomics 11, 2411
50. Koeberle, A., Siemoneit, U., Buhring, U., Northoff, H., Laufer, S., Albrecht, W., and Werz, O. (2008) Licofelone suppresses prostaglandin E2 formation by interference with the inducible microsomal prostaglandin E2 synthase-1. J. Pharmacol. Exp. Ther. 326, 975-9822
51. Rosenstock, M., Danon, A., and Rimon, G. (1999) PGHS-2 inhibitors, NS-398 and DuP-697, attenuate the inhibition of PGHS-1 by aspirin and indomethacin without altering its activity. Biochim. Biophys. Acta 1440, 127-1377
52. Di Paola, R., Mazzon, E., Maiere, D., Zito, D., Britti, D., De Majo, M., Genovese, T., and Cuzzocrea, S. (2006) Rosiglitazone reduces the evolution of experimental periodontitis in the rat. J. Dent. Res. 85, 156-1611
53. Pawelzik, S. C., Uda, N. R., Spahiu, L., Jegerschold, C., Stenberg, P., Hebert, H., Morgenstern, R., and Jakobsson, P. J. (2010) Identification of key residues determining species differences in inhibitor binding of microsomal prostaglandin E synthase-1. J. Biol. Chem. 285, 29254-292611
54. Tseng, C. H., Tzeng, C. C., Shih, P. K., Yang, C. N., Chuang, Y. C., Peng, S. I., Lin, C. S., Wang, J. P., Cheng, C. M., and Chen, Y. L. (2012) Identification of furo[3=, 2=:3,4]naphtho[1,2-d]imidazole derivatives as orally active and selective inhibitors of microsomal prostaglandin E(2) synthase-1 (mPGES-1). Mol. Divers. 16, 215-2299
55. Chang, H. H., and Meuillet, E. J. (2011) Identification and development of mPGES-1 inhibitors: where we are at? Future Med. Chem. 3, 1909-19344
56. Capone, M. L., Tacconelli, S., Di Francesco, L., Sacchetti, A., Sciulli, M. G., and Patrignani, P. (2007) Pharmacodynamic of cyclooxygenase inhibitors in humans. Prostaglandins Other Lipid Mediat. 82, 85-944
57. El-Rayes, B. F., Ali, S., Sarkar, F. H., and Philip, P. A. (2004) Cyclooxygenase-2-dependent and -independent effects of celecoxib in pancreatic cancer cell lines. Mol. Cancer Ther. 3, 1421-14266
58. Barnes, P. J. (2005) Molecular mechanisms and cellular effects of glucocorticosteroids. Immunol. Allergy Clin. North Am. 25, 451-4688
59. Cheng, W. C., Huang, R. Y., Chiang, C. Y., Chen, J. K., Liu, C. H., Chu, C. L., and Fu, E. (2010) Ameliorative effect of quercetin on the destruction caused by experimental periodontitis in rats. J. Periodontal Res. 45, 788-7955
60. Guimaraes, M. R., Coimbra, L. S., de Aquino, S. G., Spolidorio, L. C., Kirkwood, K. L., and Rossa, C., Jr. (2011) Potent antiinflammatory effects of systemically administered curcumin modulate periodontal disease in vivo. J. Periodontal Res. 46, 269-2799
61. Bruno, A., Di Francesco, L., Coletta, I., Mangano, G., Alisi, M. A., Polenzani, L., Milanese, C., Anzellotti, P., Ricciotti, E., Dovizio, M., Di Francesco, A., Tacconelli, S., Capone, M. L., and Patrignani, P. (2010) Effects of AF3442 [N-(9-ethyl-9H-carbazol- 3-yl)-2-(trifluoromethyl)benzamide], a novel inhibitor of human microsomal prostaglandin E synthase-1, on prostanoid biosynthesis in human monocytes in vitro. Biochem. Pharmacol. 79, 974-9811
62. Giroux, A., Boulet, L., Brideau, C., Chau, A., Claveau, D., Cote, B., Ethier, D., Frenette, R., Gagnon, M., Guay, J., Guiral, S., Mancini, J., Martins, E., Masse, F., Methot, N., Riendeau, D., Rubin, J., Xu, D., Yu, H., Ducharme, Y., and Friesen, R. W. (2009) Discovery of disubstituted phenanthrene imidazoles as potent, selective and orally active mPGES-1 inhibitors. Bioorg. Med. Chem. Lett. 19, 5837-58411
63. Mbalaviele, G., Pauley, A. M., Shaffer, A. F., Zweifel, B. S., Mathialagan, S., Mnich, S. J., Nemirovskiy, O. V., Carter, J., Gierse, J. K., Wang, J. L., Vazquez, M. L., Moore, W. M., and Masferrer, J. L. (2010) Distinction of microsomal prostaglandin E synthase-1 (mPGES-1) inhibition from cyclooxygenase-2 inhibition in cells using a novel, selective mPGES-1 inhibitor. Biochem. Pharmacol. 79, 1445-14544
64. Ricart, M., Guasch, H., Alberch, M., Barcelo, D., Bonnineau, C., Geiszinger, A., Farre, M., Ferrer, J., Ricciardi, F., Romani, A. M., Morin, S., Proia, L., Sala, L., Sureda, D., and Sabater, S. (2010) Triclosan persistence through wastewater treatment plants and its potential toxic effects on river biofilms. Aquat. Toxicol. 100, 346-3533
65. Saleh, S., Haddadin, R. N., Baillie, S., and Collier, P. J. (2011) Triclosan - an update. Lett. Appl. Microbiol. 52, 87-955
66. Nishikaku, F., Aono, S., and Koga, Y. (1994) Protective effects of D-penicillamine and a thiazole derivative, SM-8849, on pristaneinduced arthritis in mice. Int. J. Immunopharmacol. 16, 91-1000
67. Chang, H. H., Song, Z., Wisner, L., Tripp, T., Gokhale, V., and Meuillet, E. J. (2011) Identification of a novel class of antiinflammatory compounds with anti-tumor activity in colorectal and lung cancers. Invest. New Drugs 30, 1865-18777