The H2S-releasing naproxen derivative, ATB-346, inhibits alveolar bone loss and inflammation in rats with ligature-induced periodontitis

Medical Gas Research

Volumn 5, Issue 1, 2015, Pages

  Herrera, Bruno Schneider ^a,b   Coimbra, Leila Santana ^b   Da Silva, Agatha Ribeiro ^a   Teixeira, Simone Aparecida ^a   Costa, Soraia Katia Pereira ^a   Wallace, John Lawrence ^c   Spolidorio, Luis Carlos ^b   Muscara, Marcelo Nicolas ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

ATB 346; Bone loss; H2S releasing NSAID; Inflammation; Periodontitis

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MYELOPEROXIDASE; NAPROXEN; NAPROXEN DERIVATIVE; UNCLASSIFIED DRUG; [2 (6 METHOXYNAPTHALEN 2 YL)PROPIONIC ACID 4 THIOCARBAMOYLPHENYL ESTER];

ADULT; ALVEOLAR BONE LOSS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE DEFECT; CONTROLLED STUDY; HOLTZMAN RAT; MALE; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; PERIODONTITIS; PRIORITY JOURNAL; RAT; STOMACH MUCOSA LESION;

EID: 84930188964     PISSN: None     EISSN: 20459912     Source Type: Journal    
DOI: 10.1186/s13618-015-0025-3     Document Type: Article

References (55)

1. Page RC, Eke PI. Case definitions for use in population-based surveillance of periodontitis. J Periodontol. 2007;78(7 Suppl):1387-99.
2. Van Dyke TE, Serhan CN. Resolution of inflammation: A new paradigm for the pathogenesis of periodontal diseases. J Dent Res. 2003;82:82-90.
3. Kantarci A, Hasturk H, Van Dyke TE. Host-mediated resolution of inflammation in periodontal diseases. Periodontology 2000. 2006;40:144-63.
4. The J, Ebersole JL. Rheumatoid factor (RF) distribution in periodontal disease. J Clin Immunol. 1991;11:132-42.
5. Boggess KA, Lieff S, Murtha AP, Moss K, Beck J, Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia. Obstet Gynecol. 2003;101:227-31.
6. Offenbacher S, Boggess KA, Murtha AP, Jared HL, Lieff S, McKaig RG, et al. Progressive periodontal disease and risk of very preterm delivery. Obstet Gynecol. 2006;107:29-36.
7. Taylor GW, Burt BA, Becker MP, Genco RJ, Shlossman M, Knowler WC, et al. Severe periodontitis and risk for poor glycemic control in patients with noninsulin- dependent diabetes mellitus. J Periodontol. 1996;67(10 Suppl):1085-93.
8. Friedewald VE, Kornman KS, Beck JD, Genco R, Goldfine A, Libby P, et al. The american journal of cardiology and journal of periodontology editors' consensus: periodontitis and atherosclerotic cardiovascular disease. J Periodontol. 2009;80:1021-32.
9. Fredman G, Oh SF, Ayilavarapu S, Hasturk H, Serhan CN, Van Dyke TE. Impaired phagocytosis in localized aggressive periodontitis: rescue by resolvin E1. PLoS One. 2011;6:e24422.
10. Hasturk H, Kantarci A, Ohira T, Arita M, Ebrahimi N, Chiang N, et al. RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J. 2006;20:401-3.
11. Morton RS, Dongari-Bagtzoglou AI. Cyclooxygenase-2 is upregulated in inflamed gingival tissues. J Periodontol. 2001;72:461-9.
12. Offenbacher S, Heasman PA, Collins JG. Modulation of host PGE2 secretion as a determinant of periodontal disease expression. J Periodontol. 1993;64(5 Suppl):432-44.
13. Drisko CH. Non-surgical pocket therapy: pharmacotherapeutics. Ann Periodontol. 1996;1:491-566.
14. Holzhausen M, Spolidorio DM, Muscara MN, Hebling J, Spolidorio LC. Protective effects of etoricoxib, a selective inhibitor of cyclooxygenase-2, in experimental periodontitis in rats. J Periodontal Res. 2005;40:208-11.
15. Holzhausen M, Rossa Junior C, Marcantonio Junior E, Nassar PO, Spolidorio DM, Spolidorio LC. Effect of selective cyclooxygenase-2 inhibition on the development of ligature-induced periodontitis in rats. J Periodontol. 2002;73:1030-6.
16. Salvi GE, Lang NP. The effects of non-steroidal anti-inflammatory drugs (selective and non-selective) on the treatment of periodontal diseases. Curr Pharm Des. 2005;11:1757-69.
17. Howell TH, Jeffcoat MK, Goldhaber P, Reddy MS, Kaplan ML, Johnson HG, et al. Inhibition of alveolar bone loss in beagles with the NSAID naproxen. J Periodontal Res. 1991;26:498-501.
18. Aras H, Caglayan F, Guncu GN, Berberoglu A, Kilinc K. Effect of systemically administered naproxen sodium on clinical parameters and myeloperoxidase and elastase-like activity levels in gingival crevicular fluid. J Periodontol. 2007;78:868-73.
19. Tsai CC, Hong YC, Chen CC, Wu YM. Measurement of prostaglandin E2 and leukotriene B4 in the gingival crevicular fluid. J Dent. 1998;26:97-103.
20. Grosser T, Fries S, FitzGerald GA. Biological basis for the cardiovascular consequences of COX-2 inhibition: Therapeutic challenges and opportunities. J Clin Invest. 2006;116:4-15.
21. Wallace JL. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesn't the stomach digest itself? Physiol Rev. 2008;88:1547-65.
22. Muscara MN, Wallace JL. COX-inhibiting nitric oxide donors (CINODs): potential benefits on cardiovascular and renal function. Cardiovasc Hematol Agents Med Chem. 2006;4:155-64.
23. Distrutti E, Sediari L, Mencarelli A, Renga B, Orlandi S, Russo G, et al. 5-Amino-2-hydroxybenzoic acid 4-(5-thioxo-5H-[1, 2]dithiol-3yl)-phenyl ester (ATB-429), a hydrogen sulfide-releasing derivative of mesalamine, exerts antinociceptive effects in a model of postinflammatory hypersensitivity. J Pharmacol Exp Ther. 2006;319:447-58.
24. Fiorucci S, Orlandi S, Mencarelli A, Caliendo G, Santagada V, Distrutti E, et al. Enhanced activity of a hydrogen sulphide-releasing derivative of mesalamine (ATB-429) in a mouse model of colitis. Br J Pharmacol. 2007;150:996-1002.
25. Wallace JL, Caliendo G, Santagada V, Cirino G. Markedly reduced toxicity of a hydrogen sulphide-releasing derivative of naproxen (ATB-346). Br J Pharmacol. 2010;159:1236-46.
26. Wallace JL, Caliendo G, Santagada V, Cirino G, Fiorucci S. Gastrointestinal safety and anti-inflammatory effects of a hydrogen sulfide-releasing diclofenac derivative in the rat. Gastroenterology. 2007;132:261-71.
27. Wallace JL. Hydrogen sulfide-releasing anti-inflammatory drugs. Trends Pharmacol Sci. 2007;28:501-5.
28. Blackler R, Syer S, Bolla M, Ongini E, Wallace JL. Gastrointestinal-sparing effects of novel NSAIDs in rats with compromised mucosal defence. PLoS One. 2012;7:e35196.
29. Campolo M, Esposito E, Ahmad A, Di Paola R, Wallace JL, Cuzzocrea S. A hydrogen sulfide-releasing cyclooxygenase inhibitor markedly accelerates recovery from experimental spinal cord injury. FASEB J. 2013;27:4489-99.
30. Ekundi-Valentim E, Mesquita FP, Santos KT, de Paula MA, Florenzano J, Zanoni CI, et al. A comparative study on the anti-inflammatory effects of single oral doses of naproxen and its hydrogen sulfide (H2S)-releasing derivative ATB-346 in rats with carrageenan-induced synovitis. Med Gas Res. 2013;3:24.
31. Irie K, Ekuni D, Yamamoto T, Morita M, Yaegaki K, Ii H, et al. A single application of hydrogen sulphide induces a transient osteoclast differentiation with RANKL expression in the rat model. Arch Oral Biol. 2009;54(8):723-9.
32. Irie K, Ekuni D, Tomofuji T, Endo Y, Kasuyama K, Yaegaki K, et al. Combined effects of hydrogen sulfide and lipopolysaccharide on osteoclast differentiation in rats. J Periodontol. 2012;83:522-7.
33. Toker H, Balci Yuce H, Goze F, Ozdemir H, Akpinar A, Bostanci V. The effects of hydrogen sulphide on alveolar bone loss in periodontitis. Minerva Stomatol. 2014;63:103-10.
34. Sallay K, Sanavi F, Ring I, Pham P, Behling UH, Nowotny A. Alveolar bone destruction in the immunosuppressed rat. J Periodontal Res. 1982;17:263-74.
35. Wilensky A, Gabet Y, Yumoto H, Houri-Haddad Y, Shapira L. Three-dimensional quantification of alveolar bone loss in Porphyromonas gingivalis-infected mice using micro-computed tomography. J Periodontol. 2005;76:1282-6.
36. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-54.
37. Wallace JL, McCafferty DM, Carter L, McKnight W, Argentieri D. Tissue-selective inhibition of prostaglandin synthesis in rat by tepoxalin: Anti-inflammatory without gastropathy. Gastroenterology. 1993;105:1630-6.
38. Herrera BS, Martins-Porto R, Campi P, Holzhausen M, Teixeira SA, Mendes GD, et al. Local and cardiorenal effects of periodontitis in nitric oxide-deficient hypertensive rats. Arch Oral Biol. 2011;56:41-7.
39. Page RC, Kornman KS. The pathogenesis of human periodontitis: An introduction. Periodontology 2000. 1997;14:9-11.
40. Herrera BS, Martins-Porto R, Maia-Dantas A, Campi P, Spolidorio LC, Costa SK, et al. iNOS-derived nitric oxide stimulates osteoclast activity and alveolar bone loss in ligature-induced periodontitis in rats. J Periodontol. 2011;82:1608-15.
41. Serhan CN, Brain SD, Buckley CD, Gilroy DW, Haslett C, O'Neill LA, et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 2007;21:325-32.
42. Ciancio SG. Systemic medications: clinical significance in periodontics. J Clin Periodontol. 2002;29 Suppl 2:17-21.
43. Wang R. Physiological implications of hydrogen sulfide: A whiff exploration that blossomed. Physiol Rev. 2012;92:791-896.
44. Kimura H. Hydrogen sulfide: its production, release and functions. Amino Acids. 2011;41:113-21.
45. Flannigan KL, Ferraz JG, Wang R, Wallace JL. Enhanced synthesis and diminished degradation of hydrogen sulfide in experimental colitis: A site-specific, pro-resolution mechanism. PLoS One. 2013;8:e71962.
46. Dufton N, Natividad J, Verdu EF, Wallace JL. Hydrogen sulfide and resolution of acute inflammation: A comparative study utilizing a novel fluorescent probe. Scientific Reports. 2012;2:499.
47. Van Dyke TE. The management of inflammation in periodontal disease. J Periodontol. 2008;79(8 Suppl):1601-8.
48. El-Sharkawy H, Aboelsaad N, Eliwa M, Darweesh M, Alshahat M, Kantarci A, et al. Adjunctive treatment of chronic periodontitis with daily dietary supplementation with omega-3 fatty acids and low-dose aspirin. J Periodontol. 2010;81(11):1635-43.
49. Guo W, Cheng ZY, Zhu YZ. Hydrogen sulfide and translational medicine. Acta Pharmacol Sin. 2013;34:1284-91.
50. Wang R. Signaling pathways for the vascular effects of hydrogen sulfide. Curr Opin Nephrol Hypertens. 2011;20:107-12.
51. Szabo G, Veres G, Radovits T, Gero D, Modis K, Miesel-Groschel C, et al. Cardioprotective effects of hydrogen sulfide. Nitric Oxide. 2011;25:201-10.
52. Matsunami M, Kirishi S, Okui T, Kawabata A. Chelating luminal zinc mimics hydrogen sulfide-evoked colonic pain in mice: possible involvement of T-type calcium channels. Neuroscience. 2011;181:257-64.
53. Chattopadhyay M, Kodela R, Nath N, Barsegian A, Boring D, Kashfi K. Hydrogen sulfide-releasing aspirin suppresses NF-kappaB signaling in estrogen receptor negative breast cancer cells in vitro and in vivo. Biochem Pharmacol. 2012;83:723-32.
54. Caro AA, Thompson S, Tackett J. Increased oxidative stress and cytotoxicity by hydrogen sulfide in HepG2 cells overexpressing cytochrome P450 2E1. Cell Biol Toxicol. 2011;27:439-53.
55. Lee SK, Chung JH, Choi SC, Auh QS, Lee YM, Lee SI, et al. Sodium hydrogen sulfide inhibits nicotine and lipopolysaccharide-induced osteoclastic differentiation and reversed osteoblastic differentiation in human periodontal ligament cells. J Cell Biochem. 2013;114:1183-93.