A biochemical and immunohistochemical study of the effects of caffeic acid phenethyl ester on alveolar bone loss and oxidative stress in diabetic rats with experimental periodontitis

References

• Akman S, Canakci V, Kara A, Tozoglu U, Arabaci T, Dagsuyu İM. 2013. Therapeutic effects of alpha lipoic acid and vitamin C on alveolar bone resorption after experimental periodontitis in rats: a biochemical, histochemical, and stereologic study. J Periodontol. 84:666–674.
   PubMed Web of Science ®Google Scholar
• Akyol S, Ginis Z, Armutcu F, Ozturk G, Yigitoglu MR, Akyol O. 2012. The potential usage of caffeic acid phenethyl ester (CAPE) against chemotherapy-induced and radiotherapy-induced toxicity. Cell Biochem Funct. 30:438–443.
   PubMed Web of Science ®Google Scholar
• Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, Teepe MC, DuBose RF, Cosman D, Galibert L. 1997. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic cell function. Nature. 390:175–179.
   PubMed Web of Science ®Google Scholar
• Andrukhov O, Ulm C, Reischl H, Nguyen PQ, Matejka M, Rausch-Fan X. 2011. Serum cytokine levels in periodontitis patients in relation to the bacterial load. J Periodontol. 82:885–892.
   PubMed Web of Science ®Google Scholar
• Arabaci T, Kermen E, Ozkanlar S, Kose O, Kara A, Kizildag A, Duman SB, Ibisoglu E. 2015. Therapeutic effects of melatonin on alveolar bone resorption after experimental periodontitis in rats: a biochemical and immunohistochemical study. J Periodontol. 86:874–881.
   PubMed Web of Science ®Google Scholar
• Araujo AA, Souza TO, Moura LM, Brito GA, Aragao KS, Araujo LS, Medeiros CA, Alves MS, Araujo RF, Jr. 2013. Effect of telmisartan on levels of IL-1, TNF-alpha, down-regulated COX-2, MMP-2, MMP-9 and RANKL/RANK in an experimental periodontitis model. J Clin Periodontol. 40:1104–1111.
   PubMed Web of Science ®Google Scholar
• Balci Yuce H, Toker H, Goze F. 2014. The histopathological and morphometric investigation of the effects of systemically administered boric acid on alveolar bone loss in ligature-induced periodontitis in diabetic rats. Acta Odontol Scand. 72:729–736.
   PubMed Web of Science ®Google Scholar
• Baltacıoğlu E, Yuva P, Aydın G, Alver A, Kahraman C, Karabulut E, Akalın FA. 2014. Lipid peroxidation levels and total oxidant/antioxidant status in serum and saliva from patients with chronic and aggressive periodontitis. Oxidative stress index: a new biomarker for periodontal disease? J Periodontol. 85:1432–1441.
   Google Scholar
• Cekici A, Kantarci A, Hasturk H, Van Dyke TE. 2014. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontology 2000. 64:57–80.
   PubMed Web of Science ®Google Scholar
• Celik S, Gorur S, Aslantas O, Erdogan S, Ocak S, Hakverdi S. 2007. Caffeic acid phenethyl ester suppresses oxidative stress in Escherichia coli-induced pyelonephritis in rats. Mol Cell Biochem. 297:131–138.
   PubMed Web of Science ®Google Scholar
• Celik S, Erdogan S. 2008. Caffeic acid phenethyl ester (CAPE) protects brain against oxidative stress and inflammation induced by diabetes in rats. Mol Cell Biochem. 312:39–46.
   PubMed Web of Science ®Google Scholar
• Celik S, Erdogan S, Tuzcu M. 2009. Caffeic acid phenethyl ester (CAPE) exhibits significant potential as an antidiabetic and liver-protective agent in streptozotocin-induced diabetic rats. Pharmacol Res. 60:270–276.
   PubMed Web of Science ®Google Scholar
• Esen C, Alkan BA, Kirnap M, Akgul O, Isikoglu S, Erel O. 2012. The effects of chronic periodontitis and rheumatoid arthritis on serum and gingival crevicular fluid total antioxidant/oxidant status and oxidative stress index. J Periodontol. 83:773–779.
   PubMed Web of Science ®Google Scholar
• Gilowski Ł, Wiench R, Płocica I, Krzemiński TF. 2014. Amount of interleukin-1β and interleukin-1 receptor antagonist in periodontitis and healthy patients. Arch Oral Biol. 59:729–734.
   PubMed Web of Science ®Google Scholar
• Gowen M, Wood DD, Ihrie EJ, McGuire MK, Russell RG. 1983. An interleukin 1 like factor stimulates bone resorption in vitro. Nature. 306:378–380.
   PubMed Web of Science ®Google Scholar
• Gurkan A, Emingil G, Nizam N, Doganavsargil B, Sezak M, Kutukculer N, Atilla G. 2009. Therapeutic efficacy of vasoactive intestinal peptide in Escherichia coli lipopolysaccharide-induced experimental periodontitis in rats. J Periodontol. 80:1655–1664.
   PubMed Web of Science ®Google Scholar
• Ha J, Choi HS, Lee Y, Lee ZH, Kim HH. 2009. Caffeic acid phenethyl ester inhibits osteoclastogenesis by suppressing NFκB and downregulating NFATc1 and c-Fos. Int Immunopharmacol. 9:774–780.
   PubMed Web of Science ®Google Scholar
• Jiang ZL, Cui YQ, Gao R, Li Y, Fu ZC, Zhang B, Guan CC. 2013. Study of TNF-alpha, IL-1beta and LPS levels in the gingival crevicular fluid of a rat model of diabetes mellitus and periodontitis. Dis Mark. 34:295–304.
   PubMed Web of Science ®Google Scholar
• Karima M, Kantarci A, Ohira T, Hasturk H, Jones VL, Nam BH, Malabanan A, Trackman PC, Badwey JA, Van Dyke TE. 2005. Enhanced superoxide release and elevated protein kinase C activity in neutrophils from diabetic patients: association with periodontitis. J Leuk Biol. 78:862–870.
   PubMed Web of Science ®Google Scholar
• Kazancioglu HO, Aksakalli S, Ezirganli S, Birlik M, Esrefoglu M, Acar AH. 2015a. Effect of caffeic acid phenethyl ester on bone formation in the expanded inter-premaxillary suture. Drug Des Devel Ther. 9:6483–6488.
   Google Scholar
• Kazancioglu HO, Bereket MC, Ezirganli S, Aydin MS, Aksakalli S. 2015b. Effects of caffeic acid phenethyl ester on wound healing in calvarial defects. Acta Odontol Scand. 73:21–27.
   PubMed Web of Science ®Google Scholar
• Kim JH, Lee DE, Woo GH, Cha JH, Bak EJ, Yoo YJ. 2015. Osteocytic sclerostin expression in alveolar bone in rats with diabetes mellitus and ligature-induced periodontitis. J Periodontol. 86:1005–1011.
   PubMed Web of Science ®Google Scholar
• Koltuksuz U, Mutus HM, Kutlu R, Ozyurt H, Cetin S, Karaman A, Gurbuz N, Akyol O, Aydin NE. 2001. Effects of caffeic acid phenethyl ester and epidermal growth factor on the development of caustic esophageal stricture in rats. J Pediatr Surg. 36:1504–1509.
   PubMed Web of Science ®Google Scholar
• Kose O, Arabaci T, Kara A, Yemenoglu H, Kermen E, Kizildag A, Gedikli S, Ozkanlar S. 2016. Effects of melatonin on oxidative stress index and alveolar bone loss in diabetic rats with periodontitis. J Periodontol. 87:82–90.
   PubMed Web of Science ®Google Scholar
• Kose O, Arabaci T, Kizildag A, Erdemci B, Ozkal Eminoglu D, Gedikli S, Ozkanlar S, Zihni M, Albayrak M, Kara A, Kermen E. 2017. Melatonin prevents radiation-induced oxidative stress and periodontal tissue breakdown in irradiated rats with experimental periodontitis. J Periodontal Res. 52:438–446.
   PubMed Web of Science ®Google Scholar
• Lappin DF, Eapen B, Robertson D, Young J, Hodge PJ. 2009. Markers of bone destruction and formation and periodontitis in type 1 diabetes mellitus. J Clin Periodontol. 36:634–641.
   PubMed Web of Science ®Google Scholar
• Leitao RF, Ribeiro RA, Chaves HV, Rocha FA, Lima V, Brito GA. 2005. Nitric oxide synthase inhibition prevents alveolar bone resorption in experimental periodontitis in rats. J Periodontol. 76:956–963.
   PubMed Web of Science ®Google Scholar
• Llavaneras A, Ramamurthy NS, Heikkila P, Teronen O, Salo T, Rifkin BR, Ryan ME, Golub LM, Sorsa T. 2001. A combination of a chemically modified doxycycline and a bisphosphonate synergistically inhibits endotoxin-induced periodontal breakdown in rats. J Periodontol. 72:1069–1077.
   PubMed Web of Science ®Google Scholar
• Lowe GD. 2001. The relationship between infection, inflammation, and cardiovascular disease: an overview. Ann Periodontol. 6:1–8.
   PubMedGoogle Scholar
• Lutfioglu M, Sakallioglu U, Sakallioglu EE, Baris S, Gurgor P. 2012. The impact of dietary induced hyperparathyroidism on healthy and diseased periodontia: an experimental study in rats. J Clin Periodontol. 39:264–271.
   PubMed Web of Science ®Google Scholar
• Major CD, Gao ZY, Wolf BA. 1999. Activation of the sphingomyelinase/ceramide signal transduction pathway in insulin-secreting beta-cells: role in cytokine-induced beta-cell death. Diabetes. 48:1372–1380.
   PubMed Web of Science ®Google Scholar
• Michaluart P, Masferrer JL, Carothers AM, Subbaramaiah K, Zweifel BS, Koboldt C, Mestre JR, Grunberger D, Sacks PG, Tanabe T, Dannenberg AJ. 1999. Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation. Cancer Res. 59:2347–2352.
   PubMed Web of Science ®Google Scholar
• Nassar H, Kantarci A, van Dyke TE. 2007. Diabetic periodontitis: a model for activated innate immunity and impaired resolution of inflammation. Periodontol 2000. 43:233–244.
   PubMed Web of Science ®Google Scholar
• Okutan H, Ozcelik N, Yilmaz HR, Uz E. 2005. Effects of caffeic acid phenethyl ester on lipid peroxidation and antioxidant enzymes in diabetic rat heart. Clin Biochem. 38:191–196.
   PubMed Web of Science ®Google Scholar
• Park EH, Kahng JH. 1999. Suppressive effects of propolis in rat adjuvant arthritis. Arch Pharm Res. 22:554–558.
   PubMed Web of Science ®Google Scholar
• Rains JL, Jain SK. 2011. Oxidative stress, insulin signaling, and diabetes. Free Rad Biol Med. 50:567–575.
   PubMed Web of Science ®Google Scholar
• Santos VR, Lima JA, Goncalves TE, Bastos MF, Figueiredo LC, Shibli JA, Duarte PM. 2010. Receptor activator of nuclear factor-kappa B ligand/osteoprotegerin ratio in sites of chronic periodontitis of subjects with poorly and well-controlled type 2 diabetes. J Periodontol. 81:1455–1465.
   PubMed Web of Science ®Google Scholar
• Skamagas M, Breen TL, LeRoith D. 2008. Update on diabetes mellitus: prevention, treatment, and association with oral diseases. Oral Dis. 14:105–114.
   PubMed Web of Science ®Google Scholar
• Takeda M, Ojima M, Yoshioka H, Inaba H, Kogo M, Shizukuishi S, Nomura M, Amano A. 2006. Relationship of serum advanced glycation end products with deterioration of periodontitis in type 2 diabetes patients. J Periodontol. 77:15–20.
   PubMed Web of Science ®Google Scholar
• Tatakis DN. 1993. Interleukin-1 and bone metabolism: a review. J Periodontol. 64 (Suppl.):416–431.
   PubMedGoogle Scholar
• Taylor JJ, Preshaw PM, Lalla E. 2013. A review of the evidence for pathogenic mechanisms that may link periodontitis and diabetes. J Clin Periodontol. 40 (Suppl.):S113–S134.
   PubMedGoogle Scholar
• Thomas B, Ramesh A, Suresh S, Prasad BR. 2013. A comparative evaluation of antioxidant enzymes and selenium in the serum of periodontitis patients with diabetes mellitus type 2. Contemp Clin Dent. 4:176–180.
   PubMedGoogle Scholar
• Ucan MC, Koparal M, Agacayak S, Gunay A, Ozgoz M, Atilgan S, Yaman F. 2013. Influence of caffeic acid phenethyl ester on bone healing in a rat model. J Int Med Res. 41:1648–1654.
   PubMed Web of Science ®Google Scholar
• Wu YY, Xiao E, Graves DT. 2015. Diabetes mellitus related bone metabolism and periodontal disease. Int J Oral Sci. 7:63–72.
   PubMed Web of Science ®Google Scholar
• Yilmaz HR, Uz E, Altunbasak A, Sakalli E, Ozcelik N. 2010. Anticlastogenic effect of caffeic acid phenethyl ester on cisplatin-induced chromosome aberrations in rat bone marrow cells. Toxicol Ind Health. 26:33–37.
   PubMed Web of Science ®Google Scholar