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Protective effect of liensinine on periodontitis through its antioxidant effect in mice

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Abstract

Liensinine is the most important functional compound in lotus seeds; its protective effect on periodontitis was determined and the mechanism of its antioxidant effect was also explained. During the experiment, we could observe that liensinine could reduce the gingival index in periodontitis-induced mice, and these effects were similar to that during the treatment of periodontitis with the metronidazole drug. After the treatment with liensinine, the serum Immunoglobulin G1 (IgG1) level was found to increase and IgG2a level was found to decrease compared to the periodontitis control mice. Liensinine and metronidazole could increase the superoxide dismutase (SOD) serum levels in the periodontitis-induced mice, and both the drugs at the same concentration (200 mg/kg) showed similar SOD activities, which was found to increase. Liensinine also increased the oxidation-related factor of catalase (CAT), glutathione peroxidase, and decreased nitric oxide, malondialdehyde, and endothelin in the serum of mice, compared to the periodontitis control mice. The serum cytokine levels of Interleukin-6, tumor necrosis factor-α, and Interferon-γ in liensinine-treated mice were lower than the control mice, but higher than the normal mice. The serum IL-4 cytokine level of liensinine-treated mice was reversed, i.e., higher than the control mice. In the periodontal tissue, the mRNA and protein expressions of inhibitor of kappa B-α, transforming growth factor beta 1, Interleukin-10, Mn-SOD, Gu/Zn-SOD, and CAT were increased by the treatment with liensinine compared to the control group mice, and nuclear factor kappa B expressions showed the opposite trend. Liensinine is a good functional compound in the treatment of periodontitis, similar to metronidazole drug. Higher concentration of liensinine had better effects.

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References

  • Abbès S, Ben Salah-Abbès J, Jebali R, Younes RB, Oueslati R (2015) Interaction of aflatoxin B1 and fumonisin B1 in mice causes immunotoxicity and oxidative stress: possible protective role using lactic acid bacteria. J Immunotoxicol 14:1–9

    Google Scholar 

  • Amarnath S, Dong L, Li J, Wu Y, Chen W (2007) Endogenous TGF-beta activation by reactive oxygen species is key to Foxp3 induction in TCR-stimulated and HIV-1-infected human CD4+CD25− T cells. Retrovirology 4:57

    Article  Google Scholar 

  • Balaji TM, Vasanthi HR, Rao SR (2015) Gingival, plasma and salivary levels of melatonin in periodontally healthy individuals and chronic periodontitis patients: a pilot study. J Clin Diagn Res 9:ZC23-25

    Google Scholar 

  • Batista AC, Silva TA, Chun JH, Lara VS (2002) Nitric oxide synthesis and severity of human periodontal disease. Oral Dis 8:254–260

    Article  CAS  Google Scholar 

  • Bollyky PL, Falk BA, Long SA, Preisinger A, Braun KR, Wu RP, Evanko SP, Buckner JH, Wight TN, Nepom GT (2009) CD44 costimulation promotes FoxP3+ regulatory T cell persistence and function via production of IL-2, IL-10, and TGF-beta. J Immunol 183:2232–2241

    Article  CAS  Google Scholar 

  • Cardoso CR, Garlet GP, Moreira AP, Júnior WM, Rossi MA, Silva JS (2008) Characterization of CD4+, CD25+ natural regulatory T cells in the inflammatory infiltrate of human chronic periodontitis. J Leukoc Biol 84:311–318

    Article  CAS  Google Scholar 

  • Chen S, Wu J, Song Z, Zhang J (2000) An investigation of immunocompetence substances in normal gingival and periodontitis tissue. Chin Med J (Engl) 113:844–847

    CAS  Google Scholar 

  • Chen L, Yan X, Yan Q, Fan J, Huang H, Shi X, Han L, Han T, Zhu H (2015a) The modified JiuWei QiangHuo decoction alleviated severe lung injury induced by H1N1 influenza virus by regulating the NF-κB pathway in mice. Evid Based Complement Altern Med 2015:790739

    Google Scholar 

  • Chen XT, Tan JY, Lei LH, Chen LL (2015b) Cytokine levels in plasma and gingival crevicular fluid in chronic periodontitis. Am J Dent 28:9–12

    Google Scholar 

  • da Costa TA, Silva MJ, Alves PM, Chica JE, Barcelos EZ, Giani MA, Garlet GP, da Silva JS, Rodrigues Júnior V, Rodrigues DB, Cardoso CR (2015) Inflammation biomarkers of advanced disease in nongingival tissues of chronic periodontitis patients. Mediators Inflamm 2015:983782

    Article  Google Scholar 

  • Hajishengallis G (2015) Periodontitis: from microbial immune subversion to systemic inflammation. Nat Rev Immunol 15:30–44

    Article  CAS  Google Scholar 

  • Hienz SA, Paliwal S, Ivanovski S (2015) Mechanisms of bone resorption in periodontitis. J Immunol Res 2015:615486

    Article  Google Scholar 

  • Huseynova IM, Aliyeva DR, Aliyev JA (2014) Subcellular localization and responses of superoxide dismutase isoforms in local wheat varieties subjected to continuous soil drought. Plant Physiol Biochem 81:54–60

    Article  CAS  Google Scholar 

  • Itoga M, Konno Y, Moritoki Y, Saito Y, Ito W, Tamaki M, Kobayashi Y, Kayaba H, Kikuchi Y, Chihara J, Takeda M, Ueki S, Hirokawa M (2015) G-protein-coupled estrogen receptor agonist suppresses airway inflammation in a mouse model of asthma through IL-10. PLoS One 10:e0123210

    Article  Google Scholar 

  • Jayachandran M, Chandrasekaran B, Namasivayam N (2015) Geraniol attenuates fibrosis and exerts anti-inflammatory effects on diet induced atherogenesis by NF-κB signaling pathway. Eur J Pharmacol 762:102–111

    Article  CAS  Google Scholar 

  • Jin Y, Liu D, Fang X, Gao K, Lin X (2015) Effect of tamibarotene on innate immune response in the model of Porphyromonas gingivalis induced periodontitis. Chin J Stomatol 50:146–150

    Google Scholar 

  • Kara A, Akman S, Ozkanlar S, Tozoglu U, Kalkan Y, Canakci CF, Tozoglu S (2013) Immune modulatory and antioxidant effects of melatonin in experimental periodontitis in rats. Free Radic Biol Med 55:21–26

    Article  CAS  Google Scholar 

  • Kim HR, da Shin Y, Chung KH (2015) The role of NF-κB signaling pathway in polyhexamethylene guanidine phosphate induced inflammatory response in mouse macrophage RAW264.7 cells. Toxicol Lett 233:148–155

    Article  CAS  Google Scholar 

  • Löe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38:610–616

    Article  Google Scholar 

  • Luo K, Chen L, Chen YL, Li YF, Zhao X, Yan FH (2010) Study of the inhibitory effects of oxymatrine on bone absorption in experimental periodontitis in rats. J Fujian Med Univ 44:100–102

    Google Scholar 

  • Lv SF, Wang XH, Li HW, Zhang XL, Wang B (2015) Quantification of liensinine in rat plasma using ultra-performance liquid chromatography tandem mass spectrometry and its application to a pharmacokinetic study. J Chromatogr B Anal Technol Biomed Life Sci 992:43–46

    Article  CAS  Google Scholar 

  • Nouri HR, Varasteh A, Jaafari MR, Davies JM, Sankian M (2015) Induction of a Th1 immune response and suppression of IgE via immunotherapy with a recombinant hybrid molecule encapsulated in liposome–protamine–DNA nanoparticles in a model of experimental allergy. Immunol Res 62:280–291

    Article  CAS  Google Scholar 

  • Pan QR, Lv FL, Song N, Huang SG (2011) Effect of total glucosides of paeony on serum levels of IgG1 and IgG2a in mouse model of periodontitis. Chin J Pathophysiol 27:1462–1466

    CAS  Google Scholar 

  • Rao LJ, Lu JJ, Lv FL, Li DJ, Huang SG (2011) Effects of baicalin on serum levels of IL-6 and IL-4 in mouse periodontitis. Chin J Pathophysiol 27:550–554

    CAS  Google Scholar 

  • Ring A, Stremmel W (2000) The hepatic microvascular responses to sepsis. Semin Thromb Hemost 26:589–594

    Article  CAS  Google Scholar 

  • Sağlam M, Köseoğlu S, Hatipoğlu M, Esen HH, Köksal E (2015) Effect of sumac extract on serum oxidative status, RANKL/OPG system and alveolar bone loss in experimental periodontitis in rats. J Appl Oral Sci 23:33–41

    Google Scholar 

  • Sezer U, Erciyas K, Ustün K, Pehlivan Y, Şenyurt SZ, Aksoy N, Tarakçıoğlu M, Taysı S, Onat AM (2013) Effect of chronic periodontitis on oxidative status in patients with rheumatoid arthritis. J Periodontol 84:785–792

    Article  CAS  Google Scholar 

  • Smiley CJ, Tracy SL, Abt E, Michalowicz BS, John MT, Gunsolley J, Cobb CM, Rossmann J, Harrel SK, Forrest JL, Hujoel PP, Noraian KW, Greenwell H, Frantsve-Hawley J, Estrich C, Hanson N (2015) Evidence-based clinical practice guideline on the nonsurgical treatment of chronic periodontitis by means of scaling and root planing with or without adjuncts. J Am Dent Assoc 146:525–535

    Article  Google Scholar 

  • Souto GR, Queiroz-Junior CM, de Abreu MH, Costa FO, Mesquita RA (2014) Pro-inflammatory, Th1, Th2, Th17 cytokines and dendritic cells: a cross-sectional study in chronic periodontitis. PLoS One 9:e91636

    Article  Google Scholar 

  • Tkachev V, Goodell S, Opipari AW, Hao LY, Franchi L, Glick GD, Ferrara JL, Byersdorfer CA (2015) Programmed death-1 controls T cell survival by regulating oxidative metabolism. J Immunol 194:5789–5800

    Article  CAS  Google Scholar 

  • Tonguç MÖ, Öztürk O, Sütçü R, Ceyhan BM, Kılınç G, Sönmez Y, Yetkin Ay Z, Sahin U, Baltacıoğlu E, Kırzıoğlu FY (2011) The impact of smoking status on antioxidant enzyme activity and malondialdehyde levels in chronic periodontitis. J Periodontol 82:1320–1328

    Article  Google Scholar 

  • Trawczyńska I, Wójcik M (2015) Optimization of permeabilization process of yeast cells for catalase activity using response surface methodology. Biotechnol Biotechnol Equip 29:72–77

    Article  Google Scholar 

  • Vardar-Sengul S, Arora S, Baylas H, Mercola D (2009) Expression profile of human gingival fibroblasts induced by interleukin-1beta reveals central role of nuclear factor-kappa B in stabilizing human gingival fibroblasts during inflammation. J Periodontol 80:833–849

    Article  CAS  Google Scholar 

  • Verma RK, Bhattacharyya I, Sevilla A, Lieberman I, Pola S, Nair M, Wallet SM, Aukhil I, Kesavalu L (2010) Virulence of major periodontal pathogens and lack of humoral immune protection in a rat model of periodontal disease. Oral Dis 16:686–695

    Article  CAS  Google Scholar 

  • Winkler I, Wilczynska B, Bojarska-Junak A, Gogacz M, Adamiak A, Postawski K, Darmochwal-Kolarz D, Rechberger T, Tabarkiewicz J (2015) Regulatory T lymphocytes and transforming growth factor beta in epithelial ovarian tumors-prognostic significance. J Ovarian Res 8:39

    Article  Google Scholar 

  • Xia YF, Zhang JH, Xu ZF, Deng XM (2015) Pycnogenol, a compound isolated from the bark of pinus maritime mill, attenuates ventilator-induced lung injury through inhibiting NF-κB-mediated inflammatory response. Int J Clin Exp Med 8:1824–1833

    CAS  Google Scholar 

  • Xiong YL, Wang JL, Qian JQ (1998) Effect of liensinine on proliferation of vascular smooth muscle cells and PDGF-B, bFGF, c-sis and c-myc in spontaneously hypertensive rat. Chin J Cardiovasc Med 3:6–9

    Google Scholar 

  • Yan Q, Zhang TY, Tan N, Xu B, Xu LL, Liu XJ (2014) Regulation of liensinine on T24 bladder cancer cell proliferation and cycle. Chongqing Med 43:3268–3271

    CAS  Google Scholar 

  • Yu ZH, Zhang GY, Zhang XH, Du JD, Yang Q, He FD (2008) Effect of berberine hydrochloride on the expression of interleukin-1β and tumor necrosis factor-α in periodontal tissues in rats. West China J Stomatol 26:82–86

    CAS  Google Scholar 

  • Yu WG, Zhang HW, Yang T, Zhang DM, Deng DM (2013) Study on antioxidation of liensinine on focal cerebral ischemia-reperfusion injury in rats. Pharm Clin Chin Mater Med 29:32–35

    Google Scholar 

  • Zhao X, Kim SY, Park KY (2013) Bamboo salt has in vitro anticancer activity in HCT-116 cells and exerts anti-metastatic effects in vivo. J Med Food 16:9–19

    Article  Google Scholar 

  • Zhao X, Wang Q, Li GJ, Chen F, Qian Y, Wang R (2014) In vitro antioxidant, anti-mutagenic, anti-cancer and anti-angiogenic effects of Chinese Bowl tea. J Funct Food 7:590–598

    Article  CAS  Google Scholar 

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Correspondence to Ying Li or Xin Zhao.

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Liang Pang and Kai Zhu have contributed equally to this work.

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Pang, L., Zhu, K., Feng, X. et al. Protective effect of liensinine on periodontitis through its antioxidant effect in mice. J Korean Soc Appl Biol Chem 58, 927–936 (2015). https://doi.org/10.1007/s13765-015-0122-y

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