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Anti-Inflammatory & Anti-Allergy Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5230
ISSN (Online): 1875-614X

Research Article

3,4,5-Trihydroxybenzoic Acid Attenuates Ligature-Induced Periodontal Disease in Wistar Rats

Author(s): Ozkan Karatas* and Fikret Gevrek

Volume 20, Issue 1, 2021

Published on: 06 February, 2020

Page: [51 - 60] Pages: 10

DOI: 10.2174/1871523019666200206094335

Price: $65

Abstract

Background: 3,4,5-Trihydroxybenzoic acid, which is also known as gallic acid, is an antiinflammatory agent that could provide beneficial effects in preventing periodontal inflammation. The present study aimed to evaluate the anti-inflammatory effects of gallic acid on experimental periodontitis in Wistar rats. Alveolar bone loss, osteoclastic activity, osteoblastic activity, and collagenase activity were also determined.

Methods: Thirty-two Wistar rats were used in the present study. Study groups were created as following: Healthy control (C,n=8) group; periodontitis (P,n=8) group; periodontitis and 30 mg/kg gallic acid administered group (G30,n=8); periodontitis and 60 mg/kg gallic acid administered group (G60,n=8). Experimental periodontitis was created by placing 4-0 silk sutures around the mandibular right first molar tooth. Morphological changes in alveolar bone were determined by stereomicroscopic evaluation. Mandibles were undergone histological evaluation. Matrix metalloproteinase (MMP)-8, tissue inhibitor of MMPs (TIMP)-1, bone morphogenetic protein (BMP)-2 expressions, tartrateresistant acid phosphatase (TRAP) positive osteoclast cells, osteoblast, and inflammatory cell counts were determined.

Results: The highest alveolar bone loss was observed in the periodontitis group. Both doses of gallic acid decreased alveolar bone loss as compared to the P group. TRAP-positive osteoclast cell counts were higher in the P group, and gallic acid successfully lowered these counts. Osteoblast cells also increased in gallic acid administered groups. Inflammation in the P group was also higher than those of C, G30, and G60 groups supporting the role of gallic acid in preventing inflammation. 30 and 60 mg/kg doses of gallic acid decreased MMP-8 levels and increased TIMP-1 levels. BMP levels increased in gallic acid administered groups, similar to several osteoblasts.

Conclusion: Present results revealed an anti-inflammatory effect of gallic acid, which was indicated by decreased alveolar bone loss and collagenase activity and increased osteoblastic activity.

Keywords: Anti-inflammatory, BMP, experimental periodontitis, gallic acid, MMP-8, TIMP-1.

Graphical Abstract
[1]
Ferrero-Miliani, L.; Nielsen, O.H.; Andersen, P.S.; Girardin, S.E. Chronic inflammation: Importance of NOD2 and NALP3 in interleukin-1β generation. Clin. Exp. Immunol., 2007, 147(2), 227-235.
[PMID: 17223962]
[2]
Kumar, R.; Clermont, G.; Vodovotz, Y.; Chow, C.C. The dynamics of acute inflammation. J. Theor. Biol., 2004, 230(2), 145-155.
[http://dx.doi.org/10.1016/j.jtbi.2004.04.044] [PMID: 15321710]
[3]
Garlet, G.P.; Giannobile, W.V. Macrophages: The bridge between inflammation resolution and tissue repair? J. Dent. Res., 2018, 97(10), 1079-1081.
[http://dx.doi.org/10.1177/0022034518785857] [PMID: 29993304]
[4]
Bingham, C.O., III; Moni, M. Periodontal disease and rheumatoid arthritis: the evidence accumulates for complex pathobiologic interactions. Curr. Opin. Rheumatol., 2013, 25(3), 345-353.
[http://dx.doi.org/10.1097/BOR.0b013e32835fb8ec ] [PMID: 23455329]
[5]
Buckley, C.D.; Gilroy, D.W.; Serhan, C.N. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity, 2014, 40(3), 315-327.
[http://dx.doi.org/10.1016/j.immuni.2014.02.009] [PMID: 24656045]
[6]
Attiq, A.; Jalil, J.; Husain, K.; Ahmad, W. Raging the war against inflammation with natural products. Front. Pharmacol., 2018, 9, 976.
[http://dx.doi.org/10.3389/fphar.2018.00976] [PMID: 30245627]
[7]
Mizraji, G.; Heyman, O.; Van Dyke, T.E.; Wilensky, A. Resolvin D2 restrains TH1 immunity and prevents alveolar bone loss in murine periodontitis. Front. Immunol., 2018, 9, 785.
[http://dx.doi.org/10.3389/fimmu.2018.00785] [PMID: 29922275]
[8]
Hasturk, H.; Abdallah, R.; Kantarci, A.; Nguyen, D.; Giordano, N.; Hamilton, J.; Van Dyke, T.E. Resolvin E1 (RvE1) attenuates atherosclerotic plaque formation in diet and inflammation-induced atherogenesis. Arterioscler. Thromb. Vasc. Biol., 2015, 35(5), 1123-1133.
[http://dx.doi.org/10.1161/ATVBAHA.115.305324 ] [PMID: 25792445]
[9]
P, J.J.; Manju, S.L.; Ethiraj, K.R.; Elias, G. Safer anti-inflammatory therapy through dual COX-2/5-LOX inhibitors: A structure-based approach. Eur. J. Pharm. Sci., 2018, 121, 356-381.
[http://dx.doi.org/10.1016/j.ejps.2018.06.003] [PMID: 29883727]
[10]
Baek, J.M.; Kim, J-Y.; Lee, C.H.; Yoon, K-H.; Lee, M.S. Methyl gallate inhibits osteoclast formation and function by suppressing akt and btk-plcγ2-Ca2+ signaling and prevents lipopolysaccharide-induced bone loss. Int. J. Mol. Sci., 2017, 18(3), 581.
[http://dx.doi.org/10.3390/ijms18030581] [PMID: 28272351]
[11]
Harikrishnan, H.; Jantan, I.; Haque, M.A.; Kumolosasi, E. Anti-inflammatory effects of Phyllanthus amarus Schum. & Thonn. through inhibition of NF-κB, MAPK, and PI3K-Akt signaling pathways in LPS-induced human macrophages. BMC Complement. Altern. Med., 2018, 18(1), 224.
[http://dx.doi.org/10.1186/s12906-018-2289-3] [PMID: 30045725]
[12]
Tominari, T.; Ichimaru, R.; Yoshinouchi, S.; Matsumoto, C.; Watanabe, K.; Hirata, M.; Grundler, F.M.W.; Inada, M.; Miyaura, C. Effects of O-methylated (-)-epigallocatechin gallate (EGCG) on LPS-induced osteoclastogenesis, bone resorption, and alveolar bone loss in mice. FEBS Open Bio, 2017, 7(12), 1972-1981.
[http://dx.doi.org/10.1002/2211-5463.12340] [PMID: 29226083]
[13]
Albouchi, F.; Avola, R.; Dico, G.M.L.; Calabrese, V.; Graziano, A.C.E.; Abderrabba, M.; Cardile, V. Melaleuca styphelioides sm. polyphenols modulate interferon gamma/histamine-induced inflammation in human nctc 2544 keratinocytes. Molecules, 2018, 23(10), 2526.
[http://dx.doi.org/10.3390/molecules23102526] [PMID: 30279388]
[14]
Cheng, Y.; Li, X.; Tse, H-F.; Rong, J. Gallic acid-L-leucine conjugate protects mice against lps-induced inflammation and sepsis via correcting proinflammatory lipid mediator profiles and oxidative stress. Oxid. Med. Cell. Longev., 2018, 2018m 1081287.
[http://dx.doi.org/10.1155/2018/1081287]
[15]
Kamatham, S.; Kumar, N.; Gudipalli, P. Isolation and characterization of gallic acid and methyl gallate from the seed coats of Givotia rottleriformis Griff. and their anti-proliferative effect on human epidermoid carcinoma A431 cells. Toxicol. Rep., 2015, 2, 520-529.
[http://dx.doi.org/10.1016/j.toxrep.2015.03.001] [PMID: 28962387]
[16]
Choubey, S.; Goyal, S.; Varughese, L.R.; Kumar, V.; Sharma, A.K.; Beniwal, V. Probing gallic acid for its broad spectrum applications. Mini Rev. Med. Chem., 2018, 18(15), 1283-1293.
[http://dx.doi.org/10.2174/1389557518666180330114010] [PMID: 29600764]
[17]
Chauhan, S.; Sharma, A.; Upadhyay, N.K.; Singh, G.; Lal, U.R.; Goyal, R. In-vitro osteoblast proliferation and in-vivo anti-osteoporotic activity of Bombax ceiba with quantification of Lupeol, gallic acid and β-sitosterol by HPTLC and HPLC. BMC Complement. Altern. Med., 2018, 18(1), 233.
[http://dx.doi.org/10.1186/s12906-018-2299-1] [PMID: 30086745]
[18]
Jin, P.; Liao, L.; Lin, X.; Guo, Q.; Lin, C.; Wu, H.; Zheng, L.; Zhao, J. Stimulating effect of a novel synthesized sulfonamido-based gallate ZXHA-TC on primary osteoblasts. Yonsei Med. J., 2015, 56(3), 760-771.
[http://dx.doi.org/10.3349/ymj.2015.56.3.760] [PMID: 25837183]
[19]
Lim, H-J.; Jeon, Y-D.; Kang, S-H.; Shin, M-K.; Lee, K-M.; Jung, S-E.; Cha, J-Y.; Lee, H-Y.; Kim, B-R.; Hwang, S-W.; Lee, J.H.; Sugita, T.; Cho, O.; Myung, H.; Jin, J.S.; Lee, Y.M. Inhibitory effects of Euphorbia supina on Propionibacterium acnes-induced skin inflammation in vitro and in vivo. BMC Complement. Altern. Med., 2018, 18(1), 263.
[http://dx.doi.org/10.1186/s12906-018-2320-8] [PMID: 30261862]
[20]
Park, H-H.; Ko, S-C.; Oh, G-W.; Jang, Y-M.; Kim, Y-M.; Park, W.S.; Choi, I-W.; Jung, W-K. Characterization and biological activity of PVA hydrogel containing chitooligosaccharides conjugated with gallic acid. Carbohydr. Polym., 2018, 198, 197-205.
[http://dx.doi.org/10.1016/j.carbpol.2018.06.070] [PMID: 30092991]
[21]
Fischer, N.; Seo, E-J.; Efferth, T. Prevention from radiation damage by natural products. Phytomedicine, 2017, 47(1), 192-200.
[PMID: 30166104]
[22]
Ola-Davies, O.E.; Olukole, S.G. Gallic acid protects against bisphenol A-induced alterations in the cardio-renal system of Wistar rats through the antioxidant defense mechanism. Biomed. Pharmacother., 2018, 107, 1786-1794.
[http://dx.doi.org/10.1016/j.biopha.2018.08.108] [PMID: 30257398]
[23]
Rong, Y.; Cao, B.; Liu, B.; Li, W.; Chen, Y.; Chen, H.; Liu, Y.; Liu, T. A novel Gallic acid derivative attenuates BLM-induced pulmonary fibrosis in mice. Int. Immunopharmacol., 2018, 64, 183-191.
[http://dx.doi.org/10.1016/j.intimp.2018.08.024] [PMID: 30195109]
[24]
Setayesh, T.; Nersesyan, A.; Mišík, M.; Noorizadeh, R.; Haslinger, E.; Javaheri, T.; Lang, E.; Grusch, M.; Huber, W.; Haslberger, A. Gallic acid, a common dietary phenolic protects against high fat diet induced DNA damage. Eur. J. Nutr., 2018, 58(6), 2315-2326.
[PMID: 30039436]
[25]
Teodoro, G.R.; Gontijo, A.V.L.; Salvador, M.J.; Tanaka, M.H.; Brighenti, F.L.; Delbem, A.C.B.; Delbem, Á.C.B.; Koga-Ito, C.Y. Effects of acetone fraction from buchenavia tomentosa aqueous extract and gallic acid on candida albicans biofilms and virulence factors. Front. Microbiol., 2018, 9, 647.
[http://dx.doi.org/10.3389/fmicb.2018.00647] [PMID: 29675005]
[26]
Pacios, S.; Andriankaja, O.; Kang, J.; Alnammary, M.; Bae, J.; de Brito Bezerra, B.; Schreiner, H.; Fine, D.H.; Graves, D.T. Bacterial infection increases periodontal bone loss in diabetic rats through enhanced apoptosis. Am. J. Pathol., 2013, 183(6), 1928-1935.
[http://dx.doi.org/10.1016/j.ajpath.2013.08.017] [PMID: 24113454]
[27]
Bullon, P.; Newman, H.N.; Battino, M. Obesity, diabetes mellitus, atherosclerosis and chronic periodontitis: A shared pathology via oxidative stress and mitochondrial dysfunction? Periodontol., 2014, 64(1), 139-153.
[http://dx.doi.org/10.1111/j.1600-0757.2012.00455.x ] [PMID: 24320961]
[28]
Balci Yuce, H.; Akbulut, N.; Ocakli, S.; Kayir, O.; Elmastas, M. The effect of commercial conjugated linoleic acid products on experimental periodontitis and diabetes mellitus in Wistar rats. Acta Odontol. Scand., 2017, 75(1), 21-29.
[http://dx.doi.org/10.1080/00016357.2016.1244355] [PMID: 27897090]
[29]
Balci Yuce, H.; Lektemur Alpan, A.; Gevrek, F.; Toker, H. Investigation of the effect of astaxanthin on alveolar bone loss in experimental periodontitis. J. Periodontal Res., 2018, 53(1), 131-138.
[http://dx.doi.org/10.1111/jre.12497] [PMID: 29044575]
[30]
Kure, K.; Sato, H.; Suzuki, J.i.; Itai, A.; Aoyama, N.; Izumi, Y. A novel IkB kinase inhibitor attenuates ligature‐induced periodontal disease in mice. J. Periodontal Res., 2018, 54(2), 164-173.
[PMID: 30295325]
[31]
Hosseinzadeh, A.; Houshmand, G.; Goudarzi, M.; Sezavar, S.H.; Mehrzadi, S.; Mansouri, E.; Kalantar, M. Ameliorative effect of gallic acid on sodium arsenite-induced spleno-, cardio- and hemato-toxicity in rats. Life Sci., 2019, 217, 91-100.
[http://dx.doi.org/10.1016/j.lfs.2018.11.050] [PMID: 30472295]
[32]
Oka, Y.; Iwai, S.; Amano, H.; Irie, Y.; Yatomi, K.; Ryu, K.; Yamada, S.; Inagaki, K.; Oguchi, K. Tea polyphenols inhibit rat osteoclast formation and differentiation. J. Pharmacol. Sci., 2011, 1112190632-1112190632.
[PMID: 22186621]
[33]
Zhao, F.; Pang, W.; Zhang, Z.; Zhao, J.; Wang, X.; Liu, Y.; Wang, X.; Feng, Z.; Zhang, Y.; Sun, W.; Liu, J. Pomegranate extract and exercise provide additive benefits on improvement of immune function by inhibiting inflammation and oxidative stress in high-fat-diet-induced obesity in rats. J. Nutr. Biochem., 2016, 32, 20-28.
[http://dx.doi.org/10.1016/j.jnutbio.2016.02.003] [PMID: 27142733]
[34]
Lee, H-P.; Lin, D-J.; Yeh, M-L. Phenolic modified ceramic coating on biodegradable Mg alloy: The improved corrosion resistance and osteoblast-like cell activity. Materials (Basel), 2017, 10(7), 696.
[http://dx.doi.org/10.3390/ma10070696] [PMID: 28773055]
[35]
Huang, L.; Jin, P.; Lin, X.; Lin, C.; Zheng, L.; Zhao, J. Beneficial effects of sulfonamide based gallates on osteoblasts in vitro. Mol. Med. Rep., 2017, 15(3), 1149-1156.
[http://dx.doi.org/10.3892/mmr.2017.6142 ] [PMID: 28138702]
[36]
Hou, W.; Ye, C.; Chen, M.; Li, W.; Gao, X.; He, R.; Zheng, Q.; Zhang, W. Bergenin activates SIRT1 as a novel therapeutic agent for osteogenesis of bone mesenchymal stem cells. Front. Pharmacol., 2019, 10, 618.
[http://dx.doi.org/10.3389/fphar.2019.00618 ] [PMID: 31258473]
[37]
He, B.; Hu, M.; Li, S.D.; Yang, X.T.; Lu, Y.Q.; Liu, J.X.; Chen, P.; Shen, Z.Q. Effects of geraniin on osteoclastic bone resorption and matrix metalloproteinase-9 expression. Bioorg. Med. Chem. Lett., 2013, 23(3), 630-634.
[http://dx.doi.org/10.1016/j.bmcl.2012.12.005] [PMID: 23290455]
[38]
Toker, H.; Balci Yuce, H.; Lektemur Alpan, A.; Gevrek, F.; Elmastas, M. Morphometric and histopathological evaluation of the effect of grape seed proanthocyanidin on alveolar bone loss in experimental diabetes and periodontitis. J. Periodontal Res., 2018, 53(3), 478-486.
[http://dx.doi.org/10.1111/jre.12536] [PMID: 29446089]
[39]
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(4), 103-110.
[PMID: 24705040]
[40]
Toker, H.; Ozdemir, H.; Balcı, H.; Ozer, H. N-acetylcysteine decreases alveolar bone loss on experimental periodontitis in streptozotocin-induced diabetic rats. J. Periodontal Res., 2012, 47(6), 793-799.
[http://dx.doi.org/10.1111/j.1600-0765.2012.01497.x ] [PMID: 22712627]
[41]
Graves, D.T.; Kang, J.; Andriankaja, O.; Wada, K.; Rossa, C., Jr Animal models to study host-bacteria interactions involved in periodontitis. Front. Oral Biol., 2012, 15, 117-132.
[http://dx.doi.org/10.1159/000329675] [PMID: 22142960]
[42]
de Molon, R.S.; de Avila, E.D.; Cirelli, J.A. Host responses induced by different animal models of periodontal disease: A literature review. J. Investig. Clin. Dent., 2013, 4(4), 211-218.
[http://dx.doi.org/10.1111/jicd.12018] [PMID: 23188588]
[43]
Oz, H.S.; Puleo, D.A. Animal models for periodontal disease. BioMed Res. Int., 2011, 2011754857
[http://dx.doi.org/10.1155/2011/754857]
[44]
Yu, Z.; Song, F.; Jin, Y-C.; Zhang, W-M.; Zhang, Y.; Liu, E-J.; Zhou, D.; Bi, L-L.; Yang, Q.; Li, H.; Zhang, B.L.; Wang, S.W. Comparative pharmacokinetics of gallic acid after oral administration of gallic acid monohydrate in normal and isoproterenol-induced myocardial infarcted rats. Front. Pharmacol., 2018, 9, 328.
[http://dx.doi.org/10.3389/fphar.2018.00328 ] [PMID: 29681855]
[45]
Hajipour, S.; Sarkaki, A.; Farbood, Y.; Eidi, A.; Mortazavi, P.; Valizadeh, Z. Effect of gallic acid on dementia type of Alzheimer disease in rats: electrophysiological and histological studies. Basic Clin. Neurosci., 2016, 7(2), 97-106.
[http://dx.doi.org/10.15412/J.BCN.03070203] [PMID: 27303604]
[46]
Moghadas, M.; Edalatmanesh, M.A.; Robati, R. Histopathological analysis from gallic acid administration on hippocampal cell density, depression, and anxiety related behaviors in a trimethyltin intoxication model. Cell J., 2016, 17(4), 659-667.
[PMID: 26862525]
[47]
Maya, S.; Prakash, T.; Goli, D. Evaluation of neuroprotective effects of wedelolactone and gallic acid on aluminium-induced neurodegeneration: Relevance to sporadic amyotrophic lateral sclerosis. Eur. J. Pharmacol., 2018, 835, 41-51.
[http://dx.doi.org/10.1016/j.ejphar.2018.07.058] [PMID: 30075221]
[48]
Gholamine, B.; Houshmand, G.; Hosseinzadeh, A.; Kalantar, M.; Mehrzadi, S.; Goudarzi, M. Gallic acid ameliorates sodium arsenite-induced renal and hepatic toxicity in rats. Drug Chem. Toxicol., 2019, 42, 1-12.
[http://dx.doi.org/10.1080/01480545.2019.1591434] [PMID: 30907158]
[49]
Dianat, M.; Sadeghi, N.; Badavi, M.; Panahi, M.; Taheri Moghadam, M. Protective effects of co-administration of gallic Acid and cyclosporine on rat myocardial morphology against ischemia/reperfusion. Jundishapur J. Nat. Pharm. Prod., 2014, 9(4), e17186.
[http://dx.doi.org/10.17795/jjnpp-17186]] [PMID: 25625048]
[50]
Abnosi, M.H.; Yari, S. The toxic effect of gallic acid on biochemical factors, viability and proliferation of rat bone marrow mesenchymal stem cells was compensated by boric acid. J. Trace Elem. Med. Biol., 2018, 48, 246-253.
[http://dx.doi.org/10.1016/j.jtemb.2018.04.016] [PMID: 29773188]

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