Effect of lipopolysaccharide on the development of oxidativenitrosative stress in salivary glands and soft periodontal tissues of rats under conditions of water avoidance stress
DOI:
https://doi.org/10.15584/ejcem.2024.2.30Keywords:
bacterial lipopolysaccharide, nitric oxide, salivary glands, soft periodontal tissues, water avoidance stressAbstract
Introduction and aim. Violation in the salivary glands will inevitably cause changes in periodontium, and periodontitis can disrupt the functioning of the salivary glands. The purpose of the work is to evaluate changes in NO-synthase and arginase activities, pro- and antioxidant balance in rat salivary glands and soft periodontal tissues during administration of bacterial lipopolysaccharide (LPS) and water avoidance stress (WAS) modeling.
Material and methods. The experiment was performed on 24 rats. The animals were divided into 4 groups: control, WAS, animals injected intraperitoneally with 0.4 μg/kg of bacterial LPS of Salmonella typhi, WAS+LPS.
Results. Water avoidance stress led to decrease of inducible NO-synthase (iNOS) activity in salivary glands by 1.63 times, but decreased arginase activity by 1.15 times, superoxide production increased by 1.53 times, catalase activity decreased by 1.2 times, and malonic dialdehyde (MDA) increased by 1.19 times compared to the control. Lipopolysaccharide led to increase of constitutive NO-synthases (cNOS) activity in salivary glands by 1.48 times, but decreased arginase activity by 6.15 times, catalase activity increased by 2.6 times and superoxide dismutase activity decreased by 2.74 times, and MDA increased by 6.84 times compared to the control. Water avoidance stress + LPS in salivary glands led to decrease of cNOS and arginase activity by 1.09 and 1.19 times, respectively, superoxide production increased by 1.88 times, catalase and superoxide dismutase activity decreased by 1.06 times and 1.34 times, respectively, and MDA increased by 2.44 times compared to the control. Water avoidance stress led to increase of iNOS activity in periodontium by 1.44 times and arginase activity decreased by 1.37 times, superoxide production increased 1.32 times, catalase activity and superoxide dismutase activities decreased by 1.27 times and by 1.53 times, respectively, and MDA increased by 1.31 times compared to the control. Lipopolysaccharide led to increase of iNOS activity in the periodontium by 3.88 times, arginase activity decreased by 2.69 times, superoxide production increased 1.64 times, catalase activity increased by 4.32 times, and MDA increased by 4.51 times compared to the control. Water avoidance stress + LPS in periodontium led to increase of iNOS and cNOS activities by 1.95 times and 1.53, respectively, arginase activity decreased by 1.39 times, superoxide production increased 1.66 times, catalase activity increased by 1.11 times, and MDA increased by 1.53 times compared to the control.
Conclusion. The combination of LPS and WAS leads to changes in NO production and oxidative stress in salivary glands and the periodontium.
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Lin TC, Tseng CF, Wang YH, Yu HC, Chang YC. Patients with chronic periodontitis present increased risk for primary Sjögren syndrome: a nationwide population-based cohort study. Peer J. 2018;6:e5109. doi: 10.7717/peerj.5109
Shikama Y, Kudo Y, Ishimaru N, Funaki M. Potential Role of Free Fatty Acids in the Pathogenesis of Periodontitis and Primary Sjögren's Syndrome. Int J Mol Sci. 2017;18(4):836. doi: 10.3390/ijms18040836
Terrizzi AR, Conti MI, Martínez MP, Fernández-Solari J. The Process of Acclimation to Chronic Hypoxia Leads to Submandibular Gland and Periodontal Alterations: An Insight on the Role of Inflammatory Mediators. Mediators Inflamm. 2018;2018:6794508. doi: 10.1155/2018/6794508
Lin B, Zhao F, Liu Y, et al. Alterations in Oral Microbiota of Differentiated Thyroid Carcinoma Patients With Xerostomia After Radioiodine Therapy. Front Endocrinol (Lausanne). 2022;13:895970. doi: 10.3389/fendo.2022.895970
Pussinen PJ, Kopra E, Pietiäinen M, et al. Periodontitis and cardiometabolic disorders: The role of lipopolysaccharide and endotoxemia. Periodontol 2000. 2022;89(1):19-40. doi: 10.1111/prd.12433
Shinomiya T, Kawaguchi M, Okubo M, Kosuge Y, Yoshikawa M. mRNA expression and localization of LPS-induced β-defensin isoforms in rat salivary glands. Bull Tokyo Dent Coll. 2014;55(3):139-147. doi: 10.2209/tdcpublication.55.139
Seil M, El Ouaaliti M, Abdou Foumekoye S, Pochet S, Dehaye JP. Distinct regulation by lipopolysaccharides of the expression of interleukin-1β by murine macrophages and salivary glands. Innate Immun. 2012;18(1):14-24. doi: 10.1177/1753425910377101
Proctor GB, Shaalan AM. Disease-Induced Changes in Salivary Gland Function and the Composition of Saliva. J Dent Res. 2021;100(11):1201-1209. doi: 10.1177/00220345211004842
Han P, Bartold PM, Ivanovski S. The emerging role of small extracellular vesicles in saliva and gingival crevicular fluid as diagnostics for periodontitis. J Periodontal Res. 2022;57(1):219-231. doi: 10.1111/jre.12950
Chen M, Cai W, Zhao S, et al. Oxidative stress-related biomarkers in saliva and gingival crevicular fluid associated with chronic periodontitis: A systematic review and meta-analysis. J Clin Periodontol. 2019;46(6):608-622. doi: 10.1111/jcpe.13112
Tarasenko LM, Petrushanko TA. Stress and periodontium. Poltava; 1999.
Keremi B, Beck A, Fabian TK, et al. Stress and Salivary Glands. Curr Pharm Des. 2017;23(27):4057-4065. doi: 10.2174/1381612823666170215110648
Matsytska YK, Akimov OY, Mykytenko AO. Influence of corvitin and metformin on biochemical changes in lacrimal glands of rats during water avoidance stress modeling. Oftalmologicheskii Zhurnal. 2022;97(3):39-44. doi: 10.31288/oftalmolzh202233944
Spector AM, Postolache TT, Akram F, Scott AJ, Wadhawan A, Reynolds MA. Psychological Stress: A Predisposing and Exacerbating Factor in Periodontitis. Curr Oral Health Rep. 2020;7:208-215. doi: 10.1007/s40496-020-00282-2
Yamamoto K, Takao T, Nakayama J, et al. Water avoidance stress induces frequency through cyclooxygenase-2 expression: a bladder rat model. Int J Urol. 2012;19(2):155-162. doi: 10.1111/j.1442-2042.2011.02905.x
Mykytenko AO, Akimov OY, Neporada KS. Influence of lipopolysaccharide on the development of oxidative-nitrosative stress in the liver of rats under conditions of chronic alcohol intoxication. Fiziol Zh. 2022;68(2):29-35. doi: 10.15407/fz68.02.029
Yelinska AM, Kostenko VO. Combined effects of quercetin and modulators of redox sensitive factors on the indicators of systemic inflammatory response, carbohydrate and lipid metabolism in rats exposed to intraperitoneal and intragingival administration of salmonella typhi lipopolysaccharide. Actual Problems of the Modern Medicine: Bulletin of Ukrainian Medical Stomatological Academy. 2020;20(1):13-18. doi: 10.31718/2077-1096.20.1.13
Lane MB, Flatland B, Olin SJ, Fecteau KA, Rick M, Giori L. Analytic performance evaluation of a veterinary-specific ELISA for measurement of serum cortisol concentrations of dogs. J Am Vet Med Assoc. 2018;253(12):1580-1588. doi: 10.2460/javma.253.12.1580
Akimov OYe, Kostenko VO. Functioning of nitric oxide cycle in gastric mucosa of rats under excessive combined intake of sodium nitrate and fluoride. Ukr Biochem J. 2016;88(6):70-75. doi: 10.15407/ubj88.06.070
Yelins’ka AM, Akimov OYe, Kostenko VO. Role of AP-1 transcriptional factor in development of oxidative and nitrosative stress in periodontal tissues during systemic inflammatory response. Ukr Biochem J. 2019;91(1):80-85.
Mykytenko AO, Akimov OYe, Yeroshenko GA, Neporada KS. Influence of NF -κB on the development of oxidative-nitrosative stress in the liver of rats under conditions of chronic alcohol intoxication. Ukr Biochem J. 2022; 94(6):57-66. doi: 10.15407/ubj94.06.057
Gérard-Monnier D, Erdelmeier I, Régnard K, Moze-Henry N, Yadan JC, Chaudière J. Reactions of 1-Methyl-2-phenylindole with Malondialdehyde and 4-Hydroxyalkenals. Analytical Applications to a Colorimetric Assay of Lipid Peroxidation. Chem Res Toxicol. 1998;11(10):1176-1183.
Gaston B, Reilly J, Drazen JM, et al. Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc Natl Acad Sci USA. 1993;90:10957-10961.
Mykytenko A, Akimov O, Shevchenko O, Neporada K. Role of sulfide anion in the development of chronic alcoholic hepatitis under the conditions of modulation of adenosine monophosphate kinase – a correlational study. Eur J Clin Exp Med. 2023;21(3):567-575. doi: 10.15584/ejcem.2023.3.24
Beregova TV, Neporada KS, Skrypnyk M, et al. Efficacy of nanoceria for periodontal tissues alteration in glutamate-induced obese rats-multidisciplinary considerations for personalized dentistry and prevention. EPMA J. 2017;8(1):43-49. doi: 10.1007/s13167-017-0085-7
Feura ES, Yang L, Schoenfisch MH. Antibacterial activity of nitric oxide-releasing carboxymethylcellulose against periodontal pathogens. J Biomed Mater Res A. 2021;109(5):713-721. doi: 10.1002/jbm.a.37056
Borisov VB, Forte E. Bioenergetics and Reactive Nitrogen Species in Bacteria. Int J Mol Sci. 2022;23(13):7321. doi: 10.3390/ijms23137321
Galler KM, Weber M, Korkmaz Y, Widbiller M, Feuerer M. Inflammatory Response Mechanisms of the Dentine-Pulp Complex and the Periapical Tissues. Int J Mol Sci. 2021;22(3):1480. doi: 10.3390/ijms22031480
Yilmaz M, Demir E, Gürsoy M, Firatli E, Loimaranta V, Gürsoy UK. Salivary levels of BAFF, TWEAK, and soluble CD163 and salivary arginase activity before and after periodontal treatment. J Periodontal Res. 2023;58(3):646-654. doi: 10.1111/jre.13124
Silva MLF, Alves PM, Souza DM, et al. Analysis of Macrophage Activation Markers in an Experimental Model of Cutaneous Leishmaniasis Treated with Photodynamic Therapy Mediated by 5-Aminolevulinic Acid. Photobiomodul Photomed Laser Surg. 2019;37(5):298-304. doi: 10.1089/photob.2018.4574
Oliveira-Brito PKM, Rezende CP, Almeida F, Roque-Barreira MC, da Silva TA. iNOS/Arginase-1 expression in the pulmonary tissue over time during Cryptococcus gattii infection. Innate Immun. 2020;26(2):117-129. doi: 10.1177/1753425919869436
Gao JM, Yi SQ, Wu MS, et al. Investigation of infectivity of neonates and adults from different rat strains to Toxoplasma gondii Prugniaud shows both variation which correlates with iNOS and Arginase-1 activity and increased susceptibility of neonates to infection. Exp Parasitol. 2015;149:47-53. doi: 10.1016/j.exppara.2014.12.008
Dong J, Qu Y, Li J, et al. Cortisol inhibits NF-κB and MAPK pathways in LPS activated bovine endometrial epithelial cells. Int Immunopharmacol. 2018;56:71-77. doi: 10.1016/j.intimp.2018.01.021
Gurel SG, Sogut I, Hurdag C, Gurel A, Tutar A, Cikler-Dulger E. Effect of fulvic acid on gastric mucosa damage caused by chronic water avoidance stress. Biotech Histochem. 2022;97(3):199-206. doi: 10.1080/10520295.2021.1926541
Traini C, Idrizaj E, Garella R, et al. Otilonium Bromide treatment prevents nitrergic functional and morphological changes caused by chronic stress in the distal colon of a rat IBS model. J Cell Mol Med. 2021;25(14):6988-7000. doi: 10.1111/jcmm.16710
McKendrick JG, Emmerson E. The role of salivary gland macrophages in infection, disease and repair. Int Rev Cell Mol Biol. 2022;368:1-34. doi: 10.1016/bs.ircmb.2022.02.001
Oliveira-Paula GH, Pinheiro LC, Tanus-Santos JE. Mechanisms impairing blood pressure responses to nitrite and nitrate. Nitric Oxide. 2019;85:35-43. doi: 10.1016/j.niox.2019.01.015
Wu Y, Ding Y, Ramprasath T, Zou MH. Oxidative Stress, GTPCH1, and Endothelial Nitric Oxide Synthase Uncoupling in Hypertension. Antioxid Redox Signal. 2021;34(9):750-764. doi: 10.1089/ars.2020.8112
Du J, Zhu M, Bao H, et al. The Role of Nutrients in Protecting Mitochondrial Function and Neurotransmitter Signaling: Implications for the Treatment of Depression, PTSD, and Suicidal Behaviors. Crit Rev Food Sci Nutr. 2016;56(15):2560-2578. doi: 10.1080/10408398.2013.876960
Uchiyama J, Akiyama M, Hase K, Kumagai Y, Kim YG. Gut microbiota reinforce host antioxidant capacity via the generation of reactive sulfur species. Cell Rep. 2022;38(10):110479. doi: 10.1016/j.celrep.2022.110479
Orecchioni M, Ghosheh Y, Pramod AB, Ley K. Macrophage Polarization: Different Gene Signatures in M1(LPS+) vs. Classically and M2(LPS-) vs. Alternatively Activated Macrophages. Front Immunol. 2019;10:1084. doi: 10.3389/fimmu.2019.01084
Liu L, Guo H, Song A, et al. Progranulin inhibits LPS-induced macrophage M1 polarization via NF-кB and MAPK pathways. BMC Immunol. 2020;21(1):32. doi: 10.1186/s12865-020-00355-y
Ives A, Nomura J, Martinon F, et al. Xanthine oxidoreductase regulates macrophage IL1β secretion upon NLRP3 inflammasome activation. Nat Commun. 2015;6:6555. doi: 10.1038/ncomms7555
Wu L, Zhou C, Wu J, Chen S, Tian Z, Du Q. Corticosterone Inhibits LPS-Induced NLRP3 Inflammasome Priming in Macrophages by Suppressing Xanthine Oxidase. Mediators Inflamm. 2020;2020:6959741. doi: 10.1155/2020/6959741
Kim EN, Jeong GS. Inhibitory Effect of Periodontitis through C/EBP and 11β-Hydroxysteroid Dehydrogenase Type 1 Regulation of Betulin Isolated from the Bark of Betula platyphylla. Pharmaceutics. 2022;14(9):1868. doi: 10.3390/pharmaceutics14091868
Plecitá-Hlavatá L, Engstová H, Holendová B, et al. Mitochondrial Superoxide Production Decreases on Glucose-Stimulated Insulin Secretion in Pancreatic β Cells Due to Decreasing Mitochondrial Matrix NADH/NAD+ Ratio. Antioxid Redox Signal. 2020;33(12):789-815. doi: 10.1089/ars.2019.7800
Wang Y, Liu Z, Liu C, Liu R, Yang C, Wang L, Song L. Cortisol modulates glucose metabolism and oxidative response after acute high temperature stress in Pacific oyster Crassostrea gigas. Fish Shellfish Immunol. 2022;126:141-149. doi: 10.1016/j.fsi.2022.05.010
Saruta J, To M, Sakaguchi W, Kondo Y, Tsukinoki K. Brain-derived neurotrophic factor is related to stress and chewing in saliva and salivary glands. Jpn Dent Sci Rev. 2020;56(1):43-49. doi: 10.1016/j.jdsr.2019.11.001
Almohaimeed HM, Albadawi EA, Mohammedsaleh ZM, et al. Brain-derived Neurotropic factor (BDNF) mediates the protective effect of Cucurbita pepo L. on salivary glands of rats exposed to chronic stress evident by structural, biochemical and molecular study. J Appl Oral Sci. 2021;29:e20201080. doi: 10.1590/1678-7757-2020-1080
Paudel D, Kuramitsu Y, Uehara O, et al. Proteomic and microbiota analyses of the oral cavity during psychological stress. PLoS One. 2022;17(5):e0268155. doi: 10.1371/journal.pone.0268155
Chen H, Feng X, Yang Q, Yang K, Man S. Expression Pattern and Value of Brain-Derived Neurotrophic Factor in Periodontitis. Int Dent J. 2023;73(4):542-549. doi: 10.1016/j.identj.2023.03.002
Shi J, Song S, Wu K, Liang G, Wang A, Xu X. Role of brain-derived neurotrophic factor in endotoxaemia-induced acute lung injury. Exp Physiol. 2023;108(12):1456-1465. doi: 10.1113/EP091228
Huang Q, Wu M, Wu X, Zhang Y, Xia Y. Muscle-to-tumor crosstalk: The effect of exercise-induced myokine on cancer progression. Biochim Biophys Acta Rev Cancer. 2022;1877(5):188761. doi: 10.1016/j.bbcan.2022.188761
Montone RA, Camilli M, Del Buono MG, et al. Brain-derived neurotrophic factor in patients with acute coronary syndrome. Transl Res. 2021;231:39-54. doi: 10.1016/j.trsl.2020.11.006
Claro AE, Palanza C, Mazza M, et al. Why do we not reverse the path? Stress can cause depression, reduction of brain-derived neurotrophic factor and increased inflammation. World J Psychiatry. 2022;12(9):1264-1267. doi: 10.5498/wjp.v12.i9.1264
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