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Basic Research| Volume 47, ISSUE 7, P1126-1131, July 2021

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Maternal Apical Periodontitis Increases Insulin Resistance and Modulates the Antioxidant Defense System in the Gastrocnemius Muscle of Adult Offspring

  • Thaís Verônica Saori Tsosura
    Correspondence
    Address requests for reprints to Dr Thaís Verônica Saori Tsosura, São Paulo State University (UNESP), School of Dentistry, R. José Bonifácio, 1193, 16015-050 Araçatuba, SP, Brazil.
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil

    Programa de Pós-Graduação Multicêntrico em Ciências Fisiológicas (PPGMCF)/Sociedade Brasileira de Fisiologia (SBFis), São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Rodrigo Martins dos Santos
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil

    Programa de Pós-Graduação Multicêntrico em Ciências Fisiológicas (PPGMCF)/Sociedade Brasileira de Fisiologia (SBFis), São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Antonio Hernandes Chaves Neto
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil

    Programa de Pós-Graduação Multicêntrico em Ciências Fisiológicas (PPGMCF)/Sociedade Brasileira de Fisiologia (SBFis), São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Fernando Yamamoto Chiba
    Affiliations
    Department of Preventive and Restorative Dentistry, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Ana Carolina Nascimento Carnevali
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Maria Sara de Lima Coutinho Mattera
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Bianca Elvira Belardi
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil

    Programa de Pós-Graduação Multicêntrico em Ciências Fisiológicas (PPGMCF)/Sociedade Brasileira de Fisiologia (SBFis), São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Luciano Tavares Ângelo Cintra
    Affiliations
    Department of Preventive and Restorative Dentistry, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Nathália Evelyn da Silva Machado
    Affiliations
    Department of Preventive and Restorative Dentistry, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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  • Doris Hissako Matsushita
    Affiliations
    Department of Basic Sciences, São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil

    Programa de Pós-Graduação Multicêntrico em Ciências Fisiológicas (PPGMCF)/Sociedade Brasileira de Fisiologia (SBFis), São Paulo State University (UNESP), School of Dentistry, Araçatuba, Brazil
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Published:April 14, 2021DOI:https://doi.org/10.1016/j.joen.2021.04.003

      Abstract

      Introduction

      Maternal apical periodontitis (AP) is associated with insulin resistance (IR) in adult offspring. Oxidative stress has been linked to IR. This study investigated insulin sensitivity (IS) and oxidative stress in the gastrocnemius muscle (GM) of adult offspring of rats with AP.

      Methods

      Fifteen female Wistar rats were distributed into a control group, a group with 1 tooth with AP, and a group with 4 teeth with AP. Thirty days after AP induction, female rats were mated with healthy male rats. When male offspring reached 75 days of age, glycemia, insulinemia, and IS were determined. In the GM, the oxidative damage products (thiobarbituric acid reactive substances and carbonyl protein) and activities of enzymatic (superoxide dismutase, catalase, and glutathione peroxidase) and nonenzymatic (glutathione and total antioxidant capacity) antioxidants were quantified. Analysis of variance was performed followed by the Tukey post hoc test (P < .05).

      Results

      Maternal AP was associated with decreased IS and changes in antioxidant activities (reduced superoxide dismutase and increased catalase, glutathione peroxidase, and glutathione) and decreased thiobarbituric acid reactive substance concentration in the GM of their adult offspring. However, maternal AP does not appear to affect glycemia, carbonyl protein concentration, and the nonenzymatic total antioxidant capacity in the GM of this offspring.

      Conclusions

      Maternal AP modulates the antioxidant defense system in the GM of their adult offspring, attenuating lipid peroxidation in this tissue. This reflects part of an adaptive response of the offspring to the stimulation of the maternal chronic oral inflammatory process in which the organism acts by decreasing oxidative tissue damage in the postnatal stage. The present study improves knowledge about the impact of maternal oral inflammation on healthy offspring.

      Key Words

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      References

        • Nita M.
        • Grzybowski A.
        The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults.
        Oxid Med Cell Longev. 2016; 2016 (3164734)
        • Birben E.
        • Sahiner U.M.
        • Sackesen C.
        • et al.
        Oxidative stress and antioxidant defense.
        World Allergy Organ J. 2012; 5: 9-19
        • Hurrle S.
        • Hsu W.H.
        The etiology of oxidative stress in insulin resistance.
        Biomed J. 2017; 40: 257-262
        • Dokken B.B.
        • Saengsirisuwan V.
        • Kim J.S.
        • et al.
        Oxidative stress-induced insulin resistance in rat skeletal muscle: role of glycogen synthase kinase-3.
        Am J Physiol Endocrinol Metab. 2008; 294: E615-E621
        • Maddux B.A.
        • See W.
        • Lawrence Jr., J.C.
        • et al.
        Protection against oxidative stress-induced insulin resistance in rat L6 muscle cells by mircomolar concentrations of alpha-lipoic acid.
        Diabetes. 2001; 50: 404-410
        • Bloch-Damti A.
        • Bashan N.
        Proposed mechanisms for the induction of insulin resistance by oxidative stress.
        Antioxid Redox Signal. 2005; 7: 1553-1567
        • Tsosura T.V.
        • Chiba F.Y.
        • Mattera M.S.
        • et al.
        Maternal apical periodontitis is associated with insulin resistance in adult offspring.
        Int Endod J. 2019; 52: 1040-1050
        • Bonora E.
        • Targher G.
        • Alberiche M.
        • et al.
        Homeostasis model assessment closely mirrors the glucose clamp technique in the assessment of insulin sensitivity: studies in subjects with various degrees of glucose tolerance and insulin sensitivity.
        Diabetes Care. 2000; 23: 57-63
        • Lowry O.H.
        • Rosebrough N.J.
        • Farr A.L.
        • et al.
        Protein measurement with the folin phenol reagent.
        J Biol Chem. 1951; 193: 265-275
        • Niehaus Jr., W.G.
        • Samuelsson B.
        Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation.
        Eur J Biochem. 1968; 6: 126-130
        • Mesquita C.S.
        • Oliveira R.
        • Bento F.
        • et al.
        Simplified 2,4-dinitrophenylhydrazine spectrophotometric assay for quantification of carbonyls in oxidized proteins.
        Anal Biochem. 2014; 458: 69-71
        • Marklund S.
        • Marklund G.
        Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase.
        Eur J Biochem. 1974; 47: 469-474
        • Aebi H.
        Catalase in vitro.
        Methods Enzymol. 1984; 105: 121-126
        • Tipple T.E.
        • Rogers L.K.
        Methods for the determination of plasma or tissue glutathione levels.
        Methods Mol Biol. 2012; 889: 315-324
        • Benzie I.F.
        • Strain J.J.
        The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay.
        Anal Biochem. 1996; 239: 70-76
        • Hocher B.
        More than genes: the advanced fetal programming hypothesis.
        J Reprod Immunol. 2014; 104-105: 8-11
        • Wilcox G.
        Insulin and insulin resistance.
        Clin Biochem Rev. 2005; 26: 19-39
        • Shirakashi D.J.
        • Leal R.P.
        • Colombo N.H.
        • et al.
        Maternal periodontal disease in rats decreases insulin sensitivity and insulin signaling in adult offspring.
        J Periodontol. 2013; 84: 407-414
        • Mattera M.S.
        • Chiba F.Y.
        • Mota M.S.
        • et al.
        Maternal periodontitis decreases plasma membrane GLUT4 content in skeletal muscle of adult offspring.
        Life Sci. 2016; 148: 194-200
        • Mattera M.S.
        • Chiba F.Y.
        • Lopes F.L.
        • et al.
        Effect of maternal periodontitis on GLUT4 and inflammatory pathway in adult offspring.
        J Periodontol. 2019; 90: 884-893
        • Loh K.
        • Deng H.
        • Fukushima A.
        • et al.
        Reactive oxygen species enhance insulin sensitivity.
        Cell Metab. 2009; 10: 260-272
        • Zeb A.
        • Ullah F.
        A Simple spectrophotometric method for the determination of thiobarbituric acid reactive substances in fried fast foods.
        J Anal Methods Chem. 2016; 2016 (9412767)
        • Dalle-Donne I.
        • Rossi R.
        • Giustarini D.
        • et al.
        Protein carbonyl groups as biomarkers of oxidative stress.
        Clin Chim Acta. 2003; 329: 23-38
        • Padmavathi I.J.
        • Rao K.R.
        • Raghunath M.
        Impact of maternal chromium restriction on glucose tolerance, plasma insulin and oxidative stress in WNIN rat offspring.
        J Mol Endocrinol. 2011; 47: 261-271
        • Al-Amin M.M.
        • Alam T.
        • Hasan S.M.
        • et al.
        Prenatal maternal lipopolysaccharide administration leads to age- and region-specific oxidative stress in the early developmental stage in offspring.
        Neuroscience. 2016; 318: 84-93
        • Ighodaro O.M.
        • Akinloye O.A.
        First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid.
        Alexandria J Med. 2018; 54: 287-293
        • Zhu Y.
        • Carvey P.M.
        • Ling Z.
        Altered glutathione homeostasis in animals prenatally exposed to lipopolysaccharide.
        Neurochem Int. 2007; 50: 671-680
        • Ouardi F.Z.
        • Anarghou H.
        • Malqui H.
        • et al.
        Gestational and lactational exposure to malathion affects antioxidant status and neurobehavior in mice pups and offspring.
        J Mol Neurosci. 2019; 69: 17-27
        • Burton G.J.
        • Jauniaux E.
        Oxidative stress.
        Best Pract Res Clin Obstet Gynaecol. 2011; 25: 287-299
        • Panday S.
        • Talreja R.
        • Kavdia M.
        The role of glutathione and glutathione peroxidase in regulating cellular level of reactive oxygen and nitrogen species.
        Microvasc Res. 2020; 131 (104010)
        • Rook D.
        • Te Braake F.W.
        • Schierbeek H.
        • et al.
        Glutathione synthesis rates in early postnatal life.
        Pediatr Res. 2010; 67: 407-411
        • Young I.S.
        Measurement of total antioxidant capacity.
        J Clin Pathol. 2001; 54: 339