Maternal Periodontal Disease in Rats Decreases Insulin Sensitivity and Insulin Signaling in Adult Offspring

Shirakashi, Daisy Jaqueline; Leal, Rosana P.; Colombo, Natália Helena; Chiba, Fernando Yamamoto; Garbín, Cléa Adas Saliba; Jardim, Élerson Gaetti; Antoniali, Cristina; Sumida, Dóris Hissako

doi:10.1902/jop.2012.110372

Cited by 14 publications

(33 citation statements)

References 47 publications

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“…Similar results were observed by Shirakashi et al . (), who conducted a study in a maternal PD experimental model. It was found that adult offspring of these rats exhibit reduction in pp185 tyrosine phosphorylation after insulin stimulation in the GM and pWAT.…”

Section: Discussionmentioning

confidence: 99%

“…Shirakashi et al . () reported that adult offspring of rats with PD demonstrate IR and impairment in the initial steps of IS in the gastrocnemius muscle (GM) and the periepididymal white adipose tissue (pWAT). This suggested that localized oral inflammation during the gestational period can induce significant alterations in the IS pathway in adult offspring.…”

Section: Introductionmentioning

confidence: 99%

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Maternal apical periodontitis is associated with insulin resistance in adult offspring

et al. 2019

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Aim To investigate the plasma concentrations of glucose, insulin and tumour necrosis factor‐α (TNF‐α) of rats with maternal apical periodontitis (AP) and to explore the effect of maternal inflammation on the initial steps of insulin signalling and the inflammatory pathway in the gastrocnemius muscle (GM) and periepididymal white adipose tissue (pWAT) of adult offspring. Methodology Fifteen female Wistar rats were distributed into a control group (CN), a group with 1 tooth with AP (1AP) and a group with 4 teeth with AP (4AP). Thirty days following induction of AP, female rats from all groups were mated with healthy male rats. When male offspring reached 75 days of age, plasma concentrations of glucose, insulin and TNF‐α were quantified. Insulin resistance was evaluated by the homoeostasis model assessment of insulin resistance (HOMA‐IR) index. Phosphorylation status of pp185 tyrosine, insulin receptor substrate 1 (IRS‐1) serine, IκB kinase α/β (IKKα/β) and c‐Jun N‐terminal kinase (JNK) in the GM and pWAT were measured by Western blot. Analysis of variance was performed, followed by the Tukey's post hoc test. P values <0.05 were considered to be statistically significant. Results Maternal AP promoted insulin resistance, impaired the initial steps of insulin signalling, significantly increased plasma concentrations of insulin (P < 0.001) and TNF‐α (P < 0.05), and enhanced IKKα/β phosphorylation in the GM and pWAT (P < 0.05) of adult offspring. However, maternal AP did not affect fasting glycaemia and JNK phosphorylation in the GM and pWAT of adult offspring. Conclusions Maternal AP was associated with insulin resistance in adult offspring through alterations in insulin signalling and inflammation pathways. The study provides information on the impact of maternal AP on the development of metabolic alterations such as insulin resistance in adult offspring and reinforces the importance of preventing maternal AP in order to maintain the general health of offspring.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Maternal apical periodontitis is associated with insulin resistance in adult offspring

et al. 2019

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“…Our studies have demonstrated that the adult offspring of rats with periodontal disease show an increase in plasma levels of TNF‐α . This cytokine can activate c‐Jun N‐terminal kinases (JNK), IκB kinase β/nuclear factor‐kappa B (IKKβ/NF‐κB) and extracellular signal‐regulated protein (ERK: ERK1 and ERK2) intracellular pathways that are involved in insulin resistance .…”

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confidence: 96%

Effect of maternal periodontitis on GLUT4 and inflammatory pathway in adult offspring

Mattera

Chiba²,

Lopes

et al. 2019

Journal of Periodontology

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Background Maternal periodontal disease leads to low birth weight (LBW), insulin resistance (IR), increased TNF‐α levels, and alterations in insulin signaling in adult offspring. TNF‐α has been associated with the stimulation of IKKβ/NF‐κB, resulting in the decreased expression of GLUT4. Another mechanism that may be involved in decreasing GLUT4 expression is DNA methylation. This study aimed to evaluate in the adult offspring of rats with periodontal disease: IR, inflammatory pathways, DNA methylation, and expression of GLUT4. Methods Female Wistar rats were distributed into control and experimental periodontal disease groups. Seven days after induction of periodontal disease, both groups were mated with healthy male rats. After weaning, male offspring were distributed into control offspring (CN‐o) and periodontal disease offspring (PED‐o) groups. Body weights were measured from 0–75 days of age. At day 75, the following were measured in the offspring: IR (HOMA‐IR index); TNF‐α and NF‐κBp65 content in the gastrocnemius muscle (GM) by western blotting; IKKα/β, JNK, ERK 1/2, NF‐κBp65, and NF‐κBp50 phosphorylation status in the GM by western blotting; DNA methylation by restriction digest and real‐time PCR(qAMP); and expression of GLUT4 mRNA in the GM by real‐time PCR. Results LBW, IR, increases in TNF‐α, IKKα/β, ERK 1/2, NF‐κBp65, and NF‐κBp50 decreased expression of GLUT4 mRNA were observed in the PED‐o rats. No differences were identified in JNK phosphorylation status and DNA methylation in the evaluated regions of the GLUT4‐encoding gene Slc2a4. Conclusion Maternal periodontal disease causes LBW, IR, activation of inflammatory pathways, and decreased GLUT4 expression in the GM of adult offspring.

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“…Although the relationship between GDM and periodontitis is well established, further studies evaluating different populations are needed to improve the knowledge about this relationship (12). Shirakashi et al (13) have shown that maternal periodontal disease in rats may promote fetal programming. An increase in the degree of phosphorylation of IRS-1 serine in adipose tissue (that causes a decrease in insulin signal), as well as increased plasma concentrations of tumor necrosis factor alpha (TNF-α), interleukin 6 and resistin were observed in the adult offspring of rats with periodontal disease (13).…”

Section: Discussionmentioning

confidence: 99%

“…Shirakashi et al (13) have shown that maternal periodontal disease in rats may promote fetal programming. An increase in the degree of phosphorylation of IRS-1 serine in adipose tissue (that causes a decrease in insulin signal), as well as increased plasma concentrations of tumor necrosis factor alpha (TNF-α), interleukin 6 and resistin were observed in the adult offspring of rats with periodontal disease (13). Furthermore, periodontal pathogens can reach the amniotic cavity and cause adverse pregnancy outcomes, including preterm birth and/or low birth weight (14).…”

Section: Discussionmentioning

confidence: 99%

Relationship among Periodontal Disease, Insulin Resistance, Salivary Cortisol, and Stress Levels during Pregnancy

et al. 2016

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Pregnancy is a period involving important metabolic changes that enable the maintenance of the mother's health and development of the fetus. This study aimed to assess the relationship among periodontal disease, insulin resistance, salivary cortisol concentration and level of perceived stress in pregnant women. This was a cross-sectional study. The sample comprised 96 pregnant women between the fifth and seventh month of pregnancy registered at the Basic Health Units of the Unified Health System (SUS). The periodontal condition was assessed after obtainment free and informed consent from the participants. Participants were divided into three groups: control subjects with a healthy periodontal condition (CN; n=46), patients with gingivitis (GI; n=26), and patients with periodontitis (PI; n=24). Saliva and blood samples were collected for evaluation of salivary cortisol concentration, glycemia, insulinemia and Homeostasis Model Assessment-Insulin Resistance index. A validated survey for the assessment of perceived stress levels was also performed. PI group showed significantly higher (p<0.05) blood glucose levels (CN: 4.43±0.05; GI: 4.46±0.04; PI: 4.68±0.08), insulinemy (CN: 6.93±0.45; GI: 8.87±0.79; PI: 12.77±1.30), insulin resistance (CN: 1.40±0.10; GI: 1.81±0.18; PI: 2.66±0.29) compared with the CN and GI groups. The levels of perceived stress were higher (p<0.05) in PI and GI groups when compared to CN group (CN: 20.5±1.26; GI: 25.8±1.95; PI: 26.6±1.36). There was no significant difference in the concentration of salivary cortisol between the groups (CN: 11.13±0.58; GI: 11.96±0.74; PI: 11.47±0.74). It was concluded that there is a relationship between higher levels of perceived stress, insulin resistance and the occurrence of periodontal disease during pregnancy. This study emphasizes the importance of preventing periodontitis in order to avoid insulin resistance and stress during pregnancy since these can cause systemic complications for the mother and the fetus.

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Maternal Periodontal Disease in Rats Decreases Insulin Sensitivity and Insulin Signaling in Adult Offspring

Cited by 14 publications

References 47 publications

Maternal apical periodontitis is associated with insulin resistance in adult offspring

Maternal apical periodontitis is associated with insulin resistance in adult offspring

Effect of maternal periodontitis on GLUT4 and inflammatory pathway in adult offspring

Relationship among Periodontal Disease, Insulin Resistance, Salivary Cortisol, and Stress Levels during Pregnancy

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