TNF-α involvement in insulin resistance induced by experimental scorpion envenomation

Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few experimental studies assessing the effects of scorpion venom on adipose tissue function in vivo. To study the adipose tissue inflammation (ATI) induced by Andro...

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Published inPLoS neglected tropical diseases Vol. 6; no. 7; p. e1740
Main Authors Ait-Lounis, Aouatef, Laraba-Djebari, Fatima
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.07.2012
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Abstract Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few experimental studies assessing the effects of scorpion venom on adipose tissue function in vivo. To study the adipose tissue inflammation (ATI) induced by Androctonus australis hector (Aah) venom and to assess possible mechanisms of ATI, mice (n = 6, aged 1 month) were injected with Aah (0.45 mg/kg), toxic fraction of Aah (FTox-G50; 0.2 mg/kg) or saline solution (control). Inflammatory responses were evaluated by ELISA and cell sorting analyses in adipose tissue 45 minutes and 24 hours after injection. Quantitative real-time PCR was used to assess the regulation of genes implicated in glucose uptake. The titers of selected inflammatory cytokines (IL-1β, IL-6 and TNF-α) were also determined in sera and in insulin target tissues. The serum concentration of IL-1β rose 45 minutes after envenomation and returned to basal level after 24 hours. The pathophysiological effects of the venom after 24 hours mainly involved M1-proinflammatory macrophage infiltration in adipose tissue combined with high titers of IL-1β, IL-6 and TNF-α. Indeed, TNF-α was strongly induced in both adipose tissue and skeletal muscle. We studied the effects of Aah venom on genes implicated in insulin-stimulated glucose uptake. Insulin induced a significant increase in the expression of the mRNAs for hexokinase 2 and phosphatidylinositol 3-kinase in both skeletal muscle and adipose tissue in control mice; this upregulation was completely abolished after 24 hours in mice envenomed with Aah or FTox-G50. Our findings suggest that Aah venom induces insulin resistance by mechanisms involving TNF-α-dependent Map4k4 kinase activation in the adipose tissue.
AbstractList Background: Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few experimental studies assessing the effects of scorpion venom on adipose tissue function in vivo. Methodology/Principal Findings: To study the adipose tissue inflammation (ATI) induced by Androctonus australis hector (Aah) venom and to assess possible mechanisms of ATI, mice (n = 6, aged 1 month) were injected with Aah (0.45 mg/kg), toxic fraction of Aah (FTox-G50;0.2 mg/kg) or saline solution (control). Inflammatory responses were evaluated by ELISA and cell sorting analyses in adipose tissue 45 minutes and 24 hours after injection. Quantitative real-time PCR was used to assess the regulation of genes implicated in glucose uptake. The titers of selected inflammatory cytokines (IL-1β, IL-6 and TNF-α) were also determined in sera and in insulin target tissues. The serum concentration of IL-1 β rose 45 minutes after envenomation and returned to basal level after 24 hours. The pathophysiological effects of the venom after 24 hours mainly involved M1-proinflammatory macrophage infiltration in adipose tissue combined with high titers of IL-1 β, IL-6 and TNF-α. Indeed, TNF-α was strongly induced in both adipose tissue and skeletal muscle. We studied the effects of Aah venom on genes implicated in insulin-stimulated glucose uptake. Insulin induced a significant increase in the expression of the mRNAs for hexokinase 2 and phosphatidylinositol 3-kinase in both skeletal muscle and adipose tissue in control mice; this upregulation was completely abolished after 24 hours in mice envenomed with Aah or FTox-G50. Conclusions/Significance: Our findings suggest that Aah venom induces insulin resistance by mechanisms involving TNF- α-dependent Map4k4 kinase activation in the adipose tissue.
Androctonus australis hector ( Aah ) is the scorpion most frequently causing serious human envenomation. In Algeria, Aah is responsible for approximately 50,000 cases of scorpion envenomation per year. The Aah sting causes multi-system failure that may be fatal; the manifestations include cardiopulmonary abnormalities, lung edema and inflammation. In addition, hyperglycemia and hyperinsulinemia have been described in scorpion-envenomed animals. The mechanisms causing systemic and local inflammation are poorly understood. Here, we report that Aah venom causes pronounced upregulation of TNF-α, IL1-β and IL-6 expression in the adipose tissue, exacerbating inflammation. As the inflammatory state intensifies, 24 hours after envenomation, TNF-α and other factors are upregulated, and Map4k4 expression increases, blunting the insulin response in adipocytes by decreasing Hexokinase 2 expression. Administration of TNF-α inhibitor following the envenomation reduces Map4k4 expression and restores glucose uptake in adipose tissue. These findings provide coherent evidence linking Aah venom-induced adipose tissue inflammation to insulin resistance. The value of TNF-α inhibitors as a treatment complementary to anti-scorpion venom immunotherapy should be evaluated clinically.
Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few experimental studies assessing the effects of scorpion venom on adipose tissue function in vivo. To study the adipose tissue inflammation (ATI) induced by Androctonus australis hector (Aah) venom and to assess possible mechanisms of ATI, mice (n = 6, aged 1 month) were injected with Aah (0.45 mg/kg), toxic fraction of Aah (FTox-G50; 0.2 mg/kg) or saline solution (control). Inflammatory responses were evaluated by ELISA and cell sorting analyses in adipose tissue 45 minutes and 24 hours after injection. Quantitative real-time PCR was used to assess the regulation of genes implicated in glucose uptake. The titers of selected inflammatory cytokines (IL-1β, IL-6 and TNF-α) were also determined in sera and in insulin target tissues. The serum concentration of IL-1β rose 45 minutes after envenomation and returned to basal level after 24 hours. The pathophysiological effects of the venom after 24 hours mainly involved M1-proinflammatory macrophage infiltration in adipose tissue combined with high titers of IL-1β, IL-6 and TNF-α. Indeed, TNF-α was strongly induced in both adipose tissue and skeletal muscle. We studied the effects of Aah venom on genes implicated in insulin-stimulated glucose uptake. Insulin induced a significant increase in the expression of the mRNAs for hexokinase 2 and phosphatidylinositol 3-kinase in both skeletal muscle and adipose tissue in control mice; this upregulation was completely abolished after 24 hours in mice envenomed with Aah or FTox-G50. Our findings suggest that Aah venom induces insulin resistance by mechanisms involving TNF-α-dependent Map4k4 kinase activation in the adipose tissue.
BACKGROUND: Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few experimental studies assessing the effects of scorpion venom on adipose tissue function in vivo. METHODOLOGY/PRINCIPAL FINDINGS: To study the adipose tissue inflammation (ATI) induced by Androctonus australis hector (Aah) venom and to assess possible mechanisms of ATI, mice (n = 6, aged 1 month) were injected with Aah (0.45 mg/kg), toxic fraction of Aah (FTox-G50; 0.2 mg/kg) or saline solution (control). Inflammatory responses were evaluated by ELISA and cell sorting analyses in adipose tissue 45 minutes and 24 hours after injection. Quantitative real-time PCR was used to assess the regulation of genes implicated in glucose uptake. The titers of selected inflammatory cytokines (IL-1β, IL-6 and TNF-α) were also determined in sera and in insulin target tissues. The serum concentration of IL-1β rose 45 minutes after envenomation and returned to basal level after 24 hours. The pathophysiological effects of the venom after 24 hours mainly involved M1-proinflammatory macrophage infiltration in adipose tissue combined with high titers of IL-1β, IL-6 and TNF-α. Indeed, TNF-α was strongly induced in both adipose tissue and skeletal muscle. We studied the effects of Aah venom on genes implicated in insulin-stimulated glucose uptake. Insulin induced a significant increase in the expression of the mRNAs for hexokinase 2 and phosphatidylinositol 3-kinase in both skeletal muscle and adipose tissue in control mice; this upregulation was completely abolished after 24 hours in mice envenomed with Aah or FTox-G50. CONCLUSIONS/SIGNIFICANCE: Our findings suggest that Aah venom induces insulin resistance by mechanisms involving TNF-α-dependent Map4k4 kinase activation in the adipose tissue.
Audience Academic
Author Ait-Lounis, Aouatef
Laraba-Djebari, Fatima
AuthorAffiliation 1 Laboratory of Cellular and Molecular Biology, Faculty of Biological Sciences, University of Sciences and Technology Houari Boumediene (USTHB), Algiers, Algeria
2 Laboratory of Research and Development on Venoms, Pasteur Institute of Algeria, Algiers, Algeria
Venezuela
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Notes Conceived and designed the experiments: AAL FLD. Performed the experiments: AAL. Analyzed the data: AAL FLD. Contributed reagents/materials/analysis tools: AAL FLD. Wrote the paper: AAL FLD.
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Snippet Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few experimental...
Background: Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few...
Androctonus australis hector ( Aah ) is the scorpion most frequently causing serious human envenomation. In Algeria, Aah is responsible for approximately...
BACKGROUND: Scorpion venom induces systemic inflammation characterized by an increase in cytokine release and chemokine production. There have been few...
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StartPage e1740
SubjectTerms Adipose Tissue - physiopathology
Adipose tissues
Animals
Biology
Cytokines - analysis
Disease Models, Animal
Drug resistance
Gene expression
Gene Expression Profiling
Genetic aspects
Glucose metabolism
Health aspects
Insulin Resistance
Medicine
Mice
NF-kappaB-Inducing Kinase
Protein Serine-Threonine Kinases - metabolism
Real-Time Polymerase Chain Reaction
Scorpions
Snake Bites - complications
Tumor Necrosis Factor-alpha - metabolism
Venom
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Title TNF-α involvement in insulin resistance induced by experimental scorpion envenomation
URI https://www.ncbi.nlm.nih.gov/pubmed/22816003
https://pubmed.ncbi.nlm.nih.gov/PMC3398957
https://doaj.org/article/a4ea7a6c6e304529b57ebd6a9e414f06
Volume 6
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