Cited by 1,961Adipokines, Inflammation, and Metabolic DiseasesAdvanced Glycation End Products researchDiabetes Management and Research

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Inflammatory Cytokine Concentrations Are Acutely Increased by Hyperglycemia in Humans: Role of Oxidative Stress

Esposito, Katherine, Nappo, Francesco, Marfella, Raffaele, Giugliano, Giovanni, Giugliano, Francesco, Ciotola, Myriam, Quagliaro, Lisa, Ceriello, Antonio, Giugliano, Dario·2002·Circulation

DOI 10.1161/01.cir.0000034509.14906.ae

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Abstract

Background— Circulating levels of interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α) are elevated in diabetic patients. We assessed the role of glucose in the regulation of circulating levels of IL-6, TNF-α, and interleukin-18 (IL-18) in subjects with normal or impaired glucose tolerance (IGT), as well as the effect of the antioxidant glutathione. Methods and Results— Plasma glucose levels were acutely raised in 20 control and 15 IGT subjects and maintained at 15 mmol/L for 5 hours while endogenous insulin secretion was blocked with octreotide. In control subjects, plasma IL-6, TNF-α, and IL-18 levels rose ( P <0.01) within 2 hours of the clamp and returned to basal values at 3 hours. In another study, the same subjects received 3 consecutive pulses of intravenous glucose (0.33 g/kg) separated by a 2-hour interval. Plasma cytokine levels obtained at 3, 4, and 5 hours were higher ( P <0.05) than the corresponding values obtained during the clamp. The IGT subjects had fasting plasma IL-6 and TNF-α levels higher ( P <0.05) than those of control subjects. The increase in plasma cytokine levels during the clamping lasted longer (4 hours versus 2 hours, P <0.01) in the IGT subjects than in the control subjects, and the cytokine peaks of IGT subjects after the first glucose pulse were higher ( P <0.05) than those of control subjects. On another occasion, 10 control and 8 IGT subjects received the same glucose pulses as above during an infusion of glutathione; plasma cytokine levels did not show any significant change from baseline after the 3 glucose pulses. Conclusions— Hyperglycemia acutely increases circulating cytokine concentrations by an oxidative mechanism, and this effect is more pronounced in subjects with IGT. This suggests a causal role for hyperglycemia in the immune activation of diabetes.

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Pharmacological inhibition of NOX reduces atherosclerotic lesions, vascular ROS and immune–inflammatory responses in diabetic Apoe −/− mice
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Altered inflammatory, oxidative, and metabolic responses to exercise in pediatric obesity and type 1 diabetes
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Glycemic control and prevention of perioperative infection
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Mitochondrial Dysfunction and Mitophagy in Type 2 Diabetes: Pathophysiology and Therapeutic Targets
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Elevated Levels of Serum IL-12 and IL-18 are Associated with Lower Frequencies of CD4+CD25highFOXP3+ Regulatory T cells in Young Patients with Type 1 Diabetes
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Effects of the hydroalcoholic extract of Rosa damascena on learning and memory in male rats consuming a high-fat diet
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Narrative Review of Immunomodulatory and Anti-inflammatory Effects of Sodium-Glucose Cotransporter 2 Inhibitors: Unveiling Novel Therapeutic Frontiers
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Wopereis, S., Wolvers, D. A. W., van Erk, M., Gribnau, M. C. M., Kremer, B. H. A., van Dorsten, F. A., Boelsma, E., Garczarek, U., Cnubben, N. H. P., Frenken, L. G. J., et al. (2013) · BMC Medical Genomics · doi:10.1186/1755-8794-6-44 · Cited by 58
“…concentrations at 10 h, namely the AA-derived oxylipins involved in the LOX pathway [5(S)- HETE, 12(S)-HETE and 15(S)-HETE], in the CYP pathways [11, 12-DiHETrE 12-DiHETrE, After the OGTT challenge, the precursor free fatty acids AA, LA, DHA and EPA were significantly reduced after 2 h when…”
Mechanisms of Glucose-Induced Secretion of Pancreatic-Derived Factor (PANDER or FAM3B) in Pancreatic β-Cells
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“. The additional finding that plasma IL-6 also rises in response to both acute hyperglycemic clamp and pulse”
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Nateglinide Reduces Carotid Intima-Media Thickening in Type 2 Diabetic Patients Under Good Glycemic Control
Mita, T., Watada, H., Shimizu, T., Tamura, Y., Sato, F., Watanabe, T., Choi, J. B., Hirose, T., Tanaka, Y., & Kawamori, R. (2007) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.152835 · Cited by 57
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“Finally, glycation end products and circulating cytokines such as tumor necrosis factor a are also suspected of promoting sympathetic activity.(42) The second series of relationships identified between HRV and BGL in the present study was an association between BGL and the LF/HF ratio (also known as the sympathovagal…”
Interleukin-18 serum level is elevated in type 2 diabetes and latent autoimmune diabetes
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“Other studies examining individual risk factors for CVD have also found associations between increasing circulating IL-18 levels and individual CVD risk factors such as central adiposity (43, 44), hyperglycemia ( 45 ), and insulin resistance (43, 46).”
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Rationale for and design of the Acarbose Cardiovascular Evaluation (ACE) trial
Holman, R. R., Bethel, M. A., Chan, J. C. N., Chiasson, J., Doran, Z., Ge, J., Gerstein, H. C., Huo, Y., McMurray, J. J. V., Rydén, L., et al. (2014) · American Heart Journal · doi:10.1016/j.ahj.2014.03.021 · Cited by 56
Breast milk MSCs upregulated β-cells PDX1, Ngn3, and PCNA expression via remodeling ER stress /inflammatory /apoptotic signaling pathways in type 1 diabetic rats
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Lifestyle and Dietary Habits Affect Plasma Levels of Specific Cytokines in Healthy Subjects
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Positive association between stress hyperglycemia ratio and pulmonary infection in patients with ST-segment elevation myocardial infarction undergoing percutaneous coronary intervention
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The Role of Markers of Low-Grade Inflammation for the Early Time Course of Glycemic Control, Glucose Disappearance Rate, and β-Cell Function in Recently Diagnosed Type 1 and Type 2 Diabetes
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Exercise Training Prevents Coronary Endothelial Dysfunction in Type 2 Diabetic Mice
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Effect of Fructooligosaccharides Fraction from Psacalium decompositum on Inflammation and Dyslipidemia in Rats with Fructose-Induced Obesity
Merino-Aguilar, H., Arrieta‐Báez, D., Jiménez‐Estrada, M., Magos-Guerrero, G. A., Hernández-Bautista, R., Notario, A. D. C. S., Almanza-Pérez, J. C., Blancas‐Flores, G., Román‐Ramos, R., & Alarcón-Aguilar, F. J. (2014) · Nutrients · doi:10.3390/nu6020591 · Cited by 60
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“Activation of NF-κB through oxidative stress induced by hyperglycemia increases concentrations of circulating pro-inflammatory cytokines.(72) These inflammatory mechanisms are mediated by macrophages and play an important role in the pathogenesis of diabetic nephropathy.”
Effects of S21403 (mitiglinide) on postprandial generation of oxidative stress and inflammation in type 2 diabetic patients
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“However, the effect of the postprandial state, particularly postprandial hyperglycaemia, on CVD is still a matter of debate [21, 22]; studies show that postprandial hyperglycaemia is accompanied by an increase of both oxidative stress and inflammatory markers [11–15].”
Self-citation
Visit-to-Visit Variability of Hemoglobin A1c in People Without Diabetes and Risk of Major Adverse Cardiovascular Events and All-Cause Mortality
Ghouse, J., Skov, M. W., Kanters, J. K., Lind, B., Isaksen, J. L., Blanche, P., Haunsø, S., Køber, L., Svendsen, J. H., OLESEN, M. S., et al. (2018) · Diabetes Care · doi:10.2337/dc18-1396 · Cited by 59
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Role of clinical pathologies in myocardial injury following ischaemia and reperfusion
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Interpreting ‘anti‐inflammatory’ cytokine responses to exercise: focus on interleukin‐10
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“Although the concept of aberrant immune cell function (Dasu et al. 2008; Dasu & Jialal, 2011; Pavlou et al. 2018) and exacerbated inflammation (Esposito et al. 2002; Devaraj et al. 2006) under hyperglycaemia and/or diabetic states is well established, our findings are the first demonstration of…”
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Morchella esculenta mushroom polysaccharide attenuates diabetes and modulates intestinal permeability and gut microbiota in a type 2 diabetic mice model
Rehman, A. U., Siddiqui, N. Z., Farooqui, N. A., Alam, G., Gul, A., Ahmad, B., Asim, M., Khan, A. I., Xin, Y., Zexu, W., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.984695 · Cited by 56
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Concentration and Activity of the Soluble Form of the Interleukin-7 Receptor α in Type 1 Diabetes Identifies an Interplay Between Hyperglycemia and Immune Function
Monti, P., Brigatti, C., Krasmann, M., Ziegler, A. G., & Bonifacio, E. E. (2013) · Diabetes · doi:10.2337/db12-1726 · Cited by 60
“Hyperglycemia is the hallmark of T1D and is itself a mediator of inflammation (27).”
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Type 2 Diabetes Mellitus and Risk of Non-Hodgkin Lymphoma: A Systematic Review and Meta-Analysis
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Feeding restriction alleviates high carbohydrate diet-induced oxidative stress and inflammation of Megalobrama amblycephala by activating the AMPK-SIRT1 pathway
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Authors: Esposito, K., Nappo, F., Marfella, R., Giugliano, G., Giugliano, F., Ciotola, M., Quagliaro, L., Ceriello, A., & Giugliano, D.
Affiliations: University of Udine (IT)
ORCID: Esposito, Katherine
Marfella, Raffaele
Ceriello, Antonio
Giugliano, Dario
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2002-10-15
Volume: 106
Issue: 16
Pages: 2067-2072
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/01.cir.0000034509.14906.ae
OpenAlex: W2123560318
Cited by: 1,961
References: 36
Citations by year: 2026: 57 · 2025: 69 · 2024: 88 · 2023: 95 · 2022: 106 · 2021: 91 · 2020: 102 · 2019: 83 · 2018: 86 · 2017: 70 · 2016: 87 · 2015: 112 · 2014: 99 · 2013: 102 · 2012: 101
FWCI: 38.18
Type: journal article
Language: en
Open access: closed
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Institutional Research Information System (University of Udine) (submittedVersion)
Archivio Istituzionale della Ricerca - Università degli Studi della Campania "Luigi Vanvitelli" (submittedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Advanced Glycation End Products research
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
Keywords: hyperglycemia, inflammatory cytokines, interleukin-6, TNF-α, IL-18, impaired glucose tolerance, glutathione, oxidative stress, glucose clamp
MeSH terms: Adult, Antioxidants, Blood Glucose, Diabetes Mellitus, Type 2, Female, Glucose Tolerance Test, Glutathione, Humans, Inflammation, Kinetics, Male, Tumor Necrosis Factor-alpha, Interleukin-6, Cytokines, Glucose Intolerance, Oxidative Stress, Interleukin-18

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Inflammatory Cytokine Concentrations Are Acutely Increased by Hyperglycemia in Humans: Role of Oxidative Stress

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