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Sulwon Lecture 2018
Mitochondrial Dysfunction in Adipocytes as a Primary Cause of Adipose Tissue Inflammation
Chang-Yun Woo, Jung Eun Jang, Seung Eun Lee, Eun Hee Koh, Ki-Up Lee
Diabetes Metab J. 2019;43(3):247-256.   Published online March 27, 2019
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  • 265 Download
  • 73 Web of Science
  • 73 Crossref
AbstractAbstract PDFPubReader   

Adipose tissue inflammation is considered a major contributing factor in the development of obesity-associated insulin resistance and cardiovascular diseases. However, the cause of adipose tissue inflammation is presently unclear. The role of mitochondria in white adipocytes has long been neglected because of their low abundance. However, recent evidence suggests that mitochondria are essential for maintaining metabolic homeostasis in white adipocytes. In a series of recent studies, we found that mitochondrial function in white adipocytes is essential to the synthesis of adiponectin, which is the most abundant adipokine synthesized from adipocytes, with many favorable effects on metabolism, including improvement of insulin sensitivity and reduction of atherosclerotic processes and systemic inflammation. From these results, we propose a new hypothesis that mitochondrial dysfunction in adipocytes is a primary cause of adipose tissue inflammation and compared this hypothesis with a prevailing concept that “adipose tissue hypoxia” may underlie adipose tissue dysfunction in obesity. Recent studies have emphasized the role of the mitochondrial quality control mechanism in maintaining mitochondrial function. Future studies are warranted to test whether an inadequate mitochondrial quality control mechanism is responsible for mitochondrial dysfunction in adipocytes and adipose tissue inflammation.


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Role of NO/VASP Signaling Pathway against Obesity-Related Inflammation and Insulin Resistance
Yu Mi Kang, Francis Kim, Woo Je Lee
Diabetes Metab J. 2017;41(2):89-95.   Published online November 15, 2016
  • 4,795 View
  • 61 Download
  • 22 Web of Science
  • 20 Crossref
AbstractAbstract PDFPubReader   

Obesity has quickly become a worldwide pandemic, causing major adverse health outcomes such as dyslipidemia, type 2 diabetes mellitus, cardiovascular disease and cancers. Obesity-induced insulin resistance is the key for developing these metabolic disorders, and investigation to understand the molecular mechanisms involved has been vibrant for the past few decades. Of these, low-grade chronic inflammation is suggested as a critical concept in the development of obesity-induced insulin resistance, and the anti-inflammatory effect of nitric oxide (NO) signaling has been reported to be linked to improvement of insulin resistance in multiple organs involved in glucose metabolism. Recently, a body of evidence suggested that vasodilatory-stimulated phosphoprotein (VASP), a downstream mediator of NO signaling plays a crucial role in the anti-inflammatory effect and improvement of peripheral insulin resistance. These preclinical studies suggest that NO/VASP signaling could be an ideal therapeutic target in the treatment of obesity-related metabolic dysfunction. In this review, we introduce studies that investigated the protective role of NO/VASP signaling against obesity-related inflammation and insulin resistance in various tissues.


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A Systematic Review of Oxidative Stress and Safety of Antioxidants in Diabetes: Focus on Islets and Their Defense
Udayakumar Karunakaran, Keun-Gyu Park
Diabetes Metab J. 2013;37(2):106-112.   Published online April 16, 2013
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AbstractAbstract PDFPubReader   

A growing body of evidence suggests that hyperglycemia-induced oxidative stress plays an important role in diabetic complications, especially β-cell dysfunction and failure. Under physiological conditions, reactive oxygen species serve as second messengers that facilitate signal transduction and gene expression in pancreatic β-cells. However, under pathological conditions, an imbalance in redox homeostasis leads to aberrant tissue damage and β-cell death due to a lack of antioxidant defense systems. Taking into account the vulnerability of islets to oxidative damage, induction of endogenous antioxidant enzymes or exogenous antioxidant administration has been proposed as a way to protect β-cells against diabetic insults. Here, we consider recent insights into how the redox response becomes deregulated under diabetic conditions, as well as the therapeutic benefits of antioxidants, which may provide clues for developing strategies aimed at the treatment or prevention of diabetes associated with β-cell failure.


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Regulation of Muscle Microcirculation in Health and Diabetes
Zhenqi Liu, Seung-Hyun Ko, Weidong Chai, Wenhong Cao
Diabetes Metab J. 2012;36(2):83-89.   Published online April 17, 2012
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AbstractAbstract PDFPubReader   

Insulin increases microvascular perfusion and substrate exchange surface area in muscle, which is pivotal for hormone action and substrate exchange, by activating insulin signaling cascade in the endothelial cells to produce nitric oxide. This action of insulin is closely coupled with its metabolic action and type 2 diabetes is associated with both metabolic and microvascular insulin resistance. Muscle microvascular perfusion/volume can be assessed by 1-methylxanthine metabolism, contrast-enhanced ultrasound and positron emission tomography. In addition to insulin, several factors have been shown to recruit muscle microvasculature, including exercise or muscle contraction, mixed meals, glucagon-like peptide 1 and angiotensin II type 1 receptor (AT1R) blocker. On the other hand, factors that cause metabolic insulin resistance, such as inflammatory cytokines, free fatty acids, and selective activation of the AT1R, are capable of causing microvascular insulin resistance. Therapies targeting microvascular insulin resistance may help prevent or control diabetes and decrease the associated cardiovascular morbidity and mortality.


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Original Articles
Nitric Oxide Increases Insulin Sensitivity in Skeletal Muscle by Improving Mitochondrial Function and Insulin Signaling.
Woo Je Lee, Hyoun Sik Kim, Hye Sun Park, Mi Ok Kim, Mina Kim, Ji Young Yun, Eun Hee Kim, Sang Ah Lee, Seung Hun Lee, Eun Hee Koh, Joong Yeol Park, Ki Up Lee
Korean Diabetes J. 2009;33(3):198-205.   Published online June 1, 2009
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AbstractAbstract PDF
Accumulating evidence has suggested that nitric oxide (NO) is involved in the regulation of insulin sensitivity in skeletal muscle. Recent studies also suggested NO as an important molecule regulating mitochondrial biogenesis. This study examined the effect of the NO donor, 3-morpholinosydnonimine (SIN-1), on glucose metabolism in skeletal muscle and tested the hypothesis that NO's effect on glucose metabolism is mediated by its effect on mitochondrial function. METHODS: In Sprague-Dawley (SD) rats treated with SIN-1 for 4 weeks, insulin sensitivity was measured by a glucose clamp study. Triglyceride content and fatty acid oxidation were measured in the skeletal muscle. In addition, mitochondrial DNA content and mRNA expression of mitochondrial biogenesis markers were assessed by real-time polymerase chain reaction and expression of insulin receptor substrate (IRS)-1 and Akt were examined by Western blot analysis in skeletal muscle. In C2C12 cells, insulin sensitivity was measured by 2-deoxyglucose uptake and Western blot analysis was used to examine the expression of IRS-1 and Akt. RESULTS: SIN-1 improved insulin sensitivity in C2C12 cells and skeletal muscles of SD rats. In addition, SIN-1 decreased triglyceride content and increased fatty acid oxidation in skeletal muscle. Mitochondrial DNA contents and biogenesis in the skeletal muscle were increased by SIN-1 treatment. Moreover, SIN-1 increased the expression of phosphor-IRS-1 and phosphor-Akt in the skeletal muscle and muscle cells. CONCLUSION: Our results suggest that NO mediates glucose uptake in skeletal muscle both in vitro and in vivo by improving mitochondrial function and stimulating insulin signaling pathways.


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  • NO-Rich Diet for Lifestyle-Related Diseases
    Jun Kobayashi, Kazuo Ohtake, Hiroyuki Uchida
    Nutrients.2015; 7(6): 4911.     CrossRef
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    Jiangyong Ouyang, Rahulkumar A. Parakhia, Raymond S. Ochs
    Journal of Biological Chemistry.2011; 286(1): 1.     CrossRef
Inducible Nitric Oxide Synthase (iNOS) Expression in the Hypoxic Injury to Pancreatic Beta (MIN6) Cells.
Seung Hyun Ko, Seung Bum Kim, Kyung Ryul Ryu, Ji Won Kim, Yu Bai Ahn, Sung Dae Moon, Sung Rae Kim, Jung Min Lee, Hyuk Snag Kwon, Kun Ho Yoon, Ki Ho Song
Korean Diabetes J. 2006;30(5):336-346.   Published online September 1, 2006
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AbstractAbstract PDF
Islet transplantation is an alternative potential strategy to cure type 1 diabetes mellitus. However, two or more donors are usually needed for one recipient because a substantial part of the graft becomes nonfunctional due to several factors including hypoxia. Though hypoxic exposure of pancreatic beta cells has been reported to induce apoptotic cell death, the molecular processes involved in hypoxia-induced cell death are poorly understood. In type I diabetes, Nitric Oxide (NO) is known as an important cytokine, involved in the pathogenesis of beta cell dysfunction. Pancreatic beta cells are sensitive to the induction of inducible nitric oxide synthase (iNOS) when stimulated by TNF-a or IL-1beta. But contribution of iNOS in response to hypoxia is not yet fully understood. METHODS: Mouse insulinoma cells (MIN6) were incubated in an anaerobic chamber (75% N2/15% CO2/5% H2) for up to 12 hours. Cell viability was measured after AO/PI staining. Caspase-3 activation was also determined using Western blot analysis. Nitric Oxide (NO) release into culture medium was measured using a Griess reagent. The expression of iNOS and PDX-1 mRNA and iNOS protein was examined using real time PCR and Western blot analysis. RESULTS: Marked cell death was observed within 6 hours after hypoxic exposure of MIN6 cells (control, < 5%; 2 hr, 11.0+/-7.6%; 6 hr, 46.2+/-12.8%, P < 0.05). Immunoreactivity to activated caspase-3 was observed at 2, 4 and 6 hrs. NO production was increased in a time dependent manner. Expression of iNOS mRNA and protein was significantly increased at 4 and 6 hour after hypoxia. iNOS expression was confirmed by immunostaining. Of note, Pdx-1 mRNA expression was markedly attenuated by hypoxic treatment. Pretreatment with a selective iNOS inhibitor, 1400 W, significantly prevented beta cell death induced by hypoxic injury. CONCLUSION: Our data suggest that iNOS-NO play an important role in hypoxic injury to MIN6 cells. Therefore, iNOS-NO might be a potential therapeutic target for improving engraftment of the transplanted islets and suppression of iNOS would be helpful for prevention of beta cells damage to hypoxic injury.
The Effect of Nitric Oxide on Insulin Binding and Insulin Receptor Recycling in Bovine Aortic Endothelial Cells.
Hyuk Sang Kwon, Oak Kee Hong, Hee Soo Kim, Jung Min Lee, Sung Rae Kim, Sung Dae Moon, Sang Ah Jang, Hyun Shik Son, Kun Ho Yoon, Moo Il Kang, Bong Yun Cha, Kwang Woo Lee, Ho Young Son, Sung Koo Kang
Korean Diabetes J. 2003;27(3):213-227.   Published online June 1, 2003
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AbstractAbstract PDF
The coexistence of insulin resistance and endothelial dysfunction is commonly observed in a variety of metabolic and cardiovascular disorders, including athero-sclerosis and type 2 diabetes mellitus. Because nitric oxide (NO), or nitric oxide synthase (NOS), has been suggested as a significant contributing factor in the development of endothelial dysfunction and insulin resistance, reactive NO or NOS were investigated to see if they contribute to the insulin internalization pathway. METHODS: The production of NO (Nitrite), the expression of eNOS (endothelial NOS), insulin binding and the insulin receptor internalization and recycling, following 48 hours of incubation with bradykinin (BK), acetylcholine (Ach), NG-monomethyl- L-arginine (L-NMMA) and N-nitro-L-arginine methylester (L-NAME) in Bovine aortic endothelial cells (BAECs), were examined. RESULTS: The results were as follows: 1. In relation to the time course, the production of eNOS was increased, but was decreased after 8 hours of incubation. The production of eNOS in the L-NMMA and L-NAME treated groups was significantly decreased compared with that of the controls (p<0.05). 2. The specific insulin bindings to the receptors of the endothelial cells were maximized within 20 mins, and then decreased. At 20 mins, the binding rate of the L-NMMA treated group was significantly decreased compared to that of the controls. At a concentration of 0.4ng/ml of unlabelled insulin, the specific insulin binding of the L-NMMA treated group was significantly decreased compared to that of the controls (p<0.05). 3. The internalization of 125I-insulin into the endothelial cells, as assessed by the acid washing dissociation method, occurred rapidly. The internalized radioactivity of 125I-insulin, at 20 mins, was significantly increased in the BK and Ach groups compared with the controls (p<0.05). 4. The recycling of the internalized insulin receptors showed no significant differences between the study groups, but the recycling was slightly delayed compared with controls in the Ach group. CONCLUSION: In conclusion, the NO generating substances, BK and Ach, and the inhibitory substance, L-NMMA, may influence the binding and internalization of insulin-insulin receptors. Our results suggest that NO might contribute to the transcytosis of insulin in BAECs
Effect and Mechanism of Vascular Endothelial Growth Factor on Endothelial Nitric Oxide Synthase Expression in Aortic Endothelial Cells.
Soon Hee Lee, Jung Guk Kim, Joong Yeol Park, Sung Woo Ha, Bo Wan Kim
Korean Diabetes J. 2002;26(5):396-404.   Published online October 1, 2002
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Vascular endothelial growth factor (VEGF), a soluble angiogenic factor produced by many tumor and normal cells, is a potent angiogenic and vascular permeability factor. VEGF plays a key role in both pathological and physiological angiogenesis. There are many recent findings regarding the role of VEGF in diabetic microvascular and macrovascular diseases. Many approaches with VEGF-related therapies begin to treat and prevent these complications and have been used for the treatment of microvascular complications such as diabetic retinopathy, whereas VEGF agonists have been used to treat macrovascular complications such as myocardial infarction and peripheral limb ischemia. Nitric oxide (NO) is known to mediate many physiological and pathological functions, including modulation of vascular tone, permeability, and capillary growth. Recent reports indicate that NO may play an intimate role in VEGF signaling. Therefore, we hypothesized that the expression of eNOS may be regulated by VEGF. The objectives of the present study were to determine whether VEGF up-regulates the expression of endothelial NO synthase (eNOS) in endothelial cells and to elucidate the mechanism that mediate this response. METHODS: Endothelial cells were isolated from bovine aortae. The expression of eNOS was assessed by Northern blotting analysis. To evaluate the mechanism of VEGF-induced eNOS expression, endothelial cells were conditioned with VEGF and pretreated with phorbol-12-myristate acetate (PMA), a protein kinase C (PKC) activator, or GF109203X (GFX), a PKC inhibitor. The changes of eNOS gene expression. RESULTS: VEGF significantly increased the expression of eNOS mRNA in bovine aortic endothelial cells (BAEC) in time and dose dependent manners. PMA increased the expression of eNOS mRNA, as well as the VEGF-induced expression of eNOS mRNA in endothelial cells, while inhibition of the PKC activity, with the GFX blocked the upregulation of the VEGF-induced eNOS mRNA. CONCLUSION: The results suggest that VEGF upregulates eNOS gene expression in aortic endothelial cells, by a PKC dependent pathway and, eNOS may be important in the development of VEGF-induced angiopathy.
The Effect of Acute Hyperglycemia on Endothelial Function in Type 2 Diabetes.
Sang Jun Lee, Dong Wook Lee, In Kyu Lee
Korean Diabetes J. 2000;24(5):574-586.   Published online January 1, 2001
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Multiple studies in patients with diabetes demonstrate impaired endothelial-dependent vasodilation. But the mechanisms of vascular dysfunction in type 2 diabetes are still controversial. Some risk factors, such as dyslipidemia, hypertension and obesity, are commonly associated with type 2 diabetes. These risk factor may cause endothelial dysfunction. And hyperglycemia may have a specific role in the increased risk of vascular complications in diabetes but it remains unclear. The purpose of this study was to examine whether endothelial dysfunction occurs when acute hyperglycemia is induced by oral glucose loading. METHOD: Using the high-resolution ultrasound, we measured flow-mediated vasodilation (endothelial dependent vasodilation: FMD) during oral glucose tolerance test in 11 men (mean age: 59+/-5 years) with type 2 diabetes without chronic diabetic complications. For statistical analysis, we used paired t-test, generalized linear method (GLM) to compare FMD before and after glucose loading. RESULT: Flow-mediated vasodilation was diminished after glucose loading (13.2+/- 6.4%, 7.3+/-3.3*%, 12.8+/-5.6%, in fasting, at 1- and 2-h, respectively; *p<0.001 vs fasting). Superoxide anion formation by neutrophils was increased after glucose loading (4.65+/-2.8, 6.17+/-2.2, in fasting, at 1-h respectively: p<0.05 vs fasting)( 10-7nmol/106cells/30min). Endothelial independent vasodilation was not significantly affected by glucose loading. The concentration of triglyceride were not changed after glucose loading. CONCLUSION: This study shows that acute hyperglycemia induced by 75 gm oral glucose intake results in endothelial dysfunction. These results suggest that prolonged and repeated hyperglycemia may play an important role in the developement and progression of vascular complication in diabetes.
An Effect of Estrogen Supplementation on the Endothelium Dependent Vasodilation in Postmenopausal Women with Type 2 Diabetes Mellitus.
Jun Kim Yeo, Sang Jun Lee, In Kyu Lee
Korean Diabetes J. 2000;24(1):37-45.   Published online January 1, 2001
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Although estrogen supplementation can reduce cardiovascular events in postmenopausal women, but the mechanism that mediate this beneficial effect is unclear. Thus, we investigated the acute effect of HRT on endothelial dependent vasodilation using high resolution ultrasound in healthy and diabetic postmenopausal women. METHOD: We examined endogenous (flow dependent dilatation affer 5min cuff occlusion) and exogenous (sublingual nitroglycerin) nitric oxide mediated vasodilation in the brachial artery before and after estrogen supplementation (Premarin R 0.625 mg for 1 wk) in 16 postmenopausal women, and in 18 age-matched postmenopausal women with type 2 diabetes mellitus. RESULTS: There were no differences in age, total & LDL cholesterol level, and body mass index between the groups (p>0.05). However, HDL cholesterol level was significantly lower in patient with diabetes than in normal women (1.0+/-0.3 mmol/L in diabetes and 1.4+/-0.2 mmol/L in normal, p<0.05). Basal endothelium dependent vascular reactivity was significantly attenuated in patient with diabetes when compaired with normal subjects (8.0+/-3,9% versus 13.7+/-6.2%, p<0.05). An estrogen supplementation increased endothelium dependent vasodilation not only in patient with diabetes(from 8.0+/-3.9% to 15.1+/-4.0%, p<0.05), but also in normal women (from 13.7+/-6.2% to 20.1+/-4.7%, p<0.05). Moreover the percent increase of vascular reactivity was higher in patient with diabetes(p<0,05), In contrast, the responses to sublingual nitroglycerin were comparable in diabetes (from 21.1+/-6.0% to 22.1+/-4.1%, p>0.05), and in normal women (from 25.8+/-7.8% to 25.2+/-4.5%, p>0.05) before and after estrogen supplementation. CONCLUSION: Endothelial dysfunction was prominent in patient with diabetes and it was significantly attenuated by estrogen. These results suggest that estrogen replacement improves endothelial dependent vasodilation in healthy and diabetic postmenopausal women.
Role of Nitric Oxide on the Insulin Secretion of Rat Pancreas.
Moon Suk Nam, Sung Ki Kim, Seong Bin Hong, Yeo Joo Kim, Mi Rim Kim, Yong Seong Kim, Young Duk Song, Hyun Chul Lee, Kap Bum Huh
Korean Diabetes J. 1999;23(6):748-756.   Published online January 1, 2001
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Diabetes mellitus could occur when insulin secretion of pancreas is inadequate in response to blood glucose. The mechanisms on failure of pancreatic beta cell are still not known. Several recent experiments have reported that nitric oxide (NO) may be considered as a modulator of insulin secretion and impairment associated with the beta cell. The present study was purposed to investigate the role of nitric oxide on the secretion of insulin of rat pancreas in vivo and in vitro. METHODS: The plasma insulin and glucose were measured after intravenous injection of nitric oxide synthase (NOS) inhibitor (NG-nitro-L-arginine methyl. ester, L-NAME) in male rat. Insulin release was determmed during stimulation of NOS inhibitor and nitric oxide donor (hydroxylamine) in the isolated pancreatic islets. RESULT: 1. The insulin secretory response with L-arginine stimulation after injection of NOS inhibitor (L-NAME) in rat was increased resulting in mild hypoglycemia which recovered promptly. This showed that NO were related with L-arginine induced insulin secretion. 2. After isolation of pancreatic islet, 11,0 mM glucose induced insulin release was increased in culture media and L-arginine (1.0 mM) induced insulin release was also increased compared with control (6.72+/-0.66 vs. 3.48+/-0.42 prnol/islet/hour, p<0.05). 3. L-arginine induced insulin release was increased with L-NAME in the isolated rat pancreatic islets (12.5+/-1.38 vs, 7.23+/-0.93 ng/islet/ hour, p<0.05). 4. Glucose induced insulin release was progressively inhibited by NO donor hydroxylamine in the isolated rat pancreas islet (6.72+/-0.75 vs. 2.46+/-0.60 pmol/islet/hour p<0.05). CONCLUSION: These results strongly suggest that nitric oxide is a negative modulator of insulin release in normal rats induced by the nutrient secretagogues L-arginine and glucose in vivo and in vitro. Further investigation on the mechanism of nitric oxide in insulin secretory pathway will be necessary.
Effect of high glucose on function of cultured rabbit vascular endothelial cells.
Seok Man Son, In Ju Kim, Yong Ki Kim, Chi Dae Kim, Ki Whan Hong
Korean Diabetes J. 1997;21(2):156-167.   Published online January 1, 2001
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Vascular disease accounts for the majority of the clinical complications of diabetes mellitus. Changes in local control of vascular tone such as imbalanced production of relaxing and contracting factors by endothelium may be related to the initiation and maintenance of abnormal vascular reactivity characteristically seen in diabetic vascular complications. Cytokines and growth factors released from injured endothelial cells, T-cells, and macro-phages enhance atherogenesis. In this study, we examined NO and TNF-a released from cultured rabbit aortic endothelial cells(RAECs) under different glucose concentration to investigate the relationship between high glucose and endothelial cell dysfunction. METHODS: The thoracic and abdominal aortae of rabbit(23kg) were isolated and periadventitial connective tissue was carefully removed. Rabbit aortic endothelial cells in primary culture were prepared by the m.ethod of Schwartz with modification. RAECs were grown to confluence in 25 cm2 flask in DMEM supplemented with 20% FBS, 150pg/mL endothelial cell growth supplernent, 90pg/mL heparin, 100 U/mL penicillin and 100pg/mL streptomycin at 37'C in humidified 5% carbon dioxide in air. For experiments, confluent cells were replaced in 1 1 mm, 48 well plate containing same medium composition. Cells were then incubated in the presence or absence of FBS for various times up to 48 hours(time course) to eveluate the NO and TNF-a response to different glucose concentrations(0, 5.5, 11, 22, and 44 mmol/ L). Cells were also incubated with various concentration of ACH and ADP(10, 10', 10 and 10' mol/L) and 10' mol/L of ACH or ADP with different glucose concentrations for 24 hours to evaluate stimulated effect of ACH and ADP on NO release. RESULTS: 1) Total NO release from RAECs was significantly in a time-dependent. After 48 hours incubation, the total secretion of NO was significantly higher in culture medium with FRS than without FBS. 2) Glucose concentration resembling severe hyper-glycemic conditions(22 and 44 mmol/L) significantly inhibited NO release from RAECs, 3) Acetylcholine and ADP induced a clear dose-dependent NO release in RAECs. 4) Stimulation of acetylcholine and ADP on NO release according to different glucose concentration was not significantly higher than NO release in culture medium with glucose alone. 5) The increment in TNF-a levels was associated with a significant increase at higher glucose concentration, 6) There was a negative correlation between NO and TNF-a release in culture medium with FBS but not in culture medium without FBS. CONCLUSION: Our data show that decreased NO release and increased TNF-a release from RAECs were noted under high glucose concentration. Such interaction could play a significant role in the development of diabetic vascular complication in hyperglycernic conditions.

Diabetes Metab J : Diabetes & Metabolism Journal
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