Hyperuricemia Causes Pancreatic β-Cell Death and Dysfunction through NF-κB Signaling Pathway

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Jia, Lu ^a   Xing, Jing ^a   Ding, Ying ^a   Shen, Yachen ^a   Shi, Xuhui ^a   Ren, Wei ^c,d,e   Wan, Meng ^f   Guo, Jianjin ^c,d,e   Zheng, Shujing ^a   Liu, Yun ^a   Liang, Xiubin ^a   Su, Dongming ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b THE SECOND AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^d Shanghai Diabetes Institute   (China)

^e Shanghai Clinical Center of Diabetes   (China)

^f NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

3 (4 METHYLPHENYLSULFONYL) 2 PROPENENITRILE; BENZBROMARONE; GLUCOSE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; N(G) METHYLARGININE; NITRIC OXIDE; PROTEIN BCL 2; SODIUM CHLORIDE; TRANSCRIPTION FACTOR MAFA; URIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG MECHANISM; HYPERURICEMIA; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN SENSITIVITY; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PANCREAS ISLET DISEASE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL DEATH; CELL SURVIVAL; DRUG EFFECTS; METABOLISM; PANCREAS ISLET;

ANIMALS; APOPTOSIS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; GLUCOSE; HYPERURICEMIA; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED BALB C; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; URIC ACID;

EID: 84886386741     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078284     Document Type: Article

References (46)

1. Conen D, Wietlisbach V, Bovet P, Shamlaye C, Riesen W, et al. (2004) Prevalence of hyperuricemia and relation of serum uric acid with cardiovascular risk factors in a developing country. BMC Public Health 4: 9.
2. Zhu Y, Pandya BJ, Choi HK, (2011) Prevalence of gout and hyperuricemia in the US general population: the National Health and Nutrition Examination Survey 2007-2008. Arthritis Rheum 63: 3136-3141.
3. So A, Thorens B, (2010) Uric acid transport and disease. J Clin Invest 120: 1791-1799.
4. Kodama S, Saito K, Yachi Y, Asumi M, Sugawara A, et al. (2009) Association between serum uric acid and development of type 2 diabetes. Diabetes Care 32: 1737-1742.
5. Dehghan A, van Hoek M, Sijbrands EJ, Hofman A, Witteman JC, (2008) High serum uric acid as a novel risk factor for type 2 diabetes. Diabetes Care 31: 361-362.
6. Krishnan E, Pandya BJ, Chung L, Hariri A, Dabbous O, (2012) Hyperuricemia in young adults and risk of insulin resistance, prediabetes, and diabetes: a 15-year follow-up study. Am J Epidemiol 176: 108-116.
7. Corbett JA, Mikhael A, Shimizu J, Frederick K, Misko TP, et al. (1993) Nitric oxide production in islets from nonobese diabetic mice: aminoguanidine-sensitive and-resistant stages in the immunological diabetic process. Proc Natl Acad Sci U S A 90: 8992-8995.
8. Corbett JA, McDaniel ML, (1995) Intraislet release of interleukin 1 inhibits beta cell function by inducing beta cell expression of inducible nitric oxide synthase. J Exp Med 181: 559-568.
9. Thomas HE, Darwiche R, Corbett JA, Kay TW, (2002) Interleukin-1 plus gamma-interferon-induced pancreatic beta-cell dysfunction is mediated by beta-cell nitric oxide production. Diabetes 51: 311-316.
10. Karin M, Lin A, (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227.
11. Salehi A, Meidute Abaraviciene S, Jimenez-Feltstrom J, Ostenson CG, Efendic S, et al. (2008) Excessive islet NO generation in type 2 diabetic GK rats coincides with abnormal hormone secretion and is counteracted by GLP-1. PLoS One 3: e2165.
12. Maier B, Ogihara T, Trace AP, Tersey SA, Robbins RD, et al. (2010) The unique hypusine modification of eIF5A promotes islet beta cell inflammation and dysfunction in mice. J Clin Invest 120: 2156-2170.
13. Kataoka K, Han SI, Shioda S, Hirai M, Nishizawa M, et al. (2002) MafA is a glucose-regulated and pancreatic beta-cell-specific transcriptional activator for the insulin gene. J Biol Chem 277: 49903-49910.
14. Harmon JS, Stein R, Robertson RP, (2005) Oxidative stress-mediated, post-translational loss of MafA protein as a contributing mechanism to loss of insulin gene expression in glucotoxic beta cells. J Biol Chem 280: 11107-11113.
15. Sautin YY, Nakagawa T, Zharikov S, Johnson RJ, (2007) Adverse effects of the classic antioxidant uric acid in adipocytes: NADPH oxidase-mediated oxidative/nitrosative stress. Am J Physiol Cell Physiol 293: C584-596.
16. Su D, Zhang N, He J, Qu S, Slusher S, et al. (2007) Angiopoietin-1 production in islets improves islet engraftment and protects islets from cytokine-induced apoptosis. Diabetes 56: 2274-2283.
17. Hedeskov CJ, Capito K, (1975) The pentose cycle and insulin release in isolated mouse pancreatic islets during starvation. Biochem J 152: 571-576.
18. Chen F, Zhu Y, Tang X, Sun Y, Jia W, et al. (2011) Dynamic regulation of PDX-1 and FoxO1 expression by FoxA2 in dexamethasone-induced pancreatic beta-cells dysfunction. Endocrinology 152: 1779-1788.
19. Zhang HJ, Walseth TF, Robertson RP, (1989) Insulin secretion and cAMP metabolism in HIT cells. Reciprocal and serial passage-dependent relationships. Diabetes 38: 44-48.
20. Banakh I, Gonez LJ, Sutherland RM, Naselli G, Harrison LC, (2012) Adult pancreas side population cells expand after beta cell injury and are a source of insulin-secreting cells. PLoS One 7: e48977.
21. Roehrich ME, Mooser V, Lenain V, Herz J, Nimpf J, et al. (2003) Insulin-secreting beta-cell dysfunction induced by human lipoproteins. J Biol Chem 278: 18368-18375.
22. Yang Z, Xiaohua W, Lei J, Ruoyun T, Mingxia X, et al. (2010) Uric acid increases fibronectin synthesis through upregulation of lysyl oxidase expression in rat renal tubular epithelial cells. Am J Physiol Renal Physiol 299: F336-346.
23. Zhou Y, Fang L, Jiang L, Wen P, Cao H, et al. (2012) Uric acid induces renal inflammation via activating tubular NF-kappaB signaling pathway. PLoS One 7: e39738.
24. Zhao Z, Zhao C, Zhang XH, Zheng F, Cai W, et al. (2009) Advanced glycation end products inhibit glucose-stimulated insulin secretion through nitric oxide-dependent inhibition of cytochrome c oxidase and adenosine triphosphate synthesis. Endocrinology 150: 2569-2576.
25. Kanter M, Akpolat M, Aktas C, (2009) Protective effects of the volatile oil of Nigella sativa seeds on beta-cell damage in streptozotocin-induced diabetic rats: a light and electron microscopic study. J Mol Histol 40: 379-385.
26. Zhang X, Yong W, Lv J, Zhu Y, Zhang J, et al. (2009) Inhibition of forkhead box O1 protects pancreatic beta-cells against dexamethasone-induced dysfunction. Endocrinology 150: 4065-4073.
27. Han HJ, Lim MJ, Lee YJ, Lee JH, Yang IS, et al. (2007) Uric acid inhibits renal proximal tubule cell proliferation via at least two signaling pathways involving PKC, MAPK, cPLA2, and NF-kappaB. Am J Physiol Renal Physiol 292: F373-381.
28. Rabadi MM, Kuo MC, Ghaly T, Rabadi SM, Weber M, et al. (2012) Interaction between uric acid and HMGB1 translocation and release from endothelial cells. Am J Physiol Renal Physiol 302: F730-741.
29. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, et al. (2001) Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci U S A 98: 10845-10850.
30. Han X, Sun Y, Scott S, Bleich D, (2001) Tissue inhibitor of metalloproteinase-1 prevents cytokine-mediated dysfunction and cytotoxicity in pancreatic islets and beta-cells. Diabetes 50: 1047-1055.
31. Lin SD, Tsai DH, Hsu SR, (2006) Association between serum uric acid level and components of the metabolic syndrome. J Chin Med Assoc 69: 512-516.
32. Onat A, Uyarel H, Hergenc G, Karabulut A, Albayrak S, et al. (2006) Serum uric acid is a determinant of metabolic syndrome in a population-based study. Am J Hypertens 19: 1055-1062.
33. Oda E, Kawai R (2009) Serum uric acid levels improve prediction of incident type 2 diabetes in individuals with impaired fasting glucose: the Rancho Bernardo study: response to Krameret al. Diabetes Care 32: e125; author reply e126.
34. Nan H, Qiao Q, Soderberg S, Pitkaniemi J, Zimmet P, et al. (2008) Serum uric acid and incident diabetes in Mauritian Indian and Creole populations. Diabetes Res Clin Pract 80: 321-327.
35. Meisinger C, Doring A, Stockl D, Thorand B, Kowall B, et al. (2012) Uric acid is more strongly associated with impaired glucose regulation in women than in men from the general population: the KORA F4-Study. PLoS One 7: e37180.
36. Ishizaka N, Ishizaka Y, Toda E, Nagai R, Yamakado M, (2005) Association between serum uric acid, metabolic syndrome, and carotid atherosclerosis in Japanese individuals. Arterioscler Thromb Vasc Biol 25: 1038-1044.
37. Abreu E, Fonseca MJ, Santos AC, (2011) [Association between hyperuricemia and insulin resistance]. Acta Med Port 24Suppl 2: 565-574.
38. Wang T, Bi Y, Xu M, Huang Y, Xu Y, et al. (2011) Serum uric acid associates with the incidence of type 2 diabetes in a prospective cohort of middle-aged and elderly Chinese. Endocrine 40: 109-116.
39. Simental-Mendia LE, Rodriguez-Moran M, Guerrero-Romero F, (2009) Failure of beta-cell function to compensate lack of insulin action in hyperuricemic subjects. Diabetes Metab Res Rev 25: 535-541.
40. Cai K, Qi D, Hou X, Wang O, Chen J, et al. (2011) MCP-1 upregulates amylin expression in murine pancreatic beta cells through ERK/JNK-AP1 and NF-kappaB related signaling pathways independent of CCR2. PLoS One 6: e19559.
41. Melloul D, (2008) Role of NF-kappaB in beta-cell death. Biochem Soc Trans 36: 334-339.
42. Rayet B, Gelinas C, (1999) Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18: 6938-6947.
43. Kanellis J, Watanabe S, Li JH, Kang DH, Li P, et al. (2003) Uric acid stimulates monocyte chemoattractant protein-1 production in vascular smooth muscle cells via mitogen-activated protein kinase and cyclooxygenase-2. Hypertension 41: 1287-1293.
44. Matsuoka TA, Kaneto H, Miyatsuka T, Yamamoto T, Yamamoto K, et al. (2010) Regulation of MafA expression in pancreatic beta-cells in db/db mice with diabetes. Diabetes 59: 1709-1720.
45. Zhu Y, Ma A, Zhang H, Li C, (2013) PPARgamma Activation Attenuates Glycated-Serum Induced Pancreatic Beta-Cell Dysfunction through Enhancing Pdx1 and Mafa Protein Stability. PLoS One 8: e56386.
46. Baldwin W, McRae S, Marek G, Wymer D, Pannu V, et al. (2011) Hyperuricemia as a mediator of the proinflammatory endocrine imbalance in the adipose tissue in a murine model of the metabolic syndrome. Diabetes 60: 1258-1269.