Endoplasmic reticulum stress and Nrf2 repression in circulating cells of type 2 diabetic patients without the recommended glycemic goals

Free Radical Research

Volumn 49, Issue 3, 2015, Pages 244-252

  Mozzini, C ^a   Garbin, U ^a   Stranieri, C ^a   Pasini, A ^a   Solani, E ^a   Tinelli, I A ^a   Cominacini, L ^a   Fratta Pasini, A M ^a  

^a UNIVERSITY OF VERONA   (Italy)

Author keywords

Apoptosis; Hyperglycemia; NF kB; Oxidative stress; UPR

Indexed keywords

1 PALMITOYL 2 ARACHIDONOYLGLYCERO 3 PHOSPHORYLCHOLINE; CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN HOMOLOGOUS PROTEIN; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEME OXYGENASE 1; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MALONALDEHYDE; PHOSPHOLIPID; PHOSPHOTRANSFERASE; PROTEIN KINASE LIKE ER KINASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL; NFE2L2 PROTEIN, HUMAN;

ADULT; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE EXPRESSION; GLYCEMIC CONTROL; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VITRO STUDY; INFLAMMATION; LIPID PEROXIDATION; LONG TERM EXPOSURE; MALE; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; AGED; DOWN REGULATION; GENETICS; GLUCOSE BLOOD LEVEL; METABOLISM; MONONUCLEAR CELL; PATHOPHYSIOLOGY; UNFOLDED PROTEIN RESPONSE;

AGED; APOPTOSIS; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; HEME OXYGENASE-1; HUMANS; INFLAMMATION; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; UNFOLDED PROTEIN RESPONSE;

EID: 84925725109     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.997229     Document Type: Article

References (39)

1. Eizirik DL, Cardozo AK, Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr Rev 2008; 29: 42-61.
2. Papa FR. Endoplasmic reticulum stress, pancreatic β-cells degeneration, and diabetes. Cold Spring Harb Perspect Med 2012; 2: a007666.
3. Lipson KL, Fonseca SG, Ishigaki S, Nguyen LX, Foss E, Bortell R, et al. Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab 2006; 4: 245-254.
4. Elouil H, Bansellam M, Guiot Y, Vander Mierde D, Pascal SM, Schuit FC, Jonas JC. Acute nutrient regulation of unfolded protein response and integrated stress response in cultured rat pancreatic islets. Diabetologia 2007; 50: 1442-1452.
5. De la Cadena SG, Hernandez-Fonseca K, Camacho-Arroyo I, Massieu L. Glucose deprivation induces reticulum stress by the PERK pathway and caspase-7 and calpain-mediated caspase-12 activation. Apoptosis 2014; 19: 414-427.
6. Kaufman RJ. Orchestrating the unfolded protein response in health and disease. J Clin Invest 2002; 110: 1389-1398.
7. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529.
8. Styskal JL, Van Remmen H, Richardson A, Salmon AB. Oxidative stress and diabetes: what can we learn about insulin resistance from antioxidant mutant mouse models? Free Radic Biol Med 2012; 52: 46-58.
9. Rains JL, Jain SK. Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med 2011; 50: 567-575.
10. Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008; 132: 344-362.
11. Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signalling, and redox control. Antioxid Redox Signal 2006; 8: 1391-1418.
12. Cullinan SB, Diehl JA. PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. J Biol Chem 2004; 279: 20108-20117.
13. Singh S, Vrishni S, Singh BK, Rahman I, Kakkar P. Nrf2/ARE stress response mechanism: a control point in oxidative stress mediated dysfunction and chronic inflammatory disease. Free Radic Res 2010; 44: 1267-1288.
14. Mozzini C, Fratta Pasini A, Garbin U, Stranieri C, Pasini A, Vallerio P, Cominacini L. Increased endoplasmic reticulum stress and Nrf2 repression in peripheral blood mononuclear cells of patients with stable coronary artery disease. Free Radic Biol Med 2014; 68: 178-185.
15. Komura T, Sakai Y, Honda M, Takamura T, Matsushima K, Kaneko S. CD14 + monocytes are vulnerable and functionally impaired under endoplasmic reticulum stress in patients with type 2 diabetes. Diabetes 2010; 59: 634-643.
16. Fratta Pasini A, Anselmi M, Garbin U, Franchi E, Stranieri C, Nava MC, et al. Enhanced levels of oxidized low-density lipoprotein prime monocytes to cytokine overproduction via up-regulation of CD14 and toll-like receptor 4 in unstable angina. Arterioscler Thromb Vasc Biol 2007; 27: 1991-1997.
17. Garbin U, Fratta Pasini A, Stranieri C, Cominacini M, Pasini A, Manfro S, et al. Cigarette smoking blocks the protective expression of Nrf2/ARE pathway in peripheral mononuclear cells of young heavy smokers favouring inflammation. PLoS One 2009; 4: e8225.
18. Watson AD, Leitinger N, Navab M, Faull KF, Hörkkö S, Witztum JL, et al. Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem 1997; 272: 13597-13607.
19. Mao J, Zhang H, Luo J, Li L, Zhao R, Zhang R, Liu G. New method for HPLC separation and fluorescence detection of malonaldehyde in normal human plasma. J Chromatogr B Analyt Technol Biomed Life Sci 2006; 17: 832-838.
20. Cominacini L, Fratta Pasini A, Garbin U, Davoli A, Tosetti ML, Campagnola M, et al. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1in endothelial cells induces the activation of NF-kappa B through an increased production of intracellular reactive oxygen species. J Biol Chem 2000; 275: 12633-12638.
21. Robinson JP, Bruner LH, Bassoe CF, Hudson JL, Ward PA, Phan SH. Measurement of intracellular fluorescence of human monocytes relative of oxidative metabolism. J Leukoc Biol 1988; 43: 304-310
22. American Diabetes Association. Standard of medical care in Diabetes. Diabetes Care 2014, doi:10.2337/dc14-S014.
23. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ. Endoplasmic reticulum stress contributes to β cell apoptosis in type 2 diabetes. Diabetologia 2007; 50: 752-763.
24. Chang YC, Chuang LM. The role of oxidative stress in the pathogenesis of type 2 diabetes: from molecular mechanism to clinical implication. Am J Transl Res 2010; 2: 316-331.
25. Karunakaran U, Park KG. A systemic review of oxidative stress and safety of antioxidants in diabetes: focus on islets and their defense. Diabetes Metab J 2013; 37: 106-112.
26. Dierckx N, Horvath G, Van Gils C, Vertommen J, van de Vliet J, De Leeuw I, Manuel-y-Keenoy B. Oxidative stress status in patients with diabetes mellitus: relationship to diet. Eur J Clin Nutr 2003; 57: 999-1008.
27. Del Rio D, Stewart AJ, Pellegrini N. A review of recent studies on malondialdehyde as a toxic molecule and biological marker of oxidative status. Nutr Metab Cardiovasc Dis 2005; 15: 316-328.
28. Manohar SM, Vaikasuvu S, Deepthi K, Sachan A, Narasimha SR. An association of hyperglycemia with plasma malondialdehyde and atherogenic lipid risk factors in newly diagnosed Type 2 diabetic patients. J Res Med Sci 2013; 18: 89-93.
29. Rouhanizadeh M, Hwang J, Clempus RE, Marcu L, Lassègue B, Sevanian A, Hsiai TK. Oxidized-1-palmitoyl-2-arachidonoyl-sn-glycero-3-phosphorylcholine induces vascular endothelial superoxide production: implication of NADPH oxidase. Free Radic Biol Med 2005; 39: 1512-1522.
30. Tornatore L, Thatakura A, Benent J, Moretti M, Franzoso G. The nuclear factor kappa B signalling pathway: integrating metabolism and inflammation. Trends cell Biol 2012; 22: 557-566.
31. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010; 140: 900-917.
32. Kumar A, Takada Y, Boriek AM, Aggarwal BB. Nuclear Factor-kappaB: its role in health and disease. J Mol Med 2004; 82: 434-448.
33. Tam AB, Mercado EL, Hoffmann A, Niwa M. ER stress activates NF-kB by integrating functions of basal IKK activity, IRE1 and PERK. PLoS One 2012; 7: e45078.
34. Campo G, Avenoso A, Campo S, D'Ascola A, Traina P, Samà D, Calatroni A. NF-kB and caspases are involved in the hyaluronian and chondroitin-4-sulphate-exerted antioxidant effects in fibroblast cultures exposed to oxidative stress. J Appl Toxicol 2008; 28: 509-517.
35. Kim H, Vaziri N. Contribution of impair Nrf2-Keap1 pathway to oxidative stress and inflammation in chronic renal failure. Am J Physiol Renal Physiol 2010; 298: F662-F671.
36. Suzuki M, Betsuyaku T, Ito Y, Nagai K, Nasuhara Y, Kaga K, et al. Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2008; 39: 673-682.
37. Zhong Q, Mishra M, Kowluru RA. Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci 2013; 54: 3941-3948.
38. Monnier L, Mass K, Gainet C, Michel F, Villon L, Cristol JP. Activation of oxidative stress by acute glucose fluctuation compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA 2005; 295: 1681-1687.
39. Monnier L, Colette C, Mas E, Michel F, Cristol JP, Boegner C, Owens D. Regulation of oxidative stress by glycaemic control: evidence for an independent inhibitory effect of insulin therapy. Diabetologia 2010; 53: 562-571.