Oscillating glucose induces microRNA-185 and impairs an efficient antioxidant response in human endothelial cells

Cardiovascular Diabetology

Volumn 15, Issue 1, 2016, Pages

  La Sala, Lucia ^a   Cattaneo, Monica ^a   De Nigris, Valeria ^b   Pujadas, Gemma ^b   Testa, Roberto ^c   Bonfigli, Anna R ^c   Genovese, Stefano ^a   Ceriello, Antonio ^b  

^a IRCCS MULTIMEDICA   (Italy)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INRCA   (Italy)

Author keywords

Antioxidant defense; GPx 1; MiR 185; Oscillating glucose; Oxidative stress

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; BETA ACTIN; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUCOSE; GLUTATHIONE PEROXIDASE 1; HISTONE H2AX; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MICRORNA; MICRORNA 185; UNCLASSIFIED DRUG; ANTIOXIDANT; GLUTATHIONE PEROXIDASE; MIRN185 MICRORNA, HUMAN; SUPEROXIDE DISMUTASE;

3' UNTRANSLATED REGION; ACTB GENE; ARTICLE; ASSAY; BIOINFORMATICS; CAT GENE; CELL CULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE EXPRESSION; GPX 1 GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; LOSS OF FUNCTION ASSAY; LUCIFERASE ASSAY; OSCILLATION; OXIDATIVE STRESS; PROTEIN PROTEIN INTERACTION; SOD 1 GENE; SOD 2 GENE; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; DRUG EFFECTS; METABOLISM; OXIDATION REDUCTION REACTION;

ANTIOXIDANTS; CATALASE; ENDOTHELIAL CELLS; GLUCOSE; GLUTATHIONE PEROXIDASE; HUMANS; MICRORNAS; OXIDATION-REDUCTION; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

EID: 85007416057     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-016-0390-9     Document Type: Article

References (45)

1. Frontoni S, Di Bartolo P, Avogaro A, Bosi E, Paolisso G, Ceriello A. Glucose variability: an emerging target for the treatment of diabetes mellitus. Diabetes Res Clin Pract. 2013;102:86-95.
2. Ceriello A, Kilpatrick ES. Glycemic variability: both sides of the story. Diabetes Care. 2013;36(Suppl 2):S272-5.
3. Quagliaro L, Piconi L, Assaloni R, Martinelli L, Motz E, Ceriello A. Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation. Diabetes. 2003;52:2795-804.
4. Sun J, Xu Y, Sun S, Sun Y, Wang X. Intermittent high glucose enhances cell proliferation and VEGF expression in retinal endothelial cells: the role of mitochondrial reactive oxygen species. Mol Cell Biochem. 2010;343:27-35.
5. Sun J, Xu Y, Deng H, Sun S, Dai Z, Sun Y. Intermittent high glucose exacerbates the aberrant production of adiponectin and resistin through mitochondrial superoxide overproduction in adipocytes. J Mol Endocrinol. 2010;44:179-85.
6. Sun LQ, Chen YY, Wang X, Li XJ, Xue B, Qu L, et al. The protective effect of alpha lipoic acid on Schwann cells exposed to constant or intermittent high glucose. Biochem Pharmacol. 2012;84:961-73.
7. Kohnert KD, Freyse EJ, Salzsieder E. Glycaemic variability and pancreatic β-cell dysfunction. Curr Diabetes Rev. 2012;8:345-54.
8. Matés JM, Sánchez-Jiménez F. Antioxidant enzymes and their implications in pathophysiologic processes. Front Biosci. 1999;4:D339-45.
9. Rottiers V, Naar AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol. 2012;13:239-50.
10. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215-33.
11. Kato M, Castro NE, Natarajan R. MicroRNAs: potential mediators and biomarkers of diabetic complications. Free Radic Biol Med. 2013;64:85-94.
12. Kim V, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 2009;10:126-39.
13. Maciel-Dominguez A, Swan D, Ford D, Hesketh J. Selenium alters miRNA profile in an intestinal cell line: evidence that miR-185 regulates expression of GPX2 and SEPSH2. Mol Nutr Food Res. 2013;57(12):2195-205.
14. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. microRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell. 2007;27:91-105.
15. Rehmsmeier M, Steffen P, Hoechsmann M, Giegerich R. Fast and effective prediction of microRNA/target duplexes RNA. RNA. 2004;10:1507-17.
16. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell. 2003;115:787-98.
17. Doench JG, Sharp PA. Specificity of microRNA target selection in translational repression. Genes Dev. 2004;18(5):504-11.
18. Ceriello A, Russo PD, Amstad P, Cerutti P. High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes. 1996;45:471-7.
19. Zhu H, Shyh-Chang N, Segrè AV, Shinoda G, Shah SP, Einhorn WS, et al. The Lin28/let-7 axis regulates glucose metabolism. Cell. 2011;147:81-94.
20. Krutzfeldt J, Stoffel M. microRNAs: a new class of regulatory genes affecting metabolism. Cell Metab. 2006;4:9-12.
21. Puigserver P, Rodgers JT. Foxa2, a novel transcriptional regulator of insulin sensitivity. Nat Med. 2006;12:38-9.
22. Poy MN, Eliasson L, Krutzfeldt J, Kuwajima S, Ma X, Macdonald PE, et al. A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 2004;432:226-30.
23. Shantikumar S, Caporali A, Emanueli C. Role of microRNAs in diabetes and its cardiovascular complications. Cardiovasc Res. 2012;93:583-93.
24. Cheng Y, Liu X, Zhang S, Lin Y, Zhang C. microRNA-21 protects against the H(2)O(2)-induced injury on cardiac myocytes via its target gene PDCD4. J Mol Cell Cardiol. 2009;47(1):5-14.
25. Wang HJ, Huang YL, Shih YY, Wu HY, Peng CT, Lo WY. MicroRNA-146a decreases high glucose/thrombin-induced endothelial inflammation by inhibiting NADPH oxidase 4 expression. Mediators Inflamm. 2014;2014:379537.
26. Song J, Lee JE. ASK1 modulates expression of microRNA Let7A in microglia under high glucose in vitro condition. Front Cell Neurosci. 2015;9:198.
27. Wang L, Jia X, Jiang H, Du Y, Yang F, Si S, Hing B. MicroRNAs 185, 96, and 223 repress selective high-density lipoprotein cholesterol uptake through posttranscriptional inhibition. Mol Cell Biol. 2013;33-10:1956-64.
28. de la Morena MT, Eitson JL, Dozmorov IM, Belkaya S, Hoover AR, Anguiano E, Pascual MV, van Oers NS. Signature microRNA expression patterns identified in humans with 22q11.2 deletion/DiGeorge syndrome. Clin Immunol. 2013;147(1):11-22.
29. Kim JO, Song DW, Kwon EJ, Hong SE, Song HK, Min CK, Kim do H. miR-185 plays an anti-hypertrophic role in the heart via multiple targets in the calcium-signaling pathways. PLoS One. 2015;10(3):e0122509.
30. Kim JO, Song DW, Kwon EJ, Hong SE, Song HK, Min CK, Kim do H. miR-185 plays an anti-hypertrophic role in the heart via multiple targets in the calcium-signaling pathways. PLoS One. 2015;10(3):e0122509.
31. Venza I, Visalli M, Beninati C, Benfatto S, Teti D, Venza M. IL-10Ra expression is post-transcriptionally regulated by miR-15a, miR-185, and miR-211 in melanoma. BMC Med Genomics. 2015;8:81.
32. Okada K, et al. Association between blood glucose variability and coronary plaque instability in patients with acute coronary syndromes. Cardiovasc Diabetol. 2015;14:111.
33. Kuroda M, et al. Association between daily glucose fluctuation and coronary plaque properties in patients receiving adequate lipid-lowering therapy assessed by continuous glucose monitoring and optical coherence tomography. Cardiovasc Diabetol. 2015;14:78.
34. Yang YF, et al. Visit-to-visit glucose variability predicts the development of end-stage renal disease in type 2 diabetes: 10-year follow-up of Taiwan diabetes study. Medicine. 2015;94(44):e1804.
35. Jun JE, et al. The association between glycemic variability and diabetic cardiovascular autonomic neuropathy in patients with type 2 diabetes. Cardiovasc Diabetol. 2015;14:70.
36. La Sala L, et al. Oscillating glucose and constant high glucose induce endoglin expression in endothelial cells: the role of oxidative stress. Acta Diabetol. 2015;52:505-12.
37. Maiorino MI, et al. Reducing glucose variability with continuous subcutaneous insulin infusion increases endothelial progenitor cells in type 1 diabetes: an observational study. Endocrine. 2016;52(2):244-52.
38. Ceriello A, Morocutti A, Mercuri F, Quagliaro L, Moro M, Damante G, et al. Defective intracellular antioxidant enzyme production in type 1 diabetic patients with nephropathy. Diabetes. 2000;49:2170-7.
39. Hodgkinson AD, Bartlett T, Oates PJ, Millward BA, Demaine AG. The response of antioxidant genes to hyperglycemia is abnormal in patients with type 1 diabetes and diabetic nephropathy. Diabetes. 2003;52:846-51.
40. Hamanishi T, Furuta H, Kato H, Doi A, Tamai M, Shimomura H, et al. Functional variants in the glutathione peroxidase-1 (GPx-1) gene are associated with increased intima-media thickness of carotid arteries and risk of macrovascular diseases in japanese type 2 diabetic patients. Diabetes. 2004;53:2455-60.
41. Kalinina EV, Chernov NN, Novichkova MD. Role of glutathione, glutathione transferase, and glutaredoxin in regulation of redox-dependent processes. Biochemistry. 2014;79:1562-83.
42. Antunes F, Han D, Cadenas E. Relative contributions of heart mitochondria glutathione peroxidase and catalase to H(2)O(2) detoxification in in vivo conditions. Free Radic Biol Med. 2002;33:260-7.
43. Jones DP. Intracellular inhibition of catalase by alpha-methyldopa. Res Commun Chem Pathol Pharmacol. 1981;33:215-22.
44. Lei XG, Cheng WH, McClung JP. Metabolic regulation and function of glutathione peroxidase-1. Annu Rev Nut. 2007;27:41-61.
45. Forgione MA, Weiss N, Heydrick S, Cap A, Klings ES, Bierl C, et al. Cellular glutathione peroxidase deficiency and endothelial dysfunction. Am J Physiol Heart Circ Physiol. 2002;282:H1255-61