Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014, Article ID 379537, 12 pages
http://dx.doi.org/10.1155/2014/379537
Research Article

MicroRNA-146a Decreases High Glucose/Thrombin-Induced Endothelial Inflammation by Inhibiting NAPDH Oxidase 4 Expression

1School of Medicine, China Medical University, No. 91, Hsueh-Shih Road, Taichung 40402, Taiwan
2Division of Cardiology, Department of Medicine, China Medical University Hospital, No. 2, Yuh-Der Road, Taichung 40447, Taiwan
3Department of Biotechnology, College of Medical and Health Science, Asia University, No. 500, Lioufeng Road, Wufeng, Taichung 41354, Taiwan
4Graduate Institute of Basic Medical Science, China Medical University, No. 91, Hsueh-Shih Road, Taichung 40402, Taiwan
5Department of Life Science, National Chung Hsing University, No. 250, Kuo-Kuang Road, Taichung 40227, Taiwan
6Graduate Integration of Chinese and Western Medicine, China Medical University, No. 91, Hsueh-Shih Road, Taichung 40402, Taiwan
7Department of Pediatrics, Children’s Hospital, China Medical University Hospital, No. 2, Yuh-Der Road, Taichung 40447, Taiwan
8Department of Biotechnology, Asia University, No. 500, Lioufeng Road, Wufeng, Taichung 41354, Taiwan

Received 23 May 2014; Revised 10 August 2014; Accepted 10 August 2014; Published 14 September 2014

Academic Editor: Yung-Hsiang Chen

Copyright © 2014 Huang-Joe Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Puri, Y. Kataoka, K. Uno, and S. J. Nicholls, “The distinctive nature of atherosclerotic vascular disease in diabetes: pathophysiological and morphological insights,” Current Diabetes Reports, vol. 12, no. 3, pp. 280–285, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. C. M. Sena, A. M. Pereira, and R. Seica, “Endothelial dysfunction—a major mediator of diabetic vascular disease,” Biochim Biophys Acta, vol. 1832, no. 12, pp. 2216–2231, 2013. View at Google Scholar
  3. F. Paneni, J. A. Beckman, M. A. Creager, and F. Cosentino, “Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I,” European Heart Journal, vol. 34, no. 31, pp. 2436–2443, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. K. Bedard and K.-H. Krause, “The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology,” Physiological Reviews, vol. 87, no. 1, pp. 245–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Marin, B. Gongol, Z. Chen et al., “Mechanosensitive microRNAs-role in endothelial responses to shear stress and redox state,” Free Radical Biology and Medicine, vol. 64, pp. 61–68, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. K. D. Taganov, M. P. Boldin, K.-J. Chang, and D. Baltimore, “NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 33, pp. 12481–12486, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Hou, P. Wang, L. Lin et al., “MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2,” Journal of Immunology, vol. 183, no. 3, pp. 2150–2158, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. N. Li, X. Xu, B. Xiao et al., “H. pylori related proinflammatory cytokines contribute to the induction of miR-146a in human gastric epithelial cells,” Molecular Biology Reports, vol. 39, no. 4, pp. 4655–4661, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. T. Chen, Z. Li, W. Zhu et al., “MicroRNA-146a regulates the maturation process and pro-inflammatory cytokine secretion by targeting CD40L in oxLDL-stimulated dendritic cells,” FEBS Letters, vol. 585, no. 3, pp. 567–573, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. H. S. Cheng, N. Sivachandran, A. Lau et al., “MicroRNA-146 represses endothelial activation by inhibiting pro-inflammatory pathways,” EMBO Molecular Medicine, vol. 5, no. 7, pp. 949–966, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. C.-H. Hsieh, C.-S. Rau, S.-F. Jeng et al., “Identification of the potential target genes of microRNA-146a induced by PMA treatment in human microvascular endothelial cells,” Experimental Cell Research, vol. 316, no. 7, pp. 1119–1126, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Feng, S. Chen, K. McArthur et al., “miR-146a-mediated extracellular matrix protein production in chronic diabetes complications,” Diabetes, vol. 60, no. 11, pp. 2975–2984, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. D. S. Karolina, A. Armugam, S. Tavintharan et al., “MicroRNA 144 impairs insulin signaling by inhibiting the expression of insulin receptor substrate 1 in type 2 diabetes mellitus,” PLoS ONE, vol. 6, no. 8, Article ID e22839, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Xu, W. Wu, L. Zhang et al., “The role of MicroRNA-146a in the pathogenesis of the diabetic wound-healing impairment: correction with mesenchymal stem cell treatment,” Diabetes, vol. 61, no. 11, pp. 2906–2912, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. H.-J. Wang, W.-Y. Lo, and L.-J. Lin, “Angiotensin-(1–7) decreases glycated albumin-induced endothelial interleukin-6 expression via modulation of miR-146a,” Biochemical and Biophysical Research Communications, vol. 430, no. 3, pp. 1157–1163, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Balasubramanyam, S. Aravind, K. Gokulakrishnan et al., “Impaired miR-146a expression links subclinical inflammation and insulin resistance in Type 2 diabetes,” Molecular and Cellular Biochemistry, vol. 351, no. 1-2, pp. 197–205, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Boden, V. R. Vaidyula, C. Homko, P. Cheung, and A. K. Rao, “Circulating tissue factor procoagulant activity and thrombin generation in patients with type 2 diabetes: effects of insulin and glucose,” Journal of Clinical Endocrinology and Metabolism, vol. 92, no. 11, pp. 4352–4358, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Ay, F. Hoellerl, C. Ay et al., “Thrombin generation in type 2 diabetes with albuminuria and macrovascular disease,” European Journal of Clinical Investigation, vol. 42, no. 5, pp. 470–477, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Inoguchi, T. Sonta, H. Tsubouchi et al., “Protein kinase C-dependent increase in reactive oxygen species (ROS) production in vascular tissues of diabetes: role of vascular NAD(P)H oxidase,” Journal of the American Society of Nephrology, vol. 14, no. 8, supplement 3, pp. S227–S232, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. J. A. Holland, J. W. Meyer, M.-M. Chang, R. W. O'Donnell, D. K. Johnson, and L. M. Ziegler, “Thrombin stimulated reactive oxygen species production in cultured human endothelial cells,” Endothelium, vol. 6, no. 2, pp. 113–121, 1998. View at Google Scholar · View at Scopus
  21. H.-J. Wang, W.-Y. Lo, T.-L. Lu, and H. Huang, “(-)-Epigallocatechin-3-gallate decreases thrombin/paclitaxel-induced endothelial tissue factor expression via the inhibition of c-Jun terminal NH2 kinase phosphorylation,” Biochemical and Biophysical Research Communications, vol. 391, no. 1, pp. 716–721, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. P. N. Hopkins, “Molecular biology of atherosclerosis,” Physiological Reviews, vol. 93, no. 3, pp. 1317–1542, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. J. D. van Buul, M. Fernandez-Borja, E. C. Anthony, and P. L. Hordijk, “Expression and localization of NOX2 and NOX4 in primary human endothelial cells,” Antioxidants and Redox Signaling, vol. 7, no. 3-4, pp. 308–317, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Ago, T. Kitazono, H. Ooboshi et al., “Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase,” Circulation, vol. 109, no. 2, pp. 227–233, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Hwang, M. H. Ing, A. Salazar et al., “Pulsatile versus oscillatory shear stress regulates NADPH oxidase subunit expression: implication for native LDL oxidation,” Circulation Research, vol. 93, no. 12, pp. 1225–1232, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. L. S. Yoshida and S. Tsunawaki, “Expression of NADPH oxidases and enhanced H2O2-generating activity in human coronary artery endothelial cells upon induction with tumor necrosis factor-α,” International Immunopharmacology, vol. 8, no. 10, pp. 1377–1385, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. H. S. Park, J. N. Chun, H. Y. Jung, C. Choi, and Y. S. Bae, “Role of NADPH oxidase 4 in lipopolysaccharide-induced proinflammatory responses by human aortic endothelial cells,” Cardiovascular Research, vol. 72, no. 3, pp. 447–455, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Lee, N. M. Gharavi, H. Honda et al., “A role for NADPH oxidase 4 in the activation of vascular endothelial cells by oxidized phospholipids,” Free Radical Biology and Medicine, vol. 47, no. 2, pp. 145–151, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. B. K. Rodiño-Janeiro, M. González-Peteiro, R. Ucieda-Somoza, J. R. González-Juanatey, and E. Álvarez, “Glycated albumin, a precursor of advanced glycation end-products, up-regulates NADPH oxidase and enhances oxidative stress in human endothelial cells: molecular correlate of diabetic vasculopathy,” Diabetes/Metabolism Research and Reviews, vol. 26, no. 7, pp. 550–558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Vasa-Nicotera, H. Chen, P. Tucci et al., “MiR-146a is modulated in human endothelial cell with aging,” Atherosclerosis, vol. 217, no. 2, pp. 326–330, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. S. Basuroy, S. Bhattacharya, C. W. Leffler, and H. Parfenova, “Nox4 NADPH oxidase mediates oxidative stress and apoptosis caused by TNF-α in cerebral vascular endothelial cells,” The American Journal of Physiology—Cell Physiology, vol. 296, no. 3, pp. C422–C432, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. F. Chen, S. Haigh, S. Barman, and D. J. R. Fulton, “From form to function: the role of Nox4 in the cardiovascular system,” Frontiers in Physiology, vol. 3, p. 412, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Sedeek, G. Callera, A. Montezano et al., “Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy,” American Journal of Physiology—Renal Physiology, vol. 299, no. 6, pp. F1348–F1358, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Li, J. J. Wang, Q. Yu, K. Chen, K. Mahadev, and S. X. Zhang, “Inhibition of reactive oxygen species by lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4,” Diabetes, vol. 59, no. 6, pp. 1528–1538, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Valeri, F. Boess, A. Wolf, C. Göldlin, and U. A. Boelsterli, “Fructose and tagatose protect against oxidative cell injury by iron chelation,” Free Radical Biology and Medicine, vol. 22, no. 1-2, pp. 257–268, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. J. C. Paterna, F. Boess, A. Stäubli, and U. A. Boelsterli, “Antioxidant and cytoprotective properties of D-tagatose in cultured murine hepatocytes,” Toxicology and Applied Pharmacology, vol. 148, no. 1, pp. 117–125, 1998. View at Publisher · View at Google Scholar · View at Scopus
  37. A. C. Montezano, D. Burger, G. S. Ceravolo, H. Yusuf, M. Montero, and R. M. Touyz, “Novel nox homologues in the vasculature: focusing on Nox4 and Nox5,” Clinical Science, vol. 120, no. 4, pp. 131–141, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Serrander, L. Cartier, K. Bedard et al., “NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation,” Biochemical Journal, vol. 406, no. 1, pp. 105–114, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. K. K. Griendling, D. Sorescu, B. Lassègue, and M. Ushio-Fukai, “Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 10, pp. 2175–2183, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. C. R. Williams, X. Lu, R. L. Sutliff, and C. Michael Hart, “Rosiglitazone attenuates NF-κB-mediated Nox4 upregulation in hyperglycemia-activated endothelial cells,” American Journal of Physiology - Cell Physiology, vol. 303, no. 2, pp. C213–C223, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. C. F. Lee, S. Ullevig, H. S. Kim, and R. Asmis, “Regulation of monocyte adhesion and migration by Nox4,” PLoS ONE, vol. 8, no. 6, Article ID e66964, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. B. Lassègue, A. San Martín, and K. K. Griendling, “Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system,” Circulation Research, vol. 110, no. 10, pp. 1364–1390, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Fu, Y. Zhang, Z. Wang et al., “Regulation of NADPH oxidase activity is associated with miRNA-25-mediated NOX4 expression in experimental diabetic nephropathy,” The American Journal of Nephrology, vol. 32, no. 6, pp. 581–589, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. Z. V. Varga, K. Kupai, G. Szucs et al., “MicroRNA-25-dependent up-regulation of NADPH oxidase 4 (NOX4) mediates hypercholesterolemia-induced oxidative/nitrative stress and subsequent dysfunction in the heart,” Journal of Molecular and Cellular Cardiology, vol. 62, pp. 111–121, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Bhaumik, G. K. Scott, S. Schokrpur et al., “MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8.,” Aging, vol. 1, no. 4, pp. 402–411, 2009. View at Google Scholar · View at Scopus
  46. G. Li, C. Luna, J. Qiu, D. L. Epstein, and P. Gonzalez, “Modulation of inflammatory markers by miR-146a during replicative senescence in trabecular meshwork cells,” Investigative Ophthalmology and Visual Science, vol. 51, no. 6, pp. 2976–2985, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Schuett, M. Luchtefeld, C. Grothusen, K. Grote, and B. Schieffer, “How much is too much? Interleukin-6 and its signalling in atherosclerosis,” Thrombosis and Haemostasis, vol. 102, no. 2, pp. 215–222, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. M. T. Schram, N. Chaturvedi, C. G. Schalkwijk, J. H. Fuller, and C. D. A. Stehouwer, “Markers of inflammation are cross-sectionally associated with microvascular complications and cardiovascular disease in type 1 diabetes—the EURODIAB Prospective Complications Study,” Diabetologia, vol. 48, no. 2, pp. 370–378, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. D. J. Waugh and C. Wilson, “The interleukin-8 pathway in cancer,” Clinical Cancer Research, vol. 14, no. 21, pp. 6735–6741, 2008. View at Publisher · View at Google Scholar · View at Scopus
  50. J. C. Sluimer and M. J. Daemen, “Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis,” Journal of Pathology, vol. 218, no. 1, pp. 7–29, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Inoue, H. Komoda, M. Nonaka, M. Kameda, T. Uchida, and K. Node, “Interleukin-8 as an independent predictor of long-term clinical outcome in patients with coronary artery disease,” International Journal of Cardiology, vol. 124, no. 3, pp. 319–325, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. X. D. Wu, K. Zeng, W. L. Liu et al., “Effect of aerobic exercise on miRNA-TLR4 signaling in atherosclerosis,” International Journal of Sports Medicine, vol. 35, no. 4, pp. 344–350, 2014. View at Google Scholar