Induction of microRNA-138 by pro-inflammatory cytokines causes endothelial cell dysfunction

FEBS Letters

Volumn 588, Issue 6, 2014, Pages 906-914

  Sen, Anagha ^a   Most, Patrick ^a,b,c   Peppel, Karsten ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Angiotensin II; Cytokine; Endothelial dysfunction; Endothelial nitric oxide synthase; Endothelin 1; Tumor necrosis factor alpha

Indexed keywords

CYTOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MICRORNA; MICRORNA 138; PROTEIN S 100; PROTEIN S 100A1; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN STABILITY;

ANGIOTENSIN II; CYTOKINE; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN-1; TUMOR NECROSIS FACTOR-ALPHA;

ANGIOTENSIN II; CARDIOVASCULAR DISEASES; CELL LINE; ENDOTHELIAL CELLS; ENDOTHELIN-1; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION MEDIATORS; MAP KINASE SIGNALING SYSTEM; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASES; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; S100 PROTEINS; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84896085801     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2014.01.033     Document Type: Article

References (46)

1. D.R. Seals, K.L. Jablonski, and A.J. Donato Aging and vascular endothelial function in humans Clin. Sci. (London) 120 2011 357 375
2. R. Ross Atherosclerosis - an inflammatory disease N. Engl. J. Med. 340 1999 115 126
3. P.M. Ridker, M. Cushman, M.J. Stampfer, R.P. Tracy, and C.H. Hennekens Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men N. Engl. J. Med. 336 1997 973 979
4. P.M. Ridker, C.H. Hennekens, J.E. Buring, and N. Rifai C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women N. Engl. J. Med. 342 2000 836 843
5. R.D. Rudic, and W.C. Sessa Nitric oxide in endothelial dysfunction and vascular remodeling: clinical correlates and experimental links Am. J. Hum. Genet. 64 1999 673 677
6. T. Imanishi et al. Addition of eplerenone to an angiotensin-converting enzyme inhibitor effectively improves nitric oxide bioavailability Hypertension 51 2008 734 741
7. D. Rohde, J. Ritterhoff, M. Voelkers, H.A. Katus, T.G. Parker, and P. Most S100A1: a multifaceted therapeutic target in cardiovascular disease J. Cardiovasc. Transl. Res. 3 2010 525 537
8. C. Kraus et al. S100A1 in cardiovascular health and disease: closing the gap between basic science and clinical therapy J. Mol. Cell. Cardiol. 47 2009 445 455
9. P. Most, A. Remppis, S.T. Pleger, H.A. Katus, and W.J. Koch S100A1: a novel inotropic regulator of cardiac performance. Transition from molecular physiology to pathophysiological relevance Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 2007 R568 R577
10. S.T. Pleger et al. Endothelial S100A1 modulates vascular function via nitric oxide Circ. Res. 102 2008 786 794
11. P. Most et al. S100A1 deficiency impairs postischemic angiogenesis via compromised proangiogenic endothelial cell function and nitric oxide synthase regulation Circ. Res. 112 2013 66 78
12. E. Zelzer, Y. Levy, C. Kahana, B.Z. Shilo, M. Rubinstein, and B. Cohen Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT EMBO J. 17 1998 5085 5094
13. A. Gorlach, I. Diebold, V.B. Schini-Kerth, U. Berchner-Pfannschmidt, U. Roth, R.P. Brandes, T. Kietzmann, and R. Busse Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: role of the p22(phox)-containing NADPH oxidase Circ. Res. 89 2001 47 54
14. J.J. Haddad, and S.C. Land A non-hypoxic, ROS-sensitive pathway mediates TNF-alpha-dependent regulation of HIF-1alpha FEBS Lett. 505 2001 269 274
15. P. van Uden, N.S. Kenneth, and S. Rocha Regulation of hypoxia-inducible factor-1alpha by NF-kappaB Biochem. J. 412 2008 477 484
16. S. Bonello, C. Zahringer, R.S. BelAiba, T. Djordjevic, J. Hess, C. Michiels, T. Kietzmann, and A. Gorlach Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site Arterioscler., Thromb., Vasc. Biol. 27 2007 755 761
17. C.C. Blouin, E.L. Page, G.M. Soucy, and D.E. Richard Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1alpha Blood 103 2004 1124 1130
18. A. Sen, S. Ren, C. Lerchenmüller, J. Sun, N. Weiss, P. Most, and K. Peppel MicroRNA-138 regulates hypoxia-induced endothelial cell dysfunction by targeting S100A1 PLoS One 8 2013 e78684
19. J. Krutzfeldt, N. Rajewsky, R. Braich, K.G. Rajeev, T. Tuschl, M. Manoharan, and M. Stoffel Silencing of microRNAs in vivo with 'antagomirs' Nature 438 2005 685 689
20. H. Drexler, and B. Hornig Endothelial dysfunction in human disease J. Mol. Cell. Cardiol. 31 1999 51 60
21. S.D. Katz, K. Hryniewicz, I. Hriljac, K. Balidemaj, C. Dimayuga, A. Hudaihed, and A. Yasskiy Vascular endothelial dysfunction and mortality risk in patients with chronic heart failure Circulation 111 2005 310 314
22. R.M. Rao, L. Yang, G. Garcia-Cardena, and F.W. Luscinskas Endothelial-dependent mechanisms of leukocyte recruitment to the vascular wall Circ. Res. 101 2007 234 247
23. P. Libby Inflammation in atherosclerosis Nature 420 2002 868 874
24. U. Forstermann, and W.C. Sessa Nitric oxide synthases: regulation and function Eur. Heart J. 33 2012 829 837
25. F. Spinella, E. Garrafa, V. Di Castro, L. Rosano, M.R. Nicotra, A. Caruso, P.G. Natali, and A. Bagnato Endothelin-1 stimulates lymphatic endothelial cells and lymphatic vessels to grow and invade Cancer Res. 69 2009 2669 2676
26. L. Xia et al. The TNF-alpha/ROS/HIF-1-induced upregulation of FoxMI expression promotes HCC proliferation and resistance to apoptosis Carcinogenesis 33 2012 2250 2259
27. T. Kosaka, A. Miyajima, S. Shirotake, E. Kikuchi, M. Hasegawa, S. Mikami, and M. Oya Ets-1 and hypoxia inducible factor-1alpha inhibition by angiotensin II type-1 receptor blockade in hormone-refractory prostate cancer Prostate 70 2010 162 169
28. I. Fleming, B. Fisslthaler, S. Dimmeler, B.E. Kemp, and R. Busse Phosphorylation of Thr(495) regulates Ca(2+)/calmodulin-dependent endothelial nitric oxide synthase activity Circ. Res. 88 2001 E68 E75
29. R. Wimalasundera, S. Fexby, L. Regan, S.A. Thom, and A.D. Hughes Effect of tumour necrosis factor-alpha and interleukin 1beta on endothelium-dependent relaxation in rat mesenteric resistance arteries in vitro Br. J. Pharmacol. 138 2003 1285 1294
30. E. Vila, and M. Salaices Cytokines and vascular reactivity in resistance arteries Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1016 H1021
31. A. Shatanawi, M.J. Romero, J.A. Iddings, S. Chandra, N.S. Umapathy, A.D. Verin, R.B. Caldwell, and R.W. Caldwell Angiotensin II-induced vascular endothelial dysfunction through RhoA/Rho kinase/p38 mitogen-activated protein kinase/arginase pathway Am. J. Physiol. Cell Physiol. 300 2011 C1181 C1192
32. R.W. Guo, L.X. Yang, M.Q. Li, B. Liu, and X.M. Wang Angiotensin II induces NF-kappa B activation in HUVEC via the p38MAPK pathway Peptides 27 2006 3269 3275
33. H. Nakashima, H. Suzuki, H. Ohtsu, J.Y. Chao, H. Utsunomiya, G.D. Frank, and S. Eguchi Angiotensin II regulates vascular and endothelial dysfunction: recent topics of Angiotensin II type-1 receptor signaling in the vasculature Curr. Vasc. Pharmacol. 4 2006 67 78
34. J. Pernow, A. Shemyakin, and F. Bohm New perspectives on endothelin-1 in atherosclerosis and diabetes mellitus Life Sci. 91 2012 507 516
35. T. Imanishi et al. Renin inhibitor aliskiren improves impaired nitric oxide bioavailability and protects against atherosclerotic changes Hypertension 52 2008 563 572
36. N. Bec, A.F.C. Gorren, B. Mayer, P.P. Schmidt, K.K. Andersson, and R. Lange The role of tetrahydrobiopterin in the activation of oxygen by nitric-oxide synthase J. Inorg. Biochem. 81 2000 207 211
37. K. Brunner, A. Tortschanoff, B. Hemmens, P.J. Andrew, B. Mayer, and A.J. Kungl Sensitivity of flavin fluorescence dynamics in neuronal nitric oxide synthase to cofactor-induced conformational changes and dimerization Biochemistry 37 1998 17545 17553
38. P. Klatt et al. Characterization of heme-deficient neuronal nitric-oxide synthase reveals a role for heme in subunit dimerization and binding of the amino acid substrate and tetrahydrobiopterin J. Biol. Chem. 271 1996 7336 7342
39. P. Kotsonis, L.G. Frohlich, Z.V. Shutenko, R. Horejsi, W. Pfleiderer, and H.H. Schmidt Allosteric regulation of neuronal nitric oxide synthase by tetrahydrobiopterin and suppression of auto-damaging superoxide Biochem. J. 346 Pt 3 2000 767 776
40. B.M. List et al. Characterization of bovine endothelial nitric oxide synthase as a homodimer with down-regulated uncoupled NADPH oxidase activity: tetrahydrobiopterin binding kinetics and role of haem in dimerization Biochem. J. 323 Pt 1 1997 159 165
41. H.M. Abu-Soud, and D.J. Stuehr Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer Proc. Natl. Acad. Sci. U.S.A. 90 1993 10769 10772
42. J.F. Desjardins, A. Pourdjabbar, A. Quan, H. Leong-Poi, K. Teichert-Kuliszewska, S. Verma, and T.G. Parker Lack of S100A1 in mice confers a gender-dependent hypertensive phenotype and increased mortality after myocardial infarction Am. J. Physiol. Heart Circ. Physiol. 296 2009 H1457 H1465
43. E.G. Shesely et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase Proc. Natl. Acad. Sci. U.S.A. 93 1996 13176 13181
44. P.L. Huang, Z. Huang, H. Mashimo, K.D. Bloch, M.A. Moskowitz, J.A. Bevan, and M.C. Fishman Hypertension in mice lacking the gene for endothelial nitric oxide synthase Nature 377 1995 239 242
45. D. Fulton et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt Nature 399 1999 597 601
46. A. Kuschel, P. Simon, and S. Tug Functional regulation of HIF-1alpha under normoxia - is there more than post-translational regulation? J. Cell Physiol. 227 2012 514 524