MicroRNA-155 Regulates ROS Production, NO Generation, Apoptosis and Multiple Functions of Human Brain Microvessel Endothelial Cells under Physiological and Pathological Conditions

Journal of Cellular Biochemistry

Volumn 116, Issue 12, 2015, Pages 2870-2881

  Chen, Yanfang ^a,b   Liu, Yajing ^a   Pan, Qunwen ^a   Zhao, Yuhui ^b   He, Caixia ^a   Bi, Kexia ^a   Chen, Yusen ^a   Zhao, Bin ^a   Ma, Xiaotang ^a  

^a GUANGDONG MEDICAL UNIVERSITY   (China)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

CELL FUNCTION; HUMAN BRAIN MICROVESSEL ENDOTHELIAL CELLS; ISCHEMIC STROKE; miR155; OXIDATIVE STRESS; REGULATORY MECHANISM

Indexed keywords

CASPASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; MICRORNA 155; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; REACTIVE OXYGEN METABOLITE; LOW DENSITY LIPOPROTEIN; MICRORNA; MIRN155 MICRORNA, HUMAN;

APOPTOSIS; ARTICLE; BRAIN CAPILLARY ENDOTHELIAL CELL; CELL ADHESION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; PHYSIOLOGICAL PROCESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROVASCULATURE; PATHOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; BRAIN; CASPASE 3; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; LIPOPROTEINS, LDL; MICRORNAS; MICROVESSELS; NITRIC OXIDE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84943570889     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25234     Document Type: Article

References (54)

1. Allen CL, Bayraktutan U,. 2009. Oxidative stress and its role in the pathogenesis of ischaemic stroke. Int J Stroke 4: 461-470.
2. Arai K, Jin G, Navaratna D, Lo EH,. 2009. Brain angiogenesis in developmental and pathological processes: Neurovascular injury and angiogenic recovery after stroke. FEBS J 276: 4644-4652.
3. Bohlen HG, Zhou X, Unthank JL, Miller SJ, Bills R,. 2009. Transfer of nitric oxide by blood from upstream to downstream resistance vessels causes microvascular dilation. Am J Physiol Heart Circ Physiol 297: H1337-H1346.
4. Cai H, Harrison DG,. 2000. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87: 840-844.
5. Ceolotto G, Papparella I, Bortoluzzi A, Strapazzon G, Ragazzo F, Bratti P, Fabricio AS, Squarcina E, Gion M, Palatini P, Semplicini A,. 2011. Interplay between miR-155, AT1R A1166C polymorphism, and AT1R expression in young untreated hypertensives. Am J Hypertens 24: 241-246.
6. Chavakis E, Dernbach E, Hermann C, Mondorf UF, Zeiher AM, Dimmeler S,. 2001. Oxidized LDL inhibits vascular endothelial growth factor-induced endothelial cell migration by an inhibitory effect on the Akt/endothelial nitric oxide synthase pathway. Circulation 103: 2102-2107.
7. Chen Z, Cai Y, Zhang W, Liu X, Liu S,. 2014. Astragaloside IV inhibits platelet-derived growth factor-BB-stimulated proliferation and migration of vascular smooth muscle cells via the inhibition of p38 MAPK signaling. Exp Ther Med 8: 1253-1258.
8. Claude S, Boby C, Rodriguez-Mateos A, Spencer JP, Gerard N, Morand C, Milenkovic D,. 2014. Flavanol metabolites reduce monocyte adhesion to endothelial cells through modulation of expression of genes via p38-MAPK and p65-Nf-kB pathways. Mol Nutr Food Res 58: 1016-1027.
9. Colles SM, Maxson JM, Carlson SG, Chisolm GM,. 2001. Oxidized LDL-induced injury and apoptosis in atherosclerosis. Potential roles for oxysterols. Trends Cardiovasc Med 11: 131-138.
10. Cominacini L, Pasini AF, Garbin U, Davoli A, Tosetti ML, Campagnola M, Rigoni A, Pastorino AM, Lo Cascio V, Sawamura T,. 2000. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cells induces the activation of NF-kappaB through an increased production of intracellular reactive oxygen species. J Biol Chem 275: 12633-12638.
11. Donners MM, Wolfs IM, Stoger LJ, van der Vorst EP, Pottgens CC, Heymans S, Schroen B, Gijbels MJ, de Winther MP,. 2012. Hematopoietic miR155 deficiency enhances atherosclerosis and decreases plaque stability in hyperlipidemic mice. PLoS ONE 7: e35877.
12. Erusalimsky JD, Skene C,. 2009. Mechanisms of endothelial senescence. Exp Physiol 94: 299-304.
13. Fann DY, Lee SY, Manzanero S, Chunduri P, Sobey CG, Arumugam TV,. 2013. Pathogenesis of acute stroke and the role of inflammasomes. Ageing Res Rev 12: 941-966.
14. Gao J, Zhang C, Fu X, Yi Q, Tian F, Ning Q, Luo X,. 2013. Effects of targeted suppression of glutaryl-CoA dehydrogenase by lentivirus-mediated shRNA and excessive intake of lysine on apoptosis in rat striatal neurons. PLoS ONE 8: e63084.
15. Hansson GK, Robertson AK, Soderberg-Naucler C,. 2006. Inflammation and atherosclerosis. Annu Rev Pathol 1: 297-329.
16. Hayashi T, Matsui-Hirai H, Miyazaki-Akita A, Fukatsu A, Funami J, Ding QF, Kamalanathan S, Hattori Y, Ignarro LJ, Iguchi A,. 2006. Endothelial cellular senescence is inhibited by nitric oxide: Implications in atherosclerosis associated with menopause and diabetes. Proc Natl Acad Sci USA 103: 17018-17023.
17. He X, Zhao M, Bi XY, Yu XJ, Zang WJ,. 2013. Delayed preconditioning prevents ischemia/reperfusion-induced endothelial injury in rats: Role of ROS and eNOS. Lab Invest 93: 168-180.
18. Higashi Y, Noma K, Yoshizumi M, Kihara Y,. 2009. Endothelial function and oxidative stress in cardiovascular diseases. Circ J 73: 411-418.
19. Hong D, Bai YP, Gao HC, Wang X, Li LF, Zhang GG, Hu CP,. 2014. Ox-LDL induces endothelial cell apoptosis via the LOX-1-dependent endoplasmic reticulum stress pathway. Atherosclerosis 235: 310-317.
20. Hou M, Cui J, Liu J, Liu F, Jiang R, Liu K, Wang Y, Yin L, Liu W, Yu B,. 2014. Angiopoietin-like 4 confers resistance to hypoxia/serum deprivation-induced apoptosis through PI3K/Akt and ERK1/2 signaling pathways in mesenchymal stem cells. PLoS ONE 9: e85808.
21. Hunsberger JG, Fessler EB, Wang Z, Elkahloun AG, Chuang DM,. 2012. Post-insult valproic acid-regulated microRNAs: Potential targets for cerebral ischemia. Am J Transl Res 4: 316-332.
22. Inoue M, Itoh H, Tanaka T, Chun TH, Doi K, Fukunaga Y, Sawada N, Yamshita J, Masatsugu K, Saito T, Sakaguchi S, Sone M, Yamahara K, Yurugi T, Nakao K,. 2001. Oxidized LDL regulates vascular endothelial growth factor expression in human macrophages and endothelial cells through activation of peroxisome proliferator-activated receptor-gamma. Arterioscler Thromb Vasc Biol 21: 560-566.
23. Kim BS, Park JY, Kang HJ, Kim HJ, Lee J,. 2014. Fucoidan/FGF-2 induces angiogenesis through JNK- and p38-mediated activation of AKT/MMP-2 signalling. Biochem Biophys Res Commun 450: 1333-1338.
24. Lakhani SA, Masud A, Kuida K, Porter GA, Jr., Booth CJ, Mehal WZ, Inayat I, Flavell RA,. 2006. Caspases 3 and 7: Key mediators of mitochondrial events of apoptosis. Science 311: 847-851.
25. Lee SB, Kim JJ, Kim TW, Kim BS, Lee MS, Yoo YD,. 2010. Serum deprivation-induced reactive oxygen species production is mediated by Romo1. Apoptosis 15: 204-218.
26. Leroyer AS, Rautou PE, Silvestre JS, Castier Y, Leseche G, Devue C, Duriez M, Brandes RP, Lutgens E, Tedgui A, Boulanger CM,. 2008. CD40 ligand+ microparticles from human atherosclerotic plaques stimulate endothelial proliferation and angiogenesis a potential mechanism for intraplaque neovascularization. J Am Coll Cardiol 52: 1302-1311.
27. Leung WY, Jensen MB,. 2013. Histological quantification of angiogenesis after focal cerebral infarction: A systematic review. ISRN Neurol 2013: 853737.
28. Libby P, Ridker PM, Hansson GK,. 2009. Inflammation in atherosclerosis: From pathophysiology to practice. J Am Coll Cardiol 54: 2129-2138.
29. Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X, Turner RJ, Jickling G, Sharp FR,. 2010. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 30: 92-101.
30. Liu J, Ren Y, Kang L, Zhang L,. 2014. Oxidized low-density lipoprotein increases the proliferation and migration of human coronary artery smooth muscle cells through the upregulation of osteopontin. Int J Mol Med 33: 1341-1347.
31. Liu L, Hu Y, Fu J, Yang X, Zhang Z,. 2013. MicroRNA155 in the growth and invasion of salivary adenoid cystic carcinoma. J Oral Pathol Med 42: 140-147.
32. Liu T, Shen D, Xing S, Chen J, Yu Z, Wang J, Wu B, Chi H, Zhao H, Liang Z, Chen C,. 2013. Attenuation of exogenous angiotensin II stress-induced damage and apoptosis in human vascular endothelial cells via microRNA-155 expression. Int J Mol Med 31: 188-196.
33. Magenta A, Greco S, Gaetano C, Martelli F,. 2013. Oxidative stress and microRNAs in vascular diseases. Int J Mol Sci 14: 17319-17346.
34. Maretzky T, Evers A, Zhou W, Swendeman SL, Wong PM, Rafii S, Reiss K, Blobel CP,. 2011. Migration of growth factor-stimulated epithelial and endothelial cells depends on EGFR transactivation by ADAM17. Nat Commun 2: 229.
35. Morello F, Perino A, Hirsch E,. 2009. Phosphoinositide 3-kinase signalling in the vascular system. Cardiovasc Res 82: 261-271.
36. Nakase T, Yamazaki T, Ogura N, Suzuki A, Nagata K,. 2008. The impact of inflammation on the pathogenesis and prognosis of ischemic stroke. J Neurol Sci 271: 104-109.
37. Napoli C, 2003. Oxidation of LDL, atherogenesis, and apoptosis. Ann N Y Acad Sci 1010: 698-709.
38. Nazari-Jahantigh M, Wei Y, Noels H, Akhtar S, Zhou Z, Koenen RR, Heyll K, Gremse F, Kiessling F, Grommes J, Weber C, Schober A,. 2012. MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J Clin Invest 122: 4190-4202.
39. Palumbo B, Oguogho A, Fitscha P, Sinzinger H,. 2000. Prostaglandin E1-therapy reduces circulating adhesion molecules (ICAM-1, E-selectin, VCAM-1) in peripheral vascular disease. Vasa 29: 179-185.
40. Pasquinelli AE, 2012. MicroRNAs and their targets: Recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13: 271-282.
41. Pirillo A, Norata GD, Catapano AL,. 2013. LOX-1, OxLDL, and atherosclerosis. Mediators Inflamm 2013: 152786.
42. Qin B, Yang H, Xiao B,. 2012. Role of microRNAs in endothelial inflammation and senescence. Mol Biol Rep 39: 4509-4518.
43. Salvayre R, Auge N, Benoist H, Negre-Salvayre A,. 2002. Oxidized low-density lipoprotein-induced apoptosis. Biochim Biophys Acta 1585: 213-221.
44. Selemidis S, Dusting GJ, Peshavariya H, Kemp-Harper BK, Drummond GR,. 2007. Nitric oxide suppresses NADPH oxidase-dependent superoxide production by S-nitrosylation in human endothelial cells. Cardiovasc Res 75: 349-358.
45. Song G, Ouyang G, Bao S,. 2005. The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med 9: 59-71.
46. Sun HX, Zeng DY, Li RT, Pang RP, Yang H, Hu YL, Zhang Q, Jiang Y, Huang LY, Tang YB, Yan GJ, Zhou JG,. 2012. Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension 60: 1407-1414.
47. Vanhoutte PM, Shimokawa H, Tang EH, Feletou M,. 2009. Endothelial dysfunction and vascular disease. Acta Physiol (Oxf) 196: 193-222.
48. Verhoye E, Langlois MR, Asklepios I,. 2009. Circulating oxidized low-density lipoprotein: A biomarker of atherosclerosis and cardiovascular risk?. Clin Chem Lab Med 47: 128-137.
49. Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, Wrenn SP, Narula J,. 2005. Atherosclerotic plaque progression and vulnerability to rupture: Angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 25: 2054-2061.
50. Wang J, Chen S, Ma X, Cheng C, Xiao X, Chen J, Liu S, Zhao B, Chen Y,. 2013. Effects of endothelial progenitor cell-derived microvesicles on hypoxia/reoxygenation-induced endothelial dysfunction and apoptosis. Oxid Med Cell Longev 2013: 572729.
51. Yin KJ, Hamblin M, Chen YE,. 2014. Non-coding RNAs in cerebral endothelial pathophysiology: Emerging roles in stroke. Neurochem Int 77C: 9-16.
52. Zheng L, Xu CC, Chen WD, Shen WL, Ruan CC, Zhu LM, Zhu DL, Gao PJ,. 2010. MicroRNA-155 regulates angiotensin II type 1 receptor expression and phenotypic differentiation in vascular adventitial fibroblasts. Biochem Biophys Res Commun 400: 483-488.
53. Zhu LX, Liu J, Xie YH, Kong YY, Ye Y, Wang CL, Li GD, Wang Y,. 2004. Expression of hepatitis C virus envelope protein 2 induces apoptosis in cultured mammalian cells. World J Gastroenterol 10: 2972-2978.
54. Zhu N, Zhang D, Chen S, Liu X, Lin L, Huang X, Guo Z, Liu J, Wang Y, Yuan W, Qin Y,. 2011. Endothelial enriched microRNAs regulate angiotensin II-induced endothelial inflammation and migration. Atherosclerosis 215: 286-293.