Exogenous bradykinin inhibits tissue factor induction and deep vein thrombosis via activating the eNOS/Phosphoinositide 3-Kinase/Akt signaling pathway

Cellular Physiology and Biochemistry

Volumn 37, Issue 4, 2015, Pages 1592-1606

  Dong, Ruolan ^a   Chen, Wenshu ^b   Feng, Wenjing ^c   Xia, Congying ^a   Hu, Danli ^a   Zhang, Yanjun ^a   Yang, Yan ^a   Wang, Dao Wen ^a   Xu, Xizhen ^a   Tu, Ling ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b FUJIAN MEDICAL UNIVERSITY   (China)

^c QINGDAO UNIVERSITY   (China)

Author keywords

Bradykinin; Deep vein thrombosis; LPS; Monocytes; Tissue factor

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BRADYKININ; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; N(G) NITROARGININE METHYL ESTER; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SODIUM CHLORIDE; THROMBOPLASTIN; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; BRADYKININ B2 RECEPTOR; CHROMONE DERIVATIVE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MORPHOLINE DERIVATIVE; NITRIC OXIDE; NOS3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; DEEP VEIN THROMBOSIS; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFERIOR CAVA VEIN; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL; VEIN LIGATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; VEIN THROMBOSIS;

ANIMALS; BRADYKININ; CHROMONES; GLYCOGEN SYNTHASE KINASE 3; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MONOCYTES; MORPHOLINES; NF-KAPPA B; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, BRADYKININ B2; RNA, MESSENGER; SIGNAL TRANSDUCTION; THROMBOPLASTIN; VENOUS THROMBOSIS;

EID: 84945580047     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000438526     Document Type: Article

References (42)

1. Ho WK. Deep vein thrombosis-risks and diagnosis. Aust Fam Physician 2010;39:468-474.
2. Dai MX, Zheng XH, Yu J, Yin T, Ma MJ, Zhang L, Liu M, Ma Y, Liu LW, Gao X, Li Y, Song LQ, Wang HC. The impact of intermittent and repetitive cold stress exposure on endoplasmic reticulum stress and instability of atherosclerotic plaques. Cell Physiol Biochem 2014;34:393-404.
3. Carmeliet P, Mackman N, Moons L, Luther T, Gressens P, Van Vlaenderen I, Demunck H, Kasper M, Breier G, Evrard P, Muller M, Risau W, Edgington T, Collen D. Role of tissue factor in embryonic blood vessel development. Nature 1996;383:73-75.
4. Belting M, Ahamed J, Ruf W. Signaling of the tissue factor coagulation pathway in angiogenesis and cancer. Arterioscler Thromb Vasc Biol 2005;25:1545-1550.
5. Penn MS, Topol EJ. Tissue factor, the emerging link between inflammation, thrombosis, and vascular remodeling. Circ Res 2001;89:1-2.
6. Bogdanov VY, Balasubramanian V, Hathcock J, Vele O, Lieb M, Nemerson Y. Alternatively spliced human tissue factor: a circulating, soluble, thrombogenic protein. Nat Med 2003;9:458-462.
7. Steffel J, Luscher TF, Tanner FC. Tissue factor in cardiovascular diseases: molecular mechanisms and clinical implications. Circulation 2006;113:722-731.
8. Xu C, Gui Q, Chen W, Wu L, Sun W, Zhang N, Xu Q, Wang J, Fu X. Small interference RNA targeting tissue factor inhibits human lung adenocarcinoma growth in vitro and in vivo. J Exp Clin Cancer Res 2011;30:63.
9. Zhou J, May L, Liao P, Gross PL, Weitz JI. Inferior Vena Cava Ligation Rapidly Induces Tissue Factor Expression and Venous Thrombosis in Rats. Arterioscler Thromb Vasc Biol 2009;29:863-869.
10. Zhang WY, Wang H, Huo YQ. Acadesine Inhibits Tissue Factor Induction and Thrombus Formation by Activating the Phosphoinositide 3-Kinase/Akt Signaling Pathway. Circulation 2009;120:S1169-S1169.
11. Lopez JA, Kearon C, Lee AY. Deep venous thrombosis. Hematology Am Soc Hematol Educ Program 2004;10.1182/asheducation-2004.1.439439-456.
12. Xu X, Tu L, Jiang W, Feng W, Zhao CX, Wang DW. Bradykinin prevents the apoptosis of NIT-1 cells induced by TNF-Alpha via the PI3K/Akt and MAPK signaling pathways. Int J Mol Med 2012;29:891-898.
13. Oeseburg H, Iusuf D, van der Harst P, van Gilst WH, Henning RH, Roks AJM. Bradykinin Protects Against Oxidative Stress-Induced Endothelial Cell Senescence. Hypertension 2009;53:417-422.
14. Dong RL, Xu XZ, Li G, Feng WJ, Zhao G, Zhao JJ, Wang DW, Tu L. Bradykinin Inhibits Oxidative Stress-Induced Cardiomyocytes Senescence via Regulating Redox State. Plos One 2013;8:e77034.
15. Shariat-Madar Z, Mahdi F, Warnock M, Homeister JW, Srikanth S, Krijanovski Y, Murphey LJ, Jaffa AA, Schmaier AH. Bradykinin B2 receptor knockout mice are protected from thrombosis by increased nitric oxide and prostacyclin. Blood 2006;108:192-199.
16. Ehringer WD EM, Gray RD, Miller FN. Bradykinin antagonizes the effect of alpha-Dhrombin. Inflammation 1997;21:279-298.
17. Schmaier AH. The kallikrein-kinin and the renin-Angiotensin systems have a multilayered interaction. Am J Physiol Regul Integr Comp Physiol 2003;285:R1-13.
18. Hasan AA, Amenta S, Schmaier AH. Bradykinin and its metabolite, Arg-Pro-Pro-Gly-Phe, are selective inhibitors of alpha-Dhrombin-induced platelet activation. Circulation 1996;94:517-528.
19. Yang Y, Loscalzo J. Regulation of tissue factor expression in human microvascular endothelial cells by nitric oxide. Circulation 2000;101:2144-2148.
20. Tschudi MR, Luscher TF: [Nitric oxide: the endogenous nitrate in the cardiovascular system]. Herz 1996;21 Suppl 1:50-60.
21. Livak KJ1 ST. Analysis of relative gene expression data using real-Dime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408.
22. Brill A, Fuchs TA, Chauhan AK, Yang JJ, De Meyer SF, Kollnberger M, Wakefield TW, Lammle B, Massberg S, Wagner DD: von Willebrand factor-mediated platelet adhesion is critical for deep vein thrombosis in mouse models. Blood 2011;117:1400-1407.
23. Westrick RJ, Bodary PF, Xu Z, Shen YC, Broze GJ, Eitzman DT. Deficiency of Tissue Factor Pathway Inhibitor Promotes Atherosclerosis and Thrombosis in Mice. Circulation 2001;103:3044-3046.
24. von Bruhl ML, Stark K, Steinhart A, Chandraratne S, Konrad I, Lorenz M, Khandoga A, Tirniceriu A, Coletti R, Kollnberger M, Byrne RA, Laitinen I, Walch A, Brill A, Pfeiler S, Manukyan D, Braun S, Lange P, Riegger J, Ware J, Eckart A, Haidari S, Rudelius M, Schulz C, Echtler K, Brinkmann V, Schwaiger M, Preissner KT, Wagner DD, Mackman N, Engelmann B, Massberg S. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012;209:819-835.
25. Zhang WY, Wang JG, Wang H, Tang R, Belcher JD, Viollet B, Geng JG, Zhang CX, Wu CD, Slungaard A, Zhu CH, Huo YQ. Acadesine Inhibits Tissue Factor Induction and Thrombus Formation by Activating the Phosphoinositide 3-Kinase/Akt Signaling Pathway. Arterioscler Thromb Vasc Biol 2010;30:1000-1006.
26. Guha M, Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 2002;277:32124-32132.
27. Xia L ZH, Hu L, Xie H, Wang T, Xu Y, Liu J, Zhang X, Yan J.: Both NF-κB and c-Jun/AP-1 involved in anti-β2GPI/β2GPI-induced tissue factor expression in monocytes. Thromb Haemost 2013;109:643-651.
28. Thuringer D, Maulon L, Frelin C. Rapid transactivation of the vascular endothelial growth factor receptor KDR/Flk-1 by the bradykinin B2 receptor contributes to endothelial nitric-oxide synthase activation in cardiac capillary endothelial cells. J Biol Chem 2002;277:2028-2032.
29. Li YD, Ye BQ, Zheng SX, Wang JT, Wang JG, Chen M, Liu JG, Pei XH, Wang LJ, Lin ZX, Gupta K, Mackman N, Slungaard A, Key NS, Geng JG. NF-kappaB transcription factor p50 critically regulates tissue factor in deep vein thrombosis. J Biol Chem 2009;284:4473-4483.
30. Lindmark E, Tenno T, Siegbahn A. Role of platelet P-selectin and CD40 ligand in the induction of monocytic tissue factor expression. Arterioscler Thromb Vasc Biol 2000;20:2322-2328.
31. Muller WA. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol 2003;24:327-334.
32. Mangano DT, Miao Y, Tudor IC, Dietzel C, McSPI I, IREF. Post-reperfusion myocardial infarction-Long-Derm survival improvement using adenosine regulation with acadesine. J Am Coll Cardiol(JACC) 2006;48:206-214.
33. Eto M, Kouroedov A, Cosentino F, Luscher TF. Glycogen synthase kinase-3 mediates endothelial cell activation by tumor necrosis factor-Alpha. Circulation 2005;112:1316-1322.
34. Muller WA. Leukocyte-endothelial cell interactions in the inflammatory response. Lab Invest 2002;82:521-533.
35. Majima M, Nishiyama K, Iguchi Y, Yao K, Ogino M, Ohno T, Sunahara N, Katoh K, Tatemichi N, Takei Y, Katori M. Determination of bradykinin-(1-5) in inflammatory exudate by a new ELISA as a reliable indicator of bradykinin generation. Inflamm Res 1996;45:416-423.
36. Murphey LJ, Hachey DL, Oates JA, Morrow JD, Brown NJ. Metabolism of bradykinin in vivo in humans: Identification of BK1-5 as a stable plasma peptide metabolite. J Pharmacol Exp Ther 2000;294:263-269.
37. Morinelli TA, Webb JG, Jaffa AA, Privitera PJ, Margolius HS. A metabolic fragment of bradykinin, Arg-Pro-Pro-Gly-Phe, protects against the deleterious effects of lipopolysaccharide in rats. J Pharmacol Exp Ther 2001;296:71-76.
38. Hasan AA, Warnock M, Nieman M, Srikanth S, Mahdi F, Krishnan R, Tulinsky A, Schmaier AH. Mechanisms of Arg-Pro-Pro-Gly-Phe inhibition of thrombin. Am J Physiol Heart Circ Physiol 2003;285:H183-193.
39. Myers D, Jr., Farris D, Hawley A, Wrobleski S, Chapman A, Stoolman L, Knibbs R, Strieter R, Wakefield T. Selectins influence thrombosis in a mouse model of experimental deep venous thrombosis. J Surg Res 2002;108:212-221.
40. Schabbauer G, Tencati M, Pedersen B, Pawlinski R, Mackman N. PI3K-Akt pathway suppresses coagulation and inflammation in endotoxemic mice. Arterioscler Thromb Vasc Biol 2004;24:1963-1969.
41. Baker AK, Wang R, Mackman N, Luyendyk JP. Rapamycin enhances LPS induction of tissue factor and tumor necrosis factor-Alpha expression in macrophages by reducing IL-10 expression. Mol Immunol 2009;46:2249-2255.
42. Bae MK, Su-Ryun K, Soo-Kyung B. Visfatin enhances ICAM-1 and VCAM-1 expression through ROS-dependent NF-kappa B activation in endothelial cells. Febs J 2009;276:187-188.