Soluble thrombomodulin is a paracrine anti-apoptotic factor for vascular endothelial protection

International Journal of Cardiology

Volumn 172, Issue 2, 2014, Pages 340-349

  Chao, Ting Hsing ^a,b   Tsai, Wei Chuan ^a,b   Chen, Ju Yi ^a,b   Liu, Ping Yen ^a,b   Chung, Hsing Chun ^a,b   Tseng, Shi Ya ^a,b   Kuo, Cheng Hsiang ^b   Shi, Guey Yueh ^b   Wu, Hua Lin ^b   Li, Yi Heng ^a,b  

^a NATIONAL CHENG KUNG UNIVERSITY HOSPITAL   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Endothelium; Thrombomodulin

Indexed keywords

CASPASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAD; PROTEIN BAX; PROTEIN BCL 2; RECOMBINANT THROMBOMODULIN; STRESS ACTIVATED PROTEIN KINASE; VASCULOTROPIN; CULTURE MEDIUM; THROMBOMODULIN;

APOPTOSIS; ARTICLE; CELL COUNT; CELL GROWTH; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; ENDOTHELIUM CELL; GROWTH INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; VASCULAR ENDOTHELIUM; CELL CULTURE; CULTURE MEDIUM; CYTOLOGY; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; NICK END LABELING; PHYSIOLOGY; SIGNAL TRANSDUCTION; UMBILICAL CORD; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IN SITU NICK-END LABELING; SIGNAL TRANSDUCTION; THROMBOMODULIN; UMBILICAL CORD;

EID: 84900595659     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2014.01.009     Document Type: Article

References (32)

1. T. Stefanec Endothelial apoptosis: could it have a role in the pathogenesis and treatment of disease? Chest 117 2000 841 854
2. L. Zeng, A. Zampetaki, and A. Margariti et al. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow Proc Natl Acad Sci U S A 106 2009 8326 8331
3. E. Durand, A. Scoazec, and A. Lafont et al. In vivo induction of endothelial apoptosis leads to vessel thrombosis and endothelial denudation: a clue to the understanding of the mechanisms of thrombotic plaque erosion Circulation 109 2004 2503 2506
4. C.T. Esmon The roles of protein C and thrombomodulin in the regulation of blood coagulation J Biol Chem 264 1989 4743 4746
5. H.C. Huang, G.Y. Shi, and S.J. Jiang et al. Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain J Biol Chem 278 2003 46750 46759
6. Y.H. Li, C.H. Kuo, and G.Y. Shi et al. The role of thrombomodulin lectin-like domain in inflammation J Biomed Sci 19 2012 34
7. B. Isermann, I.A. Vinnikov, and T. Madhusudhan et al. Activated protein C protects against diabetic nephropathy by inhibiting endothelial and podocyte apoptosis Nat Med 13 2007 1349 1358
8. H. Ishii, and P.W. Majerus Thrombomodulin is present in human plasma and urine J Clin Invest 76 1985 2178 2181
9. V. Salomaa, C. Matei, and N. Aleksic et al. Soluble thrombomodulin as a predictor of incident coronary heart disease and symptomless carotid artery atherosclerosis in the Atherosclerosis Risk in Communities (ARIC) study: a case-cohort study Lancet 353 1999 1729 1734
10. C.S. Shi, G.Y. Shi, and Y.S. Chang et al. Evidence of human thrombomodulin domain as a novel angiogenic factor Circulation 111 2005 1627 1636
11. Y.H. Li, H.C. Chung, and C.Y. Luo et al. Thrombomodulin is upregulated in cardiomyocytes during cardiac hypertrophy and prevents the progression of contractile dysfunction J Card Fail 16 2010 980 990
12. F.M. Ho, S.H. Liu, C.S. Liau, P.J. Huang, and S.Y. Lin-Shiau High glucose-induced apoptosis in human endothelial cells is mediated by sequential activations of c-Jun NH(2)-terminal kinase and caspase-3 Circulation 101 2000 2618 2624
13. H. Chaudhury, M. Zakkar, and J. Boyle et al. c-Jun N-terminal kinase primes endothelial cells at atheroprone sites for apoptosis Arterioscler Thromb Vasc Biol 30 2010 546 553
14. T.L. Cheng, C.F. Teng, and W.H. Tsai et al. Multitarget therapy of malignant cancers by the head-to-tail tandem array multiple shRNAs expression system Cancer Gene Ther 16 2009 516 531
15. T.H. Chao, S.Y. Tseng, and Y.H. Li et al. A novel vasculo-angiogenic effect of cilostazol mediated by crosstalk between multiple signalling pathways including Erk/p38 MAPK signaling transduction cascade Clin Sci (Lond) 123 2012 147 159
16. A.K. Ohlin, K. Larsson, and M. Hansson Soluble thrombomodulin activity and soluble thrombomodulin antigen in plasma J Thromb Haemost 3 2005 976 982
17. M.A. Raymond, N. Vigneault, V. Luyckx, and M.J. Hébert Paracrine repercussions of preconditioning on angiogenesis and apoptosis of endothelial cells Biochem Biophys Res Commun 291 2002 261 269
18. M.A. Raymond, A. Désormeaux, and P. Laplante et al. Apoptosis of endothelial cells triggers a caspase-dependent anti-apoptotic paracrine loop active on VSMC FASEB J 18 2004 705 707
19. M.A. Raymond, A. Désormeaux, and A. Labelle et al. Endothelial stress induces the release of vitamin D-binding protein, a novel growth factor Biochem Biophys Res Commun 338 2005 1374 1382
20. M. Soulez, I. Sirois, and N. Brassard et al. Epidermal growth factor and perlecan fragments produced by apoptotic endothelial cells co-ordinately activate ERK1/2-dependent antiapoptotic pathways in mesenchymal stem cells Stem Cells 28 2010 810 820
21. J. Kim, J. Lin, R.M. Adam, C. Lamb, S.B. Shively, and M.R. Freeman An oxidative stress mechanism mediates chelerythrine-induced heparin-binding EGF-like growth factor ectodomain shedding J Cell Biochem 94 2005 39 49
22. L. Wang, J.A. Bastarache, N. Wickersham, X. Fang, M.A. Matthay, and L.B. Ware Novel role of the human alveolar epithelium in regulating intra-alveolar coagulation Am J Respir Cell Mol Biol 36 2007 497 503
23. M.W. Boehme, Y. Deng, and U. Raeth et al. Release of thrombomodulin from endothelial cells by concerted action of TNF-alpha and neutrophils: in vivo and in vitro studies Immunology 87 1996 134 140
24. M.W. Boehme, P. Galle, and W. Stremmel Kinetics of thrombomodulin release and endothelial cell injury by neutrophil-derived proteases and oxygen radicals Immunology 107 2002 340 349
25. Y.H. Li, J.H. Chen, and H.L. Wu et al. G-33A mutation in the promoter region of thrombomodulin gene and its association with coronary artery disease and plasma soluble thrombomodulin levels Am J Cardiol 85 2000 8 12
26. S.M. Lin, Y.M. Wang, and H.C. Lin et al. Serum thrombomodulin level relates to the clinical course of disseminated intravascular coagulation, multiorgan dysfunction syndrome, and mortality in patients with sepsis Crit Care Med 36 2008 683 689
27. S. Takano, S. Kimura, S. Ohdama, and N. Aoki Plasma thrombomodulin in health and diseases Blood 76 1990 2024 2029
28. T. Ozaki, C. Anas, and S. Maruyama et al. Intrarenal administration of recombinant human soluble thrombomodulin ameliorates ischaemic acute renal failure Nephrol Dial Transplant 23 2008 110 119
29. B.W. Festoff, S. Ameenuddin, and K. Santacruz et al. Neuroprotective effects of recombinant thrombomodulin in controlled contusion spinal cord injury implicates thrombin signaling J Neurotrauma 21 2004 907 922
30. T. Ikezoe, J. Yang, and C. Nishioka et al. Thrombomodulin protects endothelial cells from a calcineurin inhibitor-induced cytotoxicity by upregulation of extracellular signal-regulated kinase/myeloid leukemia cell-1 signaling Arterioscler Thromb Vasc Biol 32 2012 2259 2270
31. J.Y. Li, C.H. Su, and Y.J. Wu et al. Therapeutic angiogenesis of human early endothelial progenitor cells is enhanced by thrombomodulin Arterioscler Thromb Vasc Biol 31 2011 2518 2525
32. H. Hamada, H. Ishii, K. Sakyo, S. Horie, K. Nishiki, and M. Kazama The epidermal growth factor-like domain of recombinant human thrombomodulin exhibits mitogenic activity for Swiss 3T3 cells Blood 86 1995 225 233