Thrombosis Research
Volume 126, Issue 4 , Pages 306-310 , October 2010

Bone morphogenetic protein -7 increases thrombogenicity of lipid-rich atherosclerotic plaques via activation of tissue factor

  • M.A. Sovershaev

      Affiliations

    • Division of Internal Medicine, University Hospital of North Norway, N-9038, Tromsø, Norway
    • Hematological Research Group, Department of Clinical Medicine, The Faculty of Health Sciences, University of Tromsø, N-9037, Tromsø, Norway
    • Corresponding Author InformationCorresponding author. Division of Internal Medicine, University Hospital of North Norway, N-9038, Tromsø, Norway. Tel.: +47 77645457.
    • E.M.E. and M.A.S. contributed equally to this work.
  • ,
  • E.M. Egorina

      Affiliations

    • Division of Internal Medicine, University Hospital of North Norway, N-9038, Tromsø, Norway
    • Hematological Research Group, Department of Clinical Medicine, The Faculty of Health Sciences, University of Tromsø, N-9037, Tromsø, Norway
    • E.M.E. and M.A.S. contributed equally to this work.
  • ,
  • V.Y. Bogdanov

      Affiliations

    • University of Cincinnati College of Medicine, Department of Internal Medicine, Cincinnati, OH, 45267, USA
  • ,
  • N. Seredkina

      Affiliations

    • Molecular Pathology Research Group, Department of Medical Biology, The Faculty of Health Sciences, University of Tromsø, N-9037, Tromsø, Norway
  • ,
  • J.T. Fallon

      Affiliations

    • Department of Pathology, Mount Sinai School of Medicine, New York, NY, 10029, USA
  • ,
  • A.Y. Valkov

      Affiliations

    • Department of Pathology, University Hospital of North Norway, N-9038, Tromsø, Norway
  • ,
  • B. Østerud

      Affiliations

    • Hematological Research Group, Department of Medical Biology, The Faculty of Health Sciences, University of Tromsø, N-9037, Tromsø, Norway
  • ,
  • J.B. Hansen

      Affiliations

    • Division of Internal Medicine, University Hospital of North Norway, N-9038, Tromsø, Norway
    • Hematological Research Group, Department of Clinical Medicine, The Faculty of Health Sciences, University of Tromsø, N-9037, Tromsø, Norway

Received 3 May 2010 ,Revised 23 June 2010 ,Accepted 30 June 2010.

References 

  1. Thim T, Hagensen MK, Bentzon JF, et al. From vulnerable plaque to atherothrombosis. J Intern Med. 2008 May;263(5):506–516
  2. Burke AP, Farb A, Malcom GT, et al. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med. 1997 May 1;336(18):1276–1282
  3. Virmani R, Burke AP, Kolodgie FD, et al. Pathology of the thin-cap fibroatheroma: a type of vulnerable plaque. J Interv Cardiol. 2003 Jun;16(3):267–272
  4. Virmani R, Burke AP, Farb A, et al. Pathology of the unstable plaque. Prog Cardiovasc Dis. 2002 Mar-Apr;44(5):349–356
  5. Fuster V, Moreno PR, Fayad ZA, et al. Atherothrombosis and high-risk plaque: part I: evolving concepts. J Am Coll Cardiol. 2005 Sep 20;46(6):937–954
  6. Badimon JJ, Lettino M, Toschi V, et al. Local inhibition of tissue factor reduces the thrombogenicity of disrupted human atherosclerotic plaques: effects of tissue factor pathway inhibitor on plaque thrombogenicity under flow conditions. Circulation. 1999 Apr 13;99(14):1780–1787
  7. Thiruvikraman SV, Guha A, Roboz J, et al. In situ localization of tissue factor in human atherosclerotic plaques by binding of digoxigenin-labeled factors VIIa and X. Lab Invest. 1996 Oct;75(4):451–461
  8. Toschi V, Gallo R, Lettino M, et al. Tissue factor modulates the thrombogenicity of human atherosclerotic plaques. Circulation. 1997 Feb 4;95(3):594–599
  9. Mackman N. Role of tissue factor in hemostasis and thrombosis. Blood Cells Mol Dis. 2006 Mar-Apr;36(2):104–107
  10. Reininger AJ, Bernlochner I, Penz SM, et al. A 2-step mechanism of arterial thrombus formation induced by human atherosclerotic plaques. J Am Coll Cardiol. 2010 Mar 16;55(11):1147–1158
  11. Croce K, Libby P. Intertwining of thrombosis and inflammation in atherosclerosis. Curr Opin Hematol. 2007 Jan;14(1):55–61
  12. Ruf W, Mueller BM. Tissue factor in cancer angiogenesis and metastasis. Curr Opin Hematol. 1996 Sep;3(5):379–384
  13. Edwards RL, Rickles FR, Bobrove AM. Mononuclear cell tissue factor: cell of origin and requirements for activation. Blood. 1979 Aug;54(2):359–370
  14. Rivers RP, Hathaway WE, Weston WL. The endotoxin-induced coagulant activity of human monocytes. Br J Haematol. 1975 Jul;30(3):311–316
  15. Rauch U, Bonderman D, Bohrmann B, et al. Transfer of tissue factor from leukocytes to platelets is mediated by CD15 and tissue factor. Blood. 2000 Jul 1;96(1):170–175
  16. Rauch U, Osende JI, Fuster V, et al. Thrombus formation on atherosclerotic plaques: pathogenesis and clinical consequences. Ann Intern Med. 2001 Feb 6;134(3):224–238
  17. Kaikita K, Ogawa H, Yasue H, et al. Tissue factor expression on macrophages in coronary plaques in patients with unstable angina. Arterioscler Thromb Vasc Biol. 1997 Oct;17(10):2232–2237
  18. Saito Y, Wada H, Yamamuro M, et al. Changes of plasma hemostatic markers during percutaneous transluminal coronary angioplasty in patients with chronic coronary artery disease. Am J Hematol. 1999 Aug;61(4):238–242
  19. Kingsley DM. The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 1994 Jan;8(2):133–146
  20. Harada S, Rodan GA. Control of osteoblast function and regulation of bone mass. Nature. 2003 May 15;423(6937):349–355
  21. Massague J, Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 2000 Apr 17;19(8):1745–1754
  22. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature. 1997 Dec 4;390(6659):465–471
  23. Bostrom K, Watson KE, Horn S, et al. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 1993 Apr;91(4):1800–1809
  24. Vattikuti R, Towler DA. Osteogenic regulation of vascular calcification: an early perspective. Am J Physiol Endocrinol Metab. 2004 May;286(5):E686–E696
  25. Dorai H, Vukicevic S, Sampath TK. Bone morphogenetic protein-7 (osteogenic protein-1) inhibits smooth muscle cell proliferation and stimulates the expression of markers that are characteristic of SMC phenotype in vitro. J Cell Physiol. 2000 Jul;184(1):37–45
  26. Davies MR, Lund RJ, Hruska KA. BMP-7 is an efficacious treatment of vascular calcification in a murine model of atherosclerosis and chronic renal failure. J Am Soc Nephrol. 2003 Jun;14(6):1559–1567
  27. Cunningham NS, Paralkar V, Reddi AH. Osteogenin and recombinant bone morphogenetic protein 2B are chemotactic for human monocytes and stimulate transforming growth factor beta 1 mRNA expression. Proc Natl Acad Sci USA. 1992 Dec 15;89(24):11740–11744
  28. Detmer K, Walker AN. Bone morphogenetic proteins act synergistically with haematopoietic cytokines in the differentiation of haematopoietic progenitors. Cytokine. 2002 Jan 7;17(1):36–42
  29. Hilden K, Tuuri T, Eramaa M, et al. Expression of type II activin receptor genes during differentiation of human K562 cells and cDNA cloning of the human type IIB activin receptor. Blood. 1994 Apr 15;83(8):2163–2170
  30. Flossel C, Luther T, Albrecht S, et al. Constitutive tissue factor expression of human breast cancer cell line MCF-7 is modulated by growth factors. Eur J Cancer. 1992;28A(12):1999–2002
  31. Samad F, Pandey M, Loskutoff DJ. Tissue factor gene expression in the adipose tissues of obese mice. Proc Natl Acad Sci USA. 1998 Jun 23;95(13):7591–7596
  32. Hutter R, Valdiviezo C, Sauter BV, et al. Caspase-3 and tissue factor expression in lipid-rich plaque macrophages: evidence for apoptosis as link between inflammation and atherothrombosis. Circulation. 2004 Apr 27;109(16):2001–2008
  33. Egorina EM, Sovershaev MA, Bjorkoy G, et al. Intracellular and surface distribution of monocyte tissue factor: application to intersubject variability. Arterioscler Thromb Vasc Biol. 2005 Jul;25(7):1493–1498
  34. Hammer-Hansen S, Kofoed KF, Kelbaek H, et al. Volumetric evaluation of coronary plaque in patients presenting with acute myocardial infarction or stable angina pectoris-a multislice computerized tomography study. Am Heart J. 2009 Mar;157(3):481–487
  35. Jara A, Chacon C, Burgos ME, et al. Expression of gremlin, a bone morphogenetic protein antagonist, is associated with vascular calcification in uraemia. Nephrol Dial Transplant. 2009 Apr;24(4):1121–1129
  36. Oeth P, Parry GC, Mackman N. Regulation of the tissue factor gene in human monocytic cells. Role of AP-1, NF-kappa B/Rel, and Sp1 proteins in uninduced and lipopolysaccharide-induced expression. Arterioscler Thromb Vasc Biol. 1997 Feb;17(2):365–374
  37. Davies MR, Lund RJ, Mathew S, et al. Low turnover osteodystrophy and vascular calcification are amenable to skeletal anabolism in an animal model of chronic kidney disease and the metabolic syndrome. J Am Soc Nephrol. 2005 Apr;16(4):917–928

PII: S0049-3848(10)00366-X

doi: 10.1016/j.thromres.2010.06.026

Thrombosis Research
Volume 126, Issue 4 , Pages 306-310 , October 2010