Activated protein C accelerates venous thrombus resolution through heme oxygenase-1 induction

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 1, 2014, Pages 93-102

  Gabre, J ^a   Chabasse, C ^a   Cao, C ^a   Mukhopadhyay, S ^a   Siefert, S ^a   Bi, Y ^a   Netzel Arnett, S ^a   Sarkar, R ^a   Zhang, L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Heme oxygenase 1; Inflammation; Protein C; Thrombolytic therapy; Venous thrombosis

Indexed keywords

COLLAGEN; DROTRECOGIN; GELATINASE A; GELATINASE B; HEME OXYGENASE 1; INTERLEUKIN 6; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTOPORPHYRIN TIN; UROKINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEEP VEIN THROMBOSIS; HISTOPATHOLOGY; INFERIOR CAVA VEIN; MOUSE; NONHUMAN; POSTTHROMBOSIS SYNDROME; PRIORITY JOURNAL; PROTEIN EXPRESSION; THROMBUS; VEIN EMBOLISM; VEIN LIGATION;

HEME OXYGENASE-1; INFLAMMATION; PROTEIN C; THROMBOLYTIC THERAPY; VENOUS THROMBOSIS;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; ENZYME INDUCTION; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEME OXYGENASE-1; MICE; MICE, INBRED C57BL; PROTEIN C; REAL-TIME POLYMERASE CHAIN REACTION; VENOUS THROMBOSIS;

EID: 84891896951     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12424     Document Type: Article

References (31)

1. Ashrani AA, Heit JA. Incidence and cost burden of post-thrombotic syndrome. J Thromb Thrombolysis 2009; 28: 465-76.
2. Kahn SR. The post thrombotic syndrome. Thromb Res 2011; 127(Suppl. 3): S89-92.
3. Khanna AK, Singh S. Postthrombotic syndrome: surgical possibilities. Thrombosis 2012; 2012: 520604.
4. Bauersachs R, Berkowitz SD, Brenner B, Buller HR, Decousus H, Gallus AS, Lensing AW, Misselwitz F, Prins MH, Raskob GE, Segers A, Verhamme P, Wells P, Agnelli G, Bounameaux H, Cohen A, Davidson BL, Piovella F, Schellong S. Oral rivaroxaban for symptomatic venous thromboembolism. N Engl J Med 2010; 363: 2499-510.
5. Wakefield TW, Myers DD, Henke PK. Mechanisms of venous thrombosis and resolution. Arterioscler Thromb Vasc Biol 2008; 28: 387-91.
6. Dahi S, Lee JG, Lovett DH, Sarkar R. Differential transcriptional activation of matrix metalloproteinase-2 and membrane type-1 matrix metalloproteinase by experimental deep venous thrombosis and thrombin. J Vasc Surg 2005; 42: 539-45.
7. Wojcik BM, Wrobleski SK, Hawley AE, Wakefield TW, Myers DD Jr, Diaz JA. Interleukin-6: a potential target for post-thrombotic syndrome. Ann Vasc Surg 2011; 25: 229-39.
8. Esmon CT. The interactions between inflammation and coagulation. Br J Haematol 2005; 131: 417-30.
9. Sakata Y, Curriden S, Lawrence D, Griffin JH, Loskutoff DJ. Activated protein C stimulates the fibrinolytic activity of cultured endothelial cells and decreases antiactivator activity. Proc Natl Acad Sci USA 1985; 82: 1121-5.
10. Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science 2002; 296: 1880-2.
11. Cao C, Gao Y, Li Y, Antalis TM, Castellino FJ, Zhang L. The efficacy of activated protein C in murine endotoxemia is dependent on integrin CD11b. J Clin Invest 2010; 120: 1971-80.
12. Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood 2007; 109: 3161-72.
13. Bi Y, Gao Y, Ehirchiou D, Cao C, Kikuiri T, Le A, Shi S, Zhang L. Bisphosphonates cause osteonecrosis of the jaw-like disease in mice. Am J Pathol 2010; 177: 280-90.
14. Humphries J, McGuinness CL, Smith A, Waltham M, Poston R, Burnand KG. Monocyte chemotactic protein-1 (MCP-1) accelerates the organization and resolution of venous thrombi. J Vasc Surg 1999; 30: 894-9.
15. McGuinness CL, Humphries J, Waltham M, Burnand KG, Collins M, Smith A. Recruitment of labelled monocytes by experimental venous thrombi. Thromb Haemost 2001; 85: 1018-24.
16. Singh I, Burnand KG, Collins M, Luttun A, Collen D, Boelhouwer B, Smith A. Failure of thrombus to resolve in urokinase-type plasminogen activator gene-knockout mice: rescue by normal bone marrow-derived cells. Circulation 2003; 107: 869-75.
17. Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 2010; 80: 1895-903.
18. Tracz MJ, Juncos JP, Grande JP, Croatt AJ, Ackerman AW, Katusic ZS, Nath KA. Induction of heme oxygenase-1 is a beneficial response in a murine model of venous thrombosis. Am J Pathol 2008; 173: 1882-90.
19. Lindenblatt N, Bordel R, Schareck W, Menger MD, Vollmar B. Vascular heme oxygenase-1 induction suppresses microvascular thrombus formation in vivo. Arterioscler Thromb Vasc Biol 2004; 24: 601-6.
20. Grey ST, Tsuchida A, Hau H, Orthner CL, Salem HH, Hancock WW. Selective inhibitory effects of the anticoagulant activated protein C on the responses of human mononuclear phagocytes to LPS, IFN-gamma, or phorbol ester. J Immunol 1994; 153: 3664-72.
21. Stephenson DA, Toltl LJ, Beaudin S, Liaw PC. Modulation of monocyte function by activated protein C, a natural anticoagulant. J Immunol 2006; 177: 2115-22.
22. Toltl LJ, Beaudin S, Liaw PC. Activated protein C up-regulates IL-10 and inhibits tissue factor in blood monocytes. J Immunol 2008; 181: 2165-73.
23. Jackson CJ, Xue M, Thompson P, Davey RA, Whitmont K, Smith S, Buisson-Legendre N, Sztynda T, Furphy LJ, Cooper A, Sambrook P, March L. Activated protein C prevents inflammation yet stimulates angiogenesis to promote cutaneous wound healing. Wound Repair Regen 2005; 13: 284-94.
24. Sood V, Luke C, Miller E, Mitsuya M, Upchurch GR Jr, Wakefield TW, Myers DD, Henke PK. Vein wall remodeling after deep vein thrombosis: differential effects of low molecular weight heparin and doxycycline. Ann Vasc Surg 2010; 24: 233-41.
25. Anderson FA Jr, Spencer FA. Risk factors for venous thromboembolism. Circulation 2003; 107: I9-16.
26. Dahlback B, Carlsson M, Svensson PJ. Familial thrombophilia due to a previously unrecognized mechanism characterized by poor anticoagulant response to activated protein C: prediction of a cofactor to activated protein C. Proc Natl Acad Sci USA 1993; 90: 1004-8.
27. Deatrick KB, Eliason JL, Lynch EM, Moore AJ, Dewyer NA, Varma MR, Pearce CG, Upchurch GR, Wakefield TW, Henke PK. Vein wall remodeling after deep vein thrombosis involves matrix metalloproteinases and late fibrosis in a mouse model. J Vasc Surg 2005; 42: 140-8.
28. Roumen-Klappe EM, Janssen MC, van Rossum J, Holewijn S, van Bokhoven MM, Kaasjager K, Wollersheim H, Den Heijer M. Inflammation in deep vein thrombosis and the development of post-thrombotic syndrome: a prospective study. J Thromb Haemost 2009; 7: 582-7.
29. Cheng T, Petraglia AL, Li Z, Thiyagarajan M, Zhong Z, Wu Z, Liu D, Maggirwar SB, Deane R, Fernandez JA, LaRue B, Griffin JH, Chopp M, Zlokovic BV. Activated protein C inhibits tissue plasminogen activator-induced brain hemorrhage. Nat Med 2006; 12: 1278-85.
30. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A. Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 2004; 165: 1045-53.
31. Kerschen EJ, Fernandez JA, Cooley BC, Yang XV, Sood R, Mosnier LO, Castellino FJ, Mackman N, Griffin JH, Weiler H. Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C. J Exp Med 2007; 204: 2439-48.