Activated protein C improves ischemic flap survival and modulates proangiogenic and antiinflammatory gene expression

Plastic and Reconstructive Surgery

Volumn 123, Issue 2, 2009, Pages 502-515

  Bezuhly, Michael ^a   Morris, Steven F ^a   Juskevicius, Ridas ^a   Currie, R William ^a   West, Kenneth A ^a   Liwski, Robert S ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; EARLY GROWTH RESPONSE FACTOR 1; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; PROTEIN BCL 2; SODIUM CHLORIDE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN RECEPTOR 2; BLOOD CLOTTING FACTOR 8; INTERLEUKIN 1BETA; PROTEIN C; RECOMBINANT PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; BLEEDING; BLOOD VESSEL; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; DENSITY; GENE EXPRESSION; GRAFT NECROSIS; GRAFT SURVIVAL; HISTOLOGY; INFLAMMATORY CELL; ISCHEMIA; MALE; NONHUMAN; POSTOPERATIVE PERIOD; PREOPERATIVE PERIOD; PREOPERATIVE TREATMENT; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SKIN FLAP; THERAPY DELAY; ANIMAL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; NECROSIS; PATHOLOGY; PHYSIOLOGY; PLASTIC SURGERY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ANIMALS; APOPTOSIS; FACTOR VIII; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-1BETA; ISCHEMIA; MALE; NECROSIS; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN C; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SURGICAL FLAPS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 61449150724     PISSN: 00321052     EISSN: None     Source Type: Journal    
DOI: 10.1097/PRS.0b013e318196b87f     Document Type: Article

References (59)

1. Merchant SH, Gurule DM, Larson RS. Amelioration of ischemia-reperfusion injury with cyclic peptide blockade of ICAM-1. Am J Physiol. 2003;284:H1260-H1268.
2. Demirseren ME, Sarici M, Gokrem S,YenidunyaS. Protective effects of monoclonal antibody to intercellular adhesion molecule-1 in venous ischemia-reperfusion injury: Experimental study in rats. J Reconstr Microsurg. 2007;23:41-44.
3. Pang CY, Forrest CR, Morris SF. Pharmacological augmentation of skin flap viability: A hypothesis to mimic the surgical delay phenomenon or a wishful thought. Ann Plast Surg. 1989;22:293-306.
4. Akan M, Cakir B, Misirlioglu A, Yildirim S, Taylan G, Akoz T. Effects of clopidogrel and high dose aspirin on survival of skin flaps in rats. Scand J Plast Reconstr Surg Hand Surg. 2005; 39:7-10.
5. Engel H, Sauerbier M, Germann G, Kuntscher MV. Dose-dependent effects of nitric oxide donor in a rat flap model. Ann Plast Surg. 2007;58:456-460.
6. Kim EK, Hong JP. The effect of recombinant human eryth-ropoietin on ischemia-reperfusion injury: An experimental study in a rat TRAM flap model. Plast Reconstr Surg. 2007; 120:1774-1781.
7. Carroll CM, Carroll SM, Schuschke DH, Barker JH. Augmentation of skeletal muscle survival using platelet derived growth factor. Plast Reconstr Surg. 1998;102:407-415.
8. Padubidri A, Browne E Jr. Effect of vascular endothelial growth factor (VEGF) on survival of random extension of axial pattern skin flaps in the rat. Ann Plast Surg. 1996;37: 604-611.
9. Huang N, Khan A, Ashrafpour H, et al. Efficacy and mechanism of adenovirus-mediated VEGF-165 gene therapy for augmentation of skin flap viability. Am J Physiol. 2006;291: H127-H137.
10. Zheng Y, Yi C, Xia W, et al. Mesenchymal stem cells transduced by vascular endothelial growth factor gene for isch-emic random skin flaps. Plast Reconstr Surg. 2008;121:59-69.
11. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9:669-676.
12. JokusziesA,NiederbichlerA,Meyer-MarcottyM,Lahoda LU, Reimers K, Vogt PM. Influence of transendothelial mecha- nisms on microcirculation: Consequences for reperfusion injury after free flap transfer. Previous, current, and future aspects. J Reconstr Microsurg. 2006;22:513-518.
13. Grace PA. Ischaemia-reperfusion injury. Br J Surg. 1994;81: 637-647.
14. Banbury J, Siemionow M, Porvasnik S, Petras S, Zins JE. Muscle flaps' triphasic microcirculatory response to sympathectomy and denervation. Plast Reconstr Surg. 1999;104: 730-737.
15. Morris SF, Taylor GI. The time sequence of the delay phenomenon: When is a surgical delay effective? An experimental study. Plast Reconstr Surg. 1995;95:526-533.
16. Kharbanda RK, Peters M, Walton B, et al. Ischemic preconditioning prevents endothelial injury and systemic neutrophil activation during ischemia-reperfusion in humans in vivo. Circulation 2001;103:1624-1630.
17. Yadav SS, Sindram D, Perry DK, Clavien PA. Ischemic preconditioning protects the mouse liver by inhibition of apoptosis through a caspase-dependent pathway. Hepatology 1999; 30:1223-1231.
18. Lefer AM, Lefer DJ. The role of nitric oxide and cell adhesion molecules on the microcirculation in ischaemia-reperfusion. Cardiovasc Res. 1996;32:743-751.
19. Murphy RC, Lawrence WT, Robson MC, Heggers JP. Surgical delay and arachidonic acid metabolites: Evidence for an inflammatory mechanism. An experimental study in rats. Br J Plast Surg. 1985;38:272-277.
20. Tepper OM, Capla JM, Galiano RD, et al. Adult vasculogen-esis occurs through in situ recruitment, proliferation, and tubulization of circulating bone marrow-derived cells. Blood 2005;105:1068-1077.
21. Park S, Tepper OM, Galiano RD, et al. Selective recruitment of endothelial progenitor cells to ischemic tissues with increased neovascularization. Plast Reconstr Surg. 2004;113: 284-293.
22. Ercocen AR, Kono T, Kikuchi Y, Kitazawa Y, Nozaki M. Efficacy of the flashlamp-pumped pulsed-dye laser in nonsur-gical delay of skin flaps. Dermatol Surg. 2003;29:692-699.
23. Bernard GR, Vincent JL, Laterre PF, et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med. 2001;344:699-709.
24. Esmon CT. The endothelial protein C receptor. Curr Opin Hematol. 2006;13:382-385.
25. Vu TK, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 1991;64: 1057-1068.
26. Joyce DE, Gelbert L,Ciaccia A, DeHoff B,Grinnell BW. Gene expression profile of antithrombotic protein C defines new mechanisms modulating inflammation and apoptosis. J Biol Chem. 2001;276:11199-11203.
27. Franscini N, Bachli EB, Blau N, Leikauf MS, Schaffner A, Schoedon G. Gene expression profiling of inflamed human endothelial cells and influence of activated protein C. Circulation 2004;110:2903-2909.
28. Barnes PJ. Nuclear factor-kappa B. Int J Biochem Cell Biol. 1997;29:867-870.
29. Bartolome S, Wood JG, Casillan AJ, Simpson SQ, O'Brien-Ladner AR. Activated protein C attenuates microvascular injury during systemic hypoxia. Shock 2008;29:384-387.
30. Bae JS, Yang L, Manithody C, Rezaie AR. The ligand occupancy of endothelial protein C receptor switches the pro-tease-activated receptor 1-dependent signaling specificity of thrombin from a permeability-enhancing to a barrier-protective response in endothelial cells. Blood 2007; 110:3909-3916.
31. Cheng T, Liu D, Griffin JH, et al. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothe-lium and is neuroprotective. Nat Med. 2003;9:338-342.
32. Mosnier LO, Griffin JH. Inhibition of staurosporine-induced apoptosis of endothelial cells by activated protein C requires protease activated receptor-1 and endothelial cell protein C receptor. Biochem J. 2003;373:65-70.
33. Xue M, Thompson P, Sambrook PN, March L, Jackson CJ. Activated protein C stimulates expression of angiogenic factors in human skin cells, angiogenesis in the chick embryo and cutaneous wound healing in rodents. Clin Hemorheol Microcirc. 2006;34:153-161.
34. Jackson CJ, Xue M, Thompson P, et al. Activated protein C prevents inflammation yet stimulates angiogenesis to promote cutaneous wound healing. Wound Repair Regen. 2005; 13:284-294.
35. Bezuhly M, Liwski R, West KA, Morris SF. Activated protein C: An emerging therapeutic agent in the prevention of ischemia-reperfusion injury. J Reconstr Microsurg. 2008; 24:361-367.
36. Zhi Q, Gu Y, Kim D, Hiura A, Sumi S, Inoue K. The effect of fibrin on the survival of ischemic skin flaps in rats. Plast Reconstr Surg. 2007;120:1148-1155.
37. Chen W, Zhang F, Chen MB, Lineweaver WC. Expression of vascular endothelial growth factor receptor-2 in the muscle flap with ischemic injury in rats. J Surg Res. 2007;140:45-49.
38. Zhang F, Hu EC, Topp S, Lei M, Chen W, Lineaweaver WC. Proinflammatory cytokines gene expression inskin flaps with arterial and venous ischemia in rats. J Reconstr Microsurg. 2006;22:641-647.
39. Michlits W, Mittermayr R, Schafer R, Redl H, Aharinejad S. Fibrin-embedded administration of VEGF plasmid enhances skin flap survival. Wound Repair Regen. 2007;15:360-367.
40. Huang SS, Wei FC, Hung LM. Ischemic preconditioning attenuates postischemic leukocyte-endothelial cell interactions: Role of nitric oxide and protein kinase C. Circ J. 2006; 70:1070-1075.
41. Villaschi S, Nicosia RF. Paracrine interactions between fi-broblasts and endothelial cells in a serum-free coculture model: Modulation of angiogenesis and collagen gel contraction. Lab Invest. 1994;71:291-299.
42. McManus JF. Histological and histochemical uses of periodic acid. Biotechnic Histochem. 1948;23:99-108.
43. Zhang Q, Chang Q, Cox RA, Gong X, Gould LJ. Hyperbaric oxygen attenuates apoptosis and decreases inflammation in an ischemic wound model. J Invest Dermatol. 2008;128: 2102-2112.
44. Yang D, Morris SF. An extended dorsal island skin flap with multiple vascular territories in the rat: A new skin flap model. J Surg Res. 1999;87:164-170.
45. Pfaffl MW. Relative quantification. In: Real-Time PCR . 1st ed. London: Taylor & Francis; 2006.
46. Yamaguchi Y, Hisama N, Okajima K, et al. Pretreatment with activated protein C or active human urinary thrombomodulin attenuates the production of cytokine-induced neutrophil chemoattractant following ischemia/reperfusion in rat liver. Hepatology 1997;25:1136-1140.
47. Mizutani A, Okajima K, Uchiba M, Noguchi T. Activated protein C reduces ischemia/reperfusion-induced renal injury in rats by inhibiting leukocyte activation. Blood 2000; 95:3781-3787.
48. Schoots IG, Levi M, van Vliet AK, Maas AM, Roossink EH, van Gulik TM. Inhibition of coagulation and inflammation by activated protein C or antithrombin reduces intestinal ischemia/reperfusion injury in rats. Crit Care Med. 2004;32: 1375-1383.
49. Dillon JP, Laing AJ, Cahill RA, et al. Activated protein C attenuates acute ischaemia reperfusion injury in skeletal muscle. J Orthop Res. 2005;23:1454-1459.
50. Hoffmann JN, Vollmar B, Laschke MW, et al. Microhemo-dynamic and cellular mechanism of activated protein C action during endotoxemia. Crit Care Med. 2004;32:1011-1017.
51. Fumagalli R, Mignini MA. The safety profile of drotrecogin alpha (activated). Crit Care 2007;5(11 Suppl):S6.
52. Kerschen EJ, Fernandez JA, Cooley BC, et al. Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C. J Exp Med. 2007;204:2439-2448.
53. Asano T, Kaneko E, Shinozaki S, et al. Hyperbaric oxygen induces basic fibroblast growth factor and hepatocyte growth factor expression, and enhances blood perfusion and muscle regeneration in mouse ischemic hind limbs. Circ J. 2007;71: 405-411.
54. O'Brien LA, Richardson MA, Mehrbod SF, et al. Activated protein C decreases tumor necrosis factor related apoptosis-inducing ligand by an EPCR-independent mechanism involving Egr-1/Erk-1/2 activation. Arterioscler Thromb Vasc Biol. 2007;27:2634-2641.
55. Schweighofer B, Schultes J, Pomyie J, Hofer E. Signals and genes induced by angiogenic growth factors in comparison to inflammatory cytokines in endothelial cells. Clin Hemorheol Microcirc. 2007;37:57-62.
56. Lucerna M, Mechtcheriakova D, Kadl A, et al. NAB2, a core-pressor of EGR-1, inhibits vascular endothelial growth factor-mediated gene induction and angiogenic responses of en-dothelial cells. J Biol Chem. 2003;278:11433-11440.
57. Fahmy RG, Dass CR, Sun LQ, Chesterman CN, Khachigian LM. Transcription factor Egr-1 supports FGF-dependent an-giogenesis during neovascularization and tumor growth. Nat Med. 2003;9:1026-1032.
58. Joyce DE, Grinnell BW. Recombinant human activated protein C attenuates the inflammatory response in endothelium and monocytes by modulating nuclear factor-kappaB. Crit Care Med. 2002;30:S288-S299.
59. Burns K, Martinon F, Tschopp J. New insights into the mechanism of IL-1beta maturation. Curr Opin Immunol. 2003;15: 26-30.