Darbepoetin-alpha does not promote microvascular thrombus formation in mice: Role of eNOS-dependent protection through platelet and endothelial cell deactivation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 27, Issue 5, 2007, Pages 1191-1198

  Lindenblatt, Nicole ^a   Menger, Michael D ^b   Klar, Ernst ^a   Vollmar, Brigitte ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Endothelium; Intravital microscopy; Nitric oxide; Platelets; Thrombosis

Indexed keywords

BIOLOGICAL MARKER; CELL ADHESION MOLECULE; ERYTHROPOIETIN; NITRIC OXIDE; NOVEL ERYTHROPOIESIS STIMULATING PROTEIN; TYROSINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CARDIOVASCULAR RISK; CIRCULATION; CONTROLLED STUDY; CREMASTER MUSCLE; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROPOIESIS; EXPERIMENTAL MODEL; FLOW CYTOMETRY; HEMATOCRIT; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY; MICROVASCULATURE; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICAL SIGNIFICANCE; THROMBOCYTE FUNCTION; THROMBOGENESIS; TREATMENT DURATION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ANEMIA; ANIMALS; BLOOD PLATELETS; BLOTTING, WESTERN; CAPILLARIES; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROPOIETIN; FLOW CYTOMETRY; GENE EXPRESSION; HEMATINICS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE III; P-SELECTIN; PROGNOSIS; RNA; THROMBELASTOGRAPHY; THROMBOSIS;

EID: 34247376432     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.107.141580     Document Type: Article

References (39)

1. Krantz SB. Erythropoietin. Blood. 1991;77:419-434.
2. Jelkmann W. Molecular biology of erythropoietin. Intern Med. 2004;43:649-659.
3. Fisher JW. Erythropoietin: Physiology and pharmacology update. Exp Biol Med. 2003;228:1-14.
4. Bham B. Unhealthy competition. EMBO Reports. 2003;4:927-929.
5. Fuste B, Serradell M, Escolar G, Cases A, Mazzara R, Castillo R, Ordinas A, Diaz-Ricart M. Erythropoietin triggers a signaling pathway in endothelial cells and increases the thrombogenicity of their extracellular matrices in vitro. Thromb Haemost. 2002;88:678-685.
6. Borawski J, Mysliwiec M. Effects of recombinant erythropoietin therapy on circulating endothelial markers in hemodialysis patients. Clin Appl Thromb Hemost. 2002;8:77-84.
7. Wolf RF, Peng J, Friese P, Gilmore LS, Burstein SA, Dale GL. Erythropoietin administration increases production and reactivity of platelets in dogs. Thromb Haemost. 1997;78:1505-1509.
8. Beguin Y. Erythropoietin and platelet production. Haematologica. 1999;84:541-547.
9. Stohlawetz PJ, Dzirlo L, Hergovich N, Lackner E, Mensik C, Eichler HG, Kabrna E, Geissler K, Jilma B. Effects of erythropoietin on platelet reactivity and thrombopoiesis in humans. Blood. 2000;95:2983-2989.
10. Taylor JE, McLaren M, Henderson IS, Belch JJ, Stewart WK. Prothrombotic effect of erythropoietin in dialysis patients. Nephrol Dial Transplant. 1992;7:235-239.
11. Wolf RF, Gilmore LS, Friese P, Downs T, Burstein SA, Dale GL. Erythropoietin potentiates thrombus development in a canine arteriovenous shunt model. Thromb Haemost. 1997;77:1020-1024.
12. Cadroy Y, Hanson SR. Effects of red blood cell concentration on hemostasis and thrombus formation in a primate model. Blood. 1990;75:2185-2193.
13. Vogel J, Kiessling I, Heinicke K, Stallmach T, Ossent P, Vogel O, Aulmann M, Frietsch T, Schmid-Schonbein H, Kuschinsky W, Gassmann M. Transgenic mice overexpressing erythropoietin adapt to excessive erythrocytosis by regulating blood viscosity. Blood. 2003;102:2278-2284.
14. Shibata J, Hasegawa J, Siemens HJ, Wolber E, Dibbelt L, Li D, Katschinski DM, Fandrey J, Jelkmann W, Gassmann M, Wenger RH, Wagner KF. Hemostasis and coagulation at a hematocrit level of 0.85: functional consequences of erythrocytosis. Blood. 2003;101:4416-4422.
15. Belayev L, Khoutorova L, Zhao W, Vigdorchik A, Belayev A, Busto R, Magal E, Ginsberg MD. Neuroprotective effect of darbepoetin alfa, a novel recombinant erythropoietic protein, in focal cerebral ischemia in rats. Stroke. 2005;36:1071-1076.
16. Nieswandt B, Schulte V, Bergmeier W. Flow-cytometric analysis of mouse platelet function. Methods Mol Biol. 2004;272:255-268.
17. Baez S. An open cremaster muscle preparation for the study of blood vessels by in vivo microscopy. Microvasc Res. 1973;5:384-394.
18. 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;24:601-606.
19. Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, Wagner DD. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 1998;95:9524-9529.
20. Baker M, Wayland H. On-line volume flow rate and velocity profile measurement for blood in microvessels. Microvasc Res. 1974;7:131-143.
21. Rentzsch R Bad Blood. News@Nature (20.02.06).
22. Hasegawa Y, Takamatsu J, Iwase T, Iwasada S, Kitamura S, Iwata H. Effects of recombinant human erythropoietin on thrombosis and fibrinolysis in autologous transfusion for hip surgery. Arch Orthop Trauma Surg. 1999;119:384-387.
23. Fuste B, Diaz-Ricart M, Cases A, Lopez-Pedret J, Ordinas A, Escolar G. Erythropoietin does not modify the prothrombotic effect induced by uremic media on endothelial cells. Haematologica. 2002;87:1006-1008.
24. Klar E, Herfarth C, Messmer K. Therapeutic effect of isovolemic hemodilution with dextran 60 on the impairment of pancreatic microcirculation in acute biliary pancreatitis. Ann Surg. 1990;211:346-353.
25. Frost-Arner L, Bergqvist D. Effect of isovolemic hemodilution with dextran and albumin on thrombus formation in artificial vessel grafts inserted into the abdominal aorta of the rabbit. Microsurgery. 1995;16:357-361.
26. Farina JA Jr., Piccinato CE, Campos AD, Rossi MA. Comparative study of isovolemic hemodilution with 3% albumin, dextran-40, and prophylactic enoxaparin (LMWH) on thrombus formation at venous microanastomosis in rats. Microsurgery. 2006;26:456-464.
27. Atchabahian A, Masquelet AC. Experimental prevention of free flap thrombosis. II: Normovolemic hemodilution for thrombosis prevention. Microsurgery. 1996;17:714-716.
28. Duebener LF, Sakamoto T, Hatsuoka S, Stamm C, Zurakowski D, Vollmar B, Menger MD, Schafers HJ, Jonas RA. Effects of hematocrit on cerebral microcirculation and tissue oxygenation during deep hypothermic bypass. Circulation. 2001;104(12 Suppl 1):I260-264.
29. Quaschning T, Ruschitzka F, Stallmach T, Shaw S, Morawietz H, Goettsch W, Hermann M, Slowinski T, Theuring F, Hocher B, Luscher TF, Gassmann M. Erythropoietin-induced excessive erythrocytosis activates the tissue endothelin system in mice. FASEB J. 2003;17:259-261.
30. Smith KJ, Bleyer AJ, Little WC, Sane DC. The cardiovascular effects of erythropoietin. Cardiovasc Res. 2003;59:538-548.
31. Wiessner C, Allegrini PR, Ekatodramis D, Jewell UR, Stallmach T, Gassmann M. Increased cerebral infarct volumes in polyglobulic mice overexpressing erythropoietin. J Cereb Blood Flow Metab. 2001;21:857-864.
32. Ruschitzka FT, Wenger RH, Stallmach T, Quaschning T, de Wit C, Wagner K, Labugger R, Kelm M, Noll G, Rulicke. T, Shaw S, Lindberg RL, Rodenwaldt B, Lutz H, Bauer C, Luscher TF, Gassmann M. Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin. Proc Natl Acad Sci U S A. 2000;97:11609-11613.
33. Beleslin-Cokic BB, Cokic VP, Yu X, Weksler BB, Schechter AN, Noguchi CT. Erythropoietin and hypoxia stimulate erythropoietin receptor and nitric oxide production by endothelial cells. Blood. 2004;104:2073-2080.
34. Dimmeler S, Zeiher AM. Nitric oxide and apoptosis: another paradigm for the double-edged role of nitric oxide. Nitric Oxide. 1997;1:275-281.
35. Mannick JB, Asano K, Izumi K, Kieff E, Stamler JS. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell. 1994;79:1137-1146.
36. Mannick JB, Miao XQ, Stamler JS. Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem. 1997;272:24125-24128.
37. Rossig L, Fichtlscherer B, Breitschopf K, Haendeler J, Zeiher AM, Mulsch A, Dimmeler S. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem. 1999;274:6823-6826.
38. Broeders MA, Tangelder GJ, Slaaf DW, Reneman RS, oude Egbrink MG. Endogenous nitric oxide protects against thromboembolism in venules but not in arterioles. Arterioscler Thromb Vasc Biol. 1998;18:139-145.
39. Broeders MA, Tangelder GJ, Slaaf DW, Reneman RS, Egbrink MG. Endogenous nitric oxide and prostaglandins synergistically counteract thromboembolism in arterioles but not in venules. Arterioscler Thromb Vasc Biol. 2001;21:163-169.