Erythropoietin-induced upregulation of endothelial nitric oxide synthase but not vascular endothelial growth factor prevents musculocutaneous tissue from ischemic damage

Laboratory Investigation

Volumn 90, Issue 1, 2010, Pages 40-51

  Rezaeian, Farid ^a,b   Wettstein, Reto ^a   Egger, Jean François ^a   Sandmann, Freya ^b   Rücker, Martin ^c   Tobalem, Mickaël ^b   Vollmar, Brigitte ^d   Menger, Michael D ^e   Harder, Yves ^a,b  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF ROSTOCK   (Germany)

^e SAARLAND UNIVERSITY   (Germany)

Author keywords

Angiogenesis; Critical ischemia; ENOS; EPO; Flap surgery; Microcirculation

Indexed keywords

BEVACIZUMAB; ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; RECOMBINANT ERYTHROPOIETIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD FLOW; CAPILLARY DENSITY; CELL DEATH; CONTROLLED STUDY; DRUG MECHANISM; FLUORESCENCE MICROSCOPY; GANGRENE; GRAFT NECROSIS; HEMODYNAMICS; IMMUNOHISTOCHEMISTRY; MACROMOLECULE; MOUSE; MUSCLE ISCHEMIA; MUSCLE TISSUE; MYOCUTANEOUS FLAP; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; TISSUE INJURY; TISSUE PERFUSION; TISSUE SURVIVAL; UPREGULATION;

ANIMALS; ARTERIOLES; CAPILLARIES; ERYTHROPOIETIN; HUMANS; IMMUNOHISTOCHEMISTRY; ISCHEMIA; MICE; MICE, INBRED C57BL; MICROSCOPY; MUSCLE, SKELETAL; NECROSIS; NEOVASCULARIZATION, PHYSIOLOGIC; NITRIC OXIDE SYNTHASE TYPE III; RECOMBINANT PROTEINS; REGIONAL BLOOD FLOW; SKIN; SURGICAL FLAPS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 73349115860     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.117     Document Type: Article

References (39)

1. Krantz SB. Erythropoietin. Blood 1991; 77: 419-434.
2. Wu H, Liu X, Jaenisch R, et al. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 1995;83:59-67.
3. Lacombe C, Da Silva JL, Bruneval P, et al. Erythropoietin: sites of synthesis and regulation of secretion. Am J Kidney Dis 1991;18 (4 Suppl 1):14-19.
4. Hasegawa J, Wagner KF, Karp D, et al. Altered pulmonary vascular reactivity in mice with excessive erythrocytosis. Am J Respir Crit Care Med 2004;169:829-835.
5. Cai Z, Semenza GL. Phosphatidylinositol-3-kinase signaling is required for erythropoietin-mediated acute protection against myocardial ischemia/reperfusion injury. Circulation 2004;109:2050-2053.
6. Sakanaka M, Wen TC, Matsuda S, et al. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci USA 1998;95:4635-4640.
7. Hasselblatt M, Ehrenreich H, Siren AL. The brain erythropoietin system and its potential for therapeutic exploitation in brain disease. J Neurosurg Anesthesiol 2006;18:132-138.
8. Sepodes B, Maio R, Pinto R, et al. Recombinant human erythropoietin protects the liver from hepatic ischemia-reperfusion injury in the rat. Transpl Int 2006;19:919-926.
9. Patel NS, Sharples EJ, Cuzzocrea S, et al. Pretreatment with EPO reduces the injury and dysfunction caused by ischemia/reperfusion in the mouse kidney in vivo. Kidney Int 2004;66:983-989.
10. Contaldo C, Meier C, Elsherbiny A, et al. Human recombinant erythropoietin protects the striated muscle microcirculation of the dorsal skinfold from postischemic injury in mice. Am J Physiol Heart Circ Physiol 2007;293:H274-H283.
11. Salahudeen AK, Haider N, Jenkins J, et al. Anti-apoptotic properties of erythropoiesis stimulating proteins in models of cisplatin-induced acute kidney injury. Am J Physiol Renal Physiol 2008;294:F1354-F1365.
12. Xue YQ, Zhao LR, Guo WP, et al. Intrastriatal administration of erythropoietin protects dopaminergic neurons and improves neurobehavioral outcome in a rat model of Parkinson's disease. Neuroscience 2007;146:1245-1258.
13. Burger D, Lei M, Geoghegan-Morphet N, et al. Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase. Cardiovasc Res 2006;72:51-59.
14. 0-monophosphate levels and contractility in bovine tracheal smooth muscle. Mol Pharmacol 1977;13:330-341.
15. Bodo E, Kromminga A, Funk W, et al. Human hair follicles are an extrarenal source and a nonhematopoietic target of erythropoietin. FASEB J 2007;21:3346-3354. (Pubitemid 47565553)
16. Stewart KJ, Stewart DA, Coghlan B, et al. Complications of 278 consecutive abdominoplasties. J Plast Reconstr Aesthet Surg 2006;59:1152-1155.
17. Wettstein R, Schürch R, Banic A, et al. Review of 197 consecutive free flap reconstructions in the lower extremity. J Plast Reconstr Aesthet Surg 2008;61:772-776.
18. Ascherman JA, Patel SM, Malhotra SM, et al. Management of sternal wounds with bilateral pectoralis major myocutaneous advancement flaps in 114 consecutively treated patients: refinements in technique and outcomes analysis. Plast Reconstr Surg 2004;114:676-683.
19. Zeitani J, Bertoldo F, Bassano C, et al. Superficial wound dehiscence after median sternotomy: surgical treatment versus secondary wound healing. Ann Thorac Surg 2004;77:672-675.
20. Lehr HA, Leunig M, Menger MD, et al. Dorsal skinfold chamber technique for intravital microscopy in nude mice. Am J Pathol 1993;143:1055-1062.
21. Harder Y, Amon M, Erni D, et al. Evolution of ischemic tissue injury in a random pattern flap: a new mouse model using intravital microscopy. J Surg Res 2004;121:197-205.
22. Klyscz T, Junger M, Jung F, et al. [Cap image\-a new kind of computer-assisted video image analysis system for dynamic capillary microscopy]. Biomed Tech (Berl) 1997;42:168-175.
23. Gross JF, Aroesty J. Mathematical models of capillary flow: a critical review. Biorheology 1972;9:225-264.
24. Menger MD, Pelikan S, Steiner D, et al. Microvascular ischemia-reperfusion injury in striated muscle: significance of 'reflow paradox'. Am J Physiol 1992;263(6 Part 2):H1901-H1906. (Pubitemid 23030746)
25. Contaldo C, Elsherbiny A, Lindenblatt N, et al. Erythropoietin enhances oxygenation in critically perfused tissue through modulation of nitric oxide synthase. Shock 2009;31:599-606.
26. Kanagy NL, Perrine MF, Cheung DK, et al. Erythropoietin administration in vivo increases vascular nitric oxide synthase expression. J Cardiovasc Pharmacol 2003;42:527-533.
27. Nakano M, Satoh K, Fukumoto Y, et al. Important role of erythropoietin receptor to promote VEGF expression and angiogenesis in peripheral ischemia in mice. Circ Res 2007;100:662-669.
28. Kobayashi H, Minatoguchi S, Yasuda S, et al. Post-infarct treatment with an erythropoietin-gelatin hydrogel drug delivery system for cardiac repair. Cardiovasc Res 2008;79:611-620.
29. Westenbrink BD, Oeseburg H, Kleijn L, et al. Erythropoietin stimulates normal endothelial progenitor cell-mediated endothelial turnover, but attributes to neovascularization only in the presence of local ischemia. Cardiovasc Drugs Ther 2008;22:265-274.
30. Galeano M, Altavilla D, Bitto A, et al. Recombinant human erythropoietin improves angiogenesis and wound healing in experimental burn wounds. Crit Care Med 2006;34:1139-1146.
31. Sano H, Hosokawa K, Kidoya H, et al. Negative regulation of VEGF-induced vascular leakage by blockade of angiotensin II type 1 receptor. Arterioscler Thromb Vasc Biol 2006;26: 2673-2680.
32. Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 2002;125(Part 11):2549-2557.
33. Kurose I, Wolf R, Grisham MB, et al. Effects of an endogenous inhibitor of nitric oxide synthesis on postcapillary venules. Am J Physiol 1995;268(6 Part 2):H2224-H2231.
34. Laszlo F, Morschl E, Pavo I, et al. Nitric oxide modulates the gastrointestinal plasma extravasation following intraabdominal surgical manipulation in rats. Eur J Pharmacol 1999;375:211-215.
35. Rotter R, Menshykova M, Winkler T, et al. Erythropoietin improves functional and histological recovery of traumatized skeletal muscle tissue. J Orthop Res 2008;26:1618-1626.
36. Le Minh K, Klemm K, Abshagen K, et al. Attenuation of inflammation and apoptosis by pre-and posttreatment of darbepoetin-alpha in acute liver failure of mice. Am J Pathol 2007;170: 1954-1963.
37. Rezaeian F, Wettstein R, Amon M, et al. Erythropoietin protects critically perfused flap tissue. Ann Surg 2008;248:919-929.
38. Mori S, Sawada T, Okada T, et al. Erythropoietin and its derivative protect the intestine from severe ischemia/reperfusion injury in the rat. Surgery 2008;143:556-565.
39. Ergur BU, Kiray M, Pekcetin C, et al. Protective effect of erythropoietin pretreatment in testicular ischemia-reperfusion injury in rats. J Pediatr Surg 2008;43:722-728.