Exogenous nitric oxide requires an endothelial glycocalyx to prevent postischemic coronary vascular leak in guinea pig hearts

Critical Care

Volumn 12, Issue 3, 2008, Pages

  Bruegger, Dirk ^a   Rehm, Markus ^a   Jacob, Matthias ^a   Chappell, Daniel ^a   Stoeckelhuber, Mechthild ^a   Welsch, Ulrich ^a   Conzen, Peter ^a   Becker, Bernhard F ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; ANTIOXIDANT; HEPARAN SULFATE; HEPARIN LYASE; LACTIC ACID; NITRIC OXIDE; PEROXYNITRITE; SCAVENGER; URIC ACID;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORONARY BLOOD VESSEL; CORONARY VASCULAR RESISTANCE; EDEMA; ELECTRON MICROSCOPY; ENDOLEAK; ENDOTHELIUM INJURY; ENZYMATIC DEGRADATION; EXTRAVASATION; GLYCOCALYX; GUINEA PIG; HEART MUSCLE ISCHEMIA; HEART PROTECTION; ISOLATED HEART; NONHUMAN; PRIORITY JOURNAL; REDOX STRESS; REPERFUSION; VASCULAR ENDOTHELIUM; ANIMAL; BLOOD; HEART MUSCLE REPERFUSION; MALE; METABOLISM; REPERFUSION INJURY; ULTRASTRUCTURE;

ADENINE NUCLEOTIDES; ANIMALS; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; FREE RADICAL SCAVENGERS; GLYCOCALYX; GUINEA PIGS; HEPARIN LYASE; HEPARITIN SULFATE; LACTIC ACID; MALE; MICROSCOPY, ELECTRON; MYOCARDIAL REPERFUSION; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE; URIC ACID;

EID: 45749148221     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/cc6913     Document Type: Article

References (37)

1. Reffelmann T Kloner RA The no-reflow phenomenon: A basic mechanism of myocardial ischemia and reperfusion Basic Res Cardiol 2006, 101:359-372. 10.1007/s00395-006-0615-2 16915531
2. 2+]i and microvessel permeability Am J Physiol 1997, 272:H176-H185 9038936
3. Kubes P Granger DN Nitric oxide modulates microvascular permeability Am J Physiol 1992, 262:H611-H615. 1539722
4. Berg van den BM Vink H Spaan JA The endothelial glycocalyx protects against myocardial edema Circ Res 2003, 92:592-594. 10.1161/ 01.RES.0000065917.53950.75 12637366
5. Bruegger D Jacob M Rehm M Loetsch M Welsch U Conzen P Becker BF Atrial natriuretic peptide induces shedding of the endothelial glycocalyx in the coronary vascular bed of guinea pig hearts Am J Physiol Heart Circ Physiol 2005, 289:H1993-H1999. 10.1152/ajpheart.00218.2005 15964925
6. Jacob M Bruegger D Rehm M Welsch U Conzen P Becker BF Contrasting effects of colloid and crystalloid resuscitation fluids on cardiac vascular permeability Anesthesiology 2006, 104:1223-1231. 10.1097/ 00000542-200606000-00018 16732094
7. Mulivor AW Lipowsky HH Inflammation- and ischemia-induced shedding of venular glycocalyx Am J Physiol Heart Circ Physiol 2004, 286:H1672-H1680. 10.1152/ajpheart.00832.2003 14704229
8. Kurzelewski M Czarnowska E Beresewicz A Superoxide-and nitric oxide-derived species mediate endothelial dysfunction, endothelial glycocalyx disruption, and enhanced neutrophil adhesion in the post-ischemic guinea-pig heart J Physiol Pharmacol 2005, 56:163-178. 15985700
9. Rehm M Bruegger D Christ F Conzen P Thiel M Jacob M Chappell D Stoeckelhuber M Welsch U Reichart B Peter K Becker BF Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia Circulation 2007, 116:1896-1906. 10.1161/CIRCULATIONAHA.106.684852 17923576
10. Reitsma S Slaaf DW Vink H van Zandvoort MA oude Egbrink MG The endothelial glycocalyx: Composition, functions, and visualization Pflugers Arch 2007, 454:345-359. 1915585 17256154 10.1007/ s00424-007-0212-8
11. Vink H Constantinescu AA Spaan JA Oxidized lipoproteins degrade the endothelial surface layer: Implications for platelet-endothelial cell adhesion Circulation 2000, 101:1500-1502. 10747340
12. Jacob M Rehm M Loetsch M Paul JO Bruegger D Welsch U Conzen P Becker BF The endothelial glycocalyx prefers albumin for evoking shear stress-induced, nitric oxide-mediated coronary dilatation J Vasc Res 2007, 44:435-443. 10.1159/000104871 17622736
13. Gilles S Zahler S Welsch U Sommerhoff CP Becker BF Release of TNF-alpha during myocardial reperfusion depends on oxidative stress and is prevented by mast cell stabilizers Cardiovasc Res 2003, 60:608-616. 10.1016/j.cardiores.2003.08.016 14659806
14. Chappell D Jacob M Rehm M Stoeckelhuber M Welsch U Conzen P Becker BF Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx Biol Chem 2008, 389:79-82. 10.1515/BC.2008.005 18095872
15. Institute of Laboratory Animal Resources Guide for the Care and Use of Laboratory Animals Washington, D.C.: National Academy Press 1996.
16. Rehm M Zahler S Lotsch M Welsch U Conzen P Jacob M Becker BF Endothelial glycocalyx as an additional barrier determining extravasation of 6% hydroxyethyl starch or 5% albumin solutions in the coronary vascular bed Anesthesiology 2004, 100:1211-1223. 10.1097/00000542-200405000-00025 15114220
17. Jacob M Bruegger D Rehm M Stoeckelhuber M Welsch U Conzen P Becker BF The endothelial glycocalyx affords compatibility of Starling's principle and high cardiac interstitial albumin levels Cardiovasc Res 2007, 73:575-586. 10.1016/j.cardiores.2006.11.021 17196565
18. Mobert J Becker BF Zahler S Gerlach E Hemodynamic effects of isoprostanes (8-iso-prostaglandin F2alpha and E2) in isolated guinea pig hearts J Cardiovasc Pharmacol 1997, 29:789-794. 10.1097/ 00005344-199706000-00012 9234660
19. Becker BF Reinholz N Ozcelik T Leipert B Gerlach E Uric acid as radical scavenger and antioxidant in the heart Pflugers Arch 1989, 415:127-135. 10.1007/BF00370582 2556684
20. Vogel J Sperandio M Pries AR Linderkamp O Gaethgens P Kuschinsky W Influence of the endothelial glycocalyx on cerebral blood flow in mice J Cereb Blood Flow Metab 2000, 20:1571-1578. 10.1097/ 00004647-200011000-00007 11083232
21. Woditsch I Schror K Prostacyclin rather than endogenous nitric oxide is a tissue protective factor in myocardial ischemia Am J Physiol 1992, 263:H1390-H1396. 1443194
22. Zahler S Kupatt C Becker BF ACE-inhibition attenuates cardiac cell damage and preserves release of NO in the postischemic heart Immunopharmacology 1999, 44:27-33. 10.1016/S0162-3109(99)00108-3 10604521
23. Wang P Zweier JL Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury J Biol Chem 1996, 271:29223-29230. 10.1074/jbc.271.46.29223 8910581
24. Kupatt C Zahler S Seligmann C Massoudy P Becker BF Gerlach E Nitric oxide mitigates leukocyte adhesion and vascular leak after myocardial ischemia J Mol Cell Cardiol 1996, 28:643-654. 10.1006/jmcc.1996.0060 9011647
25. Wienen W Jungling E Kammermeier H Enzyme release into the interstitial space of the isolated rat heart induced by changes in contractile performance Cardiovasc Res 1994, 28:1292-1298. 10.1093/cvr/28.8.1292 7954636
26. Beresewicz A Czarnowska E Maczewski M Ischemic preconditioning and superoxide dismutase protect against endothelial dysfunction and endothelium glycocalyx disruption in the postischemic guinea-pig hearts Mol Cell Biochem 1998, 186:87-97. 10.1023/A:1006867214448 9774189
27. Cohen MV Yang XM Downey JM Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies Cardiovasc Res 2006, 70:231-239. 10.1016/ j.cardiores.2005.10.021 16376869
28. Jones SP Bolli R The ubiquitous role of nitric oxide in cardioprotection J Mol Cell Cardiol 2006, 40:16-23. 10.1016/j.yjmcc.2005.09.011 16288777
29. Hillegass WB Dean NA Liao L Rhinehart RG Myers PR Treatment of no-reflow and impaired flow with the nitric oxide donor nitroprusside following percutaneous coronary interventions: Initial human clinical experience J Am Coll Cardiol 2001, 37:1335-1343. 10.1016/S0735-1097(01)01138-X 11300444
30. Massoudy P Zahler S Freyholdt T Henze R Barankay A Becker BF Braun SL Meisner H Sodium nitroprusside in patients with compromised left ventricular function undergoing coronary bypass: Reduction of cardiac proinflammatory substances J Thorac Cardiovasc Surg 2000, 119:566-574. 10.1016/S0022-5223(00)70138-3 10694618
31. Freyholdt T Massoudy P Zahler S Henze R Barankay A Becker BF Meisner H Beneficial effect of sodium nitroprusside after coronary artery bypass surgery: Pump function correlates inversely with cardiac release of proinflammatory cytokines J Cardiovasc Pharmacol 2003, 42:372-378. 10.1097/00005344-200309000-00008 12960682
32. Zucchi R Limbruno U Poddighe R Mariani M Ronca G Purine release from isolated rat heart: A new approach to the study of energy metabolism J Mol Cell Cardiol 1990, 22:815-826. 10.1016/0022-2828(90)90092-G 2231746
33. Dauber IM Lesnefsky EJ VanBenthuysen KM Weil JV Horwitz LD Reactive oxygen metabolite scavengers decrease functional coronary microvascular injury due to ischemia-reperfusion Am J Physiol 1991, 260:H42-H49. 1899542
34. Becker BF Towards the physiological function of uric acid Free Radic Biol Med 1993, 14:615-631. 10.1016/0891-5849(93)90143-I 8325534
35. Lundberg JO Weitzberg E Extrapulmonary effects of nitric oxide inhalation therapy: Time to consider new dosing regimes? Crit Care 2008, 12:406. 2374642 18304375 10.1186/cc6775
36. Chappell D Jacob M Hofmann-Kiefer K Bruegger D Rehm M Conzen P Welsch U Becker BF Hydrocortisone preserves the vascular barrier by protecting the endothelial glycocalyx Anesthesiology 2007, 107:776-784. 18073553
37. Liu X Huang Y Pokreisz P Vermeersch P Marsboom G Swinnen M Verbeken E Santos J Pellens M Gillijns H Werf Van de F Bloch KD Janssens S Nitric oxide inhalation improves microvascular flow and decreases infarction size after myocardial ischemia and reperfusion J Am Coll Cardiol 2007, 50:808-817. 10.1016/j.jacc.2007.04.069 17707188