Human red blood cells at work: Identification and visualization of erythrocytic eNOS activity in health and disease

Blood

Volumn 120, Issue 20, 2012, Pages 4229-4237

  Cortese Krott, Miriam M ^a   Rodriguez Mateos, Ana ^b   Sansone, Roberto ^a   Kuhnle, Gunter G C ^b   Thasian Sivarajah, Sivatharsini ^a   Krenz, Thomas ^a   Horn, Patrick ^a   Krisp, Christoph ^c   Wolters, Dirk ^c   Heiß, Christian ^a   Kröncke, Klaus Dietrich ^a   Hogg, Neil ^d   Feelisch, Martin ^e   Kelm, Malte ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF READING   (United Kingdom)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

^e UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4,5 DIAMINOFLUORESCEIN DIACETATE; ARGININE; CALCIUM ION; CALMODULIN; CITRULLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; OXYHEMOGLOBIN;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY DISEASE; CORRELATION ANALYSIS; ELECTROSPRAY MASS SPECTROMETRY; ENDOTHELIAL DYSFUNCTION; ENZYMATIC ASSAY; ENZYME ACTIVITY; ENZYME INHIBITION; ERYTHROCYTE; FLOW CYTOMETRY; FLUORESCENCE; HUMAN; IMMUNOPRECIPITATION; LASER MICROSCOPY; LIQUID CHROMATOGRAPHY; LYMPHOCYTE; MONOCYTE; NEUTROPHIL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; THROMBOCYTE;

EID: 84869786258     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-07-442277     Document Type: Article

References (49)

1. Anand IS, Kuskowski MA, Rector TS, et al. Anemia and change in hemoglobin over time related to mortality and morbidity in patients with chronic heart failure: results from Val-HeFT. Circulation. 2005;112(8):1121-1127. (Pubitemid 41216118)
2. Kulier A, Levin J, Moser R, et al. Impact of preoperative anemia on outcome in patients undergoing coronary artery bypass graft surgery. Circulation. 2007;116(5):471-479.
3. Sabatine MS, Morrow DA, Giugliano RP, et al. Association of hemoglobin levels with clinical outcomes in acute coronary syndromes. Circulation. 2005;111(16):2042-2049. (Pubitemid 40577898)
4. Moncada S, Palmer RMJ, Higgs EA. Nitric oxide, biology pathophysiology and pharmacology. Pharmacol Rev. 1991;43:109-142.
5. Cosby K, Partovi KS, Crawford JH, et al. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med. 2003;9(12):1498-1505. (Pubitemid 38004777)
6. Webb A, Milsom A, Rathod K, et al. Mechanisms underlying erythrocyte and endothelial nitrite reduction to nitric oxide in hypoxia: role for xanthine oxidoreductase and endothelial nitric oxide synthase. Circ Res. 2008;103(9):957-964.
7. Herold S. The outer-sphere oxidation of nitrosyliron(II)hemoglobin by peroxynitrite leads to the release of nitrogen monoxide. Inorg Chem. 2004;43(13):3783-3785.
8. Jia L, Bonaventura C, Bonaventura J, et al. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature. 1996;380:221-226. (Pubitemid 26090643)
9. Gladwin MT, Lancaster Jr JR, Freeman BA, et al. Nitric oxide's reactions with hemoglobin: a view through the SNO-storm. Nat Med. 2003;9:496-500. (Pubitemid 36597087)
10. Rassaf T, Bryan NS, Maloney RE, et al. NO adducts in mammalian red blood cells: too much or too little? Nat Med. 2003;9:481-482.
11. Nagababu E, Ramasamy S, Albernethy R, et al. Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction. J Biol Chem. 2003;278:46349-46356. (Pubitemid 37452205)
12. Zweier JL, Wang P, Samouilov A, et al. Enzyme-independent formation of nitric oxide in biological tissues. Nat Med. 1995;1(8):804-809.
13. Aamand R, Dalsgaard T, Jensen FB, et al. Generation of nitric oxide from nitrite by carbonic anhydrase: a possible link between metabolic activity and vasodilation. Am J Physiol Heart Circ Physiol. 2009;297(6):H2068-H2074.
14. Ellsworth ML, Forrester T, Ellis CG, et al. The erythrocyte as a regulator of vascular tone. Am J Physiol Heart Circ Physiol. 1995;269(6):H2155-H2161. (Pubitemid 26023234)
15. Chen LY, Mehta JL. Evidence for the presence of L-arginine-nitric oxide pathway in human red blood cells: relevance in the effects of red blood cells on platelet function. J Cardiovasc Pharmacol. 1998;32:57-61. (Pubitemid 28304694)
16. Kleinbongard P, Schulz R, Rassaf T, et al. Red blood cells express a functional endothelial nitric oxide synthase. Blood. 2006;107(7):2943-2951.
17. Sprague RS, Stephenson AH, Dimmitt RA, et al. Effect of L-NAME on pressure-flow relationships in isolated rabbit lungs: role of red blood cells. Am J Physiol. 1995;269:H1941-H1948. (Pubitemid 26023209)
18. Yang BC, Nichols WW, Mehta JL. Cardioprotective effects of red blood cells on ischemia and reperfusion injury in isolated rat heart: release of nitric oxide as a potential mechanism. J Cardiovasc Pharmacol Therapeut. 1996;1:297-305.
19. Deliconstantinos G, Villiotou V, Stavrides JC, et al. Nitric oxide and peroxynitrite production by human erythrocytes: a causative factor of toxic anemia in breast cancer patients. Anticancer Res. 1995;15:1435-1446.
20. Kang ES, Ford K, Grokulsky G, et al. Normal circulating adult human red blood cells contain inactive NOS proteins. J Lab Clin Med. 2000;135:444-451.
21. Mehta JL, Metha P, Li D. Nitric oxide synthase in adult red blood cells: vestige of an earlier age or a biologically active enzyme? J Lab Clin Med. 2000;135:430-431.
22. Böhmer A, Beckmann B, Sandmann J, et al. Doubts concerning functional endothelial nitric oxide synthase in human erythrocytes. Blood. 2012;119(5):1322-1323.
23. Bhattacharya S, Chakraborty PS, Basu RS, et al. Purification and properties of insulin-activated nitric oxide synthase from human erythrocyte membranes. Arch Physiol Biochem. 2001;109(5):441-449. (Pubitemid 34499186)
24. Mihov D, Vogel J, Gassmann M, et al. Erythropoietin activates nitric oxide synthase in murine erythrocytes. Am J Physiol Cell Physiol. 2009;297(2):C378-C388.
25. Jubelin BC, Gierman JL. Erythrocytes may synthesize their own nitric oxide. Am J Hypertens. 1996;9:1214-1219.
26. Heiss C, Lauer T, Dejam A, et al. Plasma nitroso compounds are decreased in patients with endothelial dysfunction. J Am Coll Cardiol. 2006;47:573-579. (Pubitemid 43170846)
27. Kleschyov AL, Mollnau H, Oelze M, et al. Spin trapping of vascular nitric oxide using colloid Fe(II)-diethyldithiocarbamate. Biochem Biophys Res Commun. 2000;275(2):672-677.
28. Rodriguez J, Specian V, Maloney R, et al. Performance of diamino fluorophores for the localization of sources and targets of nitric oxide. Free Radic Biol Med. 2005;38(3):356-368. (Pubitemid 40075577)
29. Giblett E, Anderson J. Electrophoretic analysis of polymorphic red cell enzymes. In: Red Cell Metabolism. Beutler E. Edinburgh, United Kingdom: Churchill Livingstone; 1986;108-123.
30. Cortese MM, Suschek CV, Wetzel W, et al. Zinc protects endothelial cells from hydrogen peroxide via Nrf2-dependent stimulation of glutathione biosynthesis. Free Radic Biol Med. 2008;44(12):2002-2012.
31. Kang D, Gho YS, Suh M, et al. Highly sensitive and fast protein detection with coomassie brilliant blue in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. I Bull Korean Chem Soc. 2002;23(11):1511-1512.
32. Bredt DS, Schmidt HHHW. The citrullin assay. In: Methods in Nitric Oxide Research. Feelisch M, Stamler JS, eds. Chichester, United Kingdom: John Wiley and Son; 1996;249-255.
33. Jourd'heuil D. Increased nitric oxide-dependent nitrosylation of 4,5-diaminofluorescein by oxidants: implications for the measurement of intracellular nitric oxide. Free Radic Biol Med. 2002;33(5):676-684. (Pubitemid 35245840)
34. Dejam A, Hunter CJ, Pelletier MM, et al. Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood. 2005;106(2):734-739. (Pubitemid 40981274)
35. Hong H, Sun J, Cai W. Multimodality imaging of nitric oxide and nitric oxide synthases. Free Radic Biol Med. 2009;47(6):684-698.
36. Nagano T, Yoshimura T. Bioimaging of nitric oxide. Chem Rev. 2002;102(4):1235-1270.
37. Nakatsubo N, Kojima H, Kikuchi K, et al. Direct evidence of nitric oxide production from bovine aortic endothelial cells using new fluorescence indicators: diaminofluoresceins. FEBS Lett. 1998;427(2):263-266. (Pubitemid 28225070)
38. Williams DL. Nitrosation reactions and the chemistry of nitric oxide. Elsevier; 2004.
39. Wardman P. Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med. 2007;43(7):995-1022. (Pubitemid 47302656)
40. Godber BLJ, Doel JJ, Sapkota GP, et al. Reduction of nitrite to nitric oxide catalyzed by xanthine oxidoreductase. J Biol Chem. 2000;275(11):7757-7763. (Pubitemid 30159680)
41. Lang KS, Lang PA, Bauer C, et al. Mechanisms of suicidal erythrocyte death. Cell Physiol Biochem. 2005;15(5):195-202. (Pubitemid 40868969)
42. Bor-Kucukatay M, Wenby RB, Meiselman HJ, et al. Effects of nitric oxide on red blood cell deformability. Am J Physiol Heart Circ Physiol. 2003;284:H1577-H1584. (Pubitemid 36460769)
43. Horn P, Cortese-Krott MM, Keymel S, et al. Nitric oxide influences red blood cell velocity independently of changes in the vascular tone. Free Radic Res. 2011;45(6):653-661.
44. Vitturi DA, Teng X, Toledo JC, et al. Regulation of nitrite transport in red blood cells by hemoglobin oxygen fractional saturation. Am J Physiol Heart Circ Physiol. 2009;296(5):H1398-H1407.
45. Crawford JH, Isbell TS, Huang Z, et al. Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood. 2006;107(2):566-574. (Pubitemid 43076380)
46. Rassaf T, Heiss C, Hendgen-Cotta U, et al. Plasma nitrite reserve and endothelial function in the human forearm circulation. Free Radic Biol Med. 2006;41(2):295-301. (Pubitemid 43928502)
47. Gkaliagkousi E, Ritter J, Ferro A. Platelet-derived nitric oxide signaling and regulation. Circ Res. 2007;101(7):654-662. (Pubitemid 47494096)
48. Gladwin MT, Schechter A, Kim-Shapiro DB, et al. The emerging biology of the nitrite anion in signaling, blood flow and hypoxic nitric oxide homeostasis. Nat Chem Biol. 2005;1:308-314.
49. Kim-Shapiro DB, Schechter AN, Gladwin MT. Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol. 2006;26(4):697-705. (Pubitemid 43732141)