Endothelium-derived nitric oxide production is increased by ATP released from red blood cells incubated with hydroxyurea

Nitric Oxide - Biology and Chemistry

Volumn 38, Issue 1, 2014, Pages 1-7

  Lockwood, Sarah Y ^a   Erkal, Jayda L ^a   Spence, Dana M ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Adenosine triphosphate; Endothelial cell; Hydroxyurea; Nitric oxide; Red blood cell; Sickle cell disease

Indexed keywords

ADENOSINE TRIPHOSPHATE; DIMETICONE; HYDROXYUREA; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; POLYCARBONATE; PURINERGIC P2Y RECEPTOR ANTAGONIST;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME RELEASE; ERYTHROCYTE; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; MICROFLUIDICS; MICROPLATE READER; PRIORITY JOURNAL; BIOSYNTHESIS; DOSE RESPONSE; DRUG EFFECTS; ENDOTHELIUM; METABOLISM; MICROFLUIDIC ANALYSIS; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM; ERYTHROCYTES; HUMANS; HYDROXYUREA; MICROFLUIDIC ANALYTICAL TECHNIQUES; NITRIC OXIDE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84896758506     PISSN: 10898603     EISSN: 10898611     Source Type: Journal    
DOI: 10.1016/j.niox.2014.02.003     Document Type: Article

References (57)

1. K.L. Hassell Population estimates of sickle cell disease in the U.S. Am. J. Prev. Med. 38 2010 S512 521
2. A. Ashley-Koch, Q. Yang, and R.S. Olney Sickle hemoglobin (HbS) allele and sickle cell disease: a HuGE review Am. J. Epidemiol. 151 2000 839 845
3. C.W. Young, and S. Hodas Hydroxyurea: inhibitory effect on DNA metabolism Science 146 1964 1172 1174
4. I.H. Krakoff, N.C. Brown, and P. Reichard Inhibition of ribonucleoside diphosphate reductase by hydroxyurea Cancer Res. 28 1968 1559 1565
5. W.N. Fishbein, and P.P. Carbone Hydroxyurea: mechanism of action Science 142 1963 1069 1070
6. S. Charache, G.J. Dover, R.D. Moore, S. Eckert, S.K. Ballas, M. Koshy, P.F. Milner, E.P. Orringer, G. Phillips Jr., and O.S. Platt et al. Hydroxyurea: effects on hemoglobin F production in patients with sickle cell anemia Blood 79 1992 2555 2565
7. A. Ferster, P. Tahriri, C. Vermylen, G. Sturbois, F. Corazza, P. Fondu, C. Devalck, M.F. Dresse, W. Feremans, K. Hunninck, M. Toppet, P. Philippet, C. Van Geet, and E. Sariban Five years of experience with hydroxyurea in children and young adults with sickle cell disease Blood 97 2001 3628 3632
8. J.S. Hankins, R.E. Ware, Z.R. Rogers, L.W. Wynn, P.A. Lane, J.P. Scott, and W.C. Wang Long-term hydroxyurea therapy for infants with sickle cell anemia: the HUSOFT extension study Blood 106 2005 2269 2275
9. S.A. Zimmerman, W.H. Schultz, J.S. Davis, C.V. Pickens, N.A. Mortier, T.A. Howard, and R.E. Ware Sustained long-term hematologic efficacy of hydroxyurea at maximum tolerated dose in children with sickle cell disease Blood 103 2004 2039 2045
10. T.R. Kinney, R.W. Helms, E.E. O'Branski, K. Ohene-Frempong, W. Wang, C. Daeschner, E. Vichinsky, R. Redding-Lallinger, B. Gee, O.S. Platt, and R.E. Ware Safety of hydroxyurea in children with sickle cell anemia: results of the HUG-KIDS study, a phase I/II trial. Pediatric hydroxyurea group Blood 94 1999 1550 1554
11. M.A. el-Hazmi, A.S. Warsy, A. al-Momen, and M. Harakati Hydroxyurea for the treatment of sickle cell disease Acta Haematol. 88 1992 170 174
12. K.R. Bridges, G.D. Barabino, C. Brugnara, M.R. Cho, G.W. Christoph, G. Dover, B.M. Ewenstein, D.E. Golan, C.R. Guttmann, J. Hofrichter, R.V. Mulkern, B. Zhang, and W.A. Eaton A multiparameter analysis of sickle erythrocytes in patients undergoing hydroxyurea therapy Blood 88 1996 4701 4710
13. M.H. Steinberg Hydroxyurea treatment for sickle cell disease ScientificWorldJournal 2 2002 1706 1728
14. R.E. Ware How I use hydroxyurea to treat young patients with sickle cell anemia Blood 115 2010 5300 5311
15. V.P. Cokic, B.B. Beleslin-Cokic, M. Tomic, S.S. Stojilkovic, C.T. Noguchi, and A.N. Schechter Hydroxyurea induces the eNOS-cGMP pathway in endothelial cells Blood 108 2006 184 191
16. R.E. Glover, E.D. Ivy, E.P. Orringer, H. Maeda, and R.P. Mason Detection of nitrosyl hemoglobin in venous blood in the treatment of sickle cell anemia with hydroxyurea Mol. Pharmacol. 55 1999 1006 1010
17. M. Nahavandi, M.Q. Wyche, E. Perlin, F. Tavakkoli, and O. Castro Nitric oxide metabolites in sickle cell anemia patients after oral administration of hydroxyurea; hemoglobinopathy Hematology 5 2000 335 339
18. J. Jiang, S.J. Jordan, D.P. Barr, M.R. Gunther, H. Maeda, and R.P. Mason In vivo production of nitric oxide in rats after administration of hydroxyurea Mol. Pharmacol. 52 1997 1081 1086
19. J. Huang, M. Yakubu, D.B. Kim-Shapiro, and S.B. King Rat liver-mediated metabolism of hydroxyurea to nitric oxide Free Radic. Biol. Med. 40 2006 1675 1681
20. S.B. King The nitric oxide producing reactions of hydroxyurea Curr. Med. Chem. 10 2003 437 452
21. S.B. King Nitric oxide production from hydroxyurea Free Radic. Biol. Med. 37 2004 737 744
22. L.J. Ignarro, G.M. Buga, K.S. Wood, R.E. Byrns, and G. Chaudhuri Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide Proc. Natl. Acad. Sci. USA 84 1987 9265 9269
23. M. Raththagala, W. Karunarathne, M. Kryziniak, J. McCracken, and D.M. Spence Hydroxyurea stimulates the release of ATP from rabbit erythrocytes through an increase in calcium and nitric oxide production Eur. J. Pharmacol. 645 2010 32 38
24. A. Miseta, P. Bogner, E. Berenyi, M. Kellermayer, C. Galambos, D.N. Wheatley, and I.L. Cameron Relationship between cellular ATP, potassium, sodium and magnesium concentrations in mammalian and avian erythrocytes Biochim. Biophys. Acta 1175 1993 133 139
25. R.S. Sprague, M.L. Ellsworth, A.H. Stephenson, and A.J. Lonigro ATP: the red blood cell link to NO and local control of the pulmonary circulation Am. J. Physiol. 271 1996 H2717 2722
26. G.R. Bergfeld, and T. Forrester Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia Cardiovasc. Res. 26 1992 40 47
27. J.A. Meyer, W. Subasinghe, A.A. Sima, Z. Keltner, G.E. Reid, D. Daleke, and D.M. Spence Zinc-activated C-peptide resistance to the type 2 diabetic erythrocyte is associated with hyperglycemia-induced phosphatidylserine externalization and reversed by metformin Mol. BioSyst. 5 2009 1157 1162
28. G. Burnstock, and C. Kennedy A dual function for adenosine 5′-triphosphate in the regulation of vascular tone. Excitatory cotransmitter with noradrenaline from perivascular nerves and locally released inhibitory intravascular agent Circ. Res. 58 1986 319 330
29. M.P. Abbracchio, and G. Burnstock Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol. Ther. 64 1994 445 475
30. B.B. Fredholm, M.P. Abbracchio, G. Burnstock, J.W. Daly, T.K. Harden, K.A. Jacobson, P. Leff, and M. Williams Nomenclature and classification of purinoceptors Pharmacol. Rev. 46 1994 143 156
31. S. Motte, D. Communi, S. Pirotton, and J.M. Boeynaems Involvement of multiple receptors in the actions of extracellular ATP: the example of vascular endothelial cells Int. J. Biochem. Cell Biol. 27 1995 1 7
32. R.G. Bogle, S.B. Coade, S. Moncada, J.D. Pearson, and G.E. Mann Bradykinin and ATP stimulate l-arginine uptake and nitric oxide release in vascular endothelial cells Biochem. Biophys. Res. Commun. 180 1991 926 932
33. R. Busse, A. Ogilvie, and U. Pohl Vasomotor activity of diadenosine triphosphate and diadenosine tetraphosphate in isolated arteries Am. J. Physiol. 254 1988 H828 832
34. J.G. De Mey, M. Claeys, and P.M. Vanhoutte Endothelium-dependent inhibitory effects of acetylcholine, adenosine triphosphate, thrombin and arachidonic acid in the canine femoral artery J. Pharmacol. Exp. Ther. 222 1982 166 173
35. D.H. Kotsis, and D.M. Spence Detection of ATP-induced nitric oxide in a biomimetic circulatory vessel containing an immobilized endothelium Anal. Chem. 75 2003 145 151
36. D.M. Spence, N.J. Torrence, M.L. Kovarik, and R.S. Martin Amperometric determination of nitric oxide derived from pulmonary artery endothelial cells immobilized in a microchip channel Analyst 129 2004 995 1000
37. T. D'Amico Oblak, P. Root, and D.M. Spence Fluorescence monitoring of ATP-stimulated, endothelium-derived nitric oxide production in channels of a poly(dimethylsiloxane)-based microfluidic device Anal. Chem. 78 2006 3193 3197
38. S.T. Halpin, and D.M. Spence Direct plate-reader measurement of nitric oxide released from hypoxic erythrocytes flowing through a microfluidic device Anal. Chem. 82 2010 7492 7497 (Washington, DC, U.S.)
39. L.I. Genes, N. Tolan, M.K. Hulvey, R.S. Martin, and D.M. Spence Addressing a vascular endothelium array with blood components using underlying microfluidic channels Lab Chip 7 2007 1256 1259
40. C.J. Ku, T. D'Amico Oblak, and D.M. Spence Interactions between multiple cell types in parallel microfluidic channels: monitoring platelet adhesion to an endothelium in the presence of an anti-adhesion drug Anal. Chem. 80 2008 7543 7548
41. S. Letourneau, L. Hernandez, A.N. Faris, and D.M. Spence Evaluating the effects of estradiol on endothelial nitric oxide stimulated by erythrocyte-derived ATP using a microfluidic approach Anal. Bioanal. Chem. 397 2010 3369 3375
42. P.A. Vogel, S.T. Halpin, R.S. Martin, and D.M. Spence Microfluidic transendothelial electrical resistance measurement device that enables blood flow and postgrowth experiments Anal. Chem. 83 2011 4296 4301
43. A.K. Price, D.J. Fischer, R.S. Martin, and D.M. Spence Deformation-induced release of ATP from erythrocytes in a poly(dimethylsiloxane) -based microchip with channels that mimic resistance vessels Anal. Chem. 76 2004 4849 4855
44. A.K. Price, R.S. Martin, and D.M. Spence Monitoring erythrocytes in a microchip channel that narrows uniformly: towards an improved microfluidic-based mimic of the microcirculation J. Chromatogr. A 1111 2006 220 227
45. D.C. Duffy, J.C. McDonald, O.J. Schueller, and G.M. Whitesides Rapid prototyping of microfluidic systems in poly(dimethylsiloxane) Anal. Chem. 70 1998 4974 4984
46. A.S. Popel, and P.C. Johnson Microcirculation and hemorheology Annu. Rev. Fluid Mech. 37 2005 43 69
47. T.M. Fischer, C.W. Haest, M. Stohr, D. Kamp, and B. Deuticke Selective alteration of erythrocyte deformabiliby by SH-reagents: evidence for an involvement of spectrin in membrane shear elasticity Biochim. Biophys. Acta 510 1978 270 282
48. B.D. Schultz, A.D. DeRoos, C.J. Venglarik, A.K. Singh, R.A. Frizzell, and R.J. Bridges Glibenclamide blockade of CFTR chloride channels Am. J. Physiol. Lung Cell. Mol. Physiol. 271 1996 L192 L200
49. F.A. Ferrone, J. Hofrichter, and W.A. Eaton Kinetics of sickle hemoglobin polymerization. II. A double nucleation mechanism J. Mol. Biol. 183 1985 611 631
50. D.J. Singel, and J.S. Stamler Chemical physiology of blood flow regulation by red blood cells: the role of nitric oxide and S-nitrosohemoglobin Annu. Rev. Physiol. 67 2005 99 145
51. J.J. Olearczyk, A.H. Stephenson, A.J. Lonigro, and R.S. Sprague NO inhibits signal transduction pathway for ATP release from erythrocytes via its action on heterotrimeric G protein Gi Am. J. Physiol. Heart Circ. Physiol. 287 2004 H748 754
52. J.W. Park, B. Piknova, P.L. Huang, C.T. Noguchi, and A.N. Schechter Effect of blood nitrite and nitrate levels on murine platelet function PLoS ONE 8 2013 e55699
53. J.J. Olearczyk, M.L. Ellsworth, A.H. Stephenson, A.J. Lonigro, and R.S. Sprague Nitric oxide inhibits ATP release from erythrocytes J. Pharmacol. Exp. Ther. 309 2004 1079 1084
54. P. Kleinbongard, R. Schulz, T. Rassaf, T. Lauer, A. Dejam, T. Jax, I. Kumara, P. Gharini, S. Kabanova, B. Ozuyaman, H.G. Schnurch, A. Godecke, A.A. Weber, M. Robenek, H. Robenek, W. Bloch, P. Rosen, and M. Kelm Red blood cells express a functional endothelial nitric oxide synthase Blood 107 2006 2943 2951
55. B. Ozuyaman, M. Grau, M. Kelm, M.W. Merx, and P. Kleinbongard RBC NOS: regulatory mechanisms and therapeutic aspects Trends Mol. Med. 14 2008 314 322
56. D. Starzyk, R. Korbut, and R.J. Gryglewski Effects of nitric oxide and prostacyclin on deformability and aggregability of red blood cells of rats ex vivo and in vitro J. Physiol. Pharmacol. 50 1999 629 637
57. M. Bor-Kucukatay, R.B. Wenby, H.J. Meiselman, and O.K. Baskurt Effects of nitric oxide on red blood cell deformability Am. J. Physiol. Heart Circ. Physiol. 284 2003 H1577 1584