Redox-dependent impairment of vascular function in sickle cell disease

Free Radical Biology and Medicine

Volumn 43, Issue 11, 2007, Pages 1469-1483

  Aslan, Mutay ^a   Freeman, Bruce A ^b  

^a AKDENIZ UNIVERSITY   (Turkey)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelium; Free radicals; Nitric oxide; Sickle cell disease

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ACENOCOUMAROL; ACETYLSALICYLIC ACID; ALBUMIN; ALPHA TOCOPHEROL; ARGININE; CHONDROITIN SULFATE; DEXTRAN SULFATE; DIPYRIDAMOLE; HEPARIN; HYDROXYUREA; NITRIC OXIDE; PEPTIDE; REACTIVE OXYGEN METABOLITE; SALAZOSULFAPYRIDINE; SILDENAFIL; TBC 772; TICLOPIDINE; UNCLASSIFIED DRUG; WARFARIN;

BIOAVAILABILITY; BLEEDING; BLOOD CLOTTING; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG MECHANISM; DRUG MEGADOSE; ERYTHROCYTE ADHESIVENESS; HUMAN; LOW DRUG DOSE; NONHUMAN; OXIDATION REDUCTION REACTION; POLYMERIZATION; PRIORITY JOURNAL; PULMONARY HYPERTENSION; REPERFUSION INJURY; REVIEW; SICKLE CELL ANEMIA; TISSUE INJURY; VITAMIN SUPPLEMENTATION;

ANEMIA, SICKLE CELL; ANTI-INFLAMMATORY AGENTS; ANTICOAGULANTS; ANTIOXIDANTS; BIOLOGICAL AVAILABILITY; BLOOD COAGULATION; CELL ADHESION; ENDOTHELIUM, VASCULAR; ERYTHROCYTES; HEMOGLOBIN, SICKLE; HEMOLYSIS; HUMANS; HYDROXYUREA; LEUKOCYTES; NITRIC OXIDE; OXIDATION-REDUCTION; REPERFUSION INJURY;

EID: 35348950927     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.08.014     Document Type: Review

References (181)

1. Pauling L., Itano H.A., Singer S.J., and Wells I.C. Sickle cell anemia: a molecular disease. Science 110 (1949) 543-548
2. Ingram V.M. Gene mutations in human haemoglobin: the chemical difference between normal and sickle cell haemoglobin. Nature 180 (1957) 326-328
3. Dykes G., Crepeau R.H., and Edelstein S.J. Three-dimensional reconstruction of the fibres of sickle cell haemoglobin. Nature 272 (1978) 506-510
4. Eaton W.A., and Hofrichter J. Sickle cell hemoglobin polymerization. Adv. Protein Chem. 40 (1990) 63-279
5. In: Burtis C.A., and Ashwood E.R. (Eds). Teitz fundamentals of clinical chemistry. 4th ed. (1996), Saunders, Philadelphia
6. Hebbel R.P., Osarogiagbon R., and Kaul D. The endothelial biology of sickle cell disease: inflammation and a chronic vasculopathy. Microcirculation 11 (2004) 129-151
7. Hebbel R.P., Boogaerts M.A., Eaton J.W., and Steinberg M.H. Erythrocyte adherence to endothelium in sickle-cell anemia: a possible determinant of disease severity. N. Engl. J. Med. 302 (1980) 992-995
8. Smith B.D., and La Celle P.L. Erythrocyte-endothelial cell adherence in sickle cell disorders. Blood 68 (1986) 1050-1054
9. Hebbel R.P. Adhesive interactions of sickle erythrocytes with endothelium. J. Clin. Invest. 100 (1997) S83-S86
10. Chiang E.Y., and Frenette P.S. Sickle cell vaso-occlusion. Hematol. Oncol. Clin. North Am. 19 (2005) 771-784
11. Udani M., Zen Q., Cottman M., Leonard N., Jefferson S., Daymont C., Truskey G., and Telen M.J. Basal cell adhesion molecule/lutheran protein: the receptor critical for sickle cell adhesion to laminin. J. Clin. Invest. 101 (1998) 2550-2558
12. Parsons S.F., Spring F.A., Chasis J.A., and Anstee D.J. Erythroid cell adhesion molecules Lutheran and LW in health and disease. Baillieres Best Pract. Res. Clin. Haematol. 12 (1999) 729-745
13. Solovey A., Lin Y., Browne P., Choong S., Wayner E., and Hebbel R.P. Circulating activated endothelial cells in sickle cell anemia. N. Engl. J. Med. 337 (1997) 1584-1590
14. Bolarin D.M., Swerdlow P., Wallace A.M., and Littsey L. Serum concentrations of laminin P1 and aminoterminal propeptide of type III procollagen in sickle cell disease. Haematologia (Budapest) 29 (1998) 51-58
15. Hines P.C., Zen Q., Burney S.N., Shea D.A., Ataga K.I., Orringer E.P., Telen M.J., and Parise L.V. Novel epinephrine and cyclic AMP-mediated activation of BCAM/Lu-dependent sickle (SS) RBC adhesion. Blood 101 (2003) 3281-3287
16. Delahunty M., Zennadi R., and Telen M.J. LW protein: a promiscuous integrin receptor activated by adrenergic signaling. Transfus. Clin. Biol. 13 (2006) 44-49
17. Hermand P., Huet M., Callebaut I., Gane P., Ihanus E., Gahmberg C.G., Cartron J.P., and Bailly P. Binding sites of leukocyte beta 2 integrins (LFA-1, Mac-1) on the human ICAM-4/LW blood group protein. J. Biol. Chem. 275 (2000) 26002-26010
18. Hermand P., Gane P., Huet M., Jallu V., Kaplan C., Sonneborn H.H., Cartron J.P., and Bailly P. Red cell ICAM-4 is a novel ligand for platelet-activated alpha IIb beta 3 integrin. J. Biol. Chem. 278 (2003) 4892-4898
19. Zennadi R., Hines P.C., De Castro L.M., Cartron J.P., Parise L.V., and Telen M.J. Epinephrine acts through erythroid signaling pathways to activate sickle cell adhesion to endothelium via LW-alphavbeta3 interactions. Blood 104 (2004) 3774-3781
20. Joneckis C.C., Ackley R.L., Orringer E.P., Wayner E.A., and Parise L.V. Integrin alpha 4 beta 1 and glycoprotein IV (CD36) are expressed on circulating reticulocytes in sickle cell anemia. Blood 82 (1993) 3548-3555
21. Swerlick R.A., Eckman J.R., Kumar A., Jeitler M., and Wick T.M. Alpha 4 beta 1-integrin expression on sickle reticulocytes: vascular cell adhesion molecule-1-dependent binding to endothelium. Blood 82 (1993) 1891-1899
22. + sickle reticulocytes to endothelial cells. Blood 88 (1992) 2634-2642
23. Brittain H.A., Eckman J.R., and Wick T.M. Sickle erythrocyte adherence to large vessel and microvascular endothelium under physiologic flow is quantitatively different. J. Lab. Clin. Med. 120 (1992) 538-545
24. Jaffe E.A., Ruggiero J.T., Leung L.K., Doyle M.J., McKeown-Longo P.J., and Mosher D.F. Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix. Proc. Natl. Acad. Sci. USA 80 (1983) 998-1002
25. Brittain H.A., Eckman J.R., Swerlick R.A., Howard R.J., and Wick T.M. Thrombospondin from activated platelets promotes sickle erythrocyte adherence to human microvascular endothelium under physiologic flow: a potential role for platelet activation in sickle cell vaso-occlusion. Blood 81 (1993) 2137-2143
26. Browne P.V., Mosher D.F., Steinberg M.H., and Hebbel R.P. Disturbance of plasma and platelet thrombospondin levels in sickle cell disease. Am. J. Hematol. 51 (1996) 296-301
27. Murphy-Ullrich J.E., and Mosher D.F. Interactions of thrombospondin with endothelial cells: receptor-mediated binding and degradation. J. Cell Biol. 105 (1987) 1603-1611
28. Lee K., Gane P., Roudot-Thoraval F., Godeau B., Bachir D., Bernaudin F., Cartron J.P., Galacteros F., and Bierling P. The nonexpression of CD36 on reticulocytes and mature red blood cells does not modify the clinical course of patients with sickle cell anemia. Blood 98 (2001) 966-971
29. Brittain J.E., Mlinar K.J., Anderson C.S., Orringer E.P., and Parise L.V. Integrin-associated protein is an adhesion receptor on sickle red blood cells for immobilized thrombospondin. Blood 97 (2001) 2159-2164
30. Brittain J.E., Mlinar K.J., Anderson C.S., Orringer E.P., and Parise L.V. Activation of sickle red blood cell adhesion via integrin-associated protein/CD47-induced signal transduction. J. Clin. Invest. 107 (2001) 1555-1562
31. Brittain J.E., Han J., Ataga K.I., Orringer E.P., and Parise L.V. Mechanism of CD47-induced alpha4beta1 integrin activation and adhesion in sickle reticulocytes. J. Biol. Chem. 279 (2004) 42393-42402
32. Nachman R., Levine R., and Jaffe E.A. Synthesis of factor VIII antigen by cultured guinea pig megakaryocytes. J. Clin. Invest. 60 (1977) 914-921
33. Jaffe E.A., Hoyer L.W., and Nachman R.L. Synthesis of antihemophilic factor antigen by cultured human endothelial cells. J. Clin. Invest. 52 (1973) 2757-2764
34. Wick T.M., Moake J.L., Udden M.M., Eskin S.G., Sears D.A., and McIntire L.V. Unusually large von Willebrand factor multimers increase adhesion of sickle erythrocytes to human endothelial cells under controlled flow. J. Clin. Invest. 80 (1987) 905-910
35. Kaul D.K., Nagel R.L., Chen D., and Tsai H.M. Sickle erythrocyte-endothelial interactions in microcirculation: the role of von Willebrand factor and implications for vasoocclusion. Blood 81 (1993) 2429-2438
36. Wick T.M., Moake J.L., Udden M.M., and McIntire L.V. Unusually large von Willebrand factor multimers preferentially promote young sickle and nonsickle erythrocyte adhesion to endothelial cells. Am. J. Hematol. 42 (1993) 284-292
37. Kaul D.K., Fabry M.E., Windisch P., Baez S., and Nagel R.L. Erythrocytes in sickle cell anemia are heterogeneous in their rheological and hemodynamic characteristics. J. Clin. Invest. 72 (1983) 22-31
38. Kaul D.K., Fabry M.E., and Nagel R.L. Microvascular sites and characteristics of sickle cell adhesion to vascular endothelium in shear flow conditions: pathophysiological implications. Proc. Natl. Acad. Sci. USA 86 (1989) 3356-3360
39. Fabry M.E., Sengupta A., Suzuka S.M., Costantini F., Rubin E.M., Hofrichter J., Christoph G., Manci E., Culberson D., Factor S.M., and Nagel R.L. A second generation transgenic mouse model expressing both hemoglobin S (HbS) and HbS-Antilles results in increased phenotypic severity. Blood 86 (1995) 2419-2428
40. Kaul D.K., Fabry M.E., Costantini F., Rubin E.M., and Nagel R.L. In vivo demonstration of red cell-endothelial interaction, sickling and altered microvascular response to oxygen in the sickle transgenic mouse. J. Clin. Invest. 96 (1995) 2845-2853
41. Kaul D.K., Fabry M.E., and Nagel R.L. The pathophysiology of vascular obstruction in the sickle syndromes. Blood Rev. 10 (1996) 29-44
42. Platt O.S., Brambilla D.J., Rosse W.F., Milner P.F., Castro O., Steinberg M.H., and Klug P.P. Mortality in sickle cell disease: life expectancy and risk factors for early death. N. Engl. J. Med. 330 (1994) 1639-1644
43. Castro O., Brambilla D.J., Thorington B., Reindorf C.A., Scott R.B., Gillette P., Vera J.C., and Levy P.S. The acute chest syndrome in sickle cell disease: incidence and risk factors. The Cooperative Study of Sickle Cell Disease. Blood 84 (1994) 643-649
44. Kinney T.R., Sleeper L.A., Wang W.C., Zimmerman R.A., Pegelow C.H., Ohene-Frempong K., Wethers D.L., Bello J.A., Vichinsky E.P., Moser F.G., Gallagher D.M., DeBaun M.R., Platt O.S., and Miller S.T. Silent cerebral infarcts in sickle cell anemia: a risk factor analysis. The Cooperative Study of Sickle Cell Disease. Pediatrics 103 (1999) 640-645
45. Adler B.K., Salzman D.E., Carabasi M.H., Vaughan W.P., Reddy V.V., and Prchal J.T. Fatal sickle cell crisis after granulocyte colony-stimulating factor administration. Blood 97 (2001) 3313-3314
46. + thalassemia. Blood 97 (2001) 3998-3999
47. Turhan A., Weiss L.A., Mohandas N., Coller B.S., and Frenette P.S. Primary role for adherent leukocytes in sickle cell vascular occlusion: a new paradigm. Proc. Natl. Acad. Sci. USA 99 (2002) 3047-3051
48. House S.D., and Lipowsky H.H. Leukocyte-endothelium adhesion: microhemodynamics in mesentery of the cat. Microvasc. Res. 34 (1987) 363-379
49. Perry M.A., and Granger D.N. Role of CD11/CD18 in shear rate-dependent leukocyte-endothelial cell interactions in cat mesenteric venules. J. Clin. Invest. 87 (1991) 1798-1804
50. Sumagin R., and Sarelius I.H. TNF-alpha activation of arterioles and venules alters distribution and levels of ICAM-1 and affects leukocyte-endothelial cell interactions. Am. J. Physiol. Heart Circ. Physiol. 291 (2006) H2116-H2125
51. Middleton J., Patterson A.M., Gardner L., Schmutz C., and Ashton B.A. Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 100 (2002) 3853-3860
52. Tan P., Luscinskas F.W., and Homer-Vanniasinkam S. Cellular and molecular mechanisms of inflammation and thrombosis. Eur. J. Vasc. Endovasc. Surg. 17 (1999) 373-389
53. Francis Jr. R.B., and Haywood L.J. Elevated immunoreactive tumor necrosis factor and interleukin-1 in sickle cell disease. J. Natl. Med. Assoc. 84 (1992) 611-615
54. Makis A.C., Hatzimichael E.C., Mavridis A., and Bourantas K.L. Alpha-2-macroglobulin and interleukin-6 levels in steady-state sickle cell disease patients. Acta Haematol. 104 (2000) 164-168
55. Akohoue S.A., Shankar S., Milne G.L., Morrow J., Chen K.Y., Ajayi W.U., and Buchowski M.S. Energy expenditure, inflammation, and oxidative stress in steady-state adolescents with sickle cell anemia. Pediatr. Res. 61 (2007) 233-238
56. Michaels L.A., Ohene-Frempong K., Zhao H., and Douglas S.D. Serum levels of substance P are elevated in patients with sickle cell disease and increase further during vaso-occlusive crisis. Blood 92 (1998) 3148-3151
57. Belcher J.D., Marker P.H., Weber J.P., Hebbel R.P., and Vercellotti G.M. Activated monocytes in sickle cell disease: potential role in the activation of vascular endothelium and vaso-occlusion. Blood 96 (2000) 2451-2459
58. Hedo C.C., Aken'ova Y.A., Okpala I.E., Durojaiye A.O., and Salimonu L.S. Acute phase reactants and severity of homozygous sickle cell disease. J. Intern. Med. 233 (1993) 467-470
59. Middleton J., Neil S., Wintle J., Clark-Lewis I., Moore H., Lam C., Auer M., Hub E., and Rot A. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91 (1997) 385-395
60. Wang L., Fuster M., Sriramarao P., and Esko J.D. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat. Immunol. 6 (2005) 902-910
61. Akerley III W.L., Guyre P.M., and Davis B.H. Neutrophil activation through high-affinity Fc gamma receptor using a monomeric antibody with unique properties. Blood 77 (1991) 607-615
62. Fadlon E., Vordermeier S., Pearson T.C., Mire-Sluis A.R., Dumonde D.C., Phillips J., Fishlock K., and Brown K.A. Blood polymorphonuclear leukocytes from the majority of sickle cell patients in the crisis phase of the disease show enhanced adhesion to vascular endothelium and increased expression of CD64. Blood 91 (1998) 266-274
63. Lard L.R., Mul F.P., de Haas M., Roos D., and Duits A.J. Neutrophil activation in sickle cell disease. J. Leukocyte Biol. 66 (1999) 411-415
64. Ley K., Gaehtgens P., Fennie C., Singer M.S., Lasky L.A., and Rosen S.D. Lectin-like cell adhesion molecule 1 mediates leukocyte rolling in mesenteric venules in vivo. Blood 77 (1991) 2553-2555
65. de Haas M., Kerst J.M., van der Schoot C.E., Calafat J., Hack C.E., Nuijens J.H., Roos D., van Oers R.H., and von dem Borne A.E. Granulocyte colony-stimulating factor administration to healthy volunteers: analysis of the immediate activating effects on circulating neutrophils. Blood 84 (1994) 3885-3894
66. McEver R.P., and Cummings R.D. Cell adhesion in vascular biology: role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest. 100 (1997) 485-491
67. Bevilacqua M.P. Endothelial-leukocyte adhesion molecules. Annu. Rev. Immunol. 11 (1993) 767-804
68. Kaul D.K., and Hebbel R.P. Hypoxia/reoxygenation causes inflammatory response in transgenic sickle mice but not in normal mice. J. Clin. Invest. 106 (2000) 411-420
69. Wood K., Russell J., Hebbel R.P., and Granger D.N. Differential expression of E-and P-selectin in the microvasculature of sickle cell transgenic mice. Microcirculation 11 (2004) 377-385
70. Key N.S., Slungaard A., Dandelet L., Nelson S.C., Moertel C., Styles L.A., Kuypers F.A., and Bach R.R. Whole blood tissue factor procoagulant activity is elevated in patients with sickle cell disease. Blood 91 (1998) 4216-4223
71. Eilertsen K.E., and Osterud B. Tissue factor: (patho)physiology and cellular biology. Blood Coagul. Fibrinolysis 7 (2004) 521-538
72. Solovey A., Gui L., Key N.S., and Hebbel R.P. Tissue factor expression by endothelial cells in sickle cell anemia. J. Clin. Invest. 101 (1998) 1899-1904
73. Shet A.S., Aras O., Gupta K., Hass M.J., Rausch D.J., Saba N., Koopmeiners L., Key N.S., and Hebbel R.P. Sickle blood contains tissue factor-positive microparticles derived from endothelial cells and monocytes. Blood 102 (2003) 2678-2683
74. Solovey A., Kollander R., Shet A., Milbauer L.C., Choong S., Panoskaltsis-Mortari A., Blazar B.R., Kelm Jr. R.J., and Hebbel R.P. Endothelial cell expression of tissue factor in sickle mice is augmented by hypoxia/reoxygenation and inhibited by lovastatin. Blood 104 (2004) 840-846
75. Krishnaswamy S. The interaction of human factor VIIa with tissue factor. J. Biol. Chem. 267 (1992) 23696-23706
76. Franck P.F., Bevers E.M., Lubin B.H., Comfurius P., Chiu D.T., Op den Kamp J.A., Zwaal R.F., van Deenen L.L., and Roelofsen B. Uncoupling of the membrane skeleton from the lipid bilayer: the cause of accelerated phospholipid flip-flop leading to an enhanced procoagulant activity of sickled cells. J. Clin. Invest. 75 (1985) 183-190
77. Seigneuret M., and Devaux P.F. ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. USA 81 (1984) 3751-3755
78. de Jong K., Larkin S.K., Styles L.A., Bookchin R.M., and Kuypers F.A. Characterization of the phosphatidylserine-exposing subpopulation of sickle cells. Blood 98 (2001) 860-867
79. Monroe D.M., Hoffman M., and Roberts H.R. Platelets and thrombin generation. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 1381-1389
80. Tomer A., Harker L.A., Kasey S., and Eckman J.R. Thrombogenesis in sickle cell disease. J. Lab. Clin. Med. 137 (2001) 398-407
81. Leslie J., Langler D., Serjeant G.R., Serjeant B.E., Desai P., and Gordon Y.B. Coagulation changes during the steady state in homozygous sickle-cell disease in Jamaica. Br. J. Haematol. 30 (1975) 159-166
82. Nesheim M. Fibrinolysis and the plasma carboxypeptidase. Curr. Opin. Hematol. 5 (1998) 309-313
83. Esmon C.T. Regulation of blood coagulation. Biochim. Biophys. Acta 1477 (2000) 349-360
84. Westerman M.P., Green D., Gilman-Sachs A., Beaman K., Freels S., Boggio L., Allen S., Zuckerman L., Schlegel R., and Williamson P. Antiphospholipid antibodies, proteins C and S, and coagulation changes in sickle cell disease. J. Lab. Clin. Med. 134 (1999) 352-362
85. Wright J.G., Malia R., Cooper P., Thomas P., Preston F.E., and Serjeant G.R. Protein C and protein S in homozygous sickle cell disease: does hepatic dysfunction contribute to low levels?. Br. J. Haematol. 98 (1997) 627-631
86. Tam D.A. Protein C and protein S activity in sickle cell disease and stroke. J. Child Neurol. 12 (1997) 19-21
87. Ruggeri Z.M. Platelets in atherothrombosis. Nat. Med. 8 (2002) 1227-1234
88. Furie B., and Furie B.C. Role of platelet P-selectin and microparticle PSGL-1 in thrombus formation. Trends Mol. Med. 10 (2004) 171-178
89. Inwald D.P., Kirkham F.J., Peters M.J., Lane R., Wade A., Evans J.P., and Klein N.J. Platelet and leucocyte activation in childhood sickle cell disease: association with nocturnal hypoxaemia. Br. J. Haematol. 111 (2000) 474-481
90. Vandendries E.R., Furie B.C., and Furie B. Role of P-selectin and PSGL-1 in coagulation and thrombosis. Thromb. Haemostasis 92 (2004) 459-466
91. Wun T., Cordoba M., Rangaswami A., Cheung A.W., and Paglieroni T. Activated monocytes and platelet-monocyte aggregates in patients with sickle cell disease. Clin. Lab. Haematol. 24 (2002) 81-88
92. Aslan M., and Freeman B.A. Oxidant-mediated impairment of nitric oxide signaling in sickle cell disease-Mechanisms and consequences. Cell. Mol. Biol. (Noisy-le-grand) 50 (2004) 95-105
93. Mayer B., and Hemmens B. Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem. Sci. 22 (1997) 477-481
94. Moncada S., and Higgs A. The l-arginine-nitric oxide pathway. N. Engl. J. Med. 329 (1993) 2002-2012
95. Lincoln T.M., and Cornwell T.L. Intracellular cyclic GMP receptor proteins. FASEB J. 7 (1993) 328-338
96. Radomski M.W., Palmer R.M., and Moncada S. The role of nitric oxide and cGMP in platelet adhesion to vascular endothelium. Biochem. Biophys. Res. Commun. 148 (1987) 1482
97. Loscalzo J. Nitric oxide insufficiency, platelet activation, and arterial thrombosis. Circ. Res. 88 (2001) 756-762
98. De Caterina R., Libby P., Peng H.B., Thannickal V.J., Rajavashisth T.B., Gimbrone Jr. M.A., Shin W.S., and Liao J.K. Nitric oxide decreases cytokine-induced endothelial activation: nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J. Clin. Invest. 96 (1995) 60-68
99. Peng H.B., Libby P., and Liao J.K. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J. Biol. Chem. 270 (1995) 14214-14219
100. Abraham E. NF-kappaB activation. Crit. Care Med. 28 (2000) N100-N104
101. Khan B.V., Harrison D.G., Olbrych M.T., Alexander R.W., and Medford R.M. Nitric oxide regulates vascular cell adhesion molecule 1 gene expression and redox-sensitive transcriptional events in human vascular endothelial cells. Proc. Natl. Acad. Sci. USA 93 (1996) 9114-9119
102. Fujita H., Morita I., and Murota S. A possible mechanism for vascular endothelial cell injury elicited by activated leukocytes: a significant involvement of adhesion molecules, CD11/CD18, and ICAM-1. Arch. Biochem. Biophys. 309 (1994) 62-69
103. Broeders M.A., Tangelder G.J., Slaaf D.W., Reneman R.S., and oude Egbrink M.G. Endogenous nitric oxide protects against thromboembolism in venules but not in arterioles. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 139-145
104. Kalogeris T.J., Kevil C.G., Laroux F.S., Coe L.L., Phifer T.J., and Alexander J.S. Differential monocyte adhesion and adhesion molecule expression in venous and arterial endothelial cells. Am. J. Physiol. 276 (1999) L9-L19
105. Reiter C.D., Wang X., Tanus-Santos J.E., Hogg N., Cannon III R.O., Schechter A.N., and Gladwin M.T. Cell-free hemoglobin limits nitric oxide bioavailability in sickle-cell disease. Nat. Med. 8 (2002) 1383-1389
106. Aslan M., Thornley-Brown D., and Freeman B.A. Reactive species in sickle cell disease. Ann. N. Y. Acad. Sci. 899 (2000) 375-391
107. Aslan M., Ryan T.M., Adler B., Townes T.M., Parks D.A., Thompson J.A., Tousson A., Gladwin M.T., Patel R.P., Tarpey M.M., Batinic-Haberle I., White C.R., and Freeman B.A. Oxygen radical inhibition of nitric oxide-dependent vascular function in sickle cell disease. Proc. Natl. Acad. Sci. USA 98 (2001) 15215-15220
108. Houston M., Estevez A., Chumley P., Aslan M., Marklund S., Parks D.A., and Freeman B.A. Binding of xanthine oxidase to vascular endothelium: kinetic characterization and oxidative impairment of nitric oxide-dependent signaling. J. Biol. Chem. 274 (1999) 4985-4994
109. Wood K.C., Hebbel R.P., and Granger D.N. Endothelial cell NADPH oxidase mediates the cerebral microvascular dysfunction in sickle cell transgenic mice. FASEB J. 19 (2005) 989-991
110. Wood K.C., Hebbel R.P., Lefer D.J., and Granger D.N. Critical role of endothelial cell-derived nitric oxide synthase in sickle cell disease-induced microvascular dysfunction. Free Radic. Biol. Med. 40 (2006) 1443-1453
111. Gibson Q., and Roughton F.J.W. The kinetics and equilibria of the reactions of nitric oxide with sheep hemoglobin. J. Physiol. (London) 136 (1957) 507-526
112. Herold S., Exner M., and Nauser T. Kinetic and mechanistic studies of the NO-mediated oxidation of oxymyoglobin and oxyhemoglobin. Biochemistry 40 (2001) 3385-3395
113. Liu X. Diffusion-limited reaction of free nitric oxide with erythrocytes. J. Biol. Chem. 273 (1998) 18709-18713
114. Bensinger T.A., and Gillette P.N. Hemolysis in sickle-cell disease. Arch. Intern. Med. 133 (1974) 624-631
115. Langlois M.R., and Delanghe J.R. Biological and clinical significance of haptoglobin polymorphism in humans. Clin. Chem. 42 (1996) 1589-1600
116. Bourantas K.L., Dalekos G.N., Makis A., Chaidos A., Tsiara S., and Mavridis A. Acute phase proteins and interleukins in steady state sickle cell disease. Eur. J. Haematol. 61 (1998) 49-54
117. Kato G.J., McGowan V., Machado R.F., Little J.A., Taylor J., Morris C.R., Nichols J.S., Wang X., Poljakovic M., Morris Jr. S.M., and Gladwin M.T. Lactate dehydrogenase as a biomarker of hemolysis-associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood 107 (2006) 2279-2285
118. Morris C.R., Kato G.J., Poljakovic M., Wang X., Blackwelder W.C., Sachdev V., Hazen S.L., Vichinsky E.P., Morris Jr. S.M., and Gladwin M.T. Dysregulated arginine metabolism, hemolysis-associated pulmonary hypertension, and mortality in sickle cell disease. JAMA 294 (2005) 81-90
119. Morris C.R., Morris Jr. S.M., Hagar W., van Warmerdam J., Claster S., Kepka-Lenhart D., Machado L., Kuypers F.A., and Vichinsky E.P. Arginine therapy: a new treatment for pulmonary hypertension in sickle cell disease?. Am. J. Respir. Crit. Care Med. 168 (2003) 63-69
120. Kato G.J., Gladwin M.T., and Steinberg M.H. Deconstructing sickle cell disease: reappraisal of the role of hemolysis in the development of clinical subphenotypes. Blood Rev. 21 (2007) 37-47
121. Hsu L.L., Champion H.C., Campbell-Lee S.A., Bivalacqua T.J., Manci E.A., Diwan B.A., Schimel D.M., Cochard A.E., Wang X., Schechter A.N., Noguchi C.T., and Gladwin M.T. Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood 109 (2007) 3088-3098
122. Moestrup S.K., and Moller H.J. CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann. Med. 36 (2004) 347-354
123. Choi A.M., and Alam J. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 15 (1996) 9-19
124. Jison M.L., Munson P.J., Barb J.J., Suffredini A.F., Talwar S., Logun C., Raghavachari N., Beigel J.H., Shelhamer J.H., Danner R.L., and Gladwin M.T. Blood mononuclear cell gene expression profiles characterize the oxidant, hemolytic, and inflammatory stress of sickle cell disease. Blood 104 (2004) 270-280
125. Nath K.A., Grande J.P., Haggard J.J., Croatt A.J., Katusic Z.S., Solovey A., and Hebbel R.P. Oxidative stress and induction of heme oxygenase-1 in the kidney in sickle cell disease. Am. J. Pathol. 158 (2001) 893-903
126. Nielsen M.J., Petersen S.V., Jacobsen C., Oxvig C., Rees D., Moller H.J., and Moestrup S.K. Haptoglobin-related protein is a high-affinity hemoglobin-binding plasma protein. Blood 108 (2006) 2846-2849
127. Ou J., Ou Z., Jones D.W., Holzhauer S., Hatoum O.A., Ackerman A.W., Weihrauch D.W., Gutterman D.D., Guice K., Oldham K.T., Hillery C.A., and Pritchard Jr. K.A. L-4F, an apolipoprotein A-1 mimetic, dramatically improves vasodilation in hypercholesterolemia and sickle cell disease. Circulation 107 (2003) 2337-2341
128. Kato G.J., Hsieh M., Machado R., Taylor J., Little J., Butman J.A., Lehky T., Tisdale J., and Gladwin M.T. Cerebrovascular disease associated with sickle cell pulmonary hypertension. Am. J. Hematol. 81 (2006) 503-510
129. Hillery C.A., and Panepinto J.A. Pathophysiology of stroke in sickle cell disease. Microcirculation 11 (2004) 195-208
130. Gladwin M.T., and Kato G.J. Cardiopulmonary complications of sickle cell disease: role of nitric oxide and hemolytic anemia. Hematology Am. Soc. Hematol. Educ. Program (2005) 51-57
131. Kaul D.K., Liu X.D., Choong S., Belcher J.D., Vercellotti G.M., and Hebbel R.P. Anti-inflammatory therapy ameliorates leukocyte adhesion and microvascular flow abnormalities in transgenic sickle mice. Am. J. Physiol. Heart Circ. Physiol. 287 (2004) H293-H301
132. Nath K.A., Shah V., Haggard J.J., Croatt A.J., Smith L.A., Hebbel R.P., and Katusic Z.S. Mechanisms of vascular instability in a transgenic mouse model of sickle cell disease. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000) R1949-R1955
133. Kowaluk E.A., Seth P., and Fung H.L. Metabolic activation of sodium nitroprusside to nitric oxide in vascular smooth muscle. J. Pharmacol. Exp. Ther. 262 (1992) 916-922
134. Bayraktutan U., Draper N., Lang D., and Shah A.M. Expression of functional neutrophil-type NADPH oxidase in cultured rat coronary microvascular endothelial cells. Cardiovasc. Res. 38 (1998) 256-262
135. White K.A., and Marletta M.A. Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry 31 (1992) 6627-6631
136. Alderton W.K., Cooper C.E., and Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 57 (2001) 593-615
137. Bec N., Gorren A.C., Voelker C., Mayer B., and Lange R. Reaction of neuronal nitric-oxide synthase with oxygen at low temperature: evidence for reductive activation of the oxy-ferrous complex by tetrahydrobiopterin. J. Biol. Chem. 273 (1998) 13502-13508
138. Presta A., Siddhanta U., Wu C., Sennequier N., Huang L., Abu-Soud H.M., Erzurum S., and Stuehr D.J. Comparative functioning of dihydro-and tetrahydropterins in supporting electron transfer, catalysis, and subunit dimerization in inducible nitric oxide synthase. Biochemistry 37 (1998) 298-310
139. Eiserich J.P., Baldus S., Brennan M.L., Ma W., Zhang C., Tousson A., Castro L., Lusis A.J., Nauseef W.M., White C.R., and Freeman B.A. Myeloperoxidase, a leukocyte-derived vascular NO oxidase. Science 296 (2002) 2391-2394
140. Baldus S., Eiserich J.P., Brennan M.L., Jackson R.M., Alexander C.B., and Freeman B.A. Spatial mapping of pulmonary and vascular nitrotyrosine reveals the pivotal role of myeloperoxidase as a catalyst for tyrosine nitration in inflammatory diseases. Free Radic. Biol. Med. 33 (2002) 1010
141. Baldus S., Eiserich J.P., Mani A., Castro L., Figueroa M., Chumley P., Ma W., Tousson A., White C.R., Bullard D.C., Brennan M.L., Lusis A.J., Moore K.P., and Freeman B.A. Endothelial transcytosis of myeloperoxidase confers specificity to vascular ECM proteins as targets of tyrosine nitration. J. Clin. Invest. 108 (2001) 1759-1770
142. Osarogiagbon U.R., Choong S., Belcher J.D., Vercellotti G.M., Paller M.S., and Hebbel R.P. Reperfusion injury pathophysiology in sickle transgenic mice. Blood 96 (2000) 314-320
143. Parks D.A., and Granger D.N. Ischemia induced vascular changes: role of xanthine oxidase and hydroxyl radicals. Am. J. Physiol. 245 (1983) G285-G289
144. Lee V.G., Johnson M.L., Baust J., Laubach V.E., Watkins S.C., and Billiar T.R. The roles of iNOS in liver ischemia-reperfusion injury. Shock 16 (2001) 355-360
145. Ling H., Gengaro P.E., Edelstein C.L., Martin P.Y., Wangsiripaisan A., Nemenoff R., and Schrier R.W. Effect of hypoxia on proximal tubules isolated from nitric oxide synthase knockout mice. Kidney Int. 53 (1998) 1642-1646
146. Aslan M., Ryan T.M., Townes T.M., Coward L., Kirk M.C., Barnes S., Alexander C.B., Rosenfeld S.S., and Freeman B.A. Nitric oxide-dependent generation of reactive species in sickle cell disease: actin tyrosine nitration induces defective cytoskeletal polymerization. J. Biol. Chem. 278 (2003) 4194-4204
147. Charache S., Terrin M.L., Moore R.D., Dover G.J., Barton F.B., Eckert S.V., McMahon R.P., and Bonds D.R. Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia. N. Engl. J. Med. 332 (1995) 1317-1322
148. Smith R.D., Li J., Noguchi C.T., and Schechter A.N. Quantitative PCR analysis of HbF inducers in primary human adult erythroid cells. Blood 95 (2000) 863-869
149. Stolze K., and Nohl H. EPR studies on the oxidation of hydroxyurea to paramagnetic compounds by oxyhemoglobin. Biochem. Pharmacol. 40 (1990) 799-802
150. Glover R.E., Ivy E.D., Orringer E.P., Maeda H., and Mason R.P. Detection of nitrosyl hemoglobin in venous blood in the treatment of sickle cell anemia with hydroxyurea. Mol. Pharmacol. 55 (1999) 1006-1010
151. Ikuta T., Ausenda S., and Cappellini M.D. Mechanism for fetal globin gene expression: role of the soluble guanylate cyclase-cGMP-dependent protein kinase pathway. Proc. Natl. Acad. Sci. USA 98 (2001) 1847-1852
152. Ley T.J., DeSimone J., Noguchi C.T., Turner P.H., Schechter A.N., Heller P., and Nienhuis A.W. 5-Azacytidine increases gamma-globin synthesis and reduces the proportion of dense cells in patients with sickle cell anemia. Blood 62 (1983) 370-380
153. DeSimone J., Koshy M., Dorn L., Lavelle D., Bressler L., Molokie R., and Talischy N. Maintenance of elevated fetal hemoglobin levels by decitabine during dose interval treatment of sickle cell anemia. Blood 99 (2002) 3905-3908
154. Wahl C., Liptay S., Adler G., and Schmid R.M. Sulfasalazine: a potent and specific inhibitor of nuclear factor kappa B. J. Clin. Invest. 101 (1998) 1163-1174
155. Solovey A.A., Solovey A.N., Harkness J., and Hebbel R.P. Modulation of endothelial cell activation in sickle cell disease: a pilot study. Blood 97 (2001) 1934-1937
156. Barabino G.A., Liu X.D., Ewenstein B.M., and Kaul D.K. Anionic polysaccharides inhibit adhesion of sickle erythrocytes to the vascular endothelium and result in improved hemodynamic behavior. Blood 93 (1999) 1422-1429
157. Kaul D.K., Tsai H.M., Liu X.D., Nakada M.T., Nagel R.L., and Coller B.S. Monoclonal antibodies to alphaVbeta3 (7E3 and LM609) inhibit sickle red blood cell-endothelium interactions induced by platelet-activating factor. Blood 95 (2000) 368-374
158. Lutty G.A., Taomoto M., Cao J., McLeod D.S., Vanderslice P., McIntyre B.W., Fabry M.E., and Nagel R.L. Inhibition of TNF-alpha-induced sickle RBC retention in retina by a VLA-4 antagonist. Invest. Ophthalmol. Visual Sci. 42 (2001) 1349-1355
159. Matsui N.M., Borsig L., Rosen S.D., Yaghmai M., Varki A., and Embury S.H. P-selectin mediates the adhesion of sickle erythrocytes to the endothelium. Blood 98 (2001) 1955-1962
160. Kumar A., Eckman J.R., and Wick T.M. Inhibition of plasma-mediated adherence of sickle erythrocytes to microvascular endothelium by conformationally constrained RGD-containing peptides. Am. J. Hematol. 53 (1996) 92-98
161. Mahaseth H., Vercellotti G.M., Welch T.E., Bowlin P.R., Sonbol K.M., Hsia C.J., Li M., Bischof J.C., Hebbel R.P., and Belcher J.D. Polynitroxyl albumin inhibits inflammation and vasoocclusion in transgenic sickle mice. J. Lab. Clin. Med. 145 (2005) 204-211
162. Belcher J.D., Mahaseth H., Welch T.E., Vilback A.E., Sonbol K.M., Kalambur V.S., Bowlin P.R., Bischof J.C., Hebbel R.P., and Vercellotti G.M. Critical role of endothelial cell activation in hypoxia-induced vasoocclusion in transgenic sickle mice. Am. J. Physiol. Heart Circ. Physiol. 288 (2005) H2715-H2725
163. Salvaggio J.E., Arnold C.A., and Banov C.H. Long-term anti-coagulation in sickle-cell disease: a clinical study. N. Engl. J. Med. 269 (1963) 182-186
164. Wolters H.J., ten Cate H., Thomas L.L., Brandjes D.P., van der Ende A., van der Heiden Y., and Statius van Eps L.W. Low-intensity oral anticoagulation in sickle-cell disease reverses the prethrombotic state: promises for treatment?. Br. J. Haematol. 90 (1995) 715-717
165. Chaplin Jr. H., Monroe M.C., Malecek A.C., Morgan L.K., Michael J., and Murphy W.A. Preliminary trial of minidose heparin prophylaxis for painful sickle cell crises. East Afr. Med. J. 66 (1989) 574-584
166. Semple M.J., Al-Hasani S.F., Kioy P., and Savidge G.F. A double-blind trial of ticlopidine in sickle cell disease. Thromb. Haemostasis 51 (1984) 303-306
167. Schnog J.B., Kater A.P., Mac Gillavry M.R., Duits A.J., Lard L.R., van Der Dijs F.P., Brandjes D.P., ten Cate H., van Eps L.W., and Rojer R.A. Low adjusted-dose acenocoumarol therapy in sickle cell disease: a pilot study. Am. J. Hematol. 68 (2001) 179-183
168. Zago M.A., Costa F.F., Ismael S.J., Tone L.G., and Bottura C. Treatment of sickle cell diseases with aspirin. Acta Haematol. 72 (1984) 61-64
169. Chaplin Jr. H., Alkjaersig N., Fletcher A.P., Michael J.M., and Joist J.H. Aspirin-Dipyridamole prophylaxis of sickle cell disease pain crises. Thromb. Haemostasis 43 (1980) 218-221
170. Tomer A., Kasey S., Connor W.E., Clark S., Harker L.A., and Eckman J.R. Reduction of pain episodes and prothrombotic activity in sickle cell disease by dietary n-3 fatty acids. Thromb. Haemostasis 85 (2001) 966-974
171. Phillips G., and Tangney C.C. Relationship of plasma alpha tocopherol to index of clinical severity in individuals with sickle cell anemia. Am. J. Hematol. 41 (1992) 227-231
172. Natta C.L., Machlin L.J., and Brin M. A decrease in irreversibly sickled erythrocytes in sickle cell anemia patients given vitamin E. Am. J. Clin. Nutr. 33 (1980) 968-971
173. Oppert M., Jorres A., Barckow D., Eckardt K.U., Frei U., and Kaisers U. Inhaled nitric oxide for ARDS due to sickle cell disease. Swiss Med. Wkly. 134 (2004) 165-167
174. Sullivan K.J., Goodwin S.R., Evangelist J., Moore R.D., and Mehta P. Nitric oxide successfully used to treat acute chest syndrome of sickle cell disease in a young adolescent. Crit. Care Med. 27 (1999) 2563-2568
175. Atz A.M., and Wessel D.L. Inhaled nitric oxide in sickle cell disease with acute chest syndrome. Anesthesiology 87 (1997) 988-990
176. Weiner D.L., Hibberd P.L., Betit P., Cooper A.B., Botelho C.A., and Brugnara C. Preliminary assessment of inhaled nitric oxide for acute vaso-occlusive crisis in pediatric patients with sickle cell disease. JAMA 289 (2003) 1136-1142
177. Reyes A.A., Karl I.E., and Klahr S. Role of arginine in health and in renal disease. Am. J. Physiol. 267 (1994) F331-F346
178. Enwonwu C.O., Xu X.X., and Turner E. Nitrogen metabolism in sickle cell anemia: free amino acids in plasma and urine. Am. J. Med. Sci. 300 (1990) 366-371
179. Morris C.R., Kuypers F.A., Larkin S., Vichinsky E.P., and Styles L.A. Patterns of arginine and nitric oxide in patients with sickle cell disease with vaso-occlusive crisis and acute chest syndrome. J. Pediatr. Hematol. Oncol. 22 (2000) 515-520
180. Morris C.R., Vichinsky E.P., van Warmerdam J., Machado L., Kepka-Lenhart D., Morris Jr. S.M., and Kuypers F.A. Hydroxyurea and arginine therapy: impact on nitric oxide production in sickle cell disease. J. Pediatr. Hematol. Oncol. 25 (2003) 629-634
181. Machado R.F., Martyr S., Kato G.J., Barst R.J., Anthi A., Robinson M.R., Hunter L., Coles W., Nichols J., Hunter C., Sachdev V., Castro O., and Gladwin M.T. Sildenafil therapy in patients with sickle cell disease and pulmonary hypertension. Br. J. Haematol. 130 (2005) 445-453