Critical role of endothelial cell-derived nitric oxide synthase in sickle cell disease-induced microvascular dysfunction

Free Radical Biology and Medicine

Volumn 40, Issue 8, 2006, Pages 1443-1453

  Wood, Katherine C ^a   Hebbel, Robert P ^b   Lefer, David J ^a   Granger, D Neil ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Free radical; Hypoxia reoxygenation; Inflammation; Platelet endothelial cell adhesion; Sickle cell disease; Tetrahydrobiopterin; Thrombogenesis

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MACROGOL; SEPIAPTERIN; SUPEROXIDE; SUPEROXIDE DISMUTASE; TETRAHYDROBIOPTERIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN VEIN; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE OVEREXPRESSION; LEUKOCYTE ADHERENCE; MICROANGIOPATHY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; SICKLE CELL ANEMIA; THROMBOCYTE ADHESION; TRANSGENIC MOUSE; VENULE; WILD TYPE;

ANEMIA, SICKLE CELL; ANIMALS; CELL ADHESION; CELLS, CULTURED; LEUKOCYTES; MICE; MICE, TRANSGENIC; NITRIC OXIDE SYNTHASE TYPE III; PLATELET ADHESIVENESS; POLYETHYLENE GLYCOLS; PTERINS; SUPEROXIDE DISMUTASE;

MUS MUSCULUS;

EID: 33646060766     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2005.12.015     Document Type: Article

References (57)

1. 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
2. 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
3. Wood K., Russell J., Hebbel R.P., and Grange D.N. Differential expression of E- and P-selectin in the microvasculature of sickle cell transgenic mice. Microcirculation 11 (2004) 377-385
4. 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
5. 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
6. Wood K.C., Hebbel R.P., and Granger D.N. Endothelial cell P-selectin mediates a proinflammatory and prothrombogenic phenotype in cerebral venules of sickle cell transgenic mice. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H1608-H1614
7. 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
8. Sorescu D., Weiss D., Lassegue B., Clempus R.E., Szocs K., Sorescu G.P., Valppu L., Quinn M.T., Lambeth J.D., Vega J.D., Taylor W.R., and Griendling K.K. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105 (2002) 1429-1435
9. Harrison D.G., Cai H., Landmesser U., and Griendling K.K. Interactions of angiotensin II with NAD(P)H oxidase, oxidant stress and cardiovascular disease. J. Renin Angiotensin Aldosterone Syst. 4 (2003) 51-61
10. Ishikawa M., Stokes K.Y., Zhang J.H., Nanda A., and Granger D.N. Cerebral microvascular responses to hypercholesterolemia: roles of NADPH oxidase and P-selectin. Circ. Res. 94 (2004) 239-244
11. 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 8 (2005) 989-991
12. 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
13. Pritchard Jr. K.A., Ou J., Ou Z., Shi Y., Franciosi J.P., Signorino P., Kaul S., Ackland-Berglund C., Witte K., Holzhauer S., Mohandas N., Guice K.S., Oldham K.T., and Hillery C.A. Hypoxia-induced acute lung injury in murine models of sickle cell disease. Am. J. Physiol. Lung Cell Mol. Physiol. 286 (2004) L705-L714
14. 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
15. Kaul D.K., Liu X.D., Fabry M.E., and Nagel R.L. Impaired nitric oxide-mediated vasodilation in transgenic sickle mouse. Am. J. Physiol. Heart Circ. Physiol. 278 (2000) H1799-H1806
16. Vasquez-Vivar J., Kalyanaraman B., Martasek P., Hogg N., Masters B.S., Karoui H., Tordo P., and Pritchard Jr. K.A. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc. Natl. Acad. Sci. USA 95 (1998) 9220-9225
17. Alp N.J., McAteer M.A., Khoo J., Choudhury R.P., and Channon K.M. Increased endothelial tetrahydrobiopterin synthesis by targeted transgenic GTP-cyclohydrolase I overexpression reduces endothelial dysfunction and atherosclerosis in ApoE-knockout mice. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 445-450
18. Alp N.J., Mussa S., Khoo J., Cai S., Guzik T., Jefferson A., Goh N., Rockett K.A., and Channon K.M. Tetrahydrobiopterin-dependent preservation of nitric oxide-mediated endothelial function in diabetes by targeted transgenic GTP-cyclohydrolase I overexpression. J. Clin. Invest. 112 (2003) 725-735
19. Zheng J.S., Yang X.Q., Lookingland K.J., Fink G.D., Hesslinger C., Kapatos G., Kovesdi I., and Chen A.F. Gene transfer of human guanosine 5′-triphosphate cyclohydrolase I restores vascular tetrahydrobiopterin level and endothelial function in low renin hypertension. Circulation 108 (2003) 1238-1245
20. Noguchi C.T., Gladwin M., Diwan B., Merciris P., Smith R., Yu X., Buzard G., Fitzhugh A., Keefer L.K., Schechter A.N., and Mohandas N. Pathophysiology of a sickle cell trait mouse model: human alpha(beta)(S) transgenes with one mouse beta-globin allele. Blood Cells Mol. Dis. 27 (2001) 971-977
21. Ohashi Y., Kawashima S., Hirata K., Yamashita T., Ishida T., Inoue N., Sakoda T., Kurihara H., Yazaki Y., and Yokoyama M. Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. J. Clin. Invest. 102 (1998) 2061-2071
22. Ozaki M., Kawashima S., Hirase T., Yamashita T., Namiki M., Inoue N., Hirata Ki K., and Yokoyama M. Overexpression of endothelial nitric oxide synthase in endothelial cells is protective against ischemia-reperfusion injury in mouse skeletal muscle. Am. J. Pathol. 160 (2002) 1335-1344
23. Huang P.L., Huang Z., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., and Fishman M.C. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377 (1995) 239-242
24. Tomita Y., Sachs D.H., and Sykes M. Myelosuppressive conditioning is required to achieve engraftment of pluripotent stem cells contained in moderate doses of syngeneic bone marrow. Blood 83 (1994) 939-948
25. 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
26. Wood K.C., Hebbel R.P., and Granger D.N. Endothelial cell P-selectin mediates a proinflammatory and prothrombogenic phenotype in cerebral venules of sickle cell transgenic mice. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H1608-H1614
27. Rogers Jr. H., Zibari G.B., Roberts J., Turnage R., and Lefer D.J. Nitric oxide attenuates ischaemia-reperfusion (I/R) injury in the diabetic liver. Clin. Transplant. 18 Suppl. 12 (2004) 7-11
28. Jung O., Schreiber J.G., Geiger H., Pedrazzini T., Busse R., and Brandes R.P. gp91phox-containing NADPH oxidase mediates endothelial dysfunction in renovascular hypertension. Circulation 109 (2004) 1795-1801
29. Sawabe K., Wakasugi K.O., and Hasegawa H. Tetrahydrobiopterin uptake in supplemental administration: elevation of tissue tetrahydrobiopterin in mice following uptake of the exogenously oxidized product 7,8-dihydrobiopterin and subsequent reduction by an anti-folate-sensitive process. J. Pharmacol. Sci. 96 (2004) 124-133
30. Tailor A., and Granger D.N. Hypercholesterolemia promotes P-selectin-dependent platelet-endothelial cell adhesion in postcapillary venules. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 675-680
31. Tsujikawa A., Kiryu J., Yamashiro K., Nonaka A., Nishijima K., Honda Y., and Ogura Y. Interactions between blood cells and retinal endothelium in endotoxic sepsis. Hypertension 36 (2000) 250-258
32. Massberg S., Enders G., Leiderer R., Eisenmenger S., Vestweber D., Krombach F., and Messmer K. Platelet-endothelial cell interactions during ischemia/reperfusion: the role of P-selectin. Blood 92 (1998) 507-515
33. Beckman J.S., Minor Jr. R.L., White C.W., Repine J.E., Roseng G.M., and Freeman B.A. Superoxide dismutase and catalase conjugated to polyethylene glycol increases endothelial enzyme activity and oxidant resistance. J. Biol. Chem. 263 (1988) 6884-6892
34. French II J.A., Kenny D., Scott J.P., Hoffmann R.G., Wood J.D., Hudetz A.G., and Hillery C.A. Mechanisms of stroke in sickle cell disease: sickle erythrocytes decrease cerebral blood flow in rats after nitric oxide synthase inhibition. Blood 89 (1997) 4591-4599
35. Suschek C.V., Schnorr O., and Kolb-Bachofen V. The role of iNOS in chronic inflammatory processes in vivo: is it damage-promoting, protective, or active at all?. Curr. Mol. Med. 4 (2004) 763-775
36. Forstermann U., Boissel J.P., and Kleinert H. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 12 (1998) 773-790
37. Gahm C., Holmin S., and Mathiesen T. Temporal profiles and cellular sources of three nitric oxide synthase isoforms in the brain after experimental contusion. Neurosurgery 46 (2000) 169-177
38. Osei S.Y., Ahima R.S., Fabry M.E., Nagel R.L., and Bank N. Immunohistochemical localization of hepatic nitric oxide synthase in normal and transgenic sickle cell mice: the effect of hypoxia. Blood 88 (1996) 3583-3588
39. 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 induces defective cytoskeletal polymerization. J. Biol. Chem. 278 (2003) 4194-4204
40. 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
41. Hammerman S.I., Klings E.S., Hendra K.P., Upchurch Jr. G.R., Rishikof D.C., Loscalzo J., and Farber H.W. Endothelial cell nitric oxide production in acute chest syndrome. Am. J. Physiol. 277 (1999) H1579-H1592
42. Bank N., Kiroycheva M., Singhal P.C., Anthony G.M., Southan G.J., and Szabo C. Inhibition of nitric oxide synthase ameliorates cellular injury in sickle cell mouse kidneys. Kidney Int. 58 (2000) 82-89
43. Kuhlencordt P.J., Rosel E., Gerszten R.E., Morales-Ruiz M., Dombkowski D., Atkinson W.J., Han F., Preffer F., Rosenzweig A., Sessa W.C., Gimbrone Jr. M.A., Ertl G., and Huang P.L. Role of endothelial nitric oxide synthase in endothelial activation: insights from eNOS knockout endothelial cells. Am. J. Physiol. Cell Physiol. 286 (2004) C1195-C1202
44. Lefer D.J., Jones S.P., Girod W.G., Baines A., Grisham M.B., Cockrell A.S., Huang P.L., and Scalia R. Leukocyte-endothelial cell interactions in nitric oxide synthase-deficient mice. Am. J. Physiol. 276 (1999) H1943-H1950
45. Kawashima S., Yamashita T., Ozaki M., Ohashi Y., Azumi H., Inoue N., Hirata K., Hayashi Y., Itoh H., and Yokoyama M. Endothelial NO synthase overexpression inhibits lesion formation in mouse model of vascular remodeling. Arterioscler. Thromb. Vasc. Biol. 21 (2001) 201-207
46. Jones S.P., Greer J.J., Kakkar A.K., Ware P.D., Turnage R.H., Hicks M., van Haperen R., de Crom R., Kawashima S., Yokoyama M., and Lefer D.J. Endothelial nitric oxide synthase overexpression attenuates myocardial reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H276-H282
47. Yamashita T., Kawashima S., Ohashi Y., Ozaki M., Ueyama T., Ishida T., Inoue N., Hirata K., Akita H., and Yokoyama M. Resistance to endotoxin shock in transgenic mice overexpressing endothelial nitric oxide synthase. Circulation 101 (2000) 931-937
48. Kubes P., Suzuki M., and Granger D.N. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA 88 (1991) 4651-4655
49. Qu X.W., Thaete L.G., Rozenfeld R.A., Zhu Y., De Plaen I.G., Caplan M.S., and Hsueh W. Tetrahydrobiopterin prevents platelet-activating factor-induced intestinal hypoperfusion and necrosis: Role of neuronal nitric oxide synthase. Crit. Care Med. 33 (2005) 1050-1056
50. Morishita T., Tsutsui M., Shimokawa H., Horiuchi M., Tanimoto A., Suda O., Tasaki H., Huang P.L., Sasaguri Y., Yanagihara N., and Nakashima Y. Vasculoprotective roles of neuronal nitric oxide synthase. FASEB J. 16 (2002) 1994-1996
51. Patel K.B., Stratford M.R., Wardman P., and Everett S.A. Oxidation of tetrahydrobiopterin by biological radicals and scavenging of the trihydrobiopterin radical by ascorbate. Free Radical. Biol. Med. 32 (2002) 203-211
52. Kirsch M., Korth H.G., Stenert V., Sustmann R., and de Groot H. The autoxidation of tetrahydrobiopterin revisited. Proof of superoxide formation from reaction of tetrahydrobiopterin with molecular oxygen. J. Biol. Chem. 278 (2003) 24481-24490
53. Hebbel R.P., Eaton J.W., Balasingam M., and Steinberg M.H. Spontaneous oxygen radical generation by sickle erythrocytes. J. Clin. Invest. 70 (1982) 1253-1259
54. Berka V., Wu G., Yeh H.C., Palmer G., and Tsai A.L. Three different oxygen-induced radical species in endothelial nitric-oxide synthase oxygenase domain under regulation by L-arginine and tetrahydrobiopterin. J. Clin. Invest. 279 (2004) 32243-32251
55. Kuzkaya N., Weissmann N., Harrison D.G., and Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J. Biol. Chem. 278 (2003) 22546-22554
56. Milstien S., and Katusic Z. Oxidation of tetrahydrobiopterin by peroxynitrite: implications for vascular endothelial function. Biochem. Biophys. Res. Commun. 263 (1999) 681-684
57. Vasquez-Vivar J., Martasek P., Whitsett J., Joseph J., and Kalyanaraman B. The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study. Biochem. J. 362 (2002) 733-739