Molecular control of nitric oxide synthases in the cardiovascular system

Cardiovascular Research

Volumn 43, Issue 3, 1999, Pages 509-520

  Papapetropoulos, Andreas ^a   Rudic, Radu Daniel ^a   Sessa, William C ^a  

^a Boyer C   (United States)

Author keywords

Cardiovascular system; Molecular control; Nitric oxide synthases

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE; VASCULOTROPIN;

BLOOD VESSEL TONE; BRAIN ISCHEMIA; CARDIOVASCULAR SYSTEM; CENTRAL NERVOUS SYSTEM; CYTOLOGY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME REGULATION; GENE CONTROL; HOST RESISTANCE; HUMAN; INFLAMMATION; KNOCKOUT MOUSE; MOLECULAR BIOLOGY; MOLECULAR GENETICS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; REVIEW; SEPSIS; STROKE; TRANSCRIPTION REGULATION;

ANIMALS; BLOOD PRESSURE; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; IMMUNE SYSTEM; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; RATS; VASOMOTOR SYSTEM;

EID: 0033566680     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(99)00161-3     Document Type: Review

References (132)

1. Bredt D.S., Hwang P.M., Glatt C.E., et al. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature. 351:1991;714-718.
2. Gonzalez C., Barroso C., Martin C., Gulbenkian S., Estrada C. Neuronal nitric oxide synthase activation by vasoactive intestinal peptide in bovine cerebral arteries. J Cereb Blood Flow Metab. 17:1997;977-984.
3. Papapetropoulos A., Desai K.M., Rudic R.D., et al. Nitric oxide synthase inhibitors attenuate transforming-growth-factor-beta1-stimulated capillary organization in vitro. Am J Pathol. 150:1997;1835-1844.
4. Boulanger C.M., Heymes C., Benessiano J., et al. Neuronal nitric oxide synthase is expressed in rat vascular smooth muscle cells: activation by angiotensin II in hypertension [In Process Citation]. Circ Res. 83:1998;1271-1278.
5. Papadaki M., Tilton R.G., Eskin S.G., McIntire L.V. Nitric oxide production by cultured human aortic smooth muscle cells: stimulation by fluid flow. Am J Physiol. 274:1998;H616-626.
6. Jaffrey S.R., Snyder S.H. PIN: an associated protein inhibitor of neuronal nitric oxide synthase. Science. 274:1996;774-777.
7. Jaffrey S.R., Snowman A.M., Eliasson M.J., Cohen N.A., Snyder S.H. CAPON: a protein associated with neuronal nitric oxide synthase that regulates its interactions with PSD95. Neuron. 20:1998;115-124.
8. Garcia-Cardena G., Martasek P., Masters B.S., et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem. 272:1997;25437-25440.
9. Venema V.J., Ju H., Zou R., Venema R.C. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J Biol Chem. 272:1997;28187-28190.
10. Meng W., Ayata C., Waeber C., Huang P.L., Moskowitz M.A. Neuronal NOS-cGMP-dependent ACh-induced relaxation in pial arterioles of endothelial NOS knockout mice. Am J Physiol. 274:1998;H411-415.
11. Wilcox J.N., Subramanian R.R., Sundell C.L., et al. Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler Thromb Vasc Biol. 17:1997;2479-2488.
12. Hall A.V., Antoniou H., Wang Y., et al. Structural organization of the human neuronal nitric oxide synthase gene (NOS1). J Biol Chem. 269:1994;33082-33090.
13. Wang Y., Marsden P.A. Nitric oxide synthases: gene structure and regulation. [Review]. Adv Pharmacol. 34:1995;71-90.
14. Forstermann U., Kleinert H., Gath I., et al. Expression and expressional control of nitric oxide synthases in various cell types. [Review]. Adv Pharmacol. 34:1995;171-186.
15. Xie J., Roddy P., Rife T.K., Murad F., Young A.P. Two closely linked but separable promoters for human neuronal nitric oxide synthase gene transcription. Proc Natl Acad Sci USA. 92:1995;1242-1246.
16. Young A.P., Murad F., Vaessin H., Xie J., Rife T.K. Transcription of the human neuronal nitric oxide synthase gene in the central nervous system is mediated by multiple promoters. [Review]. Adv Pharmacol. 34:1995;91-112.
17. Wang Y., Goligorsky M.S., Lin M., Wilcox J.N., Marsden P.A. A novel, testis-specific mRNA transcript encoding an NH2-terminal truncated nitric-oxide synthase. J Biol Chem. 272:1997;11392-11401.
18. Silvagno F., Xia H., Bredt D.S. Neuronal nitric-oxide synthase-μ, an alternatively spliced isoform expressed in differentiated skeletal muscle. J Biol Chem. 271:1996;11204-11208.
19. Forstermann U., Boissel J.P., Kleinert H. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 12:1998;773-790.
20. Brenman J.E., Chao D.S., Xia H., Aldape K., Bredt D.S. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell. 82:1995;743-752.
21. Brenman J.E., Chao D.S., Gee S.H., et al. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell. 84:1996;757-767.
22. Segal SS, Brett SE, Sessa WC. Co-distribution of NOS and caveolin throughout peripheral vasculature and skeletal muscle of the hamster. Am J Physiol, in press.
23. Nakane M., Mitchell J., Forstermann U., Murad F. Phosphorylation by calcium calmodulin-dependent protein kinase II and protein kinase C modulates the activity of nitric oxide synthase. Biochem Biophys Res Commun. 180:1991;1396-1402.
24. Bredt D.S., Ferris C.D., Snyder S.H. Nitric oxide synthase regulatory sites: phosphorylation by cyclic AMP-dependent protein kinase, protein kinase C, and calcium/calmodulin protein kinase; identification of flavin and calmodulin binding sites. J. Biol. Chem. 267:1992;10976-10981.
25. Colasanti M., Persichini T., Cavalieri E., et al. Rapid inactivation of NOS-I by lipopolysaccharide plus interferon-gamma-induced tyrosine phosphorylation. J. Biol. Chem. 274:1999;9915-9917.
26. Nathan C., Xie Q.W. Regulation of biosynthesis of nitric oxide. [Review]. J Biol Chem. 269:1994;13725-13728.
27. Morris S.J., Billiar T.R. New insights into the regulation of inducible nitric oxide synthesis. [Review]. Am J Physiol. 266:1994;E829-E839.
28. Lowenstein C.J., Alley E.W., Raval P., et al. Macrophage nitric oxide synthase gene: two upstream regions mediate induction by interferon gamma and lipopolysaccharide. Proc Natl Acad Sci USA. 90:1993;9730-9734.
29. Xie Q.W., Whisnant R., Nathan C. Promoter of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial lipopolysaccharide. J Exp Med. 177:1993;1779-1784.
30. Nunokawa Y., Ishida N., Tanaka S. Promoter analysis of human inducible nitric oxide synthase gene associated with cardiovascular homeostasis. Biochem Biophys Res Commun. 200:1994;802-807.
31. Xie Q.W., Kashiwabara Y., Nathan C. Role of transcription factor NF-kappa B/Rel in induction of nitric oxide synthase. J Biol Chem. 269:1994;4705-4708.
32. Martin E., Nathan C., Xie Q.W. Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J Exp Med. 180:1994;977-984.
33. Kamijo R., Harada H., Matsuyama T., et al. Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science. 263:1994;1612-1615.
34. Spink J., Cohen J., Evans T.J. The cytokine responsive vascular smooth muscle cell enhancer of inducible nitric oxide synthase. Activation by nuclear factor-kappa. B. J Biol Chem. 270:1995;29541-29547.
35. Vodovotz Y., Bogdan C., Paik J., Xie Q., Nathan C. Mechanisms of supression of macrophage nitric oxide release by transforming growth factor β J Exp Med. 178:1993;605-613.
36. Imai T., Hirata Y., Kanno K., Marumo F. Induction of nitric oxide synthase by cyclic AMP in rat vascular smooth muscle cells. J Clin Invest. 93:1994;543-549.
37. Sirsjo A., Soderkvist P., Sundqvist T., et al. Different induction mechanisms of mRNA for inducible nitric oxide synthase in rat smooth muscle cells in culture and in aortic strips. FEBS Lett. 338:1994;191-196.
38. Perrella M.A., Patterson C., Tan L., et al. Suppression of interleukin-1β-induced nitric-oxide synthase promoter/enhancer activity by transforming growth factor-β1 in vascular smooth muscle cells. J Biol Chem. 271:1996;13776-13780.
39. Cho H.J., Xie W.-W., Calaycay J., et al. Calmodulin as a tightly bound subunit of calcium-, calmodulin-independent nitric oxide synthase. J Exp Med. 176:1992;599-604.
40. Cho H.J., Xie Q.W., Calaycay J., et al. Calmodulin is a subunit of nitric oxide synthase from macrophages. J Exp Med. 176:1992;599-604.
41. Wheeler M.A., Smith S.D., Garcia-Cardena G., et al. Bacterial infection induces nitric oxide synthase in human neutrophils. J Clin Invest. 99:1997;110-116.
42. Vodovotz Y., Russell D., Xie Q.W., Bogdan C., Nathan C. Vesicle membrane association of nitric oxide synthase on primary mouse macrophages. J Immunol. 154:1995;2914-2925.
43. Pan J., Burgher K.L., Szczepanik A.M., Ringheim G.E. Tyrosine phosphorylation of inducible nitric oxide synthase:implications for potential post-translational regulation. Biochem J. 314:1996;889-894.
44. Forstermann U., Pollock J.S., Schmidt H.H., Heller M., Murad F. Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells. Proc Natl Acad Sci USA. 88:1991;1788-1792.
45. Pollock J.S., Forstermann U., Mitchell J.A., et al. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci USA. 88:1991;10480-10484.
46. Lamas S., Marsden P.A., Li G.K., Tempst P., Michel T. Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc Natl Acad Sci USA. 89:1992;6348-6352.
47. Sessa W.C., Harrison J.K., Barber C.M., et al. Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem. 267:1992;15274-15276.
48. Balligand J.L., Kelly R.A., Marsden P.A., Smith T.W., Michel T. Control of cardiac muscle cell function by an endogenous nitric oxide signaling system. Proc Natl Acad Sci USA. 90:1993;347-351.
49. Sase K., Michel T. Expression of constitutive endothelial nitric oxide synthase in human blood platelets. Life Sci. 57:1995;2049-2055.
50. Marsden P.A., Heng H.H., Scherer S.W., et al. Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J Biol Chem. 268:1993;17478-17488.
51. Wang Y., Marsden P.A. Nitric oxide synthases: gene structure and regulation. Adv Pharmacol. 34:1995;71-90.
52. Zhang R., Min W., Sessa W.C. Functional analysis of the human endothelial nitric oxide synthase promoter. Sp1 and GATA factors are necessary for basal transcription in endothelial cells. J Biol Chem. 270:1995;15320-15326.
53. Tang J.L., Zembowicz A., Xu X.M., Wu K.K. Role of Sp1 in transcriptional activation of human nitric oxide synthase type III gene. Biochem Biophys Res Commun. 213:1995;673-680.
54. Guillot P.V., Guan J., Liu L., et al. A vascular bed-specific pathway regulates cardiac expression of endothelial nitric oxide. J Clin Invest. 103:1999;799-805.
55. Nishida K., Harrison D.G., Navas J.P., et al. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest. 90:1992;2092-2096.
56. Uematsu M., Ohara Y., Navas J.P., et al. Regulation of endothelial cell nitric oxide synthase mRNA expression by shear stress. Am J Physiol. 269:1995;C1371-C1378.
57. Sessa W.C., Pritchard K., Seyedi N., Wang J., Hintze T.H. Chronic exercise in dogs increases coronary vascular nitric oxide production and endothelial cell nitric oxide synthase gene expression. Circ Res. 74:1994;349-353.
58. Zembowicz A., Tang J.L., Wu K.K. Transcriptional induction of endothelial nitric oxide synthase type III by lysophosphatidylcholine. J Biol Chem. 270:1995;17006-17010.
59. Kanazawa K., Kawashima S., Mikami S., et al. Endothelial constitutive nitric oxide synthase protein and mRNA increased in rabbit atherosclerotic aorta despite impaired endothelium-dependent vascular relaxation. Am J Pathol. 148:1996;1949-1956.
60. Hirata K., Miki N., Kuroda Y., et al. Low concentration of oxidized low-density lipoprotein and lysophosphatidylcholine upregulate constitutive nitric oxide synthase mRNA expression in bovine aortic endothelial cells. Circ Res. 76:1995;958-962.
61. Cieslik K., Zembowicz A., Tang J.L., Wu K.K. Transcriptional regulation of endothelial nitric-oxide synthase by lysophosphatidylcholine. J Biol Chem. 273:1998;14885-14890.
62. Liao J.K., Shin W.S., Lee W.Y., Clark S.L. Oxidized low-density lipoprotein decreases the expression of endothelial nitric oxide synthase. J Biol Chem. 270:1995;319-324.
63. Laufs U., La Fata V., Plutzky J., Liao J.K. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation. 97:1998;1129-1135.
64. Laufs U., Liao J.K. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J Biol Chem. 273:1998;24266-24271.
65. Endres M., Laufs U., Huang Z., et al. Stroke protection by 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase inhibitors mediated by endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 95:1998;8880-8885.
66. Inoue N., Venema R.C., Sayegh H.S., et al. Molecular regulation of the bovine endothelial cell nitric oxide synthase by transforming growth factor-beta 1. Arterioscler Thromb Vasc Biol. 15:1995;1255-1261.
67. Yoshizumi M., Perrella M.A., Burnett J.C., Lee M. Tumor necrosis factor downregulates endothelial nitric oxide synthase mRNA by shortening its half-life. Circ Res. 73:1993;205-209.
68. Alonso J., Sanchez de Miguel L., Monton M., Casado S., Lopez-Farre A. Endothelial cytosolic proteins bind to the 3′ untranslated region of endothelial nitric oxide synthase mRNA: regulation by tumor necrosis factor alpha. Mol Cell Biol. 17:1997;5719-5726.
69. Weiner C.P., Lizasoain I., Baylis S.A., et al. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc Natl Acad Sci USA. 91:1994;5212-5216.
70. Kleinert H., Wallerath T., Euchenhofer C., et al. Estrogens increase transcription of the human endothelial NO synthase gene: analysis of the transcription factors involved. Hypertension. 31:1998;582-588.
71. Caulin-Glaser T., Garcia-Cardena G., Sarrel P., Sessa W.C., Bender J.R. 17 beta-estradiol regulation of human endothelial cell basal nitric oxide release, independent of cytosolic Ca2+ mobilization. Circ Res. 81:1997;885-892.
72. Lantin-Hermoso R.L., Rosenfeld C.R., Yuhanna I.S., et al. Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol. 273:1997;L119-L126.
73. Liu J., García-Cardeña G., Sessa W.C. Biosynthesis and palmitoylation of endothelial nitric oxide synthase: mutagenesis of palmitoylation sites, cysteines-15 and/or -26, argues against depalmitoylation-induced translocation of the enzyme. Biochemistry. 34:1995;12333-12340.
74. Liu J., García-Cardeña G., Sessa W.C. Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry. 35:1996;13277-13281.
75. Liu J., Sessa W.C. Identification of covalently bound amino-terminal myristic acid in endothelial nitric oxide synthase. J Biol Chem. 269:1994;11691-11694.
76. Sessa W.C., García-Cardeña G., Liu J., et al. The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J Biol Chem. 270:1995;17641-17644.
77. Garcia-Cardena G., Oh P., Liu J., Schnitzer J.E., Sessa W.C. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci USA. 93:1996;6448-6453.
78. Shaul P.W., Smart E.J., Robinson L.J., et al. Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem. 271:1996;6518-6522.
79. Ju H., Zou R., Venema V.J., Venema R.C. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem. 272:1997;18522-18525.
80. Ju H., Venema V.J., Marrero M.B., Venema R.C. Inhibitory interactions of the bradykinin B2 receptor with endothelial nitric-oxide synthase. J Biol Chem. 273:1998;24025-24029.
81. Ghosh S., Gachhui R., Crooks C., Wu C., Lisanti M.P., Stuehr D.J. Interaction between caveolin-1 and the reductase domain of endothelial nitric-oxide synthase. Consequences for catalysis. J Biol Chem. 273:1998;22267-22271.
82. Garcia-Cardena G., Fan R., Shah V., et al. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature. 392:1998;821-824.
83. Michel T., Li G.K., Busconi L. Phosphorylation and subcellular translocation of endothelial nitric oxide synthase. Proc Natl Acad Sci. 90:1993;6252-6256.
84. Fleming I., Bauersachs J., Fisslthaler B., Busse R. Ca2+-independent activation of the endothelial nitric oxide synthase in response to tyrosine phosphatase inhibitors and fluid shear stress. Circ Res. 82:1998;686-695.
85. Corson M.A., James N.L., Latta S.E., et al. Phosphorylation of endothelial nitric oxide synthase in response to fluid shear stress. Circ Res. 79:1996;984-991.
86. Garcia-Cardena G., Fan R., Stern D.F., Liu J., Sessa W.C. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem. 271:1996;27237-27240.
87. Hirata K., Kuroda R., Sakoda T., et al. Inhibition of endothelial nitric oxide synthase activity by protein kinase C. Hypertension. 25:1995;180-185.
88. Chen Z.P., Mitchelhill K.I., Michell B.J., et al. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 443:1999;285-289.
89. Fulton D, Gratton JP, McCabe TJ, et al. Regulation of endothelium-derived nitric oxide by Akt. Nature, in press.
90. Dimmeler, S., Fissthaler, B., Fleming, I., Assmus, B., Hermann, C., Zeiher. A., 1998. Shear stress stimulates the protein kinase Akt-involvement in the regulation of endothelial nitric oxide synthase. Circulation (Abstract). 98: I-312.
91. O'Dell T.J., Huang P.L., Dawson T.M., et al. Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS. Science. 265:1994;542-546.
92. Son H., Hawkins R.D., Martin K., et al. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell. 87:1996;1015-1023.
93. Burnett A.L., Nelson R.J., Calvin D.C., et al. Nitric oxide-dependent penile erection in mice lacking neuronal nitric oxide synthase. Mol Med. 2:1996;288-296.
94. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H., Fishman M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell. 75:1993;1273-1286.
95. Burnett A.L., Calvin D.C., Chamness S.L., et al. Urinary bladder-urethral sphincter dysfunction in mice with targeted disruption of neuronal nitric oxide synthase models idiopathic voiding disorders in humans. Nat Med. 3:1997;571-574.
96. Desai K.M., Sessa W.C., Vane J.R. Involvement of nitric oxide in the reflex relaxation of the stomach to accommodate food or fluid. Nature. 351:1991;477-479.
97. Mashimo H., He X.D., Huang P.L., Fishman M.C., Goyal R.K. Neuronal constitutive nitric oxide synthase is involved in murine enteric inhibitory neurotransmission. J Clin Invest. 98:1996;8-13.
98. Nelson R.J., Demas G.E., Huang P.L., et al. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase [see comments]. Nature. 378:1995;383-386.
99. Huang Z., Huang P.L., Panahian N., et al. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science. 265:1994;1883-1885.
100. Dawson V.L., Kizushi V.M., Huang P.L., Snyder S.H., Dawson T.M. Resistance to neurotoxicity in cortical cultures from neuronal nitric oxide synthase-deficient mice. J Neurosci. 16:1996;2479-2487.
101. Schulz J.B., Huang P.L., Matthews R.T., et al. Striatal malonate lesions are attenuated in neuronal nitric oxide synthase knockout mice. J Neurochem. 67:1996;430-433.
102. MacMicking J.D., Nathan C., Hom G., et al. Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell. 81:1995;641-650. [published erratum appears in Cell 1995 Jun 30;81(7):following 1170].
103. Wei X.Q., Charles I.G., Smith A., et al. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature. 375:1995;408-411.
104. Laubach V.E., Shesely E.G., Smithies O., Sherman P.A. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc Natl Acad Sci USA. 92:1995;10688-10692.
105. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:1992;3051-3064.
106. Moncada S., Palmer R.M., Higgs E.A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 43:1991;109-142.
107. Hickey M.J., Sharkey K.A., Sihota E.G., et al. Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia. FASEB J. 11:1997;955-964.
108. Gunnett C.A., Chu Y., Heistad D.D., Loihl A., Faraci F.M. Vascular effects of LPS in mice deficient in expression of the gene for inducible nitric oxide synthase. Am J Physiol. 275:1998;H416-421.
109. Hibbs J.B. Jr., Taintor R.R., Vavrin Z. Macrophage cytotoxicity: role for L-arginine deiminase and imino nitrogen oxidation to nitrite. Science. 235:1987;473-476.
110. Hibbs J.B. Jr., Taintor R.R., Vavrin Z., Rachlin E.M. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem Biophys Res Commun. 157:1989;87-94.
111. Stuehr D., Marletta M.A. Mammalian nitrate biosynthesis: mouse macrophages produces nitrite and nitrate in response to E. coli lipopolysaccharide. Proc Natl Acad Sci USA. 82:1985;7738-7742.
112. Stuehr D.J., Nathan C.F. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J Exp Med. 169:1989;1543-1555.
113. Garvey E.P., Oplinger J.A., Tanoury G.J., et al. Potent and selective inhibition of human nitric oxide synthases. Inhibition by non-amino acid isothioureas. J Biol Chem. 269:1994;26669-26676.
114. Furchgott R.F., Zawadski J.V. The obligatory role of the endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 288:1981;373-376.
115. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA. 84:1987;9265-9269.
116. Palmer R.M.J., Ferrige A.G., Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327:1987;524-526.
117. Huang P.L., Huang Z., Mashimo H., et al. Hypertension in mice lacking the gene for endothelial nitric oxide synthase [see comments]. Nature. 377:1995;239-242.
118. Shesely E.G., Maeda N., Kim H.S., et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 93:1996;13176-13181.
119. Godecke A., Decking U.K., Ding Z., et al. Coronary hemodynamics in endothelial NO synthase knockout mice. Circ Res. 82:1998;186-194.
120. Steudel W., Scherrer-Crosbie M., Bloch K.D., et al. Sustained pulmonary hypertension and right ventricular hypertrophy after chronic hypoxia in mice with congenital deficiency of nitric oxide synthase 3. J Clin Invest. 101:1998;2468-2477.
121. Rees D.D., Palmer R.M., Moncada S. Role of endothelium-derived nitric oxide in the regulation of blood pressure. Proc Natl Acad Sci USA. 86:1989;3375-3378.
122. G-methylarginine, an inhibitor of endothelium-derived nitric oxide synthesis, is a potent pressor agent in the guinea pig: does nitric oxide regulate blood pressure in vivo? Biochem Biophys Res Commun. 160:1989;881-886.
123. Kurihara N., Alfie M.E., Sigmon D.H., et al. Role of nNOS in blood pressure regulation in eNOS null mutant mice. Hypertension. 32:1988;856-861.
124. Faraci F.M., Sigmund C.D., Shesely E.G., Maeda N., Heistad D.D. Responses of carotid artery in mice deficient in expression of the gene for endothelial NO synthase. Am J Physiol. 274:1998;H564-H570.
125. Tronc F., Wassef M., Esposito B., et al. Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arterioscler Thromb Vasc Biol. 16:1996;1256-1262.
126. Rudic R.D., Shesely E.G., Maeda N., et al. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest. 101:1998;731-736.
127. Langille B.L., O'Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science. 231:1986;405-407.
128. Moroi M., Zhang L., Yasuda T., et al. Interaction of genetic deficiency of endothelial nitric oxide, gender, and pregnancy in vascular response to injury in mice. J Clin Invest. 101:1998;1225-1232.
129. Ziche M., Morbidelli L., Masini E., et al. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest. 94:1994;2036-2044.
130. Papapetropoulos A., Garcia-Cardena G., Madri J.A., Sessa W.C. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest. 100:1997;3131-3139.
131. Hanahan D. Signaling vascular morphogenesis and maintenance [comment]. Science. 277:1997;48-50.
132. Murohara T., Asahara T., Silve M., et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest. 101:1998;2567-2578.