Role of interferon alpha in endothelial dysfunction: Insights into endothelial nitric oxide synthase-related mechanisms

American Journal of the Medical Sciences

Volumn 348, Issue 2, 2014, Pages 168-175

  Jones Buie, Joy N ^a   Oates, Jim C ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Autoimmune disease; Endothelial dysfunction; Endothelial nitric oxide synthase; Lupus; SLE; Systemic Lupus Erythematosus; Type I interferons

Indexed keywords

ALPHA INTERFERON; ARGINASE; ARGININE; AUTOANTIBODY; C REACTIVE PROTEIN; CD11 ANTIGEN; CD18 ANTIGEN; CD40 LIGAND; DOUBLE STRANDED DNA ANTIBODY; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 17; NITRIC OXIDE; PEROXYNITRITE; PREDNISOLONE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE; TETRAHYDROBIOPTERIN; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR SP1; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

ARTERIAL WALL THICKNESS; ATHEROGENESIS; ATHEROSCLEROSIS; BIOAVAILABILITY; BRACHIAL ARTERY; CARDIOTOXICITY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR RISK; CORONARY ARTERY DISEASE; DIABETES MELLITUS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIAL PROGENITOR CELL; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; HEART FAILURE; HEPATITIS C; HUMAN; HYPERTENSION; ISCHEMIC HEART DISEASE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PREMENOPAUSE; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; THROMBOCYTE AGGREGATION; VASODILATATION;

ENDOTHELIUM, VASCULAR; HUMANS; INTERFERON-ALPHA; NITRIC OXIDE SYNTHASE TYPE III;

EID: 84905112171     PISSN: 00029629     EISSN: 15382990     Source Type: Journal    
DOI: 10.1097/MAJ.0000000000000284     Document Type: Review

References (89)

1. Berliner JA, Navab M, Fogelman AM, et al. Atherosclerosis: basic mechanisms: oxidation, inflammation, and genetics. Circulation 1995; 91(9):2488-96.
2. Cominacini L, Pasini AF, Garbin U, et al. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cellsinduces the activation of NF-kappaB through an increased production of intracellular reactive oxygen species. J Biol Chem 2000;275:12633-8.
3. Cines DB, Pollak ES, Buck CA, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998;91:3527-61.
4. Fleming I. Molecular mechanisms underlying the activation of eNOS. Pflugers Arch 2010;459:793-806.
5. Amissah-Arthur MB, Gordon C. GPs have key role in shared care of patients with SLE. Practitioner 2009;253:19-24, 12.
6. Urowitz MB, Bookman AAM, Koehler BE, et al. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med 1976; 60:221-5.
7. Korkmaz C, Cansu DU, Kasifoglu T. Myocardial infarction in young patients (, or 535 years of age) with systemic lupus erythematosus: a case report and clinical analysis of the literature. Lupus 2007;16:289-97.
8. Jude EB, Douglas JT, Anderson SG, et al. Circulating cellular adhesion molecules ICAM-1, VCAM-1, P- and E-selectin in the prediction of cardiovascular disease in diabetes mellitus. Eur J Intern Med 2002;13:185-9.
9. Deanfield J, Donald A, Ferri C, et al. Endothelial function and dysfunction. Part I: methodological issues for assessment in the different vascular beds: a statement by the orking group on endothelin and endothelial factors of the European Society of Hypertension. J Hypertens 2005;23:7-17.
10. El-Magadmi M, Bodill H, Ahmad Y, et al. Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation 2004;110:399-404.
11. Valdivielso P, Gomez-Doblas JJ, Macias M, et al. Lupus-associated endothelial dysfunction, disease activity and arteriosclerosis. Clin Exp Rheumatol 2008;26:827-33.
12. Lee SK, Kim JH, Yang WS, et al. Exogenous nitric oxide inhibits VCAM-1 expression in human peritoneal mesothelial cells. Role of cyclic GMP and NF-kappaB. Nephron 2002;90:447-54.
13. Berendji-Grun D, Kolb-Bachofen V, Kroncke KD. Nitric oxide inhibits endothelial IL-1[beta]-induced ICAM-1 gene expression at the transcriptional level decreasing Sp1 and AP-1 activity. Mol Med 2001;7:748-54.
14. Padmaja S, Huie RE. The reaction of nitric oxide with organic peroxyl radicals. Biochem Biophys Res Commun 1993;195:539-44.
15. Roberts W, Michno A, Aburima A, et al. Nitric oxide inhibits von Willebrand factor-mediated platelet adhesion and spreading through regulation of integrin alpha(IIb)beta(3) and myosin light chain. J Thromb Haemost 2009;7:2106-15.
16. Takeuchi K, Watanabe H, Tran QK, et al. Nitric oxide: inhibitory effects on endothelial cell calcium signaling, prostaglandin I2 production and nitric oxide synthase expression. Cardiovasc Res 2004;62:194-201.
17. Zervou MI, Vazgiourakis VM, Yilmaz N, et al. TRAF1/C5, eNOS, C1q, but not STAT4 and PTPN22 gene polymorphisms are associated with genetic susceptibility to systemic lupus erythematosus in Turkey. Hum Immunol 2011;72:1210-3.
18. Tesauro M, Thompson WC, Rogliani P, et al. Intracellular processing of endothelial nitric oxide synthase isoforms associated with differences in severity of cardiopulmonary diseases: cleavage of proteins with aspartate vs. glutamate at position 298. Proc Natl Acad Sci U S A 2000;97:2832-5.
19. Miyamoto Y, Saito Y, Nakayama M, et al. Replication protein A1 reduces transcription of the endothelial nitric oxide synthase gene containing a -786T-.C mutation associated with coronary spastic angina. Hum Mol Genet 2000;9:2629-37.
20. Anderson HD, Rahmutula D, Gardner DG. Tumor necrosis factoralpha inhibits endothelial nitric-oxide synthase gene promoter activity in bovine aortic endothelial cells. The J Biol Chem 2004;279:963-9.
21. Nguyen H, Chiasson VL, Chatterjee P, et al. Interleukin-17 causes Rho-kinase-mediated endothelial dysfunction and hypertension. Cardiovasc Res 2013;97:696-704.
22. Chrobak I, Lenna S, Stawski L, et al. Interferon-gamma promotes vascular remodeling in human microvascular endothelial cells by upregulating endothelin (ET)-1 and transforming growth factor (TGF) beta2. J Cell Physiol 2013;228:1774-83.
23. Chen C, Chai H, Wang X, et al. Soluble CD40 ligand induces endothelial dysfunction in human and porcine coronary artery endothelial cells. Blood 2008;112:3205-16.
24. Venugopal SK, Devaraj S, Yuhanna I, et al. Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells. Circulation 2002;106:1439-41.
25. Stauss HM, Godecke A, Mrowka R, et al. Enhanced blood pressure variability in eNOS knockout mice. Hypertension 1999;33:1359-63.
26. Feng Q, Song W, Lu X, et al. Development of heart failure and congenital septal defects in mice lacking endothelial nitric oxide synthase. Circulation 2002;106:873-9.
27. Lee TC, Zhao YD, Courtman DW, et al. Abnormal aortic valve development in mice lacking endothelial nitric oxide synthase. Circulation 2000;101:2345-8.
28. Lee PC, Salyapongse AN, Bragdon GA, et al. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol 1999;277: H1600-8.
29. Pointer MA, Daumerie G, Bridges L, et al. Physiological stress increases renal injury in eNOS-knockout mice. Hypertens Res 2012;35:318-24.
30. Li Q, Verma A, Han PY, et al. Diabetic eNOS-knockout mice develop accelerated retinopathy. Invest Ophthalmol Vis Sci 2010;51:5240-6.
31. Mohan S, Reddick RL, Musi N, et al. Diabetic eNOS knockout mice develop distinct macro- and microvascular complications. Lab Invest 2008;88:515-28.
32. Duplain H, Burcelin R, Sartori C, et al. Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 2001;104:342-5.
33. Knowles JW, Reddick RL, Jennette JC, et al. Enhanced atherosclerosis and kidney dysfunction in eNOS(-/-)Apoe(-/-) mice are ameliorated by enalapril treatment. J Clin Invest 2000;105:451-8.
34. Gilkeson GS, Mashmoushi AK, Ruiz P, et al. Endothelial nitric oxide synthase reduces crescentic and necrotic glomerular lesions, reactive oxygen production, and MCP1 production in murine lupus nephritis. PLoS One 2013;8:e64650.
35. Al Gadban MM, German J, Truman JP, et al. Lack of nitric oxide synthases increases lipoprotein immune complex deposition in the aorta and elevates plasma sphingolipid levels in lupus. Cell Immunol 2012; 276:42-51.
36. Somers EC, Zhao W, Lewis EE, et al. Type I interferons are associated with subclinical markers of cardiovascular disease in a cohort of systemic lupus erythematosus patients. PLoS One 2012;7:e37000.
37. Thacker SG, Zhao W, Smith CK, et al. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum 2012;64:2975-85.
38. Lee PY, Li Y, Richards HB, et al. Type I interferon as a novel risk factor for endothelial progenitor cell depletion and endothelial dysfunction in systemic lupus erythematosus. Arthritis Rheum 2007;56:3759-69.
39. Ronnblom L, Alm GV. A pivotal role for the natural interferon alphaproducing cells (plasmacytoid dendritic cells) in the pathogenesis of lupus. J Exp Med 2001;194:F59-63.
40. Ronnblom LE, Alm GV, Oberg KE. Possible induction of systemic lupus erythematosus by interferon-alpha treatment in a patient with a malignant carcinoid tumour. J Intern Med 1990;227:207-10.
41. Levy Z, Rachmani R, Trestman S, et al. Low-dose interferon-alpha accelerates atherosclerosis in an LDL receptor-deficient mouse model. Eur J Intern Med 2003;14:479-83.
42. Yao H, Cao CM, Jin HF, et al. Treatment of interferon-alpha in reducing the endothelium-dependent relaxation of rat thoracic aorta. Zhejiang Da Xue Xue Bao Yi Xue Ban 2003;32:202-6.
43. Werner N, Wassmann S, Ahlers P, et al. Endothelial progenitor cells correlate with endothelial function in patients with coronary artery disease. Basic Res Cardiol 2007;102:565-71.
44. Aicher A, Heeschen C, Mildner-Rihm C, et al. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat Med 2003;9:1370-6.
45. Iwakura A, Luedemann C, Shastry S, et al. Estrogen-mediated, endothelial nitric oxide synthase-dependent mobilization of bone marrowderived endothelial progenitor cells contributes to reendothelialization after arterial injury. Circulation 2003;108:3115-21.
46. Laufs U, Urhausen A, Werner N, et al. Running exercise of different duration and intensity: effect on endothelial progenitor cells in healthy subjects. Eur J Cardiovasc Prev Rehabil 2005;12:407-14.
47. George AL, Bangalore-Prakash P, Rajoria S, et al. Endothelial progenitor cell biology in disease and tissue regeneration. J Hematol Oncol 2011;4:24.
48. Denny MF, Thacker S, Mehta H, et al. Interferon-alpha promotes abnormal vasculogenesis in lupus: a potential pathway for premature atherosclerosis. Blood 2007;110:2907-15.
49. Teragawa H, Hondo T, Amano H, et al. Cardiogenic shock following recombinant alpha-2b interferon therapy for chronic hepatitis C. A case report. Jpn Heart J 1996;37:137-42.
50. Lenci I, Piccolo P, Francioso S, et al. Recurrent myocardial ischaemia during combination antiviral therapy in a patient with chronic hepatitis C and normal aminotransferase levels. Dig Liver Dis 2008;40:785-90.
51. Cauli C, Serra G, Chessa L, et al. Severe autoimmune hemolytic anemia in a patient with chronic hepatitis C during treatment with peginterferon alfa-2a and ribavirin. Haematologica 2006;91(suppl 6):ECR26.
52. Sasaki M, Sata M, Suzuki H, et al. A case of chronic hepatitis C with sinus bradycardia during IFN therapy. Kurume Med J 1998;45:161-3.
53. Kouno H, Aimitsu S, Ikemoto Y, et al. Cardiovascular complications of interferon therapy in chronic hepatitis C. Nihon Rinsho 1994;52: 1914-8.
54. Takase B, Uehata A, Fujioka T, et al. Endothelial dysfunction and decreased exercise tolerance in interferon-alpha therapy in chronic hepatitis C: relation between exercise hyperemia and endothelial function. Clin Cardiol 2001;24:286-90.
55. Takase B, Hamabe A, Uehata A, et al. Recombinant interferon alpha treatment decreases heart rate variability indices and impairs exercise tolerance in patients with chronic hepatitis. Biomed Pharmacother 2005; 1(59 suppl):S163-8.
56. Panasiuk A, Prokopowicz D, Panasiuk B. Monocyte chemotactic protein-1 and soluble adhesion molecules as possible prognostic markers of the efficacy of antiviral treatment in chronic hepatitis C. World J Gastroenterol 2004;10:3639-42.
57. Erol MK, Erol S, Koruk M, et al. Effects of interferon-alpha therapy on cardiac function in patients with chronic hepatitis B infection. Heart Vessels 2004;19:263-6.
58. Zhu Y, Tibensky I, Schmidt J, et al. Interferon-alpha in combination with chemotherapy has potent antiangiogenic properties in an orthotopic mouse model for pancreatic adenocarcinoma. J Immunother 2008;31:28-33.
59. Radaeva S, Jaruga B, Hong F, et al. Interferon-alpha activates multiple STAT signals and down-regulates c-Met in primary human hepatocytes. Gastroenterology 2002;122:1020-34.
60. Kumar S, Sun X, Wedgwood S, et al. Hydrogen peroxide decreases endothelial nitric oxide synthase promoter activity through the inhibition of AP-1 activity. Am J Physiol Lung Cell Mol Physiol 2008;295:L370-7.
61. Adam L, Black PC, Kassouf W, et al. Adenoviral mediated interferonalpha 2b gene therapy suppresses the pro-angiogenic effect of vascular endothelial growth factor in superficial bladder cancer. J Urol 2007;177:1900-6.
62. Schwartz R, Osborne-Lawrence S, Hahner L, et al. C-reactive protein downregulates endothelial NO synthase and attenuates reendothelialization in vivo in mice. Circ Res 2007;100:1452-9.
63. Yang X, Nath A, Opperman MJ, et al. The double-stranded RNAdependent protein kinase differentially regulates insulin receptor substrates 1 and 2 in HepG2 cells. Mol Biol Cell 2010;21:3449-58.
64. Chu WM, Ostertag D, Li ZW, et al. JNK2 and IKKbeta are required for activating the innate response to viral infection. Immunity 1999;11:721-31.
65. Goh KC, deVeer MJ, Williams BR. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J 2000;19:4292-7.
66. Salven P, Anttonen K, Repo H, et al. Endotoxins induce and interferon alpha suppresses vascular endothelial growth factor (VEGF) production in human peripheral blood mononuclear cells. FASEB J 2001; 15:1318-20.
67. Wada H, Nagano H, Yamamoto H, et al. Combination of interferon-alpha and 5-fluorouracil inhibits endothelial cell growth directly and by regulation of angiogenic factors released by tumor cells. BMC Cancer 2009;9:361.
68. Tsutsui M, Milstien S, Katusic ZS. Effect of tetrahydrobiopterin on endothelial function in canine middle cerebral arteries. Circ Res 1996; 79:336-42.
69. Katusic ZS, d'Uscio LV. Tetrahydrobiopterin: mediator of endothelial protection. Arterioscler Thromb Vasc Biol 2004;24:397-8.
70. Forstermann U, Closs EI, Pollock JS, et al. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 1994;23:1121-31.
71. Harrison DG. Cellular and molecular mechanisms of endothelial cell dysfunction. J Clin Invest 1997;100:2153-2157.
72. Kitagami T, Yamada K, Miura H, et al. Mechanism of systemically injected interferon-alpha impeding monoamine biosynthesis in rats: role of nitric oxide as a signal crossing the blood-brain barrier. Brain Res 2003;978:104-14.
73. Felger JC, Li L, Marvar PJ, et al. Tyrosine metabolism during interferon-alpha administration: association with fatigue and CSF dopamine concentrations. Brain Behav Immun 2013;31:153-60.
74. Cosentino F, Patton S, d'Uscio LV, et al. Tetrahydrobiopterin alters superoxide and nitric oxide release in prehypertensive rats. J Clin Invest 1998;101:1530-7.
75. Schildknecht S, van der Loo B, Weber K, et al. Endogenous peroxynitrite modulates PGHS-1-dependent thromboxane A2 formation and aggregation in human platelets. Free Radic Biol Med 2008;45:512-20.
76. Casanello P, Krause B, Torres E, et al. Reduced l-arginine transport and nitric oxide synthesis in human umbilical vein endothelial cells from intrauterine growth restriction pregnancies is not further altered by hypoxia. Placenta 2009;30:625-33.
77. Shin WS, Berkowitz DE, Ryoo SW. Increased arginase II activity contributes to endothelial dysfunction through endothelial nitric oxide synthase uncoupling in aged mice. Exp Mol Med 2012;44:594-602.
78. Kim JH, Bugaj LJ, Oh YJ, et al. Arginase inhibition restores NOS coupling and reverses endothelial dysfunction and vascular stiffness in old rats. J Appl Physiol (1985) 2009;107:1249-57.
79. Fekkes D, Bannink M, Kruit WH, et al. Influence of pegylated interferon-alpha therapy on plasma levels of citrulline and arginine in melanoma patients. Amino Acids 2007;32:121-6.
80. Lu DY, Leung YM, Su KP. Interferon-alpha induces nitric oxide synthase expression and haem oxygenase-1 down-regulation in microglia: implications of cellular mechanism of IFN-alpha-induced depression. Int J Neuropsychopharmacol 2013;16:433-44.
81. Arnal JF, Tack I, Besombes JP, et al. Nitric oxide and superoxide anion production during endothelial cell proliferation. Am J Physiol 1996;271:C1521-1526.
82. Sukumar P, Viswambharan H, Imrie H, et al. Nox2 NADPH oxidase has a critical role in insulin resistance-related endothelial cell dysfunction. Diabetes 2013;62:2130-4.
83. Guzik TJ, Sadowski J, Kapelak B, et al. Systemic regulation of vascular NAD(P)H oxidase activity and nox isoform expression in human arteries and veins. Arterioscler Thromb Vasc Biol 2004;24: 1614-20.
84. Kou B, Ni J, Vatish M, et al. Xanthine oxidase interaction with vascular endothelial growth factor in human endothelial cell angiogenesis. Microcirculation 2008;15:251-67.
85. Alp NJ, McAteer MA, Khoo J, et al. Increased endothelial tetrahydrobiopterin synthesis by targeted transgenic GTP-cyclohydrolase I overexpression reduces endothelial dysfunction and atherosclerosis in ApoE-knockout mice. Arteriosclerosis Thromb Vasc Biol 2004;24:445-50.
86. Singh U, Devaraj S, Vasquez-Vivar J, et al. C-reactive protein decreases endothelial nitric oxide synthase activity via uncoupling. J Mol Cell Cardiol 2007;43:780-91.
87. Munzel T, Daiber A, Ullrich V, et al. Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cGMP-dependent protein kinase. Arteriosclerosis Thromb Vasc Biol 2005;25:1551-7.
88. Nistala R, Whaley-Connell A, Sowers JR. Redox control of renal function and hypertension. Antioxid Redox Signal 2008;10:2047-89.
89. Nishiwaki H, Ogura Y, Miyamoto K, et al. Prednisolone, plateletactivating factor receptor antagonist, or superoxide dismutase reduced leukocyte entrapment induced by interferon alpha in retinal microcirculation. Invest Ophthalmol Vis Sci 1997;38:811-6.