Redoxmechanisms of the beneficial effects of heme oxygenase in hypertension

Journal of Hypertension

Volumn 32, Issue 7, 2014, Pages 1379-1387

  Chan, Elsa C ^a   Dusting, Gregory J ^a   Liu, Guei Sheung ^a   Jiang, Fan ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b SHANDONG UNIVERSITY   (China)

Author keywords

Bilirubin; Carbon monoxide; Heme oxygenase; Hypertension; NADPH oxidase; Oxidative stress

Indexed keywords

BILIRUBIN DERIVATIVE; BILIVERDIN; CARBON MONOXIDE; HEME OXYGENASE; HEME OXYGENASE 1; HEME OXYGENASE 2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; BILIRUBIN;

BLOOD PRESSURE REGULATION; CENTRAL NERVOUS SYSTEM; CLINICAL TRIAL (TOPIC); ENDOTHELIUM CELL; ENZYME MECHANISM; EXPERIMENTAL HYPERTENSION; HUMAN; HYPERTENSION; IN VITRO STUDY; IN VIVO STUDY; KIDNEY PARENCHYMA; META ANALYSIS (TOPIC); NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASCULITIS; ANIMAL; DISEASE MODEL; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; VASCULAR REMODELING;

ANIMALS; BILIRUBIN; BILIVERDINE; CARBON MONOXIDE; DISEASE MODELS, ANIMAL; HEME OXYGENASE-1; HUMANS; HYPERTENSION; NADPH OXIDASE; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; VASCULAR REMODELING; VASCULITIS;

EID: 84903878703     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0000000000000179     Document Type: Review

References (104)

1. Maines MD. The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 1997; 37:517-554
2. Abraham NG, Kappas A. Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 2008; 60:79-127
3. Alam J, Cook JL. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 2007; 36:166-174
4. Dulak J, Deshane J, Jozkowicz A, Agarwal A. Heme oxygenase-1 and carbon monoxide in vascular pathobiology: focus on angiogenesis. Circulation 2008; 117:231-241
5. Maines MD, Trakshel GM, Kutty RK. Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 1986; 261:411-419
6. McCoubrey WK, Huang TJ, Maines MD. Isolation and characterization of a cDNA from the rat brain that encodes hemoprotein hemeoxygenase-3. Eur J Biochem 1997; 247:725-732
7. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Ann Rev Pharmacol Toxicol 2010; 50:323-354
8. Kusumoto K, Kawahara T, Kuwano Y, Teshima-Kondo S, Morita K, Kishi K, et al. Ecabet sodium inhibits Helicobacter pylori lipopolysaccharide-induced activation of NADPH oxidase 1 or apoptosis of guinea pig gastric mucosal cells. Am J Physiol Gastrointest Liver Physiol 2005; 288:G300-G307
9. Stocker R. Antioxidant activities of bile pigments. Antioxid Redox Signal 2004; 6:841-849
10. Datla SR, Dusting GJ, Mori TA, Taylor CJ, Croft KD, Jiang F. Induction of heme oxygenase-1 in vivo suppresses NADPH oxidase derived oxidative stress. Hypertension 2007; 50:636-642
11. Seta F, Bellner L, Rezzani R, Regan RF, Dunn MW, Abraham NG, et al. Heme oxygenase-2 is a critical determinant for execution of an acute inflammatory and reparative response. Am J Pathol 2006; 169:1612-1623
12. Bellner L, Martinelli L, Halilovic A, Patil K, Puri N, Dunn MW, et al. Heme oxygenase-2 deletion causes endothelial cell activation marked by oxidative stress, inflammation, and angiogenesis. J Pharmacol Exp Ther 2009; 331:925-932
13. D'Agostino D, Mazza EJ, Neubauer JA. Heme oxygenase is necessary for the excitatory response of cultured neonatal rat rostral ventrolateral medulla neurons to hypoxia. Am J Physiol Regul Integr Comp Physiol 2009; 296:R102-R118
14. Piotrowska AP, Solari V, Caluwé DD, Puri P. Immunocolocalization of the heme oxygenase-2 and interstitial cells of Cajal in normal and aganglionic colon. J Pediatr Surg 2003; 38:73-77
15. Chin HJ, Song YR, Kim HS, Park M, Yoon HJ, Na KY, et al. The bilirubin level is negatively correlated with the incidence of hypertension in normotensive Korean population. J Korean Med Sci 2009; 24 (Suppl):S50-S56
16. Papadakis JA, Ganotakis ES, Jagroop IA, Mikhailidis DP, Winder AF. Effect of hypertension and its treatment on lipid, lipoprotein(a), fibrinogen, and bilirubin levels in patients referred for dyslipidemia. Am J Hypertens 1999; 12:673-681
17. Kreiser D, Baum M, Seidman DS, Fanaroff A, Shah D, Hendler I, et al. End tidal carbon monoxide levels are lower in women with gestational hypertension and preeclampsia. J Perinatol 2004; 24:213-217
18. Chen YH, Chau LY, Chen JW, Lin SJ. Serum bilirubin and ferritin levels link heme oxygenase-1 gene promoter polymorphism and susceptibility to coronary artery disease in diabetic patients. Diabetes Care 2008; 31:1615-1620
19. Alba G, El Bekay R, Chacon P, Reyes ME, Ramos E, Olivan J, et al. Heme oxygenase-1 expression is down-regulated by angiotensin II and under hypertension in human neutrophils. J Leukoc Biol 2008; 84:397-405
20. Djousse L, Levy D, Cupples LA, Evans JC, D'Agostino RB, Ellison RC. Total serum bilirubin and risk of cardiovascular disease in the Framingham offspring study. Am J Cardiol 2001; 87:1196-1200
21. Hopkins PN, Wu LL, Hunt SC, James BC, Vincent GM, Williams RR. Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease. Arterioscler Thromb Vasc Biol 1996; 16:e250-e255
22. Schwertner HA, Jackson WG, Tolan G. Association of low serum concentration of bilirubin with increased risk of coronary artery disease. Clin Chem 1994; 40:18-23
23. Novotny L, Vitek L. Inverse relationship between serum bilirubin and atherosclerosis in men: A meta-analysis of published studies. Exp Biol Med (Maywood) 2003; 228:568-571
24. Li JM, Shah AM. Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 2004; 287:R1014-R1030
25. Ishizaka N, León HD, Laursen JB, Fukui T, Wilcox JN, Keulenaer GD, et al. Angiotensin II-induced hypertension increases heme oxygenase-1 expression in rat aorta. Circulation 1997; 96:1923-1929
26. Aizawa T, Ishizaka N, Taguchi J, Nagai R, Mori I, Tang SS, et al. Heme oxygenase-1 is upregulated in the kidney of angiotensin II-induced hypertensive rats: Possible role in renoprotection. Hypertension 2000; 35:800-806
27. Cheng G, Lambeth JD. NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J Biol Chem 2004; 279:4737-4742
28. Teran FJ, Johnson RA, Stevenson BK, Peyton KJ, Jackson KE, Appleton SD, et al. Heme oxygenase-derived carbon monoxide promotes arteriolar endothelial dysfunction and contributes to salt-induced hypertension in Dahl salt-sensitive rats. Am J Physiol Regul Integr Comp Physiol 2005; 288:R615-R622
29. Johnson RA, Teran FJ, Durante W, Peyton KJ, Johnson FK. Enhanced heme oxygenase-mediated coronary vasodilation in Dahl salt-sensitive hypertension. Am J Hypertens 2004; 17:25-30
30. Johnson FK, Durante W, Peyton KJ, Johnson RA. Heme oxygenase inhibitor restores arteriolar nitric oxide function in Dahl rats. Hypertension 2003; 41:149-155
31. Nath KA, d'Uscio LV, Juncos JP, Croatt AJ, Manriquez MC, Pittock ST, et al. An analysis of the DOCA-salt model of hypertension in HO-1-/-mice and the Gunn rat. Am J Physiol Heart Circ Physiol 2007; 293:H333-H342
32. Wiesel P, Patel AP, Carvajal IM, Wang ZY, Pellacani A, Maemura K, et al. Exacerbation of chronic renovascular hypertension and acute renal failure in heme oxygenase-1-deficient mice. Circ Res 2001; 88:1088-1094
33. George EM, Hosick PA, Stec DE, Granger JP. Heme oxygenase inhibition increases blood pressure in pregnant rats. Am J Hypertens 2013; 26:924-930
34. Stec DE, Vera T, Storm MV, McLemore GRJ, Ryan MJ. Blood pressure and renal blow flow responses in heme oxygenase-2 knockout mice. Am J Physiol Regul Integr Comp Physiol 2009; 297:R1822-R1828
35. Yang L, Quan S, Nasjletti A, Laniado-Schwartzman M, Abraham NG. Heme oxygenase-1 gene expression modulates angiotensin IIinduced increase in blood pressure. Hypertension 2004; 43:1221-1226
36. Pradhan A, Umezu M, Fukagawa M. Heme-oxygenase upregulation ameliorates angiotensin II-induced tubulointerstitial injury and saltsensitive hypertension. Am J Nephrol 2006; 26:552-561
37. Johnson RA, Lavesa M, DeSeyn K, Scholer MJ, Nasjletti A. Heme oxygenase substrates acutely lower blood pressure in hypertensive rats. Am J Physiol 1996; 271:H1132-H1138
38. Ndisang JF, Zhao W, Wang R. Selective regulation of blood pressure by heme oxygenase-1 in hypertension. Hypertension 2002; 40:315-321
39. Cheng PY, Chen JJ, Yen MH. The expression of heme oxygenase-1 and inducible nitric oxide synthase in aorta during the development of hypertension in spontaneously hypertensive rats. Am J Hypertens 2004; 17:1127-1134
40. Wang R, Shamloul R, Wang X, Meng Q, Wu L. Sustained normalization of high blood pressure in spontaneously hypertensive rats by implanted hemin pump. Hypertension 2006; 48:685-692
41. Stec DE, Drummond HA, Gousette MU, Storm MV, Abraham NG, Csongradi E. Expression of heme oxygenase-1 in thick ascending loop of Henle attenuates angiotensin II-dependent hypertension. J Am Soc Nephrol 2012; 23:834-841
42. Motterlini R, Green CJ, Foresti R. Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal 2002; 4:615-624
43. Pflueger A, Croatt AJ, Peterson TE, Smith LA, d'Uscio LV, Katusic ZS, et al. The hyperbilirubinemic Gunn rat is resistant to the pressor effects of angiotensin II. Am J Physiol Renal Physiol 2005; 288:F552-F558
44. Pauletto P, Rattazzi M. Inflammation and hypertension: The search for a link. Nephrol Dial Transplant 2006; 21:850-853
45. Savoia C, Schiffrin EL. Vascular inflammation in hypertension and diabetes: molecular mechanisms and therapeutic interventions. Clin Sci (Lond) 2007; 112:375-384
46. Boos CJ, Lip GY. Is hypertension an inflammatory process? Curr Pharm Des 2006; 12:1623-1635
47. Savoia C, Schiffrin EL. Inflammation in hypertension. Curr Opin Nephrol Hypertens 2006; 15:152-158
48. Harrison DG, Guzik TJ, Lob HE, Madhur MS, Marvar PJ, Thabet SR, et al. Inflammation, immunity, and hypertension. Hypertension 2011; 57:132-140
49. Montecucco F, Pende A, Quercioli A, Mach F. Inflammation in the pathophysiology of essential hypertension. J Nephrol 2011; 24:23-34
50. Waki H, Gouraud SS, Maeda M, Raizada MK, Paton JF. Contributions of vascular inflammation in the brainstem for neurogenic hypertension. Respir Physiol Neurobiol 2011; 178:422-428
51. Zhu X, Fan WG, Li DP, Kung H, Lin MC. Heme oxygenase-1 system and gastrointestinal inflammation: A short review. World J Gastroenterol 2011; 17:4283-4288
52. Durante W. Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Front Biosci (Landmark Ed) 2011; 16: 2372-2388
53. Takagi T, Naito Y, Uchiyama K, Yoshikawa T. The role of heme oxygenase and carbon monoxide in inflammatory bowel disease. Redox Rep 2010; 15:193-201
54. Alcaraz MJ, Fernandez P, Guillen MI. Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr Pharm Des 2003; 9:2541-2551
55. Durante W. Protective role of heme oxygenase-1 against inflammation in atherosclerosis. Front Biosci 2011; 16:2372-2388
56. Pinto RF, Higuchi Mde L, Aiello VD. Decreased numbers of T-lymphocytes and predominance of recently recruited macrophages in the walls of peripheral pulmonary arteries from 26 patients with pulmonary hypertension secondary to congenital cardiac shunts. Cardiovasc Pathol 2004; 13:268-275
57. Vergadi E, Chang MS, Lee C, Liang OD, Liu X, Fernandez-Gonzalez A, et al. Early macrophage recruitment and alternative activation are critical for the later development of hypoxia-induced pulmonary hypertension. Circulation 2011; 123:1986-1995
58. Elmarakby AA, Faulkner J, Posey SP, Sullivan JC. Induction of hemeoxygenase-1 attenuates the hypertension and renal inflammation in spontaneously hypertensive rats. Pharmacol Res 2010; 62:400-407
59. Tracz MJ, Juncos JP, Croatt AJ, Ackerman AW, Grande JP, Knutson KL, et al. Deficiency of heme oxygenase-1 impairs renal hemodynamics and exaggerates systemic inflammatory responses to renal ischemia. Kidney Int 2007; 72:1073-1080
60. Schiffrin EL. Remodeling of resistance arteries in essential hypertension and effects of antihypertensive treatment. Am J Hypertens 2004; 17:1192-1200
61. Rizzoni D, Agabiti Rosei E. Small artery remodeling in hypertension and diabetes. Curr Hypertens Rep 2006; 8:90-95
62. Christou H, Morita T, Hsieh CM, Koike H, Arkonac B, Perrella MA, et al. Prevention of hypoxia-induced pulmonary hypertension by enhancement of endogenous heme oxygenase-1 in the rat. Circ Res 2000; 86:1224-1229
63. Vitali SH, Mitsialis SA, Liang OD, Liu X, Fernandez-Gonzalez A, Christou H, et al. Divergent cardiopulmonary actions of heme oxygenase enzymatic products in chronic hypoxia. PLoS One 2009; 4:e5978
64. Li Volti G, Wang J, Traganos F, Kappas A, Abraham NG. Differential effect of heme oxygenase-1 in endothelial and smooth muscle cell cycle progression. Biochem Biophys Res Commun 2002; 296:1077-1082
65. Chang T, Wu L, Wang R. Inhibition of vascular smooth muscle cell proliferation by chronic hemin treatment. Am J Physiol Heart Circ Physiol 2008; 295:H999-H1007
66. Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension: Clinical implications and therapeutic possibilities. Diabetes Care 2008; 31 (S2):S170-S180
67. Harrison DG, Gongora MC. Oxidative stress and hypertension. Med Clin North Am 2009; 93:621-635
68. Datla SR, Griendling KK. Reactive oxygen species, NADPH oxidases, and hypertension. Hypertension 2010; 56:325-330
69. Chan EC, Jiang F, Peshavariya HM, Dusting GJ. Regulation of cell proliferation by NADPH oxidase-mediated signaling: Potential roles in tissue repair, regenerative medicine and tissue engineering. Pharmacol Ther 2009; 122:97-108
70. Mandraffino G, Sardo MA, Riggio S, Loddo S, Imbalzano E, Alibrandi A, et al. Circulating progenitor cells are increased in newly diagnosed untreated hypertensive patients with arterial stiffening but normal carotid intima-media thickness. Hypertens Res 2011; 34:876-883
71. Zhang J, Youn JY, Kim AY, Ramirez RJ, Gao L, Ngo D, et al. NOX4-dependent hydrogen peroxide overproduction in human atrial fibrillation and HL-1 atrial cells: relationship to hypertension. Front Physiol 2012; 3:140
72. Moreno MU, San Jose G, Fortuno A, Beloqui O, Redon J, Chaves FJ, et al. A novel CYBA variant, the -675A/T polymorphism, is associated with essential hypertension. J Hypertens 2007; 25:1620-1626
73. Fujita M, Ando K, Nagae A, Fujita T. Sympathoexcitation by oxidative stress in the brain mediates arterial pressure elevation in salt-sensitive hypertension. Hypertension 2007; 50:360-367
74. Chan SH, Hsu KS, Huang CC, Wang LL, Ou CC, Chan JY. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla. Circ Res 2005; 97:772-780
75. Nozoe M, Hirooka Y, Koga Y, Sagara Y, Kishi T, Engelhardt JF, et al. Inhibition of Rac1-derived reactive oxygen species in nucleus tractus solitarius decreases blood pressure and heart rate in stroke-prone spontaneously hypertensive rats. Hypertension 2007; 50:62-68
76. Zimmerman MC, Dunlay RP, Lazartigues E, Zhang Y, Sharma RV, Engelhardt JF, et al. Requirement for Rac1-dependent NADPH oxidase in the cardiovascular and dipsogenic actions of angiotensin II in the brain. Circ Res 2004; 95:532-539
77. Peshavariya H, Jiang F, Taylor CJ, Selemidis S, Chang CW, Dusting GJ. Translation-linked mRNA destabilization accompanying seruminduced Nox4 expression in human endothelial cells. Antioxid Redox Signal 2009; 11:2399-2408
78. Kuzkaya N, Weissmann N, Harrison DG, Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: Implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 2003; 278:22546-22554
79. Murdoch CE, Alom-Ruiz SP, Wang M, Zhang M, Walker S, Yu B, et al. Role of endothelial Nox2 NADPH oxidase in angiotensin II-induced hypertension and vasomotor dysfunction. Basic Res Cardiol 2011; 106:527-538
80. Douglas G, Bendall JK, Crabtree MJ, Tatham AL, Carter EE, Hale AB, et al. Endothelial-specific Nox2 overexpression increases vascular superoxide and macrophage recruitment in ApoE(-)/(-) mice. Cardiovasc Res 2012; 94:20-29
81. Peshavariya HM, Taylor CJ, Goh C, Liu GS, Jiang F, Chan EC, et al. Annexin peptide Ac2-26 suppresses TNFa-induced inflammatory responses via inhibition of Rac1-dependent NADPH oxidase in human endothelial cells. PloS One 2013; 8:e60790
82. Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, Alom-Ruiz S, et al. Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arterioscler Thromb Vasc Biol 2011; 31:1368-1376
83. Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, et al. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res 2012; 110:1217-1225
84. Dikalova A, Clempus R, Lassegue B, Cheng G, McCoy J, Dikalov S, et al. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation 2005; 112:2668-2676
85. Gavazzi G, Banfi B, Deffert C, Fiette L, Schappi M, Herrmann F, et al. Decreased blood pressure in NOX1-deficient mice. FEBS Lett 2006; 580:497-504
86. Briones AM, Tabet F, Callera GE, Montezano AC, Yogi A, He Y, et al. Differential regulation of Nox1, Nox2 and Nox4 in vascular smooth muscle cells from WKYand SHR. J Am Soc Hypertens 2011; 5:137-153
87. Dikalova AE, Gongora MC, Harrison DG, Lambeth JD, Dikalov S, Griendling KK. Upregulation of Nox1 in vascular smooth muscle leads to impaired endothelium-dependent relaxation via eNOS uncoupling. Am J Physiol Heart Circ Physiol 2010; 299:H673-H679
88. Fulton DJ. Nox5 and the regulation of cellular function. Antioxid Redox Signal 2009; 11:2443-2452
89. Yang J, Lane PH, Pollock JS, Carmines PK. Protein kinase C-dependent NAD(P)H oxidase activation induced by type 1 diabetes in renal medullary thick ascending limb. Hypertension 2010; 55:468-473
90. Vera T, Kelsen S, Stec DE. Kidney-specific induction of heme oxygenase-1 prevents angiotensin II hypertension. Hypertension 2008; 52:660-665
91. Yogi A, Mercure C, Touyz J, Callera GE, Montezano AC, Aranha AB, et al. Renal redox-sensitive signaling, but not blood pressure, is attenuated by Nox1 knockout in angiotensin II-dependent chronic hypertension. Hypertension 2008; 51:500-506
92. Jiang F, Roberts S, Datla S, Dusting G. NO modulates NADPH oxidase function via heme oxygenase-1 in human endothelial cells. Hypertension 2006; 48:950-957
93. Moraes JA, Barcellos-de-Souza P, Rodrigues G, Nascimento-Silva V, Silva SV, Assreuy J, et al. Heme modulates smooth muscle cell proliferation and migration via NADPH oxidase: A counter-regulatory role for heme oxygenase system. Atherosclerosis 2012; 224:394-400
94. Rousset F, Nguyen MV, Grange L, Morel F, Lardy B. Heme oxygenase-1 regulates matrix metalloproteinase MMP-1 secretion and chondrocyte cell death via Nox4 NADPH oxidase activity in chondrocytes. PLoS One 2013; 8:e66478
95. Morita T. Heme oxygenase and atherosclerosis. Arterioscler Thromb Vasc Biol 2005; 25:1786-1795
96. Taille C, El-Benna J, Lanone S, Dang MC, Ogier-Denis E, Aubier M, et al. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J Biol Chem 2004; 279:28681-28688
97. Amit Y, Boneh A. Bilirubin inhibits protein kinase C activity and protein kinase C-mediated phosphorylation of endogenous substrates in human skin fibroblast. Clin Chim Acta 1993; 223:103-111
98. Basuroy S, Bhattacharya S, Leffler CW, Parfenova H. Nox4 NADPH oxidase mediates oxidative stress and apoptosis caused by TNF-alpha in cerebral vascular endothelial cells. Am J Physiol Cell Physiol 2009; 296:C422-C432
99. Wang X, Wang Y, Kim HP, Nakahira K, Ryter SW, Choi AM. Carbon monoxide protects against hyperoxia-induced endothelial cell apoptosis by inhibiting reactive oxygen species formation. J Biol Chem 2006; 282:1718-1726
100. Rodriguez AI, Gangopadhyay A, Kelley EE, Pagano PJ, Zuckerbraun BS, Bauer PM. HO-1 and CO decrease platelet-derived growth factorinduced vascular smooth muscle cell migration via inhibition of Nox1. Arterioscler Thromb Vasc Biol 2010; 30:98-104
101. Nakahira K, Kim HP, Geng XH, Nakao A, Wang X, Murase N, et al. Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts. J Exp Med 2006; 203:2377-2389
102. Kim KM, Pae HO, Zheng M, Park R, Kim YM, Chung HT. Carbon monoxide induces heme oxygenase-1 via activation of protein kinase R-like endoplasmic reticulum kinase and inhibits endothelial cell apoptosis triggered by endoplasmic reticulum stress. Circ Res 2007; 101:919-927
103. Dekker D, Dorresteijn MJ, Pijnenburg M, Heemskerk S, Rasing-Hoogveld A, Burger DM, et al. The bilirubin-increasing drug atazanavir improves endothelial function in patients with type 2 diabetes mellitus. Arterioscler Thromb Vasc Biol 2011; 31:458-463
104. Calo LA, Maso LD, Caielli P, Pagnin E, Fusaro M, Davis PA, et al. Effect of olmesartan on oxidative stress in hypertensive patients. Mechanistic support to clinical trials derived evidence. Blood Press 2011; 20:376-382.