Arginase-endothelial nitric oxide synthase imbalance contributes to endothelial dysfunction during chronic intermittent hypoxia

Journal of Hypertension

Volumn 33, Issue 3, 2015, Pages 515-524

  Krause, Bernardo J ^a,b   Del Rio, Rodrigo ^a,c   Moya, Esteban A ^a   Marquez Gutierrez, Monica ^a   Casanello, Paola ^a,b   Iturriaga, Rodrigo ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b School of Medicine   (Chile)

^c UNIVERSIDAD AUTÓNOMA DE CHILE   (Chile)

Author keywords

arginase; chronic intermittent hypoxia; endothelial dysfunction; nitric oxide; vascular reactivity

Indexed keywords

ACETYLCHOLINE; ARGINASE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENZYME INHIBITOR; GUANYLATE CYCLASE INHIBITOR; N(G) NITROARGININE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; OXYGEN; POTASSIUM CHLORIDE; ARGINASE; ARGINASE I, HUMAN; NITRIC OXIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY ENDOTHELIUM; ARTICLE; BLOOD PRESSURE; BLOOD VESSEL TONE; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME INHIBITION; EXTERNAL CAROTID ARTERY; HYPERTENSION; IMMUNOHISTOCHEMISTRY; INTERNAL CAROTID ARTERY; ISOLATION PROCEDURE; MALE; MORPHOLOGY; MYOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSITIVITY ANALYSIS; VASODILATATION; WESTERN BLOTTING; ANIMAL; ANOXIA; ARTERY; DRUG EFFECTS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULAR ENDOTHELIUM;

ACETYLCHOLINE; ANIMALS; ANOXIA; ARGINASE; ARTERIES; ENDOTHELIUM, VASCULAR; MALE; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; NITROPRUSSIDE; RATS; RATS, SPRAGUE-DAWLEY; VASODILATION;

EID: 84922343707     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0000000000000453     Document Type: Article

References (45)

1. Somers VK, White DP, Amin R, Abraham WT, Costa F, Culebras A, et al. Sleep apnea and cardiovascular disease: an American Heart Association/American College of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing. J Am Coll Cardiol 2008; 52:686-717
2. McNicholas WT, Bonsigore MR. Sleep apnoea as an independent risk factor for cardiovascular disease: current evidence, basic mechanisms and research priorities. Eur Respir J 2007; 29:156-178
3. Gozal D, Kheirandish-Gozal L. Cardiovascular morbidity in obstructive sleep apnea: oxidative stress, inflammation, and much more. Am J Respir Crit Care Med 2008; 177:369-375
4. Kohler M, Stradling JR. Mechanisms of vascular damage in obstructive sleep apnea. Nat Rev Cardiol 2010; 7:677-685
5. Iturriaga R, Moya EA, Del Rio R. Carotid body potentiation induced by intermittent hypoxia: implications for cardiorespiratory changes induced by sleep apnoea. Clin Exp Pharmacol Physiol 2009; 36:1197-1204
6. Bradley TD, Floras JS. Obstructive sleep apnoea and its cardiovascular consequences. Lancet 2009; 373:82-93
7. Del Rio R, Moya EA, Iturriaga R. Carotid body and cardiorespiratory alterations in intermittent hypoxia: the oxidative link. Eur Respir J 2010; 36:143-150
8. Marcus NJ, Li YL, Bird F, Schultz HD, Morgan BJ. Chronic intermittent hypoxia augments chemoreflex control of sympathetic activity: role of the angiotensin II type 1 receptor. Respir Physiol Neurobiol 2010; 171:36-45
9. Dumitrascu R, Heitmann J, Seeger W, Weissmann N, Schulz R. Obstructive sleep apnea, oxidative stress and cardiovascular disease: lessons from animal studies. Oxid Med Cell Longev 2013; 2013:234631
10. Monneret D, Tamisier R, Ducros V, Garrel C, Levy P, Baguet JP, et al. The impact of obstructive sleep apnea on homocysteine and carotid remodeling in metabolic syndrome. Respir Physiol Neurobiol 2012; 180:298-304
11. Drager LF, Bortolotto LA, Krieger EM, Lorenzi-Filho G. Additive effects of obstructive sleep apnea and hypertension on early markers of carotid atherosclerosis. Hypertension 2009; 53:64-69
12. Ip MS, Tse HF, Lam B, Tsang KW, Lam WK. Endothelial function in obstructive sleep apnea and response to treatment. Am J Respir Crit Care Med 2004; 169:348-353
13. Delaey C, Boussery K, Van De Voorde J. Contractility studies on isolated bovine choroidal small arteries: determination of the active and passive wall tension-internal circumference relation. Exp Eye Res 2002; 75:243-248
14. Falloon BJ, Bund SJ, Tulip JR, Heagerty AM. In vitro perfusion studies of resistance artery function in genetic hypertension. Hypertension 1993; 22:486-495
15. Wang D, Iversen J, Strandgaard S. Contractility and endotheliumdependent relaxation of resistance vessels in polycystic kidney disease rats. J Vasc Res 1999; 36:502-509
16. Del Rio R, Moya EA, Iturriaga R. Differential expression of pro-inflammatory cytokines, endothelin-1 and nitric oxide synthases in the rat carotid body exposed to intermittent hypoxia. Brain Res 2011; 1395:74-85
17. Herrera EA, Pulgar VM, Riquelme RA, Sanhueza EM, Reyes RV, Ebensperger G, et al. High-altitude chronic hypoxia during gestation and after birth modifies cardiovascular responses in newborn sheep. Am J Physiol Regul Integr Comp Physiol 2007; 292:R2234-R2240
18. Julien C, Bayat S, Levy P. Vascular reactivity to norepinephrine and acetylcholine after chronic intermittent hypoxia in mice. Respir Physiol Neurobiol 2003; 139:21-32
19. Lefebvre B, Godin-Ribuot D, Joyeux-Faure M, Caron F, Bessard G, Levy P, et al. Functional assessment of vascular reactivity after chronic intermittent hypoxia in the rat. Respir Physiol Neurobiol 2006; 150:278-286
20. Dopp JM, Philippi NR, Marcus NJ, Olson EB, Bird CE, Moran JJ, et al. Xanthine oxidase inhibition attenuates endothelial dysfunction caused by chronic intermittent hypoxia in rats. Respiration 2011; 82:458-467
21. Marcus NJ, Philippi NR, Bird CE, Li YL, Schultz HD, Morgan BJ. Effect of AT1 receptor blockade on intermittent hypoxia-induced endothelial dysfunction. Respir Physiol Neurobiol 2012; 183:67-74
22. Montanez R, Rodriguez-Caso C, Sanchez-Jimenez F, Medina MA. In silico analysis of arginine catabolism as a source of nitric oxide or polyamines in endothelial cells. Amino Acids 2008; 34:223-229
23. Santhanam L, Christianson DW, Nyhan D, Berkowitz DE. Arginase and vascular aging. J Appl Physiol 2008; 105:1632-1642
24. Del Rio R, Moya EA, Parga MJ, Madrid C, Iturriaga R. Carotid body inflammation and cardiorespiratory alterations in intermittent hypoxia. Eur Respir J 2012; 39:1492-1500
25. Krause BJ, Carrasco-Wong I, Caniuguir A, Carvajal J, Farias M, Casanello P. Endothelial eNOS/arginase imbalance contributes to vascular dysfunction in IUGR umbilical and placental vessels. Placenta 2013; 34:20-28
26. Krause BJ, Prieto CP, Munoz-Urrutia E, San Martin S, Sobrevia L, Casanello P. Role of arginase-2 and eNOS in the differential vascular reactivity and hypoxia-induced endothelial response in umbilical arteries and veins. Placenta 2012; 33:360-366
27. Dunn WR, Gardiner SM. Structural and functional properties of isolated, pressurized, mesenteric resistance arteries from a vasopressindeficient rat model of genetic hypertension. Hypertension 1995; 26:390-396
28. Laurant P, Hayoz D, Brunner HR, Berthelot A. Effect of magnesium deficiency on blood pressure and mechanical properties of rat carotid artery. Hypertension 1999; 33:1105-1110
29. Casanello P, Krause B, Torres E, Gallardo V, Gonzalez M, Prieto C, 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; 30:625-633
30. Saletu M, Sauter C, Lalouschek W, Saletu B, Kapfhammer G, Benesch T, et al. Is excessive daytime sleepiness a predictor of carotid atherosclerosis in sleep apnea? Atherosclerosis 2008; 196:810-816
31. Mulvany MJ, Halpern W. Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 1977; 41:19-26
32. Mulvany MJ, Hansen OK, Aalkjaer C. Direct evidence that the greater contractility of resistance vessels in spontaneously hypertensive rats is associated with a narrowed lumen, a thickened media, and an increased number of smooth muscle cell layers. Circ Res 1978; 43:854-864
33. Phillips SA, Olson EB, Morgan BJ, Lombard JH. Chronic intermittent hypoxia impairs endothelium-dependent dilation in rat cerebral and skeletal muscle resistance arteries. Am J Physiol Heart Circ Physiol 2004; 286:H388-H393
34. Ryoo S, Gupta G, Benjo A, Lim HK, Camara A, Sikka G, et al. Endothelial arginase II: a novel target for the treatment of atherosclerosis. Circ Res 2008; 102:923-932
35. Demougeot C, Prigent-Tessier A, Marie C, Berthelot A. Arginase inhibition reduces endothelial dysfunction and blood pressure rising in spontaneously hypertensive rats. J Hypertens 2005; 23:971-978
36. Morris SM Jr. Recent advances in arginine metabolism: roles and regulation of the arginases. Br J Pharmacol 2009; 157:922-930
37. Ignarro LJ, Buga GM, Wei LH, Bauer PM, Wu G, del Soldato P. Role of the arginine-nitric oxide pathway in the regulation of vascular smooth muscle cell proliferation. Proc Natl Acad Sci USA 2001; 98:4202-4208
38. Wei LH, Wu G, Morris SM Jr, Ignarro LJ. Elevated arginase I expression in rat aortic smooth muscle cells increases cell proliferation. Proc Natl Acad Sci USA 2001; 98:9260-9264
39. Peyton KJ, Ensenat D, Azam MA, Keswani AN, Kannan S, Liu XM, et al. Arginase promotes neointima formation in rat injured carotid arteries. Arterioscler Thromb Vasc Biol 2009; 29:488-494
40. Gao X, Xu X, Belmadani S, Park Y, Tang Z, Feldman AM, et al. TNFalpha contributes to endothelial dysfunction by upregulating arginase in ischemia/reperfusion injury. Arterioscler Thromb Vasc Biol 2007; 27:1269-1275
41. Thacher TN, Gambillara V, Riche F, Silacci P, Stergiopulos N, da Silva RF. Regulation of arginase pathway in response to wall shear stress. Atherosclerosis 2010; 210:63-70
42. Chen B, Calvert AE, Cui H, Nelin LD. Hypoxia promotes human pulmonary artery smooth muscle cell proliferation through induction of arginase. Am J Physiol Lung Cell Mol Physiol 2009; 297:L1151-L1159
43. Krotova K, Patel JM, Block ER, Zharikov S. Hypoxic upregulation of arginase II in human lung endothelial cells. Am J Physiol Cell Physiol 2010; 299:C1541-C1548
44. Prieto CP, Krause BJ, Quezada C, San Martin R, Sobrevia L, Casanello P. Hypoxia-reduced nitric oxide synthase activity is partially explained by higher arginase-2 activity and cellular redistribution in human umbilical vein endothelium. Placenta 2011; 32:932-940
45. Demougeot C, Prigent-Tessier A, Bagnost T, Andre C, Guillaume Y, Bouhaddi M, et al. Time course of vascular arginase expression and activity in spontaneously hypertensive rats. Life Sci 2007; 80:1128-1134