Selective up-regulation of arginase-1 in coronary arteries of diabetic patients

Frontiers in Immunology

Volumn 4, Issue SEP, 2013, Pages

  Bagi, Zsolt ^a   Feher, Attila ^a   Dou, Huijuan ^a   Broskova, Zuzana ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Arginase; Coronary artery; Diabetes mellitus; Endothelium; Nitric oxide

Indexed keywords

ARGINASE 1; ARGININE; CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE;

ARTERY BLOOD FLOW; BIOAVAILABILITY; CORONARY ARTERY DISEASE; DIABETIC PATIENT; ENDOTHELIAL DYSFUNCTION; HUMAN; MORTALITY; OXIDATIVE STRESS; PREVALENCE; PROTEIN EXPRESSION; REVIEW; UPREGULATION;

EID: 84885982946     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00293     Document Type: Review

References (60)

1. Nitenberg A, Valensi P, Sachs R, Dali M, Aptecar E, Attali JR. Impairment of coronary vascular reserve and ACh-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes (1993) 42:1017-25. doi: 10.2337/diabetes.42.7.1017.
2. Nemes A, Forster T, Lengyel C, Csanady M. Reduced aortic distensibility and coronary flow velocity reserve in diabetes mellitus patients with a negative coronary angiogram. Can J Cardiol (2007) 23:445-50. doi:10.1016/S0828-282X(07)70782-1.
3. Cortigiani L, Rigo F, Gherardi S, Sicari R, Galderisi M, Bovenzi F, et al. Additional prognostic value of coronary flow reserve in diabetic and nondiabetic patients with negative dipyridamole stress echocardiography by wall motion criteria. J Am Coll Cardiol (2007) 50:1354-61. doi:10.1016/j.jacc.2007.06.027.
4. Enderle MD, Benda N, Schmuelling RM, Haering HU, Pfohl M. Preserved endothelial function in IDDM patients, but not in NIDDM patients, compared with healthy subjects. Diabetes Care (1998) 21:271-7. doi:10.2337/diacare.21.2.271.
5. Ting HH, Timimi FK, Boles KS, Creager SJ, Ganz P, Creager MA. Vitamin C improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. J Clin Invest (1996) 97:22-8. doi:10.1172/JCI118394.
6. Nitenberg A, Paycha F, Ledoux S, Sachs R, Attali JR, Valensi P. Coronary artery responses to physiological stimuli are improved by deferoxamine but not by L-arginine in non-insulin-dependent diabetic patients with angiographically normal coronary arteries and no other risk factors. Circulation (1998) 97:736-43. doi:10.1161/01.CIR.97.8.736.
7. Kaneda H, Taguchi J, Kuwada Y, Hangaishi M, Aizawa T, Yamakado M, et al. Coronary artery spasm and the polymorphisms of the endothelial nitric oxide synthase gene. Circ J (2006) 70:409-13. doi:10.1253/circj.70.409.
8. Miller FJ Jr, Dellsperger KC, Gutterman DD. Pharmacologic activation of the human coronary microcirculation in vitro: endothelium-dependent dilation and differential responses to acetylcholine. Cardiovasc Res (1998) 38:744-50. doi:10.1016/S0008-6363(98)00035-2.
9. De Vriese AS, Verbeuren TJ, Van De Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol (2000) 130:963-74. doi:10.1038/sj.bjp.0703393.
10. Beleznai T, Feher A, Spielvogel D, Lansman SL, Bagi Z. Arginase 1 contributes to diminished coronary arteriolar dilation in patients with diabetes. Am J Physiol Heart Circ Physiol (2011) 300:H777-83. doi:10.1152/ajpheart.00831.2010.
11. Frisbee JC, Stepp DW. Impaired NO-dependent dilation of skeletal muscle arterioles in hypertensive diabetic obese Zucker rats. Am J Physiol Heart Circ Physiol (2001) 281:H1304-11.
12. Naderali EK, Pickavance LC, Wilding JP, Williams G. Diet-induced endothelial dysfunction in the rat is independent of the degree of increase in total body weight. Clin Sci (Lond) (2001) 100:635-41. doi:10.1042/CS20000279.
13. Erdos B, Miller AW, Busija DW. Impaired endothelium-mediated relaxation in isolated cerebral arteries from insulin-resistant rats. Am J Physiol Heart Circ Physiol (2002) 282:H2060-5.
14. Katakam PV, Tulbert CD, Snipes JA, Erdos B, Miller AW, Busija DW. Impaired insulin-induced vasodilation in small coronary arteries of Zucker obese rats is mediated by reactive oxygen species. Am J Physiol Heart Circ Physiol (2005) 288:H854-60. doi:10.1152/ajpheart.00715.2004.
15. Oltman CL, Richou LL, Davidson EP, Coppey LJ, Lund DD, Yorek MA. Progression of coronary and mesenteric vascular dysfunction in Zucker obese and Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol (2006) 291:H1780-7. doi:10.1152/ajpheart.01297.2005.
16. Katakam PV, Domoki F, Lenti L, Gaspar T, Institoris A, Snipes JA, et al. Cerebrovascular responses to insulin in rats. J Cereb Blood Flow Metab (2009) 29:1955-67. doi:10.1038/jcbfm.2009.177.
17. Bagi Z, Koller A. Lack of NO-mediation of flow-dependent arteriolar dilation in diabetes is restored by sepiapterin. J Vasc Res (2003) 40:47-57. doi:10.1159/000068938.
18. Bagi Z, Koller A, Kaley G. Peroxisome proliferator-activated receptor-{gamma} activation, by reducing oxidative stress increases NO bioavailability in coronary arterioles in type 2 diabetes. Am J Physiol Heart Circ Physiol (2004) 286:H742-8. doi:10.1152/ajpheart.00718.2003.
19. Erdei N, Toth A, Pasztor ET, Papp Z, Edes I, Koller A, et al. High-fat diet-induced reduction in nitric oxide-dependent arteriolar dilation in rats: role of xanthine oxidase-derived superoxide anion. Am J Physiol Heart Circ Physiol (2006) 291:H2107-15. doi:10.1152/ajpheart.00389.2006.
20. Jebelovszki E, Kiraly C, Erdei N, Feher A, Pasztor ET, Rutkai I, et al. High-fat diet-induced obesity leads to increased NO sensitivity of rat coronary arterioles: role of soluble guanylate cyclase activation. Am J Physiol Heart Circ Physiol (2008) 294:H2558-64. doi:10.1152/ajpheart.01198.2007.
21. Oltman CL, Kane NL, Gutterman DD, Bar RS, Dellsperger KC. Mechanism of coronary vasodilation to insulin and insulin-like growth factor I is dependent on vessel size. Am J Physiol Endocrinol Metab (2000) 279:E176-81.
22. Ruderman NB, Williamson JR, Brownlee M. Glucose and diabetic vascular disease. FASEB J (1992) 6:2905-14.
23. Bohlen HG, Lash JM. Topical hyperglycemia rapidly suppresses EDRF-mediated vasodilation of normal rat arterioles. Am J Physiol (1993) 265:H219-25.
24. Bagi Z, Koller A. Lack of nitric oxide mediation of flow-dependent arteriolar dilation in type I diabetes is restored by sepiapterin. J Vasc Res (2003) 40:47-57. doi:10.1159/000068938.
25. Bagi Z, Koller A, Kaley G. Superoxide-NO interaction decreases flow-and agonist-induced dilations of coronary arterioles in Type 2 diabetes mellitus. Am J Physiol Heart Circ Physiol (2003) 285:H1404-10.
26. Bagi Z, Koller A, Kaley G. PPARgamma activation, by reducing oxidative stress, increases NO bioavailability in coronary arterioles of mice with Type 2 diabetes. Am J Physiol Heart Circ Physiol (2004) 286:H742-8. doi:10.1152/ajpheart.00718.2003.
27. Bagi Z, Toth E, Koller A, Kaley G. Microvascular dysfunction after transient high glucose is caused by superoxide-dependent reduction in the bioavailability of NO and BH(4). Am J Physiol Heart Circ Physiol (2004) 287:H626-33. doi:10.1152/ajpheart.00074.2004.
28. Erdei N, Bagi Z, Edes I, Kaley G, Koller A. H2O2 increases production of constrictor prostaglandins in smooth muscle leading to enhanced arteriolar tone in Type 2 diabetic mice. Am J Physiol Heart Circ Physiol (2007) 292:H649-56. doi:10.1152/ajpheart.00596.2006.
29. Beckman JA, Goldfine AB, Gordon MB, Creager MA. Ascorbate restores endothelium-dependent vasodilation impaired by acute hyperglycemia in humans. Circulation (2001) 103:1618-23. doi:10.1161/01.CIR.103.12.1618.
30. Marchioli R, Schweiger C, Levantesi G, Tavazzi L, Valagussa F. Antioxidant vitamins and prevention of cardiovascular disease: epidemiological and clinical trial data. Lipids (2001) 36:S5363. doi:10.1007/s11745-001-0683-y.
31. Maxwell S, Greig L. Anti-oxidants-a protective role in cardiovascular disease? Expert Opin Pharmacother (2001) 2:1737-50. doi:10.1517/14656566.2.11.1737.
32. Gazis A, White DJ, Page SR, Cockcroft JR. Effect of oral vitamin E (alpha-tocopherol) supplementation on vascular endothelial function in Type 2 diabetes mellitus. Diabet Med (1999) 16:304-11. doi:10.1046/j.1464-5491.1999.00049.x.
33. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev (2007) 87:315-424. doi:10.1152/physrev.00029.2006.
34. Xu J, Zou MH. Molecular insights and therapeutic targets for diabetic endothelial dysfunction. Circulation (2009) 120:1266-86. doi:10.1161/CIRCULATIONAHA.108.835223.
35. Szabo C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov (2007) 6:662-80. doi:10.1038/nrd2222.
36. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol (2007) 34:906-11. doi:10.1111/j.1440-1681.2007.04638.x.
37. Vasquez-Vivar J, Kalyanaraman B, Martasek P, Hogg N, Masters BS, Karoui H, et al. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors. Proc Natl Acad Sci U S A (1998) 95:9220-5. doi:10.1073/pnas.95.16.9220.
38. Thony B, Auerbach G, Blau N. Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem J (2000) 347:1-16.
39. Ihlemann N, Rask-Madsen C, Perner A, Dominguez H, Hermann T, Kober L, et al. Tetrahydrobiopterin restores endothelial dysfunction induced by an oral glucose challenge in healthy subjects. Am J Physiol Heart Circ Physiol (2003) 285:H875-82.
40. Settergren M, Bohm F, Malmstrom RE, Channon KM, Pernow J. L-arginine and tetrahydrobiopterin protects against ischemia/reperfusion-induced endothelial dysfunction in patients with type 2 diabetes mellitus and coronary artery disease. Atherosclerosis (2009) 204:73-8. doi:10.1016/j.atherosclerosis.2008.08.034.
41. Tiefenbacher CP, Bleeke T, Vahl C, Amann K, Vogt A, Kubler W. Endothelial dysfunction of coronary resistance arteries is improved by tetrahydrobiopterin in atherosclerosis. Circulation (2000) 102:2172-9. doi:10.1161/01.CIR.102.18.2172.
42. Cunnington C, Van Assche T, Shirodaria C, Kylintireas I, Lindsay AC, Lee JM, et al. Systemic and vascular oxidation limits the efficacy of oral tetrahydrobiopterin treatment in patients with coronary artery disease. Circulation (2012) 125:1356-66. doi:10.1161/CIRCULATIONAHA.111.038919.
43. 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) 278:22546-54. doi:10.1074/jbc. M302227200.
44. Chen W, Druhan LJ, Chen CA, Hemann C, Chen YR, Berka V, et al. Peroxynitrite induces destruction of the tetrahydrobiopterin and heme in endothelial nitric oxide synthase: transition from reversible to irreversible enzyme inhibition. Biochemistry (2010) 49:3129-37. doi:10.1021/bi9016632.
45. Ishii M, Shimizu S, Nagai T, Shiota K, Kiuchi Y, Yamamoto T. Stimulation of tetrahydrobiopterin synthesis induced by insulin: possible involvement of phosphatidylinositol 3-kinase. Int J Biochem Cell Biol (2001) 33:65-73.
46. Katakam PV, Snipes JA, Steed MM, Busija DW. Insulin-induced generation of reactive oxygen species and uncoupling of nitric oxide synthase underlie the cerebrovascular insulin resistance in obese rats. J Cereb Blood Flow Metab (2012) 32:792-804. doi:10.1038/jcbfm.2011.181.
47. Gornik HL, Creager MA. Arginine and endothelial and vascular health. J Nutr (2004) 134:2880S-7S; discussion 2895S.
48. Dubois-Rande JL, Zelinsky R, Roudot F, Chabrier PE, Castaigne A, Geschwind H, et al. Effects of infusion of L-arginine into the left anterior descending coronary artery on acetylcholine-induced vasoconstriction of human atheromatous coronary arteries. Am J Cardiol (1992) 70:1269-75. doi:10.1016/0002-9149(92)90760-V.
49. Lerman A, Burnett JC Jr, Higano ST, Mckinley LJ, Holmes DR Jr. Long-term L-arginine supplementation improves small-vessel coronary endothelial function in humans. Circulation (1998) 97:2123-8. doi:10.1161/01.CIR.97.21.2123.
50. Blum A, Hathaway L, Mincemoyer R, Schenke WH, Kirby M, Csako G, et al. Oral L-arginine in patients with coronary artery disease on medical management. Circulation (2000) 101:2160-4. doi:10.1161/01.CIR.101.18.2160.
51. Schulman SP, Becker LC, Kass DA, Champion HC, Terrin ML, Forman S, et al. L-arginine therapy in acute myocardial infarction: the Vascular Interaction With Age in Myocardial Infarction (VINTAGE MI) randomized clinical trial. JAMA (2006) 295:58-64. doi:10.1001/jama.295.1.58.
52. Sourij H, Meinitzer A, Pilz S, Grammer TB, Winkelmann BR, Boehm BO, et al. Arginine bioavailability ratios are associated with cardiovascular mortality in patients referred to coronary angiography. Atherosclerosis (2011) 218:220-5. doi:10.1016/j.atherosclerosis.2011.04.041.
53. Lucotti P, Setola E, Monti LD, Galluccio E, Costa S, Sandoli EP, et al. Beneficial effects of a long-term oral L-arginine treatment added to a hypocaloric diet and exercise training program in obese, insulin-resistant type 2 diabetic patients. Am J Physiol Endocrinol Metab (2006) 291:E906-12. doi:10.1152/ajpendo.00002.2006.
54. Jenkinson CP, Grody WW, Cederbaum SD. Comparative properties of arginases. Comp Biochem Physiol B Biochem Mol Biol (1996) 114:107-32. doi:10.1016/0305-0491(95)02138-8.
55. Quitter F, Figulla HR, Ferrari M, Pernow J, Jung C. Increased arginase levels in heart failure represent a therapeutic target to rescue microvascular perfusion. Clin Hemorheol Microcirc (2013) 54:75-85. doi:10.3233/CH-2012-1617.
56. Holowatz LA, Kenney WL. Up-regulation of arginase activity contributes to attenuated reflex cutaneous vasodilatation in hypertensive humans. J Physiol (2007) 581:863-72. doi:10.1113/jphysiol.2007.128959.
57. Chen X, Niroomand F, Liu Z, Zankl A, Katus HA, Jahn L, et al. Expression of nitric oxide related enzymes in coronary heart disease. Basic Res Cardiol (2006) 101:346-53. doi:10.1007/s00395-006-0592-5.
58. Shemyakin A, Kovamees O, Rafnsson A, Bohm F, Svenarud P, Settergren M, et al. Arginase inhibition improves endothelial function in patients with coronary artery disease and type 2 diabetes mellitus. Circulation (2012) 126:2943-50. doi:10.1161/CIRCULATIONAHA.112.140335.
59. Xu W, Kaneko FT, Zheng S, Comhair SA, Janocha AJ, Goggans T, et al. Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J (2004) 18:1746-8.
60. Kashyap SR, Lara A, Zhang R, Park YM, Defronzo RA. Insulin reduces plasma arginase activity in type 2 diabetic patients. Diabetes Care (2008) 31:134-9. doi:10.2337/dc07-1198.