Endothelial arginase II and atherosclerosis

Korean Journal of Anesthesiology

Volumn 61, Issue 1, 2011, Pages 3-11

  Ryoo, Sungwoo ^a   Berkowitz, Dan E ^b   Lim, Hyun Kyo ^c  

^a Kangwon National University   (South Korea)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c Yonsei University Wonju College of Medicine   (South Korea)

Author keywords

Arginase; Atherosclerosis; Endothelial dysfunction; Endothelial nitric oxide synthase; Vascular smooth muscle cell

Indexed keywords

ARGINASE; ARGINASE 2; ARGININE; CELL ADHESION MOLECULE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDIZED LOW DENSITY LIPOPROTEIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTERIAL STIFFNESS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BIOSYNTHESIS; BLOOD VESSEL COMPLIANCE; CELL PROLIFERATION; COLLAGEN SYNTHESIS; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME SUBSTRATE; HUMAN; NONHUMAN; PROTEIN EXPRESSION; REVIEW; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

EID: 80051813635     PISSN: 20056419     EISSN: 20057563     Source Type: Journal    
DOI: 10.4097/kjae.2011.61.1.3     Document Type: Review

References (95)

1. Beller GA. Coronary heart disease in the first 30 years of the 21st century: challenges and opportunities: The 33rd Annual James B. Herrick Lecture of the Council on Clinical Cardiology of the American Heart Association. Circulation 2001; 103: 2428-35.
2. Foot DK, Lewis RP, Pearson TA, Beller GA. Demographics and cardiology, 1950-2050. J Am Coll Cardiol 2000; 35(5 Suppl B): B66-80.
3. Heart Disease and stroke statistics-2004. Paper presented at American Heart Association. Dallas, Texas. 2003
4. Bonow RO, Smaha LA, Smith SC Jr, Mensah GA, Lenfant C. World Heart Day 2002: the international burden of cardiovascular disease: responding to the emerging global epidemic. Circulation 2002; 106: 1602-5.
5. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999; 340: 115-26.
6. Khan BV, Parthasarathy SS, Alexander RW, Medford RM. Modified low density lipoprotein and its constituents augment cytokineactivated vascular cell adhesion molecule-1 gene expression in human vascular endothelial cells. J Clin Invest 1995; 95: 1262-70.
7. Dimmeler S, Haendeler J, Galle J, Zeiher AM. Oxidized lowdensity lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases. A mechanistic clue to the 'response to injury' hypothesis. Circulation 1997; 95: 1760-3.
8. Galle J, Bengen J, Schollmeyer P, Wanner C. Impairment of endothelium-dependent dilation in rabbit renal arteries by oxidized lipoprotein(a). Role of oxygen-derived radicals. Circulation 1995; 92: 1582-9.
9. Kugiyama K, Kerns SA, Morrisett JD, Roberts R, Henry PD. Impairment of endothelium-dependent arterial relaxation by lysolecithin in modified low-density lipoproteins. Nature 1990; 344: 160-2.
10. Sawamura T, Kume N, Aoyama T, Moriwaki H, Hoshikawa H, Aiba Y, et al. An endothelial receptor for oxidized low-density lipoprotein. Nature 1997;6; 386: 73-7.
11. Mehta JL, Chen J, Yu F, Li DY. Aspirin inhibits ox-LDL-mediated LOX-1 expression and metalloproteinase-1 in human coronary endothelial cells. Cardiovasc Res 2004; 64: 243-9.
12. Li D, Singh RM, Liu L, Chen H, Singh BM, Kazzaz N, et al. Oxidized- LDL through LOX-1 increases the expression of angiotensin converting enzyme in human coronary artery endothelial cells. Cardiovasc Res 2003; 57: 238-43.
13. Ohgushi M, Kugiyama K, Fukunaga K, Murohara T, Sugiyama S, Miyamoto E, et al. Protein kinase C inhibitors prevent impairment of endothelium-dependent relaxation by oxidatively modified LDL. Arterioscler Thromb 1993; 13: 1525-32.
14. Sugiyama S, Kugiyama K, Ohgushi M, Fujimoto K, Yasue H. Lysophosphatidylcholine in oxidized low-density lipoprotein increases endothelial susceptibility to polymorphonuclear leukocyteinduced endothelial dysfunction in porcine coronary arteries. Role of protein kinase C. Circ Res 1994; 74: 565-75.
15. Nihei S, Yamashita K, Tasaki H, Ozumi K, Nakashima Y. Oxidized low-density lipoprotein-induced apoptosis is attenuated by insulinactivated phosphatidylinositol 3-kinase/Akt through p38 mitogenactivated protein kinase. Clin Exp Pharmacol Physiol 2005; 32: 224-9.
16. Everson WV, Smart EJ. Influence of caveolin, cholesterol, and lipoproteins on nitric oxide synthase: implications for vascular disease. Trends Cardiovasc Med 2001; 11: 246-50.
17. Fleming I, Mohamed A, Galle J, Turchanowa L, Brandes RP, Fisslthaler B, et al. Oxidized low-density lipoprotein increases superoxide production by endothelial nitric oxide synthase by inhibiting PKCalpha. Cardiovasc Res 2005; 65: 897-906.
18. Girerd XJ, Hirsch AT, Cooke JP, Dzau VJ, Creager MA. L-arginine augments endothelium-dependent vasodilation in cholesterol-fed rabbits. Circ Res 1990; 67: 1301-8.
19. Drexler H, Zeiher AM, Meinzer K, Just H. Correction of endothelial dysfunction in coronary microcirculation of hypercholesterolaemic patients by L-arginine. Lancet 1991; 338: 1546-50.
20. Böger RH, Bode-Böger SM, Brandes RP, Phivthong-ngam L, Böhme M, Nafe R, et al. Dietary L-arginine reduces the progression of atherosclerosis in cholesterol-fed rabbits: comparison with lovastatin. Circulation 1997; 96: 1282-90.
21. Brandes RP, Brandes S, Boger RH, Bode-Boger SM, Mugge A. L-arginine supplementation in hypercholesterolemic rabbits normalizes leukocyte adhesion to non-endothelial matrix. Life Sci 2000; 66: 1519-24.
22. Böger RH, Sydow K, Borlak J, Thum T, Lenzen H, Schubert B, et al. LDL cholesterol upregulates synthesis of asymmetrical dimethylarginine in human endothelial cells: involvement of S-adenosylmethionine- dependent methyltransferases. Circ Res 2000; 87: 99-105.
23. Ito A, Tsao PS, Adimoolam S, Kimoto M, Ogawa T, Cooke JP. Novel mechanism for endothelial dysfunction: dysregulation of dimethylarginine dimethylaminohydrolase. Circulation 1999; 99: 3092-5.
24. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Aktdependent phosphorylation. Nature 1999; 399: 601-5.
25. Fisslthaler B, Dimmeler S, Hermann C, Busse R, Fleming I. Phosphorylation and activation of the endothelial nitric oxide synthase by fluid shear stress. Acta Physiol Scand 2000; 168: 81-8.
26. Vanhoutte PM. Endothelial dysfunction in hypertension. J Hypertens Suppl 1996; 14: S83-93.
27. De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol 2000; 130: 963-74.
28. Vanhoutte PM. Endothelial dysfunction and atherosclerosis. Eur Heart J 1997; 18(Suppl E): E19-29.
29. Vanhoutte PM. Endothelium-dependent responses in congestive heart failure. J Mol Cell Cardiol 1996; 28: 2233-40.
30. Andrawis N, Jones DS, Abernethy DR. Aging is associated with endothelial dysfunction in the human forearm vasculature. J Am Geriatr Soc 2000; 48: 193-8.
31. Haraguchi Y, Takiguchi M, Amaya Y, Kawamoto S, Matsuda I, Mori M. Molecular cloning and nucleotide sequence of cDNA for human liver arginase. Proc Natl Acad Sci U S A 1987; 84: 412-5.
32. Morris SM Jr, Bhamidipati D, Kepka-Lenhart D. Human type II arginase: sequence analysis and tissue-specific expression. Gene 1997; 193: 157-61.
33. Chang CI, Liao JC, Kuo L. Arginase modulates nitric oxide production in activated macrophages. Am J Physiol 1998; 274: H342-8.
34. Koga T, Koshiyama Y, Gotoh T, Yonemura N, Hirata A, Tanihara H, et al. Coinduction of nitric oxide synthase and arginine metabolic enzymes in endotoxin-induced uveitis rats. Exp Eye Res 2002; 75: 659-67.
35. Louis CA, Reichner JS, Henry WL Jr, Mastrofrancesco B, Gotoh T, Mori M, et al. Distinct arginase isoforms expressed in primary and transformed macrophages: regulation by oxygen tension. Am J Physiol 1998; 274: R775-82.
36. Que LG, George SE, Gotoh T, Mori M, Huang YC. Effects of arginase isoforms on NO Production by nNOS. Nitric Oxide 2002; 6: 1-8.
37. Sonoki T, Nagasaki A, Gotoh T, Takiguchi M, Takeya M, Matsuzaki H, et al. Coinduction of nitric-oxide synthase and arginase I in cultured rat peritoneal macrophages and rat tissues in vivo by lipopolysaccharide. J Biol Chem 1997; 272: 3689-93.
38. Modolell M, Corraliza IM, Link F, Soler G, Eichmann K. Reciprocal regulation of the nitric oxide synthase/arginase balance in mouse bone marrow-derived macrophages by TH1 and TH2 cytokines. Eur J Immunol 1995; 25: 1101-4.
39. Morris SM Jr, Kepka-Lenhart D, Chen LC. Differential regulation of arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol 1998; 275: E740-7.
40. 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 U S A 2001; 98: 4202-8.
41. Li H, Meininger CJ, Hawker JR Jr, Haynes TE, Kepka-Lenhart D, Mistry SK, et al. Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab 2001; 280: E75-82.
42. Levillain O, Balvay S, Peyrol S. Mitochondrial expression of arginase II in male and female rat inner medullary collecting ducts. J Histochem Cytochem 2005; 53: 533-41.
43. Lim HK, Lim HK, Ryoo S, Benjo A, Shuleri K, Miriel V, Baraban E, et al. Mitochondrial arginase II constrains endothelial NOS-3 activity. Am J Physiol Heart Circ Physiol 2007; 293: H3317-24.
44. Berkowitz DE, White R, Li D, Minhas KM, Cernetich A, Kim S, et al. Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels. Circulation 2003; 108: 2000-6.
45. White AR, Ryoo S, Li D, Champion HC, Steppan J, Wang D, et al. Knockdown of arginase I restores NO signaling in the vasculature of old rats. Hypertension 2006; 47: 245-51.
46. Hein TW, Zhang C, Wang W, Chang CI, Thengchaisri N, Kuo L. Ischemia-reperfusion selectively impairs nitric oxide-mediated dilation in coronary arterioles: counteracting role of arginase. FASEB J 2003; 17: 2328-30.
47. Zhang C, Hein TW, Wang W, Miller MW, Fossum TW, McDonald MM, et al. Upregulation of vascular arginase in hypertension decreases nitric oxide-mediated dilation of coronary arterioles. Hypertension 2004; 44: 935-43.
48. Johnson FK, Johnson RA, Peyton KJ, Durante W. Arginase inhibition restores arteriolar endothelial function in Dahl rats with saltinduced hypertension. Am J Physiol Regul Integr Comp Physiol 2005; 288: R1057-62.
49. Bivalacqua TJ, Hellstrom WJ, Kadowitz PJ, Champion HC. Increased expression of arginase II in human diabetic corpus cavernosum: in diabetic-associated erectile dysfunction. Biochem Biophys Res Commun 2001; 283: 923-7.
50. Ryoo S, Lemmon CA, Soucy KG, Gupta G, White AR, Nyhan D, et al. Oxidized low-density lipoprotein-dependent endothelial arginase II activation contributes to impaired nitric oxide signaling. Circ Res 2006; 99: 951-60.
51. Ming XF, Barandier C, Viswambharan H, Kwak BR, Mach F, Mazzolai L, et al. Thrombin stimulates human endothelial arginase enzymatic activity via RhoA/ROCK pathway: implications for atherosclerotic endothelial dysfunction. Circulation 2004; 110: 3708-14.
52. Nelin LD, Wang X, Zhao Q, Chicoine LG, Young TL, Hatch DM, et al. MKP-1 switches arginine metabolism from nitric oxide synthase to arginase following endotoxin challenge. Am J Physiol Cell Physiol 2007; 293: C632-40.
53. 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: 971-8.
54. Hsu LL, Champion HC, Campbell-Lee SA, Bivalacqua TJ, Manci EA, Diwan BA, et al. Hemolysis in sickle cell mice causes pulmonary hypertension due to global impairment in nitric oxide bioavailability. Blood 2007; 109: 3088-98.
55. JY. Nitric oxide and pulmonary hypertension. Korean J Anesthesiol 2010; 58: 4-14.
56. Hayashi T, Esaki T, Sumi D, Mukherjee T, Iguchi A, Chaudhuri G. Modulating role of estradiol on arginase II expression in hyperlipidemic rabbits as an atheroprotective mechanism. Proc Natl Acad Sci U S A 2006; 103: 10485-90.
57. Steppan J, Ryoo S, Schuleri KH, Gregg C, Hasan RK, White AR, et al. Arginase modulates myocardial contractility by a nitric oxide synthase 1-dependent mechanism. Proc Natl Acad Sci U S A 2006; 103: 4759-64.
58. Nawrath H, Wegener JW, Rupp J, Habermeier A, Closs EI. Voltagedependence of L-arginine transport by hCAT-2A and hCAT-2B expressed in oocytes from Xenopus laevis. Am J Physiol Cell Physiol 2000; 279: C1336-44.
59. Rotmann A, Closs EI, Liewald JF, Nawrath H. Intracellular accumulation of L-Arg, kinetics of transport, and potassium leak conductance in oocytes from Xenopus laevis expressing hCAT-1, hCAT-2A, and hCAT-2B. Biochim Biophys Acta 2004; 1660: 138-43.
60. Eisenthal R, Danson MJ, Hough DW. Catalytic efficiency and kcat/ KM: a useful comparator? Trends Biotechnol 2007; 25: 247-9.
61. Topal G, Brunet A, Walch L, Boucher JL, David-Dufilho M. Mitochondrial arginase II modulates nitric oxide synthesis through nonfreely exchangeable L-arginine pools in human endothelial cells. J Pharmacol Exp Ther 2006; 318: 1368-74.
62. Solomonson LP, Flam BR, Pendleton LC, Goodwin BL, Eichler DC. The caveolar nitric oxide synthase/arginine regeneration system for NO production in endothelial cells. J Exp Biol 2003; 206: 2083-7.
63. 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: 923-32.
64. Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD, Davidson BL. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res 1998; 82: 1298-305.
65. Suzuki H, Swei A, Zweifach BW, Schmid-Schönbein GW. In vivo evidence for microvascular oxidative stress in spontaneously hypertensive rats. Hydroethidine microfluorography. Hypertension 1995; 25: 1083-9.
66. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000; 86: 494-501.
67. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 1994; 74: 1141-8.
68. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res 2002; 91: 406-13.
69. Görlach A, Brandes RP, Nguyen K, Amidi M, Dehghani F, Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res 2000; 87: 26-32.
70. Butler R, Morris AD, Belch JJ, Hill A, Struthers AD. Allopurinol normalizes endothelial dysfunction in type 2 diabetics with mild hypertension. Hypertension 2000; 35: 746-51.
71. Harrison DG. Cellular and molecular mechanisms of endothelial cell dysfunction. J Clin Invest 1997; 100: 2153-7.
72. Cooke JP. Is atherosclerosis an arginine deficiency disease? J Investig Med 1998; 46: 377-80.
73. Abu-Soud HM, Feldman PL, Clark P, Stuehr DJ. Electron transfer in the nitric-oxide synthases. Characterization of L-arginine analogs that block heme iron reduction. J Biol Chem 1994; 269: 32318-26.
74. Asmar R, Rudnichi A, Blacher J, London GM, Safar ME. Pulse pressure and aortic pulse wave are markers of cardiovascular risk in hypertensive populations. Am J Hypertens 2001; 14: 91-7.
75. Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, et al. The Seventh report of the joint national committee on prevention, detection, evaluation, and treatment of high blood pressure: the JNC 7 report. JAMA 2003; 289: 2560-72.
76. Collins AJ, Li S, Gilbertson DT, Liu J, Chen SC, Herzog CA. Chronic kidney disease and cardiovascular disease in the Medicare population. Kidney Int Suppl 2003; 87: S24-31.
77. Dart AM, Kingwell BA. Pulse pressure--a review of mechanisms and clinical relevance. J Am Coll Cardiol 2001; 37: 975-84.
78. Miura K, Dyer AR, Greenland P, Daviglus ML, Hill M, Liu K, et al. Pulse pressure compared with other blood pressure indexes in the prediction of 25-year cardiovascular and all-cause mortality rates: The Chicago Heart Association Detection Project in Industry Study. Hypertension 2001; 38: 232-7.
79. Blacher J, Guerin AP, Pannier B, Marchais SJ, Safar ME, London GM. Impact of aortic stiffness on survival in end-stage renal disease. Circulation 1999; 99: 2434-9.
80. Chae CU, Pfeffer MA, Glynn RJ, Mitchell GF, Taylor JO, Hennekens CH. Increased pulse pressure and risk of heart failure in the elderly. JAMA 1999; 281: 634-9.
81. Fukuhara M, Matsumura K, Ansai T, Takata Y, Sonoki K, Akifusa S, et al. Prediction of cognitive function by arterial stiffness in the very elderly. Circ J 2006; 70: 756-61.
82. Kostis JB, Lawrence-Nelson J, Ranjan R, Wilson AC, Kostis WJ, Lacy CR. Association of increased pulse pressure with the development of heart failure in SHEP. Systolic Hypertension in the Elderly (SHEP) Cooperative Research Group. Am J Hypertens 2001; 14: 798-803.
83. Safar ME, Blacher J, Mourad JJ, London GM. Stiffness of carotid artery wall material and blood pressure in humans: application to antihypertensive therapy and stroke prevention. Stroke 2000; 31: 782-90.
84. Najjar SS, Scuteri A, Lakatta EG. Arterial aging: is it an immutable cardiovascular risk factor? Hypertension 2005; 46: 454-62.
85. Ferrier KE, Muhlmann MH, Baguet JP, Cameron JD, Jennings GL, Dart AM, et al. Intensive cholesterol reduction lowers blood pressure and large artery stiffness in isolated systolic hypertension. J Am Coll Cardiol 2002; 39: 1020-5.
86. Toikka JO, Niemi P, Ahotupa M, Niinikoski H, Viikari JS, Ronnemaa T, et al. Large-artery elastic properties in young men: relationships to serum lipoproteins and oxidized low-density lipoproteins. Arterioscler Thromb Vasc Biol 1999; 19: 436-41.
87. Wang YX, Halks-Miller M, Vergona R, Sullivan ME, Fitch R, Mallari C, et al. Increased aortic stiffness assessed by pulse wave velocity in apolipoprotein E-deficient mice. Am J Physiol Heart Circ Physiol 2000; 278: H428-34.
88. Chowienczyk PJ, Watts GF, Cockcroft JR, Ritter JM. Impaired endothelium- dependent vasodilation of forearm resistance vessels in hypercholesterolaemia. Lancet 1992; 340: 1430-2.
89. Sudhir K, Mullen WL, Hausmann D, Fitzgerald PJ, Chou TM, Yock PG, et al. Contribution of endothelium-derived nitric oxide to coronary arterial distensibility: an in vivo two-dimensional intravascular ultrasound study. Am Heart J 1995; 129: 726-32.
90. Fitch RM, Vergona R, Sullivan ME, Wang YX. Nitric oxide synthase inhibition increases aortic stiffness measured by pulse wave velocity in rats. Cardiovasc Res 2001; 51: 351-8.
91. Peng X, Haldar S, Deshpande S, Irani K, Kass DA. Wall stiffness suppresses Akt/eNOS and cytoprotection in pulse-perfused endothelium. Hypertension 2003; 41: 378-81.
92. Poli A, Tremoli E, Colombo A, Sirtori M, Pignoli P, Paoletti R. Ultrasonographic measurement of the common carotid artery wall thickness in hypercholesterolemic patients. A new model for the quantitation and follow-up of preclinical atherosclerosis in livinghuman subjects. Atherosclerosis 1988; 70: 253-61.
93. O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med 1999; 340: 14-22.
94. Allan PL, Mowbray PI, Lee AJ, Fowkes FG. Relationship between carotid intima-media thickness and symptomatic and asymptomatic peripheral arterial disease. The Edinburgh Artery Study. Stroke 1997; 28: 348-53.
95. Blankenhorn DH, Selzer RH, Crawford DW, Barth JD, Liu CR, Liu CH, et al. Beneficial effects of colestipol-niacin therapy on the common carotid artery. Two- and four-year reduction of intimamedia thickness measured by ultrasound. Circulation 1993; 88: 20-8.