Insights into the arginine paradox: Evidence against the importance of subcellular location of arginase and eNOS

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 5, 2013, Pages

  Elms, Shawn ^b   Chen, Feng ^a,b   Wang, Yusi ^b   Qian, Jin ^b   Askari, Bardia ^c   Yu, Yanfang ^b   Pandey, Deepesh ^b   Iddings, Jennifer ^b   Caldwell, Ruth B ^b,d   Fulton, David J R ^b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b MEDICAL COLLEGE OF GEORGIA   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Arginase; Endothelial nitric oxide synthase; L arginine; Nitric oxide; Urea

Indexed keywords

ARGINASE; ARGINASE 1; ARGINASE 2; ARGININE; CITRULLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; ORNITHINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL COMPARTMENTALIZATION; CELL LINE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; MITOCHONDRION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ARGINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; L-ARGININE; NITRIC OXIDE; UREA;

ANIMALS; AORTA; ARGINASE; ARGININE; CATTLE; CELL LINE; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CITRULLINE; COS CELLS; ENDOTHELIUM, VASCULAR; MODELS, ANIMAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; ORNITHINE;

EID: 84883412740     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00755.2012     Document Type: Article

References (75)

1. Bates TE, Loesch A, Burnstock G, Clark JB. Immunocytochemical evidence for a mitochondrially located nitric oxide synthase in brain and liver. Biochem Biophys Res Commun 213: 896-900, 1995.
2. Berkowitz DE, White R, Li D, Minhas KM, Cernetich A, Kim S, Burke S, Shoukas AA, Nyhan D, Champion HC, Hare JM. Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels. Circulation 108: 2000-2006, 2003.
3. Boucher JL, Custot J, Vadon S, Delaforge M, Lepoivre M, Tenu JP, Yapo A, Mansuy D. N omega-hydroxyl-L-Arginine, an intermediate in the L-Arginine to nitric oxide pathway, is a strong inhibitor of liver and macrophage Arginase. Biochem Biophys Res Commun 203: 1614-1621, 1994.
4. Chen PF, Wu KK. Structural elements contribute to the calcium/calmodulin dependence on enzyme activation in human endothelial nitric-oxide synthase. J Biol Chem 278: 52392-52400, 2003.
5. Chin-Dusting JP, Willems L, Kaye DM. L-Arginine transporters in cardiovascular disease: a novel therapeutic target. Pharmacol Ther 116: 428-436, 2007.
6. Church JE, Fulton D. Differences in eNOS activity because of subcellular localization are dictated by phosphorylation state rather than the local calcium environment. J Biol Chem 281: 1477-1488, 2006.
7. Closs EI, Scheld JS, Sharafi M, Forstermann U. Substrate supply for nitric-oxide synthase in macrophages and endothelial cells: role of cationic amino acid transporters. Mol Pharmacol 57: 68-74, 2000.
8. Cooke JP, Rossitch E Jr, Andon NA, Loscalzo J, Dzau VJ. Flow activates an endothelial potassium channel to release an endogenous nitrovasodilator. J Clin Invest 88: 1663-1671, 1991.
9. Daghigh F, Fukuto JM, Ash DE. Inhibition of rat liver Arginase by an intermediate in NO biosynthesis, NG-hydroxy-L-Arginine: implications for the regulation of nitric oxide biosynthesis by Arginase. Biochem Biophys Res Commun 202: 174-180, 1994.
10. De Caterina R, Libby P, Peng HB, Thannickal VJ, Rajavashisth TB, Gimbrone MA Jr, Shin WS, Liao JK. Nitric oxide decreases cytokineinduced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest 96: 60-68, 1995.
11. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol 34: 906-911, 2007.
12. Egashira K, Inou T, Hirooka Y, Kai H, Sugimachi M, Suzuki S, Kuga T, Urabe Y, Takeshita A. Effects of age on endothelium-dependent vasodilation of resistance coronary artery by acetylcholine in humans. Circulation 88: 77-81, 1993.
13. Erez A, Nagamani SC, Shchelochkov OA, Premkumar MH, Campeau PM, Chen Y, Garg HK, Li L, Mian A, Bertin TK, Black JO, Zeng H, Tang Y, Reddy AK, Summar M, O'Brien WE, Harrison DG, Mitch WE, Marini JC, Aschner JL, Bryan NS, Lee B. Requirement of Arg Ininosuccinate lyase for systemic nitric oxide production. Nat Med 17: 1619-1626, 2011.
14. Feng Y, Venema VJ, Venema RC, Tsai N, Caldwell RB. VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun 256: 192-197, 1999.
15. Flam BR, Hartmann PJ, Harrell-Booth M, Solomonson LP, Eichler DC. Caveolar localization of Arginine regeneration enzymes, Arg Ininosuccinate synthase, and lyase, with endothelial nitric oxide synthase. Nitric Oxide 5: 187-197, 2001.
16. Forstermann U, Closs EI, Pollock JS, Nakane M, Schwarz P, Gath I, Kleinert H. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 23: 1121-1131, 1994.
17. Fulton D, Babbitt R, Zoellner S, Fontana J, Acevedo L, McCabe TJ, Iwakiri Y, Sessa WC. Targeting of endothelial nitric-oxide synthase to the cytoplasmic face of the Golgi complex or plasma membrane regulates Akt-versus calcium-dependent mechanisms for nitric oxide release. J Biol Chem 279: 30349-30357, 2004.
18. Fulton D, Fontana J, Sowa G, Gratton JP, Lin M, Li KX, Michell B, Kemp BE, Rodman D, Sessa WC. Localization of endothelial nitricoxide synthase phosphorylated on serine 1179 and nitric oxide in Golgi and plasma membrane defines the existence of two pools of active enzyme. J Biol Chem 277: 4277-4284, 2002.
19. Fulton D, Gratton JP, Sessa WC. Post-translational control of endothelial nitric oxide synthase: why isn't calcium/calmodulin enough? J Pharmacol Exp Ther 299: 818-824, 2001.
20. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376, 1980.
21. Garcia-Cardena G, Oh P, Liu J, Schnitzer JE, Sessa WC. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci USA 93: 6448-6453, 1996.
22. Gotoh T, Sonoki T, Nagasaki A, Terada K, Takiguchi M, Mori M. Molecular cloning of cDNA for nonhepatic mitochondrial Arginase (Arginase II) and comparison of its induction with nitric oxide synthase in a murine macrophage-like cell line. FEBS Lett 395: 119-122, 1996.
23. Govers R, Rabelink TJ. Cellular regulation of endothelial nitric oxide synthase. Am J Physiol Renal Physiol 280: F193-F206, 2001.
24. Grasemann H, Schwiertz R, Matthiesen S, Racke K, Ratjen F. Increased Arginase activity in cystic fibrosis airways. Am J Respir Crit Care Med 172: 1523-1528, 2005.
25. Gruetter CA, Barry BK, McNamara DB, Gruetter DY, Kadowitz PJ, Ignarro L. Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide, nitroprusside and a carcinogenic nitrosoamine. J Cyclic Nucleotide Res 5: 211-224, 1979.
26. Ha YH, Milner JA, Corbin JE. Arginine requirements in immature dogs. J Nutr 108: 203-210, 1978.
27. Hanssen H, Brunini TM, Conway M, Banning AP, Roberts NB, Mann GE, Ellory JC, Mendes Ribeiro AC. Increased L-Arginine transport in human erythrocytes in chronic heart failure. Clin Sci (Lond) 94: 43-48, 1998.
28. 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 17: 2328-2330, 2003.
29. Huynh NN, Harris EE, Chin-Dusting JF, Andrews KL. The vascular effects of different Arginase inhibitors in rat isolated aorta and mesenteric arteries. Br J Pharmacol 156: 84-93, 2009.
30. Jagnandan D, Sessa WC, Fulton D. Intracellular location regulates calcium-calmodulin-dependent activation of organelle-restricted eNOS. Am J Physiol Cell Physiol 289: C1024-C1033, 2005.
31. Jenkinson CP, Grody WW, Cederbaum SD. Comparative properties of Arginases. Comp Biochem Physiol B Biochem Mol Biol 114: 107-132, 1996.
32. Johnson FK, Johnson RA, Peyton KJ, Durante W. Arginase inhibition restores arteriolar endothelial function in Dahl rats with salt-induced hypertension. Am J Physiol Regul Integr Comp Physiol 288: R1057-R1062, 2005.
33. Kampfer H, Pfeilschifter J, Frank S. Expression and activity of Arginase isoenzymes during normal and diabetes-impaired skin repair. J Invest Dermatol 121: 1544-1551, 2003.
34. Kashyap SR, Lara A, Zhang R, Park YM, DeFronzo RA. Insulin reduces plasma Arginase activity in type 2 diabetic patients. Diabetes Care 31: 134-139, 2008.
35. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 88: 4651-4655, 1991.
36. Lamas S, Marsden PA, Li GK, Tempst P, Michel T. Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc Natl Acad Sci USA 89: 6348-6352, 1992.
37. Lerman A, Zeiher AM. Endothelial function: cardiac events. Circulation 111: 363-368, 2005.
38. Li C, Huang W, Harris MB, Goolsby JM, Venema RC. Interaction of the endothelial nitric oxide synthase with the CAT-1 Arginine transporter enhances NO release by a mechanism not involving Arginine transport. Biochem J 386: 567-574, 2005.
39. Loyaga-Rendon RY, Sakamoto S, Beppu M, Aso T, Ishizaka M, Takahashi R, Azuma H. Accumulated endogenous nitric oxide synthase inhibitors, enhanced Arginase activity, attenuated dimethylArginine dimethylaminohydrolase activity and intimal hyperplasia in premenopausal human uterine arteries. Atherosclerosis 178: 231-239, 2005.
40. McDonald KK, Zharikov S, Block ER, Kilberg MS. A caveolar complex between the cationic amino acid transporter 1 and endothelial nitricoxide synthase may explain the "Arginine paradox". J Biol Chem 272: 31213-31216, 1997.
41. 2+-calmodulin and caveolin. J Biol Chem 272: 15583-15586, 1997.
42. Michel T, Li GK, Busconi L. Phosphorylation and subcellular translocation of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 90: 6252-6256, 1993.
43. Morris CR, Kato GJ, Poljakovic M, Wang X, Blackwelder WC, Sachdev V, Hazen SL, Vichinsky EP, Morris SM Jr, Gladwin MT. Dysregulated Arginine metabolism, hemolysis-associated pulmonary hypertension, and mortality in sickle cell disease. JAMA 294: 81-90, 2005.
44. Morris SM Jr. Regulation of enzymes of the urea cycle and Arginine metabolism. Annu Rev Nutr 22: 87-105, 2002.
45. Morris SM Jr, Bhamidipati D, Kepka-Lenhart D. Human type II Arginase: sequence analysis and tissue-specific expression. Gene 193: 157-161, 1997.
46. Morris SM Jr, Gao T, Cooper TK, Kepka-Lenhart D, Awad AS. Arginase-2 mediates diabetic renal injury. Diabetes 60: 3015-3022, 2011.
47. Morris SM Jr, Kepka-Lenhart D, Chen LC. Differential regulation of Arginases and inducible nitric oxide synthase in murine macrophage cells. Am J Physiol Endocrinol Metab 275: E740-E747, 1998.
48. Narayanan SP, Suwanpradid J, Saul A, Xu Z, Still A, Caldwell RW, Caldwell RB. Arginase 2 deletion reduces neuro-glial injury and improves retinal function in a model of retinopathy of prematurity. PloS One 6: e22460, 2011.
49. Ohtake A, Takiguchi M, Shigeto Y, Amaya Y, Kawamoto S, Mori M. Structural organization of the gene for rat liver-type Arginase. J Biol Chem 263: 2245-2249, 1988.
50. Qian J, Zhang Q, Church JE, Stepp DW, Rudic RD, Fulton DJ. Role of local production of endothelium-derived nitric oxide on cGMP signal-ing and S-nitrosylation. Am J Physiol Heart Circ Physiol 298: H112-H118, 2010.
51. Radomski MW, Palmer RM, Moncada S. Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium. Lancet 2: 1057-1058, 1987.
52. Rodriguez S, Richert L, Berthelot A. Increased Arginase activity in aorta of mineralocorticoid-salt hypertensive rats. Clin Exp Hypertens 22: 75-85, 2000.
53. Romero MJ, Iddings JA, Platt DH, Ali MI, Cederbaum SD, Stepp DW, Caldwell RB, Caldwell RW. Diabetes-induced vascular dysfunction involves Arginase I. Am J Physiol Heart Circ Physiol 302: H159-H166, 2012.
54. Rose WC, Haines WJ, Warner DT. The amino acid requirements of man. V. The rôle of lysine, Arginine, and tryptophan. J Biol Chem 206: 421-430, 1954.
55. Rossitch E Jr, Alexander E 3rd, Black PM, Cooke JP. L-Arginine normalizes endothelial function in cerebral vessels from hypercholesterolemic rabbits. J Clin Invest 87: 1295-1299, 1991.
56. Ryoo S, Berkowitz DE, Lim HK. Endothelial Arginase II and atherosclerosis. Korean J Anesthesiol 61: 3-11, 2011.
57. Ryoo S, Bhunia A, Chang F, Shoukas A, Berkowitz DE, Romer LH. OxLDL-dependent activation of Arginase II is dependent on the LOX-1 receptor and downstream RhoA signaling. Atherosclerosis 214: 279-287, 2011.
58. Santhanam L, Christianson DW, Nyhan D, Berkowitz DE. Arginase and vascular aging. J Appl Physiol 105: 1632-1642, 2008.
59. Scotland RS, Morales-Ruiz M, Chen Y, Yu J, Rudic RD, Fulton D, Gratton JP, Sessa WC. Functional reconstitution of endothelial nitric oxide synthase reveals the importance of serine 1179 in endotheliumdependent vasomotion. Circ Res 90: 904-910, 2002.
60. Sessa WC, Barber CM, Lynch KR. Mutation of N-myristoylation site converts endothelial cell nitric oxide synthase from a membrane to a cytosolic protein. Circ Res 72: 921-924, 1993.
61. Sessa WC, Garcia-Cardena G, Liu J, Keh A, Pollock JS, Bradley J, Thiru S, Braverman IM, Desai KM. The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J Biol Chem 270: 17641-17644, 1995.
62. Sessa WC, Harrison JK, Barber CM, Zeng D, Durieux ME, D'Angelo DD, Lynch KR, Peach MJ. Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem 267: 15274-15276, 1992.
63. Simon A, Plies L, Habermeier A, Martine U, Reining M, Closs EI. Role of neutral amino acid transport and protein breakdown for substrate supply of nitric oxide synthase in human endothelial cells. Circ Res 93: 813-820, 2003.
64. 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 318: 1368-1374, 2006.
65. Venema RC, Sayegh HS, Arnal JF, Harrison DG. Role of the enzyme calmodulin-binding domain in membrane association and phospholipid inhibition of endothelial nitric oxide synthase. J Biol Chem 270: 14705-14711, 1995.
66. Venema VJ, Marrero MB, Venema RC. Bradykinin-stimulated protein tyrosine phosphorylation promotes endothelial nitric oxide synthase translocation to the cytoskeleton. Biochem Biophys Res Commun 226: 703-710, 1996.
67. Vockley JG, Tabor DE, Kern RM, Goodman BK, Wissmann PB, Kang DS, Grody WW, Cederbaum SD. Identification of mutations (D128G, H141L) in the liver Arginase gene of patients with hyperArgininemia. Hum Mutat 4: 150-154, 1994.
68. Waddington SN, Cattell V. Arginase in glomerulonephritis. Exp Nephrol 8: 128-134, 2000.
69. Wilson AM, Harada R, Nair N, Balasubramanian N, Cooke JP. L-Arginine supplementation in peripheral arterial disease: no benefit and possible harm. Circulation 116: 188-195, 2007.
70. Wu G, Morris SM Jr. Arginine metabolism: nitric oxide and beyond. Biochem J 336: 1-17, 1998.
71. Xu W, Kaneko FT, Zheng S, Comhair SA, Janocha AJ, Goggans T, Thunnissen FB, Farver C, Hazen SL, Jennings C, Dweik RA, Arroliga AC, Erzurum SC. Increased Arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J 18: 1746-1748, 2004.
72. Zhang C, Hein TW, Wang W, Chang CI, Kuo L. Constitutive expression of Arginase in microvascular endothelial cells counteracts nitric oxide-mediated vasodilatory function. FASEB J 15: 1264-1266, 2001.
73. Zhang C, Hein TW, Wang W, Miller MW, Fossum TW, McDonald MM, Humphrey JD, Kuo L. Upregulation of vascular Arginase in hypertension decreases nitric oxide-mediated dilation of coronary arterioles. Hypertension 44: 935-943, 2004.
74. Zhang Q, Church JE, Jagnandan D, Catravas JD, Sessa WC, Fulton D. Functional relevance of Golgi-and plasma membrane-localized endothelial NO synthase in reconstituted endothelial cells. Arterioscler Thromb Vasc Biol 26: 1015-1021, 2006.
75. Zimmermann N, King NE, Laporte J, Yang M, Mishra A, Pope SM, Muntel EE, Witte DP, Pegg AA, Foster PS, Hamid Q, Rothenberg ME. Dissection of experimental asthma with DNA microarray analysis identifies Arginase in asthma pathogenesis. J Clin Invest 111: 1863-1874, 2003.