Mitochondrial arginase II constrains endothelial NOS-3 activity

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 6, 2007, Pages

  Lim, Hyun Kyo ^a,b   Lim, Hyun Kyoung ^a   Ryoo, Sungwoo ^a   Benjo, Alex ^a   Shuleri, Karl ^a   Miriel, Victor ^a   Baraban, Ezra ^a   Camara, Andre ^a   Soucy, Kevin ^a   Nyhan, Daniel ^a   Shoukas, Artin ^a   Berkowitz, Dan E ^a,c  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b Yonsei University Wonju   (South Korea)

^c JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

Mitochondria; Nitric oxide; Vascular stiffness

Indexed keywords

ACETYLCHOLINE; ARGINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MITOCHONDRIAL ARGINASE 2; N(G) NITROARGININE METHYL ESTER; PHENYLEPHRINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASODILATATION; WESTERN BLOTTING; WILD TYPE;

ACETYLCHOLINE; ANIMALS; AORTA; ARGINASE; CAROTID ARTERIES; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ELASTICITY; ENDOTHELIAL CELLS; ENZYME INHIBITORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHENYLEPHRINE; PULSATILE FLOW; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATION; VASODILATOR AGENTS;

EID: 36849049916     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00700.2007     Document Type: Article

References (30)

1. Benjo A, Gupta G, Ryoo S, Lim HK, Santhanam L, Soucy KG, Sohi JS, Pellakura L, Anderson M, Shoukas A, Gerstenblith G, Nyhan D, Huso D, Berkowitz DE. Arginase inhibition decreases vascular stiffness and increases NO production in apoE knock-out mice (Abstract). Circulation Suppl: 113: 227, 2006.
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. 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 283: 923-927, 2001.
4. Choy JC, Granville DJ, Hunt DW, McManus BM. Endothelial cell apoptosis: biochemical characteristics and potential implications for atherosclerosis. J Mol Cell Cardiol 33: 1673-1690, 2001.
5. Davidson SM, Duchen MR. Endothelial mitochondria: contributing to vascular function and disease. Circ Res 100: 1128-1141, 2007.
6. De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol 130: 963-974, 2000.
7. Demougeot C, Prigent-Tessier A, Marie C, Berthelot A. Arginase inhibition reduces endothelial dysfunction and blood pressure rising in spontaneously hypertensive rats. J Hypertens 23: 971-978, 2005.
8. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714, 2006.
9. 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.
10. Gao S, Chen J, Brodsky SV, Huang H, Adler S, Lee JH, Dhadwal N, Cohen-Gould L, Gross SS, Goligorsky MS. Docking of endothelial nitric oxide synthase (eNOS) to the mitochondrial outer membrane: a pentabasic amino acid sequence in the autoinhibitory domain of eNOS targets a proteinase K-cleavable peptide on the cytoplasmic face of mitochondria. J Biol Chem 279: 15968-15974, 2004.
11. Jenkinson CP, Grody WW, Cederbaum SD. Comparative properties of arginases. Comp Biochem Physiol B Biochem Mol Biol 114: 107-132, 1996.
12. 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.
13. ω-nitro-L-arginine methyl ester. Hypertens Res 28: 439-445, 2005.
14. Kobayashi M, Inoue K, Warabi E, Minami T, Kodama T. A simple method of isolating mouse aortic endothelial cells. J Atheroscler Thromb 12: 138-142, 2005.
15. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111: 1201-1209, 2003.
16. Levillain O, Balvay S, Peyrol S. Mitochondrial expression of arginase II in male and female rat inner medullary collecting ducts. J Histochem Cytochem 53: 533-541, 2005.
17. 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.
18. Ming XF, Barandier C, Viswambharan H, Kwak BR, Mach F, Mazzolai L, Hayoz D, Ruffieux J, Rusconi S, Montani JP, Yang Z. Thrombin stimulates human endothelial arginase enzymatic activity via RhoA/ROCK pathway: implications for atherosclerotic endothelial dysfunction. Circulation 110: 3708-3714, 2004.
19. Ryoo S, Lemmon CA, Soucy KG, Gupta G, White AR, Nyhan D, Shoukas A, Romer LH, Berkowitz DE. Oxidized low-density lipoprotein-dependent endothelial arginase II activation contributes to impaired nitric oxide signaling. Circ Res 99: 951-960, 2006.
20. 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.
21. Sowa G, Liu J, Papapetropoulos A, Rex-Haffner M, Hughes TE, Sessa WC. Trafficking of endothelial nitric-oxide synthase in living cells. Quantitative evidence supporting the role of palmitoylation as a kinetic trapping mechanism limiting membrane diffusion. J Biol Chem 274: 22524-22531, 1999.
22. Steppan J, Ryoo S, Schuleri KH, Gregg C, Hasan RK, White AR, Bugaj LJ, Khan M, Santhanam L, Nyhan D, Shoukas AA, Hare JM, Berkowitz DE. Arginase modulates myocardial contractility by a nitric oxide synthase 1-dependent mechanism. Proc Natl Acad Sci USA 103: 4759-4764, 2006.
23. Thorup C, Jones CL, Gross SS, Moore LC, Goligorsky MS. Carbon monoxide induces vasodilation and nitric oxide release but suppresses endothelial NOS. Am J Physiol Renal Physiol 277: F882-F889, 1999.
24. 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.
25. Vergnani L, Hatrik S, Ricci F, Passaro A, Manzoli N, Zuliani G, Brovkovych V, Fellin R, Malinski T. Effect of native and oxidized low-density lipoprotein on endothelial nitric oxide and superoxide production: key role of L-arginine availability. Circulation 101: 1261-1266, 2000.
26. Vockley JG, Jenkinson CP, Shukla H, Kern RM, Grody WW, Cederbaum SD. Cloning and characterization of the human type II arginase gene. Genomics 38: 118-123, 1996.
27. White AR, Ryoo S, Li D, Champion HC, Steppan J, Wang D, Nyhan D, Shoukas AA, Hare JM, Berkowitz DE. Knockdown of arginase I restores NO signaling in the vasculature of old rats. Hypertension 47: 245-251, 2006.
28. ob) mice. J Appl Physiol 89: 2382-2390, 2000.
29. 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.
30. Zmijewski JW, Moellering DR, Le Goffe C, Landar A, Ramachandran A, Darley-Usmar VM. Oxidized LDL induces mitochondrially associated reactive oxygen/nitrogen species formation in endothelial cells. Am J Physiol Heart Circ Physiol 289: H852-H861, 2005.