Role of arginase in vessel wall remodeling

Frontiers in Immunology

Volumn 4, Issue MAY, 2013, Pages

  Durante, William ^a  

^a University of Missouri   (United States)

Author keywords

Arginase; Endothelial dysfunction; Nitric oxide; Smooth muscle cell proliferation; Vascular remodeling

Indexed keywords

APOLIPOPROTEIN E; ARGINASE; ARGINASE 1; ARGINASE 2; ATORVASTATIN; BIOFLAVONOID; CATECHIN; CHOLESTEROL; CILOSTAMIDE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; EPICATECHIN GALLATE; ESTRADIOL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2; LISINOPRIL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MEVINOLIN; NITRIC OXIDE SYNTHASE; PROTEIN P21; QUERCETIN; RHO FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; SALVIA MILTIORRHIZA EXTRACT; SIMVASTATIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNINDEXED DRUG;

AGING; ARTERY INJURY; ATHEROSCLEROSIS; BLOOD VESSEL WALL; BLOOD VESSEL WALL REMODELING; CELL CYCLE ARREST; CELL PROLIFERATION; COLLAGEN SYNTHESIS; ENDOTHELIAL DYSFUNCTION; GENE EXPRESSION; HUMAN; HYPERPLASIA; HYPOXIA; NONHUMAN; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; REVIEW; SMOOTH MUSCLE FIBER;

EID: 84883773473     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00111     Document Type: Review

References (124)

1. Alef, M. J., Vallabhaneni, R., Carchman, E., Morris, S. M. Jr., Shiva, S., Wang, Y., et al. (2011). Nitrite-generated NO circumvents dysregulated arginine/NOS signaling to protect against intimal hyerplasia in Sprague-Dawley rats. J. Clin. Invest. 121, 1646-1656.
2. Bachetti, T., Comini, L., Francolini, G., Bastianon, D., Valetti, B., Cadei, M., et al. (2004). Arginase pathway in human endothelial cells in pathophysiological conditions. J. Mol. Cell. Cardiol. 37, 515-523.
3. Baek, K. J., Thiel, B. A., Lucas, S., and Steuhr, D. J. (1993). Macrophage nitric oxide synthase subunits: purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J. Biol. Chem. 268, 21120-21129.
4. Bagnost, T., Berthelot, A., Bouhaddi, M., Laurant, P., Andre, C., Guillame, Y., et al. (2008). Treatment with the arginase inhibitor Nω-hydroxy-nor-L-arginine improves vascular function and lowers blood pressure in adult spontaneously hypertensive rat. J. Hypertens. 26, 1110-1118.
5. Bagnost, T., Ma, L., da Silva, R. F., Rezakhaniha, R., Houdayer, C., Stergiopulos, N., et al. (2010). Cardiovascular effects of arginase inhibition in spontaneously hypertensive rats with fully developed hypertension. Cardiovasc. Res. 87, 569-577.
6. Bendeck, M. P., Irvin, C., and Reidy, M. A. (1996). Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. Circ. Res. 78, 1996.
7. Bonetti, P. O., Lerman, L. O., and Lerman, A. (2003). Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler. Thromb. Vasc. Biol. 23, 168-175.
8. Buga, G. M., Singh, R., Pervin, S., Rogers, N. E., Schmitz, D. A., Jenkinson, C. P., et al. (1996). Arginase activity in endothelial cells: inhibition by NG-hydroxyarginine during high-output nitric oxide production. Am. J. Physiol. 271, H1988-H1998.
9. Chandra, S., Romero, M. J., Shatanawi, A., Alkilany, A. M., Caldwell, R. B., and Caldwell, R. W. (2012). Oxidative species increase arginase activity in endothelial cells through the RhoA/Rho kinase pathway. Br. J. Pharmacol. 165, 506-519.
10. Chang, R., Chicoine, L. G., Cui, H., Kanagy, N. L., Walker, B. R., Liu, Y., et al. (2008). Cytokine-induced arginase activity in pulmonary endothelial cells is dependent on Src family tyrosine kinase activity. Am. J. Physiol. Lung Cell. Mol. Physiol. 295, L688-L697.
11. Chen, B., Calvert, A. E., Cui, H., and Nelin, L. D. (2009). Hypoxia promotes human pulmonary artery smooth muscle cell proliferation through the induction of arginase. Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L1151-L1159.
12. Chen, B., Calvert, A. E., Meng, X., and Nelin, L. D. (2012). Pharmacologic agents elevating cAMP prevent arginase II expression and proliferation of pulmonary arterial smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 47, 218-226.
13. Chicoine, L. G., Paffett, M. L., Young, T. L., and Nelin, L. D. (2004). Arginase inhibition increases nitric oxide production in bovine pulmonary arterial endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L60-L68.
14. Cho, W., Lee, C., Kang, M., Huang, Y., Giordano, F. J., Lee, P. J., et al. (2013). IL-13 receptor α2-arginase 2 pathway mediates IL-13-induced pulmonary hypertension. Am. J. Physiol. Lung Cell. Mol. Physiol. 304, L112-L124.
15. Christianson, D. W. (2005). Arginase: structure, mechanism, and physiological role in male and female sexual arousal. Acc. Chem. Res. 38, 191-201.
16. Dal-Ros, S., Bronner, C., Auger, C., and Schini-Kerth, V. B. (2012). Red wine polyphenols improve an established aging-related endothelial dysfunction in the mesenteric artery of middle-aged rats: role of oxidative stress. Biochem. Biophys. Res. Commun. 419, 381-387.
17. Demougeot, C., Prigent-Tesssier, A., Marie, C., and Berthelot, A. (2005). Arginase inhibition reduced endothelial dysfunction and blood pressure rising in spontaneously hypertensive rats. J. Hypertens. 23, 971-978.
18. Dizikes, G. J., Grody, W. W., Kern, R. M., and Cederbaum, S. D. (1986). Isolation of human liver arginase cDNA and demonstration of nonhomology between the two human arginase genes. Biochem. Biophys. Res. Commun. 141, 53-59.
19. Dolan, E., Thijs, L., Li, Y., Atkins, N., McCormack, P., McClory, S., et al. (2006). Ambulatory arterial stiffness index as a predictor of cardiovascular mortality in the Dublin Outcome Study. Hypertension 47, 365-370.
20. Dunn, J., Gutbrod, S., Webb, A., Pak, A., Jandu, S. K., Bhunia, A., et al. (2011). S-Nitrosylation of arginase I requires direct interaction with inducible nitric oxide synthase. Mol. Cell. Biochem. 355, 83-89.
21. Durante, W. (2001). Regulation of L-arginine transport and metabolism in vascular smooth muscle cells. Cell Biochem. Biophys. 35, 19-34.
22. Durante, W., Johnson, F. K., and Johnson, R. A. (2007). Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin. Exp. Pharmacol. Physiol. 34, 906-911.
23. Durante, W., Kroll, M. H., Orloff, G. J., Cunningham, J. M., Scott-Burden, T., Vanhoutte, P. M., et al. (1996a). Regulation of interleukin-1-beta-stimulated inducible nitric oxide synthase expression in cultured vascular smooth muscle cells by hemostatic proteins. Biochem. Pharmacol. 51, 847-853.
24. Durante, W., Liao, L., Iftikhar, I., Cheng, K., and Schafer, A. I. (1996b). Platelet-derived growth factor regulates vascular smooth muscle cell proliferation by inducing cationic amino acid transporter gene expression in cultured vascular smooth muscle cells. J. Biol. Chem. 271, 11838-11843.
25. Durante, W., Liao, L., Peyton, K. J., and Schafer, A. I. (1997). Lysophosphatidylcholine regulates cationic amino acid transport and metabolism in vascular smooth muscle cells: role in polyamine synthesis. J. Biol. Chem. 272, 30154-30159.
26. Durante, W., Liao, L., Peyton, K. J., and Schafer, A. I. (1998). Thrombin stimulates vascular smooth muscle cell polyamine synthesis by inducing cationic amino acid transporter and ornithine decarboxylase gene expression. Circ. Res. 83, 217-223.
27. Durante, W., Liao, L., Reyna, S. V., Peyton, K. J., and Schafer, A. I. (2000). Physiologic cyclic stretch directs L-arginine transport and metabolism to collagen synthesis in vascular smooth muscle cells. FASEB J. 14, 1775-1783.
28. Durante, W., Liao, L., Reyna, S. V., Peyton, K. J., and Schafer, A. I. (2001). Transforming growth factor-β1 stimulates L-arginine transport and metabolism in vascular smooth muscle cells: role in polyamine and collagen synthesis. Circulation 103, 1121-1127.
29. Dzau, V. J., Braun-Dellaeus, R. C., and Shedding, D. G. (2002). Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat. Med. 8, 1249-1256.
30. Elms, S. C., Toque, H. A., Rojas, M., Xu, Z., Caldwell, R. W., and Caldwell, R. B. (2013). The role of arginase I in diabetes-induced retinal vascular dysfunction in mouse and rat models of diabetes. Diabetologia 56, 654-662.
31. Feig, J. E., Vengrenyuk, Y., Reiser, V., Wu, C., Statnikov, A., Aliferis, C. F., et al. (2012). Regression of atherosclerosis is characterized by broad changes in the plaque macrophage transcriptome. PLoS ONE 7:39790. doi:10.1371/journal.pone.0039790
32. Forstermann, U., and Munzel, T. (2006). Endothelial nitric oxide synthase in vascular disease from marvel to menace. Circulation 113, 1708-1714.
33. Forstermann, U., and Sessa, W. C. (2012). Nitric oxide synthases: regulation and function. Eur. Heart J. 33, 829-837.
34. Forte, A., Finicelli, M., De Luca, P., Quarto, C., Onorati, F., Sante, P., et al. (2008). Expression profiles in surgically-induced carotid stenosis: a combined transcriptomic and proteomic investigation. J. Cell. Mol. Med. 12, 1956-1973.
35. Gao, X., Xu, X., Belmadani, S., Park, Y., Tang, Z., Feldman, A. M., et al. (2007). TNF-alpha contributes to endothelial dysfunction by upregulating arginase in ischemia/reperfusion injury. Arterioscler. Thromb. Vasc. Biol. 27, 1269-1275.
36. Garg, U. C., and Hassid, A. (1989). Nitric oxide-generating vasodilators and 8-Bromo-cyclic GMP inhibits mitogenesis and proliferation of cultured vascular smooth muscle cells. J. Clin. Invest. 83, 1774-1777.
37. Hayashi, T., Esaki, T., Sumi, D., Mukherjee, T., Iguchi, A., and Chaudhuri, G. (2006). Modulating role of estradiol on arginase II expression in hyperlipidemic rabbits as an atheroprotective mechanism. Proc. Natl. Acad. Sci. U.S.A. 103, 10485-10490.
38. Hecker, M., Sessa, W. C., Harris, H. J., Angard, E. E., and Vane, J. R. (1990). The metabolism of L-arginine and its significance for the biosynthesis of endothelium-derived relaxing factor: cultured endothelial cells recycle L-citrulline to L-arginine. Proc. Natl. Acad. Sci. U.S.A. 87, 8612-8616.
39. Hibbs, J. B. Jr., Taintor, R. R., Vavrin, Z., and Rachlin, E. M. (1988). Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157, 87-94.
40. Holowatz, L. A., and Kenney, W. L. (2007). Up-regulation of arginase activity contributes to attenuated reflex cutaneous vasodilation in hypertensive humans. J. Physiol. 581, 863-872.
41. Holowatz, L. A., Santhanam, L., Webb, A., Berkowitz, D. E., and Kenney, W. L. (2011). Oral atorvastatin therapy restores cutaneous microvascular function by decreasing arginase activity in hypercholestrolemic humans. J. Physiol. 589, 2093-2103.
42. Holowatz, L. A., Thompson, C. S., and Kenney, W. L. (2006). L-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilation in aged human skin. J. Physiol. 574, 573-581.
43. Humbert, M., Morrell, N. W., Archer, S. L., Stenmark, K. R., MacLean, M. R., Lang, I. M., et al. (2004). Cellular and molecular pathobiology of pulmonary arterial hypertension. J. Am. Coll. Cardiol. 43, 13S-24S.
44. Huynh, N., Harris, E., Chin-Dusting, J. F., and Andrews, K. (2009). The vascular effects of different arginase inhibitors in rat isolated aorta and mesenteric arteries. Br. J. Pharmacol. 156, 84-93.
45. Ishizaka, M., Nagai, K., Iwanaga, M., Imamura, M., and Azuma, H. (2007). Possible involvement of enhanced arginase activity due to up-regulated arginases and decreased hydroxyarginine in accelerating intimal hyperplasia with hyperglycemia. Vascul. Pharmacol. 47, 272-280.
46. Iyer, R. K., Yoo, P. K., Kern, R. M., Rozengurt, N., Tsao, R., O'Brien, W. E., et al. (2002). Mouse model for human arginase deficiency. Mol. Cell. Biol. 22, 4491-4498.
47. Jeffrey, T. K., and Wanstall, J. C. (2001). Pulmonary vascular remodeling: a target for therapeutic intervention in pulmonary hypertension. Pharmacol. Ther. 92, 1-20.
48. Jenkinson, C. P., Grody, W. W., and Cederbaum, S. D. (1996). Comparative properties of arginases. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 114B, 107-132.
49. Jin, Y., Calvert, T. J., Chen, B., Chicoine, L. G., Joshi, M., Bauer, J. A., et al. (2010). Mice deficient in Mkp-1 develop more severe pulmonary hypertension and greater lung protein levels of arginase in response to chronic hypoxia. Am. J. Physiol. Heart Circ. Physiol. 298, H1518-H1528.
50. Joe, Y., Zheng, M., Kim, H. J., Uddin, M. J., Park, C., Ryu do, G., et al. (2012). Salvianolic acid B exerts vasoprotective effects through the modulation of heme oxygenase-1 and arginase activity. J. Pharmacol. Exp. Ther. 341, 850-858.
51. Johnson, F. K., Johnson, R. A., Peyton, K. J., and Durante, W. (2005). Arginase inhibition restores arteriolar endothelial function in Dahl rats with salt-induced hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1057-1062.
52. Johnson, R. A., Durante, W., Craig, T., Peyton, K. J., Myers, J. G., Stewart, R. M., et al. (2010). Vascular arginase contributes to arteriolar endothelial dysfunction in a rat model of hemorrhagic shock. J. Trauma 69, 384-391.
53. Kapoor, M., Howard, R., Hall, I., and Appleton, I. (2004). Effects of epicatechin gallate on wound healing and scar formation in a full thickness incisional wound healing model in rats. Am. J. Pathol. 165, 299-307.
54. Keaney, J., Campbell, M., and Humphries, P. (2011). From RNA interference technology to effective therapy: how far have we come and how far to go. Ther. Deliv. 2, 1395-1406.
55. Khallou-Laschet, J., Varthaman, A., Fornasa, G., Compain, C., Gaston, A. T., Clement, M., et al. (2010). Macrophage plasticity in experimental atherosclerosis. PLoS ONE 5:e8852. doi:10.1371/journal.pone.0008852
56. Kim, J. H., Bugai, L. J., Oh, Y. J., Bivalacqua, T. J., Ryoo, S., Soucy, K. G., et al. (2009). Arginase inhibition restores NOS coupling and reverses endothelial dysfunction and vascular stiffness in old rats. J. Appl. Physiol. 107, 1249-1257.
57. Kobs, R. W., and Chesler, N. C. (2006). The mechanobiology of pulmonary vascular remodeling in the congenital absence of eNOS. Biomech. Model. Mechanobiol. 5, 217-225.
58. Kolpakov, V., Gordon, D., and Kulik, T. J. (1995). Nitric oxide-generating compounds inhibit total protein and collagen synthesis in cultured vascular smooth muscle cells. Circ. Res. 76, 305-309.
59. Kosenko, E., Tikhonova, L., Suslikov, A., and Kaminsky, Y. (2012). Impacts of lisinopril and lisinopril plus simvastatin on erythrocyte plasma arginase, nitrite, and nitrate in hypertensive patients. J. Clin. Pharmacol. 52, 102-109.
60. Krotova, K., Patel, J. M., Block, E. R., and Zharikov, S. (2010). Hypoxic upregulation of arginase II in human lung endothelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 299, C1541-1548.
61. Lerman, A., and Zeiher, A. M. (2005). Endothelial function: cardiac events. Circulation 111, 363-368.
62. Li, H., Meininger, C. J., Kelly, K. A., Hawker, J. R. Jr., Morris, S. M. Jr., and Wu, G. (2002). Activities of arginase I and II are limiting for endothelial cell proliferation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R64-R69.
63. Libby, P. (2002). Inflammation in atherosclerosis. Nature 420, 868-874.
64. Liu, L., Guo, X., Rao, J. N., Zou, T., Marasa, B. S., Chen, J., et al. (2006). Polyamine-modulated c-myc expression in normal intestinal epithelial cells regulates p21Cip transcription through a proximal promoter region. Biochem. J. 398, 257-267.
65. Loyaga-Rendon, R. Y., Sakamoto, S., Beppu, M., Aso, T., Ishizaka, M., Takahashi, R., et al. (2005). 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.
66. Mantovani, A., Garlanda, C., and Locati, M. (2009). Macrophage diversity and polarization in atherosclerosis: a question of balance. Arterioscler. Thromb. Vasc. Biol. 29, 1419-1423.
67. Marinova, G. V., Loyaga-Rendon, R. Y., Obayashi, S., Ishibashi, T., Kubota, T., Imamura, M., et al. (2008). Possible involvement of altered arginase activity, arginase type I and type II expressions, and nitric oxide production in occurrence of intimal hyperplasia in premenopausal human uterine arteries. J. Pharmacol. Sci. 106, 385-393.
68. Martinez, F. O., Helming, L., and Gordon, S. (2009). Alternative activation of macrophages: an immunological functional perspective. Annu. Rev. Immunol. 27, 451-483.
69. Mattace-Raso, F. U., van der Cammen, T. J., Hofman, A., van Popele, N. M., Bos, M. L., Schalekamp, M. A., et al. (2006). Arterial stiffness and risk of coronary heart disease and stroke: the Rotterdam Study. Circulation 113, 657-663.
70. Michell, D. L., Andrews, K. L., and Chin-Dusting, J. P. F. (2011). Endothelial dysfunction in hypertension: the role of arginase. Front. Biosci. (Schol. Ed.) 3, 946-960.
71. Ming, X.-F., Barandier, C., Viswambharan, H., Kwak, B. R., Mach, F., Mazzolai, L., et al. (2004). Thrombin stimulates human endothelial arginase enzymatic activity via the RhoA/ROCK pathway: implications for atherosclerotic endothelial dysfunction. Circulation 110, 3708-3714.
72. Ming, X.-F., Rajapakse, A. G., Yepuri, G., Xiong, Y., Carvas, J. M., Ruffieux, J., et al. (2012). Arginase II promotes macrophage inflammatory responses through mitochondrial reactive oxygen species, contributing to insulin resistance and atherogenesis. J. Am. Heart Assoc. 1, e000992.
73. Mirea, O., Donoiu, I., and Plesea, I. E. (2012). Arterial aging: a brief review. Rom. J. Morphol. Embryol. 53, 473-477.
74. Morris, S. M. Jr. (2009). Recent advances in arginine metabolism: roles and regulation of the arginases. Br. J. Pharmacol. 157, 922-930.
75. Morris, S. M. Jr., Bhamidipati, D., and Kepka-Lenhart, D. (1997). Human type II arginase: sequence analysis and tissue-specific expression. Gene 193, 157-161.
76. Morrison, R. F., and Seidel, E. R. (1995). Vascular endothelial cell proliferation: regulation of cellular polyamines. Cardiovasc. Res. 29, 841-847.
77. Nelin, L. D., Chicoine, L. G., Reber, K. M., English, B. K., Young, T. L., and Liu, Y. (2005). Cytokine-induced endothelial arginase expression is dependent on epidermal growth factor receptor. Am. J. Respir. Cell Mol. Biol. 33, 394-401.
78. Nikolic, J., Cvetkovic, T., and Sokolovic, D. (2003). Role of quercetin on hepatic urea production in acute renal failure. Ren. Fail. 25, 149-155.
79. Orford, J. L., Selwyn, A. P., Ganz, P., Popma, J. J., and Rogers, C. (2000). The comparative pathobiology of atherosclerosis and restenosis. Am. J. Cardiol. 86, 6H-11H.
80. Owens, G. K., Kumar, M. S., and Wamhoff, B. R. (2004). Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801.
81. Palmer, R. M. J., Ashton, D. S., and Moncada, S. (1988). Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature 333, 664-666.
82. Peyton, K. J., Ensenat, D., Azam, M. A., Keswani, A. N., Kannan, S., Liu, X.-M., et al. (2009). Arginase promotes neointima formation in rat injured carotid arteries. Arterioscler. Thromb. Vasc. Biol. 29, 488-494.
83. Regunathan, S., Youngson, C., Raasch, W., Wang, H., and Reis, D. J. (1996). Imidazoline receptors and agmatine in blood vessels: a novel system inhibiting vascular smooth muscle cell proliferation. J. Pharmacol. Exp. Ther. 276, 1272-1282.
84. Rodriguez, S., Richert, L., and Berthelot, A. (2000). Increased arginase activity in aorta of mineralocorticoid-salt hypertensive rats. Clin. Exp. Hypertens. 22, 75-85.
85. Romero, M. J., Platt, D. H., Tawfik, H. E., Labazi, M., El-Remessy, A. B., Bartoli, M., et al. (2008). Diabetes-induced coronary vascular dysfunction involves increased arginase activity. Circ. Res. 102, 95-102.
86. Ross, R. (1999). Atherosclerosis: an inflammatory disease. N. Engl. J. Med. 340, 115-126.
87. Ryoo, S., Bhunia, A., Chang, F., Shoukas, A., Berkowitz, D. E., and Romer, L. H. (2011). OxLDL-dependent activation of arginase II is dependent on the LOX-1 receptor and downstream RhoA signaling. Atherosclerosis 214, 279-287.
88. Ryoo, S., Gupta, G., Benjo, A., Lim, H. K., Camara, A., Sikka, G., et al. (2008). Endothelial arginase II. A novel target for the treatment of atherosclerosis. Circ. Res. 102, 923-932.
89. Santhanam, L., Lim, H. K., Lim, H. K., Miriel, V., Brown, T., Patel, M., et al. (2007). Inducible NO synthase dependent S-nitrosylation and activation of arginase 1 contribute to age-related endothelial dysfunction. Circ. Res. 101, 692-702.
90. Sasaki, A., Doi, S., Mizutami, S., and Azuma, H. (2007). Roles of accumulated endogenous nitric oxide synthase inhibitors, enhanced arginase activity, and attenuated nitric oxide synthase activity in endothelial cells for pulmonary hypertension in the rats. Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L1480-L1487.
91. Schiffrin, E. L. (2012). Vascular remodeling in hypertension: mechanism and treatment. Hypertension 59, 367-374.
92. Schnorr, O., Brossette, T., Momma, T.Y., Kleinbongard, P., Keen, C.L., Schroeter, H., et al. (2008). Cocao flavanols lower vascular arginase activity in human endothelial cells in vitro and in erythrocytes in vivo. Arch. Biochem. Biophys. 476, 211-215.
93. Shatanawi, A., Romero, M. J., Iddings, J. A., Chandra, S., Umpathy, N. S., Verin, A. D., et al. (2011). Angiotensin II-induced vascular endothelial dysfunction through RhoA/Rho kinase/p38 mitogen-activated protein kinase/arginase pathway. Am. J. Physiol. Cell Physiol. 300, C1181-1192.
94. Shemyakin, A., Kovamees, O., Rafnsson, A., Bohm, F., Svenarud, P., Settergren, M., et al. (2012). Arginase inhibition improves endothelial function in patients with coronary artery disease and type 2 diabetes. Circulation 126, 2943-2950.
95. Shi, O., Morris, S. M. Jr., Zoghbi, H., Porter, C. W., and O'Brien, W. E. (2001). Generation of a mouse model for arginase II deficiency by targeted disruption of the arginase II gene. Mol. Cell. Biol. 21, 811-813.
96. Shibata, N., and Glass, C. K. (2009). Regulation of macrophage function in inflammation and atherosclerosis. J. Lipid Res. 50, S277-S281.
97. Shin, W., Berkowitz, D. E., and Ryoo, S. (2012). Increased arginase II activity contributes to endothelial dysfunction through endothelial nitric oxide synthase uncoupling in aged mice. Exp. Mol. Med. 44, 594-602.
98. Sutton-Tyrrell, K., Najjar, S. S., Boudreau, R. M., Venkitachalam, L., Kupelian, V., Simonisick, E. M., et al. (2005). Elevated aortic pulse wave velocity, a marker of arterial stiffness, predicts cardiovascular events in well-functioning older adults. Circulation 111, 3384-3390.
99. Tabor, C. W., and Tabor, H. (1984). Polyamines. Annu. Rev. Biochem. 53, 749-790.
100. Taddei, S., Virdis, A., Ghiadoni, L., Salvetti, G., Bernini, G., Magagna, A., et al. (2001). Age-related reduction of NO availability and oxidative stress in humans. Hypertension 38, 274-279.
101. Teupser, D., Burkhardt, R., Wilfert, W., Haffner, I., Nebendahl, K., and Thiery, J. (2006). Identification of arginase I as a new candidate gene of atherosclerosis resistance. Arterioscler. Thromb. Vasc. Biol. 26, 365-371.
102. Thacher, T. N., Gambillara, V., Riche, F., Silacci, P., Stergiopulos, N., and da Silva, R. F. (2010). Regulation of arginase pathway in response to wall shear stress. Atherosclerosis 210, 63-70.
103. Thengchaisri, N., Hein, T. W., Wang, W., Xu, X., Li, Z., Fossum, T. W., et al. (2006). Upregulation of arginase by H2O2 impairs endothelium-dependent nitric oxide-mediated dilation of coronary arteries. Arterioscler. Thromb. Vasc. Biol. 26, 2035-2042.
104. Thomas, A. C., Sala-Newby, G. B., Ismail, Y., Johnson, J. L., Pasterkamp, G., and Newby, A. C. (2007). Genomics of foam cells and nonfoamy macrophages from rabbits identifies arginase I as a differential regulator of nitric oxide production. Arterioscler. Thromb. Vasc. Biol. 27, 571-577.
105. Toby, I. T., Chicoine, L. G., Cui, H., Chen, B., and Nelin, L. D. (2010). Hypoxia-induced proliferation of human pulmonary microvascular endothelial cells depends on epidermal growth factor receptor tyrosine kinase activation. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L600-L606.
106. Tulis, D. A., Durante, W., Peyton, K. J., Chapman, G. B., Evans, A. J., and Schafer, A. I. (2000). YC-1, a benzyl indozole derivative, stimulates vascular cGMP and inhibits neointima formation. Biochem. Biophys. Res. Commun. 279, 646-652.
107. Vaisman, B. L., Andrews, K. L., Khong, S. M. L., Wood, K. C., Moore, X. L., Fu, Y., et al. (2012). Selective endothelial overexpression of arginase II induces endothelial dysfunction and hypertension and enhances atherosclerosis in mice. PLoS ONE 7:e39487. doi:10.1371/journal.pone.0039487
108. van Varik, B. J., Rennenberg, R. J. M. W., Reutelingsperger, C. P., Kroon, A. A., de Leeuw, P. W., and Schurgers, L. J. (2012). Mechanisms of arterial remodeling: lessons from genetic diseases. Front. Genet. 3:290. doi:10.3389/fgene.2012.00290
109. Versari, D., Lerman, L. O., and Lerman, A. (2007). The importance of reendothelialization after arterial injury. Curr. Pharm. Des. 13, 1811-1824.
110. Virmani, R., Avolio, A. P., Mergner, W. J., Robinowitz, M., Herderick, E. E., Cornhill, J. F., et al. (1991). Effect of aging on aortic morphology in populations with high and low prevalence of hypertension and atherosclerosis. Comparison between occidental and Chinese communities. Am. J. Pathol. 139, 1119-1129.
111. Vockley, J. G., Jenkinson, C. P., Shukla, H., Kern, R. M., Grody, W. W., and Cederbaum, S. D. (1996). Cloning and characterization of the human type II arginase gene. Genomics 2, 118-123.
112. Wang, X., Chen, Y., Qin, W., Zhang, W., Wei, S., Wang, J., et al. (2011a). Arginase I attenuates inflammatory cytokine secretion induced by lipopolysaccharide in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 31, 1853-1860.
113. Wang, W., Hein, T. W., Zhang, C., Zawieja, D. C., Liao, J. C., and Kuo, L. (2011b). Oxidized low-density lipoprotein inhibits nitric oxide-mediated coronary arteriolar dilation by up-regulating endothelial arginase I. Microcirculation 18, 36-45.
114. Wei, L. H., Jacobs, A. T., Morris, S. M. Jr., and Ignarro, L. J. (2000). IL-4 and IL-13 upregulate arginase I expression by cAMP and JAK/STAT6 pathways in vascular smooth muscle cells. Am. J. Physiol. Cell Physiol. 279, C248-C256.
115. Wei, L. H., Wu, G., Morris, S. M. Jr., and Ignarro, L. J. (2001). Elevated arginase I expression in rat aortic smooth muscle cells increases cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 98, 9260-9264.
116. Wu, G., and Morris, S. M. Jr. (1998). Arginine metabolism: nitric oxide and beyond. Biochem. J. 336, 1-7.
117. Xu, W., Kaneko, F. T., Zheng, S., Comhair, S. A., Janocha, A. J., Goggans, T., et al. (2004). Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary hypertension. FASEB J. 18, 1746-1748.
118. Yan, Z. Q., Yokota, T., Zhang, W., and Hansson, G. K. (1996). Expression of inducible nitric oxide synthase inhibits platelet adhesion and restores blood flow in the injured artery. Circ. Res. 79, 38-44.
119. Yang, L., Lewis, C. M., Chandrasekharan, U. M., Kinney, C. M., Dicorletto, P. E., and Kashyap, V. S. (2006). Arginase activity is increased by thrombin: a mechanism for endothelial dysfunction in arterial thrombosis. J. Am. Coll. Surg. 203, 817-826.
120. Yao, L., Chandra, S., Toque, H. A., Bhatta, A., Rojas, M., Caldwell, R. B., et al. (2013). Prevention of diabetes-induced arginase activation and vascular dysfunction by Rho kinase (ROCK) knockout. Cardiovasc. Res. 97, 509-519.
121. Zeki, A. A., Bratt, J. M., Rabowsky, M., Last, J. A., and Kenyon, N. J. (2010). Simvastatin inhibits goblet cell hyperplasia and lung arginase in a mouse model of allergic asthma: a novel treatment for airway remodeling. Transl. Res. 156, 335-349.
122. Zhang, C., Hein, T. W., Wang, W., Miller, M. W., Fossum, T. W., McDonald, M. M., et al. (2004). Upregulation of vascular arginase in hypertension decreases nitric oxide-mediated dilation of coronary arterioles. Hypertension 44, 935-943.
123. Zharikov, S., Krotova, K., Hu, H., Baylis, C., Johnson, R. J., Block, E. R., et al. (2008). Uric acid decreases NO production and increases arginase activity in cultured pulmonary artery endothelial cells. Am. J. Physiol. Cell Physiol. 295, C1183-C1190.
124. Zhu, W., Chandrasekharan, U. M., Bandyopadhyay, S., Morris, S. M. Jr., DiCorletto, P. E., and Kashyap, V. S. (2010). Thrombin induces endothelial arginase through AP-1 activation. Am. J. Physiol. Cell Physiol. 298, C952-C960.