Competitive metabolism of L -arginine: arginase as a therapeutic target in asthma

Siddiqui, 2008, Structural aspects of airway re-modeling in asthma, Curr Allergy Asthma Rep, 8, 540, 10.1007/s11882-008-0098-3 Bentley, 2008, Airway smooth muscle growth in asthma: proliferation, hypertrophy, and mi-gration, Proc Am Thorac Soc, 5, 89, 10.1513/pats.200705-063VS Wilson, 1997, The measurement of reticular base-ment membrane and submucosal collagen in the asth-matic airway, Clin Exp Allergy, 27, 363, 10.1111/j.1365-2222.1997.tb00720.x 2005, ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, Am J Respir Crit Care Med, 171, 912, 10.1164/rccm.200406-710ST Singh, 2007, Selective inducible nitric oxide synthase inhibition has no effect on allergen challenge in asthma, Am J Respir Crit Care Med, 176, 988, 10.1164/rccm.200704-588OC Mabalirajan, 2010, Beneficial effects of high dose of L-arginine on airway hyperresponsiveness and airway inflammation in a murine model of asthma, J Allergy Clin Immunol, 125, 626, 10.1016/j.jaci.2009.10.065 Gaston, 2006, S-nitrosothiol signaling in respiratory biology, Am J Respir Crit Care Med, 173, 1186, 10.1164/rccm.200510-1584PP Ricciardolo, 2004, Nitric oxide in health and disease of the respiratory system, Physiol Rev, 84, 731, 10.1152/physrev.00034.2003 Lipton, 2001, S-Nitrosothiols signal the ventila-tory response to hypoxia, Nature, 413, 171, 10.1038/35093117 Li, 2000, Regulation of ciliary beat frequency by the nitric oxide-cyclic gua-nosine monophosphate signaling pathway in rat airway epithelial cells, Am J Respir Cell Mol Biol, 23, 175, 10.1165/ajrcmb.23.2.4022 Aizawa, 1999, Role of nitric oxide released from iNANC neurons in airway responsiveness in cats, Eur Respir J, 3, 775, 10.1034/j.1399-3003.1999.13d13.x Tucker, 1990, L-NG-nitroarginine inhibits non-adrenergic, non-cholinergic relaxations of guinea-pig isolated tracheal smooth muscle, Br J Pharmacol, 100, 663, 10.1111/j.1476-5381.1990.tb14072.x Kesler, 2002, Nitric Oxide–de-pendent Modulation of Smooth-Muscle Tone by Airway Parasympathetic Nerves, Am J Respir Crit Care Med, 165, 481, 10.1164/ajrccm.165.4.2004005 Kubes, 1991, Nitric oxide: an en-dogenous modulator of leukocyte adhesion, Proc Natl Acad Sci USA, 88, 4651, 10.1073/pnas.88.11.4651 De Caterina, 1995, Nitric oxide de-creases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of ad-hesion molecules and proinflammatory cytokines, J Clin Invest, 96, 60, 10.1172/JCI118074 Bernareggi, 1997, Dual action of nitric oxide on airway plasma leakage, Am J Respir Crit Care Med, 155, 869, 10.1164/ajrccm.155.3.9117019 Schmidt, 1994, NO at work, Cell, 78, 919, 10.1016/0092-8674(94)90267-4 MacMicking, 1995, Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase, Cell, 81, 641, 10.1016/0092-8674(95)90085-3 Shaw, 2007, The use of exhaled nitric oxide to guide asthma management: a randomized controlled trial, Am J Respir Crit Care Med, 176, 231, 10.1164/rccm.200610-1427OC Mathrani, 2007, Mouse models of asthma: can they give us mechanistic insights into the role of nitric oxide?, Curr Med Chem, 14, 2204, 10.2174/092986707781389628 Vercelli, 2003, Arginase: marker, effector, or candidate gene for asthma?, J Clin Invest, 111, 1815, 10.1172/JCI200318908 Kukreja, 2007, eNOS phosphorylation: a pivotal molecular switch in vasodilation and cardioprotection?, J Mol Cell Cardiol, 42, 280, 10.1016/j.yjmcc.2006.10.011 Guo, 2007, Identification of a classic cytokine-induced enhancer upstream in the human iNOS promoter, FASEB J, 21, 535, 10.1096/fj.06-6739com Marks-Konczalik, 1998, Cytokine-mediated transcriptional induction of the human inducible nitric oxide synthase gene requires both activator protein 1 and nuclear factor kappaB-binding sites, J Biol Chem, 273, 22201, 10.1074/jbc.273.35.22201 Chu, 1998, Analysis of the cytokine-stimulated human inducible nitric oxide synthase (iNOS) gene: characterization of differences between human and mouse iNOS promoters, Biochem Biophys Res Commun, 248, 871, 10.1006/bbrc.1998.9062 Shan, 2007, Localization and distribution of NOS1 in murine airways, Nitric Oxide, 17, 25, 10.1016/j.niox.2007.05.001 Asano, 1994, Constitutive and inducible nitric ox-ide synthase gene expression, regulation, and activity in human lung epithelial cells, Proc Natl Acad Sci U S A, 91, 10089, 10.1073/pnas.91.21.10089 Bratt, 2010, Nitric oxide synthase enzymes in the airways of mice exposed to ovalbumin: NOS2 ex-pression is NOS3 dependent, Mediators Inflamm, 10.1155/2010/321061 Liu, 1998, Accelerated reaction of nitric oxide with O2 with in hydrophobic interior of biological membranes, Proc Natl Acad Sci U S A, 95, 2175, 10.1073/pnas.95.5.2175 Zuckerbraun, 2010, Nitrite potently inhibits hy-poxic and inflammatory pulmonary arterial hypertension and smooth muscle proliferation via xanthine oxidore-ductase-dependent nitric oxide generation, Circulation, 121, 98, 10.1161/CIRCULATIONAHA.109.891077 Shiva, 2007, Deoxymyoglobin is a nitrite re-ductase that generates nitric oxide and regulates mito-chondrial respiration, Circ Res, 100, 654, 10.1161/01.RES.0000260171.52224.6b Gladwin, 2008, The functional nitrite reductase activity of the heme-globins, Blood, 112, 2636, 10.1182/blood-2008-01-115261 Cynober, 2007, Pharmacokinetics of arginine and related amino acids, J Nutr, 137, 1646S, 10.1093/jn/137.6.1646S Rawal, 1995, Structural specificity of substrate for S-adenosylmethionine:protein arginine N-methyltrans-ferases, Biochim Biophys Acta, 1248, 11, 10.1016/0167-4838(94)00213-Z Cantoni, 1975, Biological methylation: Selected aspects, Annu Rev Biochem, 44, 435, 10.1146/annurev.bi.44.070175.002251 MacAllister, 1994, Metabolism of methylarginines by human vasculature; implications for the regulation of nitric oxide synthesis, Br J Pharmacol, 112, 43, 10.1111/j.1476-5381.1994.tb13026.x Vieira, 2007, Creatine supplementation exacer-bates allergic lung inflammation and airway remodeling in mice, Am J Respir Cell Mol Biol, 37, 660, 10.1165/rcmb.2007-0108OC Galea, 1996, Inhibition of mammalian nitric oxide synthases by agmatine, an endogenous polyamine formed by de-carboxylation of arginine, Biochem J, 316, 247, 10.1042/bj3160247 Xiang, 2007, A GABAergic system in airway epithelium is es-sential for mucus overproduction in asthma, Nat Med, 13, 862, 10.1038/nm1604 Sackesen, 2008, A comprehensive evaluation of the en-zymatic and nonenzymatic antioxidant systems in child-hood asthma, J Allergy Clin Immunol, 122, 78, 10.1016/j.jaci.2008.03.035 Li, 2001, Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells, Am J Physiol Endocrinol Metab, 280, E75, 10.1152/ajpendo.2001.280.1.E75 Grody, 1987, Human argin-ase isozymes, Curr Top Biol Med Res, 13, 181 Agostinelli, 2010, Polyamines: fundamen-tal characters in chemistry and biology, Amino Acids, 38, 393, 10.1007/s00726-009-0396-7 Lau, 2000, Arginine, citrulline, and nitric oxide metabolism in end-stage renal disease patients, J Clin Invest, 105, 1217, 10.1172/JCI7199 Kao, 2009, Arginine, citrulline and nitric oxide metabo-lism in sepsis, Clin Sci (Lond), 117, 23, 10.1042/CS20080444 Askanazi, 1980, Muscle and plasma amino acids following injury. Influence of intercurrent infection, Ann Surg, 192, 78, 10.1097/00000658-198007000-00014 Shen, 2005, Accessibility of endothelial and inducible nitric oxide synthase to the intracellular citrulline–arginine regeneration pathway. Biochem, Pharmacol, 69, 97 Topal, 2006, Mitochondrial arginase II modulates nitric-oxide synthesis through nonfreely exchangeable L-arginine pools in human endothelial cells, J Pharmacol Exp Ther, 318, 1368, 10.1124/jpet.106.103747 Closs, 2000, Sub-strate supply for nitric oxide synthase in macrophages and endothelial cells: role of cationic amino acid trans-porters, Mol Pharmacol, 57, 68 Kenyon, 2008, Arginases I and II in lungs of ovalbumin-sensitized mice exposed to ovalbumin: sources and consequences, Toxicol Appl Pharmacol, 230, 269, 10.1016/j.taap.2008.03.004 Bratt, 2010, Arginase inhibition in airways from normal and nitric oxide synthase 2-knockout mice exposed to ovalbumin, Toxicol Appl Pharmacol, 242, 1, 10.1016/j.taap.2009.09.018 Morris, 2004, Decreased arginine bioavailabil-ity and increased serum arginase activity in asthma, Am J Respir Crit Care Med, 170, 148, 10.1164/rccm.200309-1304OC King, 2004, Arginine in asthma and lung inflammation, J Nutr, 134, 2830S, 10.1093/jn/134.10.2830S Zimmermann, 2003, Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis, J Clin Invest, 111, 1863, 10.1172/JCI200317912 Fajardo, 2004, Increased lev-els of hypoxia sensitive proteins in allergic airway in-flammation, Am J Respir Crit Care Med, 170, 477, 10.1164/rccm.200402-178OC Bratt, 2009, Arginase enzymes in isolated airways from normal and nitric oxide synthase 2-knockout mice ex-posed to ovalbumin, Toxicol Appl Pharmacol, 234, 273, 10.1016/j.taap.2008.10.007 Takahashi, 2010, Direct inhibition of ar-ginase attenuated airway allergic reactions and inflam-mation in a Dermatophagoides farinae-induced NC/Nga mouse model, Am J Physiol Lung Cell Mol Physiol, 10.1152/ajplung.00216.2009 Xia, 1996, Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury, Proc Natl Acad Sci U S A, 93, 6770, 10.1073/pnas.93.13.6770 Xia, 1998, Superoxide gen-eration from endothelial nitric-oxide synthase. A Ca2+/calmodulin-dependent and tetrahydrobiopterin regula-tory process, J Biol Chem, 273, 25804, 10.1074/jbc.273.40.25804 Sullivan, 2006, Coupled and Uncoupled NOS: Separate But Equal? Uncoupled NOS in Endothelial Cells Is a Critical Pathway for Intracellular Signaling, Circ Res, 98, 717, 10.1161/01.RES.0000217594.97174.c2 Yoneyama, 2001, Neuronal nitric oxide synthase generates superoxide from the oxygenase domain, Biochem J, 360, 247, 10.1042/0264-6021:3600247 Xia, 1997, Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophag-es, Proc Natl Acad Sci U S A, 94, 6954, 10.1073/pnas.94.13.6954 Xia, 1998, Inducible nitric-oxide synthase generates superoxide from the re-ductase domain, J Biol Chem, 273, 22635, 10.1074/jbc.273.35.22635 Niese, 2009, Bone marrow cell derived arginase I is the major source of allergen-induced lung arginase but is not required for airway hyperresponsiveness, remodeling and lung inflammatory responses in mice, BMC Immunol, 10, 33, 10.1186/1471-2172-10-33 Klasen, 2001, Glucocorticoids inhibit li-popolysaccharideinduced up-regulation of arginase in rat alveolar macrophages, Br J Pharmacol, 132, 1349, 10.1038/sj.bjp.0703951 Lindemann, 2003, Glucocorticoid inhibition of interleukin-4 (IL-4) and interleukin-13 (IL-13) induced up-regulation of arginase in rat airway fibroblasts, Naunyn Schmiedebergs Arch Pharmacol, 368, 546, 10.1007/s00210-003-0839-8 Takemoto, 2007, Transiently, paralleled upregulation of arginase and nitric oxide synthase and the ef-fect of both enzymes on the pathology of asthma, Am J Physiol Lung Cell Mol Physiol, 293, L1419, 10.1152/ajplung.00418.2006 Reczkowski, 1994, Rat liver arginase: kinetic mechanism, alternate substrates, and inhibitors, Arch Biochem Biophys, 312, 31, 10.1006/abbi.1994.1276 Shen, 2005, Accessibility of endothelial and inducible nitric oxide synthase to the intracellular citrulline–arginine regeneration pathway, Biochem Pharmacol, 69, 97, 10.1016/j.bcp.2004.09.003 Topal, 2006, Mitochondrial arginase II modulates nitric-oxide synthesis through nonfreely exchangeable L-arginine pools in human endothelial cells, J Pharmacol Exp Ther, 318, 1368, 10.1124/jpet.106.103747 Closs, 2000, Sub-strate supply for nitric oxide synthase in macrophages and endothelial cells: role of cationic amino acid trans-porters, Mol Pharmacol, 57, 68 Jiang, 2011, Modeling gas phase nitric ox-ide release in lung epithelial cells, Nitric Oxide, 10.1016/j.niox.2011.04.010 McDonald, 1997, A caveolar complex between the cationic amino acid transporter 1 and endothelial nitric-oxide synthase may explain the arginine paradox, J Biol Chem, 272, 31213, 10.1074/jbc.272.50.31213 Greene, 1993, Characterization of L-arginine transport by pulmonary artery endothelial cells, Am J Physiol, 264, L351 de Boer, 1996, Deficiency of nitric oxide in allergen-induced airway hyperreactivity to contractile agonists after the early asthmatic reaction: an ex vivo study, Br J Pharmacol, 119, 1109, 10.1111/j.1476-5381.1996.tb16011.x Ricciardolo, 1997, Impairment of bronchoprotection by nitric oxide in severe asthma, Lancet, 350, 1297, 10.1016/S0140-6736(05)62474-9 de Boer, 1999, Role of L-arginine in the defi-ciency of nitric oxide and airway hyperreactivity after the allergen-induced early asthmatic reaction in guinea-pigs, Br J Pharmacol, 128, 1114, 10.1038/sj.bjp.0702882 Meurs, 2000, Modulation of cholinergic air-way reactivity and nitric oxide production by endog-enous arginase activity, Br J Pharmacol, 130, 1793, 10.1038/sj.bjp.0703488 Maarsingh, 2005, Argin-ase attenuates inhibitory nonadrenergic noncholinergic nerve-induced nitric oxide generation and airway smooth muscle relaxation, Respir Res, 6, 23, 10.1186/1465-9921-6-23 Maarsingh, 2006, Arginase strongly impairs neuronal nitric oxide-mediat-ed airway smooth muscle relaxation in allergic asthma, Respir Res, 7, 6, 10.1186/1465-9921-7-6 Maarsingh, 2006, Role of the L-citrulline/L-arginine cycle in iNANC nerve-me-diated nitric oxide production and airway smooth muscle relaxation in allergic asthma, Eur J Pharmacol, 546, 171, 10.1016/j.ejphar.2006.07.041 Hrabák, 1992, Inverse relation in the de novo arginase synthesis and nitric oxide production in murine and rat peritoneal macrophages in long-term cultures in vitro, Comp Biochem Physiol B, 103, 839, 10.1016/0305-0491(92)90202-3 Gotoh, 1999, Arginase II downregulates nitric oxide (NO) production and prevents NO-mediated apoptosis in murine macrophage-derived RAW 264.7 cells, J Cell Biol, 144, 427, 10.1083/jcb.144.3.427 Chicoine, 2004, Argin-ase inhibition increases nitric oxide production in bovine pulmonary arterial endothelial cells, Am J Physiol Lung Cell Mol Physiol, 287, L60, 10.1152/ajplung.00194.2003 Alcorn, 2010, Strain-dependent activation of NF-kappaB in the airway epithelium and its role in aller-gic airway inflammation, Am J Physiol Lung Cell Mol Physiol, 298, L57, 10.1152/ajplung.00037.2009 Maarsingh, 2008, Arginase and pulmo-nary diseases, Naunyn Schmiedebergs Arch Pharmacol, 378, 171, 10.1007/s00210-008-0286-7 Morris, 2009, Asthma management: reinventing the wheel in sickle cell disease, Am J Hematol, 84, 234, 10.1002/ajh.21359 Morris, 2009, Recent advances in arginine metabolism: Roles and regulation of the arginases, Br J Pharmacol, 157, 922, 10.1111/j.1476-5381.2009.00278.x Cama, 2003, Design of Amino Acid Sulfonamides as Transition-State Analogue Inhibi-tors of Arginase, J Am Chem Soc, 125, 13052, 10.1021/ja036365b Ilies, 2010, 2-Aminoimidazole Amino Acids as Inhibitors of the Binuclear Manganese Metalloenzyme Human Ar-ginase I, J Med Chem, 53, 4266, 10.1021/jm100306a Colleluori, 2001, Classical and Slow-Binding Inhibitors of Human Type II Arginase, Biochemistry, 40, 9356, 10.1021/bi010783g Kim, 2001, Probing erectile function: S-(2-boronoethyl)-l-cysteine binds to arginase as a transition state analogue and enhances smooth muscle relaxation in human penile corpus cavernosum, Biochemistry, 40, 2678, 10.1021/bi002317h Maarsingh, 2008, Arginase inhibition protects against allergen-induced airway obstruction, hyperre-sponsiveness, and inflammation, Am J Respir Crit Care Med, 178, 565, 10.1164/rccm.200710-1588OC North, 2009, Functionally important role for arginase 1 in the air-way hyperresponsiveness of asthma, Am J Physiol Lung Cell Mol Physiol, 296, L911, 10.1152/ajplung.00025.2009 Maarsingh, 2011, Increased arginase activity con-tributes to airway remodelling in chronic allergic asthma, Eur Respir J, 10.1183/09031936.00057710 Trujillo-Ferrara, 1992, Antitumor effect and toxicity of two new active-site-directed irreversible ornithine decarboxylase and extrahepatic arginase inhibitors, Cancer Letters, 67, 193, 10.1016/0304-3835(92)90143-J Mayorek, 2010, Diclofenac inhibits tumor growth in a murine model of pancreatic cancer by modulation of VEGF levels and arginase ac-tivity, PLoS One, 5, e12715, 10.1371/journal.pone.0012715 Zeki, 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, 10.1016/j.trsl.2010.09.003 Yang, 2006, Inhibition of argi-nase I activity by RNA interference attenuates IL-13-induced airways hyperresponsiveness, J Immunol, 177, 5595, 10.4049/jimmunol.177.8.5595 Ckless, 2008, Inhibition of arginase activity enhances inflammation in mice with allergic airway disease, in association with increases in protein S-nitrosylation and tyrosine nitration, J Immunol, 181, 4255, 10.4049/jimmunol.181.6.4255 Mabalirajan, 2010, Beneficial effects of high dose of L-arginine on airway hyperresponsiveness and airway inflammation in a murine model of asthma, J Allergy Clin Immunol, 125, 626, 10.1016/j.jaci.2009.10.065 Bratt, 2010, Nitric oxide synthase enzymes in the airways of mice exposed to ovalbumin: NOS2 ex-pression is NOS3 dependent, Mediators Inflamm, 10.1155/2010/321061 Ten Broeke, 2006, Overexpression of endothelial nitric oxide synthase suppresses features of allergic asthma in mice, Respir Res, 5, 58, 10.1186/1465-9921-7-58 Kobayashi, 2006, The effect of overexpression of endothe-lial nitric oxide synthase on eosinophilic lung inflam-mation in a murine model, Int Immunopharmacol, 6, 1040, 10.1016/j.intimp.2005.09.016 Kenyon, 2011, L-Arginine Supplementation and Me-tabolism in Asthma, Pharmaceuticals, 4, 187, 10.3390/ph4010187 Huk, 1997, L-arginine treatment alters the ki-netics of nitric oxide and superoxide release and reduces ischemia/reperfusion injury in skeletal muscle, Circulation, 96, 667, 10.1161/01.CIR.96.2.667 Jeyabalan, 2008, Arginase blockade protects against he-patic damage in warm ischemia-reperfusion, Nitric Oxide, 19, 29, 10.1016/j.niox.2008.04.002 Reid, 2007, Liver I/R injury is improved by the argi-nase inhibitor, N(omega)-hydroxy-nor-L-arginine (nor-NOHA), Am J Physiol Gastrointest Liver Physiol, 292, G512, 10.1152/ajpgi.00227.2006 Engelman, 1995, L-arginine reduces en-dothelial inflammation and myocardial stunning during ischemia/reperfusion, Ann Thorac Surg, 60, 1275, 10.1016/0003-4975(95)00614-Q Kim, 2009, Arginase inhibition restores NOS cou-pling and reverses endothelial dysfunction and vascular stiffness in old rats, J Appl Physiol, 107, 1249, 10.1152/japplphysiol.91393.2008 Bagnost, 2008, Treatment with the arginase inhibitor N(omega)-hydroxy-nor-L-arginine improves vascular function and lowers blood pressure in adult spontaneously hypertensive rat, J Hypertens, 26, 1110, 10.1097/HJH.0b013e3282fcc357 Berkowitz, 2003, Arginase reciprocally regulates nitric oxide synthase activity and contributes to endothelial dysfunction in aging blood vessels, Circulation, 108, 2000, 10.1161/01.CIR.0000092948.04444.C7 Iniesta, 2001, The inhibition of arginase by N-(omega)-hydroxy-L-arginine controls the growth of Leishmania inside macrophages, J Exp Med, 193, 777, 10.1084/jem.193.6.777 Iniesta, 2002, Arginase I induction in mac-rophages, triggered by Th2-type cytokines, supports the growth of intracellular Leishmania parasites, Parasite Immunol, 24, 113, 10.1046/j.1365-3024.2002.00444.x Bivalacqua, 2007, Overexpression of arginase in the aged mouse penis impairs erectile function and decreases eNOS activity: influence of in vivo gene therapy of anti-arginase, Am J Physiol Heart Circ Physiol, 292, H1340, 10.1152/ajpheart.00121.2005 Lim, 2007, Mitochondrial arginase II constrains endothelial NOS-3 activity, Am J Physiol Heart Circ Physiol, 293, H3317, 10.1152/ajpheart.00700.2007