The therapeutic potential of drugs targeting the arginase pathway in asthma

Expert Opinion on Investigational Drugs

Volumn 14, Issue 10, 2005, Pages 1221-1231

  Ricciardolo, Fabio L M ^a   Zaagsma, Johan ^b   Meurs, Herman ^b  

^a G GASLINI INSTITUTE   (Italy)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Airway hyper responsiveness; Airways; Arginase; Arginase inhibitors; Asthma; Nitric oxide synthase

Indexed keywords

2 AMINO 6 BORONOHEXANOIC ACID; ANTIASTHMATIC AGENT; ARGINASE; ARGINASE INHIBITOR; BORONIC ACID DERIVATIVE; COLLAGEN; CYTOKINE; GLUCOCORTICOID; GUANIDINE DERIVATIVE; INDUCIBLE NITRIC OXIDE SYNTHASE; N HYDROXYGUANIDINIUM DERIVATIVE; N(G) HYDROXYARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; ORNITHINE; PEROXYNITRITE; POLYAMINE; PROLINE; REACTIVE NITROGEN SPECIES; S (2 BORONOETHYL) LEVO CYSTEINE; UNCLASSIFIED DRUG;

ACUTE DISEASE; ALLERGIC ASTHMA; AMINO ACID METABOLISM; ASTHMA; BRONCHODILATATION; BRONCHUS HYPERREACTIVITY; BRONCHUS REACTIVITY; CELL DAMAGE; CELL PROLIFERATION; COLLAGEN SYNTHESIS; COMPETITION; DRUG TARGETING; ENZYME SUBSTRATE; FIBROBLAST CULTURE; HUMAN; NONHUMAN; RESPIRATORY TRACT INFLAMMATION; REVIEW; SMOOTH MUSCLE CONTRACTILITY; TH2 CELL; UPREGULATION;

ANIMALS; ARGINASE; ASTHMA; DRUG DELIVERY SYSTEMS; HUMANS; SIGNAL TRANSDUCTION;

EID: 27144545487     PISSN: 13543784     EISSN: None     Source Type: Journal    
DOI: 10.1517/13543784.14.10.1221     Document Type: Review

References (86)

1. CLOSS EI, SIMON A, VEKONY N, ROTMANN A: Plasma membrane transporters for arginine. J. Nutr. (2004) 134:2752S-2759S.
2. DURANTE W: Regulation of L-arginine transport and metabolism in vascular smooth muscle cells. Cell Biochem. Biophys. (2001) 35:19-34.
3. DE GEORGE GL, HECK DE, LASKIN JD: Arginine metabolism in keratinocytes and macrophages during nitric oxide biosynthesis: multiple modes of action of nitric oxide synthase inhibitors. Biochem. Pharmacol (1997) 54:103-112.
4. WU G, MORRIS SM Jr: Arginine metabolism: nitric oxide and beyond. Biochem. J. (1998) 336:1-17.
5. RICCIARDOLO FLM, STERK PJ, GASTON B, FOLKERTS G: Nitric oxide in health and disease of the respiratory system. Physiol. Rev. (2004) 84:731-765.
6. MORRIS SM, BILLIAR TR: New insights into the regulation of inducible nitric oxide synthesis. Am. J. Physiol. Endocrinol Metab. (1994) 266:E829-E839.
7. SHAUL P, NORTH AJ, WU LC et al.: Endothelial nitric oxide synthase is expressed in cultured human bronchiolar epithelium. J. Clin. Invest. (1994) 94:2231-2236.
8. PECHKOVSKY DV, ZISSEL G, GOLDMANN T et al.: Pattern of NOS2 and NOS3 mRNA expression in human A549 cells and primary cultured AEC II. Am. J. Physiol. Lung Cell Mol. Physiol. (2002) 282:L684-L692.
9. BELVISI MG, STRETTON CD, YACOUB M, BARNES PJ: Nitric oxide is the endogenous neurotransmitter of bronchodilator nerves in humans. Eur. J. Pharmacol. (1992) 210:221-222.
10. HADDAD EB, LIU SF, SALMON M, ROBICHAUD A, BARNES PJ, CHUNG KF: Expression of inducible nitric oxide synthase mRNA in Brown Norway rats exposed to ozone: effect of dexamethasone. Eur. J. Pharmacol. (1995) 293:287-290.
11. RICCIARDOLO FLM: cNOS-iNOS paradigm and arginase in asthma. Trends Pharmacol. Sci. (2003) 24:560-561.
12. KAWAI N, BLOCH DB, FILIPPOV G et al.: Costitutive endothelial nitric oxide synthase gene expression is regulated during lung development. Am. J. Physiol. Lung Cell Mol. Physiol. (1995) 268:L589-L595.
13. GASTON B, DRAZEN JM, JANSEN A et al.: Relaxation of human bronchial smooth muscle by S-nitrosothiols in vitro. J. Pharmacol. Exp. Ther. (1994) 268:978-984.
14. NIJKAMP FP, VAN DER LINDE HJ, FOLKERTS G: Nitric oxide synthesis inhibitors induce airway hyperresponsiveness in the guinea pig in vivo and in vitro. Am. Rev. Respir. Dis. (1993) 148: 727-734.
15. RICCIARDOLO FLM, NADEL JA, YOSHIHARA S, GEPPETTI P: Evidence for reduction of bradykinin-induccd bronchoconstriction in guinea pigs by release of nitric oxide. Br. J. Pharmacol. (1994) 113:1147-1152.
16. RICCIARDOLO FLM, GEPPETTI P, MISTRETTA A et al.: Randomized double-blind placebo-controllcd study of the effect of inhibition of nitric oxide synthesis in bradykinin-induced asthma. Lancet (1996) 348:374-377.
17. RICCIARDOLO FLM, DI MARIA GU, MISTRETTA A, SAPIENZA MA, GEPPETTI P: Impairment of bronchoprotection by nitric oxide in severe asthma. Lancet (1997) 350:1297-1298.
18. MOYA MP, GOW AJ, CALIFF RM, GOLDBERG RN, STAMLER JS: Inhaled ethyl nitrite gas for persistent pulmonary hypertension of the newborn. Lancet (2002) 360:2076-2077.
19. NAGAKI M, SHIMURA MN, IROKAWA T, SASAKI T, SHIRATO K: Nitric oxide regulation of glycoconjugate secretion from feline and human airways in vitro. Respir. Physiol. (1995) 102:89-95.
20. LOUKIDES S, KHARITONOV SA, WODEHOUSE T, COLE PJ, BARNES PJ: Effect of L-arginine on mucociliary function in primary ciliary diskinesia. Lancet (1998) 352:371-372.
21. MORRIS SM Jr: Regulation of enzymes of the urea cycle and arginine metabolism. Ann. Rev. Nutr. (2002) 22:87-105.
22. SAID SI, DEY RD, DICKMAN K: Glutamate signalling in the lung. Trends Pharmacol. Sci. (2001) 22:344-345.
23. DURANTE W, LIAO L, REYNA SV, PEYTON KJ, SCHAFER AI: Transforming growth factor-beta(1) stimulates L-arginine transport and metabolism in vascular smooth muscle cells: role in polyamine and collagen synthesis. Circulation (2001) 103:1121-1127.
24. JANNE J, ALHONEN L, LEINONEN P: Polyamines: from molecular biology to clinical applications. Ann. Med. (1991) 23:241-259.
25. GILETTE JH, MITCHELL JL: Ornithine decarboxylase: a biochemical marker of repair in damaged tissue. Life Sci. (1991) 48:1501-1510.
26. MORI M, GOTOH T: Regulation of nitric oxide production by arginine metabolic enzymes. Biochem. Biophys. Res. Commun. (2000) 275:715-719.
27. PAULEAU AL, RUTSCHMAN R, LANG R, PERNIS A, WATOWICH SS, MURRAY PJ: Enhancer-mediated control of macrophage-specific arginase I expression. J. Immunol. (2004) 172:7565-7573.
28. ALBINA JE, MAHONEY EJ, DALEY JM, WESCHE DE, MORRIS SM Jr, REICHNER JS: Macrophage arginase regulation by CCAAT/enhancer-binding protein beta. Shock (2005) 23:168-172.
29. MORRIS SM Jr: Recent advances in arginine metabolism. Curr. Opin. Clin. Nutr. Metab. Care (2004) 7:45-51.
30. ZIMMERMANN N, KING NE, LAPORTE J et al.: Dissection of experimental asthma with DNA microarray analysis identifies arginase in asthma pathogenesis. J. Clin. Invest. (2003) 111:1863-1874.
31. QUE LG, KANTROW SP, JENKINSON CP, PIANTADOSI CA, HUANG Y-C: Induction of arginase isoforms in the lung during hyperoxia. Am. J. Physiol. Lung Cell Mol. Physiol. (1998) 275:L96-L102.
32. MEURS H, McKAY S, MAARSINGH H et al.: Increased arginase activity underlies allergen-induced deficiency of cNOS-derived nitric oxide and airway hyperresponsiveness. Br. J. Pharmacol. (2002) 136:391-398.
33. ENDO M, OYADOMARI S, TERASAKI Y et al.: Induction of arginase I and II in bleomycin-induced fibrosis of mouse lung. Am. J. Physiol. Lung Cell. Mol. Physiol. (2003) 285:L313-L321.
34. XU W, KANEKO FT, ZHENG S et al.: Increased arginase II and decreased NO synthesis in endothelial cells of patients with pulmonary arterial hypertension. FASEB J. (2004) 18:1746-1748.
35. GRASEMANN H, SCHWIRTZ R, RACKE K, RATJEN F: Arginase activity in sputum of patients with cystic fibrosis. Pediatr. Pulmonol. (2004) 27:241 (Supplement).
36. BOUSQUET J, JEFFERY PK, BUSSE WW, JOHNSON M, VIGNOLA AM: Asthma. From bronchoconstriction to airways inflammation and remodeling. Am. J. Respir. Crit. Care Med. (2000) 161:1720-1745.
37. SALEH D, ERNST P, LIM S, BARNES PJ, GIAID A: Increased formation of the potent oxidant peroxynitrite in the airways of asthmatic patients is associated with induction of nitric oxide synthase: effect of inhaled glucocorticoid. FASEB J. (1998) 12:929-937.
38. MEURS H, MAARSINGH H, ZAAGSMA J: Arginase and asthma: novel insights into nitric oxide homeostasis and airway hyperresponsiveness. Trends Pharmacol. Sci. (2003) 24:450-455.
39. DE BOER J, MEURS H, COERS W et al.: Deficiency of nitric oxide in allergen-induced airway hyperreactivity to contractile agonists after the early asthmatic reaction: an ex vivo study. Br. J. Pharmacol. (1996) 119:1109-1116.
40. TAYLOR DA, McGRATH JL, ORR LM, BARNES PJ, O'CONNOR BJ: Effect of endogenous nitric oxide inhibition on airway responsiveness to histamine and adenosine-5′-monophosphate in asthma. Thorax (1998) 53:483-489.
41. RICCIARDOLO FL, TREVISANI M, GEPPETTI P et al.: Role of nitric oxide and septide-insensitive NK(1) receptors in bronchoconstriction induced by aerosolised neurokinin A in guinea-pigs. Br. J. Pharmacol. (2000) 129:915-920.
42. PERSSON MG, GUSTAFSSON LE: Allergen-induced airway obstruction in guinea-pigs is associated with changes in nitric oxide levels in exhaled air. Acta Physiol. Scand. (1993) 149:461-466.
43. RICCIARDOLO FL, TIMMERS MC, SONT JK, FOLKERTS G, STERK PJ: Effect of bradykinin on allergen induced increase in exhaled nitric oxide in asthma. Thorax (2003) 58:840-845.
44. SCHUILING M, ZUIDHOF AB, BONOUVRIE MA et al.: Role of nitric oxide in the development and partial reversal of allergen-induced airway hyperreactivity in conscious, unrestrained guinea-pigs. Br. J. Pharmacol. (1998) 123:1450-1456.
45. YAN ZQ, HANSSON GK, SKOOGH BE, LOTVALL JO: Induction of nitric oxide synthase in a model of allergic occupational asthma. Allergy (1995) 50:760-764.
46. MEHTA S, DRAZEN JM, LILLY CM: Endogenous nitric oxide and allergic bronchial hyperresponsiveness in guinea pigs. Am. J. Physiol. (1997) 273:L656-L662.
47. MAARSINGH H, LEUSINK J, ZAAGSMA J, MEURS H: Role of arginase in allergen-induced iNANC nerve activity. Eur. Respir. J. (2004) 24 (Suppl. 48):681s.
48. MIURA M, YAMAUCHI H, ICHINOSE M et al.: Impairment of neural nitric oxide-mediated relaxation after antigen exposure in guinea pig airways in vitro. Am. J. Respir. Crit. Care Med. (1997) 156:217-222.
49. RICCIARDOLO FL, TIMMERS MC, GEPPETTI P et al.: Allergen-induced ampairment of bronchoprotective nitric oxide synthesis in asthma. J. Allergy Clin. Immunol. (2001) 108:198-204.
50. COLASANTI M, SUZUKI H: The dual personality of NO. Trends Pharmacol. Sci. (2000) 21:249-252.
51. THOMASSEN MJ, BUHROW IT, CONNORS MJ et al.: Nitric oxide inhibits inflammatory cytokine production by human alveolar macrophages. Am. J. Respir. Cell Mol. Biol. (1997) 17:279-283.
52. SAMB A, PRETOLANI M, DINH-XUAN AT et al.: Decreased pulmonary and tracheal smooth muscle expression and activity of type 1 nitric oxide synthase (nNOS) after ovalbumin immunization and multiple aerosol challenge in guinea pigs. Am. J. Respir. Crit. Care Med. (2001) 164:149-154.
53. BANDYOPADHYAY A, CHAKDER S, RATTAN S: Regulation of inducible and neuronal nitric oxide synthase gene expression by interferon-γ and VIP. Am. J. Physiol. (1997) 272:C1790-C1797.
54. DE BOER J, POUW FM, ZAAGSMA J, MEURS H: Effects of endogenous superoxide anion and nitric oxide on cholinergic constriction of normal and hyperreactive guinea pig airways. Am. J. Respir. Crit. Care Med. (1998) 158:1784-1789.
55. DE BOER J, DUYVENDAK M, SCHUURMAN FE et al.: Role of L-arginine in the deficiency of nitric oxide and airway hyperreactivity after the allergen-induced early asthmatic reaction in guinea-pigs. Br. J. Pharmacol. (1999) 128:1114-1120.
56. FOLKERTS G, VAN DER LINDE HJ, NIJKAMP FP: Virus-induccd airway hyperresponsiveness in guinea pigs is related to a deficiency in nitric oxide. J. Clin. Invest. (1995) 95:26-30.
57. HAMMERMANN R, HIRSCHMANN J, HEY C et al.: Cationic proteins inhibit L-arginine uptake in rat alveolar macrophages and tracheal epithelial cells. Implications for nitric oxide synthesis. Am. J. Respir. Cell Mol. Biol. (1999) 21:155-162.
58. MEURS H, SCHUURMAN FE, DUYVENDAK M, ZAAGSMA J: Deficiency of nitric oxide in polycation-induced airway hyperreactivity. Br. J. Pharmacol. (1999) 126:559-562.
59. MAARSINGH H, DE BOER J, KAUFFMAN HF, ZAAGSMA J, MEURS H: Heparin normalizes allergen-induced nitric oxide deficiency and airway hyperresponsiveness. Br. J. Pharmacol. (2004) 142:1293-1299.
60. MEURS H, HAMER MAM, PETHE S, VADON-LE GOFF S, BOUCHER J-L, ZAAGSMA J: Modulation of cholinergic airway reactivity and nitric oxide production by enogenous arginase activity. Br. J. Pharmacol. (2000) 130:1793-1798.
61. MAARSINGH H, TIO MA, ZAAGSMA J, MEURS H: Arginase attenuates inhibitory nonadrenergic noncholinergic nerve-induced nitric oxide generation and airway smooth muscle relaxation. Respir. Res. (2005) 6(1):23.
62. LINDEMANN D, RACKE K. 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. (2003) 368(6):546-550.
63. KLASEN S, HAMMERMANN R, FUHRMANN M et al.: Glucocorticoids inhibit lipopolysaccharide-induced up-regulation of arginase in rat alveolar macrophages. Br. J. Pharmacol. (2001) 132:1349-1357.
64. BLACK PN, BRODIE SM: Nitric oxide and response to inhaled bradykinin in severe asthma. Lancet (1998) 351:449-450.
65. SADEGHI-HASHJIN G, FOLKERTS G, HENRICKS PA, MUIJSERS RB, NIJKAMP FP: Peroxynitrite in airway diseases. Clin. Exp. Allergy (1998) 28:1464-1473.
66. DE BOER J, MEURS H, FLENDRIG L, KOOPAL M, ZAAGSMA J: Role of nitric oxide and superoxide in allergen-induced airway hyperreactivity after the late asthmatic reaction in guinea-pigs. Br. J. Pharmacol. (2001) 133:1235-1242.
67. MUIJSERS RB, VAN ARK I, FOLKERTS G et al.: Apocynin and 1400W prevents airway hyperresponsiveness during allergic reactions in mice. Br. J. Pharmacol. (2001) 134:434-440.
68. SUGIURA H, ICHINOSE M, OYAKE T et al.: Role of peroxynitrite in airway microvascular hyperpermeabiliry during late allergic phase in guinea pigs. Am. J. Respir. Crit. Care Med. (1999) 160:663-671.
69. XIA Y, ZWEIER JL: Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc. Natl. Acad. Sci. USA (1997) 94:6954-6958.
70. MAARSINGH H, BOSSENGA BE, BOS IS, ZAAGSMA J, MEURS H: L-arginine limitation induced by arginase and polycations causes a relative deficiency of iNOS-derived NO and airway hyperreactivity after the allergen-induced late asthmatic reaction. Am. J. Respir. Crit. Care Med. (2004) 169:A417.
71. COMHAIR SA, BHATHENA PR, DWEIK RA, KAVURU M, ERZURUM SC: Rapid loss of superoxide dismutase activity during antigen-induced asthmatic response. Lancet (2000) 355:624.
72. HOET PH, NEMERY B: Polyamines in the lung: polyamine uptake and polyamine-linked pathological or toxicological conditions. Am. J. Physiol. Lung Cell. Mol. Physiol. (2000) 278:L417-L433.
73. KUROSAWA M, SHIMIZU Y, TSUKAGOSHI H, UEKI M: Elevated levels of peripheral-blood, naturally occurring aliphatic polyamines in bronchial asthmatic patients with active symptoms. Allergy (1992) 47:638-643.
74. H2 responses in tissue repair. J. Immunol. (2003) 171:3655-3667.
75. MORRIS CR, POLJAKOVIC M, LAVRISHA L et al.: Decreased arginine bioavailability and increased serum arginase activity in asthma. Am. J. Respir. Crit. Care Med. (2004) 170:148-153.
76. KOCHANSKY L, KOSSMAN S, ROGALA E, DWORNICKI J: Arginase activity in sputum of patients with bronchial asthma. Pneum. Pol. (1980) 48:329-332.
77. ω-hydroxy-nor-L-arginine: a high affinity inhibitor of arginase well adapted to bind to its manganese cluster. J. Am. Chem. Soc. (1997) 119:4086-4087.
78. CHRISTIANSON DW: Arginase: structure, mechanism, and physiological role in male and female sexual arousal. Acc. Chem. Res. (2005) 38:191-201.
79. KIM NN, COX JD, BAGGIO RF et al.: 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 (2001) 40:2678-2688.
80. CAMA E, COLLELUORI DM, EMIG FA et al.: Human arginase II: crystal structure and physiological role in male and female sexual arousal. Biochemistry (2003) 42:8445-8451.
81. BOUCHER JL, CUSTOT J, VADON S et al.: N-o-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. (1994) 203:1614-1621.
82. MOALI C, BOUCHER JL, SARI MA, STUEHR DJ, MANSUY D: Substrate specificity of NO synthases: detailed comparison of L-arginine, homo-L-arginine, their N-o-hydroxy derivatives, and N-o-hydroxynor-L-arginine. Biochemistry (1998) 37:10453-10460.
83. XU L, HILLIARD B, CARMODY RJ et al.: Arginase and autoimmune inflammation in the central nervous system. Immunology (2003) 110:141-148.
84. VERCELLI D: Arginase: market, effector, or candidate gene for asthma? J. Clin. Invest. (2003) 111:1815-1817.
85. SAPIENZA MA, KHARITONOV SA, HORVATH I, CHUNG KF, BARNES PJ: Effect of inhaled L-arginine on exhaled nitric oxide in normal and asthmatic subjects. Thorax (1998) 53:172-175.
86. HOGMAN M, FROSTELL CG, HEDENSTROM H, HEDENSTIERNA G: Inhalation of nitric oxide modulates adult human bronchial tone. Am. Rev. Respir. Dis. (1993) 148:1474-1478.