Arginase strongly impairs neuronal nitric oxide-mediated airway smooth muscle relaxation in allergic asthma

Respiratory Research

Volumn 7, Issue , 2006, Pages

  Maarsingh, Harm ^a   Leusink, John ^a   Bos, I Sophie T ^a   Zaagsma, Johan ^a   Meurs, Herman ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; ARGINASE; ARGININE; ATROPINE; HISTAMINE; INDOMETACIN; N(G) HYDROXYARGININE; N(G) NITROARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; OVALBUMIN;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREATHING MUSCLE; CONTROLLED STUDY; ELECTRIC FIELD; ELECTROSTIMULATION; ENZYME ACTIVITY; ENZYME SUBSTRATE; MALE; NERVE; NONHUMAN; PROVOCATION TEST; SMOOTH MUSCLE RELAXATION; STATISTICAL SIGNIFICANCE; TRACHEA; ANIMAL; ASTHMA; BRONCHOCONSTRICTION; DRUG EFFECTS; ENZYMOLOGY; GERMFREE ANIMAL; GUINEA PIG; HYPERSENSITIVITY; IN VITRO STUDY; INNERVATION; METABOLISM; MUSCLE RELAXATION; PATHOPHYSIOLOGY; PHYSIOLOGY; SMOOTH MUSCLE;

ANIMALS; ARGINASE; ARGININE; ASTHMA; BRONCHOCONSTRICTION; ELECTRIC STIMULATION; GUINEA PIGS; HYPERSENSITIVITY; IN VITRO TECHNIQUES; MALE; MUSCLE RELAXATION; MUSCLE, SMOOTH; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; OVALBUMIN; SPECIFIC PATHOGEN-FREE ORGANISMS; TRACHEA;

EID: 32844458380     PISSN: 1465993X     EISSN: None     Source Type: Journal    
DOI: 10.1186/1465-9921-7-6     Document Type: Article

References (47)

1. Moncada S, Palmer RM, Higgs EA: Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. Biochem Pharmacol 1989, 38:1709-1715.
2. Ricciardolo FL: Multiple roles of nitric oxide in the airways. Thorax 2003, 58:175-182.
3. De Boer J, Meurs H, Coers W, Koopal M, Bottone AE, Visser AC, Timens W, Zaagsma J: 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.
4. Ricciardolo FL, Di Maria GU, Mistretta A, Sapienza MA, Geppetti P: Impairment of bronchoprotection by nitric oxide in severe asthma. Lancet 1997, 350:1297-1298.
5. Mehta S, Drazen JM, Lilly CM: Endogenous nitric oxide and allergic bronchial hyperresponsiveness in guinea pigs. Am J Physiol 1997, 273:L656-L662.
6. Schuiling M, Zuidhof AB, Bonouvrie MA, Venema N, Zaagsma J, Meurs H: 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.
7. Schuiling M, Meurs H, Zuidhof AB, Venema N, Zaagsma J: Dual action of iNOS-derived nitric oxide in allergen-induced airway hyperreactivity in conscious, unrestrained guinea pigs. Am J Respir Crit Care Med 1998, 158:1442-1449.
8. Ricciardolo FL, Timmers MC, Geppetti P, van SA, Brahim JJ, Sont JK, de Gouw HW, Hiemstra PS, van Krieken JH, Sterk PJ: Allergen-induced impairment of bronchoprotective nitric oxide synthesis in asthma. J Allergy Clin Immunol 2001, 108:198-204.
9. Samb A, Pretolani M, Dinh-Xuan AT, Ouksel H, Callebert J, Lisdero C, Aubier M, Boczkowski J: 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.
10. 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.
11. De Boer J, Duyvendak M, Schuurman FE, Pouw FM, Zaagsma J, Meurs H: 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.
12. Que LG, Kantrow SP, Jenkinson CP, Piantadosi CA, Huang YC: Induction of arginase isoforms in the lung during hyperoxia. Am J Physiol 1998, 275:L96-102.
13. Meurs H, Hamer MA, Pethe S, Vadon-Le GS, Boucher JL, Zaagsma J: Modulation of cholinergic airway reactivity and nitric oxide production by endogenous arginase activity. Br J Pharmacol 2000, 130:1793-1798.
14. Meurs H, McKay S, Maarsingh H, Hamer MA, Macic L, Molendijk N, Zaagsma J: Increased arginase activity underlies allergen-induced deficiency of cNOS-derived nitric oxide and airway hyperresponsiveness. Br J Pharmacol 2002, 136:391-398.
15. 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 2003, 111:1863-1874.
16. Morris CR, Poljakovic M, Lavrisha L, Machado L, Kuypers FA, Morris SMJ: Decreased arginine bioavailability and increased serum arginase activity in asthma. Am J Respir Crit Care Med 2004, 170:148-153.
17. Miura M, Yamauchi H, Ichinose M, Ohuchi Y, Kageyama N, Tomaki M, Endoh N, Shirato K: 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.
18. Tucker JF, Brave SR, Charalambous L, Hobbs AJ, Gibson A: L-NG-nitro arginine inhibits non-adrenergic, non-cholinergic relaxations of guinea-pig isolated tracheal smooth muscle. Br J Pharmacol 1990, 100:663-664.
19. Belvisi MG, Stretton D, Barnes PJ: Nitric oxide as an endogenous modulator of cholinergic neurotransmission in guinea-pig airways. Eur J Pharmacol 1991, 198:219-221.
20. Li CG, Rand MJ: Evidence that part of the NANC relaxant response of guinea-pig trachea to electrical field stimulation is mediated by nitric oxide. Br J Pharmacol 1991, 102:91-94.
21. 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.
22. Ellis JL, Undem BJ: Inhibition by L-NG-nitro-L-arginine of nonadrenergic-noncholinergic-mediated relaxations of human isolated central and peripheral airway. Am Rev Respir Dis 1992, 146:1543-1547.
23. 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, 6:23.
24. Van Amsterdam RG, Brouwer F, Zaagsma J: Analysis of the beta-adrenoceptor mediated inhibition of IgG1 and IgE dependent guinea-pig anaphylactic tracheal smooth muscle contraction. Agents Actions 1989, 26:48-51.
25. Santing RE, Meurs H, van der Mark TW, Remie R, Oosterom WC, Brouwer F, Zaagsma J: A novel method to assess airway function parameters in chronically instrumented, unrestrained guinea-pigs. Pulm Pharmacol 1992, 5:265-272.
26. Santing RE, Olymulder CG, Zaagsma J, Meurs H: Relationships among allergen-induced early and late phase airway obstructions, bronchial hyperreactivity, and inflammation in conscious, unrestrained guinea pigs. J Allergy Clin Immunol 1994, 93:1021-1030.
27. Ellis JL, Farmer SG: Effects of peptidases on non-adrenergic, non-cholinergic inhibitory responses of tracheal smooth muscle: a comparison with effects on VIP- and PHI-induced relaxation. Br J Pharmacol 1989, 96:521-526.
28. Ellis JL, Farmer SG: The effects of vasoactive intestinal peptide (VIP) antagonists, and VIP and peptide histidine isoleucine antisera on non-adrenergic, non-cholinergic relaxations of tracheal smooth muscle. Br J Pharmacol 1989, 96:513-520.
29. Wu G, Morris SMJ: Arginine metabolism: nitric oxide and beyond. Biochem J 1998, 336 ( Pt 1):1-17.
30. Hey C, Boucher JL, Vadon-Le GS, Ketterer G, Wessler I, Racke K: Inhibition of arginase in rat and rabbit alveolar macrophages by N omega-hydroxy-D,L-indospicine, effects on L-arginine utilization by nitric oxide synthase. Br J Pharmacol 1997, 121:395-400.
31. Boucher JL, Moali C, Tenu JP: Nitric oxide biosynthesis, nitric oxide synthase inhibitors and arginase competition for L-arginine utilization. Cell Mol Life Sci 1999, 55:1015-1028.
32. 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, 368:546-550.
33. Sandler NG, Mentink-Kane MM, Cheever AW, Wynn TA: Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. J Immunol 2003, 171:3655-3667.
34. 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.
35. Eynott PR, Groneberg DA, Caramori G, Adcock IM, Donnelly LE, Kharitonov S, Barnes PJ, Chung KF: Role of nitric oxide in allergic inflammation and bronchial hyperresponsiveness. Eur J Pharmacol 2002, 452:123-133.
36. Eynott PR, Paavolainen N, Groneberg DA, Noble A, Salmon M, Nath P, Leung SY, Chung KF: Role of nitric oxide in chronic allergen-induced airway cell proliferation and inflammation. J Pharmacol Exp Ther 2003, 304:22-29.
37. Hammermann R, Hirschmann J, Hey C, Mossner J, Folkerts G, Nijkamp FP, Wessler I, Racke K: 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.
38. Meurs H, Schuurman FE, Duyvendak M, Zaagsma J: Deficiency of nitric oxide in polycation-induced airway hyperreactivity. Br J Pharmacol 1999, 126:559-562.
39. Maarsingh H, de BJ, Kauffman HF, Zaagsma J, Meurs H: Heparin normalizes allergen-induced nitric oxide deficiency and airway hyperresponsiveness. Br J Pharmacol 2004, 142:1293-1299.
40. Ellis JL, Conanan ND: Modulation of relaxant responses evoked by a nitric oxide donor and by nonadrenergic, noncholinergic stimulation by isozyme-selective phosphodiesterase inhibitors in guinea pig trachea. J Pharmacol Exp Ther 1995, 272:997-1004.
41. Tanihata S, Uchiyama T: Role of nitric oxide in nonadrenergic, noncholinergic relaxation of whole tracheal tube preparations isolated from guinea pigs. Gen Pharmacol 1996, 27:827-832.
42. de Haas JR, Terpstra JS, van der ZM, Kockelbergh PG, Roffel AF, Zaagsma J: Facilitatory beta2-adrenoceptors on cholinergic and adrenergic nerve endings of the guinea pig trachea. Am J Physiol 1999, 276:L420-L425.
43. Mhanna MJ, Ferkol T, Martin RJ, Dreshaj IA, van Heeckeren AM, Kelley TJ, Haxhiu MA: Nitric oxide deficiency contributes to impairment of airway relaxation in cystic fibrosis mice. Am J Respir Cell Mol Biol 2001, 24:621-626.
44. Grasemann H, Schwiertz R, Matthiesen S, Racke K, Ratjen F: Increased Arginase Activity in Cystic Fibrosis Airways. Am J Respir Crit Care Med 2005, 170:1523-1528.
45. Cox JD, Kim NN, Traish AM, Christianson DW: Arginase-boronic acid complex highlights a physiological role in erectile function. Nat Struct Biol 1999, 6:1043-1047.
46. 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 2001, 283:923-927.
47. Baggio R, Emig FA, Christianson DW, Ash DE, Chakder S, Rattan S: Biochemical and functional profile of a newly developed potent and isozyme-selective arginase inhibitor. J Pharmacol Exp Ther 1999, 290:1409-1416.