Role of the l-citrulline/l-arginine cycle in iNANC nerve-mediated nitric oxide production and airway smooth muscle relaxation in allergic asthma

European Journal of Pharmacology

Volumn 546, Issue 1-3, 2006, Pages 171-176

  Maarsingh, Harm ^a   Leusink, John ^a   Zaagsma, Johan ^a   Meurs, Herman ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Airway hyperresponsiveness; Airway smooth muscle; Allergic asthma; Arginine; Argininosuccinate lyase; Argininosuccinate synthase; Citrulline; Guinea pig; Inhibitory nonadrenergic noncholinergic nerve; Nitric oxide synthase

Indexed keywords

2 METHYLASPARTIC ACID; ALLERGEN; ARGININE; ARGININOSUCCINATE LYASE; ARGININOSUCCINATE SYNTHASE; CITRULLINE; N(G) NITROARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; SUCCINIC ACID; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; DRUG INHIBITION; ELECTROSTIMULATION; GUINEA PIG; INHIBITORY NONADRENERGIC NONCHOLINERGIC NERVE; MALE; NERVE STIMULATION; NONADRENERGIC NONCHOLINERGIC NERVE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE RELAXATION; TRACHEA;

ALLERGENS; ANIMALS; ARGININE; ARGININOSUCCINATE LYASE; ARGININOSUCCINATE SYNTHASE; ASTHMA; CITRULLINE; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ENZYME INHIBITORS; GUINEA PIGS; MALE; MUSCLE RELAXATION; MUSCLE, SMOOTH; N-METHYLASPARTATE; NEURAL INHIBITION; NEURONS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; OVALBUMIN; SPECIFIC PATHOGEN-FREE ORGANISMS; SUCCINIC ACID; TRACHEA;

EID: 33748325836     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2006.07.041     Document Type: Article

References (38)

1. Belvisi M.G., Stretton C.D., Yacoub M., and Barnes P.J. Nitric oxide is the endogenous neurotransmitter of bronchodilator nerves in humans. Eur. J. Pharmacol. 210 (1992) 221-222
2. Chakder S., and Rattan S. L-arginine deficiency causes suppression of nonadrenergic noncholinergic nerve-mediated smooth muscle relaxation: role of l-citrulline recycling. J. Pharmacol. Exp. Ther. 282 (1997) 378-384
3. Closs E.I., Simon A., Vekony N., and Rotmann A. Plasma membrane transporters for arginine. J. Nutr. 134 (2004) 2752S-2759S
4. Curis E., Nicolis I., Moinard C., Osowska S., Zerrouk N., Benazeth S., and Cynober L. Almost all about citrulline in mammals. Amino Acids 29 (2005) 177-205
5. Daniel E.E., Wang Y.F., Salapatek A.M., Mao Y.K., and Mori M. Arginosuccinate synthetase, arginosuccinate lyase and NOS in canine gastrointestinal tract: immunocytochemical studies. Neurogastroenterol. Motil. 12 (2000) 317-334
6. De Boer J., Duyvendak M., Schuurman F.E., Pouw F.M., Zaagsma J., and 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. 128 (1999) 1114-1120
7. De Gouw H.W., Verbruggen M.B., Twiss I.M., and Sterk P.J. Effect of oral L-arginine on airway hyperresponsiveness to histamine in asthma. Thorax 54 (1999) 1033-1035
8. Ellis J.L., and Conanan N. l-citrulline reverses the inhibition of nonadrenergic, noncholinergic relaxations produced by nitric oxide synthase inhibitors in guinea pig trachea and human bronchus. J. Pharmacol. Exp. Ther. 269 (1994) 1073-1078
9. Groneberg D.A., Springer J., and Fischer A. Vasoactive intestinal polypeptide as mediator of asthma. Pulm. Pharmacol. Ther. 14 (2001) 391-401
10. Husson A., Brasse-Lagnel C., Fairand A., Renouf S., and Lavoinne A. Argininosuccinate synthetase from the urea cycle to the citrulline-NO cycle. Eur. J. Biochem. 270 (2003) 1887-1899
11. Maarsingh H., Tio M.A., Zaagsma J., and Meurs H. Arginase attenuates inhibitory nonadrenergic noncholinergic nerve-induced nitric oxide generation and airway smooth muscle relaxation. Respir. Res. 6 (2005) 23
12. Maarsingh H., Leusink J., Bos I.S.T., Zaagsma J., and Meurs H. Arginase strongly impairs neuronal nitric oxide-mediated airway smooth muscle relaxation in allergic asthma. Respir. Res. 7 (2006) 6
13. Meurs H., Hamer M.A., Pethe S., Vadon-Le Goff S., Boucher J.L., and Zaagsma J. Modulation of cholinergic airway reactivity and nitric oxide production by endogenous arginase activity. Br. J. Pharmacol. 130 (2000) 1793-1798
14. Meurs H., McKay S., Maarsingh H., Hamer M.A., Macic L., Molendijk N., and Zaagsma J. Increased arginase activity underlies allergen-induced deficiency of cNOS-derived nitric oxide and airway hyperresponsiveness. Br. J. Pharmacol. 136 (2002) 391-398
15. Meurs H., Maarsingh H., and Zaagsma J. Arginase and asthma: novel insights into nitric oxide homeostasis and airway hyperresponsiveness. Trends Pharmacol. Sci. 24 (2003) 450-455
16. Moncada S., Palmer R.M., and Higgs E.A. Biosynthesis of nitric oxide from L-arginine. A pathway for the regulation of cell function and communication. Biochem. Pharmacol. 38 (1989) 1709-1715
17. Morris S.M. Regulation of enzymes of the urea cycle and arginine metabolism. Annu. Rev. Nutr. 22 (2002) 87-105
18. Morris C.R., Poljakovic M., Lavrisha L., Machado L., Kuypers F.A., and Morris Jr. S.M. Decreased arginine bioavailability and increased serum arginase activity in asthma. Am. J. Respir. Crit. Care Med. 170 (2004) 148-153
19. Nagasaki A., Gotoh T., Takeya M., Yu Y., Takiguchi M., Matsuzaki H., Takatsuki K., and Mori M. Coinduction of nitric oxide synthase, argininosuccinate synthetase, and argininosuccinate lyase in lipopolysaccharide-treated rats. RNA blot, immunoblot, and immunohistochemical analyses. J. Biol. Chem. 271 (1996) 2658-2662
20. Rattan S., and Chakder S. l-citrulline recycling in opossum internal anal sphincter relaxation by nonadrenergic, noncholinergic nerve stimulation. Gastroenterology 112 (1997) 1250-1259
21. Ricciardolo F.L.M. Multiple roles of nitric oxide in the airways. Thorax 58 (2003) 175-182
22. Ricciardolo F.L.M., DiMaria G.U., Mistretta A., Sapienza M.A., and Geppetti P. Impairment of bronchoprotection by nitric oxide in severe asthma. Lancet 350 (1997) 1297-1298
23. Ricciardolo F.L., Timmers M.C., Geppetti P., van Schadewijk A., Brahim J.J., Sont J.K., de Gouw H.W., Hiemstra P.S., van Krieken J.H., and Sterk P.J. Allergen-induced impairment of bronchoprotective nitric oxide synthesis in asthma. J. Allergy Clin. Immunol. 108 (2001) 198-204
24. Nagasaki A., Gotoh T., Isobe H., and Mori M. Regulation of the genes for arginase isoforms and related enzymes in mouse macrophages by lipopolysaccharide. Am. J. Physiol. 277 (1999) E110-E117
25. Santing R.E., Meurs H., van der Mark T.W., Remie R., Oosterom W.C., Brouwer F., and Zaagsma J. A novel method to assess airway function parameters in chronically instrumented, unrestrained guinea-pigs. Pulm. Pharmacol. 5 (1992) 265-272
26. Santing R.E., Olymulder C.G., Zaagsma J., and 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. 93 (1994) 1021-1030
27. Shuttleworth C.W., Burns A.J., Ward S.M., O'Brien W.E., and Sanders K.M. Recycling of l-citrulline to sustain nitric oxide-dependent enteric neurotransmission. Neuroscience 68 (1995) 1295-1304
28. Shuttleworth C.W., Conlon S.B., and Sanders K.M. Regulation of citrulline recycling in nitric oxide-dependent neurotransmission in the murine proximal colon. Br. J. Pharmacol. 120 (1997) 707-713
29. Suschek C.V., Schnorr O., Hemmrich K., Aust O., Klotz L.O., Sies H., and Kolb-Bachofen V. Critical role of L-arginine in endothelial cell survival during oxidative stress. Circulation 107 (2003) 2607-2614
30. Takano H., Lim H.B., Miyabara Y., Ichinose T., Yoshikana T., and Sagai M. Oral administration of l-arginine potentiates allergen-induced airway inflammation and expression of interleukin-5 in mice. J. Pharmacol. Exp. Ther. 286 (1998) 767-771
31. Tucker J.F., Brave S.R., Charalambous L., Hobbs A.J., and Gibson A. L-NG-nitro arginine inhibits non-adrenergic, non-cholinergic relaxations of guinea-pig isolated tracheal smooth muscle. Br. J. Pharmacol. 100 (1990) 663-664
32. Van Amsterdam R.G., Brouwer F., and Zaagsma J. Analysis of the beta-adrenoceptor mediated inhibition of IgG1 and IgE dependent guinea-pig anaphylactic tracheal smooth muscle contraction. Agents Actions 26 (1989) 48-51
33. Van Geldre L.A., Timmermans J.P., and Lefebvre R.A. l-citrulline recycling by argininosuccinate synthetase and lyase in rat gastric fundus. Eur. J. Pharmacol. 455 (2002) 149-160
34. Waugh W.H., Daeschner III C.W., Files B.A., McConnell M.E., and Strandjord S.E. Oral citrulline as arginine precursor may be beneficial in sickle cell disease: early phase two results. J. Natl. Med. Assoc. 93 (2001) 363-371
35. Wu G., and Morris S.M. Arginine metabolism: nitric oxide and beyond. Biochem. J. 336 (1998) 1-17
36. Xie L., and Gross S.S. Argininosuccinate synthetase overexpression in vascular smooth muscle cells potentiates immunostimulant-induced NO production. J. Biol. Chem. 272 (1997) 16624-16630
37. Zhang B., Cao G.L., Domachowske J., Jackson M.J., Porasuphatana S., and Rosen G.M. Stable expression of varied levels of inducible nitric oxide synthase in primary cultures of endothelial cells. Anal. Biochem. 286 (2000) 198-205
38. Zhang W.Y., Gotoh T., Oyadomari S., and Mori M. Coinduction of inducible nitric oxide synthase and arginine recycling enzymes in cytokine-stimulated PC12 cells and high output production of nitric oxide. Brain Res. Mol. Brain Res. 83 (2000) 1-8