Mediators of Inflammation

Mediators of Inflammation / 2007 / Article

Research Article | Open Access

Volume 2007 |Article ID 24174 | 6 pages | https://doi.org/10.1155/2007/24174

Resting Tension Affects eNOS Activity in a Calcium-Dependent Way in Airways

Received14 Dec 2006
Accepted05 Feb 2007
Published28 Mar 2007

Abstract

The alteration of resting tension (RT) from 0.5 g to 2.5 g increased significantly airway smooth muscle contractions induced by acetylcholine (ACh) in rabbit trachea. The decrease in extracellular calcium concentration [Ca2+]o from 2 mM to 0.2 mM reduced ACh-induced contractions only at 2.5 g RT with no effect at 0.5 g RT. The nonselective inhibitor of nitric oxide synthase (NOS), NG-nitro-L-arginine methyl ester (L-NAME) increased ACh-induced contractions at 2.5 g RT. The inhibitor of inducible NOS, S-methylsothiourea or neuronal NOS, 7-nitroindazole had no effect. At 2.5 g RT, the reduction of [Ca2+]o from 2 mM to 0.2 mM abolished the effect of L-NAME on ACh-induced contractions. The NO precursor L-arginine or the tyrosine kinase inhibitors erbstatin A and genistein had no effect on ACh-induced contractions obtained at 2.5 g RT. Our results suggest that in airways, RT affects ACh-induced contractions by modulating the activity of epithelial NOS in a calcium-dependent, tyrosine-phosphorylation-independent way.

References

  1. D. H. Yates, “Role of exhaled nitric oxide in asthma,” Immunology and Cell Biology, vol. 79, no. 2, pp. 178–190, 2001. View at: Publisher Site | Google Scholar
  2. M. A. Marletta, “Nitric oxide synthase structure and mechanism,” Journal of Biological Chemistry, vol. 268, no. 17, pp. 12231–12234, 1993. View at: Google Scholar
  3. F. L. M. Ricciardolo, “Multiple roles of nitric oxide in the airways,” Thorax, vol. 58, no. 2, pp. 175–182, 2003. View at: Publisher Site | Google Scholar
  4. T. Michel and O. Feron, “Nitric oxide synthases: which, where, how, and why?,” Journal of Clinical Investigation, vol. 100, no. 9, pp. 2146–2152, 1997. View at: Google Scholar
  5. O. R. Rosales, C. M. Isales, P. Q. Barrett, C. Brophy, and B. E. Sumpio, “Exposure of endothelial cells to cyclic strain induces elevations of cytosolic Ca2+ concentration through mobilization of intracellular and extracellular pools,” Biochemical Journal, vol. 326, no. 2, pp. 385–392, 1997. View at: Google Scholar
  6. I. Fleming, J. Bauersachs, B. Fisslthaler, and R. Busse, “Ca2+-independent activation of the endothelial nitric oxide synthase in response to tyrosine phosphatase inhibitors and fluid shear stress,” Circulation Research, vol. 82, no. 6, pp. 686–695, 1998. View at: Google Scholar
  7. I. Fleming, J. Bauersachs, A. Schäfer, D. Scholz, J. Aldershvile, and R. Busse, “Isometric contraction induces the Ca2+-independent activation of the endothelial nitric oxide synthase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 3, pp. 1123–1128, 1999. View at: Publisher Site | Google Scholar
  8. K. I. Gourgoulianis, A. Domali, and P.-A. Molyvdas, “Airway responsiveness: role of inflammation, epithelium damage and smooth muscle tension,” Mediators of Inflammation, vol. 8, no. 4-5, pp. 261–263, 1999. View at: Publisher Site | Google Scholar
  9. A. A. Hatziefthimiou, E. Karetsi, E. Pratzoudis, K. I. Gourgoulianis, and P.-A. Molyvdas, “Resting tension effect on airway smooth muscle: the involvement of epithelium,” Respiratory Physiology and Neurobiology, vol. 145, no. 2-3, pp. 201–208, 2005. View at: Publisher Site | Google Scholar
  10. A. Lev, G. C. Christensen, J. P. Ryan, M. Wang, and S. G. Kelsen, “Epithelial modulation of trachealis muscle tension is calcium and temperature dependent,” Journal of Applied Physiology, vol. 67, no. 2, pp. 713–719, 1989. View at: Google Scholar
  11. M. T. Kirber, A. Guerrero-Hernández, and D. S. Bowman et al., “Multiple pathways responsible for the stretch-induced increase in Ca2+ concentration in toad stomach smooth muscle cells,” Journal of Physiology, vol. 524, no. 1, pp. 3–17, 2000. View at: Publisher Site | Google Scholar
  12. H. Zou, L. M. Lifshitz, R. A. Tuft, K. E. Fogarty, and J. J. Singer, “Visualization of Ca2+ entry through single stretch-activated cation channels,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 9, pp. 6404–6409, 2002. View at: Publisher Site | Google Scholar
  13. C. Li and Q. Xu, “Mechanical stress-initiated signal transductions in vascular smooth muscle cells,” Cellular Signalling, vol. 12, no. 7, pp. 435–445, 2000. View at: Publisher Site | Google Scholar
  14. X. Wu and M. J. Davis, “Characterization of stretch-activated cation current in coronary smooth muscle cells,” American Journal of Physiology. Heart and Circulatory Physiology, vol. 280, no. 4, pp. H1751–H1761, 2001. View at: Google Scholar
  15. C.-M. Hai and B. Szeto, “Agonist-induced myosin phosphorylation during isometric contraction and unloaded shortening in airway smooth muscle,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 262, no. 1, pp. L53–L62, 1992. View at: Google Scholar
  16. S. S. An and C.-M. Hai, “Mechanical signals and mechanosensitive modulation of intracellular [Ca2+] in smooth muscle,” American Journal of Physiology. Cell Physiology, vol. 279, no. 5, pp. C1375–C1384, 2000. View at: Google Scholar
  17. D. J. Vaughan, T. V. Brogan, M. E. Kerr, S. Deem, D. L. Luchtel, and E. R. Swenson, “Contributions of nitric oxide synthase isozymes to exhaled nitric oxide and hypoxic pulmonary vasoconstriction in rabbit lungs,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 284, no. 5, pp. L834–L843, 2003. View at: Google Scholar
  18. E. Muto, T. Hayashi, K. Yamada, T. Esaki, M. Sagai, and A. Iguchi, “Endothelial-constitutive nitric oxide synthase exists in airways and diesel exhaust particles inhibit the effect of nitric oxide,” Life Sciences, vol. 59, no. 18, pp. 1563–1570, 1996. View at: Publisher Site | Google Scholar
  19. R. Govers and T. J. Rabelink, “Cellular regulation of endothelial nitric oxide synthase,” American Journal of Physiology. Renal Physiology, vol. 280, no. 2, pp. F193–F206, 2001. View at: Google Scholar
  20. S.-F. Luo, S.-L. Pan, and W.-B. Wu et al., “Bradykinin-induced phosphoinositide hydrolysis and Ca2+ mobilization in canine cultured tracheal epithelial cells,” British Journal of Pharmacology, vol. 126, no. 6, pp. 1341–1350, 1999. View at: Publisher Site | Google Scholar
  21. R. P. Smith, R. Shellard, G. Di Benedetto, C. J. Magnus, and A. Mehta, “Interaction between calcium, neutral endopeptidase and the substance P mediated ciliary response in human respiratory epithelium,” European Respiratory Journal, vol. 9, no. 1, pp. 86–92, 1996. View at: Publisher Site | Google Scholar
  22. M. J. Sanderson and E. R. Dirksen, “Mechanosensitivity of cultured ciliated cells from the mammalian respiratory tract: implications for the regulation of mucociliary transport,” Proceedings of the National Academy of Sciences of the United States of America, vol. 83, no. 19, pp. 7302–7306, 1986. View at: Publisher Site | Google Scholar
  23. S. Boitano, M. J. Sanderson, and E. R. Dirksen, “A role for Ca2+-conducting ion channels in mechanically-induced signal transduction of airway epithelial cells,” Journal of Cell Science, vol. 107, no. 11, pp. 3037–3044, 1994. View at: Google Scholar
  24. S. Boitano, M. L. Woodruff, and E. R. Dirksen, “Evidence for voltage-sensitive, calcium-conducting channels in airway epithelial cells,” American Journal of Physiology. Cell Physiology, vol. 269, no. 6, pp. C1547–C1556, 1995. View at: Google Scholar
  25. D. Hucks, N. M. Khan, and J. P. T. Ward, “Essential role of L-arginine uptake and protein tyrosine kinase activity for NO-dependent vasorelaxation induced by stretch, isometric tension and cyclic AMP in rat pulmonary arteries,” British Journal of Pharmacology, vol. 131, no. 7, pp. 1475–1481, 2000. View at: Publisher Site | Google Scholar
  26. D. Hucks and J. P. T. Ward, “Critical dependence of the NO-mediated component of cyclic AMP-induced vasorelaxation on extracellular L-arginine in pulmonary arteries of the rat,” British Journal of Pharmacology, vol. 130, no. 5, pp. 997–1004, 2000. View at: Publisher Site | Google Scholar
  27. T. Kapsali, S. Permutt, B. Laube, N. Scichilone, and A. Togias, “Potent bronchoprotective effect of deep inspiration and its absence in asthma,” Journal of Applied Physiology, vol. 89, no. 2, pp. 711–720, 2000. View at: Google Scholar
  28. N. Scichilone, T. Kapsali, S. Permutt, and A. Togias, “Deep inspiration-induced bronchoprotection is stronger than bronchodilation,” American Journal of Respiratory and Critical Care Medicine, vol. 162, no. 3, pp. 910–916, 2000. View at: Google Scholar
  29. N. Scichilone, S. Permutt, and A. Togias, “The lack of the bronchoprotective and not the bronchodilatory ability of deep inspiration is associated with airway hyperresponsiveness,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 2, pp. 413–419, 2001. View at: Google Scholar
  30. N. Scichilone, R. Marchese, F. Catalano, A. M. Vignola, A. Togias, and V. Bellia, “Bronchodilatory effect of deep inspiration is absent in subjects with mild COPD,” Chest, vol. 125, no. 6, pp. 2029–2035, 2004. View at: Publisher Site | Google Scholar
  31. B. S. Kesler and B. J. Canning, “Regulation of baseline cholinergic tone in guinea-pig airway smooth muscle,” Journal of Physiology, vol. 518, no. 3, pp. 843–855, 1999. View at: Publisher Site | Google Scholar
  32. M. J. Rand and C. G. Li, “Nitric oxide as a neurotransmitter in peripheral nerves: nature of transmitter and mechanism of transmission,” Annual Review of Physiology, vol. 57, pp. 659–682, 1995. View at: Publisher Site | Google Scholar
  33. S. J. Gunst, J. Q. Stropp, and J. Service, “Mechanical modulation of pressure-volume characteristics of contracted canine airways in vitro,” Journal of Applied Physiology, vol. 68, no. 5, pp. 2223–2229, 1990. View at: Google Scholar
  34. X. Shen, M. F. Wu, R. S. Tepper, and S. J. Gunst, “Mechanisms for the mechanical response of airway smooth muscle to length oscillation,” Journal of Applied Physiology, vol. 83, no. 3, pp. 731–738, 1997. View at: Google Scholar
  35. D. A. Knight and S. T. Holgate, “The airway epithelium: structural and functional properties in health and disease,” Respirology, vol. 8, no. 4, pp. 432–446, 2003. View at: Publisher Site | Google Scholar

Copyright © 2007 Eudoxia Kitsiopoulou et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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