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. 1998;7(1):35–40. doi: 10.1080/09629359891360

Role of the epithelial layer in the generation of superoxide anion by the guinea-pig isolated trachea.

G Sadeghi-Hashjin 1, P A Henricks 1, G Folkerts 1, T Muis 1, J Garssen 1, F P Nijkamp 1
PMCID: PMC1781820  PMID: 9839697

Abstract

The lucigenin-dependent chemiluminescence generation by guinea-pig isolated tracheal two rings preparations was studied. Tracheal preparations stimulated with phorbol myristate acetate (PMA) or opsonized zymosan generated chemiluminescence. The total amount of chemiluminescence generated in 120 min was 754+/-63 mV x min for PMA and 4832+/-396 mV x min for zymosan. Generation of chemiluminescence was decreased by more than 50% when the tissues were co-incubated with superoxide dismutase (100 U/ml). Also, addition of direct donors of nitric oxide diminished chemiluminescence generation by zymosan-activated tracheal rings significantly by about 50%. However, the presence of the precursor or of inhibitors of nitric oxide synthase did not influence zymosan-induced chemiluminescence. Removal of the epithelial layer from tracheal rings caused an approximately 90% decrease in chemiluminescence response. However, isolated epithelial cell suspensions did not generate chemiluminescence. Histologic examination showed that the number of eosinophils in the tracheal tissue was reduced from 56+/-7 to 18+/-8 per mm basal membrane when the epithelial layer was removed. These results indicated that (1) superoxide anion formation can take place in the guinea-pig trachea, (2) eosinophils in the epithelial and submucosal layers of guinea-pig trachea are likely candidates for superoxide generation although other cell types can also be involved, and (3) besides relaxing airway smooth muscle, nitric oxide donors may also affect superoxide in the airways.

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Selected References

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  1. Allen R. C., Stjernholm R. L., Steele R. H. Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun. 1972 May 26;47(4):679–684. doi: 10.1016/0006-291x(72)90545-1. [DOI] [PubMed] [Google Scholar]
  2. Babior B. M. Oxygen-dependent microbial killing by phagocytes (first of two parts). N Engl J Med. 1978 Mar 23;298(12):659–668. doi: 10.1056/NEJM197803232981205. [DOI] [PubMed] [Google Scholar]
  3. Baggiolini M., Wymann M. P. Turning on the respiratory burst. Trends Biochem Sci. 1990 Feb;15(2):69–72. doi: 10.1016/0968-0004(90)90179-f. [DOI] [PubMed] [Google Scholar]
  4. Dikshit M., Chari S. S., Seth P., Kumari R. Interaction of nitric oxide synthase inhibitors and their D-enantiomers with rat neutrophil luminol dependent chemiluminescence response. Br J Pharmacol. 1996 Oct;119(3):578–582. doi: 10.1111/j.1476-5381.1996.tb15711.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Faulkner K., Fridovich I. Luminol and lucigenin as detectors for O2.-. Free Radic Biol Med. 1993 Oct;15(4):447–451. doi: 10.1016/0891-5849(93)90044-u. [DOI] [PubMed] [Google Scholar]
  6. Folkerts G., van der Linde H. J., Nijkamp F. P. Virus-induced airway hyperresponsiveness in guinea pigs is related to a deficiency in nitric oxide. J Clin Invest. 1995 Jan;95(1):26–30. doi: 10.1172/JCI117649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fridovich I. Superoxide radical: an endogenous toxicant. Annu Rev Pharmacol Toxicol. 1983;23:239–257. doi: 10.1146/annurev.pa.23.040183.001323. [DOI] [PubMed] [Google Scholar]
  8. Heberer M., Ernst M., Dürig M., Allgöwer M., Fischer H. Measurement of chemiluminescence in freshly drawn human blood. II. Clinical application of zymosan-induced chemiluminescence. Klin Wochenschr. 1982 Dec 1;60(23):1443–1448. doi: 10.1007/BF01720991. [DOI] [PubMed] [Google Scholar]
  9. Hulsmann A. R., Raatgeep H. R., den Hollander J. C., Stijnen T., Saxena P. R., Kerrebijn K. F., de Jongste J. C. Oxidative epithelial damage produces hyperresponsiveness of human peripheral airways. Am J Respir Crit Care Med. 1994 Feb;149(2 Pt 1):519–525. doi: 10.1164/ajrccm.149.2.8306055. [DOI] [PubMed] [Google Scholar]
  10. Jorens P. G., Vermeire P. A., Herman A. G. L-arginine-dependent nitric oxide synthase: a new metabolic pathway in the lung and airways. Eur Respir J. 1993 Feb;6(2):258–266. [PubMed] [Google Scholar]
  11. Kinnula V. L., Adler K. B., Ackley N. J., Crapo J. D. Release of reactive oxygen species by guinea pig tracheal epithelial cells in vitro. Am J Physiol. 1992 Jun;262(6 Pt 1):L708–L712. doi: 10.1152/ajplung.1992.262.6.L708. [DOI] [PubMed] [Google Scholar]
  12. Kooy N. W., Royall J. A., Ye Y. Z., Kelly D. R., Beckman J. S. Evidence for in vivo peroxynitrite production in human acute lung injury. Am J Respir Crit Care Med. 1995 Apr;151(4):1250–1254. doi: 10.1164/ajrccm/151.4.1250. [DOI] [PubMed] [Google Scholar]
  13. Kuthan H., Ullrich V. Oxidase and oxygenase function of the microsomal cytochrome P450 monooxygenase system. Eur J Biochem. 1982 Sep 1;126(3):583–588. doi: 10.1111/j.1432-1033.1982.tb06820.x. [DOI] [PubMed] [Google Scholar]
  14. McCord J. M., Fridovich I. The reduction of cytochrome c by milk xanthine oxidase. J Biol Chem. 1968 Nov 10;243(21):5753–5760. [PubMed] [Google Scholar]
  15. Morikawa M., Inoue M., Tokumaru S., Kogo H. Enhancing and inhibitory effects of nitric oxide on superoxide anion generation in human polymorphonuclear leukocytes. Br J Pharmacol. 1995 Aug;115(7):1302–1306. doi: 10.1111/j.1476-5381.1995.tb15040.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nijkamp F. P., Folkerts G. Nitric oxide and bronchial reactivity. Clin Exp Allergy. 1994 Oct;24(10):905–914. doi: 10.1111/j.1365-2222.1994.tb02721.x. [DOI] [PubMed] [Google Scholar]
  17. Nijkamp F. P., van der Linde H. J., Folkerts G. Nitric oxide synthesis inhibitors induce airway hyperresponsiveness in the guinea pig in vivo and in vitro. Role of the epithelium. Am Rev Respir Dis. 1993 Sep;148(3):727–734. doi: 10.1164/ajrccm/148.3.727. [DOI] [PubMed] [Google Scholar]
  18. Radi R., Cosgrove T. P., Beckman J. S., Freeman B. A. Peroxynitrite-induced luminol chemiluminescence. Biochem J. 1993 Feb 15;290(Pt 1):51–57. doi: 10.1042/bj2900051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rengasamy A., Johns R. A. Inhibition of nitric oxide synthase by a superoxide generating system. J Pharmacol Exp Ther. 1993 Dec;267(3):1024–1027. [PubMed] [Google Scholar]
  20. Sadeghi-Hashjin G., Folkerts G., Henricks P. A., Van de Loo P. G., Van der Linde H. J., Dik I. E., Nijkamp F. P. Induction of guinea pig airway hyperresponsiveness by inactivation of guanylate cyclase. Eur J Pharmacol. 1996 Apr 29;302(1-3):109–115. doi: 10.1016/0014-2999(96)00081-7. [DOI] [PubMed] [Google Scholar]
  21. Sadeghi-Hashjin G., Folkerts G., Henricks P. A., Verheyen A. K., van der Linde H. J., van Ark I., Coene A., Nijkamp F. P. Peroxynitrite induces airway hyperresponsiveness in guinea pigs in vitro and in vivo. Am J Respir Crit Care Med. 1996 May;153(5):1697–1701. doi: 10.1164/ajrccm.153.5.8630623. [DOI] [PubMed] [Google Scholar]
  22. Sanders S. P., Zweier J. L., Harrison S. J., Trush M. A., Rembish S. J., Liu M. C. Spontaneous oxygen radical production at sites of antigen challenge in allergic subjects. Am J Respir Crit Care Med. 1995 Jun;151(6):1725–1733. doi: 10.1164/ajrccm.151.6.7767513. [DOI] [PubMed] [Google Scholar]
  23. Saran M., Michel C., Bors W. Reaction of NO with O2-. implications for the action of endothelium-derived relaxing factor (EDRF). Free Radic Res Commun. 1990;10(4-5):221–226. doi: 10.3109/10715769009149890. [DOI] [PubMed] [Google Scholar]
  24. Wang J. F., Komarov P., de Groot H. Luminol chemiluminescence in rat macrophages and granulocytes: the role of NO, O2-/H2O2, and HOCl. Arch Biochem Biophys. 1993 Jul;304(1):189–196. doi: 10.1006/abbi.1993.1338. [DOI] [PubMed] [Google Scholar]
  25. Ward P. A. Mechanisms of endothelial cell injury. J Lab Clin Med. 1991 Nov;118(5):421–426. [PubMed] [Google Scholar]
  26. Wink D. A., Hanbauer I., Krishna M. C., DeGraff W., Gamson J., Mitchell J. B. Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci U S A. 1993 Nov 1;90(21):9813–9817. doi: 10.1073/pnas.90.21.9813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Woschnagg C., Rak S., Venge P. Oxygen radical production by blood eosinophils is reduced during birch pollen season in allergic patients. Clin Exp Allergy. 1996 Sep;26(9):1064–1072. [PubMed] [Google Scholar]
  28. YAMAZAKI I., PIETTE L. H. THE MECHANISM OF AEROBIC OXIDASE REACTION CATALYZED BY PEROXIDASE. Biochim Biophys Acta. 1963 Sep 3;77:47–64. doi: 10.1016/0006-3002(63)90468-2. [DOI] [PubMed] [Google Scholar]

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