Abstract
Carbon monoxide (CO) is an endogenously produced gas mediator produced by heme oxygenase (HO). Like nitric oxide (NO), CO is produced in the nasal mucosa. Given that induced NO synthase (iNOS) expression in nasal mucosa has been found to be up-regulated in allergic rhinitis, the current study investigated the expression of HO isoforms in allergic human nasal mucosa. Immunohistochemical staining for type 1 and 2 HO isoforms were carried out in nasal inferior turbinate mucosa from six patients with persistent allergic rhinitis, and compared with six control patients without nasal allergy. Focal and weak expression of HO-1 was observed in seromucous glands, with no difference between allergic and control specimens. Vascular endothelium, erythrocytes, smooth muscle and inflammatory cells (except macrophages) in the allergic group exhibited stronger HO-1 immunoreactivity compared to the control. Minimal expression was found in the respiratory epithelium in either group. Intravascular HO-1 expression was found in the allergic mucosa only. Intense HO-2 immunoreactivity was observed in the respiratory epithelium, vascular endothelium and seromucous glands in both allergic and control groups with no differences in intensity. In conclusion, unlike iNOS, HO-1 is minimally expressed in the nasal respiratory epithelium of either group. However, our findings suggest that it may be involved in the inflammatory process of allergic rhinitis at the submucosal level.
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References
Alcaraz MJ, Fernandez P, Guillen MI (2003) Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr Pharm Des 9:2541–2551
Andersson JA, Uddman R, Cardell LO (2000) Carbon monoxide is endogenously produced in the human nose and paranasal sinuses. J Allergy Clin Immunol 105:269–273
Andersson JA, Uddman R, Cardell LO (2002) Increased carbon monoxide levels in the nasal airways of subjects with a history of seasonal allergic rhinitis and in patients with upper respiratory tract infection. Clin Exp Allergy 32:224–227
Bachert C, Hauser U, Prem B, Rudack C, Ganzer U (1995) Proinflammatory cytokines in allergic rhinitis. Eur Arch Otorhinolaryngol 252 [Suppl 1]:S44–49
Bachert C, Wagenmann M, Hauser U (1995) Proinflammatory cytokines: measurement in nasal secretion and induction of adhesion receptor expression. Int Arch Allergy Immunol 107:106–108
Cardell LO, Ueki IF, Stjarne P, Agusti C, Takeyama K, Linden A, Nadel JA (1998) Bronchodilatation in vivo by carbon monoxide, a cyclic GMP related messenger. Br J Pharmacol 124:1065–1068
Conboy PJ, Jones NS (2000) The nose and nitric oxide: a review. Clin Otolaryngol 25:337–341
Durante W, Kroll MH, Christodoulides N, Peyton KJ, Schafer AI (1997) Nitric oxide induces heme oxygenase-1 gene expression and carbon monoxide production in vascular smooth muscle cells. Circ Res 80:557–564
Elbirt KK, Bonkovsky HL (1999) Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 111:438–447
Fernandez P, Guillen MI, Gomar F, Alcaraz MJ (2003) Expression of heme oxygenase-1 and regulation by cytokines in human osteoarthritic chondrocytes. Biochem Pharmacol 66:2049–2052
Guesdon JL, Ternynck T, Avrameas S (1979) The use of avidin-biotin interaction in immunoenzymatic techniques. J Histochem Cytochem 27:1131–1139
Horvath I, Loukides S, Wodehouse T, Kharitonov SA, Cole PJ, Barnes PJ (1998) Increased levels of exhaled carbon monoxide in bronchiectasis: a new marker of oxidative stress. Thorax 53:867–870
Kharitonov SA, Rajakulasingam K, O’Connor B, Durham SR, Barnes PJ (1997) Nasal nitric oxide is increased in patients with asthma and allergic rhinitis and may be modulated by nasal glucocorticoids. J Allergy Clin Immunol 99:58–64
Kawamoto H, Takeno S, Yajin K (1999) Increased expression of inducible nitric oxide synthase in nasal epithelial cells in patients with allergic rhinitis. Laryngoscope 109:2015–2020
Maines MD, Trakshel GM, Kutty RK (1986) Characterization of two constitutive forms of rat liver microsomal heme oxygenase. Only one molecular species of the enzyme is inducible. J Biol Chem 261:411–419
Maines MD (2000) The heme oxygenase system and its functions in the brain. Cell Mol Biol 46:573–585
Monma M, Yamaya M, Sekizawa K, Ikeda K, Suzuki N, Kikuchi T, Takasaka T, Sasaki H (1999) Increased carbon monoxide in exhaled air of patients with seasonal allergic rhinitis. Clin Exp Allergy 29:1537–1541
Paredi P, Leckie MJ, Horvath I, Kharitonov SA, Barnes PJ (1998) Exhaled carbon monoxide is elevated during allergen challenge in asthmatic patients. Eur Respir J 28 [Suppl]:127–128
Rodgers PA, Vreman HJ, Dennery PA, Stevenson DK (1994) Sources of carbon monoxide (CO) in biological systems and applications of CO detection technologies. Semin Perinatol 18:2–10
Yamaya M, Sekizawa K, Ishizuka S, Monma M, Mizuta K, Sasaki H (1998) Increased carbon monoxide in exhaled air of subjects with upper respiratory tract infections. Am J Respir Crit Care Med 158:311–314
Yamaya M, Sekizawa K, Ishizuka S, Monma M, Sasaki H, Yamara M (1999) Exhaled carbon monoxide levels during treatment of acute asthma. Eur Respir J 13:757–760. Erratum (2001) in: Eur Respir J 17:1336
Zayasu K, Sekizawa K, Okinaga S, Yamaya M, Ohrui T, Sasaki H (1997) Increased carbon monoxide in exhaled air of asthmatic patients. Am J Respir Crit Care Med 156:1140–1143
Acknowledgements
This study was supported by the Frimley Park Hospital ENT Research Fund. The authors thank S. Al-Hashimi and Professor M.G. Cook (Department of Pathology, Royal Surrey County Hospital, UK) for their assistance.
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Lo, S., Di Palma, S., Pitkin, L. et al. Localisation of heme oxygenase isoforms in allergic human nasal mucosa. Eur Arch Otorhinolaryngol 262, 595–598 (2005). https://doi.org/10.1007/s00405-004-0873-2
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DOI: https://doi.org/10.1007/s00405-004-0873-2