Abstract
Aim:
To find out if the two aspects of asthma (chronic airway inflammation and bronchial hyperresponsiveness) are related to hypersensitivity of calcium signaling in bronchial epithelial cells.
Methods:
Porcine bronchial epithelial cells (PBEC) were divided into sensitized (S) and nonsesitized (N) groups. In group S, the cells were preincubated with serum from ovalbumin sensitized guinea pigs. In group N, the cells were preincubated with serum from nonsensitized guinea pigs. Single cell calcium imaging and ELISA-based NF-κB activity were used to evaluate the histamine-stimulated intracellular free calcium level and NF-κB activity, respectively.
Results:
First, 0.1 μmol/L histamine could induce [Ca2+]i oscillations in PBEC of group S, but not in group N. Second, 1 μmol/L histamine could induce [Ca2+]i oscillations of PBEC in both group S and group N. The [Ca2+]i oscillation frequency of PBEC was significantly higher in group S than in group N, though the [Ca2+]i oscillation amplitude showed no difference between the two groups. Finally, when 10 μmol/L histamine was used to stimulate PBEC, a transient initial increase followed by a sustained elevation (FSE) of [Ca2+]i was observed in PBEC in both groups. The amplitude of the FSE of [Ca2+]i in PBEC was significantly higher in group S than in group N. The subsequent NF-κB activity was in accordance to the calcium oscillation frequency evoked by histamine, but not to the amplitude.
Conclusion:
It was suggested that the increased sensitivity of calcium signaling in bronchial epithelial cells might contribute to the exorbitant inflammation or increased susceptibility in asthmatic airway epithelial cells.
Similar content being viewed by others
Article PDF
References
Fireman P . Understanding asthma pathophysiology. Allergy Asthma Proc 2003; 24: 79–83.
Holtzman MJ, Ferdman B, Bohrer A, Turk J . Synthesis of the 1-o-Hexadecyl molecular species of platelet-activating factor by airway epithelial and vascular endothelial cells. Biochem Biophys Res Commun 1991; 177: 357–64.
Churchill L, Chilton FH, Resau JH, Bascom R, Hubbard WC, Proud D . Cyclooxygenase metabolism of endogenous arachidonic acid by cultured human tracheal epithelial cells. Am Rev Respir Dis 1989; 140: 449–59.
Ackerman V, Carpi S, Bellini A, Vassalli G, Marini M, Mattoli S . Constitutive expression of endothelin in bronchial epithelial cells of patients with symptomatic and asymptomatic asthma and modulation by histamine and interleukin-1. J Allergy Clin Immunol 1995; 96: 618–27.
Arima M, Plitt J, Stellato C, Bickel C, Motojima S, Makino S, et al. Expression of interleukin-16 human epithelial cells. Inhibition by dexamethasone. Am J Respir Cell Mol Biol 1999; 21: 684–92.
Dolmetsch RE, Xu K, Lewis RS . Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998; 6679: 933–6.
Li W, Llopis J, Whitney M, Zlokarnik G, Tsien RY . Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 1998; 392: 936–41.
Meldolesi J . Oscillation, activation, expression. Nature 1998; 392: 863–6.
Hu Q, Deshpande S, Irani K, Ziegelstein RC . [Ca2+]i oscillation frequency regulates agonist-stimulated NF-kappaB transcriptional activity. J Biol Chem 1999; 274: 33995–8.
Ouyang NT, Liu ZH, Zhong NS . Distribution of endothelin-1 in asthmatic guinea pigs. Zhonghua Jie He He Hu Xi Za Zhi 1995; 18: 151.
Wang CZ, Guo XJ, Wang SC . A guinea pig model to determine airway responsiveness in asthma. J 3rd Military Med Univ 1994; 16: 277–8. Chinese.
Wu R, Yankaskas J, Cheng E, Knowles MR, Boucher R . Growth and differentiation of human nasal epithelial cells in culture. Serum-free, hormone-supplemented medium and proteoglycan synthesis. Am Rev Respir Dis 1985; 132: 311–20.
Chen F, Wu R, Wang X . Effects of cigarette smoke extract on 713 the expression of β-catenin and tyrosine phosphorylation in airway epithelial cell. Zhong Hua Yi Xue Za Zhi 2001; 81: 406.
Hakonarson H, Maskeri N, Carter C, Grunstein MM . Regulation of TH1- and TH2-type cytokine expression and action in atopic asthmatic sensitized airway smooth muscle. J Clin Invest 1999; 103: 1077–87.
Jin S, Chen JG, Zhu LP, Liu SY, Wang DX, Hu Q . Subacute mild hypoxia increases histamine-stimulated calcium oscillation frequency in pulmonary artery endothelial cells. Prog Biochem Biophy 2005; 32: 551–6.
Konishi M, Olson A, Hollingworth S, Baylor SM . Myoplasmic binding of Fura-2 investigated by steady-state fluorescence and absorbance measurements. Biophys J 1988; 54: 1089–104.
Paltauf-Doburzynska J, Frieden M, Spitaler M, Graier WF . Histamine-induced Ca2+ oscillations in a human endothelial cell line depend on transmembrane ion flux, ryanodine receptors and endoplasmic reticulum Ca2+-ATPase. J Physiol 2000; 524: 701–13.
Renard P, Ernest I, Houbion A, Art M, Calvez HL, Raes M, et al. Development of a sensitive multi-well colorimetric assay for active NF-κB. Nucleic Acids Res 2001; 29: e21.
Jin S, Lu DQ, Ye SQ, Ye H, Zhu LP, Feng ZH, et al. A simplified probe preparation for ELISA-based NF-κB activity assay. J Biochem Biophys Methods 2005; 65: 20–9.
Black JL, Johnson PR . What determines asthma phenotype? Is it the interaction between allergy and the smooth muscle? Am J Respir Crit Care Med 2000; 161: S207–10.
Black JL, Marthan R, Armour CL, Johnson PR . Sensitization alters contractile responses and calcium influx in human airway smooth muscle. J Allergy Clin Immunol 1989; 84: 440–7.
Li C, Hu BC, Long ZJ . Effects of the decoction of Yumian Anti-asthma Formula on general serum IgE contents of asthmatic guinea pigs. Jiangsu Yao Xue Yu Lin Chuang Za Zhi 2001; 9: 14–6.
Hakonarson H, Herrick DJ, Serrano PG, Grunstein MM . Autocrine role of interleukin 1β in altered responsiveness of atopic asthmatic sensitized airway smooth muscle. J Clin Invest 1997; 99: 117–24.
Hirata N, Kohrogi H, Iwagoe H, Goto E, Hamamoto J, Fujii K, et al. Allergen exposure induces the expression of endothelial adhesion molecules in passively sensitized human bronchus: time course and the role of cytokines. Am J Respir Cell Mol Biol 1998; 18: 12–20.
Hakonarson H, Grunstein MM . Autologously up-regulated Fc receptor expression and action in airway smooth muscle mediates its altered responsiveness in the atopic asthmatic sensitized state. Proc Natl Acad Sci USA 1998; 95: 5257–62.
Matsubara T, Ziff M . Increased superoxide anion release from human endothelial cells in response to cytokines. J Immunol 1986; 137: 3295–8.
Toborek M, Blanc EM, Kaiser S, Mattson MP, Hennig B . Li-noleic acid potentiates TNF-mediated oxidative stress, disruption of calcium homeostasis, and apoptosis of cultured vascular endothelial cells. J Lipid Res 1997; 38: 2155–67.
Murphy HS, Shayman JA, Till GO, Mahrougui M, Owens CB, Ryan US, et al. Superoxide responses of endothelial cells to C5a and TNF-alpha: divergent signal transduction pathways. Am J Physiol 1992; 263: L51–9.
Deshpande SS, Angkeow P, Huang J, Ozaki M, Irani K . Rac1 inhibits TNF-α-induced endothelial cell apoptosis: dual regulation by reactive oxygen species. FASEB J 2000; 14: 1705–14.
Thabut G, El-Benna J, Samb A, Corda S, Megret J, Leseche G, et al. Tumor necrosis factor-alpha increases airway smooth muscle oxidants production through a NADPH oxidase-like system to enhance myosin light chain phosphorylation and contractility. J Biol Chem 2002; 277: 22814–21.
Hu Q, Zheng G, Zweier JL, Deshpande S, Irani K, Ziegelstein RC . NADPH oxidase activation increases the sensitivity of intracellular Ca2+ stores to inositol 1,4,5-trisphosphate in human endothelial cells. J Biol Chem 2000; 275: 15749–57.
Hu Q, Yu ZX, Ferrans VJ, Takeda K, Irani K, Ziegelstein RC . Critical role of NADPH oxidase-derived reactive oxygen species in generating Ca2+ oscillations in human aortic endothelial cells stimulated by histamine. J Biol Chem 2002; 277: 32546–51.
Lounsbury KM, Hu Q, Ziegelstein RC . Calcium signaling and oxidant stress in the vasculature. Free Radic Biol Med 2000; 28: 1362–9.
Hart LA, Krishnan VL, Adcock IM, Barnes PJ, Chung KF . Activation and localization of transcription factor, nuclear factor-kappaB, in asthma. Am J Respir Crit Care Med 1998; 158: 1585–92.
Poynter ME, Irvin CG, Janssen-Heininger YM . Rapid activation of nuclear factor-kappaB in airway epithelium in a murine model of allergic airway inflammation. Am J Pathol 2002; 160: 1325–34.
Author information
Authors and Affiliations
Corresponding author
Additional information
Projected supported by grants from the National Natural Science Foundation of China (No 30570793, No 30200099, No 30270351).
Rights and permissions
About this article
Cite this article
Jin, S., Tian, D., Chen, Jg. et al. Passive sensitization increases histamine-stimulated calcium signaling and NF-κB transcription activity in bronchial epithelial cells. Acta Pharmacol Sin 27, 708–714 (2006). https://doi.org/10.1111/j.1745-7254.2006.00334.x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1111/j.1745-7254.2006.00334.x
Keywords
This article is cited by
-
In vitro differentiation of W8B2+ human cardiac stem cells: gene expression of ionic channels and spontaneous calcium activity
Cellular & Molecular Biology Letters (2020)
-
IL-4-induced caveolin-1-containing lipid rafts aggregation contributes to MUC5AC synthesis in bronchial epithelial cells
Respiratory Research (2017)
-
Potentiation of NF‐κB‐dependent transcription and inflammatory mediator release by histamine in human airway epithelial cells
British Journal of Pharmacology (2007)