Nicotine inhibits FcεRI-induced cysteinyl leukotrienes and cytokine production without affecting mast cell degranulation through α7/α9/α10-nicotinic receptors

Journal of Immunology

Volumn 185, Issue 1, 2010, Pages 588-596

  Mishra, Neerad C ^a   Rir sima ah, Jules ^a   Boyd, R Thomas ^b   Singh, Shashi P ^a   Gundavarapu, Sravanthi ^a   Langley, Raymond J ^a   Razani Boroujerdi, Seddigheh ^a   Sopori, Mohan L ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BUNGAROTOXIN; BETA N ACETYLHEXOSAMINIDASE; BUNGAROTOXIN RECEPTOR; CALCIUM; COTININE; CYTOKINE; CYTOSOLIC PHOSPHOLIPASE A2; HISTAMINE; IMMUNOGLOBULIN E RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYLLYCACONITINE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINE; NICOTINIC RECEPTOR; PEPTIDOLEUKOTRIENE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMALL INTERFERING RNA; CHRNA10 PROTEIN, RAT; CHRNA9 PROTEIN, RAT; CYSTEINE; CYSTEINYL-LEUKOTRIENE; LEUKOTRIENE; PHOSPHOLIPASE A2;

ANIMAL CELL; ARTICLE; BASOPHIL; CALCIUM CELL LEVEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HISTAMINE RELEASE; MAST CELL DEGRANULATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; ANIMAL; BIOSYNTHESIS; BROWN NORWAY RAT; CYTOSOL; DEGRANULATION; DOWN REGULATION; ENZYMOLOGY; IMMUNOLOGY; MAST CELL; METABOLISM; PASSIVE SMOKING; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; BASOPHILS; CELL DEGRANULATION; CELL LINE, TUMOR; CYSTEINE; CYTOKINES; CYTOSOL; DOWN-REGULATION; LEUKOTRIENES; MAP KINASE SIGNALING SYSTEM; MAST CELLS; NICOTINE; PHOSPHOLIPASES A2; RATS; RATS, INBRED BN; RECEPTORS, IGE; RECEPTORS, NICOTINIC; TOBACCO SMOKE POLLUTION;

EID: 77956218434     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902227     Document Type: Article

References (70)

1. Peat, J. K., and J. Li. 1999. Reversing the trend: reducing the prevalence of asthma. J. Allergy Clin. Immunol. 103: 1-10.
2. Beasley, R., J. Crane, C. K. Lai, and N. Pearce. 2000. Prevalence and etiology of asthma. J. Allergy Clin. Immunol. 105: S466-S472.
3. Wüthrich, B. 1989. Epidemiology of the allergic diseases: are they really on the increase? Int. Arch. Allergy Appl. Immunol. 90(Suppl 1): 3-10.
4. von Mutius, E. 1998. The rising trends in asthma and allergic disease. Clin. Exp. Allergy 28(Suppl. 5): 45-49; discussion 50-51.
5. Burr, M. L., D. Wat, C. Evans, F. D. Dunstan, I. J. Doull, and British Thoracic Society Research Committee. 2006. Asthma prevalence in 1973, 1988 and 2003. Thorax 61: 296-299.
6. Turner, H., and J. P. Kinet. 1999. Signalling through the high-affinity IgE receptor Fc epsilonRI. Nature 402(6760 Suppl.):B24-B30.
7. Schwartz, L. B. 1994. Mast cells: function and contents. Curr. Opin. Immunol. 6: 91-97.
8. Mekori, Y. A., and D. D. Metcalfe. 2000. Mast cells in innate immunity. Immunol. Rev. 173: 131-140.
9. Spada, C. S., A. L. Nieves, A. H. Krauss, and D. F. Woodward. 1994. Comparison of leukotriene B4 and D4 effects on human eosinophil and neutrophil motility in vitro. J. Leukoc. Biol. 55: 183-191.
10. Dahlén, S. E., P. Hedqvist, S. Hammarström, and B. Samuelsson. 1980. Leukotrienes are potent constrictors of human bronchi. Nature 288: 484-486.
11. Henderson, W. R., Jr. 1994. The role of leukotrienes in inflammation. Ann. Intern. Med. 121: 684-697.
12. Eum, S. Y., K. Maghni, Q. Hamid, H. Campbell, D. H. Eidelman, and J. G. Martin. 2003. Involvement of the cysteinyl-leukotrienes in allergen-induced airway eosinophilia and hyperresponsiveness in the mouse. Am. J. Respir. Cell Mol. Biol. 28: 25-32.
13. Parameswaran, K., G. Cox, K. Radford, L. J. Janssen, R. Sehmi, and P. M. O'Byrne. 2002. Cysteinyl leukotrienes promote human airway smooth muscle migration. Am. J. Respir. Crit. Care Med. 166: 738-742.
14. Parameswaran, K., K. Radford, A. Fanat, J. Stephen, C. Bonnans, B. D. Levy, L. J. Janssen, and P. G. Cox. 2007. Modulation of human airway smooth muscle migration by lipid mediators and Th-2 cytokines. Am. J. Respir. Cell Mol. Biol. 37: 240-247.
15. Barbee, R. A., M. Halonen, W. Kaltenborn, M. Lebowitz, and B. Burrows. 1987. A longitudinal study of serum IgE in a community cohort: correlations with age, sex, smoking, and atopic status. J. Allergy Clin. Immunol. 79: 919-927.
16. Linneberg, A., N. H. Nielsen, F. Madsen, L. Frølund, A. Dirksen, and T. Jørgensen. 2001. Factors related to allergic sensitization to aeroallergens in a cross-sectional study in adults: The Copenhagen Allergy Study. Clin. Exp. Allergy 31: 1409-1417.
17. Sopori, M. 2002. Effects of cigarette smoke on the immune system. Natl. Rev. Immunol. 2: 372-377.
18. Jarvis, D., S. Chinn, C. Luczynska, and P. Burney. 1999. The association of smoking with sensitization to common environmental allergens: results from the European Community Respiratory Health Survey. J. Allergy Clin. Immunol. 104: 934-940.
19. Wüthrich, B., C. Schindler, T. C. Medici, J. P. Zellweger, P. Leuenberger, and SAPALDIA (Swiss Study on Air Pollution and Lung Diseases in Adults) Team. 1996. IgE levels, atopy markers and hay fever in relation to age, sex and smoking status in a normal adult Swiss population. Int. Arch. Allergy Immunol. 111: 396-402.
20. Mensinga, T. T., J. P. Schouten, B. Rijcken, S. T. Weiss, F. E. Speizer, and R. van der Lende. 1990. The relationship of eosinophilia and positive skin test reactivity to respiratory symptom prevalence in a community-based population study. J. Allergy Clin. Immunol. 86: 99-107.
21. Baldacci, S., P. Modena, L. Carrozzi, M. Pedreschi, M. Vellutini, P. Biavati, M. Simoni, T. Sapigni, G. Viegi, P. Paoletti, and C. Giuntini. 1996. Skin prick test reactivity to common aeroallergens in relation to total IgE, respiratory symptoms, and smoking in a general population sample of northern Italy. Allergy 51: 149-156.
22. Omenaas, E., P. Bakke, S. Elsayed, R. Hanoa, and A. Gulsvik. 1994. Total and specific serum IgE levels in adults: relationship to sex, age and environmental factors. Clin. Exp. Allergy 24: 530-539.
23. Sopori, M. L., W. Kozak, S. M. Savage, Y. Geng, D. Soszynski, M. J. Kluger, E. K. Perryman, and G. E. Snow. 1998. Effect of nicotine on the immune system: possible regulation of immune responses by central and peripheral mechanisms. Psychoneuroendocrinology 23: 189-204.
24. Wang, H., M. Yu, M. Ochani, C. A. Amella, M. Tanovic, S. Susarla, J. H. Li, H. Wang, H. Yang, L. Ulloa, et al. 2003. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421: 384-388.
25. Razani-Boroujerdi, S., S. P. Singh, C. Knall, F. F. Hahn, J. C. Peña-Philippides, R. Kalra, R. J. Langley, and M. L. Sopori. 2004. Chronic nicotine inhibits inflammation and promotes influenza infection. Cell. Immunol. 230: 1-9.
26. Mishra, N. C., J. Rir-Sima-Ah, R. J. Langley, S. P. Singh, J. C. Peña-Philippides, T. Koga, S. Razani-Boroujerdi, J. Hutt, M. Campen, K. C. Kim, et al. 2008. Nicotine primarily suppresses lung Th2 but not goblet cell and muscle cell responses to allergens. J. Immunol. 180: 7655-7663.
27. Razani-Boroujerdi, S., R. T. Boyd, M. I. Dávila-García, J. S. Nandi, N. C. Mishra, S. P. Singh, J. C. Pena-Philippides, R. Langley, and M. L. Sopori. 2007. T cells express alpha7-nicotinic acetylcholine receptor subunits that require a functional TCR and leukocyte-specific protein tyrosine kinase for nicotine-induced Ca2+ response. J. Immunol. 179: 2889-2898.
28. Kageyama-Yahara, N., Y. Suehiro, T. Yamamoto, and M. Kadowaki. 2008. IgE-induced degranulation of mucosal mast cells is negatively regulated via nicotinic acetylcholine receptors. Biochem. Biophys. Res. Commun. 377: 321-325.
29. Kindt, F., S. Wiegand, V. Niemeier, J. Kupfer, C. Löser, M. Nilles, H. Kurzen, W. Kummer, U. Gieler, and R. V. Haberberger. 2008. Reduced expression of nicotinic alpha subunits 3, 7, 9 and 10 in lesional and nonlesional atopic dermatitis skin but enhanced expression of alpha subunits 3 and 5 in mast cells. Br. J. Dermatol. 159: 847-857.
30. Yoshimaru, T., Y. Suzuki, T. Matsui, K. Yamashita, T. Ochiai, M. Yamaki, and K. Shimizu. 2002. Blockade of superoxide generation prevents high-affinity immunoglobulin E receptor-mediated release of allergic mediators by rat mast cell line and human basophils. Clin. Exp. Allergy 32: 612-618.
31. Ortega, E., B. Hazan, U. Zor, and I. Pecht. 1989. Mast cell stimulation by monoclonal antibodies specific for the Fc epsilon receptor yields distinct responses of arachidonic acid and leukotriene C4 secretion. Eur. J. Immunol. 19: 2251-2256.
32. Hernandez-Hansen, V., A. J. Smith, Z. Surviladze, A. Chigaev, T. Mazel, J. Kalesnikoff, C. A. Lowell, G. Krystal, L. A. Sklar, B. S. Wilson, and J. M. Oliver. 2004. Dysregulated FcepsilonRI signaling and altered Fyn and SHIP activities in Lyn-deficient mast cells. J. Immunol. 173: 100-112.
33. Chaturvedi, M. M., A. Mukhopadhyay, and B. B. Aggarwal. 2000. Assay for redox-sensitive transcription factor. Methods Enzymol. 319: 585-602.
34. Geng, Y., S. M. Savage, S. Razani-Boroujerdi, and M. L. Sopori. 1996. Effects of nicotine on the immune response. II. Chronic nicotine treatment induces T cell anergy. J. Immunol. 156: 2384-2390.
35. Razani-Boroujerdi, S., L. D. Partridge, and M. L. Sopori. 1994. Intracellular calcium signaling induced by thapsigargin in excitable and inexcitable cells. Cell Calcium 16: 467-474.
36. Bray, C., J. H. Son, and S. Meizel. 2005. Acetylcholine causes an increase of intracellular calcium in human sperm. Mol. Hum. Reprod. 11: 881-889.
37. Osman, A. A., A. D. Schrader, A. J. Hawkes, O. Akil, A. Bergeron, L. R. Lustig, and D. D. Simmons. 2008. Muscle-like nicotinic receptor accessory molecules in sensory hair cells of the inner ear. Mol. Cell. Neurosci. 38: 153-169.
38. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
39. Schwartz, L. B., R. A. Lewis, D. Seldin, and K. F. Austen. 1981. Acid hydrolases and tryptase from secretory granules of dispersed human lung mast cells. J. Immunol. 126: 1290-1294.
40. Wershil, B. K., Y. A. Mekori, T. Murakami, and S. J. Galli. 1987. 125I-fibrin deposition in IgE-dependent immediate hypersensitivity reactions in mouse skin. Demonstration of the role of mast cells using genetically mast cell-deficient mice locally reconstituted with cultured mast cells. J. Immunol. 139: 2605-2614.
41. Galli, S. J. 1993. New concepts about the mast cell. N. Engl. J. Med. 328: 257-265.
42. Mancel, E., M. Drouet, and A. Sabbah. 1999. [Membrane stabilizers (chromones and ketotifen)] Allerg. Immunol. (Paris) 31: 103-105.
43. Shakoory, B., S. M. Fitzgerald, S. A. Lee, D. S. Chi, and G. Krishnaswamy. 2004. The role of human mast cell-derived cytokines in eosinophil biology. J. Interferon Cytokine Res. 24: 271-281. (Pubitemid 38648308)
44. Lorentz, A., I. Klopp, T. Gebhardt, M. P. Manns, and S. C. Bischoff. 2003. Role of activator protein 1, nuclear factor-kappaB, and nuclear factor of activated T cells in IgE receptor-mediated cytokine expression in mature human mast cells. J. Allergy Clin. Immunol. 111: 1062-1068.
45. Ali, K., A. Bilancio, M. Thomas, W. Pearce, A. M. Gilfillan, C. Tkaczyk, N. Kuehn, A. Gray, J. Giddings, E. Peskett, et al. 2004. Essential role for the p110delta phosphoinositide 3-kinase in the allergic response. Nature 431: 1007-1011.
46. Jeong, H. J., H. N. Koo, H. J. Na, M. S. Kim, S. H. Hong, J. W. Eom, K. S. Kim, T. Y. Shin, and H. M. Kim. 2002. Inhibition of TNF-alpha and IL-6 production by Aucubin through blockade of NF-kappaB activation RBL-2H3 mast cells. Cytokine 18: 252-259.
47. Murakami, M., I. Kudo, M. Umeda, A. Matsuzawa, M. Takeda, M. Komada, Y. Fujimori, K. Takahashi, and K. Inoue. 1992. Detection of three distinct phospholipases A2 in cultured mast cells. J Biochem 111: 175-181.
48. Hirasawa, N., F. Santini, and M. A. Beaven. 1995. Activation of the mitogen-activated protein kinase/cytosolic phospholipase A2 pathway in a rat mast cell line. Indications of different pathways for release of arachidonic acid and secretory granules. J. Immunol. 154: 5391-5402.
49. Sgard, F., E. Charpantier, S. Bertrand, N. Walker, D. Caput, D. Graham, D. Bertrand, and F. Besnard. 2002. A novel human nicotinic receptor subunit, alpha10, that confers functionality to the alpha9-subunit. Mol. Pharmacol. 61: 150-159.
50. Wilson, B. S., and J. M. Oliver. 2002. Effector roles of IgE antibodies: targeting allergen to the high-affinity IgE receptor for Fc epsilon RI-dependent signaling and antigen presentation. Clin. Allergy Immunol. 16: 197-232.
51. Galli, S. J., J. Kalesnikoff, M. A. Grimbaldeston, A. M. Piliponsky, C. M.Williams, and M. Tsai. 2005. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu. Rev. Immunol. 23: 749-786.
52. Jackson, J. A., M. W. Riggs, and A. M. Spiekerman. 1992. Testosterone deficiency as a risk factor for hip fractures in men: a case-control study. Am. J. Med. Sci. 304: 4-8.
53. Chen, Y., B. P. Pappu, H. Zeng, L. Xue, S. W. Morris, X. Lin, R. Wen, and D. Wang. 2007. B cell lymphoma 10 is essential for FcepsilonR-mediated degranulation and IL-6 production in mast cells. J. Immunol. 178: 49-57. (Pubitemid 46033586)
54. Alkondon, M., E. F. Pereira, L. E. Almeida, W. R. Randall, and E. X. Albuquerque. 2000. Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 39: 2726-2739.
55. Geng, Y., S. M. Savage, L. J. Johnson, J. Seagrave, and M. L. Sopori. 1995. Effects of nicotine on the immune response. I. Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol. Appl. Pharmacol. 135: 268-278.
56. Glover, S., M. S. de Carvalho, T. Bayburt, M. Jonas, E. Chi, C. C. Leslie, and M. H. Gelb. 1995. Translocation of the 85-kDa phospholipase A2 from cytosol to the nuclear envelope in rat basophilic leukemia cells stimulated with calcium ionophore or IgE/antigen. J. Biol. Chem. 270: 15359-15367.
57. Chang, W. C., J. Di Capite, K. Singaravelu, C. Nelson, V. Halse, and A. B. Parekh. 2008. Local Ca2+ influx through Ca2+ release-activated Ca2+ (CRAC) channels stimulates production of an intracellular messenger and an intercellular pro-inflammatory signal. J. Biol. Chem. 283: 4622-4631.
58. Zaidi, A. K., E. R. Thangam, and H. Ali. 2006. Distinct roles of Ca2+ mobilization and G protein usage on regulation of Toll-like receptor function in human and murine mast cells. Immunology 119: 412-420.
59. Rivera, J., and A. Olivera. 2008. A current understanding of Fc epsilon RI-dependent mast cell activation. Curr. Allergy Asthma Rep. 8: 14-20.
60. Akimoto, M., K. Mishra, K. T. Lim, N. Tani, S. I. Hisanaga, T. Katagiri, A. Elson, K. Mizuno, and H. Yakura. 2009. Protein tyrosine phosphatase epsilon is a negative regulator of FcepsilonRI-mediated mast cell responses. Scand. J. Immunol. 69: 401-411.
61. Oliver, J. M., D. L. Burg, B. S. Wilson, J. L. McLaughlin, and R. L. Geahlen. 1994. Inhibition of mast cell Fc epsilon R1-mediated signaling and effector function by the Syk-selective inhibitor, piceatannol. J. Biol. Chem. 269: 29697-29703.
62. Zhang, J., E. H. Berenstein, R. L. Evans, and R. P. Siraganian. 1996. Transfection of Syk protein tyrosine kinase reconstitutes high affinity IgE receptor-mediated degranulation in a Syk-negative variant of rat basophilic leukemia RBL-2H3 cells. J. Exp. Med. 184: 71-79.
63. Kawakami, Y., J. Kitaura, A. B. Satterthwaite, R. M. Kato, K. Asai, S. E. Hartman, M. Maeda-Yamamoto, C. A. Lowell, D. J. Rawlings, O. N. Witte, and T. Kawakami. 2000. Redundant and opposing functions of two tyrosine kinases, Btk and Lyn, in mast cell activation. J. Immunol. 165: 1210-1219.
64. Nishizumi, H., and T. Yamamoto. 1997. Impaired tyrosine phosphorylation and Ca2+ mobilization, but not degranulation, in lyn-deficient bone marrow-derived mast cells. J. Immunol. 158: 2350-2355. (Pubitemid 127470021)
65. Vonakis, B. M., S. P. Gibbons, Jr., M. J. Rotté, E. A. Brothers, S. C. Kim, K. Chichester, and S. M. MacDonald. 2005. Regulation of rat basophilic leukemia-2H3 mast cell secretion by a constitutive Lyn kinase interaction with the high affinity IgE receptor (Fc epsilon RI). J. Immunol. 175: 4543-4554.
66. Parravicini, V., M. Gadina, M. Kovarova, S. Odom, C. Gonzalez-Espinosa, Y. Furumoto, S. Saitoh, L. E. Samelson, J. J. O'Shea, and J. Rivera. 2002. Fyn kinase initiates complementary signals required for IgE-dependent mast cell degranulation. Nat. Immunol. 3: 741-748.
67. Kawashima, K., and T. Fujii. 2004. Expression of non-neuronal acetylcholine in lymphocytes and its contribution to the regulation of immune function. Front. Biosci. 9: 2063-2085.
68. Kummer, W., K. S. Lips, and U. Pfeil. 2008. The epithelial cholinergic system of the airways. Histochem. Cell Biol. 130: 219-234.
69. Boyd, R. T. 1997. The molecular biology of neuronal nicotinic acetylcholine receptors. Crit. Rev. Toxicol. 27: 299-318.
70. Lips, K. S., P. König, K. Schätzle, U. Pfeil, G. Krasteva, M. Spies, R. V. Haberberger, S. A. Grando, and W. Kummer. 2006. Coexpression and spatial association of nicotinic acetylcholine receptor subunits alpha7 and alpha10 in rat sympathetic neurons. J. Mol. Neurosci. 30: 15-16.