Generic placeholder image

Current Respiratory Medicine Reviews

Author(s): Kengo Kobayashi, Yuriko Hirono, Honami Nakta, Kent E. Pinkerton and Minoru Takeuchi*

DOI: 10.2174/1573398X16999201105162114

DownloadDownload PDF Flyer Cite As
Cigarette Smoke Exposure Inhibits Early Phase of Antibody Production through Inhibition of Immune Functions in Alveolar Macrophage

Page: [193 - 200] Pages: 8

  • * (Excluding Mailing and Handling)

Explore Articles
About Journal
For Authors
For Editors
For Reviewers

Abstract

Background: Cigarette smoke (CS) is inhaled into the lung. Alveolar macrophage (AM) is known to play an important role in the lung immune system. However, the relationship between AM functions and antibody production by CS is not fully investigated.

Objective: Therefore, we investigated the effects of AM from CS exposed mice on antibody production. Mice were exposed to 20 cigarettes/day for 10 days. AM were obtained by broncho-alveolar lavage. Antibody production was analyzed by plaque-forming cell assay using seep red blood cell (SRBC) as antigen.

Methods: B cell proliferation was analyzed by 3H-thymidine incorporation. Phagocytic activity using fluorescein isothiocyanate-labeled SRBC and expressions of surface antigens on AM were analyzed by flow cytometry. Cytokines and NF-κB mRNA expressions of AM were analyzed by RTPCR.

Results and Discussion: Antibody production was decreased at the induction phase, but not at the expression phase by AM from smoked mice (SM) compared with non-smoked mice (NSM). B cell proliferation was decreased by cigarette extracts dose-dependently. Phagocytic activity of AM was decreased in SM compared with NSM. Expression of surface antigens on AM was decreased in SM compared with NSM. Cytokines or NF-κB mRNA expressions of AM were decreased in SM compared with NSM.

Conclusion: These results suggest that the inhibition of antibody production by cigarette smoking is caused by the inhibition of phagocytosis and expressions of surface antigens associated with antigen presentation. Such inhibition of AM functions may increase the risk of bacterial and virus infections.

Keywords: Cigarette smoke, alveolar macrophage, antigen presentation, antibody production, phagocytosis, cytokines.

Graphical Abstract

[1]
Burns M D. Cigarettes and cigarette smoking. Clin Chest Med 1991; 12(4): 631-42.
[PMID: 1747982]
[2]
Wynder L E, Hoffmann D. Tobacco and tobacco smoke. Seminars in Oncology 1976; 3(1): 5-15.
[PMID: 982079]
[3]
Rawbone RG, Burns W, Patrick RA. The measurement of ‘environmental tobacco smoke’ particulates. Toxicol Lett 1987; 35(1): 125-9.
[http://dx.doi.org/10.1016/0378-4274(87)90096-8] [PMID: 3810673]
[4]
Johnson JD, Houchens DP, Kluwe WM, Craig DK, Fisher GL. Effects of mainstream and environmental tobacco smoke on the immune system in animals and humans: a review. Crit Rev Toxicol 1990; 20(5): 369-95.
[http://dx.doi.org/10.3109/10408449009089870] [PMID: 2202327]
[5]
Sopori M. Effects of cigarette smoke on the immune system. Nat Rev Immunol 2002; 2(5): 372-7.
[http://dx.doi.org/10.1038/nri803] [PMID: 12033743]
[6]
Takeuchi M. Smoking and immune functions. Clin Immunol 2001; 36(6): 843-50.
[7]
U.S. Department of Health and Human Services. Reducing the Health Consequences of Smoking: 25 years of Progress: A Report of Surgeon General US Department of Health and Human Services 1989; 89-8411.
[8]
Barbour SE, Nakashima K, Zhang JB, et al. Tobacco and smoking: environmental factors that modify the host response (immune system) and have an impact on periodontal health. Crit Rev Oral Biol Med 1997; 8(4): 437-60.
[http://dx.doi.org/10.1177/10454411970080040501] [PMID: 9391754]
[9]
Takeuchi M, Nakajima A, Yoshikawa K, et al. Effect of smoking on immunological functions of alveolar macrophages in mice Tobacco Counters Health. Macmilan Ltd 2000; pp. 168-71.
[10]
Fels AO, Cohn ZA. The alveolar macrophage. J Appl Physiol 1986; 60(2): 353-69.
[http://dx.doi.org/10.1152/jappl.1986.60.2.353] [PMID: 3005225]
[11]
Nagai S, Takeuchi M, Watanabe K, Aung H, Izumi T. Smoking and interleukin-1 activity released from human alveolar macrophages in healthy subjects. Chest 1988; 94(4): 694-700.
[http://dx.doi.org/10.1378/chest.94.4.694]
[12]
Akinori N, Takeshi T, Shunichi A, Susumu S, Hiroyasu I. lymphocyte subpopulations among passive smokers. Journal of American Medical Association(JAMA) 2004; 291(14): 1699-700.
[http://dx.doi.org/10.1001/jama.291.14.1699-b] [PMID: 15082696]
[13]
Nagai S, Takeuchi M, Izumi T. The effect of smoking on inflammation and immunological reaction in the lung. Saishin Igaku 1989; 44: 1388-93.
[14]
Takeuchi M, Nagai S, Izumi T. Effect of smoking on natural killer cell activity in the lung. Chest 1988; 94(4): 688-93.
[http://dx.doi.org/10.1378/chest.94.4.688]
[15]
Takeuchi M, Asada H, Nagai S. Effect of tobacco smoking on antigen presenting activity in alveolar macrophage. Clin Immunol 2005; 44: 546-50.
[16]
Ortega E, Barriga C, Rodríguez AB. Decline in the phagocytic function of alveolar macrophages from mice exposed to cigarette smoke. Comp Immunol Microbiol Infect Dis 1994; 17(1): 77-84.
[http://dx.doi.org/10.1016/0147-9571(94)90009-4] [PMID: 8004937]
[17]
Castro P, Legora-Machado A, Cardilo-Reis L, et al. Inhibition of interleukin-1beta reduces mouse lung inflammation induced by exposure to cigarette smoke. Eur J Pharmacol 2004; 498(1-3): 279-86.
[http://dx.doi.org/10.1016/j.ejphar.2004.07.047] [PMID: 15364006]
[18]
Proulx L, Paré G, Bissonnette E. Alveolar macrophage cytotoxic activity is inhibited by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK), a carcinogenic component of cigarette smoke. Cancer Immunol Immunother 2007; 56(6): 831-8.
[19]
Singh SP, Kalra R, Puttfarcken P, Kozak A, Tesfaigzi J, Sopori ML. Acute and chronic nicotine exposures modulate the immune system through different pathways. Toxicol Appl Pharmacol 2000; 164: 65-72.
[http://dx.doi.org/10.1006/taap.2000.8897] [PMID: 10739745]
[20]
Sopori ML, Cherian S, Chilukuri R, Shopp GM. Cigarette smoke causes inhibition of the immune response to intratracheally administered antigens. Toxicol Appl Pharmacol 1989; 97(3): 489-99.
[http://dx.doi.org/10.1016/0041-008X(89)90254-8] [PMID: 2609346]
[21]
Kalra R, Singh P, Savage M, Finch L, Sopori M. Effects of cigarette smoke on immune response: chronic exposure to cigarette smoke impairs antigen-mediated signaling in T cells and depletes IP3-sensitive Ca2+ stores. J Pharmacol Exp Ther 2000; 293(1): 166-71.
[22]
Kalra R, Singh P, Pena-Philippides C, Langley J, Razani-Boroujerdi S, Sopori M. Immunosuppressive and anti-inflammatory effects of nicotine administered by patch in an animal model. Clin Diagn Lab Immunol 2004; 11(3): 563-8.
[http://dx.doi.org/10.1128/CDLI.11.3.563-568.2004]
[23]
Takeuchi M, Nagai S, Nakajima A, et al. Inhibition of lung natural killer cell activity by smoking: the role of alveolar macrophages. Respiration 2001; 68(3): 262-7.
[http://dx.doi.org/10.1159/000050508] [PMID: 11416246]
[24]
Takeuchi M. Studies on the immunomodulation of Propionibacteriumacnes in mice. Japanese Journal of Allergology 1982; 31(7): 381-9.
[PMID: 7181661]
[25]
Witschi H, Uyeminami D, Moran D, Espiritu I. Chemoprevention of tobacco-smoke lung carcinogenesis in mice after cessation of smoke exposure. Carcinogenesis 2000; 21(5): 977-82.
[http://dx.doi.org/10.1093/carcin/21.5.977]
[26]
Moerloose B, Pauwels A, Joos F. Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am J Respir Crit Care Med 2005; 172(2): 168-72.
[http://dx.doi.org/10.1164/rccm.200409-1174OC]
[27]
Löfdahl M, Wahlström J, Sköld M. Different inflammatory cell pattern and macrophage phenotype in chronic obstructive pulmonary disease patients, smokers and non-smokers. Clin Exp Immunol 2006; 145(3): 428-37.
[http://dx.doi.org/10.1111/j.1365-2249.2006.03154.x]
[28]
Yu M, Zheng X, Witschi H, Pinkerton K. The role of interleukin-6 in pulmonary inflammation and injury induced by exposure to environmental air pollutants. Toxicol Sci 2002; 68(2): 488-97.
[29]
Vlahos R, Bozinovski S, Jones E, et al. Differential protease, innate immunity, and NF-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. Am J Physiol Lung Cell Mol Physiol 2006; 290(5): 931-45.
[30]
Polosukhin V, Manouilova L, Romberger J, et al. Ultrastructural heterogeneity of the alveolar macrophages from tobacco smokers with chronic bronchitis. Ultrastruct Pathol 2001; 25(1): 5-11.
[31]
Pratt A, Smith H, Ladman J, Finley N. The ultrastructure of alveolar macrophages from human cigarette smokers and nonsmokers. Lab Invest 1971; 24(5): 331-8.
[32]
Robbins S, Dawe E, Goncharova I, et al. Cigarette smoke decreases pulmonary dendritic cells and impacts antiviral immune responsiveness. Am J Respir Cell Mol Biol 2004; 30(2): 202-11.
[http://dx.doi.org/10.1165/rcmb.2003-0259OC]
[33]
Goud SN, Kaplan AM, Subbarao B. Effects of cigarette smoke on the antibody responses to thymic independent antigens from different lymphoid tissues of mice. Arch Toxicol 1992; 66(3): 164-9.
[http://dx.doi.org/10.1007/BF01974009] [PMID: 1497478]
[34]
Geng Y, Savage M, Razani-Boroujerdi S, Sopori M. Effects of nicotine on the immune response. II. Chronic nicotine treatment induces T cell anergy. J Immunol 1996; 156(7): 2384-90.
[35]
Sopori M, Kozak W, Savage M, et al. Effect of nicotine on the immune system: possible regulation of immune responses by central and peripheral mechanisms. Psychoneuroendocrinology 1998; 23(2): 189-204.
[http://dx.doi.org/10.1016/S0306-4530(97)00076-0]
[36]
Okazaki N. The suppressive effects of smoking on antibody production in experimental hypersensitivity pneumonitis in rabbits. Nihon Kyobu Shikkan Gakkai Zasshi 1991; 29(8): 943-53.
[37]
Moszczyński P, Zabiński Z, Moszczyński P Jr, Rutowski J, Słowiński S, Tabarowski Z. Immunological findings in cigarette smokers. Toxicol Lett 2001; 118(3): 121-7.
[http://dx.doi.org/10.1016/S0378-4274(00)00270-8]
[38]
Vassallo R, Tamada K, Lau S, Kroening R, Chen L. Cigarette smoke extract suppresses human dendritic cell function leading to preferential induction of Th-2 priming. J Immunol 2005; 175(4): 2684-91.
[39]
Ortega E, Hueso F, Collazos E, Pedrera I, Barriga C, Rodríguez B. Phagocytosis of latex beads by alveolar macrophages from mice exposed to cigarette smoke. Comp Immunol Microbiol Infect Dis 1992; 15(2): 137-42.
[http://dx.doi.org/10.1016/0147-9571(92)90113-6]
[40]
Chen H, Cowan J, Hasday D, Vogel N, Medvedev E. Tobacco smoking inhibits expression of proinflammatory cytokines and activation of IL-1R-associated kinase, p38, and NF-kappaB in alveolar macrophages stimulated with TLR2 and TLR4 agonists. J Immunol 2007; 179(9): 6097-106.
[41]
Izumi T, Nagai S, Takeuchi M, Shimizu Y. Effect of smoking on the immune responses and allergic disorders in the lung. JapJClinImmun 1988; 11: 315-21.
[http://dx.doi.org/10.2177/jsci.11.315]
[42]
Nagai S, Aung H, Takeuchi M, Kusume K, Izumi T. IL-1 and IL-1 inhibitory activity in the culture supernatants of alveolar macrophages from patients with interstitial lung diseases. Chest 1991; 99(3): 674-80.
[43]
Zhong Y, Zhou M, Joad P, Pinkerton K. Environmental tobacco smoke suppresses nuclear factor-kappaB signaling to increase apoptosis in infant monkey lungs. Am J Respir Crit Care Med 2006; 174(4): 428-36.
[44]
Arredondo J, Chernyavsky A, Jolkovsky D, Pinkerton K, Grando S. Receptor-mediated tobacco toxicity: alterations of the NF-kappaB expression and activity downstream of alpha7 nicotinic receptor in oral keratinocytes. Life Sci 2007; 80(24): 2191-4.
[45]
Arredondo J, Chernyavsky A, Jolkovsky D, Pinkerton K, Grando S. Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/MEK1/ERK and JAK-2/STAT-3 pathways downstream of alpha7 nicotinic receptor in oral keratinocytes. FASEB J 2006; 20(12): 2093-101.