Cigarette smoke increases susceptibility to tuberculosis-evidence from in vivo and in vitro models

Shaobin Shang, Diane Ordway, Marcela Henao-Tamayo, Xiyuan Bai, Rebecca Oberley-Deegan, Crystal Shanley, Ian M. Orme, Stephanie Case, Maisha Minor, David Ackart, Laurel Hascall-Dove, Alida R. Ovrutsky, Pitchaimani Kandasamy, Dennis R. Voelker, Cherie Lambert, Brian M. Freed, Michael D. Iseman, Randall J. Basaraba, Edward D. Chan

Research output: Contribution to journalArticle

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Abstract

Background: Cigarette smoke (CS) exposure is an epidemiological risk factor for tuberculosis, although the biological basis has not been elucidated. Methods: We exposed C57BL/6 mice to CS for 14 weeks and examined their ability to control an aerosol infection of Mycobacterium tuberculosis Erdman. Results: CS-exposed mice had more M. tuberculosis isolated from the lungs and spleens after 14 and 30 d, compared with control mice. The CS-exposed mice had worse lung lesions and less lung and splenic macrophages and dendritic cells (DCs) producing interleukin12 and tumor necrosis factor α (TNF-α'). There were significantly more interleukin 10-producing macrophages and DCs in the spleens of infected CS-exposed mice than in non-CS-exposed controls. CS-exposed mice also showed a diminished influx of interferon γ-producing and TNF-α-producing CD4+ and CD8+ effector and memory T cells into the lungs and spleens. There was a trend toward an increased number of viable intracellular M. tuberculosis in macrophages isolated from humans who smoke compared with nonsmokers. THP-1 human macrophages and primary human alveolar macrophages exposed to CS extract, nicotine, or acrolein showed an increased burden of intracellular M. tuberculosis. Conclusion: CS suppresses the protective immune response to M. tuberculosis in mice, human THP-1 cells, and primary human alveolar macrophages.

Original languageEnglish (US)
Pages (from-to)1240-1248
Number of pages9
JournalJournal of Infectious Diseases
Volume203
Issue number9
DOIs
StatePublished - May 1 2011

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Smoke
Tobacco Products
Tuberculosis
Mycobacterium tuberculosis
Macrophages
Lung
Spleen
Alveolar Macrophages
Dendritic Cells
In Vitro Techniques
Acrolein
Infection Control
Aerosols
Nicotine
Inbred C57BL Mouse
Interleukin-10
Interferons
Tumor Necrosis Factor-alpha
T-Lymphocytes

ASJC Scopus subject areas

  • Immunology and Allergy
  • Infectious Diseases

Cite this

Cigarette smoke increases susceptibility to tuberculosis-evidence from in vivo and in vitro models. / Shang, Shaobin; Ordway, Diane; Henao-Tamayo, Marcela; Bai, Xiyuan; Oberley-Deegan, Rebecca; Shanley, Crystal; Orme, Ian M.; Case, Stephanie; Minor, Maisha; Ackart, David; Hascall-Dove, Laurel; Ovrutsky, Alida R.; Kandasamy, Pitchaimani; Voelker, Dennis R.; Lambert, Cherie; Freed, Brian M.; Iseman, Michael D.; Basaraba, Randall J.; Chan, Edward D.

In: Journal of Infectious Diseases, Vol. 203, No. 9, 01.05.2011, p. 1240-1248.

Research output: Contribution to journalArticle

Shang, S, Ordway, D, Henao-Tamayo, M, Bai, X, Oberley-Deegan, R, Shanley, C, Orme, IM, Case, S, Minor, M, Ackart, D, Hascall-Dove, L, Ovrutsky, AR, Kandasamy, P, Voelker, DR, Lambert, C, Freed, BM, Iseman, MD, Basaraba, RJ & Chan, ED 2011, 'Cigarette smoke increases susceptibility to tuberculosis-evidence from in vivo and in vitro models', Journal of Infectious Diseases, vol. 203, no. 9, pp. 1240-1248. https://doi.org/10.1093/infdis/jir009
Shang, Shaobin ; Ordway, Diane ; Henao-Tamayo, Marcela ; Bai, Xiyuan ; Oberley-Deegan, Rebecca ; Shanley, Crystal ; Orme, Ian M. ; Case, Stephanie ; Minor, Maisha ; Ackart, David ; Hascall-Dove, Laurel ; Ovrutsky, Alida R. ; Kandasamy, Pitchaimani ; Voelker, Dennis R. ; Lambert, Cherie ; Freed, Brian M. ; Iseman, Michael D. ; Basaraba, Randall J. ; Chan, Edward D. / Cigarette smoke increases susceptibility to tuberculosis-evidence from in vivo and in vitro models. In: Journal of Infectious Diseases. 2011 ; Vol. 203, No. 9. pp. 1240-1248.
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abstract = "Background: Cigarette smoke (CS) exposure is an epidemiological risk factor for tuberculosis, although the biological basis has not been elucidated. Methods: We exposed C57BL/6 mice to CS for 14 weeks and examined their ability to control an aerosol infection of Mycobacterium tuberculosis Erdman. Results: CS-exposed mice had more M. tuberculosis isolated from the lungs and spleens after 14 and 30 d, compared with control mice. The CS-exposed mice had worse lung lesions and less lung and splenic macrophages and dendritic cells (DCs) producing interleukin12 and tumor necrosis factor α (TNF-α'). There were significantly more interleukin 10-producing macrophages and DCs in the spleens of infected CS-exposed mice than in non-CS-exposed controls. CS-exposed mice also showed a diminished influx of interferon γ-producing and TNF-α-producing CD4+ and CD8+ effector and memory T cells into the lungs and spleens. There was a trend toward an increased number of viable intracellular M. tuberculosis in macrophages isolated from humans who smoke compared with nonsmokers. THP-1 human macrophages and primary human alveolar macrophages exposed to CS extract, nicotine, or acrolein showed an increased burden of intracellular M. tuberculosis. Conclusion: CS suppresses the protective immune response to M. tuberculosis in mice, human THP-1 cells, and primary human alveolar macrophages.",
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AU - Ordway, Diane

AU - Henao-Tamayo, Marcela

AU - Bai, Xiyuan

AU - Oberley-Deegan, Rebecca

AU - Shanley, Crystal

AU - Orme, Ian M.

AU - Case, Stephanie

AU - Minor, Maisha

AU - Ackart, David

AU - Hascall-Dove, Laurel

AU - Ovrutsky, Alida R.

AU - Kandasamy, Pitchaimani

AU - Voelker, Dennis R.

AU - Lambert, Cherie

AU - Freed, Brian M.

AU - Iseman, Michael D.

AU - Basaraba, Randall J.

AU - Chan, Edward D.

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N2 - Background: Cigarette smoke (CS) exposure is an epidemiological risk factor for tuberculosis, although the biological basis has not been elucidated. Methods: We exposed C57BL/6 mice to CS for 14 weeks and examined their ability to control an aerosol infection of Mycobacterium tuberculosis Erdman. Results: CS-exposed mice had more M. tuberculosis isolated from the lungs and spleens after 14 and 30 d, compared with control mice. The CS-exposed mice had worse lung lesions and less lung and splenic macrophages and dendritic cells (DCs) producing interleukin12 and tumor necrosis factor α (TNF-α'). There were significantly more interleukin 10-producing macrophages and DCs in the spleens of infected CS-exposed mice than in non-CS-exposed controls. CS-exposed mice also showed a diminished influx of interferon γ-producing and TNF-α-producing CD4+ and CD8+ effector and memory T cells into the lungs and spleens. There was a trend toward an increased number of viable intracellular M. tuberculosis in macrophages isolated from humans who smoke compared with nonsmokers. THP-1 human macrophages and primary human alveolar macrophages exposed to CS extract, nicotine, or acrolein showed an increased burden of intracellular M. tuberculosis. Conclusion: CS suppresses the protective immune response to M. tuberculosis in mice, human THP-1 cells, and primary human alveolar macrophages.

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