Skip to main content
Top
Published in: Respiratory Research 1/2016

Open Access 01-12-2016 | Research

Induction of pulmonary antibodies against oxidized lipids in mice exposed to cigarette smoke

Authors: Danya Thayaparan, Pamela Shen, Martin R. Stämpfli, Mathieu C. Morissette

Published in: Respiratory Research | Issue 1/2016

Login to get access

Abstract

Background

Chronic cigarette smoke exposure is known to activate the adaptive immune system; however, the functional role of these processes is currently unknown. Given the role of oxidized lipids in driving innate inflammatory responses to cigarette smoke, we investigated whether an adaptive immune response against damaged lipids was induced following chronic cigarette smoke exposure.

Methods and results

Using a well-established mouse model, we showed that cigarette smoke exposure led to a progressive increase in pulmonary antibodies against oxidized low-density lipoprotein (OxLDL). Functionally, we found that intranasal delivery of an antibody against oxidized phosphatidylcholine (anti-OxPC; clone E06) increased lipid and particle uptake by pulmonary macrophages without exacerbating cigarette smoke-induced neutrophilia. We also found that anti-OxPC treatment increased particle uptake following smoking cessation. Finally, the frequency of pulmonary macrophages with internalized particles was increased after prolonged smoke exposure, at which time lung anti-OxPC responses were highest.

Conclusions

Altogether, this is the first report to demonstrate a non-pathogenic, and possibly protective, function of a newly identified autoantibody induced by chronic cigarette smoke exposure.
Literature
1.
go back to reference Hogg JC, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004;350:2645–53.CrossRefPubMed Hogg JC, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med. 2004;350:2645–53.CrossRefPubMed
2.
go back to reference Bracke KR, et al. Role of CXCL13 in cigarette smoke-induced lymphoid follicle formation and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2013;188:343–55.CrossRefPubMed Bracke KR, et al. Role of CXCL13 in cigarette smoke-induced lymphoid follicle formation and chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2013;188:343–55.CrossRefPubMed
3.
go back to reference Morissette MC, et al. Persistence of pulmonary tertiary lymphoid tissues and anti-nuclear antibodies following cessation of cigarette smoke exposure. Respir Res. 2014;15:49.CrossRefPubMedPubMedCentral Morissette MC, et al. Persistence of pulmonary tertiary lymphoid tissues and anti-nuclear antibodies following cessation of cigarette smoke exposure. Respir Res. 2014;15:49.CrossRefPubMedPubMedCentral
4.
go back to reference Randall TD. Bronchus-associated lymphoid tissue (BALT) structure and function. Adv Immunol. 2010;107:187–241.CrossRefPubMed Randall TD. Bronchus-associated lymphoid tissue (BALT) structure and function. Adv Immunol. 2010;107:187–241.CrossRefPubMed
7.
go back to reference Motz GT, et al. Persistence of lung CD8 T cell oligoclonal expansions upon smoking cessation in a mouse model of cigarette smoke-induced emphysema. J Immunol. 2008;181:8036–43.CrossRefPubMed Motz GT, et al. Persistence of lung CD8 T cell oligoclonal expansions upon smoking cessation in a mouse model of cigarette smoke-induced emphysema. J Immunol. 2008;181:8036–43.CrossRefPubMed
8.
go back to reference Rinaldi M, et al. Antielastin B-cell and T-cell immunity in patients with chronic obstructive pulmonary disease. Thorax. 2012;67(8):694–700.CrossRefPubMed Rinaldi M, et al. Antielastin B-cell and T-cell immunity in patients with chronic obstructive pulmonary disease. Thorax. 2012;67(8):694–700.CrossRefPubMed
9.
go back to reference Lee SH, et al. Antielastin autoimmunity in tobacco smoking-induced emphysema. Nat Med. 2007;13:567–9.CrossRefPubMed Lee SH, et al. Antielastin autoimmunity in tobacco smoking-induced emphysema. Nat Med. 2007;13:567–9.CrossRefPubMed
10.
go back to reference Morissette M C, Shen P, Thayaparan D, Stampfli M R. Disruption of pulmonary lipid homeostasis drives cigarette smoke-induced lung inflammation in mice. Eur Respir J. 2015;46(5):1451–60.CrossRefPubMed Morissette M C, Shen P, Thayaparan D, Stampfli M R. Disruption of pulmonary lipid homeostasis drives cigarette smoke-induced lung inflammation in mice. Eur Respir J. 2015;46(5):1451–60.CrossRefPubMed
12.
go back to reference van Leeuwen M, Damoiseaux J, Duijvestijn A, Tervaert JW. The therapeutic potential of targeting B cells and anti-oxLDL antibodies in atherosclerosis. Autoimmun Rev. 2009;9:53–7.CrossRefPubMed van Leeuwen M, Damoiseaux J, Duijvestijn A, Tervaert JW. The therapeutic potential of targeting B cells and anti-oxLDL antibodies in atherosclerosis. Autoimmun Rev. 2009;9:53–7.CrossRefPubMed
13.
go back to reference Ammirati E, Moroni F, Magnoni M, Camici PG. The role of T and B cells in human atherosclerosis and atherothrombosis. Clin Exp Immunol. 2015;179:173–87.CrossRefPubMedPubMedCentral Ammirati E, Moroni F, Magnoni M, Camici PG. The role of T and B cells in human atherosclerosis and atherothrombosis. Clin Exp Immunol. 2015;179:173–87.CrossRefPubMedPubMedCentral
16.
go back to reference Botelho FM, et al. Innate immune processes are sufficient for driving cigarette smoke-induced inflammation in mice. Am J Respir Cell Mol Biol. 2010;42:394–403.CrossRefPubMed Botelho FM, et al. Innate immune processes are sufficient for driving cigarette smoke-induced inflammation in mice. Am J Respir Cell Mol Biol. 2010;42:394–403.CrossRefPubMed
17.
go back to reference Morissette MC, Shen P, Thayaparan D, Stampfli MR. Impacts of peroxisome proliferator-activated receptor-gamma activation on cigarette smoke-induced exacerbated response to bacteria. Eur Respir J. 2015;45:191–200.CrossRefPubMed Morissette MC, Shen P, Thayaparan D, Stampfli MR. Impacts of peroxisome proliferator-activated receptor-gamma activation on cigarette smoke-induced exacerbated response to bacteria. Eur Respir J. 2015;45:191–200.CrossRefPubMed
18.
go back to reference Botelho FM, et al. IL-1alpha/IL-1R1 expression in chronic obstructive pulmonary disease and mechanistic relevance to smoke-induced neutrophilia in mice. PLoS One. 2011;6:e28457.CrossRefPubMedPubMedCentral Botelho FM, et al. IL-1alpha/IL-1R1 expression in chronic obstructive pulmonary disease and mechanistic relevance to smoke-induced neutrophilia in mice. PLoS One. 2011;6:e28457.CrossRefPubMedPubMedCentral
19.
go back to reference Barnes PJ. Alveolar macrophages in chronic obstructive pulmonary disease (COPD). Cell Mol Biol (Noisy-le-Grand). 2004;50(Online Pub):OL627–37. Barnes PJ. Alveolar macrophages in chronic obstructive pulmonary disease (COPD). Cell Mol Biol (Noisy-le-Grand). 2004;50(Online Pub):OL627–37.
20.
go back to reference Kantor AB, Merrill CE, Herzenberg LA, Hillson JL. An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J Immunol. 1997;158:1175–86.PubMed Kantor AB, Merrill CE, Herzenberg LA, Hillson JL. An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells. J Immunol. 1997;158:1175–86.PubMed
21.
go back to reference Shaw PX, et al. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest. 2000;105:1731–40.CrossRefPubMedPubMedCentral Shaw PX, et al. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest. 2000;105:1731–40.CrossRefPubMedPubMedCentral
22.
23.
go back to reference Miller YI, et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235–48.CrossRefPubMedPubMedCentral Miller YI, et al. Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235–48.CrossRefPubMedPubMedCentral
24.
go back to reference Harishchandra RK, Saleem M, Galla HJ. Nanoparticle interaction with model lung surfactant monolayers. J R Soc Interface. 2010;7 Suppl 1:S15–26.CrossRefPubMed Harishchandra RK, Saleem M, Galla HJ. Nanoparticle interaction with model lung surfactant monolayers. J R Soc Interface. 2010;7 Suppl 1:S15–26.CrossRefPubMed
25.
go back to reference Dwivedi MV, Harishchandra RK, Koshkina O, Maskos M, Galla HJ. Size influences the effect of hydrophobic nanoparticles on lung surfactant model systems. Biophys J. 2014;106:289–98.CrossRefPubMedPubMedCentral Dwivedi MV, Harishchandra RK, Koshkina O, Maskos M, Galla HJ. Size influences the effect of hydrophobic nanoparticles on lung surfactant model systems. Biophys J. 2014;106:289–98.CrossRefPubMedPubMedCentral
26.
go back to reference Marathe GK, Prescott SM, Zimmerman GA, McIntyre TM. Oxidized LDL contains inflammatory PAF-like phospholipids. Trends Cardiovasc Med. 2001;11:139–42.CrossRefPubMed Marathe GK, Prescott SM, Zimmerman GA, McIntyre TM. Oxidized LDL contains inflammatory PAF-like phospholipids. Trends Cardiovasc Med. 2001;11:139–42.CrossRefPubMed
27.
go back to reference Nakanaga K, Hama K, Aoki J. Autotaxin--an LPA producing enzyme with diverse functions. J Biochem. 2010;148:13–24.CrossRefPubMed Nakanaga K, Hama K, Aoki J. Autotaxin--an LPA producing enzyme with diverse functions. J Biochem. 2010;148:13–24.CrossRefPubMed
28.
go back to reference Oikonomou N, et al. Pulmonary autotaxin expression contributes to the pathogenesis of pulmonary fibrosis. Am J Respir Cell Mol Biol. 2012;47:566–74.CrossRefPubMed Oikonomou N, et al. Pulmonary autotaxin expression contributes to the pathogenesis of pulmonary fibrosis. Am J Respir Cell Mol Biol. 2012;47:566–74.CrossRefPubMed
29.
go back to reference Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci. 1993;686:12–27. discussion 27.CrossRefPubMed Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci. 1993;686:12–27. discussion 27.CrossRefPubMed
30.
go back to reference Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med. 2009;360:2445–54.CrossRefPubMed Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med. 2009;360:2445–54.CrossRefPubMed
31.
go back to reference Faner, R. et al. Network Analysis of Lung Transcriptomics Reveals a Distinct B Cell Signature in Emphysema. Am J Respir Crit Care Med. 2016;193(11):1242–53.CrossRefPubMed Faner, R. et al. Network Analysis of Lung Transcriptomics Reveals a Distinct B Cell Signature in Emphysema. Am J Respir Crit Care Med. 2016;193(11):1242–53.CrossRefPubMed
Metadata
Title
Induction of pulmonary antibodies against oxidized lipids in mice exposed to cigarette smoke
Authors
Danya Thayaparan
Pamela Shen
Martin R. Stämpfli
Mathieu C. Morissette
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2016
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-016-0416-6

Other articles of this Issue 1/2016

Respiratory Research 1/2016 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.