RESEARCH PAPER
Comparison between cigarette smoke-induced emphysema and cigarette smoke extract-induced emphysema
Zhi-Hui He 1
,  
Ping Chen 2  
,  
Yan Chen 2, 3  
,  
Sheng-Dong He 2
,  
Ji-Ru Ye 2
,  
 
 
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1
Intensive Care Unit, the Second Xiangya Hospital, Central-South University, Changsha, China
2
Department of Respiratory Medicine, The Second Xiangya Hospital, Central-South University, Changsha, China
3
Division of Respiratory Disease, Department of Internal Medicine, The Second Xiangya Hospital, Central-South University, Changsha, China
4
Department of Respiratory Medicine, Hunan Provincial People’s Hospital, Changsha, China
CORRESPONDING AUTHOR
Ping Chen   

Department of Respiratory Medicine, The Second Xiangya Hospital, Central-South University, Changsha, Hunan 410011, China
Yan Chen   

Division of Respiratory Disease, Department of Internal Medicine, The Second Xiangya Hospital, Central-South University, Changsha, Hunan 410011, China
Publish date: 2015-03-25
 
Tobacco Induced Diseases 2015;13(March):6
KEYWORDS
ABSTRACT
Background:
Emphysema is the main pathological feature of COPD and also is the focus of the related research. Although several emphysema animal models have been established, exact comparison of findings is seldom. The present study aimed to compare cigarette smoke (CS) exposure-induced emphysema model and intraperitoneal injection of cigarette smoke extract (CSE)-induced emphysema model to evaluate the effectiveness of the two different modeling methods.

Methods:
Six-week-old male C57BL/6 J mice were used and randomly divided into two groups: CS exposure and intraperitoneal injection of CSE. Each group was subdivided into two subgroups: control and CS or CSE. Lung function, mean linear intercept (MLI), destructive index (DI), apoptotic index (AI), total and differential cells count in broncholavolar lavage fluid (BALF), SOD and IL-6 concentration in serum were measured.

Results:
Compared with their respective controls, lung function was significantly decreased in CS and CSE groups (P < 0.01); MLI, DI, and AI of lung tissue were significantly higher in CS and CSE groups (P < 0.01); total number of leukocytes, the number and percentage of neutrophils (NEUs), and the number of macrophages (MAC) in BALF were significantly higher in CS and CSE groups (P < 0.01); SOD concentration in serum was significantly decreased in CS and CSE groups (P < 0.01); IL-6 concentration in serum was significantly increased in in CS and CSE groups (P < 0.01). There was no significant difference between CS group and CSE group in any of the parameters described above.

Conclusions:
Both CS exposure and intraperitoneal injection of CSE could induce emphysema and the effectiveness of the two different modeling methods were equal.

 
REFERENCES (46)
1.
Fuschillo S, Martucci M, Donner CF, Balzano G. Airway bacterial colonization: the missing link between COPD and cardiovascular events? Respir Med. 2012;106:915–23.
 
2.
Miravitlles M. Cough and sputum production as risk factors for poor outcomes in patients with COPD. Respir Med. 2011;105:1118–28.
 
3.
Pryor WA, Stone K. Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci. 1993;686:12–27.
 
4.
Xu CB, Lei Y, Chen Q, Pehrson C, Larsson L, Edvinsson L. Cigarette smoke extracts promote vascular smooth muscle cell proliferation and enhances contractile responses in the vasculature and airway. Basic Clin Pharmacol Toxicol. 2010;107:940–8.
 
5.
Zhang H, Chen P, Zeng H, Zhang Y, Peng H, Chen Y, et al. Protective effect of demethylation treatment on cigarette smoke extract-induced mouse emphysema model. J Pharmacol Sci. 2013;123:159–66.
 
6.
He S, He Z, Chen Y, Ye J, Zong D, Zhang Y, et al. C-Kit/c-Kit ligand interaction of bone marrow endothelial progenitor cells is influenced in acigarette smoke extract-induced emphysema model. Exp Lung Res. 2013;39:258–67.
 
7.
World Medical Association; American Physiological Society. Guiding principles for research involving animals and human beings. Am J Physiol Regul Integr Comp Physiol. 2002;283:R281–3.
 
8.
Chen Y, Hanaoka M, Droma Y, Chen P, Voelkel NF, Kubo K. Endothelin-1 receptor antagonists prevent the development of pulmonary emphysema in rats. Eur Respir J. 2010;35:904–12.
 
9.
Zhang Y, Cao J, Chen Y, Chen P, Peng H, Cai S, et al. Intraperitoneal injection of cigarette smoke extract induced emphysema, and injury of cardiac and skeletal muscles in BALB/C mice. Exp Lung Res. 2013;39:18–31.
 
10.
Yao H, Chung S, Hwang JW, Rajendrasozhan S, Sundar IK, Dean DA, et al. SIRT1 protects against emphysema via FOXO3-mediated reduction of premature senescence in mice. J Clin Invest. 2012;122:2032–45.
 
11.
Chen Y, Hanaoka M, Chen P, Droma Y, Voelkel NF, Kubo K. Protective effect of beraprost sodium, a stable prostacyclin analog, in the development of cigarette smoke extract-induced emphysema. Am J Physiol Lung Cell Mol Physiol. 2009;296:L648–56.
 
12.
Vestbo J, Hurd SS, Agustí AG, Jones PW, Vogelmeier C, Anzueto A, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonarydisease: GOLD executive summary. Am J Respir Crit Care Med. 2013;187:347–65.
 
13.
Wright JL, Cosio M, Churg A. Animal models of chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol. 2008;295:L1–15.
 
14.
Ochs M. Estimating structural alterations in animal models of lung emphysema. Is there a gold standard? Ann Anat. 2014;196:26–33.
 
15.
American Thoracic Society. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1995;152:S77–121.
 
16.
Yang Q, Underwood MJ, Hsin MK, Liu XC, He GW. Dysfunction of pulmonary vascular endothelium in chronic obstructive pulmonary disease: basic considerations for future drug development. Curr Drug Metab. 2008;9:661–7.
 
17.
He Z, Chen Y, Chen P, Wu G, Cai S. Local inflammation occurs before systemic inflammation in patients with COPD. Respirology. 2010;15:478–84.
 
18.
Yao H, Rahman I. Current concepts on oxidative/carbonyl stress, inflammation and epigenetics in pathogenesis of chronic obstructive pulmonary disease. Toxicol Appl Pharmacol. 2011;254:72–85.
 
19.
Hillas G, Nikolakopoulou S, Hussain S, Vassilakopoulos T. Antioxidants and mucolytics in COPD management: when (if ever) and in whom? Curr Drug Targets. 2013;14:225–34.
 
20.
Yao H, Arunachalam G, Hwang JW, Chung S, Sundar IK, Kinnula VL, et al. Extracellular superoxide dismutase protects against pulmonary emphysema by attenuating oxidative fragmentation of ECM. Proc Natl Acad Sci U S A. 2010;107:15571–6.
 
21.
Biffl WL, Moore EE, Moore FA, Barnett Jr CC, Carl VS, Peterson VN. Interleukin-6 delays neutrophil apoptosis. Arch Surg. 1996;131:24–30.
 
22.
Yanbaeva DG, Dentener MA, Spruit MA, Houwing-Duistermaat JJ, Kotz D, Passos VL, et al. IL6 and CRP haplotypes are associated with COPD risk and systemic inflammation: a case–control study. BMC Med Genet. 2009;10:23.
 
23.
Ruwanpura SM, McLeod L, Miller A, Jones J, Bozinovski S, Vlahos R, et al. Interleukin-6 promotes pulmonary emphysema associated with apoptosis in mice. Am J Respir Cell Mol Biol. 2011;45:720–30.
 
24.
Bozinovski S, Hutchinson A, Thompson M, Macgregor L, Black J, Giannakis E, et al. Serum amyloid a is a biomarker of acute exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2008;177:269–78.
 
25.
Martin JG, Tamaoka M. Rat models of asthma and chronic obstructive lung disease. Pulm Pharmacol Ther. 2006;19:377–85.
 
26.
Brusselle GG, Bracke KR, Maes T, D’hulst AI, Moerloose KB, Joos GF, et al. Murine models of COPD. Pulm Pharmacol Ther. 2006;19:155–65.
 
27.
Plopper CG, Hyde DM. The non-human primate as a model for studying COPD and asthma. Pulm Pharmacol Ther. 2008;21:755–66.
 
28.
Chapman RW. Canine models of asthma and COPD. Pulm Pharmacol Ther. 2008;21:731–42.
 
29.
Abraham WM. Modeling of asthma, COPD and cystic fibrosis in sheep. Pulm Pharmacol Ther. 2008;21:743–54.
 
30.
Mahadeva R, Shapiro SD. Chronic obstructive pulmonary disease * 3: experimental animal models of pulmonary emphysema. Thorax. 2002;57:908–14.
 
31.
Wright JL, Churg A. Animal models of cigarette smoke-induced COPD. Chest. 2002;122(6 suppl):S301–6.
 
32.
Givi ME, Peck MJ, Boon L, Mortaz E. The role of dendritic cells in the pathogenesis of cigarette smoke-induced emphysema in mice. Eur J Pharmacol. 2013;721:259–66.
 
33.
Longhini-Dos-Santos N, Barbosa-de-Oliveira VA, Kozma RH, Faria CA, Stessuk T, Frei F, et al. Cell therapy with bone marrow mononuclear cells in elastase-induced pulmonary emphysema. Stem Cell Rev. 2013;9:210–8.
 
34.
Pera T, Zuidhof AB, Smit M, Menzen MH, Klein T, Flik G, et al. Arginase inhibition prevents inflammation and remodeling in a guinea pig model of chronic obstructive pulmonary disease. J Pharmacol Exp Ther. 2014;349:229–38.
 
35.
Wagner U, Staats P, Fehmann HC, Fischer A, Welte T, Groneberg DA. Analysis of airway secretions in a model of sulfur dioxide induced chronic obstructive pulmonary disease (COPD). J Occup Med Toxicol. 2006;1:12.
 
36.
Misaka S, Sato H, Yamauchi Y, Onoue S, Yamada S. Novel dry powder formulation of ovalbumin for development of COPD-like animal model: physicochemical characterization and biomarker profiling in rats. Eur J Pharm Sci. 2009;37:469–76.
 
37.
Tazaki G, Kondo T, Tajiri S, Tsuji C, Shioya S, Tanigaki T. Functional residual capacity and airway resistance in rats of COPD model induced by systemic hyaluronidase. Tokai J Exp Clin Med. 2006;31:125–7.
 
38.
Baron RM, Choi AJ, Owen CA, Choi AM. Genetically manipulated mouse models of lung disease: potential and pitfalls. Am J Physiol Lung Cell Mol Physiol. 2012;302:L485–97.
 
39.
Taraseviciene-Stewart L, Scerbavicius R, Choe KH, Moore M, Sullivan A, Nicolls MR, et al. An animal model of autoimmune emphysema. Am J Respir Crit Care Med. 2005;171:734–42.
 
40.
Pennisi E. Genomics: sequence tells mouse, human genome secrets. Science. 2002;298:1863–5.
 
41.
Jeong YY, Park HJ, Cho YW, Kim EJ, Kim GT, Mun YJ, et al. Aged red garlic extract reduces cigarette smoke extract-induced cell death in human bronchial smooth muscle cells by increasing intracellular glutathione levels. Phytother Res. 2012;26:18–25.
 
42.
Tzortzaki EG, Papi A, Neofytou E, Soulitzis N, Siafakas NM. Immune and genetic mechanisms in COPD: possible targets for therapeutic interventions. Curr Drug Targets. 2013;14:141–8.
 
43.
He ZH, Chen P, Chen Y, Zhu YQ, He SD, Ye JR, et al. Dual effects of cigarette smoke extract on proliferation of endothelial progenitor cells and the protective effect of 5-aza-2’-deoxycytidine on EPCs against the damage caused by CSE. BioMed Res Int. 2014;2014:640752.
 
44.
Nana-Sinkam SP, Lee JD, Sotto-Santiago S, Stearman RS, Keith RL, Choudhury Q, et al. Prostacyclin prevents pulmonary endothelial cell apoptosis induced by cigarette smoke. Am J Respir Crit Care Med. 2007;175:676–85.
 
45.
Taraseviciene-Stewart L, Kraskauskas D, Lee JH, Hanaoka M, Burns N, Parr J, et al. Cigarette smoke extract (CSE)-induced emphysema in mice. Am J Respir Crit Care Med. 2007;175:A529.
 
46.
Yao H, Edirisinghe I, Rajendrasozhan S, Yang SR, Caito S, Adenuga D, et al. Cigarette smoke-mediated inflammatory and oxidative responses are strain-dependent in mice. Am J Physiol Lung Cell Mol Physiol. 2008;294:L1174–86.
 
 
CITATIONS (15):
1.
Tumor necrosis factor-like weak inducer of apoptosis regulates quadriceps muscle atrophy and fiber-type alteration in a rat model of chronic obstructive pulmonary disease
Jun-Juan Lu, Qing Wang, Li Hua Xie, Qiang Zhang, Sheng Hua Sun
Tobacco Induced Diseases
 
2.
miR-34a is involved in CSE-induced apoptosis of human pulmonary microvascular endothelial cells by targeting Notch-1 receptor protein
Ying-Jiao Long, Xiao-Peng Liu, Shan-Shan Chen, Dan-Dan Zong, Yan Chen, Ping Chen
Respiratory Research
 
3.
PTEN/PI3k/AKT Regulates Macrophage Polarization in Emphysematous mice
J. Lu, L. Xie, C. Liu, Q. Zhang, S. Sun
Scandinavian Journal of Immunology
 
4.
l-Menthol alleviates cigarette smoke extract induced lung injury in rats by inhibiting oxidative stress and inflammation via nuclear factor kappa B, p38 MAPK and Nrf2 signalling pathways
Yan Liu, Ang Li, Xiuli Feng, Xiaoyan Jiang, Xiao Sun, Weizhen Huang, Xiaosong Zhu, Zhongxi Zhao
RSC Advances
 
5.
Pharmacological Investigation of the Anti-Inflammation and Anti-Oxidation Activities of Diallyl Disulfide in a Rat Emphysema Model Induced by Cigarette Smoke Extract
Yan Liu, Ang Li, Xiuli Feng, Xiao Sun, Xiaosong Zhu, Zhongxi Zhao
Nutrients
 
6.
MicroRNA-21 aggravates chronic obstructive pulmonary disease by promoting autophagy
Zhengpeng Zeng, ShengYang He, JunJuan Lu, Chun Liu, Hua Lin, ChaoQun Xu, LiHua Xie, ShengHua Sun
Experimental Lung Research
 
7.
Tobacco-Free Cigarette Smoke Exposure Induces Anxiety and Panic-Related Behaviours in Male Wistar Rats
Máira Tereza Talma Chírico, Frank Silva Bezerra, Mariana Reis Guedes, Ana Beatriz Souza, Fernanda Cacilda Silva, Glenda Campos, Sylvana Rendeiro de Noronha, Laura Batista Tavares Mesquita, Thayane Oliveira Reis, Silvia Dantas Cangussú, Deoclécio Alves Chianca-Jr, Rodrigo Cunha de Menezes
Scientific Reports
 
8.
Protective effect of methylallyl sulfone in the development of cigarette smoke extract-induced apoptosis in rats and HFL-1 cells
Ang Li, Yan Liu, Xiaosong Zhu, Xiao Sun, Xiuli Feng, Dawei Li, Jiangqiang Zhang, Meihua Zhu, Zhongxi Zhao
Biochemical and Biophysical Research Communications
 
9.
A Novel Murine Chronic Obstructive Pulmonary Disease Model and the Pathogenic Role of MicroRNA-21
Shengyang He, Liqiu Li, Shenghua Sun, Zhengpeng Zeng, Junjuan Lu, Lihua Xie
Frontiers in Physiology
 
10.
Methylallyl sulfone attenuates inflammation, oxidative stress and lung injury induced by cigarette smoke extract in mice and RAW264.7 cells
Ang Li, Yan Liu, Xiaosong Zhu, Xiao Sun, Xiuli Feng, Dawei Li, Jiangqiang Zhang, Meihua Zhu, Zhongxi Zhao
International Immunopharmacology
 
11.
Endothelial Progenitor Cells as Pathogenetic and Diagnostic Factors, and Potential Targets for GLP-1 in Combination with Metabolic Syndrome and Chronic Obstructive Pulmonary Disease
Evgenii Skurikhin, Olga Pershina, Angelina Pakhomova, Edgar Pan, Vyacheslav Krupin, Natalia Ermakova, Olga Vaizova, Anna Pozdeeva, Mariia Zhukova, Viktoriia Skurikhina, Wolf-Dieter Grimm, Alexander Dygai
International Journal of Molecular Sciences
 
12.
Notch promotes DNMT-mediated hypermethylation of Klotho leads to COPD-related inflammation
Jie Qiu, Ya-Nan Zhang, Xiwei Zheng, Peng Zhang, Gang Ma, Hai Tan
Experimental Lung Research
 
13.
Correlation analysis between depression and family fitness in chronic obstructive pulmonary disease inpatients
Xuexue Deng, Jinping Song
Medicine
 
14.
Lycopene mitigates pulmonary emphysema induced by cigarette smoke in a murine model
Keila Campos, Oliveira de, Thais Martins, Guilherme Costa, André Talvani, Camila Garcia, Laser Oliveira, Sílvia Cangussú, Daniela Costa, Frank Bezerra
The Journal of Nutritional Biochemistry
 
15.
Ergosterol attenuates cigarette smoke extract-induced COPD by modulating inflammation, oxidative stress and apoptosis in vitro and in vivo
Xiao Sun, Xiuli Feng, Dandan Zheng, Ang Li, Chunyan Li, Siying Li, Zhongxi Zhao
Clinical Science
 
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