Transcriptomic analysis of lung tissue from cigarette smoke-induced emphysema murine models and human chronic obstructive pulmonary disease show shared and distinct pathways

American Journal of Respiratory Cell and Molecular Biology

Volumn 57, Issue 1, 2017, Pages 47-58

  Yun, Jeong H ^a   Morrow, Jarrett ^a   Owen, Caroline A ^a,b   Qiu, Weiliang ^a   Glass, Kimberly ^a   Lao, Taotao ^a   Jiang, Zhiqiang ^a   Perrella, Mark A ^a   Silverman, Edwin K ^a   Zhou, Xiaobo ^a   Hersh, Craig P ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

Author keywords

Chronic obstructive pulmonary disease; Cigarette smoking; Gene expression; Mouse model

Indexed keywords

ACYL COENZYME A OXIDASE 2 BRANCHED CHAIN; AROMATIC HYDROCARBON RECEPTOR; ATP BINDING CASSETTE SUBFAMILY B PROTEIN; CIGARETTE SMOKE; CXCL17 PROTEIN; CYTOCHROME P450 1B1; EPHRIN RECEPTOR; FAM13A PROTEIN; GLUTATHIONE PEROXIDASE 2; GLUTATHIONE TRANSFERASE P1; HERPESVIRUS ENTRY MEDIATOR LIGAND; HHIP PROTEIN; KAT14 PROTEIN; NQO1 PROTEIN; PROTEIN; PYRIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR NRF2; UGT1A6A PROTEIN; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CELL DEATH; CELL SURVIVAL; CHOLESTEROL SYNTHESIS; CHRONIC OBSTRUCTIVE LUNG DISEASE; CIGARETTE SMOKE-INDUCED EMPHYSEMA; COMPARATIVE STUDY; CONNECTIVE TISSUE DISEASE; CONTROLLED STUDY; DISEASE SEVERITY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC MODEL; GENOTYPE; HISTOLOGY; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; KETOLYSIS; LIPID METABOLISM; LUNG PARENCHYMA; LYSIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SMOKING; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTOMICS; UPREGULATION; WILD TYPE; XENOBIOTIC METABOLISM; ADVERSE EFFECTS; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; LUNG; METABOLISM; PATHOLOGY; PHENOTYPE; PROCEDURES; PULMONARY EMPHYSEMA;

ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LUNG; MICE, INBRED C57BL; MODELS, GENETIC; OXIDATIVE STRESS; PHENOTYPE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; PULMONARY EMPHYSEMA; SIGNAL TRANSDUCTION; SMOKING; XENOBIOTICS;

EID: 85020234600     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2016-0328OC     Document Type: Article

References (51)

1. Mannino DM, Buist AS. Global burden of COPD: risk factors, prevalence, and future trends. Lancet 2007;370:765-773
2. Mannino D. The natural history of chronic obstructive pulmonary disease. Pneumonol Alergol Pol2011;79:139-143
3. Lundback B, Lindberg A, Lindstrom M, Ronmark E, Jonsson AC, Jonsson E, Larsson LG, Andersson S, Sandstrom T, Larsson K; Obstructive Lung Disease in Northern Sweden Studies. Not 15 but 50% of smokers develop COPD?-Report from the Obstructive Lung Disease in Northern Sweden Studies. Respir Med 2003;97:115-122
4. Silverman EK, Chapman HA, Drazen JM, Weiss ST, Rosner B, Campbell EJ, O'Donnell WJ, Reilly JJ, Ginns L, Mentzer S, et al. Genetic epidemiology of severe, early-onset chronic obstructive pulmonary disease: risk to relatives for airflow obstruction and chronic bronchitis. Am J Respir Crit Care Med 1998;157: 1770-1778
5. Berndt A, Leme AS, Shapiro SD. Emerging genetics of COPD. EMBO Mol Med 2012;4:1144-1155
6. Leberl M, Kratzer A, Taraseviciene-Stewart L. Tobacco smoke induced COPD/emphysema in the animal model-are we all on the same page? Front Physiol 2013;4:91
7. Lao T, Glass K, Qiu W, Polverino F, Gupta K, Morrow J, Mancini JD, Vuong L, Perrella MA, Hersh CP, et al. Haploinsufficiency of Hedgehog interacting protein causes increased emphysema induced by cigarette smoke through network rewiring. Genome Med 2015;7:12
8. Jiang Z, Lao T, Qiu W, Polverino F, Gupta K, Guo F, Mancini JD, Naing ZZC, Cho MH, Castaldi PJ, et al. A chronic obstructive pulmonary disease susceptibility gene, FAM13A, regulates protein stability of b-catenin. Am J Respir Crit Care Med 2016;194: 185-197
9. Guerassimov A, Hoshino Y, Takubo Y, Turcotte A, Yamamoto M, Ghezzo H, Triantafillopoulos A, Whittaker K, Hoidal JR, Cosio MG. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am J Respir Crit Care Med 2004;170: 974-980
10. Foronjy RF, Mercer BA, Maxfield MW, Powell CA, D'Armiento J, Okada Y. Structural emphysema does not correlate with lung compliance: lessons from the mouse smoking model. Exp Lung Res 2005;31:547-562
11. Laucho-Contreras ME, Taylor KL, Mahadeva R, Boukedes SS, Owen CA. Automated measurement of pulmonary emphysema and small airway remodeling in cigarette smoke-exposed mice. J Vis Exp 2015; (95):52236
12. Morrow JD, Cho MH, Hersh CP, Pinto-Plata V, Celli B, Marchetti N, Criner G, Bueno R, Washko G, Glass K, et al. DNA methylation profiling in human lung tissue identifies genes associated with COPD. Epigenetics 2016;11:1-10
13. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007; 8:118-127
14. Ritchie MD, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research 2015;43:e47
15. Benjamini YHY. Controlling the false discovery rate: α practical and powerful approach to multiple testing. J R Stat Soc B 1995;57: 289-300
16. Wang J, Duncan D, Shi Z, Zhang B. WEB-based gene set analysis toolkit (WebGestalt): update 2013. Nucleic Acids Res 2013; 41(web server issue):W77-W83
17. Cavarra E, Fardin P, Fineschi S, Ricciardi A, De Cunto G, Sallustio F, Zorzetto M, Luisetti M, Pfeffer U, Lungarella G, et al. Early response of gene clusters is associated with mouse lung resistance or sensitivity to cigarette smoke. Am J Physiol Lung Cell Mol Physiol 2009;296:L418-L429
18. Morrow JD, Zhou X, Lao T, Jiang Z, DeMeo DL, Cho MH, Qiu W, Cloonan S, Pinto-Plata V, Celli B, et al. Functional interactors of three genome-wide association study genes are differentially expressed in severe chronic obstructive pulmonary disease lung tissue. Sci Rep 2017;7:44232
19. BosséY, Postma DS, Sin DD, Lamontagne M, Couture C, Gaudreault N, Joubert P,Wong V, ElliottM, van den Berge M, et al.Molecular signature of smoking in human lung tissues. Cancer Res 2012;72:3753-3763
20. Wright JL, Cosio M, Churg A. Animal models of chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 2008;295: L1-L15
21. Izzotti A, Cartiglia C, Longobardi M, Bagnasco M, Merello A, You M, Lubet RA, De Flora S. Gene expression in the lung of p53 mutant mice exposed to cigarette smoke. Cancer Res 2004;64: 8566-8572
22. Izzotti A, Cartiglia C, Longobardi M, Balansky RM, D'Agostini F, Lubet RA, De Flora S. Alterations of gene expression in skin and lung of mice exposed to light and cigarette smoke. FASEB J 2004;18: 1559-1561
23. Meng QR, Gideon KM, Harbo SJ, Renne RA, Lee MK, Brys AM, Jones R. Gene expression profiling in lung tissues from mice exposed to cigarette smoke, lipopolysaccharide, or smoke plus lipopolysaccharide by inhalation. Inhal Toxicol 2006;18:555-568
24. Halappanavar S, Russell M, Stampfli MR, Williams A, Yauk CL. Induction of the interleukin 6/signal transducer and activator of transcription pathway in the lungs of mice sub-chronically exposed to mainstream tobacco smoke. BMC Med Genomics 2009;2:56
25. Agarwal AR, Zhao L, Sancheti H, Sundar IK, Rahman I, Cadenas E. Short-term cigarette smoke exposure induces reversible changes in energy metabolism and cellular redox status independent of inflammatory responses in mouse lungs. Am J Physiol Lung Cell Mol Physiol 2012;303:L889-L898
26. Morissette MC, Lamontagne M, BérubéJC, Gaschler G, Williams A, Yauk C, Couture C, Laviolette M, Hogg JC, Timens W, et al. Impact of cigarette smoke on the human and mouse lungs: α geneexpression comparison study. PLoS One 2014;9:1-11
27. Rangasamy T, Misra V, Zhen L, Tankersley CG, Tuder RM, Biswal S. Cigarette smoke-induced emphysema in A/J mice is associated with pulmonary oxidative stress, apoptosis of lung cells, and global alterations in gene expression. Am J Physiol Lung Cell Mol Physiol 2009;296:L888-L900
28. Gebel S, Diehl S, Pype J, Friedrichs B, Weiler H, Schuller J, Xu H, Taguchi K, Yamamoto M, Muller T. The transcriptome of Nrf22/2 mice provides evidence for impaired cell cycle progression in the development of cigarette smoke-induced emphysematous changes. Toxicol Sci 2010;115:238-252
29. Luettich K, Xiang Y, Iskandar A, Sewer A, Martin F, Talikka M, Vanscheeuwijck P, Berges A, Veljkovic E. Systems toxicology approaches enable mechanistic comparison of spontaneous and cigarette smoke-related lung tumor development in the A/J mouse model. Interdiscip Toxicol 2014;7:73-84
30. Cabanski M, Fields B, Boue S, Boukharov N, DeLeon H, Dror N, Geertz M, Guedj E, Iskandar A, Kogel U, et al. Transcriptional profiling and targeted proteomics reveals common molecular changes associated with cigarette smoke-induced lung emphysema development in five susceptible mouse strains. Inflamm Res 2015;64:471-486
31. Cloonan SM, Glass K, Laucho-Contreras ME, Bhashyam AR, Cervo M, Pabón MA, Konrad C, Polverino F, Siempos II, Perez E, et al. Mitochondrial iron chelation ameliorates cigarette smoke-induced bronchitis and emphysema in mice. Nat Med 2016;22:163-174
32. Yoshida T, Tuder RM. Pathobiology of cigarette smoke-induced chronic obstructive pulmonary disease. Physiol Rev 2007;87: 1047-1082
33. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, Yamamoto M, Petrache I, Tuder RM, Biswal S. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 2004;114:1248-1259
34. 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
35. Singh A, Ling G, Suhasini AN, Zhang P, Yamamoto M, Navas-Acien A, Cosgrove G, Tuder RM, Kensler TW, Watson WH, et al. Nrf2-dependent sulfiredoxin-1 expression protects against cigarette smoke-induced oxidative stress in lungs. Free Radic Biol Med 2009; 46:376-386
36. Morissette MC, Lamontagne M, BérubéJ-C, Gaschler G, Williams A, Yauk C, Couture C, Laviolette M, Hogg JC, Timens W, et al. Impact of cigarette smoke on the human and mouse lungs: α geneexpression comparison study. PLoS One 2014;9:e92498
37. BouéS, León H, Schlage WK, Peck MJ, Weiler H, Berges A, Vuillaume G, Martin F, Friedrichs B, Lebrun S, et al. Cigarette smoke induces molecular responses in respiratory tissues of ApoE2/2 mice that are progressively deactivated upon cessation. Toxicology 2013; 314:112-124
38. Tosello-Trampont AC, Nakada-Tsukui K, Ravichandran KS. Engulfment of apoptotic cells is negatively regulated by Rho-mediated signaling. J Biol Chem 2003;278:49911-49919
39. Richens TR, Linderman DJ, Horstmann SA, Lambert C, Xiao Y-Q, Keith RL, BoéDM, Morimoto K, Bowler RP, Day BJ, et al. Cigarette smoke impairs clearance of apoptotic cells through oxidantdependent activation of RhoA. Am J Respir Crit Care Med 2009; 179:1011-1021
40. Yokohori N, Aoshiba K, Nagai A; Respiratory Failure Research Group in Japan. Increased levels of cell death and proliferation in alveolar wall cells in patients with pulmonary emphysema. Chest 2004;125:626-632
41. Imai K, Mercer BA, Schulman LL, Sonett JR, D'Armiento JM. Correlation of lung surface area to apoptosis and proliferation in human emphysema. Eur Respir J 2005;25:250-258
42. Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF. Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 2000;106: 1311-1319
43. Tang K, Rossiter HB, Wagner PD, Breen EC. Lung-targeted VEGF inactivation leads to an emphysema phenotype in mice. J Appl Physiol (1985) 2004;97:1559-1566. [Discussion, p. 1549.]
44. Muller T, Bayer H, Myrtek D, Ferrari D, Sorichter S, Ziegenhagen MW, Zissel G, Virchow JC Jr, Luttmann W, Norgauer J, et al. The P2Y14 receptor of airway epithelial cells: coupling to intracellular Ca21 and IL-8 secretion. Am J Respir Cell Mol Biol 2005;33: 601-609
45. Moore DJ, Murdock PR, Watson JM, Faull RLM, Waldvogel HJ, Szekeres PG, Wilson S, Freeman KB, Emson PC. GPR105, α novel Gi/o-coupled UDP-glucose receptor expressed on brain glia and peripheral immune cells, is regulated by immunologic challenge: possible role in neuroimmune function. Brain Res Mol Brain Res 2003;118:10-23
46. Cho J, Yusuf R, Kook S, Attar E, Lee D, Park B, Cheng T, Scadden DT, Lee BC. Purinergic P2Y14 receptor modulates stress-induced hematopoietic stem/progenitor cell senescence. J Clin Invest 2014; 124:3159-3171
47. Barrio-Real L, Barrueco M, González-Sarmiento R, Caloca MJ. Association of α novel polymorphism of the b2-chimaerin gene (CHN2) with smoking. J Investig Med 2013;61:1129-1131
48. Liu Q-R, Drgon T, Johnson C, Walther D, Hess J, Uhl GR. Addiction molecular genetics: 639,401 SNP whole genome association identifies many "cell adhesion" genes. Am J Med Genet B Neuropsychiatr Genet 2006;141:918-925
49. Scheu S, Alferink J, Potzel T, Barchet W, Kalinke U, Pfeffer K. Targeted disruption of LIGHT causes defects in costimulatory T cell activation and reveals cooperation with lymphotoxin beta in mesenteric lymph node genesis. J Exp Med 2002;195:1613-1624
50. Maeno T, Houghton AM, Quintero PA, Grumelli S, Owen CA, Shapiro SD. CD81 T cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J Immunol 2007;178:8090-8096
51. Zeskind JE, Lenburg ME, Spira A. Translating the COPD transcriptome: insights into pathogenesis and tools for clinical management. Proc Am Thorac Soc 2008;5:834-841