Gene expression in whole lung and pulmonary macrophages reflects the dynamic pathology associated with airway surface dehydration

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Saini, Yogesh ^a   Dang, Hong ^a   Livraghi Butrico, Alessandra ^a   Kelly, Elizabeth J ^a   Jones, Lisa C ^a   O'Neal, Wanda K ^a   Boucher, Richard C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Airway surface liquid dehydration; Gene expression profiling; Inflammation; Lung development; Mucus clearance defect; Pulmonary macrophage activation; Scnn1b Tg mice

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; DISEASE COURSE; GENE; GENE CONTROL; GENE EXPRESSION; GENE OVEREXPRESSION; LUNG ALVEOLUS MACROPHAGE; LUNG DEVELOPMENT; MACROPHAGE ACTIVATION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PERINATAL PERIOD; SCNN1B GENE; TISSUE SPECIFICITY; TRANSGENE; ANIMAL; C57BL MOUSE; DEHYDRATION; DNA MICROARRAY; DOWN REGULATION; GENE EXPRESSION PROFILING; GENETICS; HUMAN; INFLAMMATION; LONGITUDINAL STUDY; LUNG; METABOLISM; MUCUS; PRINCIPAL COMPONENT ANALYSIS; TRANSGENIC MOUSE; UPREGULATION;

MUS;

EPITHELIAL SODIUM CHANNEL; SCNN1B PROTEIN, HUMAN;

ANIMALS; DEHYDRATION; DOWN-REGULATION; EPITHELIAL SODIUM CHANNELS; GENE EXPRESSION PROFILING; HUMANS; INFLAMMATION; LONGITUDINAL STUDIES; LUNG; MACROPHAGE ACTIVATION; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUCUS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PRINCIPAL COMPONENT ANALYSIS; UP-REGULATION;

EID: 84908073532     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-726     Document Type: Article

References (56)

1. Fahy JV, Dickey BF. Airway mucus function and dysfunction. N Engl J Med 2010, 363(23):2233-2247. 10.1056/NEJMra0910061, 4048736, 21121836.
2. Boucher RC. Cystic fibrosis: a disease of vulnerability to airway surface dehydration. Trends Mol Med 2007, 13(6):231-240. 10.1016/j.molmed.2007.05.001, 17524805.
3. Smith DJ, Gaffney EA, Blake JR. Modelling mucociliary clearance. Respir Physiol Neurobiol 2008, 163(1-3):178-188.
4. James AL, Wenzel S. Clinical relevance of airway remodelling in airway diseases. Eur Respir J 2007, 30(1):134-155. 10.1183/09031936.00146905, 17601971.
5. Randell SH, Boucher RC. Effective mucus clearance is essential for respiratory health. Am J Respir Cell Mol Biol 2006, 35(1):20-28. 10.1165/rcmb.2006-0082SF, 2658694, 16528010.
6. Rogers GB, Carroll MP, Serisier DJ, Hockey PM, Jones G, Bruce KD. Characterization of bacterial community diversity in cystic fibrosis lung infections by use of 16 s ribosomal DNA terminal restriction fragment length polymorphism profiling. J Clin Microbiol 2004, 42(11):5176-5183. 10.1128/JCM.42.11.5176-5183.2004, 525137, 15528712.
7. Ellerman A, Bisgaard H. Longitudinal study of lung function in a cohort of primary ciliary dyskinesia. Eur Respir J 1997, 10(10):2376-2379. 10.1183/09031936.97.10102376, 9387968.
8. Sze MA, Dimitriu PA, Hayashi S, Elliott WM, McDonough JE, Gosselink JV, Cooper J, Sin DD, Mohn WW, Hogg JC. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2012, 185(10):1073-1080. 10.1164/rccm.201111-2075OC, 3359894, 22427533.
9. Mall M, Grubb BR, Harkema JR, O'Neal WK, Boucher RC. Increased airway epithelial Na + absorption produces cystic fibrosis-like lung disease in mice. Nat Med 2004, 10(5):487-493. 10.1038/nm1028, 15077107.
10. Livraghi-Butrico A, Grubb BR, Kelly EJ, Wilkinson KJ, Yang H, Geiser M, Randell SH, Boucher RC, O'Neal WK. Genetically determined heterogeneity of lung disease in a mouse model of airway mucus obstruction. Physiol Genomics 2012, 44(8):470-484. 10.1152/physiolgenomics.00185.2011, 3339860, 22395316.
11. Wielputz MO, Eichinger M, Zhou Z, Leotta K, Hirtz S, Bartling SH, Semmler W, Kauczor HU, Puderbach M, Mall MA. In vivo monitoring of cystic fibrosis-like lung disease in mice by volumetric computed tomography. Eur Respir J 2011, 38(5):1060-1070. 10.1183/09031936.00149810, 21478215.
12. Mall MA, Harkema JR, Trojanek JB, Treis D, Livraghi A, Schubert S, Zhou Z, Kreda SM, Tilley SL, Hudson EJ, ONeal WK, Boucher RC. Development of chronic bronchitis and emphysema in beta-epithelial Na + channel-overexpressing mice. Am J Respir Crit Care Med 2008, 177(7):730-742. 10.1164/rccm.200708-1233OC, 2277210, 18079494.
13. Livraghi-Butrico A, Kelly EJ, Klem ER, Dang H, Wolfgang MC, Boucher RC, Randell SH, O'Neal WK. Mucus clearance, MyD88-dependent and MyD88-independent immunity modulate lung susceptibility to spontaneous bacterial infection and inflammation. Mucosal Immunol 2012, 5(4):397-408. 10.1038/mi.2012.17, 3377774, 22419116.
14. Amy RW, Bowes D, Burri PH, Haines J, Thurlbeck WM. Postnatal growth of the mouse lung. J Anat 1977, 124(Pt 1):131-151. 1235518, 914698.
15. Speer CP. Chorioamnionitis, postnatal factors and proinflammatory response in the pathogenetic sequence of bronchopulmonary dysplasia. Neonatology 2009, 95(4):353-361. 10.1159/000209301, 19494557.
16. Velten M, Heyob KM, Rogers LK, Welty SE. Deficits in lung alveolarization and function after systemic maternal inflammation and neonatal hyperoxia exposure. J Appl Physiol (1985) 2010, 108(5):1347-1356. 10.1152/japplphysiol.01392.2009, 2867533, 20223995.
17. Svanes C, Sunyer J, Plana E, Dharmage S, Heinrich J, Jarvis D, de Marco R, Norback D, Raherison C, Villani S, Wjst M, Svanes K, Antó JM. Early life origins of chronic obstructive pulmonary disease. Thorax 2010, 65(1):14-20. 10.1136/thx.2008.112136, 19729360.
18. Stocks J, Sonnappa S. Early life influences on the development of chronic obstructive pulmonary disease. Ther Adv Respir Dis 2013, 7(3):161-173. 10.1177/1753465813479428, 4107852, 23439689.
19. Livraghi A, Grubb BR, Hudson EJ, Wilkinson KJ, Sheehan JK, Mall MA, O'Neal WK, Boucher RC, Randell SH. Airway and lung pathology due to mucosal surface dehydration in {beta}-epithelial Na + channel-overexpressing mice: role of TNF-{alpha} and IL-4R{alpha} signaling, influence of neonatal development, and limited efficacy of glucocorticoid treatment. J Immunol 2009, 182(7):4357-4367. 10.4049/jimmunol.0802557, 2659461, 19299736.
20. Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol 2014, 14(2):81-93. 10.1038/nri3600, 24445666.
21. Snelgrove RJ, Goulding J, Didierlaurent AM, Lyonga D, Vekaria S, Edwards L, Gwyer E, Sedgwick JD, Barclay AN, Hussell T. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat Immunol 2008, 9(9):1074-1083. 10.1038/ni.1637, 18660812.
22. Bonfield TL, Konstan MW, Burfeind P, Panuska JR, Hilliard JB, Berger M. Normal bronchial epithelial cells constitutively produce the anti-inflammatory cytokine interleukin-10, which is downregulated in cystic fibrosis. Am J Respir Cell Mol Biol 1995, 13(3):257-261. 10.1165/ajrcmb.13.3.7544594, 7544594.
23. Trojanek JB, Cobos-Correa A, Diemer S, Kormann M, Schubert SC, Zhou-Suckow Z, Agrawal R, Duerr J, Wagner CJ, Schatterny J, Hirtz S, Sommerburg O, Hartl D, Schultz C, Mall MA. Airway mucus obstruction triggers macrophage activation and MMP12-dependent emphysema. Am J Respir Cell Mol Biol 2014, [Epub ahead of print].
24. Rowe SM, Jackson PL, Liu G, Hardison M, Livraghi A, Solomon GM, McQuaid DB, Noerager BD, Gaggar A, Clancy JP, ONeal W, Sorscher EJ, Abraham E, Blalock JE. Potential role of high-mobility group box 1 in cystic fibrosis airway disease. Am J Respir Crit Care Med 2008, 178(8):822-831. 10.1164/rccm.200712-1894OC, 2566793, 18658107.
25. Fleming TJ, Fleming ML, Malek TR. Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J Immunol 1993, 151(5):2399-2408.
26. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stati Soc Series B 1995, 57(1):289-300. 57 (1): 289-300.
27. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004, 20(9):1453-1454. 10.1093/bioinformatics/bth078, 14871861.
28. Saldanha AJ. Java treeview-extensible visualization of microarray data. Bioinformatics 2004, 20(17):3246-3248. 10.1093/bioinformatics/bth349, 15180930.
29. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27(3):431-432. 10.1093/bioinformatics/btq675, 3031041, 21149340.
30. Mariani TJ, Reed JJ, Shapiro SD. Expression profiling of the developing mouse lung: insights into the establishment of the extracellular matrix. Am J Respir Cell Mol Biol 2002, 26(5):541-548. 10.1165/ajrcmb.26.5.2001-00080c, 11970905.
31. Zhang K, Shi ZM, Chang YN, Hu ZM, Qi HX, Hong W. The ways of action of long non-coding RNAs in cytoplasm and nucleus. Gene 2014, 547(1):1-9. 10.1016/j.gene.2014.06.043, 24967943.
32. Krishnan J, Mishra RK. Emerging trends of long non-coding RNAs in gene activation. FEBS J 2014, 281(1):34-45. 10.1111/febs.12578, 24165279.
33. Follettie MT, Ellis DK, Donaldson DD, Hill AA, Diesl V, DeClercq C, Sypek JP, Dorner AJ, Wills-Karp M. Gene expression analysis in a murine model of allergic asthma reveals overlapping disease and therapy dependent pathways in the lung. Pharmacogenomics J 2006, 6(2):141-152. 10.1038/sj.tpj.6500357, 16402082.
34. Munitz A, Brandt EB, Mingler M, Finkelman FD, Rothenberg ME. Distinct roles for IL-13 and IL-4 via IL-13 receptor alpha1 and the type II IL-4 receptor in asthma pathogenesis. Proc Natl Acad Sci U S A 2008, 105(20):7240-7245. 10.1073/pnas.0802465105, 2386078, 18480254.
35. Adkins B, Bu Y, Vincek V, Guevara P. The primary responses of murine neonatal lymph node CD4+ cells are Th2-skewed and are sufficient for the development of Th2-biased memory. Clin Dev Immunol 2003, 10(1):43-51. 10.1080/10446670310001598474, 2270671, 14575157.
36. Adkins B. Development of neonatal Th1/Th2 function. Int Rev Immunol 2000, 19(2-3):157-171.
37. Groneck P, Gotze-Speer B, Oppermann M, Eiffert H, Speer CP. Association of pulmonary inflammation and increased microvascular permeability during the development of bronchopulmonary dysplasia: a sequential analysis of inflammatory mediators in respiratory fluids of high-risk preterm neonates. Pediatrics 1994, 93(5):712-718.
38. Snyder JC, Reynolds SD, Hollingsworth JW, Li Z, Kaminski N, Stripp BR. Clara cells attenuate the inflammatory response through regulation of macrophage behavior. Am J Respir Cell Mol Biol 2010, 42(2):161-171. 10.1165/rcmb.2008-0353OC, 2822978, 19423773.
39. Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S, Deswarte K, Malissen B, Hammad H, Lambrecht BN. Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J Exp Med 2013, 210(10):1977-1992. 10.1084/jem.20131199, 3782041, 24043763.
40. Hashimoto D, Chow A, Noizat C, Teo P, Beasley MB, Leboeuf M, Becker CD, See P, Price J, Lucas D, Greter M, Mortha A, Boyer SW, Forsberg EC, Tanaka M, van Rooijen N, García-Sastre A, Stanley ER, Ginhoux F, Frenette PS, Merad M. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 2013, 38(4):792-804. 10.1016/j.immuni.2013.04.004, 3853406, 23601688.
41. Chowdhary R, Tan SL, Pavesi G, Jin J, Dong D, Mathur SK, Burkart A, Narang V, Glurich I, Raby BA, Weiss ST, Wong L, Liu JS, Bajic VB. A database of annotated promoters of genes associated with common respiratory and related diseases. Am J Respir Cell Mol Biol 2012, 47(1):112-119. 10.1165/rcmb.2011-0419OC, 22383585.
42. Steiling K, van den Berge M, Hijazi K, Florido R, Campbell J, Liu G, Xiao J, Zhang X, Duclos G, Drizik E, Si H, Perdomo C, Dumont C, Coxson HO, Alekseyev YO, Sin D, Pare P, Hogg JC, McWilliams A, Hiemstra PS, Sterk PJ, Timens W, Chang JT, Sebastiani P, OConnor GT, Bild AH, Postma DS, Lam S, Spira A, Lenburg ME. A dynamic bronchial airway gene expression signature of chronic obstructive pulmonary disease and lung function impairment. Am J Respir Crit Care Med 2013, 187(9):933-942. 10.1164/rccm.201208-1449OC, 3707363, 23471465.
43. Chen G, Korfhagen TR, Xu Y, Kitzmiller J, Wert SE, Maeda Y, Gregorieff A, Clevers H, Whitsett JA. SPDEF is required for mouse pulmonary goblet cell differentiation and regulates a network of genes associated with mucus production. J Clin Invest 2009, 119(10):2914-2924. 2752084, 19759516.
44. Shaykhiev R, Krause A, Salit J, Strulovici-Barel Y, Harvey BG, O'Connor TP, Crystal RG. Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease. J Immunol 2009, 183(4):2867-2883. 10.4049/jimmunol.0900473, 2873685, 19635926.
45. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008, 8(12):958-969. 10.1038/nri2448, 2724991, 19029990.
46. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010, 32(5):593-604. 10.1016/j.immuni.2010.05.007, 20510870.
47. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol 2011, 11(11):723-737. 10.1038/nri3073, 3422549, 21997792.
48. Mitchell C, Provost K, Niu N, Homer R, Cohn L. IFN-gamma acts on the airway epithelium to inhibit local and systemic pathology in allergic airway disease. J Immunol 2011, 187(7):3815-3820. 10.4049/jimmunol.1100436, 3178669, 21873527.
49. Daan De Boer J, Roelofs JJ, De Vos AF, De Beer R, Schouten M, Hommes TJ, Hoogendijk AJ, De Boer OJ, Stroo I, van der Zee JS, Veer CV, van der Poll T. Lipopolysaccharide inhibits Th2 lung inflammation induced by house dust mite allergens in mice. Am J Respir Cell Mol Biol 2013, 48(3):382-389. 10.1165/rcmb.2012-0331OC, 23239494.
50. Adkins B, Leclerc C, Marshall-Clarke S. Neonatal adaptive immunity comes of age. Nat Rev Immunol 2004, 4(7):553-564. 10.1038/nri1394, 15229474.
51. Nelson MP, Christmann BS, Werner JL, Metz AE, Trevor JL, Lowell CA, Steele C. IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina. J Immunol 2011, 186(4):2372-2381. 10.4049/jimmunol.1002558, 21220696.
52. Reece JJ, Siracusa MC, Scott AL. Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect Immun 2006, 74(9):4970-4981. 10.1128/IAI.00687-06, 1594865, 16926388.
53. Kim EY, Battaile JT, Patel AC, You Y, Agapov E, Grayson MH, Benoit LA, Byers DE, Alevy Y, Tucker J, Swanson S, Tidwell R, Tyner JW, Morton JD, Castro M, Polineni D, Patterson GA, Schwendener RA, Allard JD, Peltz G, Holtzman MJ. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat Med 2008, 14(6):633-640. 10.1038/nm1770, 2575848, 18488036.
54. Cocco RE, Ucker DS. Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure. Mol Biol Cell 2001, 12(4):919-930. 10.1091/mbc.12.4.919, 32276, 11294896.
55. Murdoch C, Muthana M, Lewis CE. Hypoxia regulates macrophage functions in inflammation. J Immunol 2005, 175(10):6257-6263. 10.4049/jimmunol.175.10.6257, 16272275.
56. Souza DG, Vieira AT, Soares AC, Pinho V, Nicoli JR, Vieira LQ, Teixeira MM. The essential role of the intestinal microbiota in facilitating acute inflammatory responses. J Immunol 2004, 173(6):4137-4146. 10.4049/jimmunol.173.6.4137, 15356164.