Matched-Comparative Modeling of Normal and Diseased Human Airway Responses Using a Microengineered Breathing Lung Chip

Cell Systems

Volumn 3, Issue 5, 2016, Pages 456-466.e4

  Benam, Kambez H ^a   Novak, Richard ^a   Nawroth, Janna ^a,b   Hirano Kobayashi, Mariko ^a,c   Ferrante, Thomas C ^a   Choe, Youngjae ^a   Prantil Baun, Rachelle ^a   Weaver, James C ^a,b   Bahinski, Anthony ^a   Parker, Kevin K ^a,b   Ingber, Donald E ^a,b,c,d  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

biomarker; cell culture; cigarette smoke; cilia; cytokine; electronic cigarette; human study; lung airway; microfluidic; organ chip; transcriptomic analysis

Indexed keywords

CIGARETTE SMOKE; HEME OXYGENASE 1; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; TRANSCRIPTION FACTOR NRF2;

AIRWAY EPITHELIUM CELL; ARTICLE; BRONCHIOLE EPITHELIUM; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMPARATIVE STUDY; CONTROLLED STUDY; ELECTRONIC CIGARETTE; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IN VITRO STUDY; MUCOCILIARY CLEARANCE; NORMAL HUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SMOKING; BREATHING; EPITHELIUM CELL; LUNG;

ELECTRONIC NICOTINE DELIVERY SYSTEMS; EPITHELIAL CELLS; HUMANS; LUNG; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATION; SMOKING;

EID: 84996606989     PISSN: 24054712     EISSN: 24054720     Source Type: Journal    
DOI: 10.1016/j.cels.2016.10.003     Document Type: Article

References (58)

1. Adamson, J., Haswell, L.E., Phillips, G., Gaça, M.D., In vitro models of chronic obstructive pulmonary disease (COPD). MartÃn-Loeches, I., (eds.) Bronchitis, 2011, InTech, 41–66.
2. Adamson, J., Azzopardi, D., Errington, G., Dickens, C., McAughey, J., Gaça, M.D., Assessment of an in vitro whole cigarette smoke exposure system: The Borgwaldt RM20S 8-syringe smoking machine. Chem. Cent. J., 5, 2011, 50.
3. Anttila, S., Tuominen, P., Hirvonen, A., Nurminen, M., Karjalainen, A., Hankinson, O., Elovaara, E., CYP1A1 levels in lung tissue of tobacco smokers and polymorphisms of CYP1A1 and aromatic hydrocarbon receptor. Pharmacogenetics 11 (2001), 501–509.
4. Benam, K.H., Kok, W.L., McMichael, A.J., Ho, L.P., Alternative spliced CD1d transcripts in human bronchial epithelial cells. PLoS ONE, 6, 2011, e22726.
5. Benam, K.H., Villenave, R., Lucchesi, C., Varone, A., Hubeau, C., Lee, H.H., Alves, S.E., Salmon, M., Ferrante, T.C., Weaver, J.C., et al. Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat. Methods 13 (2016), 151–157.
6. Caramori, G., Adcock, I.M., Casolari, P., Ito, K., Jazrawi, E., Tsaprouni, L., Villetti, G., Civelli, M., Carnini, C., Chung, K.F., et al. Unbalanced oxidant-induced DNA damage and repair in COPD: a link towards lung cancer. Thorax 66 (2011), 521–527.
7. Cervellati, F., Muresan, X.M., Sticozzi, C., Gambari, R., Montagner, G., Forman, H.J., Torricelli, C., Maioli, E., Valacchi, G., Comparative effects between electronic and cigarette smoke in human keratinocytes and epithelial lung cells. Toxicology In Vitro 28 (2014), 999–1005.
8. Chen, H., Wang, L., Gong, T., Yu, Y., Zhu, C., Li, F., Wang, L., Li, C., EGR-1 regulates Ho-1 expression induced by cigarette smoke. Biochem. Biophys. Res. Commun. 396 (2010), 388–393.
9. Cipollina, C., Di Vincenzo, S., Gerbino, S., Siena, L., Gjomarkaj, M., Pace, E., Dual anti-oxidant and anti-inflammatory actions of the electrophilic cyclooxygenase-2-derived 17-oxo-DHA in lipopolysaccharide- and cigarette smoke-induced inflammation. Biochim. Biophys. Acta 1840 (2014), 2299–2309.
10. Comandini, A., Marzano, V., Curradi, G., Federici, G., Urbani, A., Saltini, C., Markers of anti-oxidant response in tobacco smoke exposed subjects: a data-mining review. Pulm. Pharmacol. Ther. 23 (2010), 482–492.
11. Dickens, J.A., Miller, B.E., Edwards, L.D., Silverman, E.K., Lomas, D.A., Tal-Singer, R., Evaluation of COPD Longitudinally to Identify Surrogate Endpoints (ECLIPSE) study investigators. COPD association and repeatability of blood biomarkers in the ECLIPSE cohort. Respir. Res., 12, 2011, 146.
12. Gao, H., Wang, L., Cui, S., Wang, M., Combination of meta-analysis and graph clustering to identify prognostic markers of ESCC. Genet. Mol. Biol. 35 (2012), 530–537.
13. Glader, P., Möller, S., Lilja, J., Wieslander, E., Löfdahl, C.G., von Wachenfeldt, K., Cigarette smoke extract modulates respiratory defence mechanisms through effects on T-cells and airway epithelial cells. Respir. Med. 100 (2006), 818–827.
14. Guan, S.P., Tee, W., Ng, D.S., Chan, T.K., Peh, H.Y., Ho, W.E., Cheng, C., Mak, J.C., Wong, W.S., Andrographolide protects against cigarette smoke-induced oxidative lung injury via augmentation of Nrf2 activity. Br. J. Pharmacol. 168 (2013), 1707–1718.
15. Han, Y.C., Zheng, Z.L., Zuo, Z.H., Yu, Y.P., Chen, R., Tseng, G.C., Nelson, J.B., Luo, J.H., Metallothionein 1 h tumour suppressor activity in prostate cancer is mediated by euchromatin methyltransferase 1. J. Pathol. 230 (2013), 184–193.
16. Harvey, B.G., Heguy, A., Leopold, P.L., Carolan, B.J., Ferris, B., Crystal, R.G., Modification of gene expression of the small airway epithelium in response to cigarette smoking. J. Mol. Med. 85 (2007), 39–53.
17. Hellermann, G.R., Nagy, S.B., Kong, X., Lockey, R.F., Mohapatra, S.S., Mechanism of cigarette smoke condensate-induced acute inflammatory response in human bronchial epithelial cells. Respir. Res., 3, 2002, 22.
18. Hogg, J.C., McDonough, J.E., Suzuki, M., Small airway obstruction in COPD: new insights based on micro-CT imaging and MRI imaging. Chest 143 (2013), 1436–1443.
19. Hsu, A.C., See, H.V., Hansbro, P.M., Wark, P.A., Innate immunity to influenza in chronic airways diseases. Respirology 17 (2012), 1166–1175.
20. Huang da, W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009), 44–57.
21. Huber, M., Siegenthaler, G., Mirancea, N., Marenholz, I., Nizetic, D., Breitkreutz, D., Mischke, D., Hohl, D., Isolation and characterization of human repetin, a member of the fused gene family of the epidermal differentiation complex. J. Invest. Dermatol. 124 (2005), 998–1007.
22. Imai, K., Dalal, S.S., Chen, E.S., Downey, R., Schulman, L.L., Ginsburg, M., D'Armiento, J., Human collagenase (matrix metalloproteinase-1) expression in the lungs of patients with emphysema. Am. J. Respir. Crit. Care Med. 163 (2001), 786–791.
23. Keatings, V.M., Collins, P.D., Scott, D.M., Barnes, P.J., Differences in interleukin-8 and tumor necrosis factor-alpha in induced sputum from patients with chronic obstructive pulmonary disease or asthma. Am. J. Respir. Crit. Care Med. 153 (1996), 530–534.
24. Kim, W., Han, T.H., Kim, H.J., Park, M.Y., Kim, K.S., Park, R.W., An automated measurement of ciliary beating frequency using a combined optical flow and peak detection. Healthc. Inform. Res. 17 (2011), 111–119.
25. Krieg, P., Schuppler, M., Koesters, R., Mincheva, A., Lichter, P., Marks, F., Repetin (Rptn), a new member of the “fused gene” subgroup within the S100 gene family encoding a murine epidermal differentiation protein. Genomics 43 (1997), 339–348.
26. Lee, E.M., Malson, J.L., Waters, A.J., Moolchan, E.T., Pickworth, W.B., Smoking topography: reliability and validity in dependent smokers. Nicotine Tob. Res. 5 (2003), 673–679.
27. Ma, Q., Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53 (2013), 401–426.
28. Mathis, C., Poussin, C., Weisensee, D., Gebel, S., Hengstermann, A., Sewer, A., Belcastro, V., Xiang, Y., Ansari, S., Wagner, S., et al. Human bronchial epithelial cells exposed in vitro to cigarette smoke at the air-liquid interface resemble bronchial epithelium from human smokers. Am. J. Physiol. Lung Cell. Mol. Physiol. 304 (2013), L489–L503.
29. Mercer, B.A., Kolesnikova, N., Sonett, J., D'Armiento, J., Extracellular regulated kinase/mitogen activated protein kinase is up-regulated in pulmonary emphysema and mediates matrix metalloproteinase-1 induction by cigarette smoke. J. Biol. Chem. 279 (2004), 17690–17696.
30. Mio, T., Romberger, D.J., Thompson, A.B., Robbins, R.A., Heires, A., Rennard, S.I., Cigarette smoke induces interleukin-8 release from human bronchial epithelial cells. Am. J. Respir. Crit. Care Med. 155 (1997), 1770–1776.
31. Misra, M., Leverette, R.D., Cooper, B.T., Bennett, M.B., Brown, S.E., Comparative in vitro toxicity profile of electronic and tobacco cigarettes, smokeless tobacco and nicotine replacement therapy products: e-liquids, extracts and collected aerosols. Int. J. Environ. Res. Public Health 11 (2014), 11325–11347.
32. Mulligan, R.M., Atkinson, C., Vertegel, A.A., Reukov, V., Schlosser, R.J., Cigarette smoke extract stimulates interleukin-8 production in human airway epithelium and is attenuated by superoxide dismutase in vitro. Am. J. Rhinol. Allergy 23 (2009), e1–e4.
33. Neilson, L., Mankus, C., Thorne, D., Jackson, G., DeBay, J., Meredith, C., Development of an in vitro cytotoxicity model for aerosol exposure using 3D reconstructed human airway tissue; application for assessment of e-cigarette aerosol. Toxicology In Vitro 29 (2015), 1952–1962.
34. Olm, M.A., Kogler, J.E. Jr., Macchione, M., Shoemark, A., Saldiva, P.H., Rodrigues, J.C., Primary ciliary dyskinesia: evaluation using cilia beat frequency assessment via spectral analysis of digital microscopy images. J. Appl. Physiol. 111:1985 (2011), 295–302.
35. Owen, C.A., Roles for proteinases in the pathogenesis of chronic obstructive pulmonary disease. Int. J. Chron. Obstruct. Pulmon. Dis. 3 (2008), 253–268.
36. Pezzulo, A.A., Starner, T.D., Scheetz, T.E., Traver, G.L., Tilley, A.E., Harvey, B.G., Crystal, R.G., McCray, P.B. Jr., Zabner, J., The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 300 (2011), L25–L31.
37. Phillips, J., Kluss, B., Richter, A., Massey, E., Exposure of bronchial epithelial cells to whole cigarette smoke: assessment of cellular responses. Altern. Lab. Anim. 33 (2005), 239–248.
38. Pierrou, S., Broberg, P., O'Donnell, R.A., Pawłowski, K., Virtala, R., Lindqvist, E., Richter, A., Wilson, S.J., Angco, G., Möller, S., et al. Expression of genes involved in oxidative stress responses in airway epithelial cells of smokers with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 175 (2007), 577–586.
39. Powell, H.A., Iyen-Omofoman, B., Baldwin, D.R., Hubbard, R.B., Tata, L.J., Chronic obstructive pulmonary disease and risk of lung cancer: the importance of smoking and timing of diagnosis. J. Thoracic Oncol. 8 (2013), e34–e35.
40. Puchelle, E., Zahm, J.M., Tournier, J.M., Coraux, C., Airway epithelial repair, regeneration, and remodeling after injury in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc. 3 (2006), 726–733.
41. Rennard, S.I., Drummond, M.B., Early chronic obstructive pulmonary disease: definition, assessment, and prevention. Lancet 385 (2015), 1778–1788.
42. Rowell, T.R., Tarran, R., Will chronic e-cigarette use cause lung disease?. Am. J. Physiol. Lung Cell. Mol. Physiol. 309 (2015), L1398–L1409.
43. Sakai, N., Tager, A.M., Fibrosis of two: epithelial cell-fibroblast interactions in pulmonary fibrosis. Biochim. Biophys. Acta 1832 (2013), 911–921.
44. Sapey, E., Stockley, R.A., COPD exacerbations. 2: aetiology. Thorax 61 (2006), 250–258.
45. Shivalingappa, P.C., Hole, R., Westphal, C.V., Vij, N., Airway exposure to e-cigarette vapors impairs autophagy and induces aggresome formation. Antioxid. Redox Signal., 2015, 10.1089/ars.2015.6367 Published online October 27, 2015.
46. Smith, C.M., Djakow, J., Free, R.C., Djakow, P., Lonnen, R., Williams, G., Pohunek, P., Hirst, R.A., Easton, A.J., Andrew, P.W., O'Callaghan, C., ciliaFA: a research tool for automated, high-throughput measurement of ciliary beat frequency using freely available software. Cilia, 1, 2012, 14.
47. Stanley, P.J., Wilson, R., Greenstone, M.A., MacWilliam, L., Cole, P.J., Effect of cigarette smoking on nasal mucociliary clearance and ciliary beat frequency. Thorax 41 (1986), 519–523.
48. Strasser, A.A., Pickworth, W.B., Patterson, F., Lerman, C., Smoking topography predicts abstinence following treatment with nicotine replacement therapy. Cancer Epidemiol. Biomarkers Prev. 13 (2004), 1800–1804.
49. Thorne, D., Adamson, J., A review of in vitro cigarette smoke exposure systems. Exp. Toxicol. Pathol. 65 (2013), 1183–1193.
50. Vastag, E., Matthys, H., Zsamboki, G., Köhler, D., Daikeler, G., Mucociliary clearance in smokers. Eur. J. Respir. Dis. 68 (1986), 107–113.
51. Viloria, C.G., Peinado, J.R., Astudillo, A., García-Suárez, O., González, M.V., Suárez, C., Cal, S., Human DESC1 serine protease confers tumorigenic properties to MDCK cells and it is upregulated in tumours of different origin. Br. J. Cancer 97 (2007), 201–209.
52. Vlahos, R., Bozinovski, S., Recent advances in pre-clinical mouse models of COPD. Clin. Sci. 126 (2014), 253–265.
53. Wong, L.B., Park, C.L., Yeates, D.B., Neuropeptide Y inhibits ciliary beat frequency in human ciliated cells via nPKC, independently of PKA. Am. J. Physiol. 275 (1998), C440–C448.
54. Wooten, J.B., Chouchane, S., McGrath, T.E., Tobacco smoke constituents affecting oxidative stress. Halliwell, B.B., Poulsen, H.E., (eds.) Cigarette Smoke and Oxidative Stress, 2006, Springer, 407.
55. Wright, J.L., Cosio, M., Churg, A., Animal models of chronic obstructive pulmonary disease. Am. J. Physiol. Lung Cell. Mol. Physiol. 295 (2008), L1–L15.
56. Yaghi, A., Zaman, A., Cox, G., Dolovich, M.B., Ciliary beating is depressed in nasal cilia from chronic obstructive pulmonary disease subjects. Respir. Med. 106 (2012), 1139–1147.
57. Zhou, H., Wang, X., Brighton, L., Hazucha, M., Jaspers, I., Carson, J.L., Increased nasal epithelial ciliary beat frequency associated with lifestyle tobacco smoke exposure. Inhal. Toxicol. 21 (2009), 875–881.
58. Zmora, P., Blazejewska, P., Moldenhauer, A.S., Welsch, K., Nehlmeier, I., Wu, Q., Schneider, H., Pöhlmann, S., Bertram, S., DESC1 and MSPL activate influenza A viruses and emerging coronaviruses for host cell entry. J. Virol. 88 (2014), 12087–12097.