The diacetyl-exposed human airway epithelial secretome: New Insights into flavoring-induced airways disease

American Journal of Respiratory Cell and Molecular Biology

Volumn 56, Issue 6, 2017, Pages 784-795

  Brass, David M ^a   Gwinn, William M ^a   Valente, Ashlee M ^a   Kelly, Francine L ^a   Brinkley, Christie D ^a   Nagler, Andrew E ^a   Moseley, M Arthur ^b   Morgan, Daniel L ^a   Palmer, Scott M ^a   Foster, Matthew W ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

2,3 butanedione; Bronchiolitis obliterans; Diacetyl; Occupational lung disease; Proteomics

Indexed keywords

2,3 BUTANEDIONE; EPIDERMAL GROWTH FACTOR RECEPTOR; PHOSPHATE BUFFERED SALINE; FLAVORING AGENT; PROTEOME;

AIR; AIRWAY EPITHELIUM CELL; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; DONOR; HUMAN; HUMAN CELL; LIQUID; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEOMICS; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT DISEASE; SECRETOME; SIGNAL TRANSDUCTION; VAPOR; CELL DIFFERENTIATION; DRUG EFFECTS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; LUNG; LUNG DISEASE; METABOLISM; PATHOLOGY; SECRETION (PROCESS);

CELL DIFFERENTIATION; DIACETYL; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; FLAVORING AGENTS; HUMANS; LUNG; LUNG DISEASES; PROTEOME; PROTEOMICS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 85020213080     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2016-0372OC     Document Type: Article

References (40)

1. Kreiss K, Gomaa A, Kullman G, Fedan K, Simoes EJ, Enright PL. Clinical bronchiolitis obliterans in workers at a microwave-popcorn plant. N Engl J Med 2002;347:330-338.
2. Lockey JE, Hilbert TJ, Levin LP, Ryan PH, White KL, Borton EK, Rice CH, McKay RT, LeMasters GK. Airway obstruction related to diacetyl exposure at microwave popcorn production facilities. Eur Respir J 2009;34:63-71.
3. Akpinar-Elci M, Travis WD, Lynch DA, Kreiss K. Bronchiolitis obliterans syndrome in popcorn production plant workers. Eur Respir J 2004;24: 298-302.
4. Kim TJ, Materna BL, Prudhomme JC, Fedan KB, Enright PL, Sahakian NM, Windham GC, Kreiss K. Industry-wide medical surveillance of California flavor manufacturing workers: cross-sectional results. Am J Ind Med 2010;53:857-865.
5. van Rooy, FG, Rooyackers JM, Prokop M, Houba R, Smit LA, Heederik DJ. Bronchiolitis obliterans syndrome in chemical workers producing diacetyl for food flavorings. Am J Respir Crit Care Med 2007;176: 498-504.
6. Foster MW, Morrison LD, Todd JL, Snyder LD, Thompson JW, Soderblom EJ, Plonk K, Weinhold KJ, Townsend R, Minnich A, et al. Quantitative proteomics of bronchoalveolar lavage fluid in idiopathic pulmonary fibrosis. J Proteome Res 2015;14:1238-1249.
7. Peters-Hall JR, Brown KJ, Pillai DK, Tomney A, Garvin LM, Wu X, Rose MC. Quantitative proteomics reveals an altered cystic fibrosis in vitro bronchial epithelial secretome. Am J Respir Cell Mol Biol 2015;53:22-32.
8. Pillai DK, Sankoorikal BJ, Johnson E, Seneviratne AN, Zurko J, Brown KJ, Hathout Y, Rose MC. Directional secretomes reflect polarityspecific functions in an in vitro model of human bronchial epithelium. Am J Respir Cell Mol Biol 2014;50:292-300.
9. Kelly FL, Sun J, Fischer BM, Voynow JA, Kummarapurugu AB, Zhang HL, Nugent JL, Beasley RF, Martinu T, Gwinn WM, et al. Diacetyl induces amphiregulin shedding in pulmonary epithelial cells and in experimental bronchiolitis obliterans. Am J Respir Cell Mol Biol 2014; 51:568-574.
10. Foster MW, Gwinn WM, Kelly FL, Brass DM, Valente AM, Moseley MA, Thompson JW, Morgan DL, Palmer SM. Proteomic analysis of primary human airway epithelial cells exposed to the respiratory toxicant diacetyl. J Proteome Res 2017;16:538-549.
11. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995;57:289-300.
12. Haw R, Hermjakob H, D'Eustachio P, Stein L. Reactome pathway analysis to enrich biological discovery in proteomics data sets. Proteomics 2011;11:3598-3613.
13. Snel B, Lehmann G, Bork P, Huynen MA. STRING: A web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. Nucleic Acids Res 2000;28:3442-3444.
14. Camaj P, Seeliger H, Ischenko I, Krebs S, Blum H, De Toni, EN, Faktorova D, Jauch KW, Bruns CJ. EFEMP1 binds the EGF receptor and activates MAPK and Akt pathways in pancreatic carcinoma cells. Biol Chem 2009;390:1293-1302.
15. Poulin GB, Ahringer J. The Caenorhabditis elegans CDT-2 ubiquitin ligase is required for attenuation of EGFR signalling in vulva precursor cells. BMC Dev Biol 2010;10:109.
16. Carrillo-Garcia C, Prochnow S, Simeonova IK, Strelau J, Holzl-Wenig G, Mandl C, Unsicker K, von Bohlen Und Halbach O, Ciccolini F. Growth/differentiation factor 15 promotes EGFR signalling, and regulates proliferation and migration in the hippocampus of neonatal and young adult mice. Development 2014;141:773-783.
17. Lee KM, Nam K, Oh S, Lim J, Kim YP, Lee JW, Yu JH, Ahn SH, Kim SB, Noh DY, et al. Extracellular matrix protein 1 regulates cell proliferation and trastuzumab resistance through activation of epidermal growth factor signaling. Breast Cancer Res 2014;16: 479.
18. Mir H, Singh R, Kloecker GH, Lillard JW Jr, Singh S. CXCR6 expression in non-small cell lung carcinoma supports metastatic process via modulating metalloproteinases. Oncotarget 2015;6:9985-9998.
19. Gabay C, Towne JE. Regulation and function of interleukin-36 cytokines in homeostasis and pathological conditions. J Leukoc Biol 2015;97:645-652.
20. Medina-Contreras O, Harusato A, Nishio H, Flannigan KL, Ngo V, Leoni G, Neumann PA, Geem D, Lili LN, Ramadas RA, et al. Cutting edge: IL-36 receptor promotes resolution of intestinal damage. J Immunol 2016; 196:34-38.
21. Ramadas RA, Ewart SL, Iwakura Y, Medoff BD, LeVine AM. IL-36a exerts pro-inflammatory effects in the lungs of mice. PLoS One 2012; 7:e45784.
22. Hu Y, Gao H, Vo C, Ke C, Pan F, Yu L, Siegel E, Hess KR, Linskey ME, Zhou YH. Anti-EGFR function of EFEMP1 in glioma cells and patient prognosis. Oncoscience 2014;1:205-215.
23. Suarez Pestana E, Tenev T, Gross S, Stoyanov B, Ogata M, Bohmer FD. The transmembrane protein tyrosine phosphatase RPTPs modulates signaling of the epidermal growth factor receptor in A431 cells. Oncogene 1999;18:4069-4079.
24. Vijayvargia R, Kaur S, Krishnasastry MV. a-Hemolysin-induced dephosphorylation of EGF receptor of A431 cells is carried out by rPTPs. Biochem Biophys Res Commun 2004;325:344-352.
25. Morris LG, Taylor BS, Bivona TG, Gong Y, Eng S, Brennan CW, Kaufman A, Kastenhuber ER, Banuchi VE, Singh B, et al. Genomic dissection of the epidermal growth factor receptor (EGFR)/PI3K pathway reveals frequent deletion of the EGFR phosphatase PTPRS in head and neck cancers. Proc Natl Acad Sci USA 2011;108: 19024-19029.
26. Farach-Carson MC, Warren CR, Harrington DA, Carson DD. Border patrol: insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol 2014;34:64-79.
27. Andersson-Sjoland A, Thiman L, Nihlberg K, Hallgren O, Rolandsson S, Skog I, Mared L, Hansson L, Eriksson L, Bjermer L, et al. Fibroblast phenotypes and their activity are changed in the wound healing process after lung transplantation. J Heart Lung Transplant 2011;30: 945-954.
28. Sakai LY, Keene DR, Morris NP, Burgeson RE. Type VII collagen is a major structural component of anchoring fibrils. J Cell Biol 1986;103: 1577-1586.
29. Leitinger B. Molecular analysis of collagen binding by the human discoidin domain receptors, DDR1 and DDR2. Identification of collagen binding sites in DDR2. J Biol Chem 2003;278: 16761-16769.
30. Vogel W, Gish GD, Alves F, Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1997;1:13-23.
31. Shrivastava A, Radziejewski C, Campbell E, Kovac L, McGlynn M, Ryan TE, Davis S, Goldfarb MP, Glass DJ, Lemke G, et al. An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell 1997;1:25-34.
32. Leitinger B. Transmembrane collagen receptors. Annu Rev Cell Dev Biol 2011;27:265-290.
33. Fu H-L, Valiathan RR, Arkwright R, Sohail A, Mihai C, Kumarasiri M, Mahasenan KV, Mobashery S, Huang P, Agarwal G, et al. Discoidin domain receptors: unique receptor tyrosine kinases in collagen-mediated signaling. J Biol Chem 2013;288:7430-7437.
34. Leitinger B. Discoidin domain receptor functions in physiological and pathological conditions. Int Rev Cell Mol Biol 2014;310:39-87.
35. Kennedy VE, Todd JL, Palmer SM. Bronchoalveolar lavage as a tool to predict, diagnose and understand bronchiolitis obliterans syndrome. Am J Transplant 2013;13:552-561.
36. Palmer SM, Flake GP, Kelly FL, Zhang HL, Nugent JL, Kirby PJ, Foley JF, Gwinn WM, Morgan DL. Severe airway epithelial injury, aberrant repair and bronchiolitis obliterans develops after diacetyl instillation in rats. PLoS One 2011;6:e17644.
37. Fedan JS, Dowdy JA, Fedan KB, Hubbs AF. Popcorn worker's lung: in vitro exposure to diacetyl, an ingredient in microwave popcorn butter flavoring, increases reactivity to methacholine. Toxicol Appl Pharmacol 2006;215:17-22.
38. Zaccone EJ, Goldsmith WT, Shimko MJ, Wells JR, Schwegler-Berry D, Willard PA, Case SL, Thompson JA, Fedan JS. Diacetyl and 2, 3- pentanedione exposure of human cultured airway epithelial cells: ion transport effects and metabolism of butter flavoring agents. Toxicol Appl Pharmacol 2015;289:542-549.
39. More SS, Raza A, Vince R. The butter flavorant, diacetyl, forms a covalent adduct with 2-deoxyguanosine, uncoils DNA, and leads to cell death. J Agric Food Chem 2012;60:3311-3317.
40. Hubbs AF, Fluharty KL, Edwards RJ, Barnabei JL, Grantham JT, Palmer SM, Kelly F, Sargent LM, Reynolds SH, Mercer RR, et al. Accumulation of ubiquitin and sequestosome-1 implicate protein damage in diacetyl-induced cytotoxicity. Am J Pathol 2016;186: 2887-2908.