Proteomic Analysis of Primary Human Airway Epithelial Cells Exposed to the Respiratory Toxicant Diacetyl

Journal of Proteome Research

Volumn 16, Issue 2, 2017, Pages 538-549

  Foster, Matthew W ^a   Gwinn, William M ^b   Kelly, Francine L ^a   Brass, David M ^a   Valente, Ashlee M ^a   Moseley, M Arthur ^a   Thompson, J Will ^a   Morgan, Daniel L ^b   Palmer, Scott M ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

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

Author keywords

BO; butanedione; butter flavoring; cornified envelope; pentanedione; PRM; repetin; RSPH4A; squamous metaplasia; TGM1

Indexed keywords

1 ACYLGLYCEROPHOSPHATE ACYLTRANSFERASE; 2,3 BUTANEDIONE; CYTOKERATIN 6; KERATIN; MONOMER; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEOME; SEQUESTOSOME 1; SPR1B PROTEIN; SPR2A PROTEIN; SPRR3 PROTEIN; UNCLASSIFIED DRUG; FLAVORING AGENT;

AIRWAY EPITHELIUM CELL; AMINO ACID SEQUENCE; ARTICLE; CELL DIFFERENTIATION; CELL LYSATE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING; CROSS REACTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; UPREGULATION; VAPOR; WESTERN BLOTTING; WHOLE CELL; ADOLESCENT; CELL CULTURE TECHNIQUE; CHEMISTRY; CILIUM; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; MALE; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; PATHOLOGY; PHOSPHORYLATION; PRIMARY CELL CULTURE; RESPIRATORY MUCOSA; ULTRASTRUCTURE; VOLATILIZATION; YOUNG ADULT;

ADOLESCENT; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CILIA; DIACETYL; EPITHELIAL CELLS; FLAVORING AGENTS; GENE EXPRESSION REGULATION; GENE ONTOLOGY; HUMANS; KERATIN-6; MALE; MIDDLE AGED; MOLECULAR SEQUENCE ANNOTATION; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEOME; RESPIRATORY MUCOSA; VOLATILIZATION; YOUNG ADULT;

EID: 85011705830     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.6b00672     Document Type: Article

References (52)

1. Kreiss, K.; Gomaa, A.; Kullman, G.; Fedan, K.; Simoes, E. J.; Enright, P. L. Clinical bronchiolitis obliterans in workers at a microwave-popcorn plant N. Engl. J. Med. 2002, 347 (5) 330-8 10.1056/NEJMoa020300
2. Kreiss, K. Flavoring-related bronchiolitis obliterans Curr. Opin Allergy Clin Immunol 2007, 7 (2) 162-7 10.1097/ACI.0b013e3280298235
3. Duling, M. G.; LeBouf, R. F.; Cox-Ganser, J. M.; Kreiss, K.; Martin, S. B., Jr.; Bailey, R. L. Environmental characterization of a coffee processing workplace with obliterative bronchiolitis in former workers J. Occup. Environ. Hyg. 2016, 13 (10) 770-81 10.1080/15459624.2016.1177649
4. Holden, V. K.; Hines, S. E. Update on flavoring-induced lung disease Curr. Opin. Pulm. Med. 2016, 22 (2) 158-64 10.1097/MCP.0000000000000250
5. Farsalinos, K. E.; Kistler, K. A.; Gillman, G.; Voudris, V. Evaluation of electronic cigarette liquids and aerosol for the presence of selected inhalation toxins Nicotine Tob. Res. 2015, 17 (2) 168-74 10.1093/ntr/ntu176
6. Allen, J. G.; Flanigan, S. S.; LeBlanc, M.; Vallarino, J.; MacNaughton, P.; Stewart, J. H.; Christiani, D. C. Flavoring Chemicals in E-Cigarettes: Diacetyl, 2,3-Pentanedione, and Acetoin in a Sample of 51 Products, Including Fruit-, Candy-, and Cocktail-Flavored E-Cigarettes Environ. Health Perspect 2016, 124 (6) 733-9 10.1289/ehp.1510185
7. Hubbs, A. F.; Battelli, L. A.; Goldsmith, W. T.; Porter, D. W.; Frazer, D.; Friend, S.; Schwegler-Berry, D.; Mercer, R. R.; Reynolds, J. S.; Grote, A.; Castranova, V.; Kullman, G.; Fedan, J. S.; Dowdy, J.; Jones, W. G. Necrosis of nasal and airway epithelium in rats inhaling vapors of artificial butter flavoring Toxicol. Appl. Pharmacol. 2002, 185 (2) 128-35
8. Hubbs, A. F.; Goldsmith, W. T.; Kashon, M. L.; Frazer, D.; Mercer, R. R.; Battelli, L. A.; Kullman, G. J.; Schwegler-Berry, D.; Friend, S.; Castranova, V. Respiratory toxicologic pathology of inhaled diacetyl in sprague-dawley rats Toxicol. Pathol. 2008, 36 (2) 330-44 10.1177/0192623307312694
9. Palmer, S. M.; Flake, G. P.; Kelly, F. L.; Zhang, H. L.; Nugent, J. L.; Kirby, P. J.; Foley, J. F.; Gwinn, W. M.; Morgan, D. L. Severe airway epithelial injury, aberrant repair and bronchiolitis obliterans develops after diacetyl instillation in rats PLoS One 2011, 6 (3) e17644 10.1371/journal.pone.0017644
10. Morgan, D. L.; Jokinen, M. P.; Price, H. C.; Gwinn, W. M.; Palmer, S. M.; Flake, G. P. Bronchial and bronchiolar fibrosis in rats exposed to 2,3-pentanedione vapors: implications for bronchiolitis obliterans in humans Toxicol. Pathol. 2012, 40 (3) 448-65 10.1177/0192623311431946
11. Morgan, D. L.; Jokinen, M. P.; Johnson, C. L.; Price, H. C.; Gwinn, W. M.; Bousquet, R. W.; Flake, G. P. Chemical Reactivity and Respiratory Toxicity of the alpha-Diketone Flavoring Agents: 2,3-Butanedione, 2,3-Pentanedione, and 2,3-Hexanedione Toxicol. Pathol. 2016, 44 (5) 763-83 10.1177/0192623316638962
12. O'Koren, E. G.; Hogan, B. L.; Gunn, M. D. Loss of basal cells precedes bronchiolitis obliterans-like pathological changes in a murine model of chlorine gas inhalation Am. J. Respir. Cell Mol. Biol. 2013, 49 (5) 788-97 10.1165/rcmb.2012-0369OC
13. Kelly, F. L.; Sun, J.; Fischer, B. M.; Voynow, J. A.; Kummarapurugu, A. B.; Zhang, H. L.; Nugent, J. L.; Beasley, R. F.; Martinu, T.; Gwinn, W. M.; Morgan, D. L.; Palmer, S. M. Diacetyl induces amphiregulin shedding in pulmonary epithelial cells and in experimental bronchiolitis obliterans Am. J. Respir. Cell Mol. Biol. 2014, 51 (4) 568-74 10.1165/rcmb.2013-0339OC
14. Zaccone, E. J.; Goldsmith, W. T.; Shimko, M. J.; Wells, J. R.; Schwegler-Berry, D.; Willard, P. A.; Case, S. L.; Thompson, J. A.; Fedan, J. S. 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 (3) 542-9 10.1016/j.taap.2015.10.004
15. Beausoleil, S. A.; Villen, J.; Gerber, S. A.; Rush, J.; Gygi, S. P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization Nat. Biotechnol. 2006, 24 (10) 1285-92 10.1038/nbt1240
16. MacLean, B.; Tomazela, D. M.; Shulman, N.; Chambers, M.; Finney, G. L.; Frewen, B.; Kern, R.; Tabb, D. L.; Liebler, D. C.; MacCoss, M. J. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments Bioinformatics 2010, 26 (7) 966-8 10.1093/bioinformatics/btq054
17. Gallien, S.; Duriez, E.; Crone, C.; Kellmann, M.; Moehring, T.; Domon, B. Targeted proteomic quantification on quadrupole-orbitrap mass spectrometer Mol. Cell. Proteomics 2012, 11 (12) 1709-23 10.1074/mcp.O112.019802
18. Peterson, A. C.; Russell, J. D.; Bailey, D. J.; Westphall, M. S.; Coon, J. J. Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics Mol. Cell. Proteomics 2012, 11 (11) 1475-88 10.1074/mcp.O112.020131
19. Hoos, M. D.; Richardson, B. M.; Foster, M. W.; Everhart, A.; Thompson, J. W.; Moseley, M. A.; Colton, C. A. Longitudinal study of differential protein expression in an Alzheimer's mouse model lacking inducible nitric oxide synthase J. Proteome Res. 2013, 12 (10) 4462-77 10.1021/pr4005103
20. Schechter, M. A.; Hsieh, M. K.; Njoroge, L. W.; Thompson, J. W.; Soderblom, E. J.; Feger, B. J.; Troupes, C. D.; Hershberger, K. A.; Ilkayeva, O. R.; Nagel, W. L.; Landinez, G. P.; Shah, K. M.; Burns, V. A.; Santacruz, L.; Hirschey, M. D.; Foster, M. W.; Milano, C. A.; Moseley, M. A.; Piacentino, V., 3rd; Bowles, D. E. Phosphoproteomic profiling of human myocardial tissues distinguishes ischemic from non-ischemic end stage heart failure PLoS One 2014, 9 (8) e104157 10.1371/journal.pone.0104157
21. Uhlen, M.; Fagerberg, L.; Hallstrom, B. M.; Lindskog, C.; Oksvold, P.; Mardinoglu, A.; Sivertsson, A.; Kampf, C.; Sjostedt, E.; Asplund, A.; Olsson, I.; Edlund, K.; Lundberg, E.; Navani, S.; Szigyarto, C. A.; Odeberg, J.; Djureinovic, D.; Takanen, J. O.; Hober, S.; Alm, T.; Edqvist, P. H.; Berling, H.; Tegel, H.; Mulder, J.; Rockberg, J.; Nilsson, P.; Schwenk, J. M.; Hamsten, M.; von Feilitzen, K.; Forsberg, M.; Persson, L.; Johansson, F.; Zwahlen, M.; von Heijne, G.; Nielsen, J.; Ponten, F. Proteomics. Tissue-based map of the human proteome Science 2015, 347 (6220) 1260419 10.1126/science.1260419
22. Lindskog, C.; Fagerberg, L.; Hallstrom, B.; Edlund, K.; Hellwig, B.; Rahnenfuhrer, J.; Kampf, C.; Uhlen, M.; Ponten, F.; Micke, P. The lung-specific proteome defined by integration of transcriptomics and antibody-based profiling FASEB J. 2014, 28 (12) 5184-96 10.1096/fj.14-254862
23. Frommer, A.; Hjeij, R.; Loges, N. T.; Edelbusch, C.; Jahnke, C.; Raidt, J.; Werner, C.; Wallmeier, J.; Grosse-Onnebrink, J.; Olbrich, H.; Cindric, S.; Jaspers, M.; Boon, M.; Memari, Y.; Durbin, R.; Kolb-Kokocinski, A.; Sauer, S.; Marthin, J. K.; Nielsen, K. G.; Amirav, I.; Elias, N.; Kerem, E.; Shoseyov, D.; Haeffner, K.; Omran, H. Immunofluorescence Analysis and Diagnosis of Primary Ciliary Dyskinesia with Radial Spoke Defects Am. J. Respir. Cell Mol. Biol. 2015, 53 (4) 563-73 10.1165/rcmb.2014-0483OC
24. Zimmers, T. A.; Jin, X.; Hsiao, E. C.; McGrath, S. A.; Esquela, A. F.; Koniaris, L. G. Growth differentiation factor-15/macrophage inhibitory cytokine-1 induction after kidney and lung injury Shock 2005, 23 (6) 543-8
25. Wu, Q.; Jiang, D.; Matsuda, J. L.; Ternyak, K.; Zhang, B.; Chu, H. W. Cigarette Smoke Induces Human Airway Epithelial Senescence via GDF15 Production Am. J. Respir. Cell Mol. Biol. 2016, 55, 429 10.1165/rcmb.2015-0143OC
26. Hubbs, A. F.; Fluharty, K. L.; Edwards, R. J.; Barnabei, J. L.; Grantham, J. T.; Palmer, S. M.; Kelly, F.; Sargent, L. M.; Reynolds, S. H.; Mercer, R. R.; Goravanahally, M. P.; Kashon, M. L.; Honaker, J. C.; Jackson, M. C.; Cumpston, A. M.; Goldsmith, W. T.; McKinney, W.; Fedan, J. S.; Battelli, L. A.; Munro, T.; Bucklew-Moyers, W.; McKinstry, K.; Schwegler-Berry, D.; Friend, S.; Knepp, A. K.; Smith, S. L.; Sriram, K. Accumulation of Ubiquitin and Sequestosome-1 Implicate Protein Damage in Diacetyl-Induced Cytotoxicity Am. J. Pathol. 2016, 186, 2887 10.1016/j.ajpath.2016.07.018
27. Herfs, M.; Hubert, P.; Poirrier, A. L.; Vandevenne, P.; Renoux, V.; Habraken, Y.; Cataldo, D.; Boniver, J.; Delvenne, P. Proinflammatory cytokines induce bronchial hyperplasia and squamous metaplasia in smokers: implications for chronic obstructive pulmonary disease therapy Am. J. Respir. Cell Mol. Biol. 2012, 47 (1) 67-79 10.1165/rcmb.2011-0353OC
28. Araya, J.; Cambier, S.; Markovics, J. A.; Wolters, P.; Jablons, D.; Hill, A.; Finkbeiner, W.; Jones, K.; Broaddus, V. C.; Sheppard, D.; Barzcak, A.; Xiao, Y.; Erle, D. J.; Nishimura, S. L. Squamous metaplasia amplifies pathologic epithelial-mesenchymal interactions in COPD patients J. Clin. Invest. 2007, 117 (11) 3551-62 10.1172/JCI32526
29. 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 1997, 43 (3) 339-48 10.1006/geno.1997.4818
30. Candi, E.; Schmidt, R.; Melino, G. The cornified envelope: a model of cell death in the skin Nat. Rev. Mol. Cell Biol. 2005, 6 (4) 328-40 10.1038/nrm1619
31. Jetten, A. M. Multistep process of squamous differentiation in tracheobronchial epithelial cells in vitro: analogy with epidermal differentiation Environ. Health Perspect 1989, 80, 149-60 10.1289/ehp.8980149
32. Candi, E.; Tarcsa, E.; Digiovanna, J. J.; Compton, J. G.; Elias, P. M.; Marekov, L. N.; Steinert, P. M. A highly conserved lysine residue on the head domain of type II keratins is essential for the attachment of keratin intermediate filaments to the cornified cell envelope through isopeptide crosslinking by transglutaminases Proc. Natl. Acad. Sci. U. S. A. 1998, 95 (5) 2067-72 10.1073/pnas.95.5.2067
33. Radner, F. P.; Fischer, J. The important role of epidermal triacylglycerol metabolism for maintenance of the skin permeability barrier function Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 2014, 1841 (3) 409-15 10.1016/j.bbalip.2013.07.013
34. Higashi, Y.; Fuda, H.; Yanai, H.; Lee, Y.; Fukushige, T.; Kanzaki, T.; Strott, C. A. Expression of cholesterol sulfotransferase (SULT2B1b) in human skin and primary cultures of human epidermal keratinocytes J. Invest. Dermatol. 2004, 122 (5) 1207-13 10.1111/j.0022-202X.2004.22416.x
35. Rearick, J. I.; Stoner, G. D.; George, M. A.; Jetten, A. M. Cholesterol sulfate accumulation in tumorigenic and nontumorigenic rat esophageal epithelial cells: evidence for defective differentiation control in tumorigenic cells Cancer Res. 1988, 48 (18) 5289-95
36. Prabhala, P.; Ammit, A. J. Tristetraprolin and its role in regulation of airway inflammation Mol. Pharmacol. 2015, 87 (4) 629-38 10.1124/mol.114.095984
37. Eckert, R. L.; Rorke, E. A. Molecular biology of keratinocyte differentiation Environ. Health Perspect 1989, 80, 109-16 10.1289/ehp.8980109
38. Rackley, C. R.; Stripp, B. R. Building and maintaining the epithelium of the lung J. Clin. Invest. 2012, 122 (8) 2724-30 10.1172/JCI60519
39. Wansleeben, C.; Barkauskas, C. E.; Rock, J. R.; Hogan, B. L. Stem cells of the adult lung: their development and role in homeostasis, regeneration, and disease Wiley Interdiscip Rev. Dev Biol. 2013, 2 (1) 131-48 10.1002/wdev.58
40. Rock, J. R.; Randell, S. H.; Hogan, B. L. Airway basal stem cells: a perspective on their roles in epithelial homeostasis and remodeling Dis. Models & Mech. 2010, 3 (9-10) 545-56 10.1242/dmm.006031
41. Hackett, N. R.; Shaykhiev, R.; Walters, M. S.; Wang, R.; Zwick, R. K.; Ferris, B.; Witover, B.; Salit, J.; Crystal, R. G. The human airway epithelial basal cell transcriptome PLoS One 2011, 6 (5) e18378 10.1371/journal.pone.0018378
42. Shaykhiev, R.; Zuo, W. L.; Chao, I.; Fukui, T.; Witover, B.; Brekman, A.; Crystal, R. G. EGF shifts human airway basal cell fate toward a smoking-associated airway epithelial phenotype Proc. Natl. Acad. Sci. U. S. A. 2013, 110 (29) 12102-7 10.1073/pnas.1303058110
43. Hutton, E.; Paladini, R. D.; Yu, Q. C.; Yen, M.; Coulombe, P. A.; Fuchs, E. Functional differences between keratins of stratified and simple epithelia J. Cell Biol. 1998, 143 (2) 487-99 10.1083/jcb.143.2.487
44. Hyder, C. L.; Pallari, H. M.; Kochin, V.; Eriksson, J. E. Providing cellular signposts - post-translational modifications of intermediate filaments FEBS Lett. 2008, 582 (14) 2140-8 10.1016/j.febslet.2008.04.064
45. Pan, X.; Kane, L. A.; Van Eyk, J. E.; Coulombe, P. A. Type I keratin 17 protein is phosphorylated on serine 44 by p90 ribosomal protein S6 kinase 1 (RSK1) in a growth- and stress-dependent fashion J. Biol. Chem. 2011, 286 (49) 42403-13 10.1074/jbc.M111.302042
46. Toivola, D. M.; Zhou, Q.; English, L. S.; Omary, M. B. Type II keratins are phosphorylated on a unique motif during stress and mitosis in tissues and cultured cells Mol. Biol. Cell 2002, 13 (6) 1857-70 10.1091/mbc.01-12-0591
47. Dalby, K. N.; Morrice, N.; Caudwell, F. B.; Avruch, J.; Cohen, P. Identification of regulatory phosphorylation sites in mitogen-activated protein kinase (MAPK)-activated protein kinase-1a/p90rsk that are inducible by MAPK J. Biol. Chem. 1998, 273 (3) 1496-505 10.1074/jbc.273.3.1496
48. Pearce, L. R.; Komander, D.; Alessi, D. R. The nuts and bolts of AGC protein kinases Nat. Rev. Mol. Cell Biol. 2010, 11 (1) 9-22 10.1038/nrm2822
49. Morgan, D. L.; Merrick, B. A.; Gerrish, K. E.; Stockton, P. S.; Wang, Y.; Foley, J. F.; Gwinn, W. M.; Kelly, F. L.; Palmer, S. M.; Ton, T. V.; Flake, G. P. Gene expression in obliterative bronchiolitis-like lesions in 2,3-pentanedione-exposed rats PLoS One 2015, 10 (2) e0118459 10.1371/journal.pone.0118459
50. Hubbs, A. F.; Fluharty, K. L.; Edwards, R. J.; Barnabei, J. L.; Grantham, J. T.; Palmer, S. M.; Kelly, F.; Sargent, L. M.; Reynolds, S. H.; Mercer, R. R.; Goravanahally, M. P.; Kashon, M. L.; Honaker, J. C.; Jackson, M. C.; Cumpston, A. M.; Goldsmith, W. T.; McKinney, W.; Fedan, J. S.; Battelli, L. A.; Munro, T.; Bucklew-Moyers, W.; McKinstry, K.; Schwegler-Berry, D.; Friend, S.; Knepp, A. K.; Smith, S. L.; Sriram, K. Accumulation of Ubiquitin and Sequestosome-1 Implicate Protein Damage in Diacetyl-Induced Cytotoxicity Am. J. Pathol. 2016, 186 (11) 2887-2908 10.1016/j.ajpath.2016.07.018
51. Chen, Y. T.; Nikulina, K.; Lazarev, S.; Bahrami, A. F.; Noble, L. B.; Gallup, M.; McNamara, N. A. Interleukin-1 as a phenotypic immunomodulator in keratinizing squamous metaplasia of the ocular surface in Sjogren's syndrome Am. J. Pathol. 2010, 177 (3) 1333-43 10.2353/ajpath.2010.100227
52. Zhou, Y.; Lee, J. Y.; Lee, C. M.; Cho, W. K.; Kang, M. J.; Koff, J. L.; Yoon, P. O.; Chae, J.; Park, H. O.; Elias, J. A.; Lee, C. G. Amphiregulin, an epidermal growth factor receptor ligand, plays an essential role in the pathogenesis of transforming growth factor-beta-induced pulmonary fibrosis J. Biol. Chem. 2012, 287 (50) 41991-2000 10.1074/jbc.M112.356824