The tobacco smoke component acrolein induces glucocorticoid resistant gene expression via inhibition of histone deacetylase

Toxicology Letters

Volumn 240, Issue 1, 2016, Pages 43-49

  Randall, Matthew J ^a,b   Haenen, Guido R M M ^a   Bouwman, Freek G ^a   van der Vliet, Albert ^b   Bast, Aalt ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Acrolein; COPD; Glucocorticoid; HDAC; Inflammation

Indexed keywords

ACROLEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE 2; HYDROCORTISONE; LIPOPOLYSACCHARIDE; TOBACCO SMOKE; TUMOR NECROSIS FACTOR ALPHA; GLUCOCORTICOID; GLUTATHIONE; INTERLEUKIN 8; MESSENGER RNA; TUMOR NECROSIS FACTOR;

ARTICLE; CELL DIFFERENTIATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; GENE EXPRESSION; MACROPHAGE; MASS SPECTROMETRY; MONOCYTE; PRIORITY JOURNAL; U937 CELL LINE; ADVERSE EFFECTS; CELL CULTURE; CHEMICALLY INDUCED; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; HUMAN; INFLAMMATION; LUNG; METABOLISM; PATHOLOGY; SMOKING; TUMOR CELL LINE; UPREGULATION;

ACROLEIN; CELL LINE, TUMOR; CELLS, CULTURED; DRUG RESISTANCE; GENE EXPRESSION; GLUCOCORTICOIDS; GLUTATHIONE; HISTONE DEACETYLASE 2; HUMANS; HYDROCORTISONE; INFLAMMATION; INTERLEUKIN-8; LIPOPOLYSACCHARIDES; LUNG; MACROPHAGES; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RNA, MESSENGER; SMOKING; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84945270494     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.10.009     Document Type: Article

References (46)

1. Adcock I.M., Ito K., Barnes P.J. Glucocorticoids: effects on gene transcription. Proc. Am. Thorac. Soc. 2004, 1:247-254.
2. Adenuga D., Yao H., March T.H., Seagrave J., Rahman I. Histone deacetylase 2 is phosphorylated, ubiquitinated, and degraded by cigarette smoke. Am. J. Respir. Cell. Mol. Biol. 2009, 40:464-473.
3. Adhikari Bishwa, Kahende Jennifer, Malarcher Ann, Pechacek Terry, Tong Van Smoking-attributable mortality, years of potential life lost, and productivity losses-United States, 2000-2004. MMWR Morbidity and Mortality Weekly Report 2008, 1226-1228. U.S. Government Printing Office, Washington, D.C.
4. Barnes P.J., Ito K., Adcock I.M. Corticosteroid resistance in chronic obstructive pulmonary disease: inactivation of histone deacetylase. Lancet 2004, 363:731-733.
5. Barnes P.J. Inhaled corticosteroids are not beneficial in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2000, 161:342-344. (discussioin 344).
6. Barnes P.J. Role of HDAC2 in the pathophysiology of COPD. Annu. Rev. Physiol. 2009, 71:451-464.
7. Borchers M.T., Wert S.E., Leikauf G.D. Acrolein-induced MUC5ac expression in rat airways. Am. J. Physiol. 1998, 274:L573-L581.
8. Cai J., Bhatnagar A., Pierce W.M. Protein modification by acrolein: formation and stability of cysteine adducts. Chem. Res. Toxicol. 2009, 22:708-716.
9. Caito S., Rajendrasozhan S., Cook S., Chung S., Yao H., Friedman A.E., Brookes P.S., Rahman I. SIRT1 is a redox-sensitive deacetylase that is post-translationally modified by oxidants and carbonyl stress. FASEB J. 2010, 24:3145-3159.
10. Chalmers G.W., Macleod K.J., Little S.A., Thomson L.J., McSharry C.P., Thomson N.C. Influence of cigarette smoking on inhaled corticosteroid treatment in mild asthma. Thorax 2002, 57:226-230.
11. Corradi M., Pignatti P., Manini P., Andreoli R., Goldoni M., Poppa M., Moscato G., Balbi B., Mutti A. Comparison between exhaled and sputum oxidative stress biomarkers in chronic airway inflammation. Eur. Respir. J. 2004, 24:1011-1017.
12. Costa D.L. Air Pollution in Casarett and Doull's Toxicology: The Basic Science of Poisons 2001, McGraw-Hill, New York. C.D. Klaassen (Ed.).
13. Counts M.E., Hsu F.S., Laffoon S.W., Dwyer R.W., Cox R.H. Mainstream smoke constituent yields and predicting relationships from a worldwide market sample of cigarette brands: ISO smoking conditions. Regul. Toxicol. Pharmacol.: RTP 2004, 39:111-134.
14. de Ruijter A.J., van Gennip A.H., Caron H.N., Kemp S., van Kuilenburg A.B. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J. 2003, 370:737-749.
15. Doyle K., Fitzpatrick F.A. Redox signaling, alkylation (carbonylation) of conserved cysteines inactivates class I histone deacetylases 1, 2, and 3 and antagonizes their transcriptional repressor function. J. Biol. Chem. 2010, 285:17417-17424.
16. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11:81-128.
17. Facchinetti F., Amadei F., Geppetti P., Tarantini F., Di Serio C., Dragotto A., Gigli P.M., Catinella S., Civelli M., Patacchini R. Alpha,beta-unsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am. J. Respir. Cell Mol. Biol. 2007, 37:617-623.
18. Fritz K.S., Galligan J.J., Smathers R.L., Roede J.R., Shearn C.T., Reigan P., Petersen D.R. 4-Hydroxynonenal inhibits SIRT3 via thiol-specific modification. Chem. Res. Toxicol. 2011, 24:651-662.
19. Hoffmann E., Dittrich-Breiholz O., Holtmann H., Kracht M. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 2002, 72:847-855.
20. Hristova M., Spiess P.C., Kasahara D.I., Randall M.J., Deng B., van der Vliet A. The tobacco smoke component, acrolein, suppresses innate macrophage responses by direct alkylation of c-Jun N-terminal kinase. Am. J. Respir. Cell Mol. Biol. 2012, 46:23-33.
21. Ito K., Lim S., Caramori G., Chung K.F., Barnes P.J., Adcock I.M. Cigarette smoking reduces histone deacetylase 2 expression, enhances cytokine expression, and inhibits glucocorticoid actions in alveolar macrophages. FASEB J. 2001, 15:1110-1112.
22. Ito K., Ito M., Elliott W.M., Cosio B., Caramori G., Kon O.M., Barczyk A., Hayashi S., Adcock I.M., Hogg J.C., Barnes P.J. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N. Engl. J. Med. 2005, 352:1967-1976.
23. Ito K., Yamamura S., Essilfie-Quaye S., Cosio B., Ito M., Barnes P.J., Adcock I.M. Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-kappaB suppression. J. Exp. Med. 2006, 203:7-13.
24. Kasahara D.I., Poynter M.E., Othman Z., Hemenway D., van der Vliet A. Acrolein inhalation suppresses lipopolysaccharide-induced inflammatory cytokine production but does not affect acute airways neutrophilia. J. Immunol. 2008, 181:736-745.
25. Kehrer J.P., Biswal S.S. The molecular effects of acrolein. Toxicol. Sci. 2000, 57:6-15.
26. LoPachin R.M., Gavin T., Petersen D.R., Barber D.S. Molecular mechanisms of 4-hydroxy-2-nonenal and acrolein toxicity: nucleophilic targets and adduct formation. Chem. Res. Toxicol. 2009, 22:1499-1508.
27. Miyake K. Endotoxin recognition molecules, toll-like receptor 4-MD-2. Semin. Immunol. 2004, 16:11-16.
28. Moretto N., Facchinetti F., Southworth T., Civelli M., Singh D., Patacchini R. Alpha,beta-unsaturated aldehydes contained in cigarette smoke elicit IL-8 release in pulmonary cells through mitogen-activated protein kinases. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296:L839-L848.
29. Myers C.R., Myers J.M., Kufahl T.D., Forbes R., Szadkowski A. The effects of acrolein on the thioredoxin system: implications for redox-sensitive signaling. Mol. Nutr. Food Res. 2011, 55:1361-1374.
30. Nott A., Watson P.M., Robinson J.D., Crepaldi L., Riccio A. S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 2008, 455:411-415.
31. Oakley R.H., Cidlowski J.A. The biology of the glucocorticoid receptor: new signaling mechanisms in health and disease. J. Allergy Clin. Immunol. 2013, 132:1033-1044.
32. Rahman I., van Schadewijk A.A., Crowther A.J., Hiemstra P.S., Stolk J., MacNee W., De Boer W.I. 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2002, 166:490-495.
33. Rahman I., Kode A., Biswas S.K. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 2006, 1:3159-3165.
34. Rajendrasozhan S., Yang S.R., Kinnula V.L., Rahman I. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 2008, 177:861-870.
35. Randall M.J., Spiess P.C., Hristova M., Hondal R.J., van der Vliet A. Acrolein-induced activation of mitogen-activated protein kinase signaling is mediated by alkylation of thioredoxin reductase and thioredoxin 1. Redox Biol. 2013, 1:265-275.
36. Randall M.J., Hristova M., van der Vliet A. Protein alkylation by the alpha,beta-unsaturated aldehyde acrolein A reversible mechanism of electrophile signaling?. FEBS Lett. 2013, 587:3808-3814.
37. Reddy S., Finkelstein E.I., Wong P.S., Phung A., Cross C.E., van der Vliet A. Identification of glutathione modifications by cigarette smoke. Free Radic. Biol. Med. 2002, 33:1490-1498.
38. Reznick A.Z., Cross C.E., Hu M.L., Suzuki Y.J., Khwaja S., Safadi A., Motchnik P.A., Packer L., Halliwell B. Modification of plasma proteins by cigarette smoke as measured by protein carbonyl formation. Biochem. J. 1992, 286(Pt. 2):607-611.
39. Ruijters E.J., Haenen G.R., Weseler A.R., Bast A. The cocoa flavanol (-)-epicatechin protects the cortisol response. Pharmacol. Res. 2014, 79:28-33.
40. Ruud T.E., Gundersen Y., Krohn C.D., Sveen O., Aasen A.O. Effects of infliximab and hydrocortisone on in vitro cytokine responses after stimulation with lipopolysaccharide. Surg. Infect. (Larchmt) 2013, 14:30-34.
41. Spiess P.C., Deng B., Hondal R.J., Matthews D.E., van der Vliet A. Proteomic profiling of acrolein adducts in human lung epithelial cells. J. Proteomics 2011, 74(11):2380-2394.
42. Valacchi G., Pagnin E., Phung A., Nardini M., Schock B.C., Cross C.E., van der Vliet A. Inhibition of NFkappaB activation and IL-8 expression in human bronchial epithelial cells by acrolein. Antioxid. Redox Signal. 2005, 7:25-31.
43. van der Toorn M., Slebos D.J., de Bruin H.G., Gras R., Rezayat D., Jorge L., Sandra K., van Oosterhout A.J. Critical role of aldehydes in cigarette smoke-induced acute airway inflammation. Respir. Res. 2013, 14:45.
44. Winkler A.R., Nocka K.N., Williams C.M. Smoke exposure of human macrophages reduces HDAC3 activity, resulting in enhanced inflammatory cytokine production. Pulm. Pharmacol. Ther. 2012, 25:286-292.
45. Yadav U.C., Ramana K.V. Regulation of NF-kappaB-induced inflammatory signaling by lipid peroxidation-derived aldehydes. Oxid. Med. Cell. Longev. 2013, 2013:690545.
46. Yao H., Rahman I. Role of histone deacetylase 2 in epigenetics and cellular senescence: implications in lung inflammaging and COPD. Am. J. Physiol. Lung Cell. Mol. Physiol. 2012, 303:L557-L566.