Carbonylation caused by cigarette smoke extract is associated with defective macrophage immunity

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 2, 2011, Pages 229-236

  Bozinovski, Steven ^a   Vlahos, Ross ^a   Zhang, Yilin ^a   Lah, Lin Chin ^a   Seow, Huei Jiunn ^a   Mansell, Ashley ^b   Anderson, Gary P ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

Carbonylation; Macrophage immunity; TLR signaling

Indexed keywords

CIGARETTE SMOKE; GLUTATHIONE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 10; MITOGEN ACTIVATED PROTEIN KINASE P38; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; SUPPRESSOR OF CYTOKINE SIGNALING 1; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR IMMUNITY; GENE EXPRESSION; LUNG ALVEOLUS MACROPHAGE; MOUSE; NEUTROPHILIA; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; PROTEIN CARBONYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PSEUDOPODIUM; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUTATHIONE; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHAGOCYTOSIS; PHOSPHORYLATION; PROTEIN CARBONYLATION; RECEPTORS, INTERLEUKIN-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMOKING; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR AP-1; TUMOR NECROSIS FACTOR-ALPHA;

MUS;

EID: 80051629986     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0272OC     Document Type: Article

References (47)

1. Arcavi L, Benowitz NL. Cigarette smoking and infection. Arch Intern Med 2004;164:2206-2216. (Pubitemid 39452980)
2. Suzuki M, Thiem VD, Yanai H, Matsubayashi T, Yoshida LM, Tho LH, Minh TT, Anh DD, Kilgore PE, Ariyoshi K. Association of environmental tobacco smoking exposure with an increased risk of hospital admissions for pneumonia in children under 5 years of age in vietnam. Thorax 2009;64:484-489.
3. Liu BQ, Peto R, Chen ZM, Boreham J, Wu YP, Li JY, Campbell TC, Chen JS. Emerging tobacco hazards in China: 1. Retrospective proportional mortality study of one million deaths. BMJ 1998;317:1411-1422. (Pubitemid 28522092)
4. Stampfli MR, Anderson GP. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 2009;9:377-384.
5. Dye JA, Adler KB. Effects of cigarette smoke on epithelial cells of the respiratory tract. Thorax 1994;49:825-834. (Pubitemid 24250245)
6. Laan M, Bozinovski S, Anderson GP. Cigarette smoke inhibits lipopolysaccharide-induced production of inflammatory cytokines by suppressing the activation of activator protein-1 in bronchial epithelial cells. J Immunol 2004;173:4164-4170. (Pubitemid 39280782)
7. Birrell MA, Wong S, Catley MC, Belvisi MG. Impact of tobacco-smoke on key signaling pathways in the innate immune response in lung macrophages. J Cell Physiol 2008;214:27-37. (Pubitemid 350220056)
8. Chen H, Cowan MJ, Hasday JD, Vogel SN, Medvedev AE. Tobacco smoking inhibits expression of proinflammatory cytokines and activation of IL-1R-associated kinase, p38, and NF-kappaB in alveolar macrophages stimulated with TLR2 and TLR4 agonists. J Immunol 2007;179:6097-6106.
9. Gaschler GJ, Zavitz CC, Bauer CM, Skrtic M, Lindahl M, Robbins CS, Chen B, Stampfli MR. Cigarette smoke exposure attenuates cytokine production by mouse alveolar macrophages. Am J Respir Cell Mol Biol 2008;38:218-226. (Pubitemid 351162844)
10. Vayssier M, Favatier F, Pinot F, Bachelet M, Polla BS. Tobacco smoke induces coordinate activation of HSF and inhibition of NFkappaB in human monocytes: effects on TNFalpha release. Biochem Biophys Res Commun 1998;252:249-256. (Pubitemid 28534659)
11. Hodge S, Hodge G, Ahern J, Jersmann H, Holmes M, Reynolds PN. Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2007;37:748-755. (Pubitemid 350211645)
12. King TE Jr, Savici D, Campbell PA. Phagocytosis and killing of Listeria monocytogenes by alveolar macrophages: smokers versus non-smokers. J Infect Dis 1988;158:1309-1316. (Pubitemid 19023296)
13. Marti-Lliteras P, Regueiro V, Morey P, Hood DW, Saus C, Sauleda J, Agusti AG, Bengoechea JA, Garmendia J. Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect Immun 2009;77:4232-4242.
14. McMaster SK, Paul-Clark MJ, Walters M, Fleet M, Anandarajah J, Sriskandan S, Mitchell JA. Cigarette smoke inhibits macrophage sensing of Gram-negative bacteria and lipopolysaccharide: relative roles of nicotine and oxidant stress. Br J Pharmacol 2008;153:536-543. (Pubitemid 351199021)
15. Witherden IR, Vanden Bon EJ, Goldstraw P, Ratcliffe C, Pastorino U, Tetley TD. Primary human alveolar Type II epithelial cell chemokine release: effects of cigarette smoke and neutrophil elastase. Am J Respir Cell Mol Biol 2004;30:500-509. (Pubitemid 38457183)
16. Pryor WA, Stone K. Oxidants in cigarette smoke: radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci 1993;686:12-27.
17. Dalle-Donne I, Aldini G, Carini M, Colombo R, Rossi R, Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med 2006;10:389-406. (Pubitemid 44870187)
18. Dalle-Donne I, Carini M, Orioli M, Vistoli G, Regazzoni L, Colombo G, Rossi R, Milzani A, Aldini G. Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radic Biol Med 2009;46:1411-1419.
19. Stadtman ER. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 1993;62:797-821. (Pubitemid 23237888)
20. Vlahos R, Bozinovski S, Jones JE, Powell J, Gras J, Lilja A, Hansen MJ, Gualano RC, Irving L, Anderson GP. Differential protease, innate immunity, and Nf-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. Am J Physiol Lung Cell Mol Physiol 2006;290:L931-L945. (Pubitemid 43725055)
21. Bozinovski S, Jones J, Beavitt SJ, Cook AD, Hamilton JA, Anderson GP. Innate immune responses to LPS in mouse lung are suppressed and reversed by neutralization of GM-CSF via repression of TLR-4. Am J Physiol Lung Cell Mol Physiol 2004;286:L877-L885. (Pubitemid 38365075)
22. Mbawuike IN, Herscowitz HB. MH-S, a murine alveolar macrophage cell line: morphological, cytochemical, and functional characteristics. J Leukoc Biol 1989;46:119-127. (Pubitemid 19188065)
23. Liu K, Anderson GP, Bozinovski S. DNA vector augments inflammation in epithelial cells via EGFR-dependent regulation of TLR4 and TLR2. Am J Respir Cell Mol Biol 2008;39:305-311.
24. Liu K, Gualano RC, Hibbs ML, Anderson GP, Bozinovski S. Epidermal growth factor receptor signaling to Erk1/2 and STATS controls the intensity of the epithelial inflammatory responses to rhinovirus infection. J Biol Chem 2008;283:9977-9985.
25. Moodie FM, Marwick JA, Anderson CS, Szulakowski P, Biswas SK, Bauter MR, Kilty I, Rahman I. Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 2004;18:1897-1899. (Pubitemid 39602276)
26. Lang T, Mansell A. The negative regulation of Toll-like receptor and associated pathways. Immunol Cell Biol 2007;85:425-434. (Pubitemid 47367504)
27. Hasday JD, Bascom R, Costa JJ, Fitzgerald T, Dubin W. Bacterial endotoxin is an active component of cigarette smoke. Chest 1999;115:829-835. (Pubitemid 29129968)
28. Larsson L, Szponar B, Pehrson C. Tobacco smoking increases dramatically air concentrations of endotoxin. Indoor Air 2004;14:421-424. (Pubitemid 39523854)
29. Berenson CS, Garlipp MA, Grove LJ, Maloney J, Sethi S. Impaired phagocytosis of nontypeable Haemophilus influenzae by human alveolar macrophages in chronic obstructive pulmonary disease. J Infect Dis 2006;194:1375-1384. (Pubitemid 44706505)
30. Richens TR, Linderman DJ, Horstmann SA, Lambert C, Xiao YQ, Keith RL, Boe DM, Morimoto K, Bowler RP, Day BJ, et al. Cigarette smoke impairs clearance of apoptotic cells through oxidant-dependent activation of RhoA. Am J Respir Crit Care Med 2009;179:1011-1021.
31. Minematsu N, Blumental-Perry A, Shapiro SD. Cigarette smoke inhibits engulfment of apoptotic cells by macrophages through inhibition of actin rearrangement. Am J Respir Cell Mol Biol. 2011;44:472-482.
32. Banan A, Zhang Y, Losurdo J, Keshavarzian A. Carbonylation and disassembly of the F-actin cytoskeleton in oxidant induced barrier dysfunction and its prevention by epidermal growth factor and transforming growth factor alpha in a human colonic cell line. Gut 2000;46:830-837. (Pubitemid 30329079)
33. Bizzozero OA, Reyes S, Ziegler J, Smerjac S. Lipid peroxidation scavengers prevent the carbonylation of cytoskeletal brain proteins induced by glutathione depletion. Neurochem Res 2007;32:2114-2122. (Pubitemid 350059855)
34. Smerjac SM, Bizzozero OA. Cytoskeletal protein carbonylation and degradation in experimental autoimmune encephalomyelitis. J Neurochem 2008;105:763-772. (Pubitemid 351562723)
35. Taylor AE, Finney-Hayward TK, Quint JK, Thomas CM, Tudhope SJ, Wedzicha JA, Barnes PJ, Donnelly LE. Defective macrophage phagocytosis of bacteria in COPD. Eur Respir J 2010;35:1039-1047.
36. Muller T, Gebel S. The cellular stress response induced by aqueous extracts of cigarette smoke is critically dependent on the intracellular glutathione concentration. Carcinogenesis 1998;19:797-801. (Pubitemid 28376769)
37. Rahman I, MacNee W. Oxidative stress and regulation of glutathione in lung inflammation. Eur Respir J 2000;16:534-554.
38. Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A. Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem Sci 2009;34:85-96.
39. Reynaert NL, van der Vliet A, Guala AS, McGovern T, Hristova M, Pantano C, Heintz NH, Heim J, Ho YS, Matthews DE, et al. Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Acad Sci USA 2006;103:13086-13091. (Pubitemid 44338920)
40. Marshall HE, Hess DT, Stamler JS. S-nitrosylation: physiological regulation of NF-kappaB. Proc Natl Acad Sci USA 2004;101:8841-8842.
41. Into T, Inomata M, Nakashima M, Shibata K, Hacker H, Matsushita K. Regulation of MYD88-dependent signaling events by S nitrosylation retards Toll-like receptor signal transduction and initiation of acute-phase immune responses. Mol Cell Biol 2008;28:1338-1347. (Pubitemid 351214135)
42. Park SW, Huq MD, Hu X, Wei LN. Tyrosine nitration on p65: a novel mechanism to rapidly inactivate nuclear factor-kappaB. Mol Cell Proteomics 2005;4:300-309. (Pubitemid 40439773)
43. Lin CC, Su TH, Wang TS. Protein carbonylation in THP-1 cells induced by cigarette smoke extract via a copper-catalyzed pathway. Chem Res Toxicol 2009;22:1232-1238.
44. Bernhard D, Csordas A, Henderson B, Rossmann A, Kind M, Wick G. Cigarette smoke metal-catalyzed protein oxidation leads to vascular endothelial cell contraction by depolymerization of microtubules. FASEB J 2005;19:1096-1107. (Pubitemid 40946435)
45. Maisonneuve E, Ducret A, Khoueiry P, Lignon S, Longhi S, Talla E, Dukan S. Rules governing selective protein carbonylation. PLoS ONE 2009;4:e7269.
46. Starosta V, Griese M. Protein oxidation by chronic pulmonary diseases in children. Pediatr Pulmonol 2006;41:67-73. (Pubitemid 43117370)
47. Mikerov AN, Umstead TM, Gan X, Huang W, Guo X, Wang G, Phelps DS, Floros J. Impact of ozone exposure on the phagocytic activity of human surfactant protein A (SP-A) and SP-A variants. Am J Physiol Lung Cell Mol Physiol 2008;294:L121-L130. (Pubitemid 351380324)