Cigarette smoke and its component acrolein augment IL-8/CXCL8 mRNA stability via p38 MAPK/MK2 signaling in human pulmonary cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 303, Issue 10, 2012, Pages

  Moretto, Nadia ^a   Bertolini, Serena ^a   Iadicicco, Claudia ^a   Marchini, Gessica ^a   Kaur, Manminder ^b   Volpi, Giorgia ^a   Patacchini, Riccardo ^a   Singh, Dave ^b   Facchinetti, Fabrizio ^a  

^a Chiesi Farmaceutici ^*  (Italy)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Airway epithelial cells; Alveolar macrophages; Bronchial smooth muscle cells; MK2; p38 MAPK

Indexed keywords

ACROLEIN; CIGARETTE SMOKE; INTERLEUKIN 8; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADULT; ARTICLE; BRONCHUS MUSCLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME STABILITY; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN TISSUE; LEUKOCYTE ACTIVATION; LUNG ALVEOLUS CELL; LUNG ALVEOLUS MACROPHAGE; MALE; NEUTROPHIL CHEMOTAXIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM; SIGNAL TRANSDUCTION; STEADY STATE; UPREGULATION;

ACROLEIN; BRONCHI; CELLS, CULTURED; CHEMOTAXIS; DACTINOMYCIN; EPITHELIAL CELLS; FEMALE; HUMANS; INTERLEUKIN-8; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MAP KINASE SIGNALING SYSTEM; MIDDLE AGED; MYOCYTES, SMOOTH MUSCLE; NEUTROPHIL ACTIVATION; NEUTROPHILS; NUCLEIC ACID SYNTHESIS INHIBITORS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PNEUMONIA; PROTEIN-SERINE-THREONINE KINASES; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; RESPIRATORY MUCOSA; RNA STABILITY; RNA, MESSENGER; TOBACCO SMOKE POLLUTION;

EID: 84869176820     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00046.2012     Document Type: Article

References (44)

1. Anderson DR, Meyers MJ, Vernier WF, Mahoney MW, Kurumbail RG, Caspers N, Poda GI, Schindler JF, Reitz DB, Mourey RJ. Pyrrolopyridine inhibitors of mitogen-activated protein kinase-activated protein kinase 2 (MK-2). J Med Chem 50: 2647-2654, 2007.
2. Bain J, Plater L, Elliott M, Shapiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P. The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315, 2007.
3. Barnes PJ. Chronic obstructive pulmonary disease. N Engl J Med 343: 269-280, 2000.
4. Barnes PJ. Alveolar macrophages as orchestrators of COPD. COPD 1: 59-70, 2004.
5. Bezzerri V, Borgatti M, Finotti A, Tamanini A, Gambari R, Cabrini G. Mapping the transcriptional machinery of the IL-8 gene in human bronchial epithelial cells. J Immunol 187: 6069-6081, 2011.
6. Bhattacharyya S, Gutti U, Mercado J, Moore C, Pollard HB, Biswas R. MAPK signaling pathways regulate IL-8 mRNA stability and IL-8 protein expression in cystic fibrosis lung epithelial cell lines. Am J Physiol Lung Cell Mol Physiol 300: L81-L87, 2011.
7. Bourcier C, Griseri P, Grépin R, Bertolotto C, Mazure N, Pagès G. Constitutive ERK activity induces downregulation of tristetraprolin, a major protein controlling interleukin8/CXCL8 mRNA stability in melanoma cells. Am J Physiol Cell Physiol 301: C609-C618, 2011.
8. Brook M, Tchen CR, Santalucia T, McIlrath J, Arthur JS, Saklatvala J, Clark AR. Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol Cell Biol 26: 2408-2418, 2006.
9. Corradi M, Rubinstein I, Andreoli R, Manini P, Caglieri A, Poli D, Alinovi R, Mutti A. Comparison between exhaled and sputum oxidative stress biomarkers in chronic airway inflammation. Eur Respir J 24: 1011-7, 2004.
10. Chung KF. Airway smooth muscle cells: contributing to and regulating airway mucosal inflammation. Eur Respir J 15: 961-968, 2000.
11. Eiserich JP, van der Vliet A, Handelman GJ, Halliwell B, Cross CE. Dietary antioxidants and cigarette smoke-induced biomolecular damage: a complex interaction. Am J Clin Nutr 62: 1490S-1500S, 1995.
12. Facchinetti F, Amadei F, Geppetti P, Tarantini F, Di Serio C, Dragotto A, Gigli PM, Catinella S, Civelli M, Patacchini R. Alpha, betaunsaturated aldehydes in cigarette smoke release inflammatory mediators from human macrophages. Am J Respir Cell Mol Biol 37: 617-623, 2007.
13. Gesser B, Lund M, Lohse N, Vestergaad C, Matsushima K, Sindet-Pedersen S, Jensen SL, Thestrup-Pedersen K, Larsen CG. IL-8 induces T cell chemotaxis, suppresses IL-4, and upregulates IL-8 production by CD4+ T cells. J Leukoc Biol 59: 407-411, 1996.
14. Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell 109 Suppl: S81-S96, 2002.
15. Govindaraju V, Michoud MC, Al-Chalabi M, Ferraro P, Powell WS, Martin JG. Interleukin-8: novel roles in human airway smooth muscle cell contraction and migration. Am J Physiol Cell Physiol 291: C957-C965, 2006.
16. Hansen MB, Nielsen SE, Berg K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J Immunol Methods 119: 203-210, 1989.
17. Harada A, Mukaida N, Matsushima K. Interleukin 8 as a novel target for intervention therapy in acute inflammatory diseases. Mol Med Today 2: 482-9, 1996.
18. Harris JO, Gonzalez-Rothi RJ. Abnormal phagolysosome fusion in pulmonary alveolar macrophages of rats exposed chronically to cigarette smoke. Am Rev Respir Dis 130: 467-471, 1984.
19. Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M. Multiple control of interleukin-8 gene expression. J Leukoc Biol 72: 847-855, 2002.
20. Howarth PH, Knox AJ, Amrani Y, Tliba O, Panettieri RA, Johnson M. Synthetic responses in airway smooth muscle. J Allergy Clin Immunol 114: S32-S50, 2004.
21. Jorens PG, Richman-Eisenstat JB, Housset BP, Graf PD, Ueki IF, Olesch J, Nadel JA. Interleukin-8 induces neutrophil accumulation but not protease secretion in the canine trachea. Am J Physiol Lung Cell Mol Physiol 263: L708-L713, 1992.
22. 2-adrenoceptor agonists and other cAMP-elevating agents on inflammatory gene expression in human ASM cells: a role for protein kinase A. Am J Physiol Lung Cell Mol Physiol 295: L505-L514, 2008.
23. Keatings VM, Collins PD, Scott DM, Barnes PJ. 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: 530-534, 1996.
24. Kent LM, Smyth LJ, Plumb J, Clayton CL, Fox SM, Ray DW, Farrow SN, Singh D. Inhibition of lipopolysaccharide-stimulated chronic obstructive pulmonary disease macrophage inflammatory gene expression by dexamethasone and the p38 mitogen-activated protein kinase inhibitor N-cyano-N'-(2-{[8-(2,6-difluorophenyl)-4-(4-fluoro-2-methylphenyl)-7-oxo-7,8-dihydropyrido[2,3-d] pyrimidin-2-yl]amino}ethyl)guanidine (SB706504). J Pharmacol Exp Ther 328: 458-468, 2009.
25. Kowalski J, Denhardt DT. Regulation of the mRNA for monocytederived neutrophil-activating peptide in differentiating HL60 promyelocytes. Mol Cell Biol 9: 1946-1957, 1989.
26. Kunsch C, Rosen CA. NF-kappa B subunit-specific regulation of the interleukin-8 promoter. Mol Cell Biol 13: 6137-6146, 1993.
27. Lambert C, Li J, Jonscher K, Yang TC, Reigan P, Quintana M, Harvey J, Freed BM. Acrolein inhibits cytokine gene expression by alkylating cysteine and arginine residues in the NF-kappaB1 DNA binding domain. J Biol Chem 282: 19666-19675, 2007.
28. Li J, Kartha S, Iasvovskaia S, Tan A, Bhat RK, Manaligod JM, Page K, Brasier AR, Hershenson MB. Regulation of human airway epithelial cell IL-8 expression by MAP kinases. Am J Physiol Lung Cell Mol Physiol 283: L690-L699, 2002.
29. Lomas DA, Lipson DA, Miller BE, Willits L, Keene O, Barnacle H, Barnes NC, Tal-Singer R; Losmapimod Study Investigators. An oral inhibitor of p38 MAP kinase reduces plasma fibrinogen in patients with chronic obstructive pulmonary disease. J Clin Pharmacol 52: 416-424, 2012
30. Luscinskas FW, Gerszten RE, Garcia-Zepeda EA, Lim YC, Yoshida M, Ding HA, Gimbrone MA Jr, Luster AD, Rosenzweig A. C-C and C-X-C chemokines trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Ann NY Acad Sci 902: 288-293, 2000.
31. Moretto N, Facchinetti F, Southworth T, Civelli M, Singh D, Patacchini R. α, β-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 296: L839-L848, 2009.
32. Moretto N, Volpi G, Pastore F, Facchinetti F. Acrolein effects in pulmonary cells: relevance to chronic obstructive pulmonary disease. Ann NY Acad Sci 1259: 39-46, 2012.
33. Mourey RJ, Burnette BL, Brustkern SJ, Daniels JS, Hirsch JL, Hood WF, Meyers MJ, Mnich SJ, Pierce BS, Saabye MJ, Schindler JF, South SA, Webb EG, Zhang J, Anderson DR. A benzothiophene inhibitor of mitogen-activated protein kinase-activated protein kinase 2 inhibits tumor necrosis factor alpha production and has oral anti-inflammatory efficacy in acute and chronic models of inflammation. J Pharmacol Exp Ther 333: 797-807, 2010.
34. Mukaida N, Mahe Y, Matsushima K. Cooperative interaction of nuclear factor-kappa B-and cis-regulatory enhancer binding protein-like factor binding elements in activating the interleukin-8 gene by pro-inflammatory cytokines. J Biol Chem 265: 21128-21133, 1990.
35. Ohori M, Takeuchi M, Maruki R, Nakajima H, Miyake H. FR180204, a novel and selective inhibitor of extracellular signal-regulated kinase, ameliorates collagen-induced arthritis in mice. Naunyn Schmiedebergs Arch Pharmacol 374: 311-316, 2007.
36. Oltmanns U, Chung KF, Walters M, John M, Mitchell JA. Cigarette smoke induces IL-8, but inhibits eotaxin and RANTES release from airway smooth muscle. Respir Res 6: 74, 2005.
37. Pang L, Knox AJ. Bradykinin stimulates IL-8 production in cultured human airway smooth muscle cells: role of cyclooxygenase products. J Immunol 161: 2509-2515, 1998.
38. Pankow W, Neumann K, Ruschoff J, von Wichert P. Human alveolar macrophages: comparison of cell size, autofluorescence, and HLA-DR antigen expression in smokers and nonsmokers. Cancer Detect Prev 19: 268-273, 1995.
39. Pesci A, Balbi B, Majori M, Cacciani G, Bertacco S, Alciato P, Donner CF. Inflammatory cells and mediators in bronchial lavage of patients with chronic obstructive pulmonary disease. Eur Respir J 12: 380-386, 1998.
40. Ronkina N, Menon MB, Schwermann J, Tiedje C, Hitti E, Kotlyarov A, Gaestel M. MAPKAP kinases MK2 and MK3 in inflammation: complex regulation of TNF biosynthesis via expression and phosphorylation of tristetraprolin. Biochem Pharmacol 80: 1915-1920, 2010.
41. Schlapbach A, Huppertz C. Low-molecular-weight MK2 inhibitors: a tough nut to crack! Future Med Chem 1: 1243-1257, 2009.
42. Srinivasan S, Yeh M, Danziger EC, Hatley ME, Riggan AE, Leitinger N, Berliner JA, Hedrick CC. Glucose regulates monocyte adhesion through endothelial production of interleukin-8. Circ Res 92: 371-377, 2003
43. Stedman RL. The chemical composition of tobacco and tobacco smoke. Chem Rev 68: 153-207, 1968.
44. Volpi G, Facchinetti F, Moretto N, Civelli M, Patacchini R. Cigarette smoke and α, β-unsaturated aldehydes elicit VEGF release through the p38 MAPK pathway in human airway smooth muscle cells and lung fibroblasts. Br J Pharmacol 163: 649-661, 2011.