MAPK- and PKC/CREB-dependent induction of interleukin-11 by the environmental contaminant formaldehyde in human bronchial epithelial cells

Toxicology

Volumn 292, Issue 1, 2012, Pages 13-22

  Lecureur, Valérie ^a   Arzel, Matthieu ^a   Ameziane, Sarah ^a   Houlbert, Noémie ^a   Le Vee, Marc ^a   Jouneau, Stéphane ^a,b   Fardel, Olivier ^a,c  

^a UNIVERSITÉ DE RENNES 1   (France)

^b Service de pneumologie   (France)

^c RENNES UNIVERSITY HOSPITAL   (France)

Author keywords

CREB; Formaldehyde; Interleukin 11; Lung epithelial cells; MAPK

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CHEMOKINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKINE; FORMALDEHYDE; INTERLEUKIN 11; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE C; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA1; VOLATILE ORGANIC COMPOUND;

ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; FIBROGENESIS; HUMAN; HUMAN CELL; INDOOR AIR POLLUTION; INTERFERON INDUCTION; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; PNEUMONIA; PRIORITY JOURNAL; UPREGULATION;

CELL LINE; CELL LINE, TUMOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENVIRONMENTAL POLLUTANTS; FORMALDEHYDE; HUMANS; INTERLEUKIN-11; MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE C; RECOMBINANT PROTEINS; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION;

EID: 84855316986     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.11.011     Document Type: Article

References (55)

1. Aggarwal S., Kim S.W., Cheon K., Tabassam F.H., Yoon J.H., Koo J.S. Nonclassical action of retinoic acid on the activation of the cAMP response element-binding protein in normal human bronchial epithelial cells. Mol. Biol. Cell 2006, 17:566-575.
2. Akagawa K.S. Functional heterogeneity of colony-stimulating factor-induced human monocyte-derived macrophages. Int. J. Hematol. 2002, 76:27-34.
3. Bamba S., Andoh A., Yasui H., Makino J., Kim S., Fujiyama Y. Regulation of IL-11 expression in intestinal myofibroblasts: role of c-Jun AP-1- and MAPK-dependent pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285:G529-G538.
4. Barlow C.A., Barrett T.F., Shukla A., Mossman B.T., Lounsbury K.M. Asbestos-mediated CREB phosphorylation is regulated by protein kinase A and extracellular signal-regulated kinases 1/2. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292:L1361-L1369.
5. Casset A., Marchand C., Purohit A., le Calve S., Uring-Lambert B., Donnay C., Meyer P., de Blay F. Inhaled formaldehyde exposure: effect on bronchial response to mite allergen in sensitized asthma patients. Allergy 2006, 61:1344-1350.
6. Coker R.K., Laurent G.J. Pulmonary fibrosis: cytokines in the balance. Eur. Respir. J. 1998, 11:1218-1221.
7. Delfino R.J. Epidemiologic evidence for asthma and exposure to air toxics: linkages between occupational, indoor, and community air pollution research. Environ. Health Perspect. 2002, 110(Suppl. 4):573-589.
8. Delghandi M.P., Johannessen M., Moens U. The cAMP signalling pathway activates CREB through PKA, p38 and MSK1 in NIH 3T3 cells. Cell. Signal. 2005, 17:1343-1351.
9. Du X., Williams D.A. Interleukin-11: review of molecular, cell biology, and clinical use. Blood 1997, 89:3897-3908.
10. Einarsson O., Geba G.P., Zhu Z., Landry M., Elias J.A. Interleukin-11: stimulation in vivo and in vitro by respiratory viruses and induction of airways hyperresponsiveness. J. Clin. Invest. 1996, 97:915-924.
11. Elias J.A., Zheng T., Einarsson O., Landry M., Trow T., Rebert N., Panuska J. Epithelial interleukin-11. Regulation by cytokines, respiratory syncytial virus, and retinoic acid. J. Biol. Chem. 1994, 269:22261-22268.
12. Elias J.A., Zheng T., Whiting N.L., Trow T.K., Merrill W.W., Zitnik R., Ray P., Alderman E.M. IL-1 and transforming growth factor-beta regulation of fibroblast-derived IL-11. J. Immunol. 1994, 152:2421-2429.
13. Ezratty V., Bonay M., Neukirch C., Orset-Guillossou G., Dehoux M., Koscielny S., Cabanes P.A., Lambrozo J., Aubier M. Effect of formaldehyde on asthmatic response to inhaled allergen challenge. Environ. Health Perspect. 2007, 115:210-214.
14. Franklin P., Dingle P., Stick S. Raised exhaled nitric oxide in healthy children is associated with domestic formaldehyde levels. Am. J. Respir. Crit. Care Med. 2000, 161:1757-1759.
15. Gallelli L., Pelaia G., D'Agostino B., Cuda G., Vatrella A., Fratto D., Gioffre V., Galderisi U., De Nardo M., Mastruzzo C., Salinaro E.T., Maniscalco M., Sofia M., Crimi N., Rossi F., Caputi M., Costanzo F.S., Maselli R., Marsico S.A., Vancheri C. Endothelin-1 induces proliferation of human lung fibroblasts and IL-11 secretion through an ET(A) receptor-dependent activation of MAP kinases. J. Cell. Biochem. 2005, 96:858-868.
16. Garrett M.H., Hooper M.A., Hooper B.M., Rayment P.R., Abramson M.J. Increased risk of allergy in children due to formaldehyde exposure in homes. Allergy 1999, 54:330-337.
17. Gerthoffer W.T., Singer C.A. MAPK regulation of gene expression in airway smooth muscle. Respir. Physiol. Neurobiol. 2003, 137:237-250.
18. Heinrich P.C., Behrmann I., Muller-Newen G., Schaper F., Graeve L. Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochem. J. 1998, 334(Pt 2):297-314.
19. Hester S.D., Benavides G.B., Yoon L., Morgan K.T., Zou F., Barry W., Wolf D.C. Formaldehyde-induced gene expression in F344 rat nasal respiratory epithelium. Toxicology 2003, 187:13-24.
20. Im H., Oh E., Mun J., Khim J.Y., Lee E., Kang H.S., Kim E., Kim H., Won N.H., Kim Y.H., Jung W.W., Sul D. Evaluation of toxicological monitoring markers using proteomic analysis in rats exposed to formaldehyde. J. Proteome Res. 2006, 5:1354-1366.
21. Iordanov M., Bender K., Ade T., Schmid W., Sachsenmaier C., Engel K., Gaestel M., Rahmsdorf H.J., Herrlich P. CREB is activated by UVC through a p38/HOG-1-dependent protein kinase. EMBO J. 1997, 16:1009-1022.
22. Johannessen M., Delghandi M.P., Seternes O.M., Johansen B., Moens U. Synergistic activation of CREB-mediated transcription by forskolin and phorbol ester requires PKC and depends on the glutamine-rich Q2 transactivation domain. Cell. Signal. 2004, 16:1187-1199.
23. Jung W.W., Kim E.M., Lee E.H., Yun H.J., Ju H.R., Jeong M.J., Hwang K.W., Sul D., Kang H.S. Formaldehyde exposure induces airway inflammation by increasing eosinophil infiltrations through the regulation of reactive oxygen species production. Environ. Toxicol. Pharmacol. 2007, 24:174-182.
24. Kastner P.E., Casset A., Pons F. Formaldehyde interferes with airway epithelium integrity and functions in a dose- and time-dependent manner. Toxicol. Lett. 2010, 200:109-116.
25. Kawaguchi M., Fujita J., Kokubu F., Huang S.K., Homma T., Matsukura S., Adachi M., Hizawa N. IL-17F-induced IL-11 release in bronchial epithelial cells via MSK1-CREB pathway. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 296:L804-L810.
26. Keller D.C., Du X.X., Srour E.F., Hoffman R., Williams D.A. Interleukin-11 inhibits adipogenesis and stimulates myelopoiesis in human long-term marrow cultures. Blood 1993, 82:1428-1435.
27. Lecureur V., Le Ferrec E., N'Diaye M., Le Vée M., Gardyn C., Gilot D., Fardel O. ERK-dependent induction of TNFalpha expression by the environmental contaminant benzo(a)pyrene in primary human macrophages. FEBS Lett. 2005, 579:1904-1910.
28. Lee C.G., Hartl D., Matsuura H., Dunlop F.M., Scotney P.D., Fabri L.J., Nash A.D., Chen N.Y., Tang C.Y., Chen Q., Homer R.J., Baca M., Elias J.A. Endogenous IL-11 signaling is essential in Th2- and IL-13-induced inflammation and mucus production. Am. J. Respir. Cell Mol. Biol. 2008, 39:739-746.
29. Lee K.S., Kim S.R., Park H.S., Park S.J., Min K.H., Lee K.Y., Jin S.M., Lee Y.C. Cysteinyl leukotriene upregulates IL-11 expression in allergic airway disease of mice. J. Allergy Clin. Immunol. 2007, 119:141-149.
30. Li L., Fan D., Wang C., Wang J.Y., Cui X.B., Wu D., Zhou Y., Wu L.L. Angiotensin II increases periostin expression via Ras/p38 MAPK/CREB and ERK1/2/TGF-beta1 pathways in cardiac fibroblasts. Cardiovasc. Res. 2011, 91:80-89.
31. Lim S.K., Kim J.C., Moon C.J., Kim G.Y., Han H.J., Park S.H. Formaldehyde induces apoptosis through decreased Prx 2 via p38 MAPK in lung epithelial cells. Toxicology 2010, 271:100-106.
32. Lino dos Santos Franco A., Damazo A.S., Beraldo de Souza H.R., Domingos H.V., Oliveira-Filho R.M., Oliani S.M., Costa S.K., Tavares de Lima W. Pulmonary neutrophil recruitment and bronchial reactivity in formaldehyde-exposed rats are modulated by mast cells and differentially by neuropeptides and nitric oxide. Toxicol. Appl. Pharmacol. 2006, 214:35-42.
33. Liu F., Thompson M.A., Wagner S., Greenberg M.E., Green M.R. Activating transcription factor-1 can mediate Ca(2+)- and cAMP-inducible transcriptional activation. J. Biol. Chem. 1993, 268:6714-6720.
34. Marwood M., Visser K., Salamonsen L.A., Dimitriadis E. Interleukin-11 and leukemia inhibitory factor regulate the adhesion of endometrial epithelial cells: implications in fertility regulation. Endocrinology 2009, 150:2915-2923.
35. McGwin G., Lienert J., Kennedy J.I. Formaldehyde exposure and asthma in children: a systematic review. Environ. Health Perspect. 2010, 118:313-317.
36. Minshall E., Chakir J., Laviolette M., Molet S., Zhu Z., Olivenstein R., Elias J.A., Hamid Q. IL-11 expression is increased in severe asthma: association with epithelial cells and eosinophils. J. Allergy Clin. Immunol. 2000, 105:232-238.
37. Norback D., Bjornsson E., Janson C., Widstrom J., Boman G. Asthmatic symptoms and volatile organic compounds, formaldehyde, and carbon dioxide in dwellings. Occup. Environ. Med. 1995, 52:388-395.
38. Ohtsuka R., Shutoh Y., Fujie H., Yamaguchi S., Takeda M., Harada T., Doi K. Rat strain difference in histology and expression of Th1- and Th2-related cytokines in nasal mucosa after short-term formaldehyde inhalation. Exp. Toxicol. Pathol. 2003, 54:287-291.
39. Palmqvist P., Lundberg P., Lundgren I., Hanstrom L., Lerner U.H. IL-1beta and TNF-alpha regulate IL-6-type cytokines in gingival fibroblasts. J. Dent. Res. 2008, 87:558-563.
40. Pelaia G., Gallelli L., D'Agostino B., Vatrella A., Cuda G., Fratto D., Renda T., Galderisi U., Piegari E., Crimi N., Rossi F., Caputi M., Costanzo F.S., Vancheri C., Maselli R., Marsico S.A. Effects of TGF-beta and glucocorticoids on map kinase phosphorylation, IL-6/IL-11 secretion and cell proliferation in primary cultures of human lung fibroblasts. J. Cell. Physiol. 2007, 210:489-497.
41. Persoz C., Achard S., Leleu C., Momas I., Seta N. An in vitro model to evaluate the inflammatory response after gaseous formaldehyde exposure of lung epithelial cells. Toxicol. Lett. 2010, 195:99-105.
42. Rager J.E., Smeester L., Jaspers I., Sexton K.G., Fry R.C. Epigenetic changes induced by air toxics: formaldehyde exposure alters miRNA expression profiles in human lung cells. Environ. Health Perspect. 2011, 119:494-500.
43. Roda C., Kousignian I., Guihenneuc-Jouyaux C., Dassonville C., Nicolis I., Just J., Momas I. Formaldehyde exposure and lower respiratory infections in infants: findings from the PARIS cohort study. Environ. Health Perspect. 2011, 119:1653-1658.
44. Rolli M., Kotlyarov A., Sakamoto K.M., Gaestel M., Neininger A. Stress-induced stimulation of early growth response gene-1 by p38/stress-activated protein kinase 2 is mediated by a cAMP-responsive promoter element in a MAPKAP kinase 2-independent manner. J. Biol. Chem. 1999, 274:19559-19564.
45. Rumchev K.B., Spickett J.T., Bulsara M.K., Phillips M.R., Stick S.M. Domestic exposure to formaldehyde significantly increases the risk of asthma in young children. Eur. Respir. J. 2002, 20:403-408.
46. Sands W.A., Palmer T.M. Regulating gene transcription in response to cyclic AMP elevation. Cell. Signal. 2008, 20:460-466.
47. Shaywitz A.J., Greenberg M.E. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem 1999, 68:821-861.
48. Suen Y., Chang M., Lee S.M., Buzby J.S., Cairo M.S. Regulation of interleukin-11 protein and mRNA expression in neonatal and adult fibroblasts and endothelial cells. Blood 1994, 84:4125-4134.
49. Taki H., Sakai T., Sugiyama E., Mino T., Kuroda A., Taki K., Hamazaki T., Koizumi H., Kobayashi M. Monokine stimulation of interleukin-11 production by human vascular smooth muscle cells in vitro. Atherosclerosis 1999, 144:375-380.
50. Tang W., Geba G.P., Zheng T., Ray P., Homer R.J., Kuhn C., Flavell R.A., Elias J.A. Targeted expression of IL-11 in the murine airway causes lymphocytic inflammation, bronchial remodeling, and airways obstruction. J. Clin. Invest. 1996, 98:2845-2853.
51. Wieslander G., Norback D., Edling C. Airway symptoms among house painters in relation to exposure to volatile organic compounds (VOCS) - a longitudinal study. Ann. Occup. Hyg. 1997, 41:155-166.
52. Zhang L., Steinmaus C., Eastmond D.A., Xin X.K., Smith M.T. Formaldehyde exposure and leukemia: a new meta-analysis and potential mechanisms. Mutat. Res. 2009, 681:150-168.
53. Zheng T., Nathanson M.H., Elias J.A. Histamine augments cytokine-stimulated IL-11 production by human lung fibroblasts. J. Immunol. 1994, 153:4742-4752.
54. Zhong S., Jansen C., She Q.B., Goto H., Inagaki M., Bode A.M., Ma W.Y., Dong Z. Ultraviolet B-induced phosphorylation of histone H3 at serine 28 is mediated by MSK1. J. Biol. Chem. 2001, 276:33213-33219.
55. Zhu Z., Lee C.G., Zheng T., Chupp G., Wang J., Homer R.J., Noble P.W., Hamid Q., Elias J.A. Airway inflammation and remodeling in asthma. Lessons from interleukin 11 and interleukin 13 transgenic mice. Am. J. Respir. Crit. Care Med. 2001, 164:S67-S70.