PPARγ inhibits airway epithelial cell inflammatory response through a MUC1-dependent mechanism

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 7, 2012, Pages

  Park, Yong Sung ^a   Lillehoj, Erik P ^b   Kato, Kosuke ^a   Park, Choon Sik ^c   Kim, Kwang Chul ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c Soonchunhyang University   (South Korea)

Author keywords

Lung; Peroxisome proliferator associated receptor ; PMA; Pseudomonas aeruginosa

Indexed keywords

INTERLEUKIN 8; LUCIFERASE; MESSENGER RNA; MUCIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHORBOL 13 ACETATE 12 MYRISTATE; TROGLITAZONE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EPITHELIUM CELL; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; REPORTER GENE; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT INFLAMMATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; CELL LINE; CHROMANS; EPITHELIAL CELLS; HUMANS; INTERLEUKIN-8; LUNG; MALE; MICE; MUCIN-1; MUCOUS MEMBRANE; PPAR GAMMA; PROMOTER REGIONS, GENETIC; PSEUDOMONAS AERUGINOSA; RNA, MESSENGER; TETRADECANOYLPHORBOL ACETATE; THIAZOLIDINEDIONES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84859473933     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00360.2011     Document Type: Article

References (62)

1. 2-adrenergic receptor expression in human airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 281: L1271-L1278, 2001.
2. Arnold R, Rihoux J, König W. Cetirizine counter-regulates interleukin-8 release from human epithelial cells (A549). Clin Exp Allergy 29: 1681-1691, 1999.
3. Baek SJ, Wilson LC, Hsi LC, Eling TE. Troglitazone, a peroxisome proliferator-activated receptor γ (PPAR γ) ligand, selectively induces the early growth response-1 gene independently of PPARγ. A novel mechanism for its anti-tumorigenic activity. J Biol Chem 278: 5845-5853, 2003.
4. Belvisi MG, Hele DJ, Birrell MA. Peroxisome proliferator-activated receptor γ agonists as therapy for chronic airway inflammation. Eur J Pharmacol 533: 101-109, 2006.
5. Belvisi MG, Mitchell JA. Targeting PPAR receptors in the airway for the treatment of inflammatory lung disease. Br J Pharmacol 158: 994-1003, 2009.
6. Blanquart C, Barbier O, Fruchart JC, Staels B, Glineur C. Peroxisome proliferator-activated receptors: regulation of transcriptional activities and roles in inflammation. J Steroid Biochem Mol Biol 85: 267-273, 2003.
7. Carlo T, Levy BD. Chemical mediators and the resolution of airway inflammation. Allergol Int 57: 299-305, 2008.
8. Choi S, Park YS, Koga T, Treloar A, Kim KC. TNF-is a key regulator of MUC1, an anti-inflammatory molecule, during airway Pseudomonas aeruginosa infection. Am J Respir Cell Mol Biol 44: 255-260, 2011.
9. Clarke N, Germain P, Altucci L, Gronemeyer H. Retinoids: Potential in cancer prevention and therapy. Expert Rev Mol Med 6: 1-23, 2004.
10. Croce MV, Isla-Larrain M, Remes-Lenicov F, Colussi AG, Lacunza E, Kim KC, Gendler SJ, Segal-Eiras A. MUC1 cytoplasmic tail detection using CT33 polyclonal and CT2 monoclonal antibodies in breast and colorectal tissue. Histol Histopathol 21: 849-855, 2006.
11. Daynes RA, Jones DC. Emerging roles of PPARs in inflammation and immunity. Nat Rev Immunol 2: 748-759, 2002.
12. Delerive P, Fruchart JC, Staels B. Peroxisome proliferator-activated receptors in inflammation control. J Endocrinol 169: 453-459, 2001.
13. Dolinay T, Szilasi M, Liu M, Choi AM. Inhaled carbon monoxide confers antiinflammatory effects against ventilator-induced lung injury. Am J Respir Crit Care Med 170: 613-620, 2004.
14. Fajas L, Auboeuf D, Raspe E, Schoonjans K, Lefebvre AM, Saladin R, Najib J, Laville M, Fruchart JC, Deeb S, Vidal-Puig A, Flier J, Briggs MR, Staels B, Vidal H, Auwerx J. The organization, promoter analysis, and expression of the human PPAR_ gene. J Biol Chem 272: 18779-18789, 1997.
15. Fitzgerald MF, Fox JC. Emerging trends in the therapy of COPD: novel anti-inflammatory agents in clinical development. Drug Discov Today 12: 479-486, 2007.
16. Giaginis C, Giagini A, Theocharis S. Peroxisome proliferator-activated receptor-(PPAR-_) ligands as potential therapeutic agents to treat arthritis. Pharmacol Res 60: 160-169, 2009.
17. Guang W, Ding H, Czinn SJ, Kim KC, Blanchard TG, Lillehoj EP. Muc1 cell surface mucin attenuates epithelial inflammation in response to a common mucosal pathogen. J Biol Chem 285: 20547-20557, 2010.
18. Haworth O, Levy BD. Endogenous lipid mediators in the resolution of airway inflammation. Eur Respir J 30: 980-992, 2007.
19. Hisatsune A, Hyun SW, Lee IJ, Georas S, Kim KC. YY1 transcription factor is not responsible for the negative regulation of hamster Muc1 transcription. Anticancer Res 24: 235-240, 2004.
20. Holden NS, Tacon CE. Principles and problems of the electrophoretic mobility shift assay. J Pharmacol Toxicol Methods 63: 7-14, 2011.
21. Holden NS, Squires PE, Kaur M, Bland R, Jones CE, Newton R. Phorbol ester-stimulated NF-_B-dependent transcription: roles for isoforms of novel protein kinase C. Cell Signal 20: 1338-1348, 2008.
22. Jany B, Betz R, Schreck R. Activation of the transcription factor NF-_B in human tracheobronchial epithelial cells by inflammatory stimuli. Eur Respir J 8: 387-391, 1995.
23. Jiang C, Ting AT, Seed B. PPAR-agonists inhibit production of monocyte inflammatory cytokines. Nature 391: 82-86, 1998.
24. Jimenez-Lara AM, Clarke N, Altucci L, Gronemeyer H. Retinoic-acidinduced apoptosis in leukemia cells. Trends Mol Med 10: 508-515, 2004.
25. Kim KC, Lillehoj EP. MUC1 mucin: a peacemaker in the lung. Am J Respir Cell Mol Biol 39: 644-647, 2008.
26. Kim SR, Lee KS, Park HS, Park SJ, Min KH, Jin SM, Lee YC. Involvement of IL-10 in peroxisome proliferator-activated receptor _-mediated anti-inflammatory response in asthma. Mol Pharmacol 68: 1568-1575, 2005.
27. Kodera Y, Takeyama K, Murayama A, Suzawa M, Masuhiro Y, Kato S. Ligand type-specific interactions of peroxisome proliferator-activated receptor _ with transcriptional coactivators. J Biol Chem 275: 33201-33204, 2000.
28. Koga T, Kuwahara I, Lillehoj EP, Lu W, Miyata T, Isohama Y, Kim KC. TNF-induces MUC1 gene transcription in lung epithelial cells: its signaling pathway and biological implication. Am J Physiol Lung Cell Mol Physiol 293: L693-L701, 2007.
29. Kovarik A, Peat N, Wilson D, Gendler SJ, Taylor-Papadimitriou J. Analysis of the tissue-specific promoter of the MUC1 gene. J Biol Chem 268: 9917-9926, 1993.
30. Kuwahara I, Lillehoj EP, Hisatsune A, Lu W, Isohama Y, Miyata T, Kim KC. Neutrophil elastase stimulates MUC1 gene expression through increased Sp1 binding to the MUC1 promoter. Am J Physiol Lung Cell Mol Physiol 289: L355-L362, 2005.
31. Kuwahara I, Lillehoj EP, Koga T, Isohama Y, Miyata T, Kim KC. The signaling pathway involved in neutrophil elastase stimulated MUC1 transcription. Am J Respir Cell Mol Biol 37: 691-698, 2007.
32. Kyo Y, Kato K, Park YS, Gajhate S, Umehara T, Lillehoj EP, Suzaki H, Kim KC. Anti-inflammatory role of MUC1 mucin during nontypeable Haemophilus influenzae infection. Am J Respir Cell Mol Biol 46: 149-156, 2012.
33. Lagow EL, Carson DD. Synergistic stimulation of MUC1 expression in normal breast epithelia and breast cancer cells by interferon-and tumor necrosis factor-_. J Cell Biochem 86: 759-772, 2002.
34. Lee IJ, Hyun SW, Nandi A, Kim KC. Transcriptional regulation of the hamster Muc1 gene: identification of a putative negative regulatory element. Am J Physiol Lung Cell Mol Physiol 284: L160-L168, 2003.
35. Lee KS, Park SJ, Hwang PH, Yi HK, Song CH, Chai OH, Kim JS, Lee M, Lee YC. PPAR-modulates allergic inflammation through upregulation of PTEN. FASEB J 19: 1033-1035, 2005.
36. Li Y, Dinwiddie DL, Harrod KS, Jiang Y, Kim KC. Anti-inflammatory effect of MUC1 during respiratory syncytial virus infection of lung epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 298: L558-L563, 2010.
37. Liang J, Jiang D, Griffith J, Yu S, Fan J, Zhao X, Bucala R, Noble PW. CD44 is a negative regulator of acute pulmonary inflammation and lipopolysaccharide-TLR signaling in mouse macrophages. J Immunol 2007;178:2469-2475.
38. Lillehoj EP, Han F, Kim KC. Mutagenesis of a Gly-Ser cleavage site in MUC1 inhibits ectodomain shedding. Biochem Biophys Res Commun 307: 743-749, 2003.
39. Liu WS, Heckman CA. The sevenfold way of PKC regulation. Cell Signal 10: 529-542, 1998.
40. Lu W, Hisatsune A, Koga T, Kato K, Kuwahara I, Lillehoj EP, Chen W, Cross AS, Gendler SJ, Gewirtz AT, Kim KC. Cutting edge: enhanced pulmonary clearance of Pseudomonas aeruginosa by Muc1 knockout mice. J Immunol 176: 3890-3894, 2006.
41. Lu W, Lillehoj EP, Kim KC. Effects of dexamethasone on Muc5ac mucin production by primary airway goblet cells. Am J Physiol Lung Cell Mol Physiol 288: L52-L60, 2005.
42. Mu YM, Yanase T, Nishi Y, Takayanagi R, Goto K, Nawata H. Combined treatment with specific ligands for PPAR_:RXR nuclear receptor system markedly inhibits the expression of cytochrome P450arom in human granulosa cancer cells. Mol Cell Endocrinol 181: 239-248, 2001.
43. Ogawa Y, Duru EA, Ameredes BT. Role of IL-10 in the resolution of airway inflammation. Curr Mol Med 8: 437-445, 2008.
44. Okada M, Yan SF, Pinsky DJ. Peroxisome proliferator-activated receptor-(PPAR-) activation suppresses ischemic induction of Egr-1 and its inflammatory gene targets. FASEB J 16: 1861-1868, 2002.
45. Pemberton LF, Rughetti A, Taylor-Papadimitriou J, Gendler SJ. The epithelial mucin MUC1 contains at least two discrete signals specifying membrane localization in cells. J Biol Chem 271: 2332-2340, 1996.
46. Perez A, van Heeckeren AM, Nichols D, Gupta S, Eastman JF, Davis PB. Peroxisome proliferator-activated receptor-in cystic fibrosis lung epithelium. Am J Physiol Lung Cell Mol Physiol 295: L303-L313, 2008.
47. Ren J, Agata N, Chen D, Li Y, Yu WH, Huang L, Raina D, Chen W, Kharbanda S, Kufe D. Human MUC1 carcinoma-associated protein confers resistance to genotoxic anticancer agents. Cancer Cell 5: 163-175, 2004.
48. Roth M, Black JL. Transcription factors in asthma: Are transcription factors a new target for asthma therapy? Curr Drug Targets 7: 589-595, 2006.
49. Royce SG, Tang ML. The effects of current therapies on airway remodeling in asthma and new possibilities for treatment and prevention. Curr Mol Pharmacol 2: 169-181, 2009.
50. Samuelsson B. Arachidonic acid metabolism: role in inflammation. Z Rheumatol 50: 3-6, 1991.
51. Serhan CN, Devchand PR. Novel anti-inflammatory targets for asthma. A role for PPARγ? Am J Respir Cell Mol Biol 24: 658-661, 2001.
52. Shalom-Barak T, Nicholas JM, Wang Y, Zhang X, Ong ES, Young TH, Gendler SJ, Evans RM, Barak Y. Peroxisome proliferator-activated receptor γ? controls MUC1 transcription in trophoblasts. Mol Cell Biol 24: 10661-10669, 2004.
53. Shanks KK, Guang W, Kim KC, Lillehoj EP. Interleukin-8 production by human airway epithelial cells in response to Pseudomonas aeruginosa clinical isolates expressing type a or type b flagellins. Clin Vaccine Immunol 17: 1196-1202, 2010.
54. Thatcher TH, Maggirwar SB, Baglole CJ, Lakatos HF, Gasiewicz TA, Phipps RP, Sime PJ. Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the NF-κB component RelB. Am J Pathol 170: 855-864, 2007.
55. Ueno K, Koga T, Kato K, Golenbock DT, Gendler SJ, Kai H, Kim KC. MUC1 mucin is a negative regulator of Toll-like receptor signaling. Am J Respir Cell Mol Biol 38: 263-268, 2008.
56. Vidal-Puig A, Jimenez-Linan M, Lowell BB, Hamann A, Hu E, Spiegelman B, Flier JS, Moller DE. Regulation of PPARβ gene expression by nutrition and obesity in rodents. J Clin Invest 97: 2553-2561, 1996.
57. Ward JE, Tan X. Peroxisome proliferator activated receptor ligands as regulators of airway inflammation and remodelling in chronic lung disease. PPAR Res 2007: 14983, 2007.
58. Woerly G, Honda K, Loyens M, Papin JP, Auwerx J, Staels B, Capron M, Dombrowicz D. Peroxisome proliferator-activated receptors α and γ downregulate allergic inflammation and eosinophil activation. J Exp Med 198: 411-421, 2003.
59. Wu W, Booth JL, Coggeshall KM, Metcalf JP. Calcium-dependent viral internalization is required for adenovirus type 7 induction of IL-8 protein. Virology 355: 18-29, 2006.
60. Yamada M, Horiguchi K, Umezawa R, Hashimoto K, Satoh T, Ozawa A, Shibusawa N, Monden T, Okada S, Shimizu H, Mori M. Troglitazone, a ligand of peroxisome proliferator-activated receptor-γ, stabilizes NUCB2 (Nesfatin) mRNA by activating the ERK1/2 pathway: Isolation and characterization of the human NUCB2 gene. Endocrinology 151: 2494-2503, 2010.
61. Yanase T, Mu YM, Nishi Y, Goto K, Nomura M, Okabe T, Takayanagi R, Nawata H. Regulation of aromatase by nuclear receptors. J Steroid Biochem Mol Biol 79: 187-192, 2001.
62. Zhou W, Hashimoto K, Goleniewska K, O'Neal JF, Ji S, Blackwell TS, Fitzgerald GA, Egan KM, Geraci MW, Peebles RS Jr. Prostaglandin I2 analogs inhibit proinflammatory cytokine production and T cell stimulatory function of dendritic cells. J Immunol 178: 702-710, 2007.