Cytokines alter glucocorticoid receptor phosphorylation in airway cells: Role of phosphatases

American Journal of Respiratory Cell and Molecular Biology

Volumn 47, Issue 4, 2012, Pages 464-473

  Bouazza, Belaid ^a   Krytska, Kateryna ^a   Debba Pavard, Manel ^a   Amrani, Yassine ^b   Honkanen, Richard E ^c   Tran, Jennifer ^a   Tliba, Omar ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

Airway remodeling; Airway smooth muscle; Asthma; Corticosteroid insensitivity; Serine threonine protein phosphatase

Indexed keywords

CYTOKINE; FLUTICASONE PROPIONATE; GAMMA INTERFERON; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 5; SERINE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AIRWAY; ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENZYME ACTIVITY; ENZYME REPRESSION; GENE CONSTRUCT; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPORTER GENE; SMOOTH MUSCLE FIBER; TRANSACTIVATION; TREATMENT DURATION;

ANDROSTADIENES; CELLS, CULTURED; CYTOKINES; GENE KNOCKDOWN TECHNIQUES; GLUCOCORTICOIDS; HUMANS; MUTATION, MISSENSE; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, GLUCOCORTICOID; RESPIRATORY SYSTEM; RNA INTERFERENCE;

EID: 84866980758     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2011-0364OC     Document Type: Article

References (54)

1. Marwick JA, Adcock IM, Chung KF. Overcoming reduced glucocorticoid sensitivity in airway disease: molecular mechanisms and therapeutic approaches. Drugs 2010;70:929-948.
2. Ogawa Y, Calhoun WJ. Phenotypic characterization of severe asthma. Curr Opin Pulm Med 2010;16:48-54.
3. Adcock IM, Ito K. Steroid resistance in asthma: a major problem requiring novel solutions or a non-issue? Curr Opin Pharmacol 2004;4:257-262. (Pubitemid 38585310)
4. Ghaffar O, Hamid Q, Renzi PM, Allakhverdi Z, Molet S, Hogg JC, Shore SA, Luster AD, Lamkhioued B. Constitutive and cytokine-stimulated expression of eotaxin by human airway smooth muscle cells. Am J Respir Crit Care Med 1999;159:1933-1942. (Pubitemid 29275066)
5. Kaur D, Saunders R, Berger P, Siddiqui S, Woodman L, Wardlaw A, Bradding P, Brightling CE. Airway smooth muscle and mast cell-derived cc chemokine ligand 19 mediate airway smooth muscle migration in asthma. Am J Respir Crit Care Med 2006;174:1179-1188. (Pubitemid 44924818)
6. Foley SC, Mogas AK, Olivenstein R, Fiset PO, Chakir J, Bourbeau J, Ernst P, Lemiere C, Martin JG, Hamid Q. Increased expression of adam33 and adam8 with disease progression in asthma. J Allergy Clin Immunol 2007;119:863-871. (Pubitemid 46527832)
7. Lee JY, Park SW, Chang HK, Kim HY, Rhim T, Lee JH, Jang AS, Koh ES, Park CS. A disintegrin and metalloproteinase 33 protein in patients with asthma: relevance to airflow limitation. Am J Respir Crit Care Med 2006;173:729-735.
8. Bhandare R, Damera G, Banerjee A, Flammer JR, Keslacy S, Rogatsky I, Panettieri RA, Amrani Y, Tliba O. Glucocorticoid receptor interacting protein-1 restores glucocorticoid responsiveness in steroid-resistant airway structural cells. Am J Respir Cell Mol Biol 2010;42:9-15.
9. Tliba O, Cidlowski JA, Amrani Y. Cd38 expression is insensitive to steroid action in cells treated with tumor necrosis factor-alpha and interferon-gamma by a mechanism involving the up-regulation of the glucocorticoid receptor beta isoform. Mol Pharmacol 2006;69:588-596. (Pubitemid 43121956)
10. Tliba O, Damera G, Banerjee A, Gu S, Baidouri H, Keslacy S, Amrani Y. Cytokines induce an early steroid resistance in airway smooth muscle cells: novel role of interferon regulatory factor-1. Am J Respir Cell Mol Biol 2008;38:463-472. (Pubitemid 351758693)
11. Banerjee A, Damera G, Bhandare R, Gu S, Lopez-Boado Y, Panettieri R Jr, Tliba O. Vitamin D and glucocorticoids differentially modulate chemokine expression in human airway smooth muscle cells. Br J Pharmacol 2008;155:84-92.
12. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 2008;8:183-192. (Pubitemid 351323287)
13. Oakley RH, Sar M, Cidlowski JA. The human glucocorticoid receptor beta isoform: expression, biochemical properties, and putative function. J Biol Chem 1996;271:9550-9559.
14. Pujols L, Mullol J, Torrego A, Picado C. Glucocorticoid receptors in human airways. Allergy 2004;59:1042-1052. (Pubitemid 39294696)
15. Galliher-Beckley AJ, Cidlowski JA. Emerging roles of glucocorticoid receptor phosphorylation in modulating glucocorticoid hormone action in health and disease. IUBMB Life 2009;61:979-986.
16. Godowski PJ, Rusconi S, Miesfeld R, Yamamoto KR. Glucocorticoid receptor mutants that are constitutive activators of transcriptional enhancement. Nature 1987;325:365-368. (Pubitemid 17053179)
17. Hollenberg SM, Evans RM. Multiple and cooperative trans-activation domains of the human glucocorticoid receptor. Cell 1988;55:899-906.
18. Wang Z, Frederick J, Garabedian MJ. Deciphering the phosphorylation "Code" of the glucocorticoid receptor in vivo. J Biol Chem 2002;277:26573-26580. (Pubitemid 34967155)
19. Almlof T, Wright AP, Gustafsson JA. Role of acidic and phosphorylated residues in gene activation by the glucocorticoid receptor. J Biol Chem 1995;270:17535-17540.
20. Chen W, Dang T, Blind RD, Wang Z, Cavasotto CN, Hittelman AB, Rogatsky I, Logan SK, Garabedian MJ. Glucocorticoid receptor phosphorylation differentially affects target gene expression. Mol Endocrinol 2008;22:1754-1766.
21. Ismaili N, Garabedian MJ. Modulation of glucocorticoid receptor function via phosphorylation. Ann N Y Acad Sci 2004;1024:86-101. (Pubitemid 38879595)
22. Kumar R, Calhoun WJ. Differential regulation of the transcriptional activity of the glucocorticoid receptor through site-specific phosphorylation. Biologics 2008;2:845-854.
23. Zhou J, Cidlowski JA. The human glucocorticoid receptor: one gene, multiple proteins and diverse responses. Steroids 2005;70:407-417. (Pubitemid 40616039)
24. Zuo Z, Urban G, Scammell JG, Dean NM, McLean TK, Aragon I, Honkanen RE. Ser/thr protein phosphatase type 5 (pp5) is a negative regulator of glucocorticoid receptor-mediated growth arrest. Biochemistry 1999;38:8849-8857. (Pubitemid 29334645)
25. Miller AL, Webb MS, Copik AJ, Wang Y, Johnson BH, Kumar R, Thompson EB. P38 mitogen-activated protein kinase (mapk) is a key mediator in glucocorticoid-induced apoptosis of lymphoid cells: correlation between p38 mapk activation and site-specific phosphorylation of the human glucocorticoid receptor at serine 211. Mol Endocrinol 2005;19:1569-1583. (Pubitemid 41002986)
26. Itoh M, Adachi M, Yasui H, Takekawa M, Tanaka H, Imai K. Nuclear export of glucocorticoid receptor is enhanced by c-jun n-terminal kinase-mediated phosphorylation. Mol Endocrinol 2002;16:2382-2392. (Pubitemid 35155548)
27. Rogatsky I, Logan SK, Garabedian MJ. Antagonism of glucocorticoid receptor transcriptional activation by the c-jun n-terminal kinase. Proc Natl Acad Sci USA 1998;95:2050-2055. (Pubitemid 28145892)
28. Kino T, Ichijo T, Amin ND, Kesavapany S, Wang Y, Kim N, Rao S, Player A, Zheng YL, Garabedian MJ, et al. Cyclin-dependent kinase 5 differentially regulates the transcriptional activity of the glucocorticoid receptor through phosphorylation: clinical implications for the nervous system response to glucocorticoids and stress. Mol Endocrinol 2007;21:1552-1568. (Pubitemid 47001081)
29. Krstic MD, Rogatsky I, Yamamoto KR, Garabedian MJ. Mitogen-activated and cyclin-dependent protein kinases selectively and differentially modulate transcriptional enhancement by the glucocorticoid receptor.Mol Cell Biol 1997;17:3947-3954. (Pubitemid 27281870)
30. Bantel H, Schmitz ML, Raible A, Gregor M, Schulze-Osthoff K. Critical role of nf-kappab and stress-activated protein kinases in steroid unresponsiveness. FASEB J 2002;16:1832-1834.
31. Irusen E, Matthews JG, Takahashi A, Barnes PJ, Chung KF, Adcock IM. P38 mitogen-activated protein kinase-induced glucocorticoid receptor phosphorylation reduces its activity: role in steroid-insensitive asthma. J Allergy Clin Immunol 2002;109:649-657. (Pubitemid 34327193)
32. Chinkers M. Protein phosphatase 5 in signal transduction. Trends Endocrinol Metab 2001;12:28-32. (Pubitemid 33713183)
33. Zhang Y, Leung DY, Nordeen SK, Goleva E. Estrogen inhibits glucocorticoid action via protein phosphatase 5 (pp5)-mediated glucocorticoid receptor dephosphorylation. J Biol Chem 2009;284:24542-24552.
34. Tliba O, Tliba S, Da Huang C, Hoffman RK, DeLong P, Panettieri RA Jr, Amrani Y. Tumor necrosis factor alpha modulates airway smooth muscle function via the autocrine action of interferon beta. J Biol Chem 2003;278:50615-50623. (Pubitemid 37548909)
35. Swingle MR, Amable L, Lawhorn BG, Buck SB, Burke CP, Ratti P, Fischer KL, Boger DL, Honkanen RE. Structure-activity relationship studies of fostriecin, cytostatin, and key analogs, with pp1, pp2a, pp5, and(beta12-beta13)-chimeras (pp1/pp2a and pp5/pp2a), provide further insight into the inhibitory actions of fostriecin family inhibitors. J Pharmacol Exp Ther 2009;331:45-53.
36. Swingle MR, Honkanen RE, Ciszak EM. Structural basis for the catalytic activity of human serine/threonine protein phosphatase-5. J Biol Chem 2004;279:33992-33999. (Pubitemid 39063050)
37. Chen W, Rogatsky I, Garabedian MJ. Med14 and med1 differentially regulate target-specific gene activation by the glucocorticoid receptor. Mol Endocrinol 2006;20:560-572. (Pubitemid 43291208)
38. Burnstein KL, Jewell CM, Sar M, Cidlowski JA. Intragenic sequences of the human glucocorticoid receptor complementary DNA mediate hormone-inducible receptor messenger RNA down-regulation through multiple mechanisms. Mol Endocrinol 1994;8:1764-1773.
39. Fukawa E, Tanaka H, Makino Y, Hirano F, Akama H, Kawai S, Makino I. Homologous down-regulation of the glucocorticoid receptor down-modulates cellular hormone responsiveness in human histiocytic lymphoma u937 cells. Endocr J 1994;41:623-630.
40. Govindan MV, Pothier F, Leclerc S, Palaniswami R, Xie B. Human glucocorticoid receptor gene promotor-homologous down regulation. J Steroid Biochem Mol Biol 1991;40:317-323.
41. Mason SA, Housley PR. Site-directed mutagenesis of the phosphorylation sites in the mouse glucocorticoid receptor. J Biol Chem 1993;268:21501-21504. (Pubitemid 23320636)
42. Webster JC, Jewell CM, Bodwell JE, Munck A, Sar M, Cidlowski JA. Mouse glucocorticoid receptor phosphorylation status influences multiple functions of the receptor protein. J BiolChem1997;272:9287-9293. (Pubitemid 27154940)
43. Li LB, Goleva E, Hall CF, Ou LS, Leung DY. Superantigen-induced corticosteroid resistance of human T cells occurs through activation of the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase (mek-erk) pathway. J Allergy Clin Immunol 2004;114:1059-1069. (Pubitemid 39469145)
44. Somers JP, DeFranco DB. Effects of okadaic acid, a protein phosphatase inhibitor, on glucocorticoid receptor-mediated enhancement. Mol Endocrinol 1992;6:26-34.
45. DeFranco DB, Qi M, Borror KC, Garabedian MJ, Brautigan DL. Protein phosphatase types 1 and/or 2a regulate nucleocytoplasmic shuttling of glucocorticoid receptors. Mol Endocrinol 1991;5:1215-1228.
46. Kaur M, Chivers JE, Giembycz MA, Newton R. Long-acting beta2-adrenoceptor agonists synergistically enhance glucocorticoid-dependent transcription in human airway epithelial and smooth muscle cells. Mol Pharmacol 2008;73:203-214. (Pubitemid 350294211)
47. Kobayashi Y, Mercado N, Miller-Larsson A, Barnes P, Ito K. Formoterol regulates nuclear translocation of glucocorticoid receptor by direct activation of protien phosphatase pp2a. Am J Respir Crit Care Med 2011;183:A4081.
48. Wang Z, Chen W, Kono E, Dang T, Garabedian MJ. Modulation of glucocorticoid receptor phosphorylation and transcriptional activity by a c-terminal-associated protein phosphatase. Mol Endocrinol 2007;21:625-634.
49. Golden T, Aragon IV, Zhou G, Cooper SR, Dean NM, Honkanen RE. Constitutive over expression of serine/threonine protein phosphatase 5 (pp5) augments estrogen-dependent tumor growth in mice. Cancer Lett 2004;215:95-100. (Pubitemid 39221464)
50. Urban G, Golden T, Aragon IV, Scammell JG, Dean NM, Honkanen RE. Identification of an estrogen-inducible phosphatase (pp5) that converts mcf-7 human breast carcinoma cells into an estrogen-independent phenotype when expressed constitutively. J Biol Chem 2001;276:27638-27646.
51. Zhou G, Golden T, Aragon IV, Honkanen RE. Ser/thr protein phosphatase 5 inactivates hypoxia-induced activation of an apoptosis signal-regulating kinase 1/mkk-4/jnk signaling cascade. J Biol Chem 2004;279:46595-46605. (Pubitemid 39518304)
52. Kang H, Sayner SL, Gross KL, Russell LC, Chinkers M. Identification of amino acids in the tetratricopeptide repeat and c-terminal domains of protein phosphatase 5 involved in autoinhibition and lipid activation. Biochemistry 2001;40:10485-10490. (Pubitemid 32816658)
53. Silverstein AM, Galigniana MD, Chen MS, Owens-Grillo JK, Chinkers M, Pratt WB. Protein phosphatase 5 is a major component of glucocorticoid receptor.Hsp90 complexes with properties of an fk506-binding immunophilin. J Biol Chem 1997;272:16224-16230. (Pubitemid 27276441)
54. Yang J, Roe SM, Cliff MJ, Williams MA, Ladbury JE, Cohen PT, Barford D. Molecular basis for tpr domain-mediated regulation of protein phosphatase 5. EMBO J 2005;24:1-10. (Pubitemid 40188458)