Protein phosphatase 5 mediates corticosteroid insensitivity in airway smooth muscle in patients with severe asthma

Allergy: European Journal of Allergy and Clinical Immunology

Volumn 72, Issue 1, 2017, Pages 126-136

  Chachi, L ^a   Abbasian, M ^a   Gavrila, A ^a   Alzahrani, A ^a   Tliba, O ^b   Bradding, P ^a   Wardlaw, A J ^a   Brightling, C ^a   Amrani, Y ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

airway smooth muscle; corticosteroid insensitivity; corticosteroid receptor; protein phosphatase; receptor phosphorylation

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; DEXAMETHASONE; EOTAXIN; FLUTICASONE; GLUCOCORTICOID INDUCED LEUCINE ZIPPER; GLUCOCORTICOID RECEPTOR ALPHA; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN; PROTEIN PHOSPHATASE 5; RANTES; SERINE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANTIASTHMATIC AGENT; BIOLOGICAL MARKER; CORTICOSTEROID; CYTOKINE; GLUCOCORTICOID RECEPTOR; NUCLEAR PROTEIN;

ADULT; AIRWAY SMOOTH MUSCLE CELL; ARTICLE; ASTHMA; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FORCED VITAL CAPACITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; BIOSYNTHESIS; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; DRUG TOLERANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LUNG FUNCTION TEST; METABOLISM; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; SMOOTH MUSCLE CELL;

ADRENAL CORTEX HORMONES; ADULT; ANTI-ASTHMATIC AGENTS; ASTHMA; BIOMARKERS; CYTOKINES; DRUG TOLERANCE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MIDDLE AGED; MYOCYTES, SMOOTH MUSCLE; NUCLEAR PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; RECEPTORS, GLUCOCORTICOID; RESPIRATORY FUNCTION TESTS; RESPONSE ELEMENTS; SEVERITY OF ILLNESS INDEX;

EID: 84987703655     PISSN: 01054538     EISSN: 13989995     Source Type: Journal    
DOI: 10.1111/all.13003     Document Type: Article

References (44)

1. Gibeon D, Chung KF. The investigation of severe asthma to define phenotypes. Clin Exp Allergy 2012;42:678–692.
2. Barnes PJ. Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease. J Allergy Clin Immunol 2013;131:636–645.
3. Poon AH, Eidelman DH, Martin JG, Laprise C, Hamid Q. Pathogenesis of severe asthma. Clin Exp Allergy 2012;42:625–637.
4. Matthews JG, Ito K, Barnes PJ, Adcock IM. Defective glucocorticoid receptor nuclear translocation and altered histone acetylation patterns in glucocorticoid-resistant patients. J Allergy Clin Immunol 2004;113:1100–1108.
5. Mercado N, Hakim A, Kobayashi Y, Meah S, Usmani OS, Chung KF et al. Restoration of corticosteroid sensitivity by p38 mitogen activated protein kinase inhibition in peripheral blood mononuclear cells from severe asthma. PLoS One 2012;7:e41582.
6. 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.
7. Hew M, Bhavsar P, Torrego A, Meah S, Khorasani N, Barnes PJ et al. Relative corticosteroid insensitivity of peripheral blood mononuclear cells in severe asthma. Am J Respir Crit Care Med 2006;174:134–141.
8. Goleva E, Li LB, Eves PT, Strand MJ, Martin RJ, Leung DY. Increased glucocorticoid receptor beta alters steroid response in glucocorticoid-insensitive asthma. Am J Respir Crit Care Med 2006;173:607–616.
9. Dombret MC, Alagha K, Philippe Boulet L, Yves Brillet P, Joos G, Laviolette M et al. Bronchial thermoplasty: a new therapeutic option for the treatment of severe, uncontrolled asthma in adults. Eur Respir Rev 2014;23:510–518.
10. Amrani Y. Airway smooth muscle modulation and airway hyper-responsiveness in asthma: new cellular and molecular paradigms. Exp Rev Clin Immunol 2006;2:353–364.
11. Kaur D, Saunders R, Berger P, Siddiqui S, Woodman L, Wardlaw A et al. 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.
12. Foley SC, Mogas AK, Olivenstein R, Fiset PO, Chakir J, Bourbeau J et al. Increased expression of ADAM33 and ADAM8 with disease progression in asthma. J Allergy Clin Immunol 2007;119:863–871.
13. Zhang J, Shan L, Koussih L, Redhu NS, Halayko AJ, Chakir J et al. Pentraxin 3 (PTX3) expression in allergic asthmatic airways: role in airway smooth muscle migration and chemokine production. PLoS One 2012;7:e34965.
14. Kaur D, Doe C, Woodman L, Wan WY, Sutcliffe A, Hollins F et al. Mast cell-airway smooth muscle crosstalk: the role of thymic stromal lymphopoietin. Chest 2012;142:76–85.
15. Bhandare R, Damera G, Banerjee A, Flammer JR, Keslacy S, Rogatsky I et al. Glucocorticoid receptor interacting protein-1 restores glucocorticoid responsiveness in steroid-resistant airway structural cells. Am J Respir Cell Mol Biol 2010;42:9–15.
16. Bouazza B, Krytska K, Debba-Pavard M, Amrani Y, Honkanen RE, Tran J et al. Cytokines alter glucocorticoid receptor phosphorylation in airway cells: role of phosphatases. Am J Respir Cell Mol Biol 2012;47:464–473.
17. Chachi L, Shikotra A, Duffy SM, Tliba O, Brightling C, Bradding P et al. Functional KCa3.1 channels regulate steroid insensitivity in bronchial smooth muscle cells. J Immunol 2013;191:2624–2636.
18. 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.
19. Tliba O, Damera G, Banerjee A, Gu S, Baidouri H, Keslacy S et al. 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.
20. Hinds TD Jr, Sanchez ER. Protein phosphatase 5. Int J Biochem Cell Biol 2008;40:2358–2362.
21. Chang PJ, Bhavsar PK, Michaeloudes C, Khorasani N, Chung KF. Corticosteroid insensitivity of chemokine expression in airway smooth muscle of patients with severe asthma. J Allergy Clin Immunol 2012;130:877–885.
22. Perry MM, Baker JE, Gibeon DS, Adcock IM, Chung KF. Airway smooth muscle hyperproliferation is regulated by microRNA-221 in severe asthma. Am J Respir Cell Mol Biol 2014;50:7–17.
23. Chang PJ, Michaeloudes C, Zhu J, Shaikh N, Baker J, Chung KF et al. Impaired nuclear translocation of the glucocorticoid receptor in corticosteroid-insensitive airway smooth muscle in severe asthma. Am J Respir Crit Care Med 2015;191:54–62.
24. British Thoracic Society Scottish Intercollegiate Guidelines Network. British guideline on the management of asthma. Thorax 2008;63(Suppl 4):iv1–iv121.
25. Brightling CE, Ammit AJ, Kaur D, Black JL, Wardlaw AJ, Hughes JM et al. The CXCL10/CXCR3 axis mediates human lung mast cell migration to asthmatic airway smooth muscle. Am J Respir Crit Care Med 2005;171:1103–1108.
26. Siddiqui S, Mistry V, Doe C, Roach K, Morgan A, Wardlaw A et al. Airway hyperresponsiveness is dissociated from airway wall structural remodeling. J Allergy Clin Immunol 2008;122:335–341.
27. Yick CY, Zwinderman AH, Kunst PW, Grunberg K, Mauad T, Fluiter K et al. Glucocorticoid-induced changes in gene expression of airway smooth muscle in patients with asthma. Am J Respir Crit Care Med 2013;187:1076–1084.
28. Prefontaine D, Nadigel J, Chouiali F, Audusseau S, Semlali A, Chakir J et al. Increased IL-33 expression by epithelial cells in bronchial asthma. J Allergy Clin Immunol 2010;125:752–754.
29. Li JJ, Tay HL, Maltby S, Xiang Y, Eyers F, Hatchwell L et al. MicroRNA-9 regulates steroid-resistant airway hyperresponsiveness by reducing protein phosphatase 2A activity. J Allergy Clin Immunol 2015;136:462–473.
30. Kobayashi Y, Mercado N, Barnes PJ, Ito K. Defects of protein phosphatase 2A causes corticosteroid insensitivity in severe asthma. PLoS One 2011;6:e27627.
31. 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.
32. Hinds TD Jr, Stechschulte LA, Cash HA, Whisler D, Banerjee A, Yong W et al. Protein phosphatase 5 mediates lipid metabolism through reciprocal control of glucocorticoid receptor and peroxisome proliferator-activated receptor-gamma (PPARgamma). J Biol Chem 2011;286:42911–42922.
33. Zuo Z, Urban G, Scammell JG, Dean NM, McLean TK, Aragon I et al. Ser/Thr protein phosphatase type 5 (PP5) is a negative regulator of glucocorticoid receptor-mediated growth arrest. Biochemistry 1999;38:8849–8857.
34. Ismaili N, Garabedian MJ. Modulation of glucocorticoid receptor function via phosphorylation. Ann N Y Acad Sci 2004;1024:86–101.
35. Avenant C, Ronacher K, Stubsrud E, Louw A, Hapgood JP. Role of ligand-dependent GR phosphorylation and half-life in determination of ligand-specific transcriptional activity. Mol Cell Endocrinol 2010;327:72–88.
36. Zhang Y, Leung DY, Goleva E. Anti-inflammatory and corticosteroid-enhancing actions of vitamin D in monocytes of patients with steroid-resistant and those with steroid-sensitive asthma. J Allergy Clin Immunol 2014;133:1744–1752.
37. Kaminska M, Foley S, Maghni K, Storness-Bliss C, Coxson H, Ghezzo H et al. Airway remodeling in subjects with severe asthma with or without chronic persistent airflow obstruction. J Allergy Clin Immunol 2009;124:45–51.
38. Shannon J, Ernst P, Yamauchi Y, Olivenstein R, Lemiere C, Foley S et al. Differences in airway cytokine profile in severe asthma compared to moderate asthma. Chest 2008;133:420–426.
39. Brightling C, Berry M, Amrani Y. Targeting TNF-alpha: a novel therapeutic approach for asthma. J Allergy Clin Immunol 2008;121:5–10.
40. Clark AR, Belvisi MG. Maps and legends: the quest for dissociated ligands of the glucocorticoid receptor. Pharmacol Ther 2012;134:54–67.
41. Sukkar MB, Issa R, Xie S, Oltmanns U, Newton R, Chung KF. Fractalkine/CX3CL1 production by human airway smooth muscle cells: induction by IFN-gamma and TNF-alpha and regulation by TGF-beta and corticosteroids. Am J Physiol Lung Cell Mol Physiol 2004;287:L1230–L1240.
42. Banerjee A, Damera G, Bhandare R, Gu S, Lopez-Boado Y, Panettieri R Jr et al. Vitamin D and glucocorticoids differentially modulate chemokine expression in human airway smooth muscle cells. Br J Pharmacol 2008;155:84–92.
43. Gavrila A, Chachi L, Tliba O, Brightling C, Amrani Y. The plant derivative compound a inhibits the production of corticosteroid-resistant chemokines by airway smooth muscle cells. Am J Respir Cell Mol Biol 2015;53:728–737.
44. Reddy PJ, Aksoy MO, Yang Y, Li XX, Ji R, Kelsen SG. Inhibition by salmeterol and cilomilast of fluticasone-enhanced IP-10 release in airway epithelial cells. COPD 2008;5:5–11.