Roflumilast N-oxide reverses corticosteroid resistance in neutrophils from patients with chronic obstructive pulmonary disease

Journal of Allergy and Clinical Immunology

Volumn 134, Issue 2, 2014, Pages

  Milara, Javier ^a,b   Lluch, Javier ^a,d   Almudever, Patricia ^a,c   Freire, Jose ^e   Xiaozhong, Qian ^e   Cortijo, Julio ^a,c,d  

^a HOSPITAL GENERAL UNIVERSITARIO DE VALENCIA   (Spain)

^b UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

^c UNIVERSITY OF VALENCIA   (Spain)

^d INSTITUTO DE SALUD CARLOS III   (Spain)

^e FOREST RESEARCH INSTITUTE   (United States)

Author keywords

chronic obstructive pulmonary disease; corticosteroid resistance; dexamethasone; neutrophil; Roflumilast

Indexed keywords

CIGARETTE SMOKE; CORTICOSTEROID; DEXAMETHASONE; GELATINASE B; GLUCOCORTICOID RECEPTOR BETA; HISTONE DEACETYLASE; HISTONE DEACETYLASE 2; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; MULTIDRUG RESISTANCE PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE DELTA; PHOSPHODIESTERASE IV; ROFLUMILAST; UNCLASSIFIED DRUG; AMINOPYRIDINE DERIVATIVE; BENZAMIDE DERIVATIVE; BIOLOGICAL MARKER; CYCLOPROPANE DERIVATIVE; DRUG MIXTURE; ISOMERASE; MIF PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE; PHOSPHODIESTERASE IV INHIBITOR; ROFLUMILAST N-OXIDE;

AGED; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME RELEASE; FEMALE; FORCED EXPIRATORY VOLUME; GENE ACTIVITY; GENE EXPRESSION; HUMAN; MALE; NEUTROPHIL; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMOKING; UPREGULATION; CHEMISTRY; DRUG EFFECTS; DRUG MIXTURE; DRUG RESISTANCE; ISOLATION AND PURIFICATION; METABOLISM; MIDDLE AGED; PATHOLOGY; PHARMACOLOGY; PRIMARY CELL CULTURE; TOBACCO;

ADRENAL CORTEX HORMONES; AGED; AMINOPYRIDINES; BENZAMIDES; BIOLOGICAL MARKERS; COMPLEX MIXTURES; CYCLOPROPANES; DEXAMETHASONE; DRUG RESISTANCE; DRUG SYNERGISM; FEMALE; GENE EXPRESSION; HISTONE DEACETYLASES; HUMANS; INTERLEUKIN-8; INTRAMOLECULAR OXIDOREDUCTASES; LIPOPOLYSACCHARIDES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; MATRIX METALLOPROTEINASE 9; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE PHOSPHATASES; NEUTROPHILS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHODIESTERASE 4 INHIBITORS; PRIMARY CELL CULTURE; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; TOBACCO;

EID: 84905578194     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.02.001     Document Type: Article

References (62)

1. R.A. Pauwels, and K.F. Rabe Burden and clinical features of chronic obstructive pulmonary disease (COPD) Lancet 364 2004 613 620
2. N. Roche, R. Marthan, P. Berger, A. Chambellan, P. Chanez, and B. Aguilaniu et al. Beyond corticosteroids: future prospects in the management of inflammation in COPD Eur Respir Rev 20 2011 175 182
3. P.J. Barnes Mechanisms and resistance in glucocorticoid control of inflammation J Steroid Biochem Mol Biol 120 2010 76 85
4. T.J. Torphy Phosphodiesterase isozymes: molecular targets for novel antiasthma agents Am J Respir Crit Care Med 157 1998 351 370
5. A. Hatzelmann, E.J. Morcillo, G. Lungarella, S. Adnot, S. Sanjar, and R. Beume et al. The preclinical pharmacology of roflumilast - a selective, oral phosphodiesterase 4 inhibitor in development for chronic obstructive pulmonary disease Pulm Pharmacol Ther 23 2010 235 256
6. D.C. Grootendorst, S.A. Gauw, R.M. Verhoosel, P.J. Sterk, J.J. Hospers, and D. Bredenbroker et al. Reduction in sputum neutrophil and eosinophil numbers by the PDE4 inhibitor roflumilast in patients with COPD Thorax 62 2007 1081 1087
7. A.S. Cowburn, A.M. Condliffe, N. Farahi, C. Summers, and E.R. Chilvers Advances in neutrophil biology: clinical implications Chest 134 2008 606 612
8. S.V. Culpitt, W. Maziak, S. Loukidis, J.A. Nightingale, J.L. Matthews, and P.J. Barnes Effect of high dose inhaled steroid on cells, cytokines, and proteases in induced sputum in chronic obstructive pulmonary disease Am J Respir Crit Care Med 160 1999 1635 1639
9. N.A. Jones, V. Boswell-Smith, R. Lever, and C.P. Page The effect of selective phosphodiesterase isoenzyme inhibition on neutrophil function in vitro Pulm Pharmacol Ther 18 2005 93 101
10. J. Plumb, K. Gaffey, B. Kane, B. Malia-Milanes, R. Shah, and A. Bentley et al. Reduced glucocorticoid receptor expression and function in airway neutrophils Int Immunopharmacol 12 2012 26 33
11. S.I. Rennard, P.M. Calverley, U.M. Goehring, D. Bredenbroker, and F.J. Martinez Reduction of exacerbations by the PDE4 inhibitor roflumilast - the importance of defining different subsets of patients with COPD Respir Res 12 2011 18
12. R.A. O'Donnell, C. Peebles, J.A. Ward, A. Daraker, G. Angco, and P. Broberg et al. Relationship between peripheral airway dysfunction, airway obstruction, and neutrophilic inflammation in COPD Thorax 59 2004 837 842
13. A. Noguera, S. Batle, C. Miralles, J. Iglesias, X. Busquets, and W. MacNee et al. Enhanced neutrophil response in chronic obstructive pulmonary disease Thorax 56 2001 432 437
14. E.J. Oudijk, J.W. Lammers, and L. Koenderman Systemic inflammation in chronic obstructive pulmonary disease Eur Respir J Suppl 46 2003 5s 13s
15. E.J. Oudijk, E.H. Nijhuis, M.D. Zwank, E.A. van de Graaf, H.J. Mager, and P.J. Coffer et al. Systemic inflammation in COPD visualised by gene profiling in peripheral blood neutrophils Thorax 60 2005 538 544
16. T. Terashima, B. Wiggs, D. English, J.C. Hogg, and S.F. van Eeden The effect of cigarette smoking on the bone marrow Am J Respir Crit Care Med 155 1997 1021 1026
17. J.K. Quint, and J.A. Wedzicha The neutrophil in chronic obstructive pulmonary disease J Allergy Clin Immunol 119 2007 1065 1071
18. J.A. Stockley, G.M. Walton, J.M. Lord, and E. Sapey Aberrant neutrophil functions in stable chronic obstructive pulmonary disease: the neutrophil as an immunotherapeutic target Int Immunopharmacol 17 2013 1211 1217
19. I. Rahman, E. Swarska, M. Henry, J. Stolk, and W. MacNee Is there any relationship between plasma antioxidant capacity and lung function in smokers and in patients with chronic obstructive pulmonary disease? Thorax 55 2000 189 193
20. E.M. Drost, K.M. Skwarski, J. Sauleda, N. Soler, J. Roca, and A. Agusti et al. Oxidative stress and airway inflammation in severe exacerbations of COPD Thorax 60 2005 293 300
21. J. Milara, G. Juan, T. Peiro, A. Serrano, and J. Cortijo Neutrophil activation in severe, early-onset COPD patients versus healthy non-smoker subjects in vitro: effects of antioxidant therapy Respiration 83 2012 147 158
22. K.J. Baines, J.L. Simpson, and P.G. Gibson Innate immune responses are increased in chronic obstructive pulmonary disease PLoS One 6 2011 e18426
23. A. Hatzelmann, and C. Schudt Anti-inflammatory and immunomodulatory potential of the novel PDE4 inhibitor roflumilast in vitro J Pharmacol Exp Ther 297 2001 267 279
24. P.A. Martorana, R. Beume, M. Lucattelli, L. Wollin, and G. Lungarella Roflumilast fully prevents emphysema in mice chronically exposed to cigarette smoke Am J Respir Crit Care Med 172 2005 848 853
25. T. Moodley, S.M. Wilson, T. Joshi, C.F. Rider, P. Sharma, and D. Yan et al. Phosphodiesterase 4 inhibitors augment the ability of formoterol to enhance glucocorticoid-dependent gene transcription in human airway epithelial cells: a novel mechanism for the clinical efficacy of roflumilast in severe chronic obstructive pulmonary disease Mol Pharmacol 83 2013 894 906
26. P.J. Barnes, and I.M. Adcock Glucocorticoid resistance in inflammatory diseases Lancet 373 2009 1905 1917
27. K. Ito, M. Ito, W.M. Elliott, B. Cosio, G. Caramori, and O.M. Kon et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease N Engl J Med 352 2005 1967 1976
28. K. Ito, S. Lim, G. Caramori, B. Cosio, K.F. Chung, and I.M. Adcock et al. A molecular mechanism of action of theophylline: Induction of histone deacetylase activity to decrease inflammatory gene expression Proc Natl Acad Sci U S A 99 2002 8921 8926
29. L.P. Sousa, A.F. Carmo, B.M. Rezende, F. Lopes, D.M. Silva, and A.L. Alessandri et al. Cyclic AMP enhances resolution of allergic pleurisy by promoting inflammatory cell apoptosis via inhibition of PI3K/Akt and NF-kappaB Biochem Pharmacol 78 2009 396 405
30. J.A. Marwick, G. Caramori, C.S. Stevenson, P. Casolari, E. Jazrawi, and P.J. Barnes et al. Inhibition of PI3Kdelta restores glucocorticoid function in smoking-induced airway inflammation in mice Am J Respir Crit Care Med 179 2009 542 548
31. P.J. Barnes Corticosteroid resistance in patients with asthma and chronic obstructive pulmonary disease J Allergy Clin Immunol 131 2013 636 645
32. G. Neeck, A. Kluter, H. Dotzlaw, and M. Eggert Involvement of the glucocorticoid receptor in the pathogenesis of rheumatoid arthritis Ann N Y Acad Sci 966 2002 491 495
33. L. Pujols, J. Mullol, and C. Picado Alpha and beta glucocorticoid receptors: relevance in airway diseases Curr Allergy Asthma Rep 7 2007 93 99
34. M. Honda, F. Orii, T. Ayabe, S. Imai, T. Ashida, and T. Obara et al. Expression of glucocorticoid receptor beta in lymphocytes of patients with glucocorticoid-resistant ulcerative colitis Gastroenterology 118 2000 859 866
35. D.L. Kozaci, Y. Chernajovsky, and I.C. Chikanza The differential expression of corticosteroid receptor isoforms in corticosteroid-resistant and -sensitive patients with rheumatoid arthritis Rheumatology (Oxford) 46 2007 579 585
36. A.R. Sousa, S.J. Lane, J.A. Cidlowski, D.Z. Staynov, and T.H. Lee Glucocorticoid resistance in asthma is associated with elevated in vivo expression of the glucocorticoid receptor beta-isoform J Allergy Clin Immunol 105 2000 943 950
37. L.B. Li, D.Y. Leung, R.J. Martin, and E. Goleva Inhibition of histone deacetylase 2 expression by elevated glucocorticoid receptor beta in steroid-resistant asthma Am J Respir Crit Care Med 182 2010 877 883
38. S.H. Korn, F.B. Thunnissen, G.J. Wesseling, J.W. Arends, and E.F. Wouters Glucocorticoid receptor mRNA levels in bronchial epithelial cells of patients with COPD: influence of glucocorticoids Respir Med 92 1998 1102 1109
39. L.Y. Liu, M. Zeng, C.M. Xie, J.H. Gao, Y.S. Yan, and G.F. Lu et al. [Oxidative stress status in patients with chronic obstructive pulmonary disease and its relation to glucocorticoid receptor levels] Nan Fang Yi Ke Da Xue Xue Bao 28 2008 992 996
40. J.L. Ortiz, J. Milara, J. Lluch, A. De Diego, C. Sanz, and J. Cortijo Phosphodiesterase-4 inhibition improves corticosteroid insensitivity in pulmonary endothelial cells under oxidative stress Allergy 68 2013 64 73
41. M. Ariga, B. Neitzert, S. Nakae, G. Mottin, C. Bertrand, and M.P. Pruniaux et al. Nonredundant function of phosphodiesterases 4D and 4B in neutrophil recruitment to the site of inflammation J Immunol 173 2004 7531 7538
42. J. Milara, M. Armengot, P. Banuls, H. Tenor, R. Beume, and E. Artigues et al. Roflumilast N-oxide, a PDE4 inhibitor, improves cilia motility and ciliated human bronchial epithelial cells compromised by cigarette smoke in vitro Br J Pharmacol 166 2012 2243 2262
43. S. Muzaffar, J.Y. Jeremy, G.D. Angelini, and N. Shukla NADPH oxidase 4 mediates upregulation of type 4 phosphodiesterases in human endothelial cells J Cell Physiol 227 2012 1941 1950
44. Y. Ishiguro, T. Ohkawara, H. Sakuraba, K. Yamagata, H. Hiraga, and S. Yamaguchi et al. Macrophage migration inhibitory factor has a proinflammatory activity via the p38 pathway in glucocorticoid-resistant ulcerative colitis Clin Immunol 120 2006 335 341
45. A.G. Rossi, C. Haslett, N. Hirani, A.P. Greening, I. Rahman, and C.N. Metz et al. Human circulating eosinophils secrete macrophage migration inhibitory factor (MIF). Potential role in asthma J Clin Invest 101 1998 2869 2874
46. F.F. Wang, L.A. Zhu, Y.Q. Zou, H. Zheng, A. Wilson, and C.D. Yang et al. New insights into the role and mechanism of macrophage migration inhibitory factor in steroid-resistant patients with systemic lupus erythematosus Arthritis Res Ther 14 2012 R103
47. T. Gaber, S. Schellmann, K.B. Erekul, M. Fangradt, K. Tykwinska, and M. Hahne et al. Macrophage migration inhibitory factor counterregulates dexamethasone-mediated suppression of hypoxia-inducible factor-1 alpha function and differentially influences human CD4+ T cell proliferation under hypoxia J Immunol 186 2011 764 774
48. L.L. Santos, H. Fan, P. Hall, D. Ngo, C.R. Mackay, and G. Fingerle-Rowson et al. Macrophage migration inhibitory factor regulates neutrophil chemotactic responses in inflammatory arthritis in mice Arthritis Rheum 63 2011 960 970
49. J.M. Daun, and J.G. Cannon Macrophage migration inhibitory factor antagonizes hydrocortisone-induced increases in cytosolic IkappaBalpha Am J Physiol Regul Integr Comp Physiol 279 2000 R1043 R1049
50. D. Aeberli, Y. Yang, A. Mansell, L. Santos, M. Leech, and E.F. Morand Endogenous macrophage migration inhibitory factor modulates glucocorticoid sensitivity in macrophages via effects on MAP kinase phosphatase-1 and p38 MAP kinase FEBS Lett 580 2006 974 981
51. T. Roger, A.L. Chanson, M. Knaup-Reymond, and T. Calandra Macrophage migration inhibitory factor promotes innate immune responses by suppressing glucocorticoid-induced expression of mitogen-activated protein kinase phosphatase-1 Eur J Immunol 35 2005 3405 3413
52. C.D. Coldren, J.A. Nick, K.R. Poch, M.D. Woolum, B.W. Fouty, and J.M. O'Brien et al. Functional and genomic changes induced by alveolar transmigration in human neutrophils Am J Physiol Lung Cell Mol Physiol 291 2006 L1267 L1276
53. S.E. Wenzel Asthma phenotypes: the evolution from clinical to molecular approaches Nat Med 18 2012 716 725
54. J. Milara, G. Juan, T. Peiro, A. Serrano, and J. Cortijo Neutrophil activation in severe, early-onset COPD patients versus healthy non-smoker subjects in vitro: effects of antioxidant therapy Respiration 83 2012 147 158
55. J. Milara, J.L. Ortiz, G. Juan, R. Guijarro, P. Almudever, and M. Martorell et al. Cigarette smoke exposure up-regulates endothelin receptor B in human pulmonary artery endothelial cells: molecular and functional consequences Br J Pharmacol 161 2010 1599 1615
56. Y. Su, W. Han, C. Giraldo, Y. De Li, and E.R. Block Effect of cigarette smoke extract on nitric oxide synthase in pulmonary artery endothelial cells Am J Respir Cell Mol Biol 19 1998 819 825
57. M.L. Fermino, C.D. Polli, K.A. Toledo, F.T. Liu, D.K. Hsu, and M.C. Roque-Barreira et al. LPS-induced galectin-3 oligomerization results in enhancement of neutrophil activation PLoS One 6 2011 e26004
58. K. Strandberg, K. Blidberg, K. Sahlander, L. Palmberg, and K. Larsson Effect of formoterol and budesonide on chemokine release, chemokine receptor expression and chemotaxis in human neutrophils Pulm Pharmacol Ther 23 2010 316 323
59. S. Suri, M.A. Taylor, A. Verity, S. Tribolo, P.W. Needs, and P.A. Kroon et al. A comparative study of the effects of quercetin and its glucuronide and sulfate metabolites on human neutrophil function in vitro Biochem Pharmacol 76 2008 645 653
60. J.L. Ortiz, J. Milara, J. Lluch, A. De Diego, C. Sanz, and J. Cortijo Phosphodiesterase-4 inhibition improves corticosteroid insensitivity in pulmonary endothelial cells under oxidative stress Allergy 68 2013 64 73
61. J. Milara, M. Armengot, P. Banuls, H. Tenor, R. Beume, and E. Artigues et al. Roflumilast N-oxide, a PDE4 inhibitor, improves cilia motility and ciliated human bronchial epithelial cells compromised by cigarette smoke in vitro Br J Pharmacol 166 2012 2243 2262
62. C. Elbim, S. Pillet, M.H. Prevost, A. Preira, P.M. Girard, and N. Rogine et al. The role of phagocytes in HIV-related oxidative stress J Clin Virol 20 2001 99 109