MicroRNA-9 regulates steroid-resistant airway hyperresponsiveness by reducing protein phosphatase 2A activity

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 2, 2015, Pages 462-473

  Li, Jing Jing ^a   Tay, Hock L ^a   Maltby, Steven ^a   Xiang, Yang ^a,c   Eyers, Fiona ^a   Hatchwell, Luke ^b   Zhou, Hong ^a   Toop, Hamish D ^d   Morris, Jonathan C ^d   Nair, Parameswaran ^e   Mattes, Joerg ^b   Foster, Paul S ^a,f   Yang, Ming ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF NEWCASTLE   (Australia)

^c Central South University   (China)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e MCMASTER UNIVERSITY   (Canada)

^f UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

innate immunity; MicroRNA; protein phosphatase 2A; pulmonary macrophages; steroid resistant airway hyperresponsiveness

Indexed keywords

ANTAGOMIR; DEXAMETHASONE; FINGOLIMOD; GAMMA INTERFERON; GLUCOCORTICOID RECEPTOR; ISOPROTEIN; MESSENGER RNA; MICRORNA 9; PHOSPHOPROTEIN PHOSPHATASE 2A; SMALL UNTRANSLATED RNA; GLUCOCORTICOID; LIPOPOLYSACCHARIDE; LUCIFERASE; MICRORNA; MIRN9 MICRORNA, MOUSE; OLIGONUCLEOTIDE; OVALBUMIN; PHOSPHOPROTEIN PHOSPHATASE 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CELL FUNCTION; CELLULAR DISTRIBUTION; COMPUTER MODEL; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; LUNG INFILTRATE; LUNG PARENCHYMA; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; RNA TRANSLATION; SIGNAL TRANSDUCTION; SPUTUM; STEROID RESISTANT ASTHMA; WILD TYPE; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BRONCHIAL HYPERREACTIVITY; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; EGG HYPERSENSITIVITY; EOSINOPHIL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; LUNG ALVEOLUS MACROPHAGE; METABOLISM; NEUTROPHIL; PATHOLOGY; PRIMARY CELL CULTURE; REPORTER GENE;

ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; DEXAMETHASONE; DISEASE MODELS, ANIMAL; EGG HYPERSENSITIVITY; EOSINOPHILS; GENE EXPRESSION REGULATION; GENES, REPORTER; GLUCOCORTICOIDS; HUMANS; INTERFERON-GAMMA; LIPOPOLYSACCHARIDES; LUCIFERASES; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; MICRORNAS; NEUTROPHILS; OLIGONUCLEOTIDES; OVALBUMIN; PRIMARY CELL CULTURE; PROTEIN PHOSPHATASE 2; RECEPTORS, GLUCOCORTICOID; SIGNAL TRANSDUCTION;

EID: 84938737977     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.11.044     Document Type: Article

References (69)

1. J.L. Simpson, R. Scott, M.J. Boyle, and P.G. Gibson Inflammatory subtypes in asthma: assessment and identification using induced sputum Respirology 11 2006 54 61
2. P.G. Gibson Tackling asthma phenotypes in community studies Thorax 64 2009 369 370
3. S.E. Wenzel, L.B. Schwartz, E.L. Langmack, J.L. Halliday, J.B. Trudeau, R.L. Gibbs, and et al. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics Am J Respir Crit Care Med 160 1999 1001 1008
4. G.P. Anderson Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease Lancet 372 2008 1107 1119
5. G.P. Currie, J.G. Douglas, and L.G. Heaney Difficult to treat asthma in adults BMJ 338 2009 b494
6. P.J. Barnes, and I.M. Adcock Glucocorticoid resistance in inflammatory diseases Lancet 373 2009 1905 1917
7. J.L. Simpson, R.J. Scott, M.J. Boyle, and P.G. Gibson Differential proteolytic enzyme activity in eosinophilic and neutrophilic asthma Am J Respir Crit Care Med 172 2005 559 565
8. J.L. Simpson, T.V. Grissell, J. Douwes, R.J. Scott, M.J. Boyle, and P.G. Gibson Innate immune activation in neutrophilic asthma and bronchiectasis Thorax 62 2007 211 218
9. J.J. Li, W. Wang, K.J. Baines, N.A. Bowden, P.M. Hansbro, P.G. Gibson, and et al. IL-27/IFN-gamma induce MyD88-dependent steroid-resistant airway hyperresponsiveness by inhibiting glucocorticoid signaling in macrophages J Immunol 185 2010 4401 4409
10. M. Yang, R.K. Kumar, P.M. Hansbro, and P.S. Foster Emerging roles of pulmonary macrophages in driving the development of severe asthma J Leukoc Biol 91 2012 557 569
11. N.H. ten Hacken, Y. Oosterhoff, H.F. Kauffman, L. Guevarra, T. Satoh, D.J. Tollerud, and et al. Elevated serum interferon-gamma in atopic asthma correlates with increased airways responsiveness and circadian peak expiratory flow variation Eur Respir J 11 1998 312 316
12. N.G. Hansbro, J.C. Horvat, P.A. Wark, and P.M. Hansbro Understanding the mechanisms of viral induced asthma: new therapeutic directions Pharmacol Ther 117 2008 313 353
13. J.L. Simpson, S. Phipps, and P.G. Gibson Inflammatory mechanisms and treatment of obstructive airway diseases with neutrophilic bronchitis Pharmacol Ther 124 2009 86 95
14. M. Yang, R.K. Kumar, and P.S. Foster Pathogenesis of steroid-resistant airway hyperresponsiveness: interaction between IFN-gamma and TLR4/MyD88 pathways J Immunol 182 2009 5107 5115
15. M. Yang, R.K. Kumar, and P.S. Foster Interferon-gamma and pulmonary macrophages contribute to the mechanisms underlying prolonged airway hyperresponsiveness Clin Exp Allergy 40 2010 163 173
16. A. Collison, J. Mattes, M. Plank, and P.S. Foster Inhibition of house dust mite-induced allergic airways disease by antagonism of microRNA-145 is comparable to glucocorticoid treatment J Allergy Clin Immunol 128 2011 160 167.e4
17. J. Mattes, A. Collison, M. Plank, S. Phipps, and P.S. Foster Antagonism of microRNA-126 suppresses the effector function of TH2 cells and the development of allergic airways disease Proc Natl Acad Sci U S A 106 2009 18704 18709
18. R.C. Lee, R.L. Feinbaum, and V. Ambros The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 Cell 75 1993 843 854
19. N.C. Lau, L.P. Lim, E.G. Weinstein, and D.P. Bartel An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans Science 294 2001 858 862
20. M. Hafner, M. Ascano Jr., and T. Tuschl New insights in the mechanism of microRNA-mediated target repression Nat Struct Mol Biol 18 2011 1181 1182
21. Y. Wang, X. Li, and H. Hu Transcriptional regulation of co-expressed microRNA target genes Genomics 98 2011 445 452
22. N. Ma, Y. Xiang, Y. Zhang, and X. Gao A microRNA "target pools" remains mysterious J Cell Biochem 113 2012 1 2
23. L.A. O'Neill, F.J. Sheedy, and C.E. McCoy MicroRNAs: the fine-tuners of Toll-like receptor signalling Nat Rev Immunol 11 2011 163 175
24. H.F. Lodish, B. Zhou, G. Liu, and C.Z. Chen Micromanagement of the immune system by microRNAs Nat Rev Immunol 8 2008 120 130
25. A.L. Kasinski, and F.J. Slack MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy Nat Rev Cancer 11 2011 849 864
26. N. McCarthy Cancer: Small losses, big gains with microRNAs Nat Rev Genet 11 2010 8
27. M. Iborra, F. Bernuzzi, P. Invernizzi, and S. Danese MicroRNAs in autoimmunity and inflammatory bowel disease: crucial regulators in immune response Autoimmun Rev 11 2012 305 314
28. I.K. Oglesby, N.G. McElvaney, and C.M. Greene MicroRNAs in inflammatory lung disease - master regulators or target practice? Respir Res 11 2010 148
29. J.R. Pekow, and J.H. Kwon MicroRNAs in inflammatory bowel disease Inflamm Bowel Dis 18 2012 187 193
30. M. Plank, S. Maltby, J. Mattes, and P.S. Foster Targeting translational control as a novel way to treat inflammatory disease: the emerging role of MicroRNAs Clin Exp Allergy 43 2013 981 999
31. P.S. Foster, M. Plank, A. Collison, H.L. Tay, G.E. Kaiko, J. Li, and et al. The emerging role of microRNAs in regulating immune and inflammatory responses in the lung Immunol Rev 253 2013 198 215
32. A. Collison, C. Herbert, J.S. Siegle, J. Mattes, P.S. Foster, and R.K. Kumar Altered expression of microRNA in the airway wall in chronic asthma: miR-126 as a potential therapeutic target BMC Pulm Med 11 2011 29
33. M. Kumar, T. Ahmad, A. Sharma, U. Mabalirajan, A. Kulshreshtha, A. Agrawal, and et al. Let-7 microRNA-mediated regulation of IL-13 and allergic airway inflammation J Allergy Clin Immunol 128 2011 1077 1085 e10
34. J.S. Mohamed, M.A. Lopez, and A.M. Boriek Mechanical stretch up-regulates microRNA-26a and induces human airway smooth muscle hypertrophy by suppressing glycogen synthase kinase-3beta J Biol Chem 285 2010 29336 29347
35. S. Uchida, A. Nishida, K. Hara, T. Kamemoto, M. Suetsugi, M. Fujimoto, and et al. Characterization of the vulnerability to repeated stress in Fischer 344 rats: possible involvement of microRNA-mediated down-regulation of the glucocorticoid receptor Eur J Neurosci 27 2008 2250 2261
36. A. Kotani, D. Ha, J. Hsieh, P.K. Rao, D. Schotte, M.L. den Boer, and et al. miR-128b is a potent glucocorticoid sensitizer in MLL-AF4 acute lymphocytic leukemia cells and exerts cooperative effects with miR-221 Blood 114 2009 4169 4178
37. G.M. Loewen, E. Tracy, F. Blanchard, D. Tan, J. Yu, S. Raza, and et al. Transformation of human bronchial epithelial cells alters responsiveness to inflammatory cytokines BMC Cancer 5 2005 145
38. B.P. Lewis, C.B. Burge, and D.P. Bartel Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets Cell 120 2005 15 20
39. Y. Kobayashi, N. Mercado, P.J. Barnes, and K. Ito Defects of protein phosphatase 2A causes corticosteroid insensitivity in severe asthma PLoS One 6 2011 e27627
40. J. Lamb, E.D. Crawford, D. Peck, J.W. Modell, I.C. Blat, M.J. Wrobel, and et al. The connectivity map: using gene-expression signatures to connect small molecules, genes, and disease Science 313 2006 1929 1935
41. K. Ito, K.F. Chung, and I.M. Adcock Update on glucocorticoid action and resistance J Allergy Clin Immunol 117 2006 522 543
42. H. Hakonarson, U.S. Bjornsdottir, E. Halapi, J. Bradfield, F. Zink, M. Mouy, and et al. Profiling of genes expressed in peripheral blood mononuclear cells predicts glucocorticoid sensitivity in asthma patients Proc Natl Acad Sci U S A 102 2005 14789 14794
43. U.Y. Yu, and J.H. Ahn Phosphorylation on the PPP2R5D B regulatory subunit modulates the biochemical properties of protein phosphatase 2A BMB Rep 43 2010 263 267
44. J.H. Ahn, Y. Kim, H.S. Kim, P. Greengard, and A.C. Nairn Protein kinase C-dependent dephosphorylation of tyrosine hydroxylase requires the B56delta heterotrimeric form of protein phosphatase 2A PLoS One 6 2011 e26292
45. J.V. Louis, E. Martens, P. Borghgraef, C. Lambrecht, W. Sents, S. Longin, and et al. Mice lacking phosphatase PP2A subunit PR61/B'delta (Ppp2r5d) develop spatially restricted tauopathy by deregulation of CDK5 and GSK3beta Proc Natl Acad Sci U S A 108 2011 6957 6962
46. J.H. Ahn, T. McAvoy, S.V. Rakhilin, A. Nishi, P. Greengard, and A.C. Nairn Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56delta subunit Proc Natl Acad Sci U S A 104 2007 2979 2984
47. D.B. DeFranco, M. Qi, K.C. Borror, M.J. Garabedian, and D.L. Brautigan Protein phosphatase types 1 and/or 2A regulate nucleocytoplasmic shuttling of glucocorticoid receptors Mol Endocrinol 5 1991 1215 1228
48. C. Leucht, C. Stigloher, A. Wizenmann, R. Klafke, A. Folchert, and L. Bally-Cuif MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary Nat Neurosci 11 2008 641 648
49. M. Shibata, D. Kurokawa, H. Nakao, T. Ohmura, and S. Aizawa MicroRNA-9 modulates Cajal-Retzius cell differentiation by suppressing Foxg1 expression in mouse medial pallium J Neurosci 28 2008 10415 10421
50. V. Plaisance, A. Abderrahmani, V. Perret-Menoud, P. Jacquemin, F. Lemaigre, and R. Regazzi MicroRNA-9 controls the expression of Granuphilin/Slp4 and the secretory response of insulin-producing cells J Biol Chem 281 2006 26932 26942
51. H.Y. Wan, L.M. Guo, T. Liu, M. Liu, X. Li, and H. Tang Regulation of the transcription factor NF-kappaB1 by microRNA-9 in human gastric adenocarcinoma Mol Cancer 9 2010 16
52. M.I. Almeida, R.M. Reis, and G.A. Calin MYC-microRNA-9-metastasis connection in breast cancer Cell Res 20 2010 603 604
53. J. Zhang, V. Chintalgattu, T. Shih, D. Ai, Y. Xia, and A.Y. Khakoo MicroRNA-9 is an activation-induced regulator of PDGFR-beta expression in cardiomyocytes J Mol Cell Cardiol 51 2011 337 346
54. F. Bazzoni, M. Rossato, M. Fabbri, D. Gaudiosi, M. Mirolo, L. Mori, and et al. Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals Proc Natl Acad Sci U S A 106 2009 5282 5287
55. F. Dilda, G. Gioia, L. Pisani, L. Restelli, C. Lecchi, F. Albonico, and et al. Escherichia coli lipopolysaccharides and Staphylococcus aureus enterotoxin B differentially modulate inflammatory microRNAs in bovine monocytes Vet J 192 2012 514 516
56. I.M. Adcock, and P.J. Barnes Molecular mechanisms of corticosteroid resistance Chest 134 2008 394 401
57. A.J. Galliher-Beckley, and J.A. Cidlowski Emerging roles of glucocorticoid receptor phosphorylation in modulating glucocorticoid hormone action in health and disease IUBMB Life 61 2009 979 986
58. W. Chen, T. Dang, R.D. Blind, Z. Wang, C.N. Cavasotto, A.B. Hittelman, and et al. Glucocorticoid receptor phosphorylation differentially affects target gene expression Mol Endocrinol 22 2008 1754 1766
59. I. Rogatsky, S.K. Logan, and M.J. Garabedian Antagonism of glucocorticoid receptor transcriptional activation by the c-Jun N-terminal kinase Proc Natl Acad Sci U S A 95 1998 2050 2055
60. Y.T. Ip, and R.J. Davis Signal transduction by the c-Jun N-terminal kinase (JNK) - from inflammation to development Curr Opin Cell Biol 10 1998 205 219
61. T.P. Shanley, N. Vasi, A. Denenberg, and H.R. Wong The serine/threonine phosphatase, PP2A: endogenous regulator of inflammatory cell signaling J Immunol 166 2001 966 972
62. Y. Xu, Y. Xing, Y. Chen, Y. Chao, Z. Lin, E. Fan, and et al. Structure of the protein phosphatase 2A holoenzyme Cell 127 2006 1239 1251
63. A. Collison, L. Hatchwell, N. Verrills, P.A. Wark, A.P. de Siqueira, M. Tooze, and et al. The E3 ubiquitin ligase midline 1 promotes allergen and rhinovirus-induced asthma by inhibiting protein phosphatase 2A activity Nat Med 19 2013 232 237
64. M. Idzko, H. Hammad, M. van Nimwegen, M. Kool, T. Muller, T. Soullie, and et al. Local application of FTY720 to the lung abrogates experimental asthma by altering dendritic cell function J Clin Invest 116 2006 2935 2944
65. E. Sawicka, C. Zuany-Amorim, C. Manlius, A. Trifilieff, V. Brinkmann, D.M. Kemeny, and et al. Inhibition of Th1- and Th2-mediated airway inflammation by the sphingosine 1-phosphate receptor agonist FTY720 J Immunol 171 2003 6206 6214
66. C.H. Switzer, R.Y. Cheng, T.M. Vitek, D.J. Christensen, D.A. Wink, and M.P. Vitek Targeting SET/I(2)PP2A oncoprotein functions as a multi-pathway strategy for cancer therapy Oncogene 30 2011 2504 2513
67. S.A. Saddoughi, S. Gencer, Y.K. Peterson, K.E. Ward, A. Mukhopadhyay, J. Oaks, and et al. Sphingosine analogue drug FTY720 targets I2PP2A/SET and mediates lung tumour suppression via activation of PP2A-RIPK1-dependent necroptosis EMBO Mol Med 5 2013 105 121
68. L. Hatchwell, J. Girkin, M.D. Dun, M. Morten, N. Verrills, H.D. Toop, and et al. Salmeterol attenuates chemotactic responses in rhinovirus-induced exacerbation of allergic airways disease by modulating protein phosphatase 2A J Allergy Clin Immunol 133 2014 1720 1727
69. S. Saito, M. Miyaji-Yamaguchi, T. Shimoyama, and K. Nagata Functional domains of template-activating factor-I as a protein phosphatase 2A inhibitor Biochem Biophys Res Commun 259 1999 471 475