Constitutive high expression of protein arginine methyltransferase 1 in asthmatic airway smooth muscle cells is caused by reduced microRNA-19a expression and leads to enhanced remodeling

Journal of Allergy and Clinical Immunology

Volumn 140, Issue 2, 2017, Pages 510-524.e3

  Sun, Qingzhu ^a,b   Liu, Li ^a   Wang, Hui ^b   Mandal, Jyotshna ^b   Khan, Petra ^b   Hostettler, Katrin E ^b   Stolz, Daiana ^b   Tamm, Michael ^b   Molino, Antonio ^c   Lardinois, Didier ^d   Lu, Shemin ^a   Roth, Michael ^b  

^a MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Airway wall remodeling; extracellular signal regulated kinase; miR 19a; primary airway smooth muscle cell; protein arginine methyltransferase 1; STAT1

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ACETYLSALICYLIC ACID; BUDESONIDE PLUS FORMOTEROL; CICLESONIDE; FENOTEROL; FENOTEROL PLUS IPRATROPIUM BROMIDE; FLUTICASONE FUROATE; FLUTICASONE FUROATE PLUS VILANTEROL; FLUTICASONE PROPIONATE PLUS FORMOTEROL FUMARATE; FLUTICASONE PROPIONATE PLUS SALMETEROL XINAFOATE; FORMOTEROL; FORMOTEROL FUMARATE; INDACATEROL; INFLIXIMAB; MICRORNA; MICRORNA 19A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONTELUKAST; OMALIZUMAB; PANTOPRAZOLE; PLATELET DERIVED GROWTH FACTOR BB; PREDNISOLONE; PREDNISONE; PROTEIN ARGININE METHYLTRANSFERASE; SALBUTAMOL; SMALL INTERFERING RNA; STAT1 PROTEIN; TIOTROPIUM BROMIDE; UNCLASSIFIED DRUG; UNINDEXED DRUG; COLLAGEN TYPE 1; FIBRINOGEN; MESSENGER RNA; MIRN19 MICRORNA, HUMAN; PRMT1 PROTEIN, HUMAN; REPRESSOR PROTEIN; STAT1 PROTEIN, HUMAN;

ADULT; AGED; AIRWAY REMODELING; AIRWAY SMOOTH MUSCLE CELL; ARTICLE; ASTHMA; CELL ACTIVATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG BIOPSY; LUNG PARENCHYMA; MALE; MIDDLE AGED; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; VERY ELDERLY; CELL CULTURE; GENETICS; LUNG; METABOLISM; PATHOLOGY; SMOOTH MUSCLE CELL;

AGED; AGED, 80 AND OVER; AIRWAY REMODELING; ASTHMA; CELLS, CULTURED; COLLAGEN TYPE I; FEMALE; FIBRINOGEN; HUMANS; LUNG; MALE; MICRORNAS; MIDDLE AGED; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYOCYTES, SMOOTH MUSCLE; PROTEIN-ARGININE N-METHYLTRANSFERASES; REPRESSOR PROTEINS; RNA, MESSENGER; STAT1 TRANSCRIPTION FACTOR;

EID: 85026293578     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.11.013     Document Type: Article

References (45)

1. Gosens, R., Grainge, C., Bronchoconstriction and airway biology potential impact and therapeutic opportunities. Chest 147 (2015), 798–803.
2. Kariyawasam, H.H., Aizen, M., Barkans, J., Robinson, D.S., Kay, A.B., Remodeling and airway hyperresponsiveness but not cellular inflammation persist after allergen challenge in asthma. Am J Respir Crit Care Med 175 (2007), 896–904.
3. Grainge, C.L., Lau, L.C., Ward, J.A., Dulay, V., Lahiff, G., Wilson, S., et al. Effect of bronchoconstriction on airway remodeling in asthma. N Engl J Med 364 (2011), 2006–2015.
4. Bourke, J.E., Li, X., Foster, S.R., Wee, E., Dagher, H., Ziogas, J., et al. Collagen remodelling by airway smooth muscle is resistant to steroids and beta(2)-agonists. Eur Respir J 37 (2011), 173–182.
5. Dolhnikoff, M., da Silva, L.F.F., de Araujo, B.B., Gomes, H.A.P., Fernezlian, S., Mulder, A., et al. The outer wall of small airways is a major site of remodeling in fatal asthma. J Allergy Clin Immunol 123 (2009), 1090–1097.
6. Hosoki, K., Ying, S., Corrigan, C., Qi, H.B., Kurosky, A., Jennings, K., et al. Analysis of a panel of 48 cytokines in BAL fluids specifically identifies IL-8 levels as the only cytokine that distinguishes controlled asthma from uncontrolled asthma, and correlates inversely with FEV1. PLoS One, 10, 2015, e0126035.
7. Lewis, C.C., Chu, H.W., Westcott, J.Y., Tucker, A., Langmack, E.L., Sutherland, E.R., et al. Airway fibroblasts exhibit a synthetic phenotype in severe asthma. J Allergy Clin Immunol 115 (2005), 534–540.
8. Hirota, J.A., Ask, K., Farkas, L., Smith, J.A., Ellis, R., Rodriguez-Lecompte, J.C., et al. In vivo role of platelet-derived growth factor-BB in airway smooth muscle proliferation in mouse lung. Am J Respir Cell Mol Biol 45 (2011), 566–572.
9. Ito, I., Fixman, E.D., Asai, K., Yoshida, M., Gounni, A.S., Martin, J.G., et al. Platelet-derived growth factor and transforming growth factor-beta modulate the expression of matrix metalloproteinases and migratory function of human airway smooth muscle cells. Clin Exp Allergy 39 (2009), 1370–1380.
10. Harb, H., Renz, H., Update on epigenetics in allergic disease. J Allergy Clin Immunol 135 (2015), 15–24.
11. Nicholson, T.B., Chen, T.P., Richard, S., The physiological and pathophysiological role of PRMT1-mediated protein arginine methylation. Pharmacol Res 60 (2009), 466–474.
12. Sun, Q., Liu, L., Roth, M., Tian, J., He, Q., Zhong, B., et al. PRMT1 upregulated by epithelial proinflammatory cytokines participates in COX2 expression in fibroblasts and chronic antigen-induced pulmonary inflammation. J Immunol 195 (2015), 298–306.
13. Sun, Q., Yang, X., Zhong, B., Jiao, F., Li, C., Li, D., et al. Upregulated protein arginine methyltransferase 1 by IL-4 increases eotaxin-1 expression in airway epithelial cells and participates in antigen-induced pulmonary inflammation in rats. J Immunol 188 (2012), 3506–3512.
14. Sun, Q., Liu, L., Mandal, J., Molino, A., Stolz, D., Tamm, M., et al. PDGF-BB induces PRMT1 expression through ERK1/2 dependent STAT1 activation and regulates remodeling in primary human lung fibroblasts. Cell Signal 28 (2016), 307–315.
15. Ambros, V., The functions of animal microRNAs. Nature 431 (2004), 350–355.
16. Deshpande, D.A., Dileepan, M., Walseth, T.F., Subramanian, S., Kannan, M.S., MicroRNA regulation of airway inflammation and airway smooth muscle function: relevance to asthma. Drug Dev Res 76 (2015), 286–295.
17. Mendell, J.T., miRiad roles for the miR-17-92 cluster in development and disease. Cell 133 (2008), 217–222.
18. Zhou, P., Ma, L., Zhou, J., Jiang, M., Rao, E., Zhao, Y., et al. miR-17-92 plays an oncogenic role and conveys chemo-resistance to cisplatin in human prostate cancer cells. Int J Oncol 48 (2016), 1737–1748.
19. Johnson, P.R.A., Roth, M., Tamm, M., Hughes, M., Ge, Q., King, G., et al. Airway smooth muscle cell proliferation is increased in asthma. Am J Respir Crit Care Med 164 (2001), 474–477.
20. Lambers, C., Qi, Y., Eleni, P., Costa, L., Zhong, J., Tamm, M., et al. Extracellular matrix composition is modified by beta(2)-agonists through cAMP in COPD. Biochem Pharmacol 91 (2014), 400–408.
21. Chakir, J., Haj-Salem, I., Gras, D., Joubert, P., Beaudoin, E.L., Biardel, S., et al. Effects of bronchial thermoplasty on airway smooth muscle and collagen deposition in asthma. Ann Am Thorac Soc 12 (2015), 1612–1618.
22. Denner, D.R., Doeing, D.C., Hogarth, D.K., Dugan, K., Naureckas, E.T., White, S.R., Airway inflammation after bronchial thermoplasty for severe asthma. Ann Am Thorac Soc 12 (2015), 1302–1309.
23. Karakiulakis, G., Papakonstantinou, E., Aletras, A.J., Tamm, M., Roth, M., Cell type-specific effect of hypoxia and platelet-derived growth factor-BB on extracellular matrix turnover and its consequences for lung remodeling. J Biol Chem 282 (2007), 908–915.
24. Simon, A.R., Takahashi, S., Severgnini, M., Fanburg, B.L., Cochran, B.H., Role of the JAK-STAT pathway in PDGF-stimulated proliferation of human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 282 (2002), L1296–L1304.
25. Westergren-Thorsson, G., Larsen, K., Nihlberg, K., Andersson-Sjoland, A., Hallgren, O., Marko-Varga, G., et al. Pathological airway remodelling in inflammation. Clin Respir J 4:suppl 1 (2010), 1–8.
26. Jones, R.L., Elliot, J.G., James, A.L., Estimating airway smooth muscle cell volume and number in airway sections. Sources of variability. Am J Respir Cell Mol Biol 50 (2014), 246–252.
27. Togo, S., Holz, O., Liu, X., Sugiura, H., Kamio, K., Wang, X., et al. Lung fibroblast repair functions in patients with chronic obstructive pulmonary disease are altered by multiple mechanisms. Am J Respir Crit Care Med 178 (2008), 248–260.
28. Ingram, J.L., Bonner, J.C., EGF and PDGF receptor tyrosine kinases as therapeutic targets for chronic lung diseases. Curr Mol Med 6 (2006), 409–421.
29. Ammit, A.J., Panettieri, R.A. Jr., Invited review: the circle of life: cell cycle regulation in airway smooth muscle. J Appl Physiol (1985) 91 (2001), 1431–1437.
30. Page, K., Hershenson, M.B., Mitogen-activated signaling and cell cycle regulation in airway smooth muscle. Front Biosci 5 (2000), D258–D267.
31. Laliena, A., San Miguel, B., Crespo, I., Alvarez, M., Gonzalez-Gallego, J., Tunon, M.J., Melatonin attenuates inflammation and promotes regeneration in rabbits with fulminant hepatitis of viral origin. J Pineal Res 53 (2012), 270–278.
32. Escobar, J., Pereda, J., Lopez-Rodas, G., Sastre, J., Redox signaling and histone acetylation in acute pancreatitis. Free Radic Biol Med 52 (2012), 819–837.
33. Li, P.C., Sheu, M.J., Ma, W.F., Pan, C.H., Sheu, J.H., Wu, C.H., Anti-restenotic roles of dihydroaustrasulfone alcohol involved in inhibiting PDGF-BB-stimulated proliferation and migration of vascular smooth muscle cells. Mar Drugs 13 (2015), 3046–3060.
34. Pintus, G., Tadolini, B., Posadino, A.M., Sanna, B., Debidda, M., Carru, C., et al. PKC/Raf/MEK/ERK signaling pathway modulates native-LDL-induced E2F-1 gene expression and endothelial cell proliferation. Cardiovasc Res 59 (2003), 934–944.
35. Yu, Z., Xu, J., Liu, J., Wu, J., Lee, C.M., Yu, L., et al. Epithelium-specific Ets-like transcription factor 1, ESE-1, regulates ICAM-1 expression in cultured lung epithelial cell lines. Mediators Inflamm, 2015, 2015, 547928.
36. Fang, Y., Zhong, L., Lin, M., Zhou, X., Jing, H., Ying, M., et al. MEK/ERK dependent activation of STAT1 mediates dasatinib-induced differentiation of acute myeloid leukemia. PLoS One, 8, 2013, e66915.
37. Liu, W.M., Liang, Q.L., Balzar, S., Wenzel, S., Gorska, M., Alam, R., Cell-specific activation profile of extracellular signal-regulated kinase 1/2, Jun N-terminal kinase, and p38 mitogen-activated protein kinases in asthmatic airways. J Allergy Clin Immunol 121 (2008), 893–902.
38. Burgess, J.K., Lee, J.H., Ge, Q., Ramsay, E.E., Poniris, M.H., Parmentier, J., et al. Dual ERK and phosphatidylinositol 3-kinase pathways control airway smooth muscle proliferation: differences in asthma. J Cell Physiol 216 (2008), 673–679.
39. Joshi, S.R., Comer, B.S., McLendon, J.M., Gerthoffer, W.T., MicroRNA regulation of smooth muscle phenotype. Mol Cell Pharmacol 4 (2012), 1–16.
40. Solberg, O.D., Ostrin, E.J., Love, M.I., Peng, J.C., Bhakta, N.R., Hou, L., et al. Airway 2pithelial miRNA expression is altered in asthma. Am J Respir Crit Care Med 186 (2012), 965–974.
41. Martinez-Nunez, R.T., Bondanese, V.P., Louafi, F., Francisco-Garcia, A.S., Rupani, H., Bedke, N., et al. A microRNA network dysregulated in asthma controls IL-6 production in bronchial epithelial cells. PLoS One, 9, 2014, e111659.
42. Simpson, L.J., Patel, S., Bhakta, N.R., Choy, D.F., Brightbill, H.D., Ren, X., et al. A microRNA upregulated in asthma airway T cells promotes TH2 cytokine production. Nat Immunol 15 (2014), 1162–1170.
43. Simeone-Penney, M.C., Severgnini, M., Rozo, L., Takahashi, S., Cochran, B.H., Simon, A.R., PDGF-induced human airway smooth muscle cell proliferation requires STAT3 and the small GTPase Rac1. Am J Physiol Lung Cell Mol Physiol 294 (2008), L698–L704.
44. Berair, R., Saunders, R., Brightling, C.E., Origins of increased airway smooth muscle mass in asthma. BMC Med, 11, 2013, 145.
45. Krymskaya, V.P., Goncharova, E.A., Ammit, A.J., Lim, P.N., Goncharov, D.A., Eszterhas, A., et al. Src is necessary and sufficient for human airway smooth muscle cell proliferation and migration. FASEB J, 18, 2004, 428.