Airway smooth muscle hyperproliferation is regulated by MicroRNA-221 in severe asthma

American Journal of Respiratory Cell and Molecular Biology

Volumn 50, Issue 1, 2014, Pages 7-17

  Perry, Mark M ^a   Baker, Josie E ^a   Gibeon, David S ^a,b   Adcock, Ian M ^a,b   Chung, Kian Fan ^a,b  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

ASM; IL 6; MicroRNA; Proliferation; Steroid Insensitivity

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE INHIBITOR; DEXAMETHASONE; INTERLEUKIN 6; MESSENGER RNA; MICRORNA 221; MICRORNA 222; PROTEIN P21; PROTEIN P27; TRANSFORMING GROWTH FACTOR BETA;

AIRWAY SMOOTH MUSCLE; ARTICLE; ASTHMA; BRONCHUS BIOPSY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE SEVERITY; DNA SYNTHESIS; ENZYME LINKED IMMUNOSORBENT ASSAY; FETAL CALF SERUM; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; RNA ANALYSIS; SMOOTH MUSCLE FIBER;

ADULT; ASTHMA; BRONCHI; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; HUMANS; INTERLEUKIN-6; MALE; MICRORNAS; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84891750914     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0067OC     Document Type: Article

References (49)

1. Bousquet J, Jeffery PK, Busse WW, Johnson M, Vignola AM. Asthma: from bronchoconstriction to airways inflammation and remodeling. Am J Respir Crit Care Med 2000; 161: 1720-1745. (Pubitemid 30329053)
2. Chung KF. Should treatments for asthma be aimed at the airway smooth muscle? Expert Rev Respir Med 2007; 1: 209-217.
3. Halayko AJ, Amrani Y. Mechanisms of inflammation-mediated airway smooth muscle plasticity and airways remodeling in asthma. Respir Physiol Neurobiol 2003; 137: 209-222. (Pubitemid 37153283)
4. Michaeloudes C, Chang PJ, Petrou M, Chung KF. Transforming growth factor-b and nuclear factor E2-related factor 2 regulate antioxidant responses in airway smooth muscle cells: role in asthma. Am J Respir Crit Care Med 2011; 184: 894-903.
5. Michaeloudes C, Sukkar MB, Khorasani NM, Bhavsar PK, Chung KF. TGF-β regulates Nox4, MnSOD and catalase expression, and IL-6 release in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2011; 300: L295-L304.
6. Chung KF, Godard P, Adelroth E, Ayres J, Barnes N, Barnes P, Bel E, Burney P, Chanez P, Connett G, et al. Difficult/therapy-resistant asthma: the need for an integrated approach to define clinical phenotypes, evaluate risk factors, understand pathophysiology and find novel therapies: ERS Task Force on Difficult/Therapy-Resistant Asthma. Eur Respir J 1999; 13: 1198-1208. (Pubitemid 29288952)
7. Benayoun L, Druilhe A, Dombret MC, Aubier M, Pretolani M. Airway structural alterations selectively associated with severe asthma. Am J Respir Crit Care Med 2003; 167: 1360-1368. (Pubitemid 36609720)
8. Macedo P, Hew M, Torrego A, Jouneau S, Oates T, Durham A, Chung KF. Inflammatory biomarkers in airways of patients with severe asthma compared with non-severe asthma. Clin Exp Allergy 2009; 39: 1668-1676.
9. Johnson PR, Roth M, Tamm M, Hughes M, Ge Q, King G, Burgess JK, Black JL. Airway smooth muscle cell proliferation is increased in asthma. Am J Respir Crit Care Med 2001; 164: 474-477. (Pubitemid 32778219)
10. Trian T, Benard G, Begueret H, Rossignol R, Girodet PO, Ghosh D, Ousova O, Vernejoux JM, Marthan R, Tunon-de-Lara JM, et al. Bronchial smooth muscle remodeling involves calcium-dependent enhanced mitochondrial biogenesis in asthma. J Exp Med 2007; 204: 3173-3181.
11. Hassan M, Jo T, Risse PA, Tolloczko B, Lemière C, Olivenstein R, Hamid Q, Martin JG. Airway smooth muscle remodeling is a dynamic process in severe long-standing asthma. J Allergy Clin Immunol 2010; 125: 1037-1045, e3.
12. Bhavsar P, Hew M, Khorasani N, Torrego A, Barnes PJ, Adcock I, Chung KF. Relative corticosteroid insensitivity of alveolar macrophages in severe asthma compared with non-severe asthma. Thorax 2008; 63: 784-790.
13. Hew M, Bhavsar P, Torrego A, Meah S, Khorasani N, Barnes PJ, Adcock I, Chung KF. Relative corticosteroid insensitivity of peripheral blood mononuclear cells in severe asthma. Am J Respir Crit Care Med 2006; 174: 134-141. (Pubitemid 44015386)
14. Roth M, Johnson PR, Borger P, Bihl MP, Rüdiger JJ, King GG, Ge Q, Hostettler K, Burgess JK, Black JL, et al. Dysfunctional interaction of C/EBPalpha and the glucocorticoid receptor in asthmatic bronchial smooth-muscle cells. N Engl J Med 2004; 351: 560-574. (Pubitemid 39025173)
15. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
16. Kuhn AR, Schlauch K, Lao R, Halayko AJ, Gerthoffer WT, Singer CA. MicroRNA expression in human airway smooth muscle cells: role of miR-25 in regulation of airway smooth muscle phenotype. Am J Respir Cell Mol Biol 2010; 42: 506-513.
17. le Sage C, Nagel R, Egan DA, Schrier M, Mesman E, Mangiola A, Anile C, Maira G, Mercatelli N, Ciafrè SA, et al. Regulation of the p27(kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J 2007; 26: 3699-3708. (Pubitemid 47236875)
18. Liu X, Cheng Y, Zhang S, Lin Y, Yang J, Zhang C. A necessary role of miR-221 and miR-222 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res 2009; 104: 476-487.
19. Zhang C, Zhang J, Zhang A, Wang Y, Han L, You Y, Pu P, Kang C. PUMA is a novel target of miR-221/222 in human epithelial cancers. Int J Oncol 2010; 37: 1621-1626.
20. Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. Induction of microRNA-221 by platelet-derived growth factor signaling is critical for modulation of vascular smooth muscle phenotype. J Biol Chem 2009; 284: 3728-3738.
21. American Thoracic Society. Proceedings of the ATS Workshop on Refractory Asthma: current understanding, recommendations, and unanswered questions. Am J Respir Crit Care Med 2000; 162: 2341-2351.
22. 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.
23. Perry MM, Hui CK, Whiteman M, Wood ME, Adcock I, Kirkham P, Michaeloudes C, Chung KF. Hydrogen sulfide inhibits proliferation and release of IL-8 from human airway smooth muscle cells. Am J Respir Cell Mol Biol 2011; 45: 746-752.
24. Moschos SA, Jones SW, Perry MM, Williams AE, Erjefalt JS, Turner JJ, Barnes PJ, Sproat BS, Gait MJ, Lindsay MA. Lung delivery studies using siRNA conjugated to TAT(48-60) and penetratin reveal peptide induced reduction in gene expression and induction of innate immunity. Bioconjug Chem 2007; 18: 1450-1459. (Pubitemid 47464052)
25. Perry MM, Moschos SA, Williams AE, Shepherd NJ, Larner-Svensson HM, Lindsay MA. Rapid changes in microRNA-146a expression negatively regulate the IL-1beta-induced inflammatory response in human lung alveolar epithelial cells. J Immunol 2008; 180: 5689-5698.
26. Larner-Svensson HM, Williams AE, Tsitsiou E, Perry MM, Jiang X, Chung KF, Lindsay MA. Pharmacological studies of the mechanism and function of interleukin-1beta-induced miRNA-146a expression in primary human airway smooth muscle. Respir Res 2010; 11: 68.
27. Xie S, Sukkar MB, Issa R, Khorasani NM, Chung KF. Mechanisms of induction of airway smooth muscle hyperplasia by transforming growth factor-beta. Am J Physiol Lung Cell Mol Physiol 2007; 293: L245-L253. (Pubitemid 47080733)
28. Burgess JK, Johnson PR, Ge Q, Au WW, Poniris MH, McParland BE, King G, Roth M, Black JL. Expression of connective tissue growth factor in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2003; 167: 71-77. (Pubitemid 36015920)
29. Brightling CE, Ammit AJ, Kaur D, Black JL, Wardlaw AJ, Hughes JM, Bradding P. 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. (Pubitemid 40663721)
30. John AE, Zhu YM, Brightling CE, Pang L, Knox AJ. Human airway smooth muscle cells from asthmatic individuals have CXCL8 hypersecretion due to increased NF-kappa B p65, C/EBP beta, and RNA polymerase II binding to the CXCL8 promoter. J Immunol 2009; 183: 4682-4692.
31. Chan V, Burgess JK, Ratoff JC, O'Connor BJ, Greenough A, Lee TH, Hirst SJ. Extracellular matrix regulates enhanced eotaxin expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 2006; 174: 379-385. (Pubitemid 44223117)
32. Chung KF. Airway smooth muscle cells: contributing to and regulating airway mucosal inflammation? Eur Respir J 2000; 15: 961-968. (Pubitemid 30321858)
33. Felicetti F, Errico MC, Bottero L, Segnalini P, Stoppacciaro A, Biffoni M, Felli N, Mattia G, Petrini M, Colombo MP, et al. The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms. Cancer Res 2008; 68: 2745-2754. (Pubitemid 351556272)
34. Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL, Jacob S, Majumder S. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27kip1. J Biol Chem 2008; 283: 29897-29903.
35. Sun T, Yang M, Kantoff PW, Lee GSM. Role of microRNA-221/-222 in cancer development and progression. Cell Cycle 2009; 8: 2315-2316.
36. Chun-Zhi Z, Lei H, An-Ling Z, Yan-Chao F, Xiao Y, Guang-Xiu W, Zhi- Fan J, Pei-Yu P, Qing-Yu Z, Chun-Sheng K. MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer 2010; 10: 367.
37. Minami Y, Satoh M, Maesawa C, Takahashi Y, Tabuchi T, Itoh T, Nakamura M. Effect of atorvastatin on microRNA 221/222 expression in endothelial progenitor cells obtained from patients with coronary artery disease. Eur J Clin Invest 2009; 39: 359-367.
38. Galardi S, Mercatelli N, Giorda E, Massalini S, Frajese GV, Ciafrè SA, Farace MG. miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27kip1. J Biol Chem 2007; 282: 23716-23724. (Pubitemid 47311902)
39. Tuccoli A, Poliseno L, Rainaldi G. miRNAs regulate miRNAs: coordinated transcriptional and post-transcriptional regulation. Cell Cycle 2006; 5: 2473-2476. (Pubitemid 44785824)
40. Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, Zucman-Rossi J. MicroRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology 2008; 47: 1955-1963. (Pubitemid 351952843)
41. Obernosterer G, Leuschner PJ, Alenius M, Martinez J. Posttranscriptional regulation of microRNA expression. RNA 2006; 12: 1161-1167.
42. Wulczyn FG, Smirnova L, Rybak A, Brandt C, Kwidzinski E, Ninnemann O, Strehle M, Seiler A, Schumacher S, Nitsch R. Post-transcriptional regulation of the LET-7 microRNA during neural cell specification. FASEB J 2007; 21: 415-426. (Pubitemid 46213489)
43. Davis BN, Hilyard AC, Lagna G, Hata A. Smad proteins control Droshamediated microRNA maturation. Nature 2008; 454: 56-61. (Pubitemid 351931982)
44. Ozsolak F, Poling LL, Wang Z, Liu H, Liu XS, Roeder RG, Zhang X, Song JS, Fisher DE. Chromatin structure analyses identify miRNA promoters. Genes Dev 2008; 22: 3172-3183.
45. Galardi S, Mercatelli N, Farace MG, CiafrèSA. NF-κ β and c-Jun induce the expression of the oncogenic miR-221 and miR-222 in prostate carcinoma and glioblastoma cells. Nucleic Acids Res 2011; 39: 3892-3902.
46. Terasawa K, Ichimura A, Sato F, Shimizu K, Tsujimoto G. Sustained activation of ERK1/2 by NGF induces microRNA-221 and 222 in PC12 cells. FEBS J 2009; 276: 3269-3276.
47. Williams AE, Larner-Svensson H, Perry MM, Campbell GA, Herrick SE, Adcock IM, Erjefalt JS, Chung KF, Lindsay MA. MicroRNA expression profiling in mild asthmatic human airways and effect of corticosteroid therapy. PLoS ONE 2009; 4: e5889.
48. Ito K, Chung KF, Adcock IM. Update on glucocorticoid action and resistance. J Allergy Clin Immunol 2006; 117: 522-543. (Pubitemid 43340215)
49. Moschos SA, Williams AE, Perry MM, Birrell MA, Belvisi MG, Lindsay MA. Expression profiling in vivo demonstrates rapid changes in lung microRNA levels following lipopolysaccharide-induced inflammation but not in the anti-inflammatory action of glucocorticoids. BMC Genomics 2007; 8: 240.