MiR-199a-5p silencing regulates the unfolded protein response in chronic obstructive pulmonary disease and α1-antitrypsin deficiency

American Journal of Respiratory and Critical Care Medicine

Volumn 189, Issue 3, 2014, Pages 263-273

  Hassan, Tidi ^a   Carroll, Tomás P ^a   Buckley, Patrick G ^b   Cummins, Robert ^a   O'Neill, Shane J ^a   McElvaney, Noel G ^a   Greene, Catherine M ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b BEAUMONT HOSPITAL   (Ireland)

Author keywords

1 antitrypsin; Chronic obstructive pulmonary disease; MIR 199a 5p; Promoter hypermethylation; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ALPHA 1 ANTITRYPSIN; GLUCOSE REGULATED PROTEIN 78; LUCIFERASE; MICRORNA; MICRORNA 199A 5P; PROTEIN P50; UNCLASSIFIED DRUG;

ADULT; ALPHA 1 ANTITRYPSIN DEFICIENCY; ARTICLE; CELL ISOLATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CLINICAL ARTICLE; FEMALE; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; MALE; MONOCYTE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYROSEQUENCING; RECEPTOR DOWN REGULATION; REPORTER GENE; UNFOLDED PROTEIN RESPONSE; WESTERN BLOTTING;

ADULT; ALPHA 1-ANTITRYPSIN DEFICIENCY; ASYMPTOMATIC DISEASES; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CYTOKINES; FEMALE; GENE EXPRESSION PROFILING; GENE SILENCING; HUMANS; MALE; METHYLATION; MICRORNAS; MIDDLE AGED; MONOCYTES; PHENOTYPE; POLYMERASE CHAIN REACTION; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; SEQUENCE ANALYSIS, RNA; STRESS, PHYSIOLOGICAL; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 84893562352     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201306-1151OC     Document Type: Article

References (53)

1. Silverman EK, Sandhaus RA. Clinical practice: alpha1-antitrypsin deficiency. N Engl J Med 2009;360:2749-2757.
2. Rogers J, Kalsheker N, Wallis S, Speer A, Coutelle CH, Woods D, Humphries SE. The isolation of a clone for human alpha 1-antitrypsin and the detection of alpha 1-antitrypsin in mRNA from liver and leukocytes. Biochem Biophys Res Commun 1983;116:375-382.
3. Cichy J, Potempa J, Travis J. Biosynthesis of alpha1-proteinase inhibitor by human lung-derived epithelial cells. J Biol Chem 1997;272: 8250-8255.
4. Carroll TP, Greene CM, O'Connor CA, Nolan AM, O'Neill SJ, McElvaney NG. Evidence for unfolded protein response activation in monocytes from individuals with alpha-1 antitrypsin deficiency. J Immunol 2010; 184:4538-4546.
5. Greene CM, McElvaney NG. Z α-1 antitrypsin deficiency and the endoplasmic reticulum stress response World J Gastrointest Pharmacol Ther 2010;1:94-101.
6. Malhotra JD, Kaufman RJ. The endoplasmic reticulum and the unfolded protein response. Semin Cell Dev Biol 2007;18:716-731.
7. Wiseman RL, Haynes CM, Ron D. SnapShot: the unfolded protein response. Cell 2010;140:590-595.e2.
8. Mori K. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 2000;101:451-454.
9. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999;397: 271-274.
10. Yoshida HT, Matsui T, Yamamoto A, Okada T, Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001;107:881-891.
11. Kaneko M, Niinuma Y, Nomura Y. Activation signal of nuclear factorkappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol Pharm Bull 2003;26:931-935.
12. Lawless MW, Greene CM, Mulgrew A, Taggart CC, O'Neill SJ, McElvaney NG. Activation of endoplasmic reticulum-specific stress responses associated with the conformational disease Z alpha 1-antitrypsin deficiency. J Immunol 2004;172:5722-5726.
13. Greene CM, Miller SD, Carroll TP, Oglesby IK, Ahmed F, O'Mahony M, Taggart CC, McElvaney NG, O'Neill SJ. Anti-apoptotic effects of Z alpha1-antitrypsin in human bronchial epithelial cells. Eur Respir J 2010;35:1155-1163.
14. Hidvegi T, Schmidt BZ, Hale P, Perlmutter DH. Accumulation of mutant alpha1-antitrypsin Z in the endoplasmic reticulum activates caspases-4 and -12, NFkappaB, and BAP31 but not the unfolded protein response. J Biol Chem 2005;280:39002-39015.
15. Hengstermann A, Müller T. Endoplasmic reticulum stress induced by aqueous extracts of cigarette smoke in 3T3 cells activates the unfolded-protein-response-dependent PERK pathway of cell survival. Free Radic Biol Med 2008;44:1097-1107.
16. Jorgensen E, Stinson A, Shan L, Yang J, Gietl D, Albino AP. Cigarette smoke induces endoplasmic reticulum stress and the unfolded protein response in normal and malignant human lung cells. BMC Cancer 2008;8:229.
17. Tagawa Y, Hiramatsu N, Kasai A, Hayakawa K, Okamura M, Yao J, et al. Induction of apoptosis by cigarette smoke via ROS-dependent endoplasmic reticulum stress and CCAAT/enhancer-binding protein-homologous protein (CHOP). Free Radic Biol Med 2008;45:50-59.
18. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006;13:1097-1101.
19. Hassan T, McKiernan PJ, McElvaney NG, Cryan SA, Greene CM. Therapeutic modulation of miRNA for the treatment of proinflammatory lung diseases. Expert Rev Anti Infect Ther 2012;10: 359-368.
20. Bartoszewski R, Brewer JW, Rab A, Crossman DK, Bartoszewska S, Kapoor N, Fuller C, Collawn JF, Bebok Z. The unfolded protein response (UPR)-activated transcription factor X-box-binding protein 1 (XBP1) induces microRNA-346 expression that targets the human antigen peptide transporter 1 (TAP1) mRNA and governs immune regulatory genes. J Biol Chem 2011;286:41862-41870.
21. Behrman S, Acosta-Alvear D, Walter P. A CHOP-regulated microRNA controls rhodopsin expression. J Cell Biol 2011;192:919-927.
22. Belmont PJ, Chen WJ, Thuerauf DJ, Glembotski CC. Regulation of microRNA expression in the heart by the ATF6 branch of the ER stress response. J Mol Cell Cardiol 2012;52:1176-1182.
23. Qiu W, Baccarelli A, Carey VJ, Boutaoui N, Bacherman H, Klanderman B, Rennard S, Agusti A, Anderson W, Lomas DA, et al. Variable DNA methylation is associated with chronic obstructive pulmonary disease and lung function. Am J Respir Crit Care Med 2012;185: 373-381.
24. Belinsky SA, Klinge DM, Dekker JD, Smith MW, Bocklage TJ, Gilliland FD, Crowell RE, Karp DD, Stidley CA, Picchi MA. Gene promoter methylation in plasma and sputum increases with lung cancer risk. Clin Cancer Res 2005;11:6505-6511.
25. Talikka M, Sierro N, Ivanov NV, Chaudhary N, Peck MJ, Hoeng J, Coggins CR, Peitsch MC. Genomic impact of cigarette smoke, with application to three smoking-related diseases. Crit Rev Toxicol 2012; 42:877-889.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-408.
27. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 2002;415:92-96.
28. Sakurai K, Furukawa C, Haraguchi T, Inada K, Shiogama K, Tagawa T, Fujita S, Ueno Y, Ogata A, Ito M, et al. MicroRNAs miR-199a-5p and -3p target the Brm subunit of SWI/SNF to generate a doublenegative feedback loop in a variety of human cancers. Cancer Res 2011;71:1680-1689.
29. Cheung HH, Davis AJ, Lee TL, Pang AL, Nagrani S, Rennert OM, Chan WY. Methylation of an intronic region regulates miR-199a in testicular tumor malignancy. Oncogene 2011;30:3404-3415.
30. Duan Q, Wang X, Gong W, Ni L, Chen C, He X, Chen F, Yang L, Wang P, Wang DW. ER stress negatively modulates the expression of the miR-199a/214 cluster to regulates tumor survival and progression in human hepatocellular cancer. PLoS ONE 2012;7:e31518.
31. Shatseva T, Lee DY, Deng Z, Yang BB. MicroRNA miR-199a-3p regulates cell proliferation and survival by targeting caveolin-2. J Cell Sci 2011;124:2826-2836.
32. Geraghty P, Wallace A, D'Armiento JM. Induction of the unfolded protein response by cigarette smoke is primarily an activating transcription factor 4-C/EBP homologous protein mediated process. Int J Chron Obstruct Pulmon Dis 2011;6:309-319.
33. Kelsen SG, Duan X, Ji R, Perez O, Liu C, Merali S. Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am J Respir Cell Mol Biol 2008;38:541-550.
34. Su SF, Chang YW, Andreu-Vieyra C, Fang JY, Yang Z, Han B, Lee AS, Liang G. miR-30d, miR-181a and miR-199a-5p cooperatively suppress the endoplasmic reticulum chaperone and signaling regulator GRP78 in cancer. Oncogene 2013;32:4694-4701.
35. Dai BH, Geng L, Wang Y, Sui CJ, Xie F, Shen RX, Shen WF, Yang JM. microRNA-199a-5p protects hepatocytes from bile acid-induced sustained endoplasmic reticulum stress. Cell Death Dis 2013;4:e604.
36. Chan YC, Roy S, Huang Y, Khanna S, Sen CK. The microRNA miR-199a-5p down-regulation switches on wound angiogenesis by derepressing the v-ets erythroblastosis virus E26 oncogene homolog 1-matrix metalloproteinase-1 pathway. J Biol Chem 2012;287: 41032-41043.
37. Tsukigi M, Bilim V, Yuuki K, Ugolkov A, Naito S, Nagaoka A, Kato T, Motoyama T, Tomita Y. Re-expression of miR-199a suppresses renal cancer cell proliferation and survival by targeting GSK-3β. Cancer Lett 2012;315:189-197.
38. Hassan T, Smith SG, Gaughan K, Oglesby IK, O'Neill S, McElvaney NG, Greene CM; CM. Isolation and identification of cell-specific microRNAs targeting a messenger RNA using a biotinylated antisense oligonucleotide capture affinity technique. Nucleic Acids Res 2013;41:e71.
39. Lujambio A, Ropero S, Ballestar E, Fraga MF, Cerrato C, Setién F, Casado S, Suarez-Gauthier A, Sanchez-Cespedes M, Git A, et al. Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Res 2007;67:1424-1429.
40. Lamy A, Sesboüé R, Bourguignon J, Dautréaux B, Métayer J, Frébourg T, Thiberville L. Aberrant methylation of the CDKN2a/p16INK4a gene promoter region in preinvasive bronchial lesions: a prospective study in high-risk patients without invasive cancer. Int J Cancer 2002;100:189-193.
41. Monick MM, Beach SR, Plume J, Sears R, Gerrard M, Brody GH, Philibert RA. Coordinated changes in AHRR methylation in lymphoblasts and pulmonary macrophages from smokers. Am J Med Genet B Neuropsychiatr Genet 2012;159B:141-151.
42. Lin RK, Hsieh YS, Lin P, Hsu HS, Chen CY, Tang YA, Lee CF, Wang YC. The tobacco-specific carcinogen NNK induces DNA methyltransferase 1 accumulation and tumor suppressor gene hypermethylation in mice and lung cancer patients. J Clin Invest 2010;120:521-532.
43. Shuangshoti S, Hourpai N, Pumsuk U, Mutirangura A. Line-1 hypomethylation in multistage carcinogenesis of the uterine cervix. Asian Pac J Cancer Prev 2007;8:307-309.
44. Tangkijvanich P, Hourpai N, Rattanatanyong P, Wisedopas N, Mahachai V, Mutirangura A. Serum LINE-1 hypomethylation as a potential prognostic marker for hepatocellular carcinoma. Clin Chim Acta 2007;379:127-133.
45. Liu F, Killian JK, Yang M, Walker RL, Hong JA, Zhang M, Davis S, Zhang Y, Hussain M, Xi S, et al. Epigenomic alterations and gene expression profiles in respiratory epithelia exposed to cigarette smoke condensate. Oncogene 2010;29:3650-3664.
46. Hsiung DT, Marsit CJ, Houseman EA, Eddy K, Furniss CS, McClean MD, Kelsey KT. Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2007;16:108-114.
47. Figueiredo JC, Grau MV, Wallace K, Levine AJ, Shen L, Hamdan R, Chen X, Bresalier RS, McKeown-Eyssen G, Haile RW, et al. Global DNA hypomethylation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol Biomarkers Prev 2009;18:1041-1049.
48. Hillemacher T, Frieling H, Moskau S, Muschler MA, Semmler A, Kornhuber J, Klockgether T, Bleich S, Linnebank M. Global DNA methylation is influenced by smoking behaviour. Eur Neuropsychopharmacol 2008;18:295-298.
49. Wangsri S, Subbalekha K, Kitkumthorn N, Mutirangura A. Patterns and possible roles of LINE-1 methylation changes in smoke-exposed epithelia. PLoS ONE 2012;7:e45292.
50. Yang YM, Liu GT. Damaging effect of cigarette smoke extract on primary cultured human umbilical vein endothelial cells and its mechanism. Biomed Environ Sci 2004;17:121-134.
51. Mizuno S, Bogaard HJ, Gomez-Arroyo J, Alhussaini A, Kraskauskas D, Cool CD, Voelkel NF. MicroRNA-199a-5p is associated with hypoxia-inducible factor-1α expression in lungs from patients with COPD. Chest 2012;142:663-672.
52. Sanfiorenzo C, Ilie MI, Belaid A, Barlési F, Mouroux J, Marquette CH, Brest P, Hofman P. Two panels of plasma microRNAs as noninvasive biomarkers for prediction of recurrence in resectable NSCLC. PLoS ONE 2013;8:e54596.
53. Lino Cardenas CL, Henaoui IS, Courcot E, Roderburg C, Cauffiez C, Aubert S, Copin MC, Wallaert B, Glowacki F, Dewaeles E, et al. miR-199a-5p Is upregulated during fibrogenic response to tissue injury and mediates TGFbeta-induced lung fibroblast activation by targeting caveolin-1. PLoS Genet 2013;9:e1003291.