Skip to main content

Advertisement

SpringerLink
Log in

Role of microRNAs in malignant mesothelioma

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Malignant mesothelioma (MM) is an aggressive tumor, mainly derived from the pleura, which is predominantly associated with exposure to asbestos fibers. The prognosis of MM patients is particularly severe, with a median survival of approximately 9–12 months and latency between exposure and diagnosis ranging from 20–50 years (median 30 years). Emerging evidence has demonstrated that tumor aggressiveness is associated with genome and gene expression abnormalities; therefore, several studies have recently focused on the role of microRNAs (miRNAs) in MM tumorigenesis. miRNAs are small non-protein coding single-stranded RNAs (17–22 nucleotides) involved in numerous cellular processes that negatively regulate gene expression by modulating the expression of downstream target genes. miRNAs are often deregulated in cancer; in particular, the differential miRNA expression profiles of MM cells compared to unaffected mesothelial cells have suggested potential roles of miRNAs as either oncogenes or tumor suppressor genes in MM oncogenesis. In this review, the mechanism of MM carcinogenesis was evaluated through the analysis of the published miRNA expression data. The roles of miRNAs as diagnostic biomarkers and prognostic factors for potential therapeutic strategies will be presented and discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

MM:

Malignant mesothelioma

ADC:

Adenocarcinoma

CEA:

Carcinoembryonic antigen

EPP:

Extrapleural pneumonectomy

P/D:

Pleurectomy/decortications

SMRP:

Soluble mesothelin-related peptides

miRNAs/miR:

MicroRNA

qRT-PCR:

Quantitative real-time polymerase chain reaction

FFPE:

Formalin-fixed paraffin-embedded

VEGF:

Vascular endothelial growth factor

NSCLC:

Non-small cell lung cancer

CDKN1:

Cyclin-dependent kinase inhibitor 1

RMP:

Reactive mesothelial proliferations

PPP6C:

Serine/threonine-protein phosphatase 6

References

  1. Wagner JC, Sleggs CA, Marchand P (1960) Diffuse pleural mesothelioma and asbestos exposure in the North Western Cape Province. Br J Ind Med 17:260–271

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Albin M, Magnani C, Krstev S, Rapiti E, Sheferl I (1999) Asbestos and cancer: an overview of current trends in Europe. Environ Health Perspect 107(Suppl 2):289–298

    Article  PubMed Central  PubMed  Google Scholar 

  3. Ismail-Khan R, Robinson LA, Williams CC Jr, Garrett CR, Bepler G, Simon GR (2006) Malignant pleural mesothelioma: a comprehensive review. Cancer Control 13:255–263

    PubMed  Google Scholar 

  4. Carbone M, Kratzke RA, Testa JR (2002) The pathogenesis of mesothelioma. Semin Oncol 29:2–17

    Article  CAS  PubMed  Google Scholar 

  5. Kaufman AJ, Pass HI (2008) Current concepts in malignant pleural mesothelioma. Expert Rev Anticancer Ther 8:293–303

    Article  CAS  PubMed  Google Scholar 

  6. Bridda A, Padoan I, Mencarelli R, Frego M (2007) Peritoneal mesothelioma: a review. MedGenMed 9:32

    PubMed Central  PubMed  Google Scholar 

  7. Husain AN, Colby T, Ordonez N, Krausz T, Attanoos R, Beasley MB, Borczuk AC, Butnor K, Cagle PT, Chirieac LR, Churg A, Dacic S, Fraire A, Galateau-Salle F, Gibbs A, Gown A, Hammar S, Litzky L, Marchevsky AM, Nicholson AG, Roggli V, Travis WD, Wick M, International Mesothelioma Interest Group (2013) Guidelines for pathologic diagnosis of malignant mesothelioma: 2012 update of the consensus statement from the International Mesothelioma Interest Group. Arch Pathol Lab Med 137:647–667

    Article  PubMed  Google Scholar 

  8. Robinson BW, Musk AW, Lake RA (2005) Malignant mesothelioma. Lancet 366:397–408

    Article  CAS  PubMed  Google Scholar 

  9. Grondin SC, Sugarbaker DJ (1999) Malignant mesothelioma of the pleural space. Oncology (Williston Park) 13:919–926 (discussion 926, 931–932)

    CAS  Google Scholar 

  10. Neumann V, Löseke S, Nowak D, Herth FJ, Tannapfel A (2013) Malignant pleural mesothelioma: incidence, etiology, diagnosis, treatment, and occupational health. Dtsch Arztebl Int 110:319–326

    PubMed Central  PubMed  Google Scholar 

  11. Bölükbas S, Schirren J (2013) Malignant pleural mesothelioma : Comparison of radical pleurectomy und extrapleural pneumonectomy. Chirurg 84:487–491

    Article  PubMed  Google Scholar 

  12. Rice D (2011) Surgical therapy of mesothelioma. Recent Results Cancer Res 189:97–125

    Article  PubMed  Google Scholar 

  13. Cao C, Tian D, Manganas C, Matthews P, Yan TD (2012) Systematic review of trimodality therapy for patients with malignant pleural mesothelioma. Ann Cardiothorac Surg 1:428–437

    PubMed Central  PubMed  Google Scholar 

  14. Kaufman AJ, Flores RM (2011) Surgical treatment of malignant pleural mesothelioma. Curr Treat Options Oncol 12:201–216

    Article  PubMed  Google Scholar 

  15. Butchart EG, Ashcroft T, Barnsley WC, Holden MP (1976) Pleuropneumonectomy in the management of diffuse malignant mesothelioma of the pleura. Experience with 29 patients. Thorax 31:15–24

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Stewart DJ, Martin-Ucar A, Pilling JE, Edwards JG, O’Byrne KJ, Waller DA (2004) The effect of extent of local resection on patterns of disease progression in malignant mesothelioma. Ann Thorac Surg 78:245–252

    Article  PubMed  Google Scholar 

  17. Treasure T, Lang-Lazdunski L, Waller D, Bliss JM, Tan C, Entwisle J, Snee M, O’Brien M, Thomas G, Senan S, O’Byrne K, Kilburn LS, Spicer J, Landau D, Edwards J, Coombes G, Darlison L, Peto J, MARS trialists (2011) Extra-pleural pneumonectomy versus no extra-pleural pneumonectomy for patients with malignant pleural mesothelioma: clinical outcomes of the Mesothelioma and Radical Surgery (MARS) randomised feasibility study. Lancet Oncol 12:763–772

    Article  PubMed Central  PubMed  Google Scholar 

  18. Soysal O, Karaoğlanoğlu N, Demiracan S, Topçu S, Taştepe I, Kaya S, Unlü M, Celtin G (1997) Pleurectomy/decortication for palliation in malignant pleural mesothelioma: results of surgery. Eur J Cardiothorac Surg 11:210–213

    Article  CAS  PubMed  Google Scholar 

  19. Vogelzang NJ, Rusthoven JJ, Symanowski J, Denham C, Kaukel E, Ruffie P, Gatzemeier U, Boyer M, Emri S, Manegold C, Niyikiza C, Paoletti P (2003) Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J Clin Oncol 21:2636–2644

    Article  CAS  PubMed  Google Scholar 

  20. van Meerbeeck JP, Gaafar R, Manegold C, Klaveren RJ, Van Marck EA, Vincent M, Legrand C, Bottomley A, Debruyne C, Giaccone G, European Organisation for Research and Treatment of Cancer Lung Cancer Group; National Cancer Institute of Canada (2005) Randomized phase III study of cisplatin with or without raltitrexed in patients with malignant pleural mesothelioma: an intergroup study of the European Organisation for Research and Treatment of Cancer Lung Cancer Group and the National Cancer Institute of Canada. J Clin Oncol 23:6881–6889

    Article  PubMed  Google Scholar 

  21. van Meerbeeck JP, Baas P, Debruyne C, Groen HJ, Manegold C, Ardizzoni A, Gridelli C, van Marck EA, Lentz M, Giaccone G (1999) A phase II study of gemcitabine in patients with malignant pleural mesothelioma. European Organization for Research and Treatment of Cancer Lung Cancer Cooperative Group. Cancer 85:2577–2582

    Article  PubMed  Google Scholar 

  22. Stebbing J, Powles T, McPherson K, Shamash J, Wells P, Sheaff MT, Slater S, Rudd RM, Fennell D, Steele JP (2009) The efficacy and safety of weekly vinorelbine in relapsed malignant pleural mesothelioma. Lung Cancer 63:94–97

    Article  PubMed  Google Scholar 

  23. Scherpereel A, Astoul P, Baas P, Berghmans T, Clayson H, de Vuyst P, Galateau-Salle F, Hennequin C, Hillerdal G, Le Péchoux C, Mutti L, Pairon JC, Stahel R, van Houtte P, van Meerbeeck J, Waller D, Weder W, European Respiratory Society/European Society of Thoracic Surgeons Task Force (2010) Guidelines of the European Respiratory Society and the European Society of Thoracic Surgeons for the management of malignant pleura mesothelioma. Eur Respir J 35:479–495

    Article  CAS  PubMed  Google Scholar 

  24. Dhalluin X, Scherpereel A (2011) Chemotherapy and radiotherapy for mesothelioma. Recent Results Cancer Res 189:127–147

    Article  CAS  PubMed  Google Scholar 

  25. Sienel W, Kirschbaum A, Passlick B (2008) Multimodal therapy for malignant pleural mesothelioma including extrapleural pneumonectomy. Zentralbl Chir 133:231–237

    Article  CAS  PubMed  Google Scholar 

  26. Sugarbaker DJ, Garcia JP, Richards WG, Harpole DH Jr, Healy-Baldini E, DeCamp MM Jr, Mentzer SJ, Liptay MJ, Strauss GM, Swanson SJ (1996) Extrapleural pneumonectomy in the multimodality therapy of malignant pleural mesothelioma. Results in 120 consecutive patients. Ann Surg 224:288–294 (discussion 294–296)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Klebe S, Henderson DW (2011) Early stages of mesothelioma, screening and biomarkers. Recent Results Cancer Res 189:169–193

    Article  CAS  PubMed  Google Scholar 

  28. Paganuzzi Onetto M, Marroni P, Filiberti R, Tassara E, Parodi S, Felletti R (2011) Diagnostic value of CYFRA 21-1 tumor marker and CEA in pleural effusion due to mesothelioma. Chest 119:1138–1142

    Article  Google Scholar 

  29. Onda M, Nagata S, Ho M, Bera TK, Hassan R, Alexander RH, Pastan I (2006) Megakaryocyte potentiation factor cleaved from mesothelin precursor is a useful tumor marker in the serum of patients with mesothelioma. Clin Cancer Res 12:4225–4423

    Article  CAS  PubMed  Google Scholar 

  30. Pass HI, Lott D, Lonardo F, Harbut M, Liu Z, Tang N, Carbone M, Webb C, Wali A (2005) Asbestos exposure, pleural mesothelioma, and serum osteopontin levels. N Engl J Med 353:1564–1573

    Article  CAS  PubMed  Google Scholar 

  31. Robinson BW, Creaney J, Lake R, Nowak A, Musk AW, de Klerk N, Winzell P, Hellstrom KE, Hellstrom I (2003) Mesothelin-family proteins and diagnosis of mesothelioma. Lancet 362:1612–1616

    Article  CAS  PubMed  Google Scholar 

  32. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  33. Esquela-Kerscher A, Slack FJ (2006) Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 6:259–269

    Article  CAS  PubMed  Google Scholar 

  34. Bentwich I (2005) Prediction and validation of microRNAs and their targets. FEBS Lett 579:5904–5910

    Article  CAS  PubMed  Google Scholar 

  35. Jean D, Daubriac J, Le Pimpec-Barthes F, Galateau-Salle F, Jaurand MC (2012) Molecular changes in mesothelioma with an impact on prognosis and treatment. Arch Pathol Lab Med 136:277–293

    Article  CAS  PubMed  Google Scholar 

  36. Rosenfeld N, Aharonov R, Meiri E, Rosenwald S, Spector Y, Zepeniuk M, Benjamin H, Shabes N, Tabak S, Levy A, Lebanony D, Goren Y, Silberschein E, Targan N, Ben-Ari A, Gilad S, Sion-Vardy N, Tobar A, Feinmesser M, Kharenko O, Nativ O, Nass D, Perelman M, Yosepovich A, Shalmon B, Polak-Charcon S, Fridman E, Avniel A, Bentwich I, Bentwich Z, Cohen D, Chajut A, Barshack I (2008) MicroRNAs accurately identify cancer tissue origin. Nat Biotechnol 26:462–469

    Article  CAS  PubMed  Google Scholar 

  37. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D, Yerushalmi N, Benjamin H, Kushnir M, Cholakh H, Melamed N, Bentwich Z, Hod M, Goren Y, Chajut A (2008) Serum microRNAs are promising novel biomarkers. PLoS One 3:e3148

    Article  PubMed Central  PubMed  Google Scholar 

  38. Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, Galas DJ, Wang K (2010) The microRNA spectrum in 12 body fluids. Clin Chem 56:1733–1741

    Article  CAS  PubMed  Google Scholar 

  39. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O’Briant KC, Allen A, Lin DW, Urban N, Drescher CW, Knudsen BS, Stirewalt DL, Gentleman R, Vessella RL, Nelson PS, Martin DB, Tewari M (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA 105:10513–10518

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, Guo J, Zhang Y, Chen J, Guo X, Li Q, Li X, Wang W, Zhang Y, Wang J, Jiang X, Xiang Y, Xu C, Zheng P, Zhang J, Li R, Zhang H, Shang X, Gong T, Ning G, Wang J, Zen K, Zhang J, Zhang CY (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18:997–1006

    Article  CAS  PubMed  Google Scholar 

  41. McDonald JS, Milosevic D, Reddi HV, Grebe SK, Algeciras-Schimnich A (2011) Analysis of circulating microRNA: preanalytical and analytical challenges. Clin Chem 57:833–840

    Article  CAS  PubMed  Google Scholar 

  42. Fabbri M (2013) MicroRNAs and cancer: towards a personalized medicine. Curr Mol Med 13:751–756

    Article  CAS  PubMed  Google Scholar 

  43. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, Croce CM (2002) Frequent deletions and down-regulation of micro-RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci USA 99:15524–15529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Heneghan HM, Miller N, Lowery AJ, Sweeney KJ, Kerin MJ (2009) MicroRNAs as novel biomarkers for breast cancer. J Oncol 2009:950201

    CAS  PubMed  Google Scholar 

  45. Roldo C, Missiaglia E, Hagan JP, Falconi M, Capelli P, Bersani S, Calin GA, Volinia S, Liu CG, Scarpa A, Croce CM (2006) MicroRNA expression abnormalities in pancreatic endocrine and acinar tumors are associated with distinctive pathologic features and clinical behavior. J Clin Oncol 24:4677–4684

    Article  CAS  PubMed  Google Scholar 

  46. Xu YZ, Xi QH, Ge WL, Zhang XQ (2013) Identification of serum microRNA-21 as a biomarker for early detection and prognosis in human epithelial ovarian cancer. Asian Pac J Cancer Prev 14:1057–1060

    Article  PubMed  Google Scholar 

  47. Raponi M, Dossey L, Jatkoe T, Wu X, Chen G, Fan H, Beer DG (2009) MicroRNA classifiers for predicting prognosis of squamous cell lung cancer. Cancer Res 69:5776–5783

    Article  CAS  PubMed  Google Scholar 

  48. Pass HI, Beer DG, Joseph S, Massion P (2013) Biomarkers and molecular testing for early detection, diagnosis, and therapeutic prediction of lung cancer. Thorac Surg Clin 23:211–224

    Article  PubMed  Google Scholar 

  49. Nadal E, Chen G, Gallegos M, Lin L, Ferrer-Torres D, Truini A, Wang Z, Lin J, Reddy RM, Llatjos R, Escobar I, Moya J, Chang AC, Cardenal F, Capella G, Beer DG (2013) Epigenetic inactivation of microRNA-34b/c predicts poor disease-free survival in early stage lung adenocarcinoma. Clin Cancer Res 19:6842–6852

    Google Scholar 

  50. Minoia C, Sturchio E, Porro B, Ficociello B, Zambelli A, Imbriani M (2011) MicroRNAs as biological indicators of environmental and occupational exposure to asbestos. G Ital Med Lav Ergon 33:420–434

    PubMed  Google Scholar 

  51. Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6:857–866

    Article  CAS  PubMed  Google Scholar 

  52. Yin JQ, Zhao RC, Morris KV (2008) Profiling microRNA expression with microarrays. Trends Biotechnol 26:70–76

    Article  CAS  PubMed  Google Scholar 

  53. Chen C, Ridzon DA, Broomer AJ, Zhou Z, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:e179

    Article  PubMed Central  PubMed  Google Scholar 

  54. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, Knuutila S (2009) CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma—a miRNA microarray analysis. Genes Chromosomes Cancer 48:615–623

    Article  CAS  PubMed  Google Scholar 

  55. Santarelli L, Strafella E, Staffolani S, Amati M, Emanuelli M, Sartini D, Pozzi V, Carbonari D, Bracci M, Pignotti E, Mazzanti P, Sabbatini A, Ranaldi R, Gasparini S, Neuzil J, Tomasetti M (2011) Association of MiR-126 with soluble mesothelin-related peptides, a marker for malignant mesothelioma. PLoS One 6:e18232

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Liu B, Peng XC, Zheng XL, Wang J, Qin YW (2009) MiR-126 restoration down-regulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo. Lung Cancer 66:169–175

    Article  PubMed  Google Scholar 

  57. Tomasetti M, Staffolani S, Nocchi L, Neuzil J, Strafella E, Manzella N, Mariotti L, Bracci M, Valentino M, Amati M, Santarelli L (2012) Clinical significance of circulating miR-126 quantification in malignant mesothelioma patients. Clin Biochem 45:575–581

    Article  CAS  PubMed  Google Scholar 

  58. Benjamin H, Lebanony D, Rosenwald S, Cohen L, Gibori H, Barabash N, Ashkenazi K, Goren E, Meiri E, Morgenstern S, Perelman M, Barshack I, Goren Y, Edmonston TB, Chajut A, Aharonov R, Bentwich Z, Rosenfeld N, Cohen D (2010) A diagnostic assay based on microRNA expression accurately identifies malignant pleural mesothelioma. J Mol Diagn 12:771–779

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Gee GV, Koestler DC, Christensen BC, Sugarbaker DJ, Ugolini D, Ivaldi GP, Resnick MB, Houseman EA, Kelsey KT, Marsit CJ (2010) Downregulated microRNAs in the differential diagnosis of malignant pleural mesothelioma. Int J Cancer 127:2859–2869

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 103:2257–2261

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Busacca S, Germano S, De Cecco L, Rinaldi M, Comoglio F, Favero F, Murer B, Mutti L, Pierotti M, Gaudino G (2010) MicroRNA signature of malignant mesothelioma with potential diagnostic and prognostic implications. Am J Respir Cell Mol Biol 42:312–319

    Article  CAS  PubMed  Google Scholar 

  62. Andersen M, Grauslund M, Muhammad-Ali M, Ravn J, Sørensen JB, Andersen CB, Santoni-Rugiu E (2012) Are differentially expressed microRNAs useful in the diagnostics of malignant pleural mesothelioma? APMIS 120:767–769

    Article  PubMed  Google Scholar 

  63. Balatti V, Maniero S, Ferracin M, Veronese A, Negrini M, Ferrocci G, Martini F, Tognon MG (2011) MicroRNAs dysregulation in human malignant pleural mesothelioma. J Thorac Oncol 6:844–851

    Article  PubMed  Google Scholar 

  64. Pass HI, Goparaju C, Ivanov S, Donington J, Carbone M, Hoshen M, Cohen D, Chajut A, Rosenwald S, Dan H, Benjamin S, Aharonov R (2010) hsa-miR-29c* is linked to the prognosis of malignant pleural mesothelioma. Cancer Res 70:1916–1924

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. Kirschner MB, Cheng YY, Badrian B, Kao SC, Creaney J, Edelman JJ, Armstrong NJ, Vallely MP, Musk AW, Robinson BW, McCaughan BC, Klebe S, Mutsaers SE, van Zandwijk N, Reid G (2012) Increased circulating miR-625-3p: a potential biomarker for patients with malignant pleural mesothelioma. J Thorac Oncol 7:1184–1191

    Article  CAS  PubMed  Google Scholar 

  66. Weber DG, Johnen G, Bryk O, Jöckel KH, Brüning T (2012) Identification of miRNA-103 in the cellular fraction of human peripheral blood as a potential biomarker for malignant mesothelioma—a pilot study. PLoS ONE 7:e30221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  67. Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, Volinia S, Guler G, Morrison CD, Chan KK, Marcucci G, Calin GA, Huebner K, Croce CM (2007) MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci USA 104:15805–15810

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Pekarsky Y, Santanam U, Cimmino A, Palamarchuk A, Efanov A, Maximov V, Volinia S, Alder H, Liu CG, Rassenti L, Calin GA, Hagan JP, Kipps T, Croce CM (2006) Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res 66:11590–11593

    Article  CAS  PubMed  Google Scholar 

  69. Gebeshuber CA, Zatloukal K, Martinez J (2009) miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 10:400–405

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  70. Ivanov SV, Miller J, Lucito R, Tang C, Ivanova AV, Pei J, Carbone M, Cruz C, Beck A, Webb C, Nonaka D, Testa JR, Pass HI (2009) Genomic events associated with progression of pleural malignant mesothelioma. Int J Cancer 124:589–599

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Ivanov SV, Goparaju CM, Lopez P, Zavadil J, Toren-Haritan G, Rosenwald S, Hoshen M, Chajut A, Cohen D, Pass HI (2010) Pro-tumorigenic effects of miR-31 loss in mesothelioma. J Biol Chem 285:22809–22817

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Kubo T, Toyooka S, Tsukuda K, Sakaguchi M, Fukazawa T, Soh J, Asano H, Ueno T, Muraoka T, Yamamoto H, Nasu Y, Kishimoto T, Pass HI, Matsui H, Huh NH, Miyoshi S (2011) Epigenetic silencing of microRNA-34b/c plays an important role in the pathogenesis of malignant pleural mesothelioma. Clin Cancer Res 17:4965–4974

    Article  CAS  PubMed  Google Scholar 

  73. Maki Y, Asano H, Toyooka S, Soh J, Kubo T, Katsui K, Ueno T, Shien K, Muraoka T, Tanaka N, Yamamoto H, Tsukuda K, Kishimoto T, Kanazawa S, Miyoshi S (2012) MicroRNA miR-34b/c enhances cellular radiosensitivity of malignant pleural mesothelioma cells. Anticancer Res 32:4871–4875

    CAS  PubMed  Google Scholar 

  74. Tanaka N, Toyooka S, Soh J, Tsukuda K, Shien K, Furukawa M, Muraoka T, Maki Y, Ueno T, Yamamoto H, Asano H, Otsuki T, Miyoshi S (2013) Downregulation of microRNA-34 induces cell proliferation and invasion of human mesothelial cells. Oncol Rep 29:2169–2174

    PubMed  Google Scholar 

  75. Muraoka T, Soh J, Toyooka S, Aoe K, Fujimoto N, Hashida S, Maki Y, Tanaka N, Shien K, Furukawa M, Yamamoto H, Asano H, Tsukuda K, Kishimoto T, Otsuki T, Miyoshi S (2013) The degree of microRNA-34b/c methylation in serum-circulating DNA is associated with malignant pleural mesothelioma. Lung Cancer [Epub ahead of print]

  76. Khodayari N, Mohammed KA, Goldberg EP, Nasreen N (2011) EphrinA1 inhibits malignant mesothelioma tumor growth via let-7 microRNA-mediated repression of the RAS oncogene. Cancer Gene Ther 18:806–816

    Article  CAS  PubMed  Google Scholar 

  77. Goparaju CM, Blasberg JD, Volinia S, Palatini J, Ivanov S, Donington JS, Croce C, Carbone M, Yang H, Pass HI (2011) ONCONASE-mediated NFKβ downregulation in malignant pleural mesothelioma. Oncogene 30:2767–2777

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, Majumder S, Liu CG, Volinia S, Croce CM, Schmittgen TD, Ghoshal K, Jacob ST (2008) Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res 68:5049–5058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Yoshino H, Chiyomaru T, Enokida H, Kawakami K, Tatarano S, Nishiyama K, Nohata N, Seki N, Nakagawa M (2011) The tumour-suppressive function of miR-1 and miR-133a targeting TAGLN2 in bladder cancer. Br J Cancer 104:808–818

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Xu Y, Zheng M, Merritt RE, Shrager JB, Wakelee H, Kratzke RA, Hoang CD (2013) miR-1 induces growth arrest and apoptosis in malignant mesothelioma. Chest 144:1632–1643

    Article  CAS  PubMed  Google Scholar 

  81. Bonci D, Coppola V, Musumeci M, Addario A, Giuffrida R, Memeo L, D’Urso L, Pagliuca A, Biffoni M, Labbaye C, Bartucci M, Muto G, Peschle C, De Maria R (2008) The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat Med 14:1271–1277

    Article  CAS  PubMed  Google Scholar 

  82. Bandi N, Zbinden S, Gugger M, Arnold M, Kocher V, Hasan L, Kappeler A, Brunner T, Vassella E (2009) miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res 69:5553–5559

    Article  CAS  PubMed  Google Scholar 

  83. Wang X, Wang J, Ma H, Zhang J, Zhou X (2012) Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med Oncol 29:919–927

    Article  CAS  PubMed  Google Scholar 

  84. Bhattacharya R, Nicoloso M, Arvizo R, Wang E, Cortez A, Rossi S, Calin GA, Mukherjee P (2009) MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer Res 69:9090–9095

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  85. Reid G, Pel ME, Kirschner MB, Cheng YY, Mugridge N, Weiss J, Williams M, Wright C, Edelman JJ, Vallely MP, McCaughan BC, Klebe S, Brahmbhatt H, Macdiarmid JA, van Zandwijk N (2013) Restoring expression of miR-16: a novel approach to therapy for malignant pleural mesothelioma. Ann Oncol 24:3128–3135

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lung Cancer Unit, IRCCS A.O.U. San Martino IST-Istituto Nazionale per la Ricerca sul Cancro, L.go Rosanna Benzi 10, 16132, Genova, Italy

    A. Truini, S. Coco, A. Alama, C. Genova, C. Sini, M. G. Dal Bello, G. Barletta, E. Rijavec, G. Burrafato & F. Grossi

  2. Medical Oncology B, IRCCS A.O.U. San Martino IST-Istituto Nazionale per la Ricerca sul Cancro, L.go Rosanna Benzi 10, 16132, Genova, Italy

    F. Boccardo

  3. Dipartimento di Medicina Interna e Specialità Mediche (DIMI), Università di Genova, V.le Benedetto XV 6, 16132, Genova, Italy

    F. Boccardo

Authors
  1. A. Truini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Coco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Alama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Genova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Sini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. G. Dal Bello
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Barletta
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. E. Rijavec
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. G. Burrafato
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. F. Boccardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. F. Grossi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Truini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Truini, A., Coco, S., Alama, A. et al. Role of microRNAs in malignant mesothelioma. Cell. Mol. Life Sci. 71, 2865–2878 (2014). https://doi.org/10.1007/s00018-014-1584-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-014-1584-5

Keywords

Search

Navigation