Molecular classification of malignant pleural mesothelioma: Identification of a poor prognosis subgroup linked to the epithelial-to-mesenchymal transition

Clinical Cancer Research

Volumn 20, Issue 5, 2014, Pages 1323-1334

  De Reynies, Aurelien ^a   Jaurand, Marie Claude ^b,c   Renier, Annie ^b,c   Couchy, Gabrielle ^b,c   Hysi, Ilir ^f   Elarouci, Nabila ^a   Galateau Sallé, Francoise ^h,i   Copin, Marie Christine ^g   Hofman, Paul ^j   Cazes, Aurelie ^d   Andujar, Pascal ^k,l   Imbeaud, Sandrine ^b,c   Petel, Fabien ^a   Pairon, Jean Claude ^k,l   Le Pimpec Barthes, Francoise ^b,c,e   Zucman Rossi, Jessica ^b,c   Jean, Didier ^b,c  

^a Ligue Nationale Contre le Cancer Programme Cartes d'Identité des Tumeurs CIT   (France)

^b Université Paris 13   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d AP HP GHU Ouest Laboratoire d'Anatomie Pathologique   (France)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^f LILLE UNIVERSITY HOSPITAL   (France)

^g UNIV LILLE   (France)

^h CAEN UNIVERSITY HOSPITAL   (France)

ⁱ Axe 2: 'Biology and Innovative Therapeutics for Locally Aggressive Cancers'   (France)

^j PASTEUR HOSPITAL   (France)

^k CENTRE HOSPITALIER INTERCOMMUNAL DE CRÉTEIL   (France)

^l INSERM U955   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; RNA;

ADULT; AGED; ARTICLE; BAP1 GENE; CANCER CELL CULTURE; CANCER CLASSIFICATION; CANCER SURVIVAL; CDKN2A GENE; CDKN2B GENE; CONTROLLED STUDY; DNA EXTRACTION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE MUTATION; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; NF2 GENE; NUCLEOTIDE SEQUENCE; PLEURA MESOTHELIOMA; PRIORITY JOURNAL; PROGNOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; TP53 GENE; TUMOR GENE; VERY ELDERLY;

AGED; CLUSTER ANALYSIS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; HUMANS; LUNG NEOPLASMS; MALE; MESOTHELIOMA; MIDDLE AGED; MUTATION; NEOPLASM STAGING; PLEURAL NEOPLASMS; PROGNOSIS; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN THIOLESTERASE;

EID: 84895808711     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2429     Document Type: Article

References (58)

1. Huang SX, Jaurand MC, Kamp DW, Whysner J, Hei TK. Role of mutagenicity in asbestos fiber-induced carcinogenicity and other diseases. J Toxicol Environ Health B Crit Rev 2011;14:179-245.
2. Scherpereel A, Astoul P, Baas P, Berghmans T, Clayson H, de Vuyst P, et al. Guidelines of the European Respiratory Society and the European Society of Thoracic Surgeons for the management of malignant pleural mesothelioma. Eur Respir J 2010;35:479-95.
3. Musti M, Kettunen E, Dragonieri S, Lindholm P, Cavone D, Serio G, et al. Cytogenetic and molecular genetic changes in malignant mesothelioma. Cancer Genet Cytogenet 2006;170:9-15.
4. Lindholm PM, Salmenkivi K, Vauhkonen H, Nicholson AG, Anttila S, Kinnula VL, et al. Gene copy number analysis in malignant pleural mesothelioma using oligonucleotide array CGH. Cytogenet Genome Res 2007;119:46-52.
5. Taniguchi T, Karnan S, Fukui T, Yokoyama T, Tagawa H, Yokoi K, et al. Genomic profiling of malignant pleural mesothelioma with array-based comparative genomic hybridization shows frequent non-randomchromosomal alteration regions including JUN amplification on 1p32. Cancer Sci 2007;98:438-46.
6. Jean D, Daubriac J, Le Pimpec-Barthes F, Galateau-Salle F, Jaurand MC. Molecular changes in mesothelioma with an impact on prognosis and treatment. Arch Pathol Lab Med 2012;136:277-93.
7. Jean D, Thomas E, Manie E, Renier A, de Reynies A, Lecomte C, et al. Syntenic relationships between genomic profiles of fiber-induced murine and human malignant mesothelioma. Am J Pathol 2011;178: 881-94.
8. Kindler HL, Karrison TG, Gandara DR, Lu C, Krug LM, Stevenson JP, et al. Multicenter, double-blind, placebo-controlled, randomized phase II trial of gemcitabine/cisplatin plus bevacizumab or placebo in patients with malignant mesothelioma. J Clin Oncol 2012;30: 2509-15.
9. Bertino P, Carbone M, Pass H. Chemotherapy of malignant pleural mesothelioma. Expert Opin Pharmacother 2009;10:99-107.
10. Betta PG, Magnani C, Bensi T, Trincheri NF, Orecchia S. Immunohistochemistry and molecular diagnostics of pleural malignant mesothelioma. Arch Pathol Lab Med 2012;136:253-61.
11. Husain AN, Colby T,OrdonezN, Krausz T, Attanoos R, Beasley MB, et al. Guidelines for pathologic diagnosis of malignant mesothelioma: 2012 update of the consensus statement from the International Mesothelioma Interest Group. Arch Pathol Lab Med 2012; 137:647-67.
12. Goto Y, Shinjo K, Kondo Y, Shen L, Toyota M, Suzuki H, et al. Epigenetic profiles distinguish malignant pleural mesothelioma from lung adenocarcinoma. Cancer Res 2009;69:9073-82.
13. Christensen BC, Houseman EA, Godleski JJ, Marsit CJ, Longacker JL, Roelofs CR, et al. Epigenetic profiles distinguish pleural mesothelioma from normal pleura and predict lung asbestos burden and clinical outcome. Cancer Res 2009;69:227-34.
14. Gordon GJ, Rockwell GN, Jensen RV, Rheinwald JG, Glickman JN, Aronson JP, et al. Identification of novel candidate oncogenes and tumor suppressors in malignant pleural mesothelioma using large-scale transcriptional profiling. Am J Pathol 2005;166: 1827-40.
15. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, et al. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma-a miRNA microarray analysis. Genes Chromosomes Cancer 2009;48:615-23.
16. Xu Y, Zheng M, Merritt RE, Shrager JB, Wakelee H, Kratzke RA, et al. miR-1 induces growth arrest and apoptosis in malignant mesothelioma. Chest 2013;144:1632-43.
17. Husain AN, Colby TV, Ordonez NG, Krausz T, Borczuk A, Cagle PT, et al. Guidelines for pathologic diagnosis of malignant mesothelioma: a consensus statement from the International Mesothelioma Interest Group. Arch Pathol Lab Med 2009;133:1317-31.
18. Zeng L, Fleury-Feith J, Monnet I, Boutin C, Bignon J, Jaurand MC. Immunocytochemical characterization of cell lines from human malignant mesothelioma: characterization of human mesothelioma cell lines by immunocytochemistry with a panel of monoclonal antibodies. Hum Pathol 1994;25:227-34.
19. Zeng L, Buard A, Monnet I, Boutin C, Fleury J, Saint-Etienne L, et al. In vitro effects of recombinant human interferon g on human mesothelioma cell lines. Int J Cancer 1993;55:515-20.
20. Bott M, Brevet M, Taylor BS, Shimizu S, Ito T,Wang L, et al. The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma. Nat Genet 2011; 43:668-72.
21. Andujar P, Wang J, Descatha A, Galateau-Salle F, Abd-Alsamad I, Billon-Galland MA, et al. p16INK4A inactivation mechanisms in nonsmall-cell lung cancer patients occupationally exposed to asbestos. Lung Cancer 2010;67:23-30.
22. Andujar P, Pairon JC, Renier A, Descatha A, Hysi I, Abd-Alsamad I, et al. Differential mutation profiles and similar intronic TP53 polymorphisms in asbestos-related lung cancer and pleural mesothelioma. Mutagenesis 2013;28:323-31.
23. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003;31:e15.
24. Cairo S, Armengol C, De Reynies A, Wei Y, Thomas E, Renard CA, et al. Hepatic stem-like phenotype and interplay of Wnt/b-catenin and Myc signaling in aggressive childhood liver cancer. Cancer Cell 2008;14: 471-84.
25. Tibshirani R, Hastie T, Narasimhan B, Chu G. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci U S A 2002;99:6567-72.
26. Efron B, Tibshirani R. Empirical Bayes methods and false discovery rates for microarrays. Genet Epidemiol 2002;23:70-86.
27. Goeman JJ, van de Geer SA, de Kort F, van Houwelingen HC. A global test for groups of genes: testing association with a clinical outcome. Bioinformatics 2004;20:93-9.
28. Dinu I, Potter JD, Mueller T, Liu Q, Adewale AJ, Jhangri GS, et al. Improving gene set analysis of microarray data by SAM-GS. BMC Bioinform 2007;8:242.
29. Goeman JJ, Buhlmann P. Analyzing gene expression data in terms of gene sets: methodological issues. Bioinformatics 2007;23:980-7.
30. Levallet G, Vaisse-Lesteven M, Le Stang N, Ilg AG, Brochard P, Astoul P, et al. Plasma cell membrane localization of c-MET predicts longer survival in patients with malignant mesothelioma: a series of 157 cases from the MESOPATH Group. J Thorac Oncol 2012;7:599-606.
31. Zavadil J, Bottinger EP. TGF-b and epithelial-to-mesenchymal transitions. Oncogene 2005;24:5764-74.
32. Thiery JP, Sleeman JP. Complex networks orchestrate epithelialmesenchymal transitions. Nat Rev Mol Cell Biol 2006;7:131-42.
33. Zeisberg M, Neilson EG. Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 2009;119:1429-37.
34. Taube JH, Herschkowitz JI, Komurov K, Zhou AY, Gupta S, Yang J, et al. Core epithelial-to-mesenchymal transition interactome geneexpression signature is associated with claudin-low and metaplastic breast cancer subtypes. Proc Natl Acad SciUS A2010;107:15449-54.
35. Dhalluin X, Scherpereel A. Treatment of malignant pleural mesothelioma: current status and future directions. Monaldi Arch Chest Dis 2010;73:79-85.
36. Greillier L, Marco S, Barlesi F. Targeted therapies in malignant pleural mesothelioma: a review of clinical studies. Anticancer Drugs 2011;22: 199-205.
37. Jakobsen JN, Sorensen JB. Review on clinical trials of targeted treatments in malignant mesothelioma. Cancer Chemother Pharmacol 2011;68:1-15.
38. Hoang CD, D'Cunha J, Kratzke MG, Casmey CE, Frizelle SP, Maddaus MA, et al. Gene expression profiling identifies matriptase overexpression in malignant mesothelioma. Chest 2004;125:1843-52.
39. Gueugnon F, Leclercq S, Blanquart C, Sagan C, Cellerin L, Padieu M, et al. Identification of novel markers for the diagnosis of malignant pleural mesothelioma. Am J Pathol 2011;178:1033-42.
40. Lopez-Rios F, Chuai S, Flores R, Shimizu S, Ohno T, Wakahara K, et al. Global gene expression profiling of pleural mesotheliomas: overexpression of aurora kinases and P16/CDKN2A deletion as prognostic factors and critical evaluation of microarray-based prognostic prediction. Cancer Res 2006;66:2970-9.
41. Kanamori-Katayama M, Kaiho A, Ishizu Y, Okamura-Oho Y, Hino O, Abe M, et al. LRRN4 and UPK3B are markers of primary mesothelial cells. PLoS ONE 2011;6:e25391.
42. Idell S, Pueblitz S, Emri S, Gungen Y, Gray L, Kumar A, et al. Regulation of fibrin deposition by malignant mesothelioma.AmJ Pathol 1995;147: 1318-29.
43. Mutsaers SE, Prele CM, Brody AR, Idell S. Pathogenesis of pleural fibrosis. Respirology 2004;9:428-40.
44. Pass HI, Liu Z, Wali A, Bueno R, Land S, Lott D, et al. Gene expression profiles predict survival and progression of pleural mesothelioma. Clin Cancer Res 2004;10:849-59.
45. Gordon GJ, Jensen RV, Hsiao LL, Gullans SR, Blumenstock JE, Richards WG, et al. Using gene expression ratios to predict outcome among patients with mesothelioma. J Natl Cancer Inst 2003;95: 598-605.
46. Gordon GJ, Rockwell GN, Godfrey PA, Jensen RV, Glickman JN, Yeap BY, et al. Validation of genomics-based prognostic tests in malignant pleural mesothelioma. Clin Cancer Res 2005;11:4406-14.
47. Gordon GJ, Dong L, Yeap BY, RichardsWG,Glickman JN, Edenfield H, et al. Four-gene expression ratio test for survival in patients undergoing surgery for mesothelioma. J Natl Cancer Inst 2009;101:678-86.
48. Testa JR, Cheung M, Pei J, Below JE, Tan Y, Sementino E, et al. Germline BAP1 mutations predispose to malignant mesothelioma. Nat Genet 2011;43:1022-5.
49. Kapur P, Pena-Llopis S, Christie A, Zhrebker L, Pavia-Jimenez A, Rathmell WK, et al. Effects on survival of BAP1 and PBRM1 mutations in sporadic clear-cell renal-cell carcinoma: a retrospective analysis with independent validation. Lancet Oncol 2013;14:159-67.
50. Harbour JW, Onken MD, Roberson ED, Duan S, Cao L, Worley LA, et al. Frequent mutation of BAP1 in metastasizing uveal melanomas. Science 2010;330:1410-3.
51. Zauderer MG, Bott M, McMillan R, Sima CS, Rusch V, Krug LM, et al. Clinical characteristics of patients with malignant pleural mesothelioma harboring somatic BAP1 mutations. J Thorac Oncol 2013;8:1430-3.
52. Abutaily AS, Addis BJ, RocheWR. Immunohistochemistry in the distinction between malignant mesothelioma and pulmonary adenocarcinoma: a critical evaluation of new antibodies. J Clin Pathol 2002;55:662-8.
53. Fassina A, Cappellesso R, Guzzardo V, Dalla Via L, Piccolo S, Ventura L, et al. Epithelial-mesenchymal transition in malignant mesothelioma. Mod Pathol 2012;25:86-99.
54. Merikallio H, Paakko P, Salmenkivi K, Kinnula V, Harju T, Soini Y. Expression of snail, twist, and Zeb1 in malignant mesothelioma. APMIS 2013;121:1-10.
55. Schramm A, Opitz I, Thies S, Seifert B, Moch H, Weder W, et al. Prognostic significance of epithelial-mesenchymal transition in malignant pleural mesothelioma. Eur J Cardiothorac Surg 2010;37:566-72.
56. Wendt MK, Tian M, Schiemann WP. Deconstructing the mechanisms and consequences of TGF-b-induced EMT during cancer progression. Cell Tissue Res 2012;347:85-101.
57. Akhurst RJ, Hata A. Targeting the TGF-b signalling pathway in disease. Nat Rev Drug Discov 2012;11:790-811.
58. Lamouille S, Subramanyam D, Blelloch R, Derynck R. Regulation of epithelial-mesenchymal and mesenchymal-epithelial transitions by microRNAs. Curr Opin Cell Biol 2013;25:200-7.