Tumor suppressor alterations cooperate to drive aggressive mesotheliomas with enriched cancer stem cells via a p53-miR-34a-c-met axis

Cancer Research

Volumn 74, Issue 4, 2014, Pages 1261-1271

  Menges, Craig W ^a   Kadariya, Yuwaraj ^a   Altomare, Deborah ^b   Talarchek, Jacqueline ^a   Neumann Domer, Erin ^a   Wu, Yue ^a,d   Xiao, Guang Hui ^d   Shapiro, Irina M ^c   Kolev, Vihren N ^c   Pachter, Jonathan A ^c   Klein Szanto, Andres J ^a   Testa, Joseph R ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

^c Verastem Oncology Chief Medical Officer   (United States)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ASBESTOS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENES, NEUROFIBROMATOSIS 2; GENES, P53; GENES, TUMOR SUPPRESSOR; MESOTHELIOMA; MICE; MICE, SCID; MICE, TRANSGENIC; MICRORNAS; MUTATION; NEOPLASM INVASIVENESS; NEOPLASTIC STEM CELLS; PLEURAL NEOPLASMS; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84894263067     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2062     Document Type: Article

References (41)

1. Finn RS, Brims FJ, Gandhi A, Olsen N, Musk AW, Maskell NA, et al. Postmortem findings of malignant pleural mesothelioma: a two-center study of 318 patients. Chest 2012;142:1267-73.
2. Bianchi AB, Mitsunaga SI, Cheng JQ, Klein WM, Jhanwar SC, Sei-zinger B, et al. High frequency of inactivating mutations in the neuro-fibromatosis type 2 gene (NF2) in primary malignant mesotheliomas. Proc Natl Acad Sci USA 1995;92:10854-8.
3. Cheng JQ, Jhanwar SC, Klein WM, Bell DW, Lee WC, Altomare DA, et al. p16 alterations and deletion mapping of 9p21-p22 in malignant mesothelioma. Cancer Res 1994;54:5547-51.
4. Ladanyi M, Zauderer MG, Krug LM, Ito T, McMillan R, Bott M, etal. New strategies in pleural mesothelioma: BAP1 and NF2 as novel targets for therapeutic development and risk assessment. Clin Cancer Res 2012;18:4485-90.
5. Altomare DA, Vaslet CA, Skele KL, De Rienzo A, Devarajan K, Jhanwar SC, et al. A mouse model recapitulating molecular features of human mesothelioma. Cancer Res 2005;65:8090-5.
6. Sherr CJ. The INK4a/ARF network in tumour suppression. Nat Rev Mol Cell Biol 2001;2:731-7.
7. Altomare DA, Menges CW, Xu J, Pei J, Zhang L, Tadevosyan A, et al. Losses of both products of the Cdkn2a/Arf locus contribute to asbestos-induced mesothelioma development and cooperate to accelerate tumorigenesis. PLoS ONE 2011;6:e18828.
8. 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.
9. Menges CW, Chen Y, Mossman BT, Chernoff J, Yeung AT, Testa JR. A phosphotyrosine proteomic screen identifies multiple tyrosine kinase signaling pathways aberrantly activated in malignant mesothelioma. Genes Cancer 2010;1:493-505.
10. van der Bij S, Koffijberg H, Burgers JA, Baas P, van de Vijver MJ, de Mol BA, et al. Prognosis and prognostic factors of patients with mesothelioma: a population-based study. Br J Cancer 2012; 107:161-4.
11. De Bacco F, Casanova E, Medico E, Pellegatta S, Orzan F, Albano R, et al. The MET oncogene is a functional marker of a glioblastoma stem cell subtype. Cancer Res 2012;72:4537-50.
12. Joo KM, Jin J, Kim E, Ho Kim K, Kim Y, Gu Kang B, et al. MET signaling regulates glioblastoma stem cells. Cancer Res 2012;72: 3828-38.
13. Li Y, Li A, Glas M, Lal B, Ying M, Sang Y, et al. c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Natl Acad Sci USA 2011;108:9951-6.
14. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA. Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 2010;148:3-15.
15. Ghani FI, Yamazaki H, Iwata S, Okamoto T, Aoe K, Okabe K, et al. Identification of cancer stem cell markers in human malignant meso-thelioma cells. Biochem Biophys Res Commun 2011;404:735-42.
16. Cortes-Dericks L, Carboni GL, Schmid RA, Karoubi G. Putative cancer stem cells in malignant pleural mesothelioma show resistance to cisplatin and pemetrexed. Int J Oncol 2010;37:437-44.
17. Kim KU, Wilson SM, Abayasiriwardana KS, Collins R, Fjellbirkeland L, Xu Z, et al. A novel in vitro model of human mesothelioma for studying tumor biology and apoptotic resistance. Am J Respir Cell Mol Biol 2005;33:541-8.
18. Morrison R, Schleicher SM, Sun Y, Niermann KJ, Kim S, Spratt DE, et al. Targeting the mechanisms of resistance to chemotherapy and radiotherapy with the cancer stem cell hypothesis. J Oncol 2011; 2011:941876.
19. Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, et al. Association of breast cancer stem cells identified by aldehyde dehy-drogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 2009;15:4234-41.
20. Varghese S, Whipple R, Martin SS, Alexander HR. Multipotent cancer stem cells derived from human malignant peritoneal mesothelioma promote tumorigenesis. PLoS ONE 2012;7:e52825.
21. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B, et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010;16:45-55.
22. Goudar RK. Review of pemetrexed in combination with cisplatin for the treatment of malignant pleural mesothelioma. Ther Clin Risk Manag 2008;4:205-11.
23. Lohberger B, Rinner B, Stuendl N, Absenger M, Liegl-Atzwanger B, Walzer SM, et al. Aldehyde dehydrogenase 1, a potential marker for cancer stem cells in human sarcoma. PLoS ONE 2012;7:e43664.
24. Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, et al. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res 2008;14: 4085-95.
25. Jagadeeswaran R, Ma PC, Seiwert TY, Jagadeeswaran S, Zumba O, Nallasura V, et al. Functional analysis of c-Met/hepatocyte growth factor pathway in malignant pleural mesothelioma. Cancer Res 2006; 66:352-61.
26. Posadas EM, Figlin RA. Understanding the role of MET kinase in cancer therapy. J Clin Oncol 2013;31:169-70.
27. Wong MY, Yu Y, Walsh WR, Yang JL. microRNA-34 family and treatment of cancers with mutant or wild-type p53 (Review). Int J Oncol 2011;38:1189-95.
28. Nguyen DX. Tracing the origins of metastasis. J Pathol 2011;223: 195-204.
29. Buchanan SG, Hendle J, Lee PS, Smith CR, Bounaud PY, Jessen KA, et al. SGX523 is an exquisitely selective, ATP-competitive inhibitor of the MET receptor tyrosine kinase with antitumor activity in vivo. Mol Cancer Ther 2009;8:3181-90.
30. Jongsma J, van Montfort E, Vooijs M, Zevenhoven J, Krimpenfort P, van der Valk M, et al. A conditional mouse model for malignant mesothelioma. Cancer Cell 2008;13:261-71.
31. Taguchi T, Jhanwar SC, Siegfried JM, Keller SM, Testa JR. Recurrent deletions of specific chromosomal sites in 1p, 3p, 6q, and 9p in human malignant mesothelioma. Cancer Res 1993;53:4349-55.
32. 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.
33. Yoshikawa Y, Sato A, Tsujimura T, Emi M, Morinaga T, Fukuoka K, et al. Frequent inactivation of the BAP1 gene in epithelioid-type malignant mesothelioma. Cancer Sci 2012;103:868-74.
34. Mukohara T, Civiello G, Davis IJ, Taffaro ML, Christensen J, Fisher DE, et al. Inhibition of the met receptor in mesothelioma. Clin Cancer Res 2005;11:8122-30.
35. Tolnay E, Kuhnen C, Wiethege T, Konig JE, Voss B, Muller KM. Hepatocyte growth factor/scatter factor and its receptor c-Met are overexpressed and associated with an increased microvessel density in malignant pleural mesothelioma. J Cancer Res Clin Oncol 1998; 124:291-6.
36. Hwang CI, Matoso A, Corney DC, Flesken-Nikitin A, Korner S, Wang W, et al. Wild-type p53 controls cell motility and invasion by dual regulation of MET expression. Proc Natl Acad Sci USA 2011; 108:14240-5.
37. 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.
38. Kubo T, Toyooka S, Tsukuda K, Sakaguchi M, Fukazawa T, Soh J, et al. Epigenetic silencing of microRNA-34b/c plays an important role in the pathogenesis of malignant pleural mesothelioma. Clin Cancer Res 2011;17:4965-74.
39. Tanaka N, Toyooka S, Soh J, Tsukuda K, Shien K, Furukawa M, et al. Downregulation of microRNA-34 induces cell proliferation and invasion of human mesothelial cells. Oncol Rep 2013;29: 2169-74.
40. 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.
41. Christensen BC, Godleski JJ, Marsit CJ, Houseman EA, Lopez-Fagundo CY, Longacker JL, et al. Asbestos exposure predicts cell cycle control gene promoter methylation in pleural mesothelioma. Carcinogenesis 2008;29:1555-9.