Whole genome analyses of a well-differentiated liposarcoma reveals novel SYT1 and DDR2 rearrangements

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Egan, Jan B ^a   Barrett, Michael T ^b   Champion, Mia D ^a,c   Middha, Sumit ^c   Lenkiewicz, Elizabeth ^b   Evers, Lisa ^b   Francis, Princy ^a   Schmidt, Jessica ^a   Shi, Chang Xin ^a   Van Wier, Scott ^a   Badar, Sandra ^a   Ahmann, Gregory ^a   Kortuem, K Martin ^a   Boczek, Nicole J ^d   Fonseca, Rafael ^a   Craig, David W ^b   Carpten, John D ^b   Borad, Mitesh J ^a   Stewart, A Keith ^a  

^a MAYO CLINIC   (United States)

^b TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^c MAYO CLINIC   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MDM2; PROTEIN TYROSINE PHOSPHATASE RECEPTOR TYPE Q; RECEPTOR PROTEIN; SYNAPTOTAGMIN I; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME 11; CHROMOSOME 12; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; DDR2 GENE; GENE; GENE AMPLIFICATION; GENE CLUSTER; GENE FUSION; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; LIPOSARCOMA; MDM2 GENE; NAV3 GENE; NUCLEOTIDE SEQUENCE; PAWR GENE; RETROPOSON; SYT1 GENE;

CHROMOSOMES, HUMAN, PAIR 11; CHROMOSOMES, HUMAN, PAIR 12; DNA, NEOPLASM; FEMALE; GENE AMPLIFICATION; GENE REARRANGEMENT; GENES, NEOPLASM; GENOME-WIDE ASSOCIATION STUDY; GENOMIC INSTABILITY; HUMANS; LIPOSARCOMA; MALE; MULTIGENE FAMILY; NEOPLASM PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, MITOGEN; SYNAPTOTAGMIN I;

EID: 84895560276     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087113     Document Type: Article

References (79)

1. Fletcher CDM, Unni KK, Mertens F (Eds.) (2002) Pathology and Genetics of Tumours of Soft Tissue and Bone. Lyon: IARC Press. 415 p.
2. Crago AM, Singer S (2011) Clinical and molecular approaches to well differentiated and dedifferentiated liposarcoma. Curr Opin Oncol 23: 373-378.
3. Hameed M (2007) Pathology and genetics of adipocytic tumors. Cytogenet Genome Res 118: 138-147.
4. Conyers R, Young S, Thomas DM (2011) Liposarcoma: molecular genetics and therapeutics. Sarcoma 2011: 483154.
5. Boland MV, Quigley HA (2011) Evaluation of a combined index of optic nerve structure and function for glaucoma diagnosis. BMC Ophthalmol 11: 6.
6. Jones RL, Fisher C, Al-Muderis O, Judson IR (2005) Differential sensitivity of liposarcoma subtypes to chemotherapy. Eur J Cancer 41: 2853-2860. (Pubitemid 41713123)
7. Laurino L, Furlanetto A, Orvieto E, Dei Tos AP (2001) Well-differentiated liposarcoma (atypical lipomatous tumors). Semin Diagn Pathol 18: 258-262. (Pubitemid 33089752)
8. Sreekantaiah C, Karakousis CP, Leong SP, Sandberg AA (1992) Cytogenetic findings in liposarcoma correlate with histopathologic subtypes. Cancer 69: 2484-2495.
9. Pedeutour F, Forus A, Coindre JM, Berner JM, Nicolo G, et al. (1999) Structure of the supernumerary ring and giant rod chromosomes in adipose tissue tumors. Genes Chromosomes Cancer 24: 30-41. (Pubitemid 28544460)
10. Dei Tos AP, Doglioni C, Piccinin S, Sciot R, Furlanetto A, et al. (2000) Coordinated expression and amplification of the MDM2, CDK4, and HMGI-C genes in atypical lipomatous tumours. J Pathol 190: 531-536. (Pubitemid 30164482)
11. Forus A, Weghuis DO, Smeets D, Fodstad O, Myklebost O, et al. (1995) Comparative genomic hybridization analysis of human sarcomas: I. Occurrence of genomic imbalances and identification of a novel major amplicon at 1q21-q22 in soft tissue sarcomas. Genes Chromosomes Cancer 14: 8-14.
12. Mandahl N, Hoglund M, Mertens F, Rydholm A, Willen H, et al. (1994) Cytogenetic aberrations in 188 benign and borderline adipose tissue tumors. Genes Chromosomes Cancer 9: 207-215. (Pubitemid 24074738)
13. Italiano A, Bianchini L, Keslair F, Bonnafous S, Cardot-Leccia N, et al. (2008) HMGA2 is the partner of MDM2 in well-differentiated and dedifferentiated liposarcomas whereas CDK4 belongs to a distinct inconsistent amplicon. Int J Cancer 122: 2233-2241. (Pubitemid 351542325)
14. Pilotti S, Della Torre G, Lavarino C, Sozzi G, Minoletti F, et al. (1998) Molecular abnormalities in liposarcoma: role of MDM2 and CDK4-containing amplicons at 12q13-22. J Pathol 185: 188-190. (Pubitemid 28270932)
15. Tap WD, Eilber FC, Ginther C, Dry SM, Reese N, et al. (2011) Evaluation of well-differentiated/de-differentiated liposarcomas by high-resolution oligonucleotide array-based comparative genomic hybridization. Genes Chromosomes Cancer 50: 95-112.
16. Italiano A, Bianchini L, Gjernes E, Keslair F, Ranchere-Vince D, et al. (2009) Clinical and biological significance of CDK4 amplification in well-differentiated and dedifferentiated liposarcomas. Clin Cancer Res 15: 5696-5703.
17. Erickson-Johnson MR, Seys AR, Roth CW, King AA, Hulshizer RL, et al. (2009) Carboxypeptidase M: a biomarker for the discrimination of well-differentiated liposarcoma from lipoma. Mod Pathol 22: 1541-1547.
18. Rubin BP, Dal Cin P (2001) The genetics of lipomatous tumors. Semin Diagn Pathol 18: 286-293. (Pubitemid 33089756)
19. Ruiz C, Lenkiewicz E, Evers L, Holley T, Robeson A, et al. (2011) Advancing a clinically relevant perspective of the clonal nature of cancer. Proc Natl Acad Sci U S A 108: 12054-12059.
20. Asmann YW, Middha S, Hossain A, Baheti S, Li Y, et al. (2011) TREAT: a bioinformatics tool for variant annotations and visualizations in targeted and exome sequencing data. Bioinformatics 28: 277-278.
21. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498.
22. Goya R, Sun MG, Morin RD, Leung G, Ha G, et al. (2010) SNVMix: predicting single nucleotide variants from next-generation sequencing of tumors. Bioinformatics 26: 730-736.
23. Kumar P, Henikoff S, Ng PC (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081.
24. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
25. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
26. Chin SF, Daigo Y, Huang HE, Iyer NG, Callagy G, et al. (2003) A simple and reliable pretreatment protocol facilitates fluorescent in situ hybridisation on tissue microarrays of paraffin wax embedded tumour samples. Mol Pathol 56: 275-279. (Pubitemid 37243919)
27. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, et al. (2002) The human genome browser at UCSC. Genome Res 12: 996-1006. (Pubitemid 34662293)
28. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 15: 403-410.
29. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
30. Jurka J, Klonowski P, Dagman V, Pelton P (1996) CENSOR - a program for identification and elimination of repetitive elements from DNA sequences. Comput Chem 20: 119-121. (Pubitemid 126405358)
31. Wheeler TJ, Clements J, Eddy SR, Hubley R, Jones TA, et al. (2013) Dfam: a database of repetitive DNA based on profile hidden Markov models. Nucleic Acids Res 41: D70-82.
32. Pickeral OK, Makałowski W, Boguski MS, Boeke JD (2000) Frequent human genomic DNA transduction driven by LINE-1 retrotransposition. Genome Res 10: 411-415.
33. Goodier JL, Ostertag EM, Kazazian HHJ (2000) Transduction of 3′-flanking sequences is common in L1 retrotransposition. Hum Mol Genet 9: 653-657. (Pubitemid 30154024)
34. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) ClustalW and ClustalX version 2. Bioinformatics 23: 2947-2948.
35. Wang L, Wang S, Li W (2012) RSeQC: quality control of RNA-seq experiments. Bioinformatics 28: 2184-2185.
36. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
37. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
38. Kim D, Salzberg SL (2011) TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 12: R72.
39. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, et al. (2011) COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 39: D945-950.
40. Haines DS (1997) The mdm2 proto-oncogene. Leuk Lymphoma 26: 227-238.
41. Willenbrock K, Kuppers R, Renne C, Brune V, Eckerle S, et al. (2006) Common features and differences in the transcriptome of large cell anaplastic lymphoma and classical Hodgkin's lymphoma. Haematologica 91: 596-604. (Pubitemid 43799453)
42. Hammerman PS, Sos ML, Ramos AH, Xu C, Dutt A, et al. (2011) Mutations in the DDR2 kinase gene identify a novel therapeutic target in squamous cell lung cancer. Cancer Discov 1: 78-89.
43. Chua HH, Yeh TH, Wang YP, Huang YT, Sheen TS, et al. (2008) Upregulation of discoidin domain receptor 2 in nasopharyngeal carcinoma. Head Neck 30: 427-436.
44. Bai Y, Li J, Fang B, Edwards A, Zhang G, et al. (2012) Phosphoproteomics identifies driver tyrosine kinases in sarcoma cell lines and tumors. Cancer Res 72: 2501-2511.
45. Lee NO, Park JW, Lee JA, Shim JH, Kong SY, et al. (2012) Dual action of a selective cyclooxygenase-2 inhibitor on vascular endothelial growth factor expression in human hepatocellular carcinoma cells: novel involvement of discoidin domain receptor 2. J Cancer Res Clin Oncol 138: 73-84.
46. Rodrigues R, Roque L, Espadinha C, Pinto A, Domingues R, et al. (2007) Comparative genomic hybridization, BRAF, RAS, RET, and oligo-array analysis in aneuploid papillary thyroid carcinomas. Oncol Rep 18: 917-926.
47. Ford CE, Lau SK, Zhu CQ, Andersson T, Tsao MS, et al. (2007) Expression and mutation analysis of the discoidin domain receptors 1 and 2 in non-small cell lung carcinoma. Br J Cancer 96: 808-814. (Pubitemid 46380188)
48. Ruiz PA, Jarai G (2012) Discoidin domain receptors regulate the migration of primary human lung fibroblasts through collagen matrices. Fibrogenesis Tissue Repair 5: 3.
49. Vogel WF, Abdulhussein R, Ford CE (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18: 1108-1116. (Pubitemid 43674043)
50. Day E, Waters B, Spiegel K, Alnadaf T, Manley PW, et al. (2008) Inhibition of collagen-induced discoidin domain receptor 1 and 2 activation by imatinib, nilotinib and dasatinib. Eur J Pharmacol 599: 44-53.
51. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561-568.
52. Kanehisa MaG, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28: 27-30.
53. Keppler OT, Hinderlich S, Langner J, Schwartz-Albiez R, Reutter W, et al. (1999) UDP-GlcNAc 2-epimerase: a regulator of cell surface sialylation. Science 284: 1372-1376. (Pubitemid 29289666)
54. Szak ST, Pickeral OK, Landsman D, Boeke JD (2003) Identifying related L1 retrotransposons by analyzing 39 transduced sequences. Genome Biol 4: R30.
55. Pfeiffer MJ, Smit FP, Sedelaar JP, Schalken JA (2011) Steroidogenic enzymes and stem cell markers are upregulated during androgen deprivation in prostate cancer. Mol Med 17: 657-664.
56. Solyom S, Ewing AD, Rahrmann EP, Doucet T, Nelson HH, et al. (2012) Extensive somatic L1 retrotransposition in colorectal tumors. Genome Res 22: 2328-2338.
57. Wei W, Gilbert N, Ooi SL, Lawler JF, Ostertag EM, et al. (2001) Human L1 retrotransposition: cis preference versus trans complementation. Mol Cell Biol 21: 1429-1439. (Pubitemid 32114989)
58. Aksoy O, Chicas A, Zeng T, Zhao Z, McCurrach M, et al. (2012) The atypical E2F family member E2F7 couples the p53 and RB pathways during cellular senescence. Genes Dev 26: 1546-1557.
59. Carvajal LA, Hamard PJ, Tonnessen C, Manfredi JJ (2012) E2F7, a novel target, is up-regulated by p53 and mediates DNA damage-dependent transcriptional repression. Genes Dev 26: 1533-1545.
60. Jung H, Kim WK, Kim do H, Cho YS, Kim SJ, et al. (2009) Involvement of PTP-RQ in differentiation during adipogenesis of human mesenchymal stem cells. Biochem Biophys Res Commun 383: 252-257.
61. Koso H, Takeda H, Yew CC, Ward JM, Nariai N, et al. (2012) Transposon mutagenesis identifies genes that transform neural stem cells into gliomainitiating cells. Proc Natl Acad Sci USA 109: E2998-3007.
62. Kool J, Berns A (2009) High-throughput insertional mutagenesis screens in mice to identify oncogenic networks. Nat Rev Cancer 9: 389-399.
63. Peng PD, Cohen CJ, Yang S, al e (2009) Efficient nonviral Sleeping Beauty transposon based TCR gene transfer to peripheral blood lymphocytes confers antigen-specific antitumor reactivity. Gene Ther 16: 1042-1049.
64. Jin Z, Maiti S, Huls H, al e (2011) Comparative genomic integration profiling of Sleeping Beauty transposons mobilized with high efficacy from integrase-defective Lentiviral vectors in primary human cells. Mol Ther 19: 1499-1510.
65. Jones RB, Garrison KE, Wong JC, Duan EH, Nixon DF, et al. (2008) Nucleoside analogue reverse transcriptase inhibitors differentially inhibit human LINE-1 retrotransposition. PloS one 3: e1547.
66. Carlini F, Ridolfi B, Molinari A, Parisi C, Bozzuto G, et al. (2010) The reverse transcription inhibitor abacavir shows anticancer activity in prostate cancer cell lines. PloS one 5: e14221.
67. Panagopoulos I, Mandahl N, Mitelman F, Aman P (1995) Two distinct FUS breakpoint clusters in myxoid liposarcoma and acute myeloid leukemia with the translocations t(12;16) and t(16;21). Oncogene 11: 1133-1137.
68. Crozat A, Aman P, Mandahl N, Ron D (1993) Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature 363: 640-644. (Pubitemid 23227627)
69. Ichikawa H, Shimizu K, Hayashi Y, Ohki M (1994) An RNA-binding protein gene, TLS/FUS, is fused to ERG in human myeloid leukemia with t(16;21) chromosomal translocation. Cancer Res 54: 2865-2868. (Pubitemid 24187764)
70. Rabbitts TH, Forster A, Larson R, Nathan P (1994) Chromosomal translocations in human cancer. Nature 372: 143-149. (Pubitemid 24347832)
71. Shimizu K, Ichikawa H, Tojo A, Kaneko Yea (1993) An ets-related gene, ERG, is rearranged in human myeloid leukemia with t(16;21) chromosomal translocation. Proc Natl Acad Sci USA 90: 10280-10284. (Pubitemid 23328296)
72. Kathir KM, Gao L, Rajalingam D, Daily AE, Brixey S, et al. (2010) NMR characterization of copper and lipid interactions of the C2B domain of synaptotagmin I-relevance to the non-classical secretion of the human acidic fibroblast growth factor (hFGF-1). Biochim Biophys Acta 1798: 297-302.
73. Alves F, Vogel W, Mossie K, Millauer B, Hofler H, et al. (1995) Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10: 609-618.
74. Badiola I, Villace P, Basaldua I, Olaso E (2011) Downregulation of discoidin domain receptor 2 in A375 human melanoma cells reduces its experimental liver metastasis ability. Oncol Rep 26: 971-978.
75. Olaso E, Ikeda K, Eng FJ, Xu L, Wang LH, et al. (2001) DDR2 receptor promotes MMP-2-mediated proliferation and invasion by hepatic stellate cells. J Clin Invest 108: 1369-1378. (Pubitemid 33107765)
76. Olaso E, Labrador JP, Wang L, Ikeda K, Eng FJ, et al. (2002) Discoidin domain receptor 2 regulates fibroblast proliferation and migration through the extracellular matrix in association with transcriptional activation of matrix metalloproteinase-2. J Biol Chem 277: 3606-3613. (Pubitemid 34953233)
77. Badiola I, Olaso E, Crende O, Friedman SL, Vidal-Vanaclocha F (2011) Discoidin domain receptor 2 deficiency predisposes hepatic tissue to colon carcinoma metastasis. Gut 61: 1465-1472.
78. Maeyama M, Koga H, Selvendiran K, Yanagimoto C, Hanada S, et al. (2008) Switching in discoid domain receptor expressions in SLUG-induced epithelial-mesenchymal transition. Cancer 113: 2823-2831.
79. Pitini V, Arrigo C, Di Mirto C, Mondello P, Altavilla G (2013) Response to dasatinib in a patient with SQCC of the lung harboring a discoid-receptor-2 and synchronous chronic myelogenous leukemia. Lung Cancer 82: 171-172.