TERT promoter hotspot mutations are recurrent in myxoid liposarcomas but rare in other soft tissue sarcoma entities

Journal of Experimental and Clinical Cancer Research

Volumn 33, Issue 1, 2014, Pages

  Koelsche, Christian ^a,b   Renner, Marcus ^a   Hartmann, Wolfgang ^c   Brandt, Regine ^a   Lehner, Burkhard ^a   Waldburger, Nina ^a   Alldinger, Ingo ^a   Schmitt, Thomas ^a   Egerer, Gerlinde ^a   Penzel, Roland ^a   Wardelmann, Eva ^c   Schirmacher, Peter ^a   Von Deimling, Andreas ^a,b   Mechtersheimer, Gunhild ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

Mutation; Myxoid liposarcoma; Promoter; Sarcoma; Soft tissue; Solitary fibrous tumor; TERT

Indexed keywords

TELOMERASE REVERSE TRANSCRIPTASE;

ALVEOLAR SOFT PART SARCOMA; ALVEOLAR SOFT PART TUMOR; ANGIOSARCOMA; ARTICLE; CANCER RECURRENCE; CLEAR CELL SARCOMA; DEDIFFERENTIATED LIPOSARCOMA; DERMATOFIBROSARCOMA PROTUBERANS; EPITHELIOID SARCOMA; EXTRASKELETAL MYXOID CHONDROSARCOMA; FEMALE; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; LEIOMYOSARCOMA; LIPOSARCOMA; LOW GRADE FIBROMYXOID SARCOMA; MAJOR CLINICAL STUDY; MALE; MALIGNANT PERIPHERAL NERVE SHEATH TUMOR; MYXOFIBROSARCOMA; MYXOSARCOMA; PHENOTYPE; PLEOMORPHIC LIPOSARCOMA; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; PROMOTER REGION; SARCOMA CELL; SOFT TISSUE SARCOMA; SOLITARY FIBROUS TUMOR; SYNOVIAL SARCOMA; UNDIFFERENTIATED PLEOMORPHIC SARCOMA;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; BASE SEQUENCE; FEMALE; GENETIC ASSOCIATION STUDIES; HUMANS; LIPOSARCOMA, MYXOID; MALE; MIDDLE AGED; POINT MUTATION; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; SOFT TISSUE NEOPLASMS; TELOMERASE; TELOMERE HOMEOSTASIS; YOUNG ADULT;

EID: 84899506710     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-33-33     Document Type: Article

References (53)

1. Fletcher CDM, Bridge JA, Hogendoorn PCW, Mertens F, WHO Classification of Tumours of Soft Tissue and Bone Lyon: IARC Press 2013
2. General Considerations. Goldblum JR, Folpe AL, Weiss SW, In Enzinger and Weiss's Soft Tissue Tumors City: Mosby, Enzinger and Weiss's Soft Tissue Tumors, 6 Book General Considerations. 2013 1 10
3. Completely resected recurrent soft tissue sarcoma: primary anatomic site governs outcomes. Stojadinovic A, Yeh A, Brennan MF, J Am Coll Surg 2002 194 436 447 10.1016/S1072-7515(02)01120-1 11949749 (Pubitemid 34274840)
4. Advances in sarcoma genomics and new therapeutic targets. Taylor BS, Barretina J, Maki RG, Antonescu CR, Singer S, Ladanyi M, Nat Rev Cancer 2011 11 541 557 10.1038/nrc3087 21753790
5. Integrative DNA methylation and gene expression analysis in high-grade soft tissue sarcomas. Renner M, Wolf T, Meyer H, Hartmann W, Penzel R, Ulrich A, Lehner B, Hovestadt V, Czwan E, Egerer G, Schmitt T, Alldinger I, Renker EK, Ehemann V, Eils R, Wardelmann E, Buttner R, Lichter P, Brors B, Schirmacher P, Mechtersheimer G, Genome Biol 2013 14 137 10.1186/gb-2013-14-12-r137 24345474
6. Genetics of soft tissue tumors. van de Rijn M, Fletcher JA, Annu Rev Pathol 2006 1 435 466 10.1146/annurev.pathol.1.110304.100052 18039122
7. The role of telomere biology in cancer. Xu L, Li S, Stohr BA, Annu Rev Pathol 2013 8 49 78 10.1146/annurev-pathol-020712-164030 22934675
8. Specific association of human telomerase activity with immortal cells and cancer. Kim NW, Piatyszek MA, Prowse KR, Harley CB, West MD, Ho PL, Coviello GM, Wright WE, Weinrich SL, Shay JW, Science 1994 266 2011 2015 10.1126/science.7605428 7605428
9. Understanding and exploiting hTERT promoter regulation for diagnosis and treatment of human cancers. Kyo S, Takakura M, Fujiwara T, Inoue M, Cancer Sci 2008 99 1528 1538 10.1111/j.1349-7006.2008.00878.x 18754863
10. TERT promoter mutations in cancer development. Heidenreich B, Rachakonda PS, Hemminki K, Kumar R, Curr Opin Genet Dev 2014 24 30 37
11. TERT promoter mutations in familial and sporadic melanoma. Figl A, Rachakonda PS, Fischer C, Sucker A, Gast A, Kadel S, Moll I, Nagore E, Hemminki K, Schadendorf D, Kumar R, Science 2013 339 959 961 10.1126/science.1230062 23348503
12. Highly recurrent TERT promoter mutations in human melanoma. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA, Science 2013 339 957 959 10.1126/science.1229259 23348506
13. Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss. Arita H, Narita Y, Fukushima S, Tateishi K, Matsushita Y, Yoshida A, Miyakita Y, Ohno M, Collins VP, Kawahara N, Shibui S, Ichimura K, Acta Neuropathol 2013 126 267 276 10.1007/s00401-013-1141-6 23764841
14. TERT promoter mutations in ocular melanoma distinguish between conjunctival and uveal tumours. Griewank KG, Murali R, Schilling B, Scholz S, Sucker A, Song M, Susskind D, Grabellus F, Zimmer L, Hillen U, Steuhl KP, Schadendorf D, Westekemper H, Zeschnigk M, Br J Cancer 2013 109 497 501 10.1038/bjc.2013.312 23799844
15. TERT promoter mutations are frequent in atypical fibroxanthomas and pleomorphic dermal sarcomas. Griewank KG, Schilling B, Murali R, Bielefeld N, Schwamborn M, Sucker A, Zimmer L, Hillen U, Schaller J, Brenn T, Schadendorf D, Mentzel T, Mod Pathol 2014 27 502 508 10.1038/modpathol.2013.168 24030750
16. TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Killela PJ, Reitman ZJ, Jiao Y, Bettegowda C, Agrawal N, Diaz LA Jr, Friedman AH, Friedman H, Gallia GL, Giovanella BC, Grollman AP, He TC, He Y, Hruban RH, Jallo GI, Mandahl N, Meeker AK, Mertens F, Netto GJ, Rasheed BA, Riggins GJ, Rosenquist TA, Schiffman M, Shih Ie M, Theodorescu D, Torbenson MS, Velculescu VE, Wang TL, Wentzensen N, Wood LD, et al. Proc Natl Acad Sci USA 2013 110 6021 6026 10.1073/pnas.1303607110 23530248
17. Distribution of TERT promoter mutations in pediatric and adult tumors of the nervous system. Koelsche C, Sahm F, Capper D, Reuss D, Sturm D, Jones DT, Kool M, Northcott PA, Wiestler B, Bohmer K, Meyer J, Mawrin C, Hartmann C, Mittelbronn M, Platten M, Brokinkel B, Seiz M, Herold-Mende C, Unterberg A, Schittenhelm J, Weller M, Pfister S, Wick W, Korshunov A, von Deimling A, Acta Neuropathol 2013 126 907 915 10.1007/s00401-013-1195-5 24154961
18. Frequent somatic TERT promoter mutations in thyroid cancer: higher prevalence in advanced forms of the disease. Landa I, Ganly I, Chan TA, Mitsutake N, Matsuse M, Ibrahimpasic T, Ghossein RA, Fagin JA, J Clin Endocrinol Metab 2013 98 1562 1566 10.1210/jc.2013-2383 23833040
19. Highly prevalent TERT promoter mutations in aggressive thyroid cancers. Liu X, Bishop J, Shan Y, Pai S, Liu D, Murugan AK, Sun H, El-Naggar AK, Xing M, Endocr Relat Cancer 2013 20 603 610 10.1530/ERC-13-0210 23766237
20. Highly prevalent TERT promoter mutations in bladder cancer and glioblastoma. Liu X, Wu G, Shan Y, Hartmann C, von Deimling A, Xing M, Cell Cycle 2013 12 1637 1638 10.4161/cc.24662 23603989
21. High frequency of telomerase reverse-transcriptase promoter somatic mutations in hepatocellular carcinoma and preneoplastic lesions. Nault JC, Mallet M, Pilati C, Calderaro J, Bioulac-Sage P, Laurent C, Laurent A, Cherqui D, Balabaud C, Zucman Rossi J, Nat Commun 2013 4 2218 23887712
22. TERT promoter mutations in primary and secondary glioblastomas. Nonoguchi N, Ohta T, Oh JE, Kim YH, Kleihues P, Ohgaki H, Acta Neuropathol 2013 126 931 937 10.1007/s00401-013-1163-0 23955565
23. TERT promoter mutations are highly recurrent in SHH subgroup medulloblastoma. Remke M, Ramaswamy V, Peacock J, Shih DJ, Koelsche C, Northcott PA, Hill N, Cavalli FM, Kool M, Wang X, Mack SC, Barszczyk M, Morrissy AS, Wu X, Agnihotri S, Luu B, Jones DT, Garzia L, Dubuc AM, Zhukova N, Vanner R, Kros JM, French PJ, Van Meir EG, Vibhakar R, Zitterbart K, Chan JA, Bognar L, Klekner A, Lach B, et al. Acta Neuropathol 2013 126 917 929 10.1007/s00401-013-1198-2 24174164
24. Mutations of the TERT promoter are common in basal cell carcinoma and squamous cell carcinoma. Scott GA, Laughlin TS, Rothberg PG, Mod Pathol 2014 27 516 523 10.1038/modpathol.2013.167 24030752
25. Frequency of TERT promoter mutations in human cancers. Vinagre J, Almeida A, Populo H, Batista R, Lyra J, Pinto V, Coelho R, Celestino R, Prazeres H, Lima L, Melo M, da Rocha AG, Preto A, Castro P, Castro L, Pardal F, Lopes JM, Santos LL, Reis RM, Cameselle-Teijeiro J, Sobrinho-Simoes M, Lima J, Maximo V, Soares P, Nat Commun 2013 4 2185 23887589
26. High incidence of activating TERT promoter mutations in meningiomas undergoing malignant progression. Goutagny S, Nault JC, Mallet M, Henin D, Rossi JZ, Kalamarides M, Brain Pathol 2014 24 184 189 10.1111/bpa.12110
27. High telomerase activity and high HTRT mRNA expression differentiate pure myxoid and myxoid/round-cell liposarcomas. Schneider-Stock R, Jaeger V, Rys J, Epplen JT, Roessner A, Int J Cancer 2000 89 63 68 10.1002/(SICI)1097- 0215(20000120)89:1<63:AID-IJC10>3.0.CO;2-V 10719732 (Pubitemid 30078751)
28. Telomere maintenance mechanisms in liposarcomas: association with histologic subtypes and disease progression. Costa A, Daidone MG, Daprai L, Villa R, Cantu S, Pilotti S, Mariani L, Gronchi A, Henson JD, Reddel RR, Zaffaroni N, Cancer Res 2006 66 8918 8924 10.1158/0008-5472.CAN-06-0273 16951210 (Pubitemid 44449211)
29. Correlation between p38 mitogen-activated protein kinase and human telomerase reverse transcriptase in sarcomas. Matsuo T, Shimose S, Kubo T, Fujimori J, Yasunaga Y, Sugita T, Ochi M, J Exp Clin Cancer Res 2012 31 5 10.1186/1756-9966-31-5 22243975
30. Elevated telomerase activity, c-MYC-, and hTERT mRNA expression: association with tumour progression in malignant lipomatous tumours. Schneider-Stock R, Boltze C, Jager V, Epplen J, Landt O, Peters B, Rys J, Roessner A, J Pathol 2003 199 517 525 10.1002/path.1315 12635143 (Pubitemid 36416558)
31. Telomerase activity and hTERT mRNA expression can be heterogeneous and does not correlate with telomere length in soft tissue sarcomas. Yan P, Benhattar J, Coindre JM, Guillou L, Int J Cancer 2002 98 851 856 10.1002/ijc.10285 11948462 (Pubitemid 34286680)
32. Telomerase activity in human development is regulated by human telomerase reverse transcriptase (hTERT) transcription and by alternate splicing of hTERT transcripts. Ulaner GA, Hu JF, Vu TH, Giudice LC, Hoffman AR, Cancer Res 1998 58 4168 4172 9751630 (Pubitemid 28440575)
33. Inactive C-terminal telomerase reverse transcriptase insertion splicing variants are dominant-negative inhibitors of telomerase. Zhu S, Rousseau P, Lauzon C, Gandin V, Topisirovic I, Autexier C, Biochimie 2014 doi: 10.1016/j.biochi.2013.12.023
34. Telomerase regulation. Cifuentes-Rojas C, Shippen DE, Mutat Res 2012 730 20 27 10.1016/j.mrfmmm.2011.10.003 22032831
35. Altered telomeres in tumors with ATRX and DAXX mutations. Heaphy CM, de Wilde RF, Jiao Y, Klein AP, Edil BH, Shi C, Bettegowda C, Rodriguez FJ, Eberhart CG, Hebbar S, Offerhaus GJ, McLendon R, Rasheed BA, He Y, Yan H, Bigner DD, Oba-Shinjo SM, Marie SK, Riggins GJ, Kinzler KW, Vogelstein B, Hruban RH, Maitra A, Papadopoulos N, Meeker AK, Science 2011 333 425 10.1126/science.1207313 21719641
36. Assaying and investigating alternative lengthening of telomeres activity in human cells and cancers. Henson JD, Reddel RR, FEBS Lett 2010 584 3800 3811 10.1016/j.febslet.2010.06.009 20542034
37. High level of telomerase RNA gene expression is associated with chromatin modification, the ALT phenotype and poor prognosis in liposarcoma. Cairney CJ, Hoare SF, Daidone MG, Zaffaroni N, Keith WN, Br J Cancer 2008 98 1467 1474 10.1038/sj.bjc.6604328 18414473 (Pubitemid 351543588)
38. Prognostic relevance of ALT-associated markers in liposarcoma: a comparative analysis. Venturini L, Motta R, Gronchi A, Daidone M, Zaffaroni N, BMC Cancer 2010 10 254 10.1186/1471-2407-10-254 20525266
39. A robust assay for alternative lengthening of telomeres in tumors shows the significance of alternative lengthening of telomeres in sarcomas and astrocytomas. Henson JD, Hannay JA, McCarthy SW, Royds JA, Yeager TR, Robinson RA, Wharton SB, Jellinek DA, Arbuckle SM, Yoo J, Robinson BG, Learoyd DL, Stalley PD, Bonar SF, Yu D, Pollock RE, Reddel RR, Clin Cancer Res 2005 11 217 225 15671549 (Pubitemid 40075798)
40. Whole-genome profiling in liposarcomas reveals genetic alterations common to specific telomere maintenance mechanisms. Johnson JE, Gettings EJ, Schwalm J, Pei J, Testa JR, Litwin S, von Mehren M, Broccoli D, Cancer Res 2007 67 9221 9228 10.1158/0008-5472.CAN-07-1133 17909028 (Pubitemid 47535909)
41. Telomere lengths of translocation-associated and nontranslocation- associated sarcomas differ dramatically. Montgomery E, Argani P, Hicks JL, DeMarzo AM, Meeker AK, Am J Pathol 2004 164 1523 1529 10.1016/S0002-9440(10) 63710-8 15111298 (Pubitemid 38529754)
42. Liposarcomas: diagnostic pitfalls and new insights. Dei Tos AP, Histopathology 2014 64 38 52 10.1111/his.12311 24118009
43. Microarray-based copy number and expression profiling in dedifferentiated and pleomorphic liposarcoma. Fritz B, Schubert F, Wrobel G, Schwaenen C, Wessendorf S, Nessling M, Korz C, Rieker RJ, Montgomery K, Kucherlapati R, Mechtersheimer G, Eils R, Joos S, Lichter P, Cancer Res 2002 62 2993 2998 12036902 (Pubitemid 34602383)
44. Molecular abnormalities in liposarcoma: role of MDM2 and CDK4-containing amplicons at 12q13-22. Pilotti S, Della Torre G, Lavarino C, Sozzi G, Minoletti F, Vergani B, Azzarelli A, Rilke F, Pierotti MA, J Pathol 1998 185 188 190 10.1002/(SICI)1096-9896(199806)185:2<188:AID-PATH53>3.0.CO;2-2 9713346 (Pubitemid 28270932)
45. Distinct chromosomal imbalances in pleomorphic and in high-grade dedifferentiated liposarcomas. Rieker RJ, Joos S, Bartsch C, Willeke F, Schwarzbach M, Otano-Joos M, Ohl S, Hogel J, Lehnert T, Lichter P, Otto HF, Mechtersheimer G, Int J Cancer 2002 99 68 73 10.1002/ijc.10287 11948494 (Pubitemid 34273200)
46. Subtype specific prognostic nomogram for patients with primary liposarcoma of the retroperitoneum, extremity, or trunk. Dalal KM, Kattan MW, Antonescu CR, Brennan MF, Singer S, Ann Surg 2006 244 381 391 16926564
47. Alternative lengthening of telomeres and survival in patients with glioblastoma multiforme. Hakin-Smith V, Jellinek DA, Levy D, Carroll T, Teo M, Timperley WR, McKay MJ, Reddel RR, Royds JA, Lancet 2003 361 836 838 10.1016/S0140-6736(03)12681-5 12642053 (Pubitemid 36331849)
48. ATRX loss refines the classification of anaplastic gliomas and identifies a subgroup of IDH mutant astrocytic tumors with better prognosis. Wiestler B, Capper D, Holland-Letz T, Korshunov A, von Deimling A, Pfister SM, Platten M, Weller M, Wick W, Acta Neuropathol 2013 126 443 451 10.1007/s00401-013-1156-z 23904111
49. Meningeal hemangiopericytoma and solitary fibrous tumors carry the NAB2-STAT6 fusion and can be diagnosed by nuclear expression of STAT6 protein. Schweizer L, Koelsche C, Sahm F, Piro RM, Capper D, Reuss DE, Pusch S, Habel A, Meyer J, Gock T, Jones DT, Mawrin C, Schittenhelm J, Becker A, Heim S, Simon M, Herold-Mende C, Mechtersheimer G, Paulus W, Konig R, Wiestler OD, Pfister SM, von Deimling A, Acta Neuropathol 2013 125 651 658 10.1007/s00401-013-1117-6 23575898
50. Telomerase activity is a biomarker for high grade malignant peripheral nerve sheath tumors in neurofibromatosis type 1 individuals. Mantripragada KK, Caley M, Stephens P, Jones CJ, Kluwe L, Guha A, Mautner V, Upadhyaya M, Genes Chromosomes Cancer 2008 47 238 246 10.1002/gcc.20525 18069666 (Pubitemid 351162854)
51. Pathology of peripheral nerve sheath tumors: diagnostic overview and update on selected diagnostic problems. Rodriguez FJ, Folpe AL, Giannini C, Perry A, Acta Neuropathol 2012 123 295 319 10.1007/s00401-012-0954-z 22327363
52. Telomere maintenance mechanisms in malignant peripheral nerve sheath tumors: expression and prognostic relevance. Venturini L, Daidone MG, Motta R, Cimino-Reale G, Hoare SF, Gronchi A, Folini M, Keith WN, Zaffaroni N, Neuro Oncol 2012 14 736 744 10.1093/neuonc/nos083 22516689
53. Presence of telomerase activity in different musculoskeletal tumor histotypes and correlation with aggressiveness. Sangiorgi L, Gobbi GA, Lucarelli E, Sartorio SM, Mordenti M, Ghedini I, Maini V, Scrimieri F, Reggiani M, Bertoja AZ, Benassi MS, Picci P, Int J Cancer 2001 95 156 161 10.1002/1097-0215(20010520)95:3<156:AID-IJC1027>3.0.CO;2-L 11307148 (Pubitemid 32477230)