Upregulating mutations in the TERT promoter commonly occur in adult malignant gliomas and are strongly associated with total 1p19q loss

Acta Neuropathologica

Volumn 126, Issue 2, 2013, Pages 267-276

  Arita, Hideyuki ^a   Narita, Yoshitaka ^a   Fukushima, Shintaro ^b   Tateishi, Kensuke ^c   Matsushita, Yuko ^a   Yoshida, Akihiko ^d   Miyakita, Yasuji ^a   Ohno, Makoto ^a   Collins, V Peter ^e   Kawahara, Nobutaka ^c   Shibui, Soichiro ^a   Ichimura, Koichi ^b  

^a NATIONAL CANCER CENTER   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d NATIONAL CANCER CENTER HOSPITAL   (Japan)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Glioblastoma; IDH1; Oligodendroglioma; Telomerase; TERT; Total 1p19q loss

Indexed keywords

TELOMERASE REVERSE TRANSCRIPTASE;

ADULT; AGED; ARTICLE; ASTROCYTOMA; CANCER SURVIVAL; CDKN2A GENE; CHROMOSOME 1P; CHROMOSOME LOSS; CONTROLLED STUDY; DNA METHYLATION; EGFR GENE; FEMALE; GENE; GENE AMPLIFICATION; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE MUTATION; GLIOBLASTOMA; GLIOMA; HISTOPATHOLOGY; HOMOZYGOSITY; HUMAN; HUMAN CELL; IDH GENE; MAJOR CLINICAL STUDY; MALE; MDM2 GENE; OLIGODENDROGLIOMA; PATHOGENESIS; PRIORITY JOURNAL; PTEN GENE; PYROSEQUENCING; TERT GENE; TP53 GENE; UPREGULATION;

ADULT; AGED; BRAIN NEOPLASMS; CELL LINE, TUMOR; CHROMOSOMES, HUMAN, PAIR 1; CHROMOSOMES, HUMAN, PAIR 19; FEMALE; GLIOBLASTOMA; HUMANS; INCIDENCE; MALE; MIDDLE AGED; MUTATION; OLIGODENDROGLIOMA; PROGNOSIS; PROMOTER REGIONS, GENETIC; SURVIVAL ANALYSIS; TELOMERASE; TRANSLOCATION, GENETIC; UP-REGULATION;

EID: 84881095932     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1141-6     Document Type: Article

References (37)

1. Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, Hruban RH, Rodriguez FJ, Cahill DP, McLendon R, Riggins G, Velculescu VE, Oba-Shinjo SM, Marie SK, Vogelstein B, Bigner D, Yan H, Papadopoulos N, Kinzler KW (2011) Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science 333:1453-1455
2. Boldrini L, Pistolesi S, Gisfredi S, Ursino S, Ali G, Pieracci N, Basolo F, Parenti G, Fontanini G (2006) Telomerase activity and hTERT mRNA expression in glial tumors. Int J Oncol 28:1555-1560
3. Conomos D, Pickett HA, Reddel RR (2013) Alternative lengthening of telomeres: remodeling the telomere architecture. Front Oncol 3:27
4. Dome JS, Chung S, Bergemann T, Umbricht CB, Saji M, Carey LA, Grundy PE, Perlman EJ, Breslow NE, Sukumar S (1999) High telomerase reverse transcriptase (hTERT) messenger RNA level correlates with tumor recurrence in patients with favorable histology Wilms' tumor. Cancer Res 59:4301-4307
5. Fukushima T, Yoshino A, Katayama Y, Watanabe T, Kusama K, Moro I (2002) Prediction of clinical course of diffusely infiltrating astrocytomas from telomerase expression and quantitated activity level. Cancer Lett 187:191-198
6. Hakin-Smith V, Jellinek DA, Levy D, Carroll T, Teo M, Timperley WR, McKay MJ, Reddel RR, Royds JA (2003) Alternative lengthening of telomeres and survival in patients with glioblastoma multiforme. Lancet 361:836-838
7. Heaphy CM, Subhawong AP, Hong SM, Goggins MG, Montgomery EA, Gabrielson E, Netto GJ, Epstein JI, Lotan TL, Westra WH, Shih Ie M, Iacobuzio-Donahue CA, Maitra A, Li QK, Eberhart CG, Taube JM, Rakheja D, Kurman RJ, Wu TC, Roden RB, Argani P, De Marzo AM, Terracciano L, Torbenson M, Meeker AK (2011) Prevalence of the alternative lengthening of telomeres telomere maintenance mechanism in human cancer subtypes. Am J Pathol 179:1608-1615
8. 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 (2005) A robust assay for alternative lengthening of telomeres in tumors shows the significance of alternative lengthening of telomeres in sarcomas and astrocytomas. Clin Cancer Res 11:217-225
9. Hiraga S, Ohnishi T, Izumoto S, Miyahara E, Kanemura Y, Matsumura H, Arita N (1998) Telomerase activity and alterations in telomere length in human brain tumors. Cancer Res 58:2117-2125
10. Horn S, Figl A, Rachakonda PS, Fischer C, Sucker A, Gast A, Kadel S, Moll I, Nagore E, Hemminki K, Schadendorf D, Kumar R (2013) TERT promoter mutations in familial and sporadic melanoma. Science 339:959-961
11. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA (2013) Highly recurrent TERT promoter mutations in human melanoma. Science 339:957-959
12. Ichimura K (2012) Molecular pathogenesis of IDH mutations in gliomas. Brain Tumor Pathol 29:131-139
13. Ichimura K, Bolin MB, Goike HM, Schmidt EE, Moshref A, Collins VP (2000) Deregulation of the p14ARF/MDM2/p53 pathway is a prerequisite for human astrocytic gliomas with G1-S transition control gene abnormalities. Cancer Res 60:417-424
14. Ichimura K, Pearson DM, Kocialkowski S, Backlund LM, Chan R, Jones DT, Collins VP (2009) IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro Oncol 11:341-347
15. Jiao Y, Killela PJ, Reitman ZJ, Rasheed AB, Heaphy CM, de Wilde RF, Rodriguez FJ, Rosemberg S, Oba-Shinjo SM, Nagahashi Marie SK, Bettegowda C, Agrawal N, Lipp E, Pirozzi C, Lopez G, He Y, Friedman H, Friedman AH, Riggins GJ, Holdhoff M, Burger P, McLendon R, Bigner DD, Vogelstein B, Meeker AK, Kinzler KW, Papadopoulos N, Diaz LA, Yan H (2012) Frequent ATRX, CIC, and FUBP1 mutations refine the classification of malignant gliomas. Oncotarget 3:709-722
16. Kannan K, Inagaki A, Silber J, Gorovets D, Zhang J, Kastenhuber ER, Heguy A, Petrini JH, Chan TA, Huse JT (2012) Whole-exome sequencing identifies ATRX mutation as a key molecular determinant in lower-grade glioma. Oncotarget 3:1194-1203
17. 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 IM, Theodorescu D, Torbenson MS, Velculescu VE, Wang TL, Wentzensen N, Wood LD, Zhang M, McLendon RE, Bigner DD, Kinzler KW, Vogelstein B, Papadopoulos N, Yan H (2013) TERT promoter mutations occur frequently in gliomas and a subset of tumors derived from cells with low rates of self-renewal. Proc Natl Acad Sci USA 110:6021-6026
18. Langford LA, Piatyszek MA, Xu R, Schold SC Jr, Shay JW (1995) Telomerase activity in human brain tumours. Lancet 346:1267-1268
19. Le S, Zhu JJ, Anthony DC, Greider CW, Black PM (1998) Telomerase activity in human gliomas. Neurosurgery 42:1120-1124
20. Liu XY, Gerges N, Korshunov A, Sabha N, Khuong-Quang DA, Fontebasso AM, Fleming A, Hadjadj D, Schwartzentruber J, Majewski J, Dong Z, Siegel P, Albrecht S, Croul S, Jones DT, Kool M, Tonjes M, Reifenberger G, Faury D, Zadeh G, Pfister S, Jabado N (2012) Frequent ATRX mutations and loss of expression in adult diffuse astrocytic tumors carrying IDH1/IDH2 and TP53 mutations. Acta Neuropathol 124:615-625
21. Lotsch D, Ghanim B, Laaber M, Wurm G, Weis S, Lenz S, Webersinke G, Pichler J, Berger W, Spiegl-Kreinecker S (2013) Prognostic significance of telomerase-associated parameters in glioblastoma: effect of patient age. Neuro Oncol 15:423-432
22. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97-109
23. Maida Y, Yasukawa M, Furuuchi M, Lassmann T, Possemato R, Okamoto N, Kasim V, Hayashizaki Y, Hahn WC, Masutomi K (2009) An RNA-dependent RNA polymerase formed by TERT and the RMRP RNA. Nature 461:230-235
24. Masutomi K, Hahn WC (2003) Telomerase and tumorigenesis. Cancer Lett 194:163-172
25. McCabe MG, Ichimura K, Liu L, Plant K, Backlund LM, Pearson DM, Collins VP (2006) High-resolution array-based comparative genomic hybridization of medulloblastomas and supratentorial primitive neuroectodermal tumors. J Neuropathol Exp Neurol 65:549-561
26. Mulholland S, Pearson DM, Hamoudi RA, Malley DS, Smith CM, Weaver JM, Jones DT, Kocialkowski S, Backlund LM, Collins VP, Ichimura K (2012) MGMT CpG island is invariably methylated in adult astrocytic and oligodendroglial tumors with IDH1 or IDH2 mutations. Int J Cancer 131:1104-1113
27. Nguyen DN, Heaphy CM, de Wilde RF, Orr BA, Odia Y, Eberhart CG, Meeker AK, Rodriguez FJ (2012) Molecular and morphologic correlates of the alternative lengthening of telomeres phenotype in high-grade astrocytomas. Brain Pathol 23:237-243
28. Okita Y, Narita Y, Miyakita Y, Ohno M, Matsushita Y, Fukushima S, Sumi M, Ichimura K, Kayama T, Shibui S (2012) IDH1/2 mutation is a prognostic marker for survival and predicts response to chemotherapy for grade II gliomas concomitantly treated with radiation therapy. Int J Oncol [Epub ahead of print]
29. Ruden M, Puri N (2012) Novel anticancer therapeutics targeting telomerase. Cancer Treat Rev 39:444-456
30. Sahm F, Koelsche C, Meyer J, Pusch S, Lindenberg K, Mueller W, Herold-Mende C, von Deimling A, Hartmann C (2012) CIC and FUBP1 mutations in oligodendrogliomas, oligoastrocytomas and astrocytomas. Acta Neuropathol 123:853-860
31. Sano T, Asai A, Mishima K, Fujimaki T, Kirino T (1998) Telomerase activity in 144 brain tumours. Br J Cancer 77:1633-1637
32. Schmidt EE, Ichimura K, Goike HM, Moshref A, Liu L, Collins VP (1999) Mutational profile of the PTEN gene in primary human astrocytic tumors and cultivated xenografts. J Neuropathol Exp Neurol 58:1170-1183
33. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E, Jacob K, Sturm D, Fontebasso AM, Quang DA, Tonjes M, Hovestadt V, Albrecht S, Kool M, Nantel A, Konermann C, Lindroth A, Jager N, Rausch T, Ryzhova M, Korbel JO, Hielscher T, Hauser P, Garami M, Klekner A, Bognar L, Ebinger M, Schuhmann MU, Scheurlen W, Pekrun A, Fruhwald MC, Roggendorf W, Kramm C, Durken M, Atkinson J, Lepage P, Montpetit A, Zakrzewska M, Zakrzewski K, Liberski PP, Dong Z, Siegel P, Kulozik AE, Zapatka M, Guha A, Malkin D, Felsberg J, Reifenberger G, von Deimling A, Ichimura K, Collins VP, Witt H, Milde T, Witt O, Zhang C, Castelo-Branco P, Lichter P, Faury D, Tabori U, Plass C, Majewski J, Pfister SM, Jabado N (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482:226-231
34. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996
35. TCGA (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061-1068
36. Yip S, Butterfield YS, Morozova O, Chittaranjan S, Blough MD, An J, Birol I, Chesnelong C, Chiu R, Chuah E, Corbett R, Docking R, Firme M, Hirst M, Jackman S, Karsan A, Li H, Louis DN, Maslova A, Moore R, Moradian A, Mungall KL, Perizzolo M, Qian J, Roldan G, Smith EE, Tamura-Wells J, Thiessen N, Varhol R, Weiss S, Wu W, Young S, Zhao Y, Mungall AJ, Jones SJ, Morin GB, Chan JA, Cairncross JG, Marra MA (2012) Concurrent CIC mutations, IDH mutations, and 1p/19q loss distinguish oligodendrogliomas from other cancers. J Pathol 226:7-16
37. Zeng N, Liu L, McCabe MG, Jones DT, Ichimura K, Collins VP (2009) Real-time quantitative polymerase chain reaction (qPCR) analysis with fluorescence resonance energy transfer (FRET) probes reveals differential expression of the four ERBB4 juxtamembrane region variants between medulloblastoma and pilocytic astrocytoma. Neuropathol Appl Neurobiol 35:353-366