Fol. Biol. 2016, 62, 194-202

https://doi.org/10.14712/fb2016062050194

IDH1/2 Mutation and MGMT Promoter Methylation – the Relevant Survival Predictors in Czech Patients with Brain Gliomas

Filip Kramář1, M. Minárik2, L. Benešová2, T. Halková2, D. Netuka1, O. Bradáč1, V. Beneš1

1Department of Neurosurgery and Neurooncology, First Faculty of Medicine, Charles University and Military University Hospital Prague, Czech Republic
2Center for Applied Genomics of Solid Tumors (CEGES), Genomac Research Institute, Ltd, Prague, Czech Republic

Received January 2016
Accepted June 2016

References

1. Bauchet, L., Zouaoui, S., Darlix, A., Menjot de Champfleur, N., Ferreira, E., Fabbro, M., Kerr, C., Taillandier, L. (2014) Assessment and treatment relevance in elderly glioblastoma patients. Neuro Oncol. 16, 1459-1468. <https://doi.org/10.1093/neuonc/nou063>
2. Cairncross, G., Wang, M., Shaw, E., Jenkins, R., Brachman, D., Buckner, J., Fink, K., Souhami, L., Laperriere, N., Curran, W., Mehta, M. (2013) Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J. Clin. Oncol. 31, 337-343. <https://doi.org/10.1200/JCO.2012.43.2674>
3. Cairncross, J. G., Ueki, K., Zlatescu, M. C., Lisle, D. K., Finkelstein, D. M., Hammond, R. R., Silver, J. S., Stark, P. C., Macdonald, D. R., Ino, Y., Ramsay, D. A., Louis, D. N. (1998) Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J. Natl. Cancer Inst. 90, 1473-1479. <https://doi.org/10.1093/jnci/90.19.1473>
4. Cairncross, J. G., Wang, M., Jenkins, R. B., Shaw, E. G., Giannini, C., Brachman, D. G., Buckner, J. C., Fink, K. L., Souhami, L., Laperriere, N. J., Huse, J. T., Mehta, M. P., Curran, W. J. (2014) Benefit from procarbazine, lomustine, and vincristine in oligodendroglial tumors is associated with mutation of IDH. J. Clin. Oncol. 32, 783-790. <https://doi.org/10.1200/JCO.2013.49.3726>
5. Camelo-Piragua, S., Jansen, M., Ganguly, A., Kim, J. C., Louis, D. N., Nutt, C. L. (2010) Mutant IDH1-specific immunohistochemistry distinguishes diffuse astrocytoma from astrocytosis. Acta Neuropathol. 119, 509–511. <https://doi.org/10.1007/s00401-009-0632-y>
6. Chang-Halpenny, C. N., Yeh, J., Lien, W. W. (2015) Elderly patients with glioblastoma multiforme treated with concurrent temozolomide and standard- versus abbreviatedcourse radiotherapy. Perm. J. 19, 15-20. <https://doi.org/10.7812/TPP/14-083>
7. Dang, L., White, D. W., Gross, S., Bennett, B. D., Bittinger, M. A., Driggers, E. M., Fantin, V. R., Jang, H. G., Jin, S., Keenan, M. C., Marks, K. M., Prins, R. M., Ward, P. S., Yen, K. E., Liau, L. M., Rabinowitz, J. D., Cantley, L. C., Thompson, C. B., Vander Heiden, M. G., Su, S. M. (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462, 739. <https://doi.org/10.1038/nature08617>
8. Eckel-Passow, J. E., Lachance, D. H., Molinaro, A. M., Walsh, K. M., Decker, P. A., Sicotte, H., Pekmezci, M., Rice, T., Kosel, M. L., Smirnov, I. V., Sarkar, G., Caron, A. A., Kollmeyer, T. M., Praska, C. E., Chada, A. R., Halder, C., Hansen, H. M., McCoy, L. S., Bracci, P. M., Marshall, R., Zheng, S., Reis, G. F., Pico, A. R., O’Neill, B. P., Buckner, J. C., Giannini, C., Huse, J. T., Perry, A., Tihan, T., Berger, M. S., Chang, S. M., Prados, M. D., Wiemels, J., Wiencke, J. K., Wrensch, M. R., Jenkins, R. B. (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N. Engl. J. Med. 372, 2499-2508. <https://doi.org/10.1056/NEJMoa1407279>
9. Fuente, M. I. de la, Young, R. J., Rubel, J., Rosenblum, M., Tisnado, J., Briggs, S., Arevalo-Perez, J., Cross, J. R., Campos, C., Straley, K., Zhu, D., Dong, C., Thomas, A., Omuro, A. A., Nolan, C. P., Pentsova, E., Kaley, T. J., Oh, J. H., Noeske, R., Maher, E., Choi, C., Gutin, P. H., Holodny, A. I., Yen, K., DeAngelis, L. M., Mellinghoff, I. K., Thakur, S. B. (2015) Integration of 2-hydroxyglutarateproton magnetic resonance spectroscopy into clinical practice for disease monitoring in isocitrate dehydrogenasemutant glioma. Neuro Oncol. 18, 283-290. <https://doi.org/10.1093/neuonc/nov307>
10. Hegi, M. E., Diserens, A.-C. Gorlia, T., Hamou, M.-F., de Tribolet, N., Weller, M., Kross, J. M., Hainfellner, J. A., Mason, W., Mariani, L., Bromberg, J. E. C., Hau, P., Mirimanoff, R. O., Cairncross, J. G., Janzer, R. C., Stupp, R. (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 352, 997-1003. <https://doi.org/10.1056/NEJMoa043331>
11. Hömig-Hölzel, C., Savola, S. (2012) Multiplex ligation-dependent probe amplification (MLPA) in tumor diagnostics and prognostics. Diagn. Mol. Pathol. 21, 189-206. <https://doi.org/10.1097/PDM.0b013e3182595516>
12. Horbinski, C., Kelly, L., Nikiforov, Y. E., Durso, M. B., Nikiforova, M. N. (2010) Detection of IDH1 and IDH2 mutations by fluorescence melting curve analysis as a diagnostic tool for brain biopsies. J. Mol. Diagn. 12, 487-492. <https://doi.org/10.2353/jmoldx.2010.090228>
13. Jakola, A. S., Unsgård, G., Myrmel, K. S., Kloster, R., Torp, S. H., Sagberg, L. M., Lindal, S., Solheim, O. (2014) Surgical strategies in low-grade gliomas and implications for longterm quality of life. J. Clin. Neurosci. 21, 1304-1309. <https://doi.org/10.1016/j.jocn.2013.11.027>
14. Karnofsky, D. A., Abelmann, W. H., Craver, L. F., Burchenal, J. H. (1948) The use of the nitrogen mustards in the palliative treatment of carcinoma. With particular reference to bronchogenic carcinoma. Cancer 1, 634-656. <https://doi.org/10.1002/1097-0142(194811)1:4<634::AID-CNCR2820010410>3.0.CO;2-L>
15. Leu, S., von Felten, S., Frank, S., Boulay, J.-L., Mariani, L. (2016) IDH mutation is associated with higher risk of malignant transformation in low-grade glioma. J. Neurooncol. 127, 363-372. <https://doi.org/10.1007/s11060-015-2048-y>
16. Lhotska, H., Zemanova, Z., Cechova, H., Ransdorfova, S., Lizcova, L., Kramar, F., Krejcik, Z., Svobodova, K., Bystricka, D., Hrabal, P., Dohnalova, A., Michalova, K. (2015) Genetic and epigenetic characterization of lowgrade gliomas reveals frequent methylation of the MLH3 gene. Genes Chromosomes Cancer 54, 655-667. <https://doi.org/10.1002/gcc.22266>
17. Li, L., Paz, A. C., Wilky, B. A., Johnson, B., Galoian, K., Rosenberg, A., Hu, G., Tinoco, G., Bodamer, O., Trent, J. C. (2015) Treatment with a small molecule mutant IDH1 inhibitor suppresses tumorigenic activity and decreases production of the oncometabolite 2-hydroxyglutarate in human chondrosarcoma cells. PLoS One, 10, e0133813. <https://doi.org/10.1371/journal.pone.0133813>
18. Megova, M., Drabek, J., Koudelakova, V., Trojanec, R., Kalita, O., Hajduch, M. (2014) Isocitrate dehydrogenase 1 and 2 mutations in gliomas. J. Neurosci. Res. 92, 1611-1620. <https://doi.org/10.1002/jnr.23456>
19. Molenaar, R. J., Verbaan, D., Lamba, S., Zanon, C., Jeuken, J. W. M., Boots-Sprenger, S. H. E., Wesseling, P., Hulsebos, T. J. M., Troost, D., van Tilborg, A. A., Leenstra, S., Vandertop, W. P., Bardelli, A., van Noorden, C. J. F., Bleeker, F. E. (2014) The combination of IDH1 mutations and MGMT methylation status predicts survival in glioblastoma better than either IDH1 or MGMT alone. Neuro Oncol. 16, 1263-1273. <https://doi.org/10.1093/neuonc/nou005>
20. Noushmehr, H., Weisenberger, D. J., Diefes, K., Phillips, H. S., Pujara, K., Berman, B. P., Pan, F., Pelloski, C. E., Sulman, E. P., Bhat, K. P., Verhaak, R. G. W., Hoadley, K. A., Hayes, D. N., Perou, C. M., Schmidt, H. K., Ding, L., Wilson, R. K., Van Den Berg, D., Shen, H., Bengtsson, H., Neuvial, P., Cope, L. M., Buckley, J., Herman, J. G., Baylin, S. B., Laird, P. W., Aldape, K., Cancer Genome Atlas Research Network (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17, 510-522. <https://doi.org/10.1016/j.ccr.2010.03.017>
21. Parsons, D. W., Jones, S., Zhang, X., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I.-M., Gallia, G. L., Olivi, A., McLendon, R., Rasheed, B. A., Keir, S., Nikolskaya, T., Nikolsky, Y., Busam, D. A., Tekleab, H., Diaz, L. A., Hartigan, J., Smith, D. R., Strausberg, R. L., Marie, S. K. N., Shinjo, S. M. O., Yan, H., Riggins, G. J., Bigner, D. D., Karchin, R., Papadopoulos, N., Parmigiani, G., Vogelstein, B., Velculescu, V. E., Kinzler, K. W. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321, 1807-1812. <https://doi.org/10.1126/science.1164382>
22. Rankeillor, K. L., Cairns, D. A., Loughrey, C., Short, S. C., Chumas, P., Ismail, A., Chakrabarty, A., Lawler, S. E., Roberts, P. (2014) Methylation-specific multiplex ligationdependent probe amplification identifies promoter methylation events associated with survival in glioblastoma. J. Neurooncol. 117, 243-251. <https://doi.org/10.1007/s11060-014-1372-y>
23. Rauscher, J., Beschorner, R., Gierke, M., Bisdas, S., Braun, C., Ebner, F. H., Schittenhelm, J. (2014) WT1 expression increases with malignancy and indicates unfavourable outcome in astrocytoma. J. Clin. Pathol. 67, 556-561. <https://doi.org/10.1136/jclinpath-2013-202114>
24. Schiff, D., Purow, B. (2013) Neuro-oncology: five new things. Neurol. Clin. Pract. 3, 326-333. <https://doi.org/10.1212/CPJ.0b013e3182a1ba35>
25. Senft, C., Bink, A., Franz, K., Vatter, H., Gasser, T., Seifert, V. (2011) Intraoperative MRI guidance and extent of resection in glioma surgery: a randomised, controlled trial. The Lancet Oncol. 12, 997-1003. <https://doi.org/10.1016/S1470-2045(11)70196-6>
26. Shah, M. A., Denton, E. L., Arrowsmith, C. H., Lupien, M., Schapira, M. (2014) A global assessment of cancer genomic alterations in epigenetic mechanisms. Epigenetics Chromatin 7, 29. <https://doi.org/10.1186/1756-8935-7-29>
27. Stupp, R., Mason, W. P., van den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J. B., Belanger, K., Brandes, A. A., Marosi, C., Bogdahn, U., Curschmann, J., Janzer, R. C., Ludwin, S. K., Gorlia, T., Allgeier, A., Lacombe, D., Cairncross, J. G., Eisenhauer, E., Mirimanoff, R. O. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987-996. <https://doi.org/10.1056/NEJMoa043330>
28. Sturm, D., Witt, H., Hovestadt, V., Khuong-Quang, D.-A., Jones, D. T. W., Konermann, C., Pfaff, E., Tönjes, M., Sill, M., Bender, S., Kool, M., Zapatka, M., Becker, N., Zucknick, M., Hielscher, T., Liu, X.-Y., Fontebasso, A. M., Ryzhova, M., Albrecht, S., Jacob, K., Wolter, M., Ebinger, M., Schuhmann, M. U., van Meter, T., Frühwald, M. C., Hauch, H., Pekrun, A., Radlwimmer, B., Niehues, T., von Komorowski, G., Dürken, M., Kulozik, A. E., Madden, J., Donson, A., Foreman, N. K., Drissi, R., Fouladi, M., Scheurlen, W., von Deimling, A., Monoranu, C., Roggendorf, W., Herold-Mende, C., Unterberg, A., Kramm, C. M., Felsberg, J., Hartmann, C., Wiestler, B., Wick, W., Milde, T., Witt, O., Lindroth, A. M., Schwartzentruber, J., Faury, D., Fleming, A., Zakrzewska, M., Liberski, P. P., Zakrzewski, K., Hauser, P., Garami, M., Klekner, A., Bognar, L., Morrissy, S., Cavalli, F., Taylor, M. D., van Sluis, P., Koster, J., Versteeg, R., Volckmann, R., Mikkelsen, T., Aldape, K., Reifenberger, G., Collins, V. P., Majewski, J., Korshunov, A., Lichter, P., Plass, C., Jabado, N., Pfister, S. M. (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22, 425-437. <https://doi.org/10.1016/j.ccr.2012.08.024>
29. Suijker, J., Oosting, J., Koornneef, A., Struys, E. A., Salomons, G. S., Schaap, F. G., Waaijer, C. J. F., Wijers-Koster, P. M., Briaire-de Bruijn, I. H., Haazen, L., Riester, S. M., Dudakovic, A., Danen, E., Cleton-Jansen, A.-M., van Wijnen, A. J., Bovée, J. V. M. G. (2015) Inhibition of mutant IDH1 decreases D-2-HG levels without affecting tumorigenic properties of chondrosarcoma cell lines. Oncotarget 6, 12505-12519. <https://doi.org/10.18632/oncotarget.3723>
30. Takano, S., Kato, Y., Yamamoto, T., Liu, X., Ishikawa, E., Kaneko, M. K., Ogasawara, S., Matsuda, M., Noguchi, M., Matsumura, A. (2015) Diagnostic advantage of double immunohistochemistry using two mutation-specific anti-IDH antibodies (HMab-1 and MsMab-1) in gliomas. Brain Tumor Pathol. 32, 169-175. <https://doi.org/10.1007/s10014-015-0214-8>
31. The Cancer Genome Atlas Research Network (2015) Comprehensive, integrative genomic analysis of diffuse lowergrade gliomas. N. Engl. J. Med., 372, 2481–2498. <https://doi.org/10.1056/NEJMoa1402121>
32. Turcan, S., Rohle, D., Goenka, A., Walsh, L. A., Fang, F., Yilmaz, E., Campos, C., Fabius, A. W. M., Lu, C., Ward, P. S., Thompson, C. B., Kaufman, A., Guryanova, O., Levine, R., Heguy, A., Viale, A., Morris, L. G. T., Huse, J. T., Mellinghoff, I. K., Chan, T. A. (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483, 479-483. <https://doi.org/10.1038/nature10866>
33. Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.-H., Ito, S., Yang, C., Wang, P., Xiao, M.-T., Liu, L., Jiang, W., Liu, J., Zhang, J., Wang, B., Frye, S., Zhang, Y., Xu, Y., Lei, Q., Guan, K.-L., Zhao, S., Xiong, Y. (2011) Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of α-ketoglutarate-dependent dioxygenases. Cancer Cell 19, 17-30. <https://doi.org/10.1016/j.ccr.2010.12.014>
34. Yan, H., Parsons, D. W., Jin, G., McLendon, R., Rasheed, B. A., Yuan, W., Kos, I., Batinic-Haberle, I., Jones, S., Riggins, G. J., Friedman, H., Friedman, A., Reardon, D., Herndon, J., Kinzler, K. W., Velculescu, V. E., Vogelstein, B., Bigner, D. D. (2009) IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360, 765-773. <https://doi.org/10.1056/NEJMoa0808710>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive