Detection of Dual IDH1 and IDH2 Mutations by Targeted Next-Generation Sequencing in Acute Myeloid Leukemia and Myelodysplastic Syndromes

Journal of Molecular Diagnostics

Volumn 17, Issue 6, 2015, Pages 661-668

  Platt, Mia Y ^a,b   Fathi, Amir T ^a,b   Borger, Darrell R ^a,b   Brunner, Andrew M ^a,b   Hasserjian, Robert P ^a,b   Balaj, Leonora ^a,b   Lum, Amy ^c   Yip, Stephen ^c   Dias Santagata, Dora ^a,b   Zheng, Zongli ^a,b   Le, Long P ^a,b   Graubert, Timothy A ^a,b   Iafrate, A John ^a,b   Nardi, Valentina ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE 2, HUMAN;

ACUTE MYELOBLASTIC LEUKEMIA; ADULT; AGED; ARTICLE; CHRONIC MYELOMONOCYTIC LEUKEMIA; DNA ISOLATION; FEMALE; GENE FREQUENCY; GENE MUTATION; GENETIC VARIABILITY; GENOTYPING TECHNIQUE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MULTIPLEX POLYMERASE CHAIN REACTION; MUTATIONAL ANALYSIS; MYELODYSPLASTIC SYNDROME; NEXT GENERATION SEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISM; ACUTE MYELOID LEUKEMIA; ALLELE; GENETICS; HIGH THROUGHPUT SEQUENCING; MIDDLE AGED; MUTATION; PROCEDURES;

AGED; ALLELES; FEMALE; GENE FREQUENCY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; ISOCITRATE DEHYDROGENASE; LEUKEMIA, MYELOID, ACUTE; MALE; MIDDLE AGED; MUTATION; MYELODYSPLASTIC SYNDROMES;

EID: 84943602339     PISSN: 15251578     EISSN: 19437811     Source Type: Journal    
DOI: 10.1016/j.jmoldx.2015.06.004     Document Type: Article

References (35)

1. E.R. Mardis, L. Ding, D.J. Dooling, D.E. Larson, M.D. McLellan, K. Chen, and et al. Recurring mutations found by sequencing an acute myeloid leukemia genome N Engl J Med 361 2009 1058 1066
2. Cancer Genome Atlas Research Network Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia N Engl J Med 368 2013 2059 2074
3. P.S. Ward, J. Patel, D.R. Wise, O. Abdel-Wahab, B.D. Bennett, H.A. Coller, J.R. Cross, V.R. Fantin, C.V. Hedvat, A.E. Perl, J.D. Rabinowitz, M. Carroll, S.M. Su, K.A. Sharp, R.L. Levine, and C.B. Thompson The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate Cancer Cell 17 2010 225 234
4. G. Marcucci, K. Maharry, Y.Z. Wu, M.D. Radmacher, K. Mrozek, D. Margeson, K.B. Holland, S.P. Whitman, H. Becker, S. Schwind, K.H. Metzeler, B.L. Powell, T.H. Carter, J.E. Kolitz, M. Wetzler, A.J. Carroll, M.R. Baer, M.A. Caligiuri, R.A. Larson, and C.D. Bloomfield IDH1 and IDH2 gene mutations identify novel molecular subsets within de novo cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study J Clin Oncol 28 2010 2348 2355
5. C.L. Green, C.M. Evans, L. Zhao, R.K. Hills, A.K. Burnett, D.C. Linch, and R.E. Gale The prognostic significance of IDH2 mutations in AML depends on the location of the mutation Blood 118 2011 409 412
6. J.P. Patel, M. Gonen, M.E. Figueroa, H. Fernandez, Z. Sun, J. Racevskis, P. Van Vlierberghe, I. Dolgalev, S. Thomas, O. Aminova, K. Huberman, J. Cheng, A. Viale, N.D. Socci, A. Heguy, A. Cherry, G. Vance, R.R. Higgins, R.P. Ketterling, R.E. Gallagher, M. Litzow, M.R. van den Brink, H.M. Lazarus, J.M. Rowe, S. Luger, A. Ferrando, E. Paietta, M.S. Tallman, A. Melnick, O. Abdel-Wahab, and R.L. Levine Prognostic relevance of integrated genetic profiling in acute myeloid leukemia N Engl J Med 366 2012 1079 1089
7. J.A. Losman, R.E. Looper, P. Koivunen, S. Lee, R.K. Schneider, C. McMahon, G.S. Cowley, D.E. Root, B.L. Ebert, and W.G. Kaelin Jr. (R)-2-hydroxyglutarate is sufficient to promote leukemogenesis and its effects are reversible Science 339 2013 1621 1625
8. S. Chotirat, W. Thongnoppakhun, W. Wanachiwanawin, and C.U. Auewarakul Acquired somatic mutations of isocitrate dehydrogenases 1 and 2 (IDH1 and IDH2) in preleukemic disorders Blood Cells Mol Dis 54 2015 286 291
9. T.L. Lin, Y. Nagata, H.W. Kao, M. Sanada, Y. Okuno, C.F. Huang, D.C. Liang, M.C. Kuo, C.L. Lai, E.H. Lee, Y.S. Shih, H. Tanaka, Y. Shiraishi, K. Chiba, T.H. Lin, J.H. Wu, S. Miyano, S. Ogawa, and L.Y. Shih Clonal leukemic evolution in myelodysplastic syndromes with TET2 and IDH1/2 mutations Haematologica 99 2014 28 36
10. J.S. Welch, T.J. Ley, D.C. Link, C.A. Miller, D.E. Larson, D.C. Koboldt, and et al. The origin and evolution of mutations in acute myeloid leukemia Cell 150 2012 264 278
11. M.E. Figueroa, O. Abdel-Wahab, C. Lu, P.S. Ward, J. Patel, A. Shih, Y. Li, N. Bhagwat, A. Vasanthakumar, H.F. Fernandez, M.S. Tallman, Z. Sun, K. Wolniak, J.K. Peeters, W. Liu, S.E. Choe, V.R. Fantin, E. Paietta, B. Lowenberg, J.D. Licht, L.A. Godley, R. Delwel, P.J. Valk, C.B. Thompson, R.L. Levine, and A. Melnick Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation Cancer Cell 18 2010 553 567
12. P. Paschka, R.F. Schlenk, V.I. Gaidzik, M. Habdank, J. Kronke, L. Bullinger, D. Spath, S. Kayser, M. Zucknick, K. Gotze, H.A. Horst, U. Germing, H. Dohner, and K. Dohner IDH1 and IDH2 mutations are frequent genetic alterations in acute myeloid leukemia and confer adverse prognosis in cytogenetically normal acute myeloid leukemia with NPM1 mutation without FLT3 internal tandem duplication J Clin Oncol 28 2010 3636 3643
13. J. Popovici-Muller, J.O. Saunders, F.G. Salituro, J.M. Travins, S. Yan, F. Zhao, S. Gross, L. Dang, K.E. Yen, H. Yang, K.S. Straley, S. Jin, K. Kunii, V.R. Fantin, S. Zhang, Q. Pan, D. Shi, S.A. Biller, and S.M. Su Discovery of the first potent inhibitors of mutant IDH1 that lower tumor 2-HG in vivo ACS Med Chem Lett 3 2012 850 855
14. D. Rohle, J. Popovici-Muller, N. Palaskas, S. Turcan, C. Grommes, C. Campos, J. Tsoi, O. Clark, B. Oldrini, E. Komisopoulou, K. Kunii, A. Pedraza, S. Schalm, L. Silverman, A. Miller, F. Wang, H. Yang, Y. Chen, A. Kernytsky, M.K. Rosenblum, W. Liu, S.A. Biller, S.M. Su, C.W. Brennan, T.A. Chan, T.G. Graeber, K.E. Yen, and I.K. Mellinghoff An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells Science 340 2013 626 630
15. F. Wang, J. Travins, B. DeLaBarre, V. Penard-Lacronique, S. Schalm, E. Hansen, K. Straley, A. Kernytsky, W. Liu, C. Gliser, H. Yang, S. Gross, E. Artin, V. Saada, E. Mylonas, C. Quivoron, J. Popovici-Muller, J.O. Saunders, F.G. Salituro, S. Yan, S. Murray, W. Wei, Y. Gao, L. Dang, M. Dorsch, S. Agresta, D.P. Schenkein, S.A. Biller, S.M. Su, S. de Botton, and K.E. Yen Targeted inhibition of mutant IDH2 in leukemia cells induces cellular differentiation Science 340 2013 622 626
16. E. Hansen, C. Quivoron, K. Straley, R.M. Lemieux, J. Popovici-Muller, H. Sadrzadeh, A.T. Fathi, C. Gliser, M. David, V. Saada, J.-B. Micol, O. Bernard, M. Dorsch, H. Yang, M. Su, S. Agresta, S. de Botton, V. Penard-Lacronique, and K. Yen AG-120, an oral, selective, first-in-class, potent inhibitor of mutant IDH1, reduces intracellular 2HG and induces cellular differentiation in TF-1 R132H cells and primary human IDH1 mutant AML patient samples treated ex vivo Blood 124 2014 3734
17. A.H. Shih, K.R. Shank, C. Meydan, A.M. Intlekofer, P. Ward, C.B. Thompson, A.M. Melnick, J. Travins, K. Straley, C. Gliser, K. Yen, and R.L. Levine AG-221, a small molecule mutant IDH2 inhibitor, remodels the epigenetic state of IDH2-mutant cells and induces alterations in self-renewal/differentiation in IDH2-mutant AML model in vivo Blood 124 2014 437
18. C. Quivoron, M. David, K. Straley, J. Travins, H. Kim, Y. Chen, D. Zhu, V. Saada, O. Bawa, P. Opolon, M. Polrot, J.-B. Micol, C. Willekens, O. Bernard, H. Yang, S. Agresta, S. de Botton, K. Yen, and V. Penard-Lacronique AG-221, an oral, selective, first-in-class, potent IDH2-R140Q mutant inhibitor, induces differentiation in a xenotransplant model Blood 124 2014 3735
19. E.M. Stein, J.K. Altman, R. Collins, D.J. DeAngelo, A.T. Fathi, I. Flinn, A. Frankel, R.L. Levine, B.C. Medeiros, M. Patel, D.A. Pollyea, G.J. Roboz, R.M. Stone, R.T. Swords, M.S. Tallman, S. Agresta, B. Fan, H. Yang, K. Yen, and S. de Botton AG-221, an oral, selective, first-in-class, potent inhibitor of the IDH2 mutant metabolic enzyme, induces durable remissions in a phase I study in patients with IDH2 mutation positive advanced hematologic malignancies Blood 124 2014 115
20. B. Fan, Y. Chen, F. Wang, K. Yen, L. Utley, C. Almon, S. Biller, S. Agresta, and H. Yang Evaluation of pharmacokinetic-pharmacodynamic (PKPD) relationship of an oral, selective, first-in-class, potent IDH2 inhibitor, AG-221, from a phase 1 trial in patients with advanced IDH2 mutant positive hematologic malignancies Blood 124 2014 3737
21. Z. Zheng, M. Liebers, B. Zhelyazkova, Y. Cao, D. Panditi, K.D. Lynch, J. Chen, H.E. Robinson, H.S. Shim, J. Chmielecki, W. Pao, J.A. Engelman, A.J. Iafrate, and L.P. Le Anchored multiplex PCR for targeted next-generation sequencing Nat Med 20 2014 1479 1484
22. H. Li, and R. Durbin Fast and accurate short read alignment with Burrows-Wheeler transform Bioinformatics 25 2009 1754 1760
23. K. Cibulskis, M.S. Lawrence, S.L. Carter, A. Sivachenko, D. Jaffe, C. Sougnez, S. Gabriel, M. Meyerson, E.S. Lander, and G. Getz Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples Nat Biotechnol 31 2013 213 219
24. O. Westesson, M. Skinner, and I. Holmes Visualizing next-generation sequencing data with JBrowse Brief Bioinform 14 2013 172 177
25. H. Yan, D.W. Parsons, G. Jin, R. McLendon, B.A. Rasheed, W. Yuan, I. Kos, I. Batinic-Haberle, S. Jones, G.J. Riggins, H. Friedman, A. Friedman, D. Reardon, J. Herndon, K.W. Kinzler, V.E. Velculescu, B. Vogelstein, and D.D. Bigner IDH1 and IDH2 mutations in gliomas N Engl J Med 360 2009 765 773
26. D.W. Parsons, S. Jones, X. Zhang, J.C. Lin, R.J. Leary, P. Angenendt, P. Mankoo, H. Carter, I.M. Siu, G.L. Gallia, A. Olivi, R. McLendon, B.A. Rasheed, S. Keir, T. Nikolskaya, Y. Nikolsky, D.A. Busam, H. Tekleab, L.A. Diaz Jr., J. Hartigan, D.R. Smith, R.L. Strausberg, S.K. Marie, S.M. Shinjo, H. Yan, G.J. Riggins, D.D. Bigner, R. Karchin, N. Papadopoulos, G. Parmigiani, B. Vogelstein, V.E. Velculescu, and K.W. Kinzler An integrated genomic analysis of human glioblastoma multiforme Science 321 2008 1807 1812
27. D.A. Kerr, H.U. Lopez, V. Deshpande, F.J. Hornicek, Z. Duan, Y. Zhang, A.E. Rosenberg, D.R. Borger, and G.P. Nielsen Molecular distinction of chondrosarcoma from chondroblastic osteosarcoma through IDH1/2 mutations Am J Surg Pathol 37 2013 787 795
28. M. Arai, S. Nobusawa, H. Ikota, S. Takemura, and Y. Nakazato Frequent IDH1/2 mutations in intracranial chondrosarcoma: a possible diagnostic clue for its differentiation from chordoma Brain Tumor Pathol 29 2012 201 206
29. M.F. Amary, K. Bacsi, F. Maggiani, S. Damato, D. Halai, F. Berisha, R. Pollock, P. O'Donnell, A. Grigoriadis, T. Diss, M. Eskandarpour, N. Presneau, P.C. Hogendoorn, A. Futreal, R. Tirabosco, and A.M. Flanagan IDH1 and IDH2 mutations are frequent events in central chondrosarcoma and central and periosteal chondromas but not in other mesenchymal tumours J Pathol 224 2011 334 343
30. D.R. Borger, K.K. Tanabe, K.C. Fan, H.U. Lopez, V.R. Fantin, K.S. Straley, D.P. Schenkein, A.F. Hezel, M. Ancukiewicz, H.M. Liebman, E.L. Kwak, J.W. Clark, D.P. Ryan, V. Deshpande, D. Dias-Santagata, L.W. Ellisen, A.X. Zhu, and A.J. Iafrate Frequent mutation of isocitrate dehydrogenase (IDH)1 and IDH2 in cholangiocarcinoma identified through broad-based tumor genotyping Oncologist 17 2012 72 79
31. A.T. Fathi, H. Sadrzadeh, A.H. Comander, M.J. Higgins, A. Bardia, A. Perry, M. Burke, R. Silver, C.R. Matulis, K.S. Straley, K.E. Yen, S. Agresta, H. Kim, D.P. Schenkein, and D.R. Borger Isocitrate dehydrogenase 1 (IDH1) mutation in breast adenocarcinoma is associated with elevated levels of serum and urine 2-hydroxyglutarate Oncologist 19 2014 602 607
32. O. Kosmider, V. Gelsi-Boyer, L. Slama, F. Dreyfus, O. Beyne-Rauzy, B. Quesnel, M. Hunault-Berger, B. Slama, N. Vey, C. Lacombe, E. Solary, D. Birnbaum, O.A. Bernard, and M. Fontenay Mutations of IDH1 and IDH2 genes in early and accelerated phases of myelodysplastic syndromes and MDS/myeloproliferative neoplasms Leukemia 24 2010 1094 1096
33. A. Chaturvedi, M.M. Araujo Cruz, N. Jyotsana, A. Sharma, H. Yun, K. Gorlich, M. Wichmann, A. Schwarzer, M. Preller, F. Thol, J. Meyer, R. Haemmerle, E.A. Struys, E.E. Jansen, U. Modlich, Z. Li, L.M. Sly, R. Geffers, R. Lindner, D.J. Manstein, U. Lehmann, J. Krauter, A. Ganser, and M. Heuser Mutant IDH1 promotes leukemogenesis in vivo and can be specifically targeted in human AML Blood 122 2013 2877 2887
34. C.J. Pirozzi, Z.J. Reitman, and H. Yan Releasing the block: setting differentiation free with mutant IDH inhibitors Cancer Cell 23 2013 570 572
35. M.A. Quail, M. Smith, P. Coupland, T.D. Otto, S.R. Harris, T.R. Connor, A. Bertoni, H.P. Swerdlow, and Y. Gu A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers BMC Genomics 13 2012 341