Robustness of amplicon deep sequencing underlines its utility in clinical applications

Journal of Molecular Diagnostics

Volumn 15, Issue 4, 2013, Pages 473-484

  Grossmann, Vera ^a   Roller, Andreas ^a   Klein, Hans Ulrich ^b   Weissmann, Sandra ^a   Kern, Wolfgang ^a   Haferlach, Claudia ^a   Dugas, Martin ^b   Haferlach, Torsten ^a   Schnittger, Susanne ^a   Kohlmann, Alexander ^a  

^a MLL MUNICH LEUKEMIA LABORATORY   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; DNA METHYLTRANSFERASE 3A; K RAS PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR RUNX1;

AMPLICON; AMPLICON DEEP SEQUENCING; ANALYTIC METHOD; ANALYTICAL PARAMETERS; ARTICLE; CLINICAL ARTICLE; DIAGNOSTIC ACCURACY; DILUTION; DISEASE COURSE; GENE AMPLIFICATION; HUMAN; LEUKEMIA; LIMIT OF DETECTION; MICROFLUIDIC ANALYSIS; MINIMAL RESIDUAL DISEASE; MUTATIONAL ANALYSIS; ONCOGENE N RAS; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; STATISTICAL ANALYSIS;

DNA PRIMERS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; MUTATION; NEOPLASMS; SEQUENCE ANALYSIS, DNA;

EID: 84879307454     PISSN: 15251578     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmoldx.2013.03.003     Document Type: Article

References (44)

1. A. Kohlmann, V. Grossmann, H.U. Klein, S. Schindela, T. Weiss, B. Kazak, F. Dicker, S. Schnittger, M. Dugas, W. Kern, C. Haferlach, and T. Haferlach Next-generation sequencing technology reveals a characteristic pattern of molecular mutations in 72.8% of chronic myelomonocytic leukemia by detecting frequent alterations in TET2, CBL, RAS, and RUNX1 J Clin Oncol 28 2010 3858 3865
2. A. Kohlmann, H.U. Klein, S. Weissmann, S. Bresolin, T. Chaplin, H. Cuppens, E. Haschke-Becher, B. Garicochea, V. Grossmann, B. Hanczaruk, K. Hebestreit, C. Gabriel, I. Iacobucci, J.H. Jansen, K.G. Te, L.L. van de, G. Martinelli, K. McGowan, M.R. Schweiger, B. Timmermann, P. Vandenberghe, B.D. Young, M. Dugas, and T. Haferlach The Interlaboratory RObustness of Next-generation sequencing (IRON) study: a deep sequencing investigation of TET2, CBL and KRAS mutations by an international consortium involving 10 laboratories Leukemia 25 2011 1840 1848
3. A. Kohlmann, V. Grossmann, and T. Haferlach Integration of next-generation sequencing into clinical practice: are we there yet? Semin Oncol 39 2012 26 36
4. A.S. Gargis, L. Kalman, M.W. Berry, D.P. Bick, D.P. Dimmock, and T. Hambuch Assuring the quality of next-generation sequencing in clinical laboratory practice Nature Biotechnol 30 2012 1033 1036
5. D. Grimwade, P. Vyas, and S. Freeman Assessment of minimal residual disease in acute myeloid leukemia Curr Opin Oncol 22 2010 656 663
6. S. Stilgenbauer, and T. Zenz Understanding and managing ultra high-risk chronic lymphocytic leukemia Hematology Am Soc Hematol Educ Program 2010 2010 481 488
7. H. Dohner, E.H. Estey, S. Amadori, F.R. Appelbaum, T. Buchner, A.K. Burnett, H. Dombret, P. Fenaux, D. Grimwade, R.A. Larson, F. Lo-Coco, T. Naoe, D. Niederwieser, G.J. Ossenkoppele, M.A. Sanz, J. Sierra, M.S. Tallman, B. Lowenberg, and C.D. Bloomfield Diagnosis and management of acute myeloid leukemia in adults: recommendations from an international expert panel, on behalf of the European LeukemiaNet Blood 115 2010 453 474
8. H.B. Ommen, S. Schnittger, J.V. Jovanovic, I.B. Ommen, H. Hasle, M. Ostergaard, D. Grimwade, and P. Hokland Strikingly different molecular relapse kinetics in NPM1c. PML-RARA, RUNX1-RUNX1T1, and CBFB-MYH11 acute myeloid leukemias Blood 115 2010 198 205
9. S. Schnittger, W. Kern, C. Tschulik, T. Weiss, F. Dicker, B. Falini, C. Haferlach, and T. Haferlach Minimal residual disease levels assessed by NPM1 mutation-specific RQ-PCR provide important prognostic information in AML Blood 114 2009 2220 2231
10. M. Osato, N. Asou, E. Abdalla, K. Hoshino, H. Yamasaki, T. Okubo, H. Suzushima, K. Takatsuki, T. Kanno, K. Shigesada, and Y. Ito Biallelic and heterozygous point mutations in the runt domain of the AML1/PEBP2alphaB gene associated with myeloblastic leukemias Blood 93 1999 1817 1824
11. C. Roumier, V. Eclache, M. Imbert, F. Davi, E. MacIntyre, R. Garand, P. Talmant, P. Lepelley, J.L. Lai, O. Casasnovas, M. Maynadie, F. Mugneret, C. Bilhou-Naberra, F. Valensi, I. Radford, M.J. Mozziconacci, C. Arnoulet, E. Duchayne, N. Dastugue, P. Cornillet, S. Daliphard, F. Garnache, N. Boudjerra, H. Jouault, O. Fenneteau, B. Pedron, R. Berger, G. Flandrin, P. Fenaux, and C. Preudhomme M0 AML, clinical and biologic features of the disease, including AML1 gene mutations: a report of 59 cases by the Groupe Francais d'Hematologie Cellulaire (GFHC) and the Groupe Francais de Cytogenetique Hematologique (GFCH) Blood 101 2003 1277 1283
12. M. Jadersten, L. Saft, A. Smith, A. Kulasekararaj, S. Pomplun, G. Gohring, A. Hedlund, R. Hast, B. Schlegelberger, A. Porwit, E. Hellstrom-Lindberg, and G.J. Mufti TP53 mutations in low-risk myelodysplastic syndromes with del(5q) predict disease progression J Clin Oncol 29 2011 1971 1979
13. F.G. Rucker, R.F. Schlenk, L. Bullinger, S. Kayser, V. Teleanu, H. Kett, M. Habdank, C.M. Kugler, K. Holzmann, V.I. Gaidzik, P. Paschka, G. Held, M. von Lilienfeld-Toal, M. Lubbert, S. Frohling, T. Zenz, J. Krauter, B. Schlegelberger, A. Ganser, P. Lichter, K. Dohner, and H. Dohner TP53 alterations in acute myeloid leukemia with complex karyotype correlate with specific copy number alterations, monosomal karyotype, and dismal outcome Blood 119 2012 2114 2121
14. T. Zenz, B. Eichhorst, R. Busch, T. Denzel, S. Habe, D. Winkler, A. Buhler, J. Edelmann, M. Bergmann, G. Hopfinger, M. Hensel, M. Hallek, H. Dohner, and S. Stilgenbauer TP53 mutation and survival in chronic lymphocytic leukemia J Clin Oncol 28 2010 4473 4479
15. T. Ernst, A.J. Chase, J. Score, C.E. Hidalgo-Curtis, C. Bryant, A.V. Jones, K. Waghorn, K. Zoi, F.M. Ross, A. Reiter, A. Hochhaus, H.G. Drexler, A. Duncombe, F. Cervantes, D. Oscier, J. Boultwood, F.H. Grand, and N.C. Cross Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders Nat Genet 42 2010 722 726
16. G. Nikoloski, S.M. Langemeijer, R.P. Kuiper, R. Knops, M. Massop, E.R. Tönnissen, A. van der Heijden, T.N. Scheele, P. Vandenberghe, T. de Witte, B.A. van der Reijden, and J.H. Jansen Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes Nat Genet 42 2010 665 667
17. F. Delhommeau, S. Dupont, V. Della Valle, C. James, S. Trannoy, A. Massé, O. Kosmider, J.P. Le Couedic, F. Robert, A. Alberdi, Y. Lécluse, I. Plo, F.J. Dreyfus, C. Marzac, N. Casadevall, C. Lacombe, S.P. Romana, P. Dessen, J. Soulier, F. Viguié, M. Fontenay, W. Vainchenker, and O.A. Bernard Mutation in TET2 in myeloid cancers N Engl J Med 360 2009 2289 2301
18. S. Weissmann, T. Alpermann, V. Grossmann, A. Kowarsch, N. Nadarajah, C. Eder, F. Dicker, A. Fasan, C. Haferlach, T. Haferlach, W. Kern, S. Schnittger, and A. Kohlmann Landscape of TET2 mutations in acute myeloid leukemia Leukemia 26 2012 934 942
19. A.J. Dunbar, L.P. Gondek, C.L. O'Keefe, H. Makishima, M.S. Rataul, H. Szpurka, M.A. Sekeres, X.F. Wang, M.A. McDevitt, and J.P. Maciejewski 250K single nucleotide polymorphism array karyotyping identifies acquired uniparental disomy and homozygous mutations, including novel missense substitutions of c-Cbl, in myeloid malignancies Cancer Res 68 2008 10349 10357
20. H. Makishima, H. Cazzolli, H. Szpurka, A. Dunbar, R. Tiu, J. Huh, H. Muramatsu, C. O'Keefe, E. Hsi, R.L. Paquette, S. Kojima, A.F. List, M.A. Sekeres, M.A. McDevitt, and J.P. Maciejewski Mutations of e3 ubiquitin ligase cbl family members constitute a novel common pathogenic lesion in myeloid malignancies J Clin Oncol 27 2009 6109 6116
21. T.J. Ley, L. Ding, M.J. Walter, M.D. McLellan, T. Lamprecht, and D.E. Larson DNMT3A mutations in acute myeloid leukemia N Engl J Med 363 2010 2424 2433
22. X.S. Puente, M. Pinyol, V. Quesada, L. Conde, G.R. Ordonez, and N. Villamor Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia Nature 475 2011 101 105
23. D. Rossi, S. Rasi, G. Fabbri, V. Spina, M. Fangazio, F. Forconi, R. Marasca, L. Laurenti, A. Bruscaggin, M. Cerri, S. Monti, S. Cresta, R. Fama, P.L. De, P. Bulian, V. Gattei, A. Guarini, S. Deaglio, D. Capello, R. Rabadan, L. Pasqualucci, R. la-Favera, R. Foa, and G. Gaidano Mutations of NOTCH1 are an independent predictor of survival in chronic lymphocytic leukemia Blood 119 2012 521 529
24. V. Grossmann, E. Tiacci, A.B. Holmes, A. Kohlmann, M.P. Martelli, and W. Kern Whole-exome sequencing identifies somatic mutations of BCOR in acute myeloid leukemia with normal karyotype Blood 118 2011 6153 6163
25. E. Tiacci, V. Trifonov, G. Schiavoni, A. Holmes, W. Kern, and M.P. Martelli BRAF mutations in hairy-cell leukemia N Engl J Med 364 2011 2305 2315
26. K. Yoshida, M. Sanada, Y. Shiraishi, D. Nowak, Y. Nagata, R. Yamamoto, Y. Sato, A. Sato-Otsubo, A. Kon, M. Nagasaki, G. Chalkidis, Y. Suzuki, M. Shiosaka, R. Kawahata, T. Yamaguchi, M. Otsu, N. Obara, M. Sakata-Yanagimoto, K. Ishiyama, H. Mori, F. Nolte, W.K. Hofmann, S. Miyawaki, S. Sugano, C. Haferlach, H.P. Koeffler, L.Y. Shih, T. Haferlach, S. Chiba, H. Nakauchi, S. Miyano, and S. Ogawa Frequent pathway mutations of splicing machinery in myelodysplasia Nature 478 2011 64 69
27. V.I. Gaidzik, L. Bullinger, R.F. Schlenk, A.S. Zimmermann, J. Rock, P. Paschka, A. Corbacioglu, J. Krauter, B. Schlegelberger, A. Ganser, D. Spath, A. Kundgen, I.G. Schmidt-Wolf, K. Gotze, D. Nachbaur, M. Pfreundschuh, H.A. Horst, H. Dohner, and K. Dohner RUNX1 mutations in acute myeloid leukemia: results from a comprehensive genetic and clinical analysis from the AML Study Group J Clin Oncol 29 2011 1364 1372
28. S. Schnittger, F. Dicker, W. Kern, N. Wendland, J. Sundermann, T. Alpermann, C. Haferlach, and T. Haferlach RUNX1 mutations are frequent in de novo AML with noncomplex karyotype and confer an unfavorable prognosis Blood 117 2011 2348 2357
29. S. Chiaretti, S. Tavolaro, M. Marinelli, M. Messina, G.I. Del, F.R. Mauro, S. Santangelo, A. Piciocchi, N. Peragine, S. Truong, N. Patten, E.M. Ghia, I. Torrente, M.S. De Propris, M. Nanni, J. Lawrence, A. Guarini, and R. Foa Evaluation of TP53 mutations with the AmpliChip p53 research test in chronic lymphocytic leukemia: correlation with clinical outcome and gene expression profiling Genes Chromosomes Cancer 50 2011 263 274
30. T. Zenz, D. Vollmer, M. Trbusek, J. Smardova, A. Benner, and T. Soussi TP53 mutation profile in chronic lymphocytic leukemia: evidence for a disease specific profile from a comprehensive analysis of 268 mutations Leukemia 24 2010 2072 2079
31. E.R. Mardis, L. Ding, D.J. Dooling, D.E. Larson, M.D. McLellan, and K. Chen Recurring mutations found by sequencing an acute myeloid leukemia genome N Engl J Med 361 2009 1058 1066
32. C. James, V. Ugo, J.P. Le Couedic, J. Staerk, F. Delhommeau, C. Lacout, L. Garcon, H. Raslova, R. Berger, A. Naceur-Griscelli, J.L. Villeval, S.N. Constantinescu, N. Casadevall, and W. Vainchenker A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera Nature 434 2005 1144 1148
33. V. Grossmann, W. Kern, S. Harbich, T. Alpermann, S. Jeromin, S. Schnittger, C. Haferlach, T. Haferlach, and A. Kohlmann Prognostic relevance of RUNX1 mutations in T-cell acute lymphoblastic leukemia Haematologica 96 2011 1874 1877
34. J. Zernant, C. Schubert, K.M. Im, T. Burke, C.M. Brown, G.A. Fishman, S.H. Tsang, P. Gouras, M. Dean, and R. Allikmets Analysis of the ABCA4 gene by next-generation sequencing Invest Ophthalmol Vis Sci 52 2011 8479 8487
35. V. Grossmann, A. Kohlmann, C. Eder, C. Haferlach, W. Kern, N.C. Cross, T. Haferlach, and S. Schnittger Molecular profiling of chronic myelomonocytic leukemia reveals diverse mutations in >80% of patients with TET2 and EZH2 being of high prognostic relevance Leukemia 25 2011 877 879
36. V. Grossmann, A. Kohlmann, M. Zenger, S. Schindela, C. Eder, S. Weissmann, S. Schnittger, W. Kern, M.C. Muller, A. Hochhaus, T. Haferlach, and C. Haferlach A deep-sequencing study of chronic myeloid leukemia patients in blast crisis (BC-CML) detects mutations in 76.9% of cases Leukemia 25 2011 557 560
37. F. Dicker, S. Schnittger, T. Haferlach, W. Kern, and C. Schoch Immunostimulatory oligonucleotide-induced metaphase cytogenetics detect chromosomal aberrations in 80% of CLL patients: a study of 132 CLL cases with correlation to FISH, IgVH status, and CD38 expression Blood 108 2006 3152 3160
38. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, K. Hornik, T. Hothorn, W. Huber, S. Iacus, R. Irizarry, F. Leisch, C. Li, M. Maechler, A.J. Rossini, G. Sawitzki, C. Smith, G. Smyth, L. Tierney, J.Y. Yang, and J. Zhang Bioconductor: open software development for computational biology and bioinformatics Genome Biol 5 2004 R80
39. H.U. Klein, C. Bartenhagen, A. Kohlmann, V. Grossmann, C. Ruckert, T. Haferlach, and M. Dugas R453Plus1Toolbox: an R/Bioconductor package for analyzing Roche 454 Sequencing data Bioinformatics 27 2011 1162 1163
40. V. Grossmann, S. Schnittger, S. Schindela, H.U. Klein, C. Eder, M. Dugas, W. Kern, T. Haferlach, C. Haferlach, and A. Kohlmann Strategy for robust detection of insertions, deletions, and point mutations in CEBPA, a GC-rich content gene, using 454 next-generation deep-sequencing technology J Mol Diagn 13 2011 129 136
41. J.J. Bartko The intraclass correlation coefficient as a measure of reliability Psychol Rep 19 1966 3 11
42. T. Zenz, S. Frohling, D. Mertens, H. Dohner, and S. Stilgenbauer Moving from prognostic to predictive factors in chronic lymphocytic leukaemia (CLL) Best Pract Res Clin Haematol 23 2010 71 84
43. S. Schnittger, U. Bacher, C. Haferlach, T. Alpermann, W. Kern, and T. Haferlach Diversity of the juxtamembrane and TKD1 mutations (exons 13-15) in the FLT3 gene with regards to mutant load, sequence, length, localization, and correlation with biological data Genes Chromosomes Cancer 51 2012 910 924
44. M.P. Strout, G. Marcucci, C.D. Bloomfield, and M.A. Caligiuri The partial tandem duplication of ALL1 (MLL) is consistently generated by Alu-mediated homologous recombination in acute myeloid leukemia Proc Natl Acad Sci U S A 95 1998 2390 2395