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JUNB, DUSP2, SGK1, SOCS1 and CREBBP are frequently mutated in T-cell/histiocyte-rich large B-cell lymphoma
Bianca Schuhmacher, Julia Bein, Tobias Rausch, Vladimir Benes, Thomas Tousseyn, Martine Vornanen, Maurilio Ponzoni, Lorenz Thurner, Randy Gascoyne, Christian Steidl, Ralf Küppers, Martin-Leo Hansmann, Sylvia Hartmann
Haematologica February 2019 104: 330-337; doi:10.3324/haematol.2018.203224
Bianca Schuhmacher
Dr. Senckenberg Institute of Pathology, Goethe University, Frankfurt am Main, Germany
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Julia Bein
Dr. Senckenberg Institute of Pathology, Goethe University, Frankfurt am Main, Germany
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Tobias Rausch
Genecore, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany Genome Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
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Vladimir Benes
Genecore, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
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Thomas Tousseyn
Department of Pathology, University Hospitals K.U. Leuven, Belgium
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Martine Vornanen
Department of Pathology, Tampere University Hospital and University of Tampere, Finland
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Maurilio Ponzoni
Unit of Lymphoid Malignancies, Department of Pathology, Scientific Institute San Raffaele, Milan, Italy
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Lorenz Thurner
José Carreras Center for Immuno and Gene Therapy and Internal Medicine I, Saarland University Medical School, Homburg, Saar, Germany Department of Internal Medicine 2, Hospital of the J. W. Goethe University, Frankfurt am Main, Germany
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Randy Gascoyne
Department of Pathology and Laboratory Medicine and the Centre for Lymphoid Cancer, British Columbia Cancer Agency, University of British Columbia, Vancouver, Canada
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Christian Steidl
Department of Pathology and Laboratory Medicine and the Centre for Lymphoid Cancer, British Columbia Cancer Agency, University of British Columbia, Vancouver, Canada
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Ralf Küppers
Institute of Cell Biology (Cancer Research), Faculty of Medicine, University of Duisburg-Essen, Essen, Germany Deutsches Konsortium für Translationale Krebsforschung (DKTK), Germany
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Martin-Leo Hansmann
Dr. Senckenberg Institute of Pathology, Goethe University, Frankfurt am Main, Germany Reference and Consultant Center for Lymphoma and Lymph Node Diagnostics, Goethe University, Frankfurt am Main, Germany Frankfurt Institute of Advanced Studies, Frankfurt am Main, Germany
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Sylvia Hartmann
Dr. Senckenberg Institute of Pathology, Goethe University, Frankfurt am Main, Germany Reference and Consultant Center for Lymphoma and Lymph Node Diagnostics, Goethe University, Frankfurt am Main, Germany
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  • For correspondence: s.hartmann@em.uni-frankfurt.de

Author Affiliations

  1. Bianca Schuhmacher1,
  2. Julia Bein1,
  3. Tobias Rausch2,3,
  4. Vladimir Benes2,
  5. Thomas Tousseyn4,
  6. Martine Vornanen5,
  7. Maurilio Ponzoni6,
  8. Lorenz Thurner7,8,
  9. Randy Gascoyne9,
  10. Christian Steidl9,
  11. Ralf Küppers10,11,
  12. Martin-Leo Hansmann1,12,13 and
  13. Sylvia Hartmann1,12⇑
  1. 1Dr. Senckenberg Institute of Pathology, Goethe University, Frankfurt am Main, Germany
  2. 2Genecore, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
  3. 3Genome Biology Unit, European Molecular Biology Laboratory (EMBL), Heidelberg, Germany
  4. 4Department of Pathology, University Hospitals K.U. Leuven, Belgium
  5. 5Department of Pathology, Tampere University Hospital and University of Tampere, Finland
  6. 6Unit of Lymphoid Malignancies, Department of Pathology, Scientific Institute San Raffaele, Milan, Italy
  7. 7José Carreras Center for Immuno and Gene Therapy and Internal Medicine I, Saarland University Medical School, Homburg, Saar, Germany
  8. 8Department of Internal Medicine 2, Hospital of the J. W. Goethe University, Frankfurt am Main, Germany
  9. 9Department of Pathology and Laboratory Medicine and the Centre for Lymphoid Cancer, British Columbia Cancer Agency, University of British Columbia, Vancouver, Canada
  10. 10Institute of Cell Biology (Cancer Research), Faculty of Medicine, University of Duisburg-Essen, Essen, Germany
  11. 11Deutsches Konsortium für Translationale Krebsforschung (DKTK), Germany
  12. 12Reference and Consultant Center for Lymphoma and Lymph Node Diagnostics, Goethe University, Frankfurt am Main, Germany
  13. 13Frankfurt Institute of Advanced Studies, Frankfurt am Main, Germany
  1. Correspondence:
    s.hartmann{at}em.uni-frankfurt.de
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Data supplements

  • Schuhmacher et al. Supplementary Appendix

    Schuhmacher et al. Supplementary appendix provided by the authors.

    Files in this Data Supplement:

    • Adobe PDF - 2018.203224.SCHUHMACHER_SUPPL.pdf
  • Disclosures and Contributions

    Files in this Data Supplement:

    • Adobe PDF - 2018_203224-Disclosures_and_Contributions.pdf

ARTICLE FIGURES & DATA

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  • Figure 1.
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    Figure 1.

    Genes recurrently affected by mutations and their mutational load in nodular lymphocyte-predominant Hodgkin lymphoma and T-cell/histiocyte-rich large B-cell lymphoma. (A) Frequencies of recurrently mutated genes (≥2 cases) in six cases of NLPHL A/B (blue), 11 cases of NLPHL C/D/E (green) and nine cases of THRLBCL (red) sorted by overall recurrence. (B) Mutated genes per case in NLPHL A/B, NLPHL C/D/E and THRLBCL. (C) Number of SNVs per case in NLPHL A/B, NLPHL C/D/E and THRLBCL. (D) Scatter plot of SNVs per case and kbp of CCDS in the seven most recurrently mutated genes in NLPHL A/B, NLPHL C/D/E and THRL-BCL. In (B-D), horizontal lines correspond to medians; P-values by Kruskal-Wallis test are indicated in the case of statistical significance. *P<0.05, **P<0.01, ***P<0.001. NLPHL: nodular lymphocyte-predominant Hodgkin lymphoma; THRLBCL: T-cell/histiocyte-rich large B-cell lymphoma; SNVs: single nucleotide variants; CCDS: Consensus coding sequence.

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    Figure 2.

    Mutation patterns in the most recurrently mutated genes in nodular lymphocyte-predominant Hodgkin lymphoma and T-cell/histiocyte-rich large B-cell lymphoma. Schematic overview of the mutational distribution in the most recurrently mutated genes. For each gene missense (triangles), stop gain (spheres) and splice site (squares) mutations are mapped to coding exons (top) and protein domains (bottom). Mutations are color-coded according to the occurrence in the groups (blue: NLPHL A/B; green: NLPHL C/D/E; red: THRLBCL). Amino acid positions of protein domains are adopted from the Uniprot database (www.uniprot.org) and refer to the canonical sequences (JUNB: P17275, DUSP2: Q05923, SGK1: O00141, SOCS1: O15524, CREBBP: Q92793, FN1: P02751, TRRAP: Q9Y4A5). bZIP: basic leucine zipper motif; DsPc: dual specific phosphatase, catalytic domain; Pkinase: protein kinase domain; AGC-kinase C: AGC-kinase C-terminal domain; Rhod: rhodanese; SH2: Src homology 2 domain; KIR: kinase inhibitory region; CH1/2/3: cysteine/hystidine-rich region; KIX: kinase inducible domain; BROMO: bromodomain; HAT: histone acetyltransferase domain; Q: poly glutamine stretch; FN: fibronectin; TP53: tumor suppressor p53 binding site; FAT: FRAP-ATM-TRRAP domain; FATC: FAT C-terminal; PI3K/PI4K: phosphatidylinositol 3-kinase/phosphatidylinositol 4-kinase domain; NLPHL: nodular lymphocyte-predominant Hodgkin lymphoma; THRLBCL: T-cell/histiocyte-rich large B-cell lymphoma.

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    Figure 3.

    Characteristics of somatic mutations and activation-induced cytidine deaminase expression in nodular lymphocyte-predominant Hodgkin lymphoma and T-cell/histiocyte-rich large B-cell lymphoma. (A) Analysis of distribution of mutations to SHM hotspot motifs. (B) Ratio of mutations at C:G sites to A:T sites. (C) Ratio of transition to transversion mutations. In (A-C) synonymous SNVs were considered in addition to non-synonymous SNVs. Asterisks denote statistical significance. *P<0.05, **P<0.01, ***P<0.001. P-values by χ2 test. (D) Expression of AICDA in the LP cells of NLPHL (400× magnification). (E) Expression of AICDA in the tumor cells of THRLBCL (400× magnification). Tumor cells are highlighted by arrows. AICDA: activation-induced cytidine deaminase; NLPHL: nodular lymphocyte-predominant Hodgkin lymphoma; THRLBCL: T-cell/histiocyte-rich large B-cell lymphoma; SHM: somatic hypermutation; SNVs: single nucleotide variants.

Tables

  • Figures
  • Table 1.

    Clinical information on nodular lymphocyte-predominant Hodgkin lymphoma and T-cell/histiocyte-rich large B-cell lymphoma patients.

    Table 1.
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Haematologica: 104 (2)
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JUNB, DUSP2, SGK1, SOCS1 and CREBBP are frequently mutated in T-cell/histiocyte-rich large B-cell lymphoma
Bianca Schuhmacher, Julia Bein, Tobias Rausch, Vladimir Benes, Thomas Tousseyn, Martine Vornanen, Maurilio Ponzoni, Lorenz Thurner, Randy Gascoyne, Christian Steidl, Ralf Küppers, Martin-Leo Hansmann, Sylvia Hartmann
Haematologica Feb 2019, 104 (2) 330-337; DOI: 10.3324/haematol.2018.203224

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Bianca Schuhmacher, Julia Bein, Tobias Rausch, Vladimir Benes, Thomas Tousseyn, Martine Vornanen, Maurilio Ponzoni, Lorenz Thurner, Randy Gascoyne, Christian Steidl, Ralf Küppers, Martin-Leo Hansmann, Sylvia Hartmann
Haematologica Feb 2019, 104 (2) 330-337; DOI: 10.3324/haematol.2018.203224
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