Timing the initiation of multiple myeloma.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
21 04 2020
Historique:
received: 10 10 2019
accepted: 26 03 2020
entrez: 23 4 2020
pubmed: 23 4 2020
medline: 4 8 2020
Statut: epublish

Résumé

The evolution and progression of multiple myeloma and its precursors over time is poorly understood. Here, we investigate the landscape and timing of mutational processes shaping multiple myeloma evolution in a large cohort of 89 whole genomes and 973 exomes. We identify eight processes, including a mutational signature caused by exposure to melphalan. Reconstructing the chronological activity of each mutational signature, we estimate that the initial transformation of a germinal center B-cell usually occurred during the first 2

Identifiants

pubmed: 32317634
doi: 10.1038/s41467-020-15740-9
pii: 10.1038/s41467-020-15740-9
pmc: PMC7174344
doi:

Substances chimiques

Minor Histocompatibility Antigens 0
Proteins 0
RNA, Messenger 0
AICDA (activation-induced cytidine deaminase) EC 3.5.4.-
APOBEC-1 Deaminase EC 3.5.4.36
APOBEC1 protein, human EC 3.5.4.36
APOBEC3A protein, human EC 3.5.4.5
APOBEC3B protein, human EC 3.5.4.5
Cytidine Deaminase EC 3.5.4.5

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

1917

Subventions

Organisme : BLRD VA
ID : I01 BX001584
Pays : United States
Organisme : NCI NIH HHS
ID : P01 CA155258
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA008748
Pays : United States
Organisme : NCI NIH HHS
ID : P50 CA100707
Pays : United States

Références

McGranahan, N. & Swanton, C. Clonal heterogeneity and tumor evolution: past, present. Future Cell 168, 613–628 (2017).
pubmed: 28187284 pmcid: 28187284
Gerstung, M. et al. The evolutionary history of 2,658 cancers. Nature 578, 122–128 (2020).
pubmed: 32025013 pmcid: 7054212 doi: 10.1038/s41586-019-1907-7
Yates, L. R. & Campbell, P. J. Evolution of the cancer genome. Nat. Rev. Genet. 13, 795–806 (2012).
pubmed: 23044827 pmcid: 3666082 doi: 10.1038/nrg3317
Lee, J. J. et al. Tracing oncogene rearrangements in the mutational history of lung adenocarcinoma. Cell 177, 1842.e21–1857.e21 (2019).
Mitchell, T. J. et al. Timing the landmark events in the evolution of clear cell renal cell cancer: TRACERx renal. Cell 173, 611.e17–623.e17 (2018).
doi: 10.1016/j.cell.2018.02.020
Alexandrov, L. B. et al. Clock-like mutational processes in human somatic cells. Nat. Genet. 47, 1402–1407 (2015).
pubmed: 4783858 pmcid: 4783858 doi: 10.1038/ng.3441
Blokzijl, F. et al. Tissue-specific mutation accumulation in human adult stem cells during life. Nature 538, 260–264 (2016).
pubmed: 27698416 pmcid: 5536223 doi: 10.1038/nature19768
Korber, V. et al. Evolutionary trajectories of IDH(WT) glioblastomas reveal a common path of early tumorigenesis instigated years ahead of initial diagnosis. Cancer Cell 35, 692.e12–704.e12 (2019).
doi: 10.1016/j.ccell.2019.02.007
Alexandrov, L. B. et al. The repertoire of mutational signatures in human cancer. Nature 578, 94–101 (2020).
pubmed: 32025018 pmcid: 7054213 doi: 10.1038/s41586-020-1943-3
Rajkumar, S. V., Landgren, O. & Mateos, M. V. Smoldering multiple myeloma. Blood 125, 3069–3075 (2015).
pubmed: 25838344 pmcid: 4432003 doi: 10.1182/blood-2014-09-568899
Landgren, O. et al. Association of immune marker changes with progression of monoclonal gammopathy of undetermined significance to multiple myeloma. JAMA Oncol. 5, 1293–1301 (2019).
doi: 10.1001/jamaoncol.2019.1568
Maura, F. et al. Moving from cancer burden to cancer genomics for smoldering myeloma: a review. JAMA Oncol. https://doi.org/10.1001/jamaoncol.2019.4659 (2019).
doi: 10.1001/jamaoncol.2019.4659 pubmed: 31830214 pmcid: 31830214
Manier, S. et al. Genomic complexity of multiple myeloma and its clinical implications. Nat. Rev. Clin. Oncol. 14, 100–113 (2017).
pubmed: 27531699 doi: 10.1038/nrclinonc.2016.122 pmcid: 27531699
Morgan, G. J., Walker, B. A. & Davies, F. E. The genetic architecture of multiple myeloma. Nat. Rev. Cancer 12, 335–348 (2012).
pubmed: 22495321 doi: 10.1038/nrc3257 pmcid: 22495321
Maura, F. et al. Genomic landscape and chronological reconstruction of driver events in multiple myeloma. Nat. Commun. 10, 3835 (2019).
pubmed: 31444325 pmcid: 6707220 doi: 10.1038/s41467-019-11680-1
Fittall, M. W. & Van Loo, P. Translating insights into tumor evolution to clinical practice: promises and challenges. Genome Med. 11, 20 (2019).
pubmed: 30925887 pmcid: 6440005 doi: 10.1186/s13073-019-0632-z
Bolli, N. et al. Genomic patterns of progression in smoldering multiple myeloma. Nat. Commun. 9, 3363 (2018).
pubmed: 30135448 pmcid: 6105687 doi: 10.1038/s41467-018-05058-y
Maura, F. et al. A practical guide for mutational signature analysis in hematological malignancies. Nat. Commun. 10, 2969 (2019).
pubmed: 31278357 pmcid: 6611883 doi: 10.1038/s41467-019-11037-8
Weinhold, N. et al. Clonal selection and double-hit events involving tumor suppressor genes underlie relapse in myeloma. Blood 128, 1735–1744 (2016).
pubmed: 27516441 pmcid: 5043128 doi: 10.1182/blood-2016-06-723007
Kumar, S. et al. International Myeloma Working Group consensus criteria for response and minimal residual disease assessment in multiple myeloma. Lancet Oncol. 17, e328–346 (2016).
pubmed: 27511158 doi: 10.1016/S1470-2045(16)30206-6 pmcid: 27511158
Ziccheddu, B. et al. Integrative analysis of the genomic and transcriptomic landscape of double-refractory multiple myeloma. Blood Adv. 4, 830–844 (2020).
pubmed: 32126144 pmcid: 7065476 doi: 10.1182/bloodadvances.2019000779
Kucab, J. E. et al. A compendium of mutational signatures of environmental agents. Cell 177, 821.e16–836.e16 (2019).
doi: 10.1016/j.cell.2019.03.001
Lawrence, M. S. et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499, 214–218 (2013).
pubmed: 23770567 pmcid: 3919509 doi: 10.1038/nature12213
Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415–421 (2013).
pubmed: 3776390 pmcid: 3776390 doi: 10.1038/nature12477
Bolli, N. et al. Heterogeneity of genomic evolution and mutational profiles in multiple myeloma. Nat. Commun. 5, 2997 (2014).
pubmed: 24429703 pmcid: 3905727 doi: 10.1038/ncomms3997
Maura, F. et al. Biological and prognostic impact of APOBEC-induced mutations in the spectrum of plasma cell dyscrasias and multiple myeloma cell lines. Leukemia https://doi.org/10.1038/leu.2017.345 (2017).
doi: 10.1038/leu.2017.345 pubmed: 29209044 pmcid: 29209044
Walker, B. A. et al. APOBEC family mutational signatures are associated with poor prognosis translocations in multiple myeloma. Nat. Commun. 6, 6997 (2015).
pubmed: 25904160 pmcid: 4568299 doi: 10.1038/ncomms7997
Hoang, P. H. et al. Whole-genome sequencing of multiple myeloma reveals oncogenic pathways are targeted somatically through multiple mechanisms. Leukemia https://doi.org/10.1038/s41375-018-0103-3 (2018).
doi: 10.1038/s41375-018-0103-3 pubmed: 29654271 pmcid: 6224406
Chan, K. et al. An APOBEC3A hypermutation signature is distinguishable from the signature of background mutagenesis by APOBEC3B in human cancers. Nat. Genet. 47, 1067–1072 (2015).
pubmed: 26258849 pmcid: 4594173 doi: 10.1038/ng.3378
Kasar, S. et al. Whole-genome sequencing reveals activation-induced cytidine deaminase signatures during indolent chronic lymphocytic leukaemia evolution. Nat. Commun. 6, 8866 (2015).
pubmed: 26638776 pmcid: 4686820 doi: 10.1038/ncomms9866
Puente, X. S. et al. Non-coding recurrent mutations in chronic lymphocytic leukaemia. Nature 526, 519–524 (2015).
pubmed: 26200345 doi: 10.1038/nature14666 pmcid: 26200345
Mesin, L., Ersching, J. & Victora, G. D. Germinal center B cell dynamics. Immunity 45, 471–482 (2016).
pubmed: 27653600 pmcid: 5123673 doi: 10.1016/j.immuni.2016.09.001
Puig, N. et al. The predominant myeloma clone at diagnosis, CDR3 defined, is constantly detectable across all stages of disease evolution. Leukemia 29, 1435–1437 (2015).
pubmed: 25567133 doi: 10.1038/leu.2015.7 pmcid: 25567133
Rustad, E. H. et al. Stability and uniqueness of clonal immunoglobulin CDR3 sequences for MRD tracking in multiple myeloma. Am. J. Hematol. 94, 1364–1373 (2019).
pubmed: 31571261 doi: 10.1002/ajh.25641 pmcid: 31571261
Pasqualucci, L. et al. Expression of the AID protein in normal and neoplastic B cells. Blood 104, 3318–3325 (2004).
pubmed: 15304391 doi: 10.1182/blood-2004-04-1558 pmcid: 15304391
Ledergor, G. et al. Single cell dissection of plasma cell heterogeneity in symptomatic and asymptomatic myeloma. Nat. Med. 24, 1867–1876 (2018).
pubmed: 30523328 doi: 10.1038/s41591-018-0269-2 pmcid: 30523328
Maura, F. et al. Role of AID in the temporal pattern of acquisition of driver mutations in multiple myeloma. Leukemia https://doi.org/10.1038/s41375-019-0689-0 (2019).
Lee-Six, H. et al. The landscape of somatic mutation in normal colorectal epithelial cells. Nature 574, 532–537 (2019).
pubmed: 31645730 doi: 10.1038/s41586-019-1672-7 pmcid: 31645730
Moore, L. et al. The mutational landscape of normal human endometrial epithelium. Preprint at https://doi.org/10.1101/505685 (Nature, 2018).
Rasche, L. et al. Spatial genomic heterogeneity in multiple myeloma revealed by multi-region sequencing. Nat. Commun. 8, 268 (2017).
pubmed: 28814763 pmcid: 5559527 doi: 10.1038/s41467-017-00296-y
Attal, M. et al. Lenalidomide, bortezomib, and dexamethasone with transplantation for myeloma. N. Engl. J. Med. 376, 1311–1320 (2017).
pubmed: 28379796 pmcid: 6201242 doi: 10.1056/NEJMoa1611750
Pich, O. et al. The mutational footprints of cancer therapies. Nat. Genet. 51, 1732–1740 (2019).
pubmed: 31740835 doi: 10.1038/s41588-019-0525-5 pmcid: 31740835
Wuillème, S. et al. Assessment of tumoral plasma cells in apheresis products for autologous stem cell transplantation in multiple myeloma. Bone Marrow Transplant. 51, 1143–1145 (2016).
pubmed: 27042840 doi: 10.1038/bmt.2016.74 pmcid: 27042840
Radivoyevitch, T. et al. Risk of acute myeloid leukemia and myelodysplastic syndrome after autotransplants for lymphomas and plasma cell myeloma. Leuk. Res. 74, 130–136 (2018).
pubmed: 30055822 pmcid: 6219911 doi: 10.1016/j.leukres.2018.07.016
Cowan, G. et al. Massive parallel IGHV gene sequencing reveals a germinal center pathway in origins of human multiple myeloma. Oncotarget 6, 13229–13240 (2015).
pubmed: 25929340 pmcid: 4537010 doi: 10.18632/oncotarget.3644
Sungalee, S. et al. Germinal center reentries of BCL2-overexpressing B cells drive follicular lymphoma progression. J. Clin. Invest. 124, 5337–5351 (2014).
pubmed: 25384217 pmcid: 4348942 doi: 10.1172/JCI72415
Nair, S. et al. Clonal immunoglobulin against lysolipids in the origin of myeloma. N. Engl. J. Med. 374, 555–561 (2016).
pubmed: 26863356 pmcid: 4804194 doi: 10.1056/NEJMoa1508808
Nair, S. et al. Antigen-mediated regulation in monoclonal gammopathies and myeloma. JCI insight https://doi.org/10.1172/jci.insight.98259 (2018).
Landgren, O. et al. Monoclonal gammopathy of undetermined significance (MGUS) consistently precedes multiple myeloma: a prospective study. Blood 113, 5412–5417 (2009).
pubmed: 19179464 pmcid: 2689042 doi: 10.1182/blood-2008-12-194241
Rajkumar, S. V. et al. International Myeloma Working Group updated criteria for the diagnosis of multiple myeloma. Lancet Oncol. 15, e538–e548 (2014).
doi: 10.1016/S1470-2045(14)70442-5
Murray, D. et al. in International Myeloma Workshop. https://www.ncbi.nlm.nih.gov/pubmed/31836698 (2019).
Deshwar, A. G. et al. PhyloWGS: reconstructing subclonal composition and evolution from whole-genome sequencing of tumors. Genome Biol. 16, 35 (2015).
pubmed: 25786235 pmcid: 4359439 doi: 10.1186/s13059-015-0602-8
Cibulskis, K. et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31, 213–219 (2013).
pubmed: 3833702 pmcid: 3833702 doi: 10.1038/nbt.2514
Jones, D. et al. cgpCaVEManWrapper: simple execution of CaVEMan in order to detect somatic single nucleotide variants in NGS data. Curr. Protoc. Bioinformatics 56, 15.10.11–15.10.18 (2016).
Fan, Y. et al. MuSE: accounting for tumor heterogeneity using a sample-specific error model improves sensitivity and specificity in mutation calling from sequencing data. Genome Biol. 17, 178 (2016).
pubmed: 27557938 pmcid: 4995747 doi: 10.1186/s13059-016-1029-6
Campbell, P. J. et al. Pan-cancer analysis of whole genomes. Nature 578, 82–93 (2020).
doi: 10.1038/s41586-020-1969-6
Jin, Y. et al. Active enhancer and chromatin accessibility landscapes chart the regulatory network of primary multiple myeloma. Blood 10, 2138–2150 (2018).
doi: 10.1182/blood-2017-09-808063

Auteurs

Even H Rustad (EH)

Myeloma Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Venkata Yellapantula (V)

Myeloma Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Daniel Leongamornlert (D)

The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.

Niccolò Bolli (N)

Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.
Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Guy Ledergor (G)

Division of Hematology/Oncology, Department of Medicine, University of California, San Francisco, CA, USA.

Ferran Nadeu (F)

Patologia Molecular de Neoplàsies Limfoides, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), 08036, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Cáncer (CIBERONC), 28029, Madrid, Spain.

Nicos Angelopoulos (N)

The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.

Kevin J Dawson (KJ)

The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.

Thomas J Mitchell (TJ)

The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.

Robert J Osborne (RJ)

The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.

Bachisio Ziccheddu (B)

Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.
Department of Molecular Biotechnologies and Health Sciences, University of Turin, Turin, Italy.

Cristiana Carniti (C)

Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Vittorio Montefusco (V)

Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Paolo Corradini (P)

Department of Oncology and Hemato-Oncology, University of Milan, Milan, Italy.
Department of Medical Oncology and Hematology, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Kenneth C Anderson (KC)

Jerome Lipper Multiple Myeloma Center, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.

Philippe Moreau (P)

CRCINA, SIRIC ILIAD, University Hospital of Nantes, Nantes, France.

Elli Papaemmanuil (E)

Computational Oncology Service, Department of Epidemiology & Biostatistics, Center for Computational Oncology, Memorial Sloan Kettering Cancer Center, New York, NY, 10065, USA.

Ludmil B Alexandrov (LB)

Department of Cellular and Molecular Medicine and Department of Bioengineering and Moores Cancer Center, University of California, La Jolla, San Diego, CA, USA.

Xose S Puente (XS)

Unitat Hematopatologia, Hospital Clínic of Barcelona, Universitat de Barcelona, 08036, Barcelona, Spain.
Departamento de Bioquimica y Biologia Molecular, Instituto Universitario de Oncologia (IUOPA), Universidad de Oviedo, Oviedo, Spain.

Elias Campo (E)

Patologia Molecular de Neoplàsies Limfoides, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), 08036, Barcelona, Spain.
Centro de Investigación Biomédica en Red de Cáncer (CIBERONC), 28029, Madrid, Spain.
Unitat Hematopatologia, Hospital Clínic of Barcelona, Universitat de Barcelona, 08036, Barcelona, Spain.

Reiner Siebert (R)

Institute of Human Genetics, Ulm University and Ulm University Medical Center, Ulm, Germany.

Herve Avet-Loiseau (H)

IUC-Oncopole, and CRCT INSERM U1037, 31100, Toulouse, France.

Ola Landgren (O)

Myeloma Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.

Nikhil Munshi (N)

Jerome Lipper Multiple Myeloma Center, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.
Veterans Administration Boston Healthcare System, West Roxbury, MA, USA.

Peter J Campbell (PJ)

The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK.

Francesco Maura (F)

Myeloma Service, Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA. mauraf@mskcc.org.
The Cancer, Ageing and Somatic Mutation Programme, Wellcome Sanger Institute, Hinxton, Cambridgeshire, CB10 1SA, UK. mauraf@mskcc.org.

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