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The spatio-temporal evolution of multiple myeloma from baseline to relapse-refractory states

Author

Listed:
  • Leo Rasche

    (University of Arkansas for Medical Sciences
    University Hospital of Würzburg
    University Hospital of Würzburg)

  • Carolina Schinke

    (University of Arkansas for Medical Sciences)

  • Francesco Maura

    (University of Miami)

  • Michael A. Bauer

    (University of Arkansas for Medical Sciences)

  • Cody Ashby

    (University of Arkansas for Medical Sciences)

  • Shayu Deshpande

    (University of Arkansas for Medical Sciences)

  • Alexandra M. Poos

    (University Hospital of Heidelberg)

  • Maurizio Zangari

    (University of Arkansas for Medical Sciences)

  • Sharmilan Thanendrarajan

    (University of Arkansas for Medical Sciences)

  • Faith E. Davies

    (New York University Langone Health)

  • Brian A. Walker

    (Indiana University)

  • Bart Barlogie

    (University of Arkansas for Medical Sciences)

  • Ola Landgren

    (University of Miami)

  • Gareth J. Morgan

    (New York University Langone Health)

  • Frits Rhee

    (University of Arkansas for Medical Sciences)

  • Niels Weinhold

    (University of Arkansas for Medical Sciences
    University Hospital of Heidelberg)

Abstract

Deciphering Multiple Myeloma evolution in the whole bone marrow is key to inform curative strategies. Here, we perform spatial-longitudinal whole-exome sequencing, including 140 samples collected from 24 Multiple Myeloma patients during up to 14 years. Applying imaging-guided sampling we observe three evolutionary patterns, including relapse driven by a single-cell expansion, competing/co-existing sub-clones, and unique sub-clones at distinct locations. While we do not find the unique relapse sub-clone in the baseline focal lesion(s), we show a close phylogenetic relationship between baseline focal lesions and relapse disease, highlighting focal lesions as hotspots of tumor evolution. In patients with ≥3 focal lesions on positron-emission-tomography at diagnosis, relapse is driven by multiple distinct sub-clones, whereas in other patients, a single-cell expansion is typically seen (p

Suggested Citation

  • Leo Rasche & Carolina Schinke & Francesco Maura & Michael A. Bauer & Cody Ashby & Shayu Deshpande & Alexandra M. Poos & Maurizio Zangari & Sharmilan Thanendrarajan & Faith E. Davies & Brian A. Walker , 2022. "The spatio-temporal evolution of multiple myeloma from baseline to relapse-refractory states," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32145-y
    DOI: 10.1038/s41467-022-32145-y
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    References listed on IDEAS

    as
    1. Niccolò Bolli & Francesco Maura & Stephane Minvielle & Dominik Gloznik & Raphael Szalat & Anthony Fullam & Inigo Martincorena & Kevin J. Dawson & Mehmet Kemal Samur & Jorge Zamora & Patrick Tarpey & H, 2018. "Genomic patterns of progression in smoldering multiple myeloma," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    2. Heather J. Landau & Venkata Yellapantula & Benjamin T. Diamond & Even H. Rustad & Kylee H. Maclachlan & Gunes Gundem & Juan Medina-Martinez & Juan Arango Ossa & Max F. Levine & Yangyu Zhou & Rajya Kap, 2021. "Author Correction: Accelerated single cell seeding in relapsed multiple myeloma," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    3. Niccolo Bolli & Hervé Avet-Loiseau & David C. Wedge & Peter Van Loo & Ludmil B. Alexandrov & Inigo Martincorena & Kevin J. Dawson & Francesco Iorio & Serena Nik-Zainal & Graham R. Bignell & Jonathan W, 2014. "Heterogeneity of genomic evolution and mutational profiles in multiple myeloma," Nature Communications, Nature, vol. 5(1), pages 1-13, May.
    4. Philip J. Stephens & Patrick S. Tarpey & Helen Davies & Peter Van Loo & Chris Greenman & David C. Wedge & Serena Nik-Zainal & Sancha Martin & Ignacio Varela & Graham R. Bignell & Lucy R. Yates & Elli , 2012. "The landscape of cancer genes and mutational processes in breast cancer," Nature, Nature, vol. 486(7403), pages 400-404, June.
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    6. L. Rasche & S. S. Chavan & O. W. Stephens & P. H. Patel & R. Tytarenko & C. Ashby & M. Bauer & C. Stein & S. Deshpande & C. Wardell & T. Buzder & G. Molnar & M. Zangari & F. Rhee & S. Thanendrarajan &, 2017. "Spatial genomic heterogeneity in multiple myeloma revealed by multi-region sequencing," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    7. Eileen M. Boyle & Shayu Deshpande & Ruslana Tytarenko & Cody Ashby & Yan Wang & Michael A. Bauer & Sarah K. Johnson & Christopher P. Wardell & Sharmilan Thanendrarajan & Maurizio Zangari & Thierry Fac, 2021. "The molecular make up of smoldering myeloma highlights the evolutionary pathways leading to multiple myeloma," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
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