IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32145-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32145-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-32145-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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. 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.
    3. 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.
    4. 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.
    5. Francesco Maura & Niccoló Bolli & Nicos Angelopoulos & Kevin J. Dawson & Daniel Leongamornlert & Inigo Martincorena & Thomas J. Mitchell & Anthony Fullam & Santiago Gonzalez & Raphael Szalat & Federic, 2019. "Genomic landscape and chronological reconstruction of driver events in multiple myeloma," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Mark Bustoros & Shankara Anand & Romanos Sklavenitis-Pistofidis & Robert Redd & Eileen M. Boyle & Benny Zhitomirsky & Andrew J. Dunford & Yu-Tzu Tai & Selina J. Chavda & Cody Boehner & Carl Jannes Neu, 2022. "Genetic subtypes of smoldering multiple myeloma are associated with distinct pathogenic phenotypes and clinical outcomes," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Lukas John & Alexandra M. Poos & Alexander Brobeil & Carolina Schinke & Stefanie Huhn & Nina Prokoph & Raphael Lutz & Barbara Wagner & Maurizio Zangari & Stephan M. Tirier & Jan-Philipp Mallm & Sabrin, 2023. "Resolving the spatial architecture of myeloma and its microenvironment at the single-cell level," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. S. Mouron & M. J. Bueno & A. Lluch & L. Manso & I. Calvo & J. Cortes & J. A. Garcia-Saenz & M. Gil-Gil & N. Martinez-Janez & J. V. Apala & E. Caleiras & Pilar Ximénez-Embún & J. Muñoz & L. Gonzalez-Co, 2022. "Phosphoproteomic analysis of neoadjuvant breast cancer suggests that increased sensitivity to paclitaxel is driven by CDK4 and filamin A," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    4. Yanis Tazi & Juan E. Arango-Ossa & Yangyu Zhou & Elsa Bernard & Ian Thomas & Amanda Gilkes & Sylvie Freeman & Yoann Pradat & Sean J. Johnson & Robert Hills & Richard Dillon & Max F. Levine & Daniel Le, 2022. "Unified classification and risk-stratification in Acute Myeloid Leukemia," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. David G. Coffey & Francesco Maura & Edgar Gonzalez-Kozlova & J. Javier Diaz-Mejia & Ping Luo & Yong Zhang & Yuexin Xu & Edus H. Warren & Travis Dawson & Brian Lee & Hui Xie & Eric Smith & Amanda Ciard, 2023. "Immunophenotypic correlates of sustained MRD negativity in patients with multiple myeloma," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Luan Nguyen & Arne Hoeck & Edwin Cuppen, 2022. "Machine learning-based tissue of origin classification for cancer of unknown primary diagnostics using genome-wide mutation features," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    7. Danielle C. Croucher & Laura M. Richards & Serges P. Tsofack & Daniel Waller & Zhihua Li & Ellen Nong Wei & Xian Fang Huang & Marta Chesi & P. Leif Bergsagel & Michael Sebag & Trevor J. Pugh & Suzanne, 2021. "Longitudinal single-cell analysis of a myeloma mouse model identifies subclonal molecular programs associated with progression," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    8. Zhe Jiang & YoungJun Ju & Amjad Ali & Philip E. D. Chung & Patryk Skowron & Dong-Yu Wang & Mariusz Shrestha & Huiqin Li & Jeff C. Liu & Ioulia Vorobieva & Ronak Ghanbari-Azarnier & Ethel Mwewa & Maria, 2023. "Distinct shared and compartment-enriched oncogenic networks drive primary versus metastatic breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    9. Karama Asleh & Gian Luca Negri & Sandra E. Spencer Miko & Shane Colborne & Christopher S. Hughes & Xiu Q. Wang & Dongxia Gao & C. Blake Gilks & Stephen K. L. Chia & Torsten O. Nielsen & Gregg B. Morin, 2022. "Proteomic analysis of archival breast cancer clinical specimens identifies biological subtypes with distinct survival outcomes," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    10. Naser Ansari-Pour & Yonglan Zheng & Toshio F. Yoshimatsu & Ayodele Sanni & Mustapha Ajani & Jean-Baptiste Reynier & Avraam Tapinos & Jason J. Pitt & Stefan Dentro & Anna Woodard & Padma Sheila Rajagop, 2021. "Whole-genome analysis of Nigerian patients with breast cancer reveals ethnic-driven somatic evolution and distinct genomic subtypes," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    11. Maximilian Merz & Almuth Maria Anni Merz & Jie Wang & Lei Wei & Qiang Hu & Nicholas Hutson & Cherie Rondeau & Kimberly Celotto & Ahmed Belal & Ronald Alberico & AnneMarie W. Block & Hemn Mohammadpour , 2022. "Deciphering spatial genomic heterogeneity at a single cell resolution in multiple myeloma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Rebecca Boiarsky & Nicholas J. Haradhvala & Jean-Baptiste Alberge & Romanos Sklavenitis-Pistofidis & Tarek H. Mouhieddine & Oksana Zavidij & Ming-Chieh Shih & Danielle Firer & Mendy Miller & Habib El-, 2022. "Single cell characterization of myeloma and its precursor conditions reveals transcriptional signatures of early tumorigenesis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Carolina Terragna & Andrea Poletti & Vincenza Solli & Marina Martello & Elena Zamagni & Lucia Pantani & Enrica Borsi & Ilaria Vigliotta & Gaia Mazzocchetti & Silvia Armuzzi & Barbara Taurisano & Nicol, 2024. "Multi-dimensional scaling techniques unveiled gain1q&loss13q co-occurrence in Multiple Myeloma patients with specific genomic, transcriptional and adverse clinical features," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32145-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.