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Detection of diagnostic and prognostic methylation-based signatures in liquid biopsy specimens from patients with meningiomas

Author

Listed:
  • Grayson A. Herrgott

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • James M. Snyder

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Ruicong She

    (Biostatistics, Henry Ford Health)

  • Tathiane M. Malta

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Thais S. Sabedot

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Ian Y. Lee

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Jacob Pawloski

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Guilherme G. Podolsky-Gondim

    (University of Sao Paulo)

  • Karam P. Asmaro

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Jiaqi Zhang

    (Biostatistics, Henry Ford Health)

  • Cara E. Cannella

    (Biostatistics, Henry Ford Health)

  • Kevin Nelson

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Bartow Thomas

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Ana C. deCarvalho

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Laura A. Hasselbach

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Kelly M. Tundo

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Rehnuma Newaz

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Andrea Transou

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Natalia Morosini

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Victor Francisco

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Laila M. Poisson

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health
    Biostatistics, Henry Ford Health)

  • Dhananjay Chitale

    (Henry Ford Health)

  • Abir Mukherjee

    (Henry Ford Health)

  • Maritza S. Mosella

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Adam M. Robin

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Tobias Walbert

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Mark Rosenblum

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Tom Mikkelsen

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Steven Kalkanis

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Daniela P. C. Tirapelli

    (University of Sao Paulo)

  • Daniel J. Weisenberger

    (University of Southern California)

  • Carlos G. Carlotti

    (University of Sao Paulo)

  • Jack Rock

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health)

  • Ana Valeria Castro

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health
    Michigan State University)

  • Houtan Noushmehr

    (Omics Laboratory, Hermelin Brain Tumor Center, Henry Ford Health
    Michigan State University)

Abstract

Recurrence of meningiomas is unpredictable by current invasive methods based on surgically removed specimens. Identification of patients likely to recur using noninvasive approaches could inform treatment strategy, whether intervention or monitoring. In this study, we analyze the DNA methylation levels in blood (serum and plasma) and tissue samples from 155 meningioma patients, compared to other central nervous system tumor and non-tumor entities. We discover DNA methylation markers unique to meningiomas and use artificial intelligence to create accurate and universal models for identifying and predicting meningioma recurrence, using either blood or tissue samples. Here we show that liquid biopsy is a potential noninvasive and reliable tool for diagnosing and predicting outcomes in meningioma patients. This approach can improve personalized management strategies for these patients.

Suggested Citation

  • Grayson A. Herrgott & James M. Snyder & Ruicong She & Tathiane M. Malta & Thais S. Sabedot & Ian Y. Lee & Jacob Pawloski & Guilherme G. Podolsky-Gondim & Karam P. Asmaro & Jiaqi Zhang & Cara E. Cannel, 2023. "Detection of diagnostic and prognostic methylation-based signatures in liquid biopsy specimens from patients with meningiomas," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41434-z
    DOI: 10.1038/s41467-023-41434-z
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    References listed on IDEAS

    as
    1. Farshad Nassiri & Jeff Liu & Vikas Patil & Yasin Mamatjan & Justin Z. Wang & Rupert Hugh-White & Andrew M. Macklin & Shahbaz Khan & Olivia Singh & Shirin Karimi & Rosario I. Corona & Lydia Y. Liu & Ca, 2021. "A clinically applicable integrative molecular classification of meningiomas," Nature, Nature, vol. 597(7874), pages 119-125, September.
    2. David Capper & David T. W. Jones & Martin Sill & Volker Hovestadt & Daniel Schrimpf & Dominik Sturm & Christian Koelsche & Felix Sahm & Lukas Chavez & David E. Reuss & Annekathrin Kratz & Annika K. We, 2018. "DNA methylation-based classification of central nervous system tumours," Nature, Nature, vol. 555(7697), pages 469-474, March.
    3. Hong-Tao Li & Liya Xu & Daniel J. Weisenberger & Meng Li & Wanding Zhou & Chen-Ching Peng & Kevin Stachelek & David Cobrinik & Gangning Liang & Jesse L. Berry, 2022. "Characterizing DNA methylation signatures of retinoblastoma using aqueous humor liquid biopsy," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    4. Joshua Moss & Judith Magenheim & Daniel Neiman & Hai Zemmour & Netanel Loyfer & Amit Korach & Yaacov Samet & Myriam Maoz & Henrik Druid & Peter Arner & Keng-Yeh Fu & Endre Kiss & Kirsty L. Spalding & , 2018. "Comprehensive human cell-type methylation atlas reveals origins of circulating cell-free DNA in health and disease," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    5. Lucas A. Salas & Ze Zhang & Devin C. Koestler & Rondi A. Butler & Helen M. Hansen & Annette M. Molinaro & John K. Wiencke & Karl T. Kelsey & Brock C. Christensen, 2022. "Enhanced cell deconvolution of peripheral blood using DNA methylation for high-resolution immune profiling," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Ankur Chakravarthy & Andrew Furness & Kroopa Joshi & Ehsan Ghorani & Kirsty Ford & Matthew J. Ward & Emma V. King & Matt Lechner & Teresa Marafioti & Sergio A. Quezada & Gareth J. Thomas & Andrew Febe, 2018. "Pan-cancer deconvolution of tumour composition using DNA methylation," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
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