IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41434-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41434-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41434-z?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. 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. 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.
    3. 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.
    4. 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.
    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.
    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. Tianyu Zhu & Huige Tong & Zhaozhen Du & Stephan Beck & Andrew E. Teschendorff, 2024. "An improved epigenetic counter to track mitotic age in normal and precancerous tissues," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. S. John Liu & Tim Casey-Clyde & Nam Woo Cho & Jason Swinderman & Melike Pekmezci & Mark C. Dougherty & Kyla Foster & William C. Chen & Javier E. Villanueva-Meyer & Danielle L. Swaney & Harish N. Vasud, 2024. "Epigenetic reprogramming shapes the cellular landscape of schwannoma," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Kobe Ridder & Huiwen Che & Kaat Leroy & Bernard Thienpont, 2024. "Benchmarking of methods for DNA methylome deconvolution," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Maria Pouyiourou & Bianca N. Kraft & Timothy Wohlfromm & Michael Stahl & Boris Kubuschok & Harald Löffler & Ulrich T. Hacker & Gerdt Hübner & Lena Weiss & Michael Bitzer & Thomas Ernst & Philipp Schüt, 2023. "Nivolumab and ipilimumab in recurrent or refractory cancer of unknown primary: a phase II trial," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    5. Marjan M. Naeini & Felicity Newell & Lauren G. Aoude & Vanessa F. Bonazzi & Kalpana Patel & Guy Lampe & Lambros T. Koufariotis & Vanessa Lakis & Venkateswar Addala & Olga Kondrashova & Rebecca L. John, 2023. "Multi-omic features of oesophageal adenocarcinoma in patients treated with preoperative neoadjuvant therapy," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Xi Lu & Naga Prathyusha Maturi & Malin Jarvius & Irem Yildirim & Yonglong Dang & Linxuan Zhao & Yuan Xie & E-Jean Tan & Pengwei Xing & Rolf Larsson & Mårten Fryknäs & Lene Uhrbom & Xingqi Chen, 2022. "Cell-lineage controlled epigenetic regulation in glioblastoma stem cells determines functionally distinct subgroups and predicts patient survival," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    7. Claire Vinel & Gabriel Rosser & Loredana Guglielmi & Myrianni Constantinou & Nicola Pomella & Xinyu Zhang & James R. Boot & Tania A. Jones & Thomas O. Millner & Anaelle A. Dumas & Vardhman Rakyan & Je, 2021. "Comparative epigenetic analysis of tumour initiating cells and syngeneic EPSC-derived neural stem cells in glioblastoma," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    8. Peng Dai & Lucia Ruojia Wu & Sherry Xi Chen & Michael Xiangjiang Wang & Lauren Yuxuan Cheng & Jinny Xuemeng Zhang & Pengying Hao & Weijie Yao & Jabra Zarka & Ghayas C. Issa & Lawrence Kwong & David Yu, 2021. "Calibration-free NGS quantitation of mutations below 0.01% VAF," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    9. Kate E. Stanley & Tatjana Jatsenko & Stefania Tuveri & Dhanya Sudhakaran & Lore Lannoo & Kristel Calsteren & Marie Borre & Ilse Parijs & Leen Coillie & Kris Bogaert & Rodrigo Almeida Toledo & Liesbeth, 2024. "Cell type signatures in cell-free DNA fragmentation profiles reveal disease biology," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Michaël Noë & Dimitrios Mathios & Akshaya V. Annapragada & Shashikant Koul & Zacharia H. Foda & Jamie E. Medina & Stephen Cristiano & Christopher Cherry & Daniel C. Bruhm & Noushin Niknafs & Vilmos Ad, 2024. "DNA methylation and gene expression as determinants of genome-wide cell-free DNA fragmentation," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    11. Danni A. Gadd & Robert F. Hillary & Daniel L. McCartney & Liu Shi & Aleks Stolicyn & Neil A. Robertson & Rosie M. Walker & Robert I. McGeachan & Archie Campbell & Shen Xueyi & Miruna C. Barbu & Claire, 2022. "Integrated methylome and phenome study of the circulating proteome reveals markers pertinent to brain health," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. Ankur Chakravarthy & Ian Reddin & Stephen Henderson & Cindy Dong & Nerissa Kirkwood & Maxmilan Jeyakumar & Daniela Rothschild Rodriguez & Natalia Gonzalez Martinez & Jacqueline McDermott & Xiaoping Su, 2022. "Integrated analysis of cervical squamous cell carcinoma cohorts from three continents reveals conserved subtypes of prognostic significance," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    13. Yaping Liu & Sarah C. Reed & Christopher Lo & Atish D. Choudhury & Heather A. Parsons & Daniel G. Stover & Gavin Ha & Gregory Gydush & Justin Rhoades & Denisse Rotem & Samuel Freeman & David W. Katz &, 2024. "FinaleMe: Predicting DNA methylation by the fragmentation patterns of plasma cell-free DNA," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    14. Lucia Ruojia Wu & Peng Dai & Michael Xiangjiang Wang & Sherry Xi Chen & Evan N. Cohen & Gitanjali Jayachandran & Jinny Xuemeng Zhang & Angela V. Serrano & Nina Guanyi Xie & Naoto T. Ueno & James M. Re, 2022. "Ensemble of nucleic acid absolute quantitation modules for copy number variation detection and RNA profiling," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    15. Mark W. Youngblood & Zeynep Erson-Omay & Chang Li & Hinda Najem & Süleyman Coșkun & Evgeniya Tyrtova & Julio D. Montejo & Danielle F. Miyagishima & Tanyeri Barak & Sayoko Nishimura & Akdes Serin Harma, 2023. "Super-enhancer hijacking drives ectopic expression of hedgehog pathway ligands in meningiomas," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Caroline Hoffmann & Floriane Noel & Maximilien Grandclaudon & Lucile Massenet-Regad & Paula Michea & Philemon Sirven & Lilith Faucheux & Aurore Surun & Olivier Lantz & Mylene Bohec & Jian Ye & Weihua , 2022. "PD-L1 and ICOSL discriminate human Secretory and Helper dendritic cells in cancer, allergy and autoimmunity," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    17. Harish N. Vasudevan & Emily Payne & Cyrille L. Delley & S. John Liu & Kanish Mirchia & Matthew J. Sale & Sydney Lastella & Maria Sacconi Nunez & Calixto-Hope G. Lucas & Charlotte D. Eaton & Tim Casey-, 2024. "Functional interactions between neurofibromatosis tumor suppressors underlie Schwann cell tumor de-differentiation and treatment resistance," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    18. Alicia-Marie Conway & Simon P. Pearce & Alexandra Clipson & Steven M. Hill & Francesca Chemi & Dan Slane-Tan & Saba Ferdous & A. S. Md Mukarram Hossain & Katarzyna Kamieniecka & Daniel J. White & Clai, 2024. "A cfDNA methylation-based tissue-of-origin classifier for cancers of unknown primary," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    19. Xiao Zhou & Zhen Cheng & Mingyu Dong & Qi Liu & Weiyang Yang & Min Liu & Junzhang Tian & Weibin Cheng, 2022. "Tumor fractions deciphered from circulating cell-free DNA methylation for cancer early diagnosis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    20. Marc Cicero Schubert & Stella Judith Soyka & Amr Tamimi & Emanuel Maus & Julian Schroers & Niklas Wißmann & Ekin Reyhan & Svenja Kristin Tetzlaff & Yvonne Yang & Robert Denninger & Robin Peretzke & Ca, 2024. "Deep intravital brain tumor imaging enabled by tailored three-photon microscopy and analysis," Nature Communications, Nature, vol. 15(1), pages 1-21, 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:14:y:2023:i:1:d:10.1038_s41467-023-41434-z. 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.