Sarcoma classification by DNA methylation profiling

Christian Koelsche; Daniel Schrimpf; Damian Stichel; Martin Sill; Felix Sahm; David E. Reuss; Mirjam Blattner; Barbara Worst; Christoph E. Heilig; Katja Beck; Peter Horak; Simon Kreutzfeldt; Elke Paff; Sebastian Stark; Pascal Johann; Florian Selt; Jonas Ecker; Dominik Sturm; Kristian W. Pajtler; Annekathrin Reinhardt; Annika K. Wefers; Philipp Sievers; Azadeh Ebrahimi; Abigail Suwala; Francisco Fernández-Klett; Belén Casalini; Andrey Korshunov; Volker Hovestadt; Felix K. F. Kommoss; Mark Kriegsmann; Matthias Schick; Melanie Bewerunge-Hudler; Till Milde; Olaf Witt; Andreas E. Kulozik; Marcel Kool; Laura Romero-Pérez; Thomas G. P. Grünewald; Thomas Kirchner; Wolfgang Wick; Michael Platten; Andreas Unterberg; Matthias Uhl; Amir Abdollahi; J. rgen Debus; Burkhard Lehner; Christian Thomas; Martin Hasselblatt; Werner Paulus; Christian Hartmann; Ori Staszewski; Marco Prinz; J. rgen Hench; Stephan Frank; Yvonne M. H. Versleijen-Jonkers; Marije E. Weidema; Thomas Mentzel; Klaus Griewank; Enrique de Álava; Juan D. az Martín; Miguel A. Idoate Gastearena; Kenneth Tou-En Chang; Sharon Yin Yee Low; Adrian Cuevas-Bourdier; Michel Mittelbronn; Martin Mynarek; Stefan Rutkowski; Ulrich Schüller; Viktor F. Mautner; Jens Schittenhelm; Jonathan Serrano; Matija Snuderl; Reinhard Büttner; Thomas Klingebiel; Rolf Buslei; Manfred Gessler; Pieter Wesseling; Winand N. M. Dinjens; Sebastian Brandner; Zane Jaunmuktane; Iben Lyskjær; Peter Schirmacher; Albrecht Stenzinger; Benedikt Brors; Hanno Glimm; Christoph Heining; Oscar M. Tirado; Miguel Sáinz-Jaspeado; Jaume Mora; Javier Alonso; Xavier Garcia del Muro; Sebastian Moran; Manel Esteller; Jamal K. Benhamida; Marc Ladanyi; Eva Wardelmann; Cristina Antonescu; Adrienne Flanagan; Uta Dirksen; Peter Hohenberger; Daniel Baumhoer; Wolfgang Hartmann; Christian Vokuhl; Uta Flucke; Iver Petersen; Gunhild Mechtersheimer; David Capper; David T. W. Jones; Stefan Fröhling; Stefan M. Pfister; Andreas von Deimling

doi:10.1038/s41467-020-20603-4

Sarcoma classification by DNA methylation profiling

Christian Koelsche
, Daniel Schrimpf
, Damian Stichel
, Martin Sill
, Felix Sahm
, David E. Reuss
, Mirjam Blattner
, Barbara Worst
, Christoph E. Heilig
, Katja Beck
, Peter Horak
, Simon Kreutzfeldt
, Elke Paff
, Sebastian Stark
, Pascal Johann
, Florian Selt
, Jonas Ecker
, Dominik Sturm
, Kristian W. Pajtler
, Annekathrin Reinhardt

Annika K. Wefers, Philipp Sievers, Azadeh Ebrahimi, Abigail Suwala, Francisco Fernández-Klett, Belén Casalini, Andrey Korshunov, Volker Hovestadt, Felix K. F. Kommoss, Mark Kriegsmann, Matthias Schick, Melanie Bewerunge-Hudler, Till Milde, Olaf Witt, Andreas E. Kulozik, Marcel Kool, Laura Romero-Pérez, Thomas G. P. Grünewald, Thomas Kirchner, Wolfgang Wick, Michael Platten, Andreas Unterberg, Matthias Uhl, Amir Abdollahi, J. rgen Debus, Burkhard Lehner, Christian Thomas, Martin Hasselblatt, Werner Paulus, Christian Hartmann, Ori Staszewski, Marco Prinz, J. rgen Hench, Stephan Frank, Yvonne M. H. Versleijen-Jonkers, Marije E. Weidema, Thomas Mentzel, Klaus Griewank, Enrique de Álava, Juan D. az Martín, Miguel A. Idoate Gastearena, Kenneth Tou-En Chang, Sharon Yin Yee Low, Adrian Cuevas-Bourdier, Michel Mittelbronn, Martin Mynarek, Stefan Rutkowski, Ulrich Schüller, Viktor F. Mautner, Jens Schittenhelm, Jonathan Serrano, Matija Snuderl, Reinhard Büttner, Thomas Klingebiel, Rolf Buslei, Manfred Gessler, Pieter Wesseling, Winand N. M. Dinjens, Sebastian Brandner, Zane Jaunmuktane, Iben Lyskjær, Peter Schirmacher, Albrecht Stenzinger, Benedikt Brors, Hanno Glimm, Christoph Heining, Oscar M. Tirado, Miguel Sáinz-Jaspeado, Jaume Mora, Javier Alonso, Xavier Garcia del Muro, Sebastian Moran, Manel Esteller, Jamal K. Benhamida, Marc Ladanyi, Eva Wardelmann, Cristina Antonescu, Adrienne Flanagan, Uta Dirksen, Peter Hohenberger, Daniel Baumhoer, Wolfgang Hartmann, Christian Vokuhl, Uta Flucke, Iver Petersen, Gunhild Mechtersheimer, David Capper, David T. W. Jones, Stefan Fröhling, Stefan M. Pfister, Andreas von Deimling^*

^*Corresponding author for this work

German Cancer Research Center
Heidelberg University
Hopp Children’s Cancer Center Heidelberg (KiTZ), Heidelberg, Germany
Broad Institute
Harvard University
Ludwig Maximilian University of Munich
Heidelberg Institute of Radiation Oncology (HIRO), National Center for Radiation Research in Oncology (NCRO), Heidelberg, Germany
Heidelberg Ion-Beam Therapy Center (HIT), Heidelberg, Germany
University of Münster
Hannover Medical School
University of Freiburg
University of Basel
Radboud University Medical Center
Dermatopathology Bodensee, Friedrichshafen, Germany
University of Duisburg-Essen
Hospital Universitario Virgen del Rocio
University of Seville
University of Navarra
KK Women's and Children's Hospital
National Neuroscience Institute of Singapore
National Center of Pathology (NCP), Laboratoire National de Santé (LNS), Dudelange, Luxembourg
Luxembourg Center of Neuropathology (LCNP), Luxembourg, Luxembourg
University of Luxembourg
Luxembourg Institute of Health
University of Hamburg
University of Tübingen
New York University
University of Cologne
Department of Pediatric Hematology and Oncology, University Children’s Hospital, Frankfurt/Main, Germany
Institute of Pathology, Sozialstiftung Bamberg, Klinikum am Bruderwald, Bamberg, Germany
University of Würzburg
Princess Maxima Center for Pediatric Oncology, 3584 CS, Utrecht, The Netherlands
Amsterdam UMC - University of Amsterdam
Erasmus University Rotterdam
University College London
National Hospital for Neurology and Neurosurgery, London, United Kingdom
Technische Universität Dresden
German Cancer Consortium (DKTK), Dresden, Germany
Bellvitge Biomedical Research Institute
Department of Hematology and Oncology, Hospital Sant Joan de Déu, Barcelona, Spain
Instituto de Salud Carlos III
University of Barcelona
Josep Carreras Leukaemia Research Institute
Centro de Investigacion Biomedica en Red Cancer (CIBERONC), Madrid, Spain
ICREA
Memorial Sloan-Kettering Cancer Center
Royal National Orthopaedic Hospital NHS Trust
Kiel University
Institute of Pathology, SRH Poliklinik Gera GmbH, Gera, Germany
Friedrich Schiller University Jena
Charité – Universitätsmedizin Berlin
National Center for Tumor Diseases Heidelberg
Heidelberg University Hospital
Hopp Children’s Cancer Center Heidelberg (KiTZ)
Brigham and Women’s Hospital
National Center for Radiation Research in Oncology (NCRO)
University Hospital Münster
Albert-Ludwigs-University Freiburg
Radboud University Nijmegen
Luxembourg Centre of Neuropathology (LCNP)
University Medical Center Hamburg-Eppendorf
University Hospital of Cologne
Princess Máxima Center for Pediatric Oncology
University of Amsterdam
Great Ormond St Hospital for Children NHS Trust
Department of Pediatric Onco-Hematology and Developmental Tumor Biology Laboratory, Hospital Sant Joan de Déu, Barcelona, Catalonia, Spain

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Abstract

Sarcomas are malignant soft tissue and bone tumours affecting adults, adolescents and children. They represent a morphologically heterogeneous class of tumours and some entities lack defining histopathological features. Therefore, the diagnosis of sarcomas is burdened with a high inter-observer variability and misclassification rate. Here, we demonstrate classification of soft tissue and bone tumours using a machine learning classifier algorithm based on array-generated DNA methylation data. This sarcoma classifier is trained using a dataset of 1077 methylation profiles from comprehensively pre-characterized cases comprising 62 tumour methylation classes constituting a broad range of soft tissue and bone sarcoma subtypes across the entire age spectrum. The performance is validated in a cohort of 428 sarcomatous tumours, of which 322 cases were classified by the sarcoma classifier. Our results demonstrate the potential of the DNA methylation-based sarcoma classification for research and future diagnostic applications.

Original language	English
Article number	498
Journal	Nature communications
Volume	12
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-20603-4
Publication status	Published - 1 Dec 2021

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Sarcoma-classification-by-dna-methylation-profiling.pdfFinal published version, 2.38 MBLicence: CC BY

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Koelsche, C., Schrimpf, D., Stichel, D., Sill, M., Sahm, F., Reuss, D. E., Blattner, M., Worst, B., Heilig, C. E., Beck, K., Horak, P., Kreutzfeldt, S., Paff, E., Stark, S., Johann, P., Selt, F., Ecker, J., Sturm, D., Pajtler, K. W., ... von Deimling, A. (2021). Sarcoma classification by DNA methylation profiling. Nature communications, 12(1), Article 498. https://doi.org/10.1038/s41467-020-20603-4

@article{406f9ff2e80b4ae7aa49553a5d6b9ec7,

title = "Sarcoma classification by DNA methylation profiling",

abstract = "Sarcomas are malignant soft tissue and bone tumours affecting adults, adolescents and children. They represent a morphologically heterogeneous class of tumours and some entities lack defining histopathological features. Therefore, the diagnosis of sarcomas is burdened with a high inter-observer variability and misclassification rate. Here, we demonstrate classification of soft tissue and bone tumours using a machine learning classifier algorithm based on array-generated DNA methylation data. This sarcoma classifier is trained using a dataset of 1077 methylation profiles from comprehensively pre-characterized cases comprising 62 tumour methylation classes constituting a broad range of soft tissue and bone sarcoma subtypes across the entire age spectrum. The performance is validated in a cohort of 428 sarcomatous tumours, of which 322 cases were classified by the sarcoma classifier. Our results demonstrate the potential of the DNA methylation-based sarcoma classification for research and future diagnostic applications.",

author = "Christian Koelsche and Daniel Schrimpf and Damian Stichel and Martin Sill and Felix Sahm and Reuss, \{David E.\} and Mirjam Blattner and Barbara Worst and Heilig, \{Christoph E.\} and Katja Beck and Peter Horak and Simon Kreutzfeldt and Elke Paff and Sebastian Stark and Pascal Johann and Florian Selt and Jonas Ecker and Dominik Sturm and Pajtler, \{Kristian W.\} and Annekathrin Reinhardt and Wefers, \{Annika K.\} and Philipp Sievers and Azadeh Ebrahimi and Abigail Suwala and Francisco Fern{\'a}ndez-Klett and Bel{\'e}n Casalini and Andrey Korshunov and Volker Hovestadt and Kommoss, \{Felix K. F.\} and Mark Kriegsmann and Matthias Schick and Melanie Bewerunge-Hudler and Till Milde and Olaf Witt and Kulozik, \{Andreas E.\} and Marcel Kool and Laura Romero-P{\'e}rez and Gr{\"u}newald, \{Thomas G. P.\} and Thomas Kirchner and Wolfgang Wick and Michael Platten and Andreas Unterberg and Matthias Uhl and Amir Abdollahi and Debus, \{J. rgen\} and Burkhard Lehner and Christian Thomas and Martin Hasselblatt and Werner Paulus and Christian Hartmann and Ori Staszewski and Marco Prinz and Hench, \{J. rgen\} and Stephan Frank and Versleijen-Jonkers, \{Yvonne M. H.\} and Weidema, \{Marije E.\} and Thomas Mentzel and Klaus Griewank and \{de {\'A}lava\}, Enrique and Mart{\'i}n, \{Juan D. az\} and Gastearena, \{Miguel A. Idoate\} and Chang, \{Kenneth Tou-En\} and Low, \{Sharon Yin Yee\} and Adrian Cuevas-Bourdier and Michel Mittelbronn and Martin Mynarek and Stefan Rutkowski and Ulrich Sch{\"u}ller and Mautner, \{Viktor F.\} and Jens Schittenhelm and Jonathan Serrano and Matija Snuderl and Reinhard B{\"u}ttner and Thomas Klingebiel and Rolf Buslei and Manfred Gessler and Pieter Wesseling and Dinjens, \{Winand N. M.\} and Sebastian Brandner and Zane Jaunmuktane and Iben Lyskj{\ae}r and Peter Schirmacher and Albrecht Stenzinger and Benedikt Brors and Hanno Glimm and Christoph Heining and Tirado, \{Oscar M.\} and Miguel S{\'a}inz-Jaspeado and Jaume Mora and Javier Alonso and \{del Muro\}, \{Xavier Garcia\} and Sebastian Moran and Manel Esteller and Benhamida, \{Jamal K.\} and Marc Ladanyi and Eva Wardelmann and Cristina Antonescu and Adrienne Flanagan and Uta Dirksen and Peter Hohenberger and Daniel Baumhoer and Wolfgang Hartmann and Christian Vokuhl and Uta Flucke and Iver Petersen and Gunhild Mechtersheimer and David Capper and Jones, \{David T. W.\} and Stefan Fr{\"o}hling and Pfister, \{Stefan M.\} and \{von Deimling\}, Andreas",

note = "Funding Information: This work was funded by Deutsche Krebshilfe grant 70112499, the NCT Heidelberg and an Illumina Medical Research Grant. Part of this work was funded by the National Institute of Health Research (to S.B. and Z.J.) and to UCLH Biomedical research centre (BRC399/NS/RB/101410). Human tissues were obtained from University College London NHS Foundation Trust as part of the UK Brain Archive Information Network (BRAIN UK, Ref: 18/004) which is funded by the Medical Research Council and Brain Tumour Research UK. The methylation profiling at NYU is supported by a grant from the Friedberg Charitable Foundation (to M.Sn.). M.Mi. would like to thank the Luxembourg National Research Fond (FNR) for the support (FNR PEARL P16/BM/ 11192868 grant). Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

day = "1",

doi = "10.1038/s41467-020-20603-4",

language = "English",

volume = "12",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

number = "1",

}

Koelsche, C, Schrimpf, D, Stichel, D, Sill, M, Sahm, F, Reuss, DE, Blattner, M, Worst, B, Heilig, CE, Beck, K, Horak, P, Kreutzfeldt, S, Paff, E, Stark, S, Johann, P, Selt, F, Ecker, J, Sturm, D, Pajtler, KW, Reinhardt, A, Wefers, AK, Sievers, P, Ebrahimi, A, Suwala, A, Fernández-Klett, F, Casalini, B, Korshunov, A, Hovestadt, V, Kommoss, FKF, Kriegsmann, M, Schick, M, Bewerunge-Hudler, M, Milde, T, Witt, O, Kulozik, AE, Kool, M, Romero-Pérez, L, Grünewald, TGP, Kirchner, T, Wick, W, Platten, M, Unterberg, A, Uhl, M, Abdollahi, A, Debus, JR, Lehner, B, Thomas, C, Hasselblatt, M, Paulus, W, Hartmann, C, Staszewski, O, Prinz, M, Hench, JR, Frank, S, Versleijen-Jonkers, YMH, Weidema, ME, Mentzel, T, Griewank, K, de Álava, E, Martín, JDA, Gastearena, MAI, Chang, KT-E, Low, SYY, Cuevas-Bourdier, A, Mittelbronn, M, Mynarek, M, Rutkowski, S, Schüller, U, Mautner, VF, Schittenhelm, J, Serrano, J, Snuderl, M, Büttner, R, Klingebiel, T, Buslei, R, Gessler, M, Wesseling, P, Dinjens, WNM, Brandner, S, Jaunmuktane, Z, Lyskjær, I, Schirmacher, P, Stenzinger, A, Brors, B, Glimm, H, Heining, C, Tirado, OM, Sáinz-Jaspeado, M, Mora, J, Alonso, J, del Muro, XG, Moran, S, Esteller, M, Benhamida, JK, Ladanyi, M, Wardelmann, E, Antonescu, C, Flanagan, A, Dirksen, U, Hohenberger, P, Baumhoer, D, Hartmann, W, Vokuhl, C, Flucke, U, Petersen, I, Mechtersheimer, G, Capper, D, Jones, DTW, Fröhling, S, Pfister, SM & von Deimling, A 2021, 'Sarcoma classification by DNA methylation profiling', Nature communications, vol. 12, no. 1, 498. https://doi.org/10.1038/s41467-020-20603-4

TY - JOUR

T1 - Sarcoma classification by DNA methylation profiling

AU - Koelsche, Christian

AU - Schrimpf, Daniel

AU - Stichel, Damian

AU - Sill, Martin

AU - Sahm, Felix

AU - Reuss, David E.

AU - Blattner, Mirjam

AU - Worst, Barbara

AU - Heilig, Christoph E.

AU - Beck, Katja

AU - Horak, Peter

AU - Kreutzfeldt, Simon

AU - Paff, Elke

AU - Stark, Sebastian

AU - Johann, Pascal

AU - Selt, Florian

AU - Ecker, Jonas

AU - Sturm, Dominik

AU - Pajtler, Kristian W.

AU - Reinhardt, Annekathrin

AU - Wefers, Annika K.

AU - Sievers, Philipp

AU - Ebrahimi, Azadeh

AU - Suwala, Abigail

AU - Fernández-Klett, Francisco

AU - Casalini, Belén

AU - Korshunov, Andrey

AU - Hovestadt, Volker

AU - Kommoss, Felix K. F.

AU - Kriegsmann, Mark

AU - Schick, Matthias

AU - Bewerunge-Hudler, Melanie

AU - Milde, Till

AU - Witt, Olaf

AU - Kulozik, Andreas E.

AU - Kool, Marcel

AU - Romero-Pérez, Laura

AU - Grünewald, Thomas G. P.

AU - Kirchner, Thomas

AU - Wick, Wolfgang

AU - Platten, Michael

AU - Unterberg, Andreas

AU - Uhl, Matthias

AU - Abdollahi, Amir

AU - Debus, J. rgen

AU - Lehner, Burkhard

AU - Thomas, Christian

AU - Hasselblatt, Martin

AU - Paulus, Werner

AU - Hartmann, Christian

AU - Staszewski, Ori

AU - Prinz, Marco

AU - Hench, J. rgen

AU - Frank, Stephan

AU - Versleijen-Jonkers, Yvonne M. H.

AU - Weidema, Marije E.

AU - Mentzel, Thomas

AU - Griewank, Klaus

AU - de Álava, Enrique

AU - Martín, Juan D. az

AU - Gastearena, Miguel A. Idoate

AU - Chang, Kenneth Tou-En

AU - Low, Sharon Yin Yee

AU - Cuevas-Bourdier, Adrian

AU - Mittelbronn, Michel

AU - Mynarek, Martin

AU - Rutkowski, Stefan

AU - Schüller, Ulrich

AU - Mautner, Viktor F.

AU - Schittenhelm, Jens

AU - Serrano, Jonathan

AU - Snuderl, Matija

AU - Büttner, Reinhard

AU - Klingebiel, Thomas

AU - Buslei, Rolf

AU - Gessler, Manfred

AU - Wesseling, Pieter

AU - Dinjens, Winand N. M.

AU - Brandner, Sebastian

AU - Jaunmuktane, Zane

AU - Lyskjær, Iben

AU - Schirmacher, Peter

AU - Stenzinger, Albrecht

AU - Brors, Benedikt

AU - Glimm, Hanno

AU - Heining, Christoph

AU - Tirado, Oscar M.

AU - Sáinz-Jaspeado, Miguel

AU - Mora, Jaume

AU - Alonso, Javier

AU - del Muro, Xavier Garcia

AU - Moran, Sebastian

AU - Esteller, Manel

AU - Benhamida, Jamal K.

AU - Ladanyi, Marc

AU - Wardelmann, Eva

AU - Antonescu, Cristina

AU - Flanagan, Adrienne

AU - Dirksen, Uta

AU - Hohenberger, Peter

AU - Baumhoer, Daniel

AU - Hartmann, Wolfgang

AU - Vokuhl, Christian

AU - Flucke, Uta

AU - Petersen, Iver

AU - Mechtersheimer, Gunhild

AU - Capper, David

AU - Jones, David T. W.

AU - Fröhling, Stefan

AU - Pfister, Stefan M.

AU - von Deimling, Andreas

N1 - Funding Information: This work was funded by Deutsche Krebshilfe grant 70112499, the NCT Heidelberg and an Illumina Medical Research Grant. Part of this work was funded by the National Institute of Health Research (to S.B. and Z.J.) and to UCLH Biomedical research centre (BRC399/NS/RB/101410). Human tissues were obtained from University College London NHS Foundation Trust as part of the UK Brain Archive Information Network (BRAIN UK, Ref: 18/004) which is funded by the Medical Research Council and Brain Tumour Research UK. The methylation profiling at NYU is supported by a grant from the Friedberg Charitable Foundation (to M.Sn.). M.Mi. would like to thank the Luxembourg National Research Fond (FNR) for the support (FNR PEARL P16/BM/ 11192868 grant). Publisher Copyright: © 2021, The Author(s).

PY - 2021/12/1

Y1 - 2021/12/1

N2 - Sarcomas are malignant soft tissue and bone tumours affecting adults, adolescents and children. They represent a morphologically heterogeneous class of tumours and some entities lack defining histopathological features. Therefore, the diagnosis of sarcomas is burdened with a high inter-observer variability and misclassification rate. Here, we demonstrate classification of soft tissue and bone tumours using a machine learning classifier algorithm based on array-generated DNA methylation data. This sarcoma classifier is trained using a dataset of 1077 methylation profiles from comprehensively pre-characterized cases comprising 62 tumour methylation classes constituting a broad range of soft tissue and bone sarcoma subtypes across the entire age spectrum. The performance is validated in a cohort of 428 sarcomatous tumours, of which 322 cases were classified by the sarcoma classifier. Our results demonstrate the potential of the DNA methylation-based sarcoma classification for research and future diagnostic applications.

AB - Sarcomas are malignant soft tissue and bone tumours affecting adults, adolescents and children. They represent a morphologically heterogeneous class of tumours and some entities lack defining histopathological features. Therefore, the diagnosis of sarcomas is burdened with a high inter-observer variability and misclassification rate. Here, we demonstrate classification of soft tissue and bone tumours using a machine learning classifier algorithm based on array-generated DNA methylation data. This sarcoma classifier is trained using a dataset of 1077 methylation profiles from comprehensively pre-characterized cases comprising 62 tumour methylation classes constituting a broad range of soft tissue and bone sarcoma subtypes across the entire age spectrum. The performance is validated in a cohort of 428 sarcomatous tumours, of which 322 cases were classified by the sarcoma classifier. Our results demonstrate the potential of the DNA methylation-based sarcoma classification for research and future diagnostic applications.

UR - https://www.scopus.com/pages/publications/85099975144

U2 - 10.1038/s41467-020-20603-4

DO - 10.1038/s41467-020-20603-4

M3 - Article

C2 - 33479225

SN - 2041-1723

VL - 12

JO - Nature communications

JF - Nature communications

IS - 1

M1 - 498

ER -

Sarcoma classification by DNA methylation profiling

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