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Spatial structure governs the mode of tumour evolution

View ORCID ProfileRobert Noble, Dominik Burri, View ORCID ProfileJakob Nikolas Kather, View ORCID ProfileNiko Beerenwinkel
doi: https://doi.org/10.1101/586735
Robert Noble
1Department of Biosystems Science and Engineering, ETH Zurich, 4058 Basel, Switzerland
2SIB Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
3Department of Evolutionary Biology and Environmental Studies, University of Zurich, 8057 Zurich, Switzerland
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Dominik Burri
1Department of Biosystems Science and Engineering, ETH Zurich, 4058 Basel, Switzerland
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Jakob Nikolas Kather
4German Cancer Consortium (DKTK), Heidelberg, Germany
5Applied Tumor Immunity, German Cancer Research Center (DKFZ), Heidelberg, Germany
6Internal Medicine III, University Hospital RWTH Aachen, Aachen, Germany
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Niko Beerenwinkel
1Department of Biosystems Science and Engineering, ETH Zurich, 4058 Basel, Switzerland
2SIB Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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Abstract

Characterizing the mode – the way, manner, or pattern – of evolution in tumours is important for clinical forecasting and optimizing cancer treatment. DNA sequencing studies have inferred various modes, including branching, punctuated and neutral evolution, but it is unclear why a particular pattern predominates in any given tumour [1]. Here we propose that differences in tumour architecture alone can explain the variety of observed patterns. We examine this hypothesis using spatially explicit population genetic models and demonstrate that, within biologically relevant parameter ranges, tumours are expected to exhibit diverse evolutionary modes including four archetypal “oncoevotypes”: rapid clonal expansion (predicted in leukaemia); progressive diversification (in colorectal adenomas and early-stage colorectal carcinomas); branching evolution (in invasive glandular tumours); and almost neutral evolution (in certain non-glandular and poorly differentiated solid tumours). We thus provide a simple, mechanistic explanation for a wide range of empirical observations. Oncoevotypes are driven by differences in cell dispersal and cell-cell interactions, which we show are essential for accurately characterizing, forecasting and controlling tumour evolution.

Footnotes

  • ↵* robert.noble{at}bsse.ethz.ch

  • ↵+ niko.beerenwinkel{at}bsse.ethz.ch

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 23, 2019.
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Spatial structure governs the mode of tumour evolution
Robert Noble, Dominik Burri, Jakob Nikolas Kather, Niko Beerenwinkel
bioRxiv 586735; doi: https://doi.org/10.1101/586735
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Spatial structure governs the mode of tumour evolution
Robert Noble, Dominik Burri, Jakob Nikolas Kather, Niko Beerenwinkel
bioRxiv 586735; doi: https://doi.org/10.1101/586735

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