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Maximizing binary interactome mapping with a minimal number of assays

View ORCID ProfileSoon Gang Choi, Julien Olivet, Patricia Cassonnet, Pierre-Olivier Vidalain, Katja Luck, Luke Lambourne, Kerstin Spirohn, Irma Lemmens, Mélanie Dos Santos, Caroline Demeret, Louis Jones, Sudharshan Rangarajan, Wenting Bian, Eloi P. Coutant, Yves L. Janin, Sylvie van der Werf, Philipp Trepte, Erich E. Wanker, Javier De Las Rivas, Jan Tavernier, Jean-Claude Twizere, Tong Hao, David E. Hill, Marc Vidal, Michael A. Calderwood, Yves Jacob
doi: https://doi.org/10.1101/530790
Soon Gang Choi
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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  • ORCID record for Soon Gang Choi
Julien Olivet
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
4Laboratory of Viral Interactomes, Unit of Molecular Biology of Diseases, Groupe Interdisciplinaire de Génomique Appliquée (GIGA Institute), University of Liège, 7 Place du 20 Août, 4000 Liège, Belgium
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Patricia Cassonnet
5Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015 Paris, France
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Pierre-Olivier Vidalain
6Équipe Chimie, Biologie, Modélisation et Immunologie pour la Thérapie (CBMIT), Laboratoire de Chimie et Biochimie Pharmacologiques et Toxicologiques (LCBPT), Centre Interdisciplinaire Chimie Biologie-Paris (CICB-Paris), UMR8601, CNRS, Université Paris Descartes, 45 rue des Saints-Pères, 75006 Paris, France
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Katja Luck
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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Luke Lambourne
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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Kerstin Spirohn
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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Irma Lemmens
7Center for Medical Biotechnology, Vlaams Instituut voor Biotechnologie (VIB), 3 Albert Baertsoenkaai, 9000 Ghent, Belgium
8Cytokine Receptor Laboratory (CRL), Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, 3 Albert Baertsoenkaai, 9000 Ghent, Belgium
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Mélanie Dos Santos
5Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015 Paris, France
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Caroline Demeret
5Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015 Paris, France
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Louis Jones
9Centre de Bioinformatique, Biostatistique et Biologie Intégrative (C3BI), Institut Pasteur, 28 rue du Docteur Roux, 75015 Paris, France
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Sudharshan Rangarajan
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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Wenting Bian
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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Eloi P. Coutant
10Département de Biologie Structurale et Chimie, Unité de Chimie et Biocatalyse, Institut Pasteur, UMR3523, CNRS, 28 rue du Docteur Roux, 75015 Paris, France.
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Yves L. Janin
10Département de Biologie Structurale et Chimie, Unité de Chimie et Biocatalyse, Institut Pasteur, UMR3523, CNRS, 28 rue du Docteur Roux, 75015 Paris, France.
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Sylvie van der Werf
5Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015 Paris, France
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Philipp Trepte
11Neuroproteomics, Max Delbrück Center for Molecular Medicine, 10 Robert-Rössle-Str., 13125 Berlin, Germany
12Brain Development and Disease, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), 3 Dr. Bohr-Gasse, 1030 Vienna, Austria
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Erich E. Wanker
11Neuroproteomics, Max Delbrück Center for Molecular Medicine, 10 Robert-Rössle-Str., 13125 Berlin, Germany
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Javier De Las Rivas
13Cancer Research Center (CiC-IBMCC, CSIC/USAL), Consejo Superior de Investigaciones Científicas (CSIC), University of Salamanca (USAL), Campus Miguel de Unamuno, 37007 Salamanca, Spain
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Jan Tavernier
7Center for Medical Biotechnology, Vlaams Instituut voor Biotechnologie (VIB), 3 Albert Baertsoenkaai, 9000 Ghent, Belgium
8Cytokine Receptor Laboratory (CRL), Department of Biomolecular Medicine, Faculty of Medicine and Health Sciences, Ghent University, 3 Albert Baertsoenkaai, 9000 Ghent, Belgium
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Jean-Claude Twizere
4Laboratory of Viral Interactomes, Unit of Molecular Biology of Diseases, Groupe Interdisciplinaire de Génomique Appliquée (GIGA Institute), University of Liège, 7 Place du 20 Août, 4000 Liège, Belgium
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Tong Hao
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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David E. Hill
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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Marc Vidal
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
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  • For correspondence: marc_vidal@dfci.harvard.edu michael_calderwood@dfci.harvard.edu yves.jacob@pasteur.fr
Michael A. Calderwood
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
2Department of Genetics, Blavatnik Institute, Harvard Medical School (HMS), 77 Avenue Louis Pasteur, Boston, MA 02115, USA
3Department of Cancer Biology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA 02215, USA
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  • For correspondence: marc_vidal@dfci.harvard.edu michael_calderwood@dfci.harvard.edu yves.jacob@pasteur.fr
Yves Jacob
1Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute (DFCI), 450 Brookline Avenue, Boston, MA 02215, USA
5Département de Virologie, Unité de Génétique Moléculaire des Virus à ARN (GMVR), Institut Pasteur, UMR3569, Centre National de la Recherche Scientifique (CNRS), Université Paris Diderot, Sorbonne Paris Cité, 28 rue du Docteur Roux, 75015 Paris, France
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  • For correspondence: marc_vidal@dfci.harvard.edu michael_calderwood@dfci.harvard.edu yves.jacob@pasteur.fr
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ABSTRACT

Complementary assays are required to comprehensively map complex biological entities such as genomes, proteomes and interactome networks. However, how various assays can be optimally combined to approach completeness while maintaining high precision often remains unclear. Here, we propose a framework for binary protein-protein interaction (PPI) mapping based on optimally combining assays and/or assay versions to maximize detection of true positive interactions, while avoiding detection of random protein pairs. We have engineered a novel NanoLuc two-hybrid (N2H) system that integrates 12 different versions, differing by protein expression systems and tagging configurations. The resulting union of N2H versions recovers as many PPIs as 10 distinct assays combined. Thus, to further improve PPI mapping, developing alternative versions of existing assays might be as productive as designing completely new assays. Our findings should be applicable to systematic mapping of other biological landscapes.

Footnotes

  • We updated the manuscript to reflect comments from the reviewers. This version was submitted for final publication.

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 August 09, 2019.
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Maximizing binary interactome mapping with a minimal number of assays
Soon Gang Choi, Julien Olivet, Patricia Cassonnet, Pierre-Olivier Vidalain, Katja Luck, Luke Lambourne, Kerstin Spirohn, Irma Lemmens, Mélanie Dos Santos, Caroline Demeret, Louis Jones, Sudharshan Rangarajan, Wenting Bian, Eloi P. Coutant, Yves L. Janin, Sylvie van der Werf, Philipp Trepte, Erich E. Wanker, Javier De Las Rivas, Jan Tavernier, Jean-Claude Twizere, Tong Hao, David E. Hill, Marc Vidal, Michael A. Calderwood, Yves Jacob
bioRxiv 530790; doi: https://doi.org/10.1101/530790
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Maximizing binary interactome mapping with a minimal number of assays
Soon Gang Choi, Julien Olivet, Patricia Cassonnet, Pierre-Olivier Vidalain, Katja Luck, Luke Lambourne, Kerstin Spirohn, Irma Lemmens, Mélanie Dos Santos, Caroline Demeret, Louis Jones, Sudharshan Rangarajan, Wenting Bian, Eloi P. Coutant, Yves L. Janin, Sylvie van der Werf, Philipp Trepte, Erich E. Wanker, Javier De Las Rivas, Jan Tavernier, Jean-Claude Twizere, Tong Hao, David E. Hill, Marc Vidal, Michael A. Calderwood, Yves Jacob
bioRxiv 530790; doi: https://doi.org/10.1101/530790

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