An empirical framework for binary interactome mapping (original) (raw)

References

  1. Vidal, M. Interactome modeling. FEBS Lett. 579, 1834–1838 (2005).
    Article CAS Google Scholar
  2. Rual, J.F. et al. Towards a proteome-scale map of the human protein-protein interaction network. Nature 437, 1173–1178 (2005).
    Article CAS Google Scholar
  3. Stelzl, U. et al. A human protein-protein interaction network: a resource for annotating the proteome. Cell 122, 957–968 (2005).
    Article CAS Google Scholar
  4. Ewing, R.M. et al. Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol. Syst. Biol. 3, 89 (2007).
    Article Google Scholar
  5. Peri, S. et al. Human protein reference database as a discovery resource for proteomics. Nucleic Acids Res. 32, D497–D501 (2004).
    Article CAS Google Scholar
  6. Zanzoni, A. et al. MINT: a Molecular INTeraction database. FEBS Lett. 513, 135–140 (2002).
    Article CAS Google Scholar
  7. Bader, G.D. et al. BIND–The Biomolecular Interaction Network Database. Nucleic Acids Res. 29, 242–245 (2001).
    Article CAS Google Scholar
  8. Hermjakob, H. et al. IntAct: an open source molecular interaction database. Nucleic Acids Res. 32, D452–D455 (2004).
    Article CAS Google Scholar
  9. Xenarios, I. et al. DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions. Nucleic Acids Res. 30, 303–305 (2002).
    Article CAS Google Scholar
  10. Mewes, H.W. et al. MIPS: a database for genomes and protein sequences. Nucleic Acids Res. 30, 31–34 (2002).
    Article CAS Google Scholar
  11. Ramani, A.K., Bunescu, R.C., Mooney, R.J. & Marcotte, E.M. Consolidating the set of known human protein-protein interactions in preparation for large-scale mapping of the human interactome. Genome Biol. 6, R40 (2005).
    Article Google Scholar
  12. Lehner, B. & Fraser, A.G. A first-draft human protein-interaction map. Genome Biol. 5, R63 (2004).
    Article Google Scholar
  13. Hart, G.T., Ramani, A.K. & Marcotte, E.M. How complete are current yeast and human protein-interaction networks? Genome Biol. 7, 120 (2006).
    Article Google Scholar
  14. Futschik, M.E., Chaurasia, G. & Herzel, H. Comparison of human protein-protein interaction maps. Bioinformatics 23, 605–611 (2007).
    Article CAS Google Scholar
  15. von Mering, C. et al. Comparative assessment of large-scale data sets of protein-protein interactions. Nature 417, 399–403 (2002).
    Article CAS Google Scholar
  16. Reguly, T. et al. Comprehensive curation and analysis of global interaction networks in Saccharomyces cerevisiae. J. Biol. 5, 11 (2006).
    Article Google Scholar
  17. Gandhi, T.K. et al. Analysis of the human protein interactome and comparison with yeast, worm and fly interaction datasets. Nat. Genet. 38, 285–293 (2006).
    Article CAS Google Scholar
  18. Patil, A. & Nakamura, H. Filtering high-throughput protein-protein interaction data using a combination of genomic features. BMC Bioinformatics 6, 100 (2005).
    Article Google Scholar
  19. Huang, H., Jedynak, B.M. & Bader, J.S. Where have all the interactions gone? Estimating the coverage of two-hybrid protein interaction maps. PLoS Comput. Biol. 3, e214 (2007).
    Article Google Scholar
  20. D'Haeseleer, P. & Church, G.M. Estimating and improving protein interaction error rates. Proc. IEEE Comput. Syst. Bioinform. Conf. 216–223 (2004).
  21. Grigoriev, A. On the number of protein-protein interactions in the yeast proteome. Nucleic Acids Res. 31, 4157–4161 (2003).
    Article CAS Google Scholar
  22. Deane, C.M., Salwinski, L., Xenarios, I. & Eisenberg, D. Protein interactions: two methods for assessment of the reliability of high throughput observations. Mol. Cell. Proteomics 1, 349–356 (2002).
    Article CAS Google Scholar
  23. Sprinzak, E., Sattath, S. & Margalit, H. How reliable are experimental protein-protein interaction data? J. Mol. Biol. 327, 919–923 (2003).
    Article CAS Google Scholar
  24. Rual, J.F. et al. Human ORFeome version 1.1: a platform for reverse proteomics. Genome Res. 14, 2128–2135 (2004).
    Article CAS Google Scholar
  25. Cusick, M.E. et al. Literature-curated protein interaction datasets. Nat. Methods (in the press).
  26. Braun, P. et al. An experimentally derived confidence score for binary protein-protein interactions. Nat. Methods advance online publication, doi:10.1038/nmeth.1281 (7 December 2008).
  27. Eyckerman, S. et al. Design and application of a cytokine-receptor-based interaction trap. Nat. Cell Biol. 3, 1114–1119 (2001).
    Article CAS Google Scholar
  28. Stumpf, M.P. et al. Estimating the size of the human interactome. Proc. Natl. Acad. Sci. USA 105, 6959–6964 (2008).
    Article CAS Google Scholar
  29. Ramírez, F., Schlicker, A., Assenov, Y., Lengauer, T. & Albrecht, M. Computational analysis of human protein interaction networks. Proteomics 7, 2541–2552 (2007).
    Article Google Scholar
  30. Collins, S.R. et al. Towards a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol. Cell. Proteomics 6, 439–450 (2007).
    Article CAS Google Scholar
  31. Fields, C., Adams, M.D., White, O. & Venter, J.C. How many genes in the human genome? Nat. Genet. 7, 345–346 (1994).
    Article CAS Google Scholar
  32. Lemmens, I., Lievens, S., Eyckerman, S. & Tavernier, J. Reverse MAPPIT detects disruptors of protein-protein interactions in human cells. Nat. Protoc. 1, 92–97 (2006).
    Article CAS Google Scholar

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Acknowledgements

We thank members of CCSB and the Vidal, Barabasi, Wanker and Tavernier laboratories and S. Sahasrabuddhe, R. Bell, R. Chettier and C. Wiggins for helpful discussions; E. Smith for help generating Figure 1; and Agencourt Biosciences for sequencing assistance. This work was supported by the US National Human Genome Research Institute (2R01HG001715 and 5P50HG004233 to M.V. and F.P.R.), the US National Cancer Institute (5U54CA112952 to J. Nevins, subcontract to M.V.; and 5U01CA105423 to S.H. Orkin, project to M.V.), the US National Institutes of Health (IH U01 A1070499-01 and U56 CA113004 to A.-L.B. and postdoctoral training grant fellowship T32CA09361 to K.V.), the Ellison Foundation (to M.V.), the W.M. Keck Foundation (to M.V.), Dana-Farber Cancer Institute Institute Sponsored Research funds (to M.V.), the US National Science Foundation (ITR DMR-0926737 and IIS-0513650 to A.-L.B.), Deutsches Bundesministerium für Bildung und Forschung (NGFN2, KB-P04T01, KB-P04T03 and 01GR0471 to E.E.W. and U.S.), Deutsche Forschungsgemeinschaft (SFB 577 and SFB618 to E.E.W.), the University of Ghent and the “Fonds Wetenschappelijk Onderzoek–Vlaanderen” (FWO-V) G.0031.06 (GOA12051401 to J. Tavernier) and the National Cancer Institute of Canada (to C.B.). I.L. is a postdoctoral fellow with the FWO-V. M.V. is a “Chercheur Qualifié Honoraire” from the Fonds de la Recherche Scientifique (French Community of Belgium).

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Author notes

  1. Kavitha Venkatesan, Jean-François Rual, Kathrin Heinzmann, Sebiha Cevik, Christophe Simon, Heather Borick, Niels Klitgord, Maciej Lalowski & Albert-László Barabási
    Present address: Present addresses: Novartis Institutes for Biomedical Research, 250 Massachusetts Avenue, Cambridge, Massachusetts 02139, USA (K.V.), Department of Cell Biology, Harvard Medical School, 240 Longwood Avenue, Boston, Massachusetts 02115, USA (J.-F.R.), Centre for Cancer Therapeutics, The Institute of Cancer Research, 15 Cotswold Road, Sutton, SM2 5NG, UK (K.H.), University College Dublin, School of Biomolecular and Biomedical Science, Belfield, Dublin 4, Ireland (S.C.), Genome Exploration Research Group, RIKEN Genomic Sciences Center, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan (C.S.), Department of Biological Sciences, Clemson University, 132 Long Hall, Clemson, South Carolina 29634, USA (H.B.), Bioinformatics Program, Boston University, 24 Cummington Street, Boston, Massachusetts 02215, USA (N.K.), Protein Chemistry/Proteomics/Peptide Synthesis and Array Unit, Biomedicum Helsinki, University of Helsinki, Haartmaninkatu 8, FI-00014 Helsinki, Finland (M.L.) and Center for Complex Network Research and Departments of Physics, Biology and Computer Sciences, Northeastern University, 360 Huntington Avenue, Boston, Massachusetts 02115, USA (A.-L.B.).,
  2. Kavitha Venkatesan, Jean-François Rual, Alexei Vazquez, Ulrich Stelzl and Irma Lemmens: These authors contributed equally to this work.

Authors and Affiliations

  1. Center for Cancer Systems Biology and Department of Cancer Biology, Dana-Farber Cancer Institute, 1 Jimmy Fund Way, Boston, 02115, Massachusetts, USA
    Kavitha Venkatesan, Jean-François Rual, Alexei Vazquez, Tomoko Hirozane-Kishikawa, Tong Hao, Kwang-Il Goh, Muhammed A Yildirim, Nicolas Simonis, Kathrin Heinzmann, Fana Gebreab, Julie M Sahalie, Sebiha Cevik, Christophe Simon, Elizabeth Dann, Alex Smolyar, Haiyuan Yu, David Szeto, Heather Borick, Amélie Dricot, Niels Klitgord, Ryan R Murray, Chenwei Lin, Pascal Braun, Michael E Cusick, Frederick P Roth, David E Hill, Albert-László Barabási & Marc Vidal
  2. Department of Genetics, Harvard Medical School, 77 Avenue Louis Pasteur, Boston, 02115, Massachusetts, USA
    Kavitha Venkatesan, Jean-François Rual, Tomoko Hirozane-Kishikawa, Tong Hao, Muhammed A Yildirim, Nicolas Simonis, Kathrin Heinzmann, Fana Gebreab, Julie M Sahalie, Sebiha Cevik, Christophe Simon, Elizabeth Dann, Alex Smolyar, Haiyuan Yu, David Szeto, Heather Borick, Amélie Dricot, Niels Klitgord, Ryan R Murray, Chenwei Lin, Pascal Braun, Michael E Cusick, David E Hill & Marc Vidal
  3. Center for Complex Network Research and Department of Physics, University of Notre Dame, 225 Nieuwland Science Hall, Notre Dame, 46556, Indiana, USA
    Alexei Vazquez, Kwang-Il Goh & Albert-László Barabási
  4. The Simons Center for Systems Biology, Institute for Advanced Study, Einstein Drive, Princeton, 08540, New Jersey, USA
    Alexei Vazquez
  5. Max Delbrück Center for Molecular Medicine, Robert-Roessle-Straße 10, Berlin, D-13125, Germany
    Ulrich Stelzl, Martina Zenkner, Arunachalam Vinayagam, Maciej Lalowski, Jan Timm, Kirstin Rau & Erich E Wanker
  6. Otto-Warburg Laboratory, Max Planck Institute for Molecular Genetics, Ihnestraße 63-73, Berlin, D-14195, Germany
    Ulrich Stelzl
  7. Department of Medical Protein Research, and Department of Biochemistry, Vlaams Instituut voor Biotechnologie, Faculty of Medicine and Health Sciences, Ghent University, Albert Baertsoenkaai 3, Ghent, 9000, Belgium
    Irma Lemmens, Anne-Sophie de Smet & Jan Tavernier
  8. Banting and Best Department of Medical Research and Department of Molecular Genetics, Terrence Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, 160 College Street, Toronto, M5S 3E1, Ontario, Canada
    Xiaofeng Xin & Charles Boone
  9. Department of Physics, Korea University, 1 Anam-dong 5-ga, Seongbuk-gu, Seoul, 136-713, Korea
    Kwang-Il Goh
  10. School of Engineering and Applied Sciences, Harvard University, 29 Oxford Street, Cambridge, 02138, Massachusetts, USA
    Muhammed A Yildirim
  11. Department of Biochemistry and Molecular Pharmacology, Harvard Medical School, 250 Longwood Avenue, Boston, 02115, Massachusetts, USA
    Frederick P Roth

Authors

  1. Kavitha Venkatesan
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  2. Jean-François Rual
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  3. Alexei Vazquez
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  4. Ulrich Stelzl
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  5. Irma Lemmens
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  6. Tomoko Hirozane-Kishikawa
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  7. Tong Hao
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  8. Martina Zenkner
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  9. Xiaofeng Xin
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  10. Kwang-Il Goh
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  11. Muhammed A Yildirim
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  12. Nicolas Simonis
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  13. Kathrin Heinzmann
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  14. Fana Gebreab
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  15. Julie M Sahalie
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  16. Sebiha Cevik
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  17. Christophe Simon
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  18. Anne-Sophie de Smet
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  19. Elizabeth Dann
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  20. Alex Smolyar
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  21. Arunachalam Vinayagam
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  22. Haiyuan Yu
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  23. David Szeto
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  24. Heather Borick
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  25. Amélie Dricot
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  26. Niels Klitgord
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  27. Ryan R Murray
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  28. Chenwei Lin
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  29. Maciej Lalowski
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  30. Jan Timm
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  31. Kirstin Rau
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  32. Charles Boone
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  33. Pascal Braun
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  34. Michael E Cusick
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  35. Frederick P Roth
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  36. David E Hill
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  37. Jan Tavernier
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  38. Erich E Wanker
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  39. Albert-László Barabási
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  40. Marc Vidal
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Contributions

K.V., J.-F.R., A. Vazquez, U.S., I.L., J. Tavernier, E.E.W., A.-L.B. and M.V. conceived the project. K.V., J.-F.R., A. Vazquez, U.S. and I.L. coordinated the experiments and data analyses. J.-F.R., U.S., T.H.-K., M.Z., X.X., K.H., F.G., J.M.S., P.B., H.Y., S.C., C.S., E.D., J. Timm, K.R. and C.B. conducted the Y2H experiments. J.-F.R., T.H.-K. and C.S. conducted the high-throughput ORF cloning for MAPPIT experiments. I.L. and A.-S.d.S. conducted the MAPPIT experiments. K.V., A. Vazquez, T.H., K.-I.G., M.A.Y., A. Vinayagam, N.S., N.K., C.L., M.L. and F.P.R. conducted the computational and statistical analyses. M.E.C., A.S., H.B., J.-F.R. and K.V. conducted the literature-curated interaction recuration analyses. D.S., A.D. and R.R.M. provided laboratory support. K.V., J.-F.R., A. Vazquez, U.S., I.L., M.E.C., D.E.H., J. Tavernier, E.E.W., A.-L.B. and M.V. wrote the manuscript. D.E.H, J. Tavernier, E.E.W., A.-L.B. and M.V. codirected the project.

Corresponding authors

Correspondence toJan Tavernier, Erich E Wanker, Albert-László Barabási or Marc Vidal.

Supplementary information

Supplementary Text and Figures

Supplementary Figure 1; Supplementary Tables 2,3,5; Supplementary Data 1–4; Supplementary Methods (PDF 2639 kb)

Supplementary Table 1

List of interactions in various datasets used in pair wise test experiments using MAPPIT and Y2H-CCSB assays (XLS 144 kb)

Supplementary Table 4

Scores for the Y2H-CCSB and MAPPIT experiments on the hsPRS-v1 and hsRRS-v1 to compute assay sensitivity and background positive rate and scores on subsets of the LC, MDC-HI1 and CCSB-HI1 interaction datasets (XLS 78 kb)

Supplementary Table 6

Identity of the ORFs making up the Y2H-CCSB repeat screens (XLS 396 kb)

Supplementary Table 7

Interactions found in the Y2H-CCSB repeat screens (XLS 69 kb)

Supplementary Table 8

Interactions found in the Y2H-CCSB repeat screens reported according to MIMIX specifications (XLS 207 kb)

Supplementary Table 9

Identity of the ORFs making up the MDC-HI1 search space (space II) (XLS 159 kb)

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Venkatesan, K., Rual, JF., Vazquez, A. et al. An empirical framework for binary interactome mapping.Nat Methods 6, 83–90 (2009). https://doi.org/10.1038/nmeth.1280

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