Error message

No crossref credentials set for sci

Dynamic Complex Formation During the Yeast Cell Cycle

Science, 4 February 2005
Vol. 307, Issue 5710, p. 724-727
DOI: 10.1126/science.1105103

Dynamic Complex Formation During the Yeast Cell Cycle

  1. Ulrik de Lichtenberg1,*,
  2. Lars Juhl Jensen2,*,
  3. Søren Brunak1,
  4. Peer Bork2,3,
  1. 1 Center for Biological Sequence Analysis, Technical University of Denmark, DK-2800 Lyngby, Denmark.
  2. 2 European Molecular Biology Laboratory, D-69117 Heidelberg, Germany.
  3. 3 Max-Delbrück-Centre for Molecular Medicine, D-13092 Berlin, Germany.
  1. To whom correspondence should be addressed. E-mail: bork{at}embl.de
  • * These authors contributed equally to this work.

Abstract

To analyze the dynamics of protein complexes during the yeast cell cycle, we integrated data on protein interactions and gene expression. The resulting time-dependent interaction network places both periodically and constitutively expressed proteins in a temporal cell cycle context, thereby revealing previously unknown components and modules. We discovered that most complexes consist of both periodically and constitutively expressed subunits, which suggests that the former control complex activity by a mechanism of just-in-time assembly. Consistent with this, we show that additional regulation through targeted degradation and phosphorylation by Cdc28p (Cdk1) specifically affects the periodically expressed proteins.

    • Received for publication 10 September 2004.
    • Accepted for publication 9 December 2004.

    Citation:

    U. de Lichtenberg, L. J. Jensen, S. Brunak, and P. Bork, Dynamic Complex Formation During the Yeast Cell Cycle. Science 307, 724-727 (2005).

    MyProteinNet: build up-to-date protein interaction networks for organisms, tissues and user-defined contexts
    O. Basha, D. Flom, R. Barshir, I. Smoly, S. Tirman, and E. Yeger-Lotem
    Nucleic Acids Res 0, gkv515v1-gkv515 (18 May 2015)

    Modeling disease progression using dynamics of pathway connectivity
    X. Ma, L. Gao, and K. Tan
    Bioinformatics 30, 2343-2350 (15 August 2014)

    Tissue specificity and the human protein interaction network
    A. Bossi, and B. Lehner
    Mol Syst Biol 5, 260-260 (28 July 2014)

    Revealing static and dynamic modular architecture of the eukaryotic protein interaction network
    K. Komurov, and M. White
    Mol Syst Biol 3, 110-110 (28 July 2014)

    Identification of tightly regulated groups of genes during Drosophila melanogaster embryogenesis
    S. D. Hooper, S. Boue, R. Krause, L. J. Jensen, C. E. Mason, M. Ghanim, K. P. White, E. E. Furlong, and P. Bork
    Mol Syst Biol 3, 72-72 (28 July 2014)

    Network-based prediction of protein function
    R. Sharan, I. Ulitsky, and R. Shamir
    Mol Syst Biol 3, 88-88 (28 July 2014)

    Cell cycle regulation by feed-forward loops coupling transcription and phosphorylation
    A. Csikasz-Nagy, O. Kapuy, A. Toth, C. Pal, L. J. Jensen, F. Uhlmann, J. J. Tyson, and B. Novak
    Mol Syst Biol 5, 236-236 (28 July 2014)

    Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium
    V. van Noort, J. Seebacher, S. Bader, S. Mohammed, I. Vonkova, M. J. Betts, S. Kuhner, R. Kumar, T. Maier, M. O'Flaherty et al.
    Mol Syst Biol 8, 571-571 (23 July 2014)

    Differential network biology
    T. Ideker, and N. J. Krogan
    Mol Syst Biol 8, 565-565 (23 July 2014)

    Cell type-specific nuclear pores: a case in point for context-dependent stoichiometry of molecular machines
    A. Ori, N. Banterle, M. Iskar, A. Andres-Pons, C. Escher, H. Khanh Bui, L. Sparks, V. Solis-Mezarino, O. Rinner, P. Bork et al.
    Mol Syst Biol 9, 648-648 (21 July 2014)

    Identifying protein complexes and functional modules--from static PPI networks to dynamic PPI networks
    B. Chen, W. Fan, J. Liu, and F.-X. Wu
    Brief Bioinform 15, 177-194 (1 March 2014)

    Interactions Affected by Arginine Methylation in the Yeast Protein-Protein Interaction Network
    M. A. Erce, D. Abeygunawardena, J. K. K. Low, G. Hart-Smith, and M. R. Wilkins
    MCP 12, 3184-3198 (1 November 2013)

    Dissection of Cdk1-cyclin complexes in vivo
    P. H. Ear, M. J. Booth, D. Abd-Rabbo, J. Kowarzyk Moreno, C. Hall, D. Chen, J. Vogel, and S. W. Michnick
    Proc. Natl. Acad. Sci. USA 110, 15716-15721 (24 September 2013)

    Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes
    A. Cumberworth, G. Lamour, M. M. Babu, and J. Gsponer
    Biochem. J. 454, 361-369 (15 September 2013)

    A context-sensitive framework for the analysis of human signalling pathways in molecular interaction networks
    A. Lan, M. Ziv-Ukelson, and E. Yeger-Lotem
    Bioinformatics 29, i210-i216 (1 July 2013)

    An integrated approach to identify causal network modules of complex diseases with application to colorectal cancer
    Z. Wen, Z.-P. Liu, Z. Liu, Y. Zhang, and L. Chen
    J Am Med Inform Assoc 20, 659-667 (1 July 2013)

    Predicting Physical Interactions between Protein Complexes
    T. Clancy, E. A. Rodland, S. Nygard, and E. Hovig
    MCP 12, 1723-1734 (1 June 2013)

    Detection of transcriptional triggers in the dynamics of microbial growth: application to the respiratorily versatile bacterium Shewanella oneidensis
    Q. K. Beg, M. Zampieri, N. Klitgord, S. B. Collins, C. Altafini, M. H. Serres, and D. Segre
    Nucleic Acids Res 40, 7132-7149 (1 August 2012)

    Enabling Computational Proteomics by Public and Local Data Management Systems
    K. Helsens, and L. Martens
    Circ Cardiovasc Genet 5, 266-266 (1 April 2012)

    How to cluster gene expression dynamics in response to environmental signals
    Y. Wang, M. Xu, Z. Wang, M. Tao, J. Zhu, L. Wang, R. Li, S. A. Berceli, and R. Wu
    Brief Bioinform 13, 162-174 (1 March 2012)

    Phosphosite Mapping of P-type Plasma Membrane H+-ATPase in Homologous and Heterologous Environments
    E. L. Rudashevskaya, J. Ye, O. N. Jensen, A. T. Fuglsang, and M. G. Palmgren
    J Biol Chem 287, 4904-4913 (10 February 2012)

    Construction of a Large Extracellular Protein Interaction Network and Its Resolution by Spatiotemporal Expression Profiling
    S. Martin, C. Sollner, V. Charoensawan, B. Adryan, B. Thisse, C. Thisse, S. Teichmann, and G. J. Wright
    MCP 9, 2654-2665 (1 December 2010)

    Protein evolution in yeast transcription factor subnetworks
    Y. Wang, E. A. Franzosa, X.-S. Zhang, and Y. Xia
    Nucleic Acids Res 38, 5959-5969 (1 October 2010)

    Reverse engineering dynamic temporal models of biological processes and their relationships
    N. Ramakrishnan, S. Tadepalli, L. T. Watson, R. F. Helm, M. Antoniotti, and B. Mishra
    Proc. Natl. Acad. Sci. USA 107, 12511-12516 (13 July 2010)

    Functional Modules in the Arabidopsis Core Cell Cycle Binary Protein-Protein Interaction Network
    J. Boruc, H. Van den Daele, J. Hollunder, S. Rombauts, E. Mylle, P. Hilson, D. Inze, L. De Veylder, and E. Russinova
    Plant Cell 22, 1264-1280 (1 April 2010)

    Toward the dynamic interactome: it's about time
    T. M. Przytycka, M. Singh, and D. K. Slonim
    Brief Bioinform 0, bbp057v1-bbp057 (8 January 2010)

    Proteome Organization in a Genome-Reduced Bacterium
    S. Kuhner, V. van Noort, M. J. Betts, A. Leo-Macias, C. Batisse, M. Rode, T. Yamada, T. Maier, S. Bader, P. Beltran-Alvarez et al.
    Science 326, 1235-1240 (27 November 2009)

    POLAR MAPPER: a computational tool for integrated visualization of protein interaction networks and mRNA expression data
    J. P. Goncalves, M. Graos, and A. X.C.N. Valente
    J R Soc Interface 6, 881-896 (6 October 2009)

    Conserved principles of mammalian transcriptional regulation revealed by RNA half-life
    C. C. Friedel, L. Dolken, Z. Ruzsics, U. H. Koszinowski, and R. Zimmer
    Nucleic Acids Res 37, e115-e115 (1 September 2009)

    Transcriptional Analysis of the Candida albicans Cell Cycle
    P. Cote, H. Hogues, and M. Whiteway
    Mol. Biol. Cell 20, 3363-3373 (15 July 2009)

    Computational systems biology of the cell cycle
    A. Csikasz-Nagy, H. Hogues, and M. Whiteway
    Brief Bioinform 10, 424-434 (1 July 2009)

    Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation
    R. Narayanaswamy, M. Levy, M. Tsechansky, G. M. Stovall, J. D. O'Connell, J. Mirrielees, A. D. Ellington, and E. M. Marcotte
    Proc. Natl. Acad. Sci. USA 106, 10147-10152 (23 June 2009)

    Functional organization of the yeast proteome by a yeast interactome map
    A. X. C. N. Valente, S. B. Roberts, G. A. Buck, and Y. Gao
    Proc. Natl. Acad. Sci. USA 106, 1490-1495 (3 February 2009)

    Challenges and Rewards of Interaction Proteomics
    S. J. Wodak, S. Pu, J. Vlasblom, and B. Seraphin
    MCP 8, 3-18 (1 January 2009)

    STRING 8--a global view on proteins and their functional interactions in 630 organisms
    L. J. Jensen, M. Kuhn, M. Stark, S. Chaffron, C. Creevey, J. Muller, T. Doerks, P. Julien, A. Roth, M. Simonovic et al.
    Nucleic Acids Res 37, D412-D416 (1 January 2009)

    Physical protein-protein interactions predicted from microarrays
    T.-t. Soong, K. O. Wrzeszczynski, and B. Rost
    Bioinformatics 24, 2608-2614 (15 November 2008)

    BIOCHEMISTRY: Not Comparable, But Complementary
    L. J. Jensen, and P. Bork
    Science 322, 56-57 (3 October 2008)

    VistaClara: an expression browser plug-in for Cytoscape
    R. Kincaid, A. Kuchinsky, and M. Creech
    Bioinformatics 24, 2112-2114 (15 September 2008)

    The extensive and condition-dependent nature of epistasis among whole-genome duplicates in yeast
    G. Musso, M. Costanzo, M. Huangfu, A. M. Smith, J. Paw, B.-J. San Luis, C. Boone, G. Giaever, C. Nislow, A. Emili et al.
    Genome Res 18, 1092-1099 (1 July 2008)

    Plk1- and {beta}-TrCP-dependent degradation of Bora controls mitotic progression
    A. Seki, J. A. Coppinger, H. Du, C.-Y. Jang, J. R. Yates, and G. Fang
    JCB 181, 65-78 (3 April 2008)

    Genome-wide inference of protein interaction sites: lessons from the yeast high-quality negative protein-protein interaction dataset
    J. Guo, X. Wu, D.-Y. Zhang, and K. Lin
    Nucleic Acids Res 36, 2002-2011 (1 April 2008)

    Impact of systems biology on metabolic engineering of Saccharomyces cerevisiae
    J. Nielsen, and M. C. Jewett
    FEMS Yeast Res 8, 122-131 (1 February 2008)

    High-resolution timing of cell cycle-regulated gene expression
    M. Rowicka, A. Kudlicki, B. P. Tu, and Z. Otwinowski
    Proc. Natl. Acad. Sci. USA 104, 16892-16897 (23 October 2007)

    LICORN: learning cooperative regulation networks from gene expression data
    M. Elati, P. Neuvial, M. Bolotin-Fukuhara, E. Barillot, F. Radvanyi, and C. Rouveirol
    Bioinformatics 23, 2407-2414 (15 September 2007)

    Thematic review series: Systems Biology Approaches to Metabolic and Cardiovascular Disorders. Multi-organ whole-genome measurements and reverse engineering to uncover gene networks underlying complex traits
    J. Tegner, J. Skogsberg, and J. Bjorkegren
    J. Lipid Res. 48, 267-277 (1 February 2007)

    Transcriptional regulation of protein complexes within and across species
    K. Tan, T. Shlomi, H. Feizi, T. Ideker, and R. Sharan
    Proc. Natl. Acad. Sci. USA 104, 1283-1288 (23 January 2007)

    CellCircuits: a database of protein network models
    H. C. Mak, M. Daly, B. Gruebel, and T. Ideker
    Nucleic Acids Res 35, D538-D545 (12 January 2007)

    Relating Three-Dimensional Structures to Protein Networks Provides Evolutionary Insights
    P. M. Kim, L. J. Lu, Y. Xia, and M. B. Gerstein
    Science 314, 1938-1941 (22 December 2006)

    A Complex Oscillating Network of Signaling Genes Underlies the Mouse Segmentation Clock
    M.-L. Dequeant, E. Glynn, K. Gaudenz, M. Wahl, J. Chen, A. Mushegian, and O. Pourquie
    Science 314, 1595-1598 (8 December 2006)

    A Network-based Analysis of Polyanion-binding Proteins Utilizing Yeast Protein Arrays
    N. Salamat-Miller, J. Fang, C. W. Seidel, A. M. Smalter, Y. Assenov, M. Albrecht, and C. R. Middaugh
    MCP 5, 2263-2278 (1 December 2006)

    Genome-wide functional analysis of human cell-cycle regulators
    M. Mukherji, R. Bell, L. Supekova, Y. Wang, A. P. Orth, S. Batalov, L. Miraglia, D. Huesken, J. Lange, C. Martin et al.
    Proc. Natl. Acad. Sci. USA 103, 14819-14824 (3 October 2006)

    Global topological features of cancer proteins in the human interactome
    P. F. Jonsson, and P. A. Bates
    Bioinformatics 22, 2291-2297 (15 September 2006)

    The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle.
    T. Pramila, W. Wu, S. Miles, W. S. Noble, and L. L. Breeden
    Genes Dev. 20, 2266-2278 (15 August 2006)

    HURP controls spindle dynamics to promote proper interkinetochore tension and efficient kinetochore capture
    J. Wong, and G. Fang
    JCB 173, 879-891 (19 June 2006)

    Cell Wall Assembly in Saccharomyces cerevisiae
    G. Lesage, and H. Bussey
    Microbiol. Mol. Biol. Rev. 70, 317-343 (1 June 2006)

    The origins and evolution of functional modules: lessons from protein complexes
    J. B. Pereira-Leal, E. D. Levy, and S. A. Teichmann
    Phil Trans R Soc B 361, 507-517 (29 March 2006)

    Modelling in molecular biology: describing transcription regulatory networks at different scales
    T. Schlitt, and A. Brazma
    Phil Trans R Soc B 361, 483-494 (29 March 2006)

    Genome-wide prediction and characterization of interactions between transcription factors in Saccharomyces cerevisiae
    X. Yu, J. Lin, T. Masuda, N. Esumi, D. J. Zack, and J. Qian
    Nucleic Acids Res 34, 917-927 (6 February 2006)

    Yeast Protein Interactome topology provides framework for coordinated-functionality.
    A. X. C. N. Valente, and M. E. Cusick
    Nucleic Acids Res 34, 2812-2819 (1 January 2006)

    Prediction of yeast protein-protein interaction network: insights from the Gene Ontology and annotations.
    X. Wu, L. Zhu, J. Guo, D.-Y. Zhang, and K. Lin
    Nucleic Acids Res 34, 2137-2150 (1 January 2006)

    Ace2p contributes to fission yeast septin ring assembly by regulating mid2+ expression
    C. S. Petit, S. Mehta, R. H. Roberts, and K. L. Gould
    J. Cell Sci. 118, 5731-5742 (15 December 2005)

    Medusa: a simple tool for interaction graph analysis
    S. D. Hooper, and P. Bork
    Bioinformatics 21, 4432-4433 (15 December 2005)

    Expression Clustering Reveals Detailed Co-expression Patterns of Functionally Related Proteins during B Cell Differentiation: A Proteomic Study Using a Combination of One-Dimensional Gel Electrophoresis, LC-MS/MS, and Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC)
    E. P. Romijn, C. Christis, M. Wieffer, J. W. Gouw, A. Fullaondo, P. van der Sluijs, I. Braakman, and A. J. R. Heck
    MCP 4, 1297-1310 (1 September 2005)

    Metabolic Engineering in the -omics Era: Elucidating and Modulating Regulatory Networks
    G. N. Vemuri, and A. A. Aristidou
    Microbiol. Mol. Biol. Rev. 69, 197-216 (1 June 2005)

    Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882