Evolution and topology in the yeast protein interaction network.

The integrity of the yeast protein-protein interaction network is maintained by a few highly connected proteins, or hubs, which hold the numerous less-connected proteins together. The structural importance and the increased essentiality of these proteins suggest that they are likely to be conserved in evolution, implying a strong relationship between the number of interactions and their evolutionary distance to its orthologs in other organisms. The existence of this coherence was recently reported to strongly depend on the quality of the protein interaction and orthologs data. Here, we introduce a novel method, the evolutionary excess retention (ER), allowing us to uncover a robust and strong correlation between the conservation, essentiality, and connectivity of a yeast protein. We conclude that the relevance of the hubs for the network integrity is simultaneously reflected by a considerable probability of simultaneously being evolutionarily conserved and essential, an observation that does not have an equivalent for nonessential proteins. Providing a thorough assessment of the impact noisy and incomplete data have on our findings, we conclude that our results are largely insensitive to the quality of the utilized data.

[1]  Laurence D. Hurst,et al.  Do essential genes evolve slowly? , 1999, Current Biology.

[2]  Albert-László Barabási,et al.  Error and attack tolerance of complex networks , 2000, Nature.

[3]  T. Ito,et al.  Toward a protein-protein interaction map of the budding yeast: A comprehensive system to examine two-hybrid interactions in all possible combinations between the yeast proteins. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Christian E. V. Storm,et al.  Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. , 2001, Journal of molecular biology.

[5]  A. Barabasi,et al.  Lethality and centrality in protein networks , 2001, Nature.

[6]  Jong H. Park,et al.  Mapping protein family interactions: intramolecular and intermolecular protein family interaction repertoires in the PDB and yeast. , 2001, Journal of molecular biology.

[7]  L. Koski,et al.  The Closest BLAST Hit Is Often Not the Nearest Neighbor , 2001, Journal of Molecular Evolution.

[8]  Marek S. Skrzypek,et al.  YPDTM, PombePDTM and WormPDTM: model organism volumes of the BioKnowledgeTM Library, an integrated resource for protein information , 2001, Nucleic Acids Res..

[9]  S. Fields,et al.  Networking proteins in yeast , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[10]  R. Ozawa,et al.  A comprehensive two-hybrid analysis to explore the yeast protein interactome , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A. Wagner The yeast protein interaction network evolves rapidly and contains few redundant duplicate genes. , 2001, Molecular biology and evolution.

[12]  Gary D Bader,et al.  Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry , 2002, Nature.

[13]  E. Koonin,et al.  Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. , 2002, Genome research.

[14]  Ioannis Xenarios,et al.  DIP, the Database of Interacting Proteins: a research tool for studying cellular networks of protein interactions , 2002, Nucleic Acids Res..

[15]  P. Bork,et al.  Functional organization of the yeast proteome by systematic analysis of protein complexes , 2002, Nature.

[16]  B. Snel,et al.  Comparative assessment of large-scale data sets of protein–protein interactions , 2002, Nature.

[17]  A. E. Hirsh,et al.  Evolutionary Rate in the Protein Interaction Network , 2002, Science.

[18]  Stefan Wuchty,et al.  Interaction and domain networks of yeast , 2002, Proteomics.

[19]  Eugene V Koonin,et al.  No simple dependence between protein evolution rate and the number of protein-protein interactions: only the most prolific interactors tend to evolve slowly , 2003, BMC Evolutionary Biology.

[20]  Dennis P Wall,et al.  A simple dependence between protein evolution rate and the number of protein-protein interactions , 2003, BMC Evolutionary Biology.

[21]  D. Goldberg,et al.  Assessing experimentally derived interactions in a small world , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  D. P. Wall,et al.  Detecting putative orthologs , 2003, Bioinform..

[23]  Gary G. Yen,et al.  Fitting to the Power-Law Distribution , 2004 .