Protein function, connectivity, and duplicability in yeast.

Protein-protein interaction networks have evolved mainly through connectivity rewiring and gene duplication. However, how protein function influences these processes and how a network grows in time have not been well studied. Using protein-protein interaction data and genomic data from the budding yeast, we first examined whether there is a correlation between the age and connectivity of yeast proteins. A steady increase in connectivity with protein age is observed for yeast proteins except for those that can be traced back to Eubacteria. Second, we investigated whether protein connectivity and duplicability vary with gene function. We found a higher average duplicability for proteins interacting with external environments than for proteins localized within intracellular compartments. For example, proteins that function in the cell periphery (mainly transporters) show a high duplicability but are lowly connected. Conversely, proteins that function within the nucleus (e.g., transcription, RNA and DNA metabolisms, and ribosome biogenesis and assembly) are highly connected but have a low duplicability. Finally, we found a negative correlation between protein connectivity and duplicability.

[1]  Hunter B. Fraser,et al.  Modularity and evolutionary constraint on proteins , 2005, Nature Genetics.

[2]  E. Levanon,et al.  Evolution of multicellularity in Metazoa: comparative analysis of the subcellular localization of proteins in Saccharomyces, Drosophila and Caenorhabditis , 2004, Cell biology international.

[3]  Massimo Marchiori,et al.  Error and attacktolerance of complex network s , 2004 .

[4]  B. André,et al.  A genomic view of yeast membrane transporters. , 2001, Current opinion in cell biology.

[5]  Ronald W. Davis,et al.  Role of duplicate genes in genetic robustness against null mutations , 2003, Nature.

[6]  E. Koonin,et al.  Selection in the evolution of gene duplications , 2002, Genome Biology.

[7]  Sandra Tenreiro,et al.  The multidrug resistance transporters of the major facilitator superfamily, 6 years after disclosure of Saccharomyces cerevisiae genome sequence. , 2002, Journal of biotechnology.

[8]  B. Dujon,et al.  Phylogenetic classification of transporters and other membrane proteins from Saccharomyces cerevisiae , 2002, Functional & Integrative Genomics.

[9]  C. Pál,et al.  Dosage sensitivity and the evolution of gene families in yeast , 2003, Nature.

[10]  Gary D Bader,et al.  A Combined Experimental and Computational Strategy to Define Protein Interaction Networks for Peptide Recognition Modules , 2001, Science.

[11]  Lan V. Zhang,et al.  Evidence for dynamically organized modularity in the yeast protein–protein interaction network , 2004, Nature.

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

[13]  D. Gevers,et al.  Gene duplication and biased functional retention of paralogs in bacterial genomes. , 2004, Trends in microbiology.

[14]  E. O’Shea,et al.  Global analysis of protein expression in yeast , 2003, Nature.

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

[16]  M. Pilar Francino,et al.  An adaptive radiation model for the origin of new gene functions , 2005 .

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

[18]  R. Veitia,et al.  Exploring the etiology of haploinsufficiency. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[20]  B. Birren,et al.  Sequencing and comparison of yeast species to identify genes and regulatory elements , 2003, Nature.

[21]  B. Dujon,et al.  Genome evolution in yeasts , 2004, Nature.

[22]  Richard W. Lusk,et al.  Organismal complexity, protein complexity, and gene duplicability , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Wen-Hsiung Li,et al.  Evolution of the yeast protein interaction network , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  James R. Knight,et al.  A comprehensive analysis of protein–protein interactions in Saccharomyces cerevisiae , 2000, Nature.

[25]  L. Fulton,et al.  Finding Functional Features in Saccharomyces Genomes by Phylogenetic Footprinting , 2003, Science.

[26]  Erik L. L. Sonnhammer,et al.  Inparanoid: a comprehensive database of eukaryotic orthologs , 2004, Nucleic Acids Res..

[27]  M. Gerstein,et al.  Structure and evolution of transcriptional regulatory networks. , 2004, Current opinion in structural biology.

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

[29]  E. Wolf,et al.  A computationally directed screen identifying interacting coiled coils from Saccharomyces cerevisiae. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Fields,et al.  A protein interaction map for cell polarity development , 2001, The Journal of cell biology.

[31]  Natalia Maltsev,et al.  Higher Gene Duplicabilities for Metabolic Proteins Than for Nonmetabolic Proteins in Yeast and E. coli , 2004, Journal of Molecular Evolution.

[32]  Ian Dix,et al.  Yeast Yeast 2000; 17: 95±110. Research Article , 2000 .

[33]  J. Rothberg,et al.  Gaining confidence in high-throughput protein interaction networks , 2004, Nature Biotechnology.

[34]  Albert,et al.  Topology of evolving networks: local events and universality , 2000, Physical review letters.

[35]  A. Goffeau,et al.  The pleitropic drug ABC transporters from Saccharomyces cerevisiae. , 2001, Journal of molecular microbiology and biotechnology.

[36]  Sarah A Teichmann,et al.  Novel specificities emerge by stepwise duplication of functional modules. , 2005, Genome research.

[37]  Ronald W. Davis,et al.  Functional profiling of the Saccharomyces cerevisiae genome , 2002, Nature.

[38]  Jianzhi Zhang,et al.  Gene Complexity and Gene Duplicability , 2005, Current Biology.

[39]  R. Solé,et al.  Evolving protein interaction networks through gene duplication. , 2003, Journal of Theoretical Biology.

[40]  S. Wuchty.  Evolution and topology in the yeast protein interaction network. , 2004, Genome research.

[41]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[42]  Victor Kunin,et al.  Functional evolution of the yeast protein interaction network. , 2004, Molecular biology and evolution.

[43]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[44]  E. O’Shea,et al.  Global analysis of protein localization in budding yeast , 2003, Nature.

[45]  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.