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Reconstruction of ancestral protein interaction networks for the bZIP transcription factors.

ABSTRACT: As whole-genome protein-protein interaction datasets become available for a wide range of species, evolutionary biologists have the opportunity to address some of the unanswered questions surrounding the evolution of these complex systems. Protein interaction networks from divergent organisms may be compared to investigate how gene duplication, deletion, and rewiring processes have shaped the evolution of their contemporary structures. However, current approaches for comparing observed networks from multiple species lack the phylogenetic context necessary to reconstruct the evolutionary history of a network. Here we show how probabilistic modeling can provide a platform for the quantitative analysis of multiple protein interaction networks. We apply this technique to the reconstruction of ancestral networks for the bZIP family of transcription factors and find that excellent agreement is obtained with an alternative sequence-based method for the prediction of leucine zipper interactions. Further analysis shows our probabilistic method to be significantly more robust to the presence of noise in the observed network data than a simple parsimony-based approach. In addition, the integration of evidence over multiple species means that the same method may be used to improve the quality of noisy interaction data for extant species. The ancestral states of a protein interaction network have been reconstructed here by using an explicit probabilistic model of network evolution. We anticipate that this model will form the basis of more general methods for probing the evolutionary history of biochemical networks.

SUBMITTER: Pinney JW

PROVIDER: S-EPMC2154451 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Cellular functions are based on the complex interplay of proteins, therefore the structure and dynamics of these protein-protein interaction (PPI) networks are the key to the functional understanding of cells. In the last years, large-scale PPI networks of several model organisms were investigated. A number of theoretical models have been developed to explain both the network formation and the current structure. Favored are models based on duplication and divergence of genes, as they most closely represent the biological foundation of network evolution. However, studies are often based on simulated instead of empirical data or they cover only single organisms. Methodological improvements now allow the analysis of PPI networks of multiple organisms simultaneously as well as the direct modeling of ancestral networks. This provides the opportunity to challenge existing assumptions on network evolution. We utilized present-day PPI networks from integrated datasets of seven model organisms and developed a theoretical and bioinformatic framework for studying the evolutionary dynamics of PPI networks. A novel filtering approach using percolation analysis was developed to remove low confidence interactions based on topological constraints. We then reconstructed the ancient PPI networks of different ancestors, for which the ancestral proteomes, as well as the ancestral interactions, were inferred. Ancestral proteins were reconstructed using orthologous groups on different evolutionary levels. A stochastic approach, using the duplication-divergence model, was developed for estimating the probabilities of ancient interactions from today's PPI networks. The growth rates for nodes, edges, sizes and modularities of the networks indicate multiplicative growth and are consistent with the results from independent static analysis. Our results support the duplication-divergence model of evolution and indicate fractality and multiplicative growth as general properties of the PPI network structure and dynamics.

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Reconstruction of ancestral protein interaction networks for the bZIP transcription factors.

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