An inter‐species protein–protein interaction network across vast evolutionary distance

Abstract In cellular systems, biophysical interactions between macromolecules underlie a complex web of functional interactions. How biophysical and functional networks are coordinated, whether all biophysical interactions correspond to functional interactions, and how such biophysical‐versus‐functi...

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Main Authors: Quan Zhong, Samuel J Pevzner, Tong Hao, Yang Wang, Roberto Mosca, Jörg Menche, Mikko Taipale, Murat Taşan, Changyu Fan, Xinping Yang, Patrick Haley, Ryan R Murray, Flora Mer, Fana Gebreab, Stanley Tam, Andrew MacWilliams, Amélie Dricot, Patrick Reichert, Balaji Santhanam, Lila Ghamsari, Michael A Calderwood, Thomas Rolland, Benoit Charloteaux, Susan Lindquist, Albert‐László Barabási, David E Hill, Patrick Aloy, Michael E Cusick, Yu Xia, Frederick P Roth, Marc Vidal
Format: Article
Language:English
Published: Springer Nature 2016-04-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20156484
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author Quan Zhong
Samuel J Pevzner
Tong Hao
Yang Wang
Roberto Mosca
Jörg Menche
Mikko Taipale
Murat Taşan
Changyu Fan
Xinping Yang
Patrick Haley
Ryan R Murray
Flora Mer
Fana Gebreab
Stanley Tam
Andrew MacWilliams
Amélie Dricot
Patrick Reichert
Balaji Santhanam
Lila Ghamsari
Michael A Calderwood
Thomas Rolland
Benoit Charloteaux
Susan Lindquist
Albert‐László Barabási
David E Hill
Patrick Aloy
Michael E Cusick
Yu Xia
Frederick P Roth
Marc Vidal
author_facet Quan Zhong
Samuel J Pevzner
Tong Hao
Yang Wang
Roberto Mosca
Jörg Menche
Mikko Taipale
Murat Taşan
Changyu Fan
Xinping Yang
Patrick Haley
Ryan R Murray
Flora Mer
Fana Gebreab
Stanley Tam
Andrew MacWilliams
Amélie Dricot
Patrick Reichert
Balaji Santhanam
Lila Ghamsari
Michael A Calderwood
Thomas Rolland
Benoit Charloteaux
Susan Lindquist
Albert‐László Barabási
David E Hill
Patrick Aloy
Michael E Cusick
Yu Xia
Frederick P Roth
Marc Vidal
author_sort Quan Zhong
collection DOAJ
description Abstract In cellular systems, biophysical interactions between macromolecules underlie a complex web of functional interactions. How biophysical and functional networks are coordinated, whether all biophysical interactions correspond to functional interactions, and how such biophysical‐versus‐functional network coordination is shaped by evolutionary forces are all largely unanswered questions. Here, we investigate these questions using an “inter‐interactome” approach. We systematically probed the yeast and human proteomes for interactions between proteins from these two species and functionally characterized the resulting inter‐interactome network. After a billion years of evolutionary divergence, the yeast and human proteomes are still capable of forming a biophysical network with properties that resemble those of intra‐species networks. Although substantially reduced relative to intra‐species networks, the levels of functional overlap in the yeast–human inter‐interactome network uncover significant remnants of co‐functionality widely preserved in the two proteomes beyond human–yeast homologs. Our data support evolutionary selection against biophysical interactions between proteins with little or no co‐functionality. Such non‐functional interactions, however, represent a reservoir from which nascent functional interactions may arise.
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spelling doaj.art-8947e4a722804e5f9ef09601ac31c1ba2024-10-28T09:23:27ZengSpringer NatureMolecular Systems Biology1744-42922016-04-0112411910.15252/msb.20156484An inter‐species protein–protein interaction network across vast evolutionary distanceQuan Zhong0Samuel J Pevzner1Tong Hao2Yang Wang3Roberto Mosca4Jörg Menche5Mikko Taipale6Murat Taşan7Changyu Fan8Xinping Yang9Patrick Haley10Ryan R Murray11Flora Mer12Fana Gebreab13Stanley Tam14Andrew MacWilliams15Amélie Dricot16Patrick Reichert17Balaji Santhanam18Lila Ghamsari19Michael A Calderwood20Thomas Rolland21Benoit Charloteaux22Susan Lindquist23Albert‐László Barabási24David E Hill25Patrick Aloy26Michael E Cusick27Yu Xia28Frederick P Roth29Marc Vidal30Center for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteJoint IRB‐BSC‐CRG Program in Computational Biology, Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and TechnologyCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteWhitehead Institute for Biomedical ResearchCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteWhitehead Institute for Biomedical ResearchCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteJoint IRB‐BSC‐CRG Program in Computational Biology, Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and TechnologyCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteCenter for Cancer Systems Biology (CCSB) and Department of Cancer Biology, Dana‐Farber Cancer InstituteAbstract In cellular systems, biophysical interactions between macromolecules underlie a complex web of functional interactions. How biophysical and functional networks are coordinated, whether all biophysical interactions correspond to functional interactions, and how such biophysical‐versus‐functional network coordination is shaped by evolutionary forces are all largely unanswered questions. Here, we investigate these questions using an “inter‐interactome” approach. We systematically probed the yeast and human proteomes for interactions between proteins from these two species and functionally characterized the resulting inter‐interactome network. After a billion years of evolutionary divergence, the yeast and human proteomes are still capable of forming a biophysical network with properties that resemble those of intra‐species networks. Although substantially reduced relative to intra‐species networks, the levels of functional overlap in the yeast–human inter‐interactome network uncover significant remnants of co‐functionality widely preserved in the two proteomes beyond human–yeast homologs. Our data support evolutionary selection against biophysical interactions between proteins with little or no co‐functionality. Such non‐functional interactions, however, represent a reservoir from which nascent functional interactions may arise.https://doi.org/10.15252/msb.20156484Cross‐species complementationNetwork evolutionSelection
spellingShingle Quan Zhong
Samuel J Pevzner
Tong Hao
Yang Wang
Roberto Mosca
Jörg Menche
Mikko Taipale
Murat Taşan
Changyu Fan
Xinping Yang
Patrick Haley
Ryan R Murray
Flora Mer
Fana Gebreab
Stanley Tam
Andrew MacWilliams
Amélie Dricot
Patrick Reichert
Balaji Santhanam
Lila Ghamsari
Michael A Calderwood
Thomas Rolland
Benoit Charloteaux
Susan Lindquist
Albert‐László Barabási
David E Hill
Patrick Aloy
Michael E Cusick
Yu Xia
Frederick P Roth
Marc Vidal
An inter‐species protein–protein interaction network across vast evolutionary distance
Molecular Systems Biology
Cross‐species complementation
Network evolution
Selection
title An inter‐species protein–protein interaction network across vast evolutionary distance
title_full An inter‐species protein–protein interaction network across vast evolutionary distance
title_fullStr An inter‐species protein–protein interaction network across vast evolutionary distance
title_full_unstemmed An inter‐species protein–protein interaction network across vast evolutionary distance
title_short An inter‐species protein–protein interaction network across vast evolutionary distance
title_sort inter species protein protein interaction network across vast evolutionary distance
topic Cross‐species complementation
Network evolution
Selection
url https://doi.org/10.15252/msb.20156484
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