Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions

Rocco Moretti; Sarel J Fleishman; Rudi Agius; Mieczyslaw Torchala; Paul A Bates; Panagiotis L Kastritis; João Garcia Lopes Maia Rodrigues; Mikaël Trellet; Alexandre M J J Bonvin; Meng Cui; Marianne Rooman; Dimitri Gillis; Yves Dehouck; Iain Moal; Miguel Romero-Durana; Laura Perez-Cano; Chiara Pallara; Brian Jimenez; Juan Fernandez-Recio; Samuel Flores; Michael Pacella; Krishna Praneeth Kilambi; Jeffrey J Gray; Petr Popov; Sergei Grudinin; Juan Esquivel-Rodríguez; Daisuke Kihara; Nan Zhao; Dmitry Korkin; Xiaolei Zhu; Omar N A Demerdash; Julie C Mitchell; Eiji Kanamori; Yuko Tsuchiya; Haruki Nakamura; Hasup Lee; Hahnbeom Park; Chaok Seok; Jamica Sarmiento; Shide Liang; Shusuke Teraguchi; Daron M Standley; Hiromitsu Shimoyama; Genki Terashi; Mayuko Takeda-Shitaka; Mitsuo Iwadate; Hideaki Umeyama; Dmitri Beglov; David R Hall; Dima Kozakov; Sandor Vajda; Brian G Pierce; Howook Hwang; Thom Vreven; Zhiping Weng; Yangyu Huang; Haotian Li; Xiufeng Yang; Xiaofeng Ji; Shiyong Liu; Yi Xiao; Martin Zacharias; Sanbo Qin; Huan-Xiang Zhou; Sheng-You Huang; Xiaoqin Zou; Sameer Velankar; Joël Janin; Shoshana J Wodak; David Baker; João Garcia Lopes Maia Rodrigues

doi:10.1002/prot.24356

Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions

Rocco Moretti, Sarel J Fleishman, Rudi Agius, Mieczyslaw Torchala, Paul A Bates, Panagiotis L Kastritis, João Garcia Lopes Maia Rodrigues, Mikaël Trellet, Alexandre M J J Bonvin, Meng Cui, Marianne Rooman, Dimitri Gillis, Yves Dehouck, Iain Moal, Miguel Romero-Durana, Laura Perez-Cano, Chiara Pallara, Brian Jimenez, Juan Fernandez-Recio, Samuel FloresMichael Pacella, Krishna Praneeth Kilambi, Jeffrey J Gray, Petr Popov, Sergei Grudinin, Juan Esquivel-Rodríguez, Daisuke Kihara, Nan Zhao, Dmitry Korkin, Xiaolei Zhu, Omar N A Demerdash, Julie C Mitchell, Eiji Kanamori, Yuko Tsuchiya, Haruki Nakamura, Hasup Lee, Hahnbeom Park, Chaok Seok, Jamica Sarmiento, Shide Liang, Shusuke Teraguchi, Daron M Standley, Hiromitsu Shimoyama, Genki Terashi, Mayuko Takeda-Shitaka, Mitsuo Iwadate, Hideaki Umeyama, Dmitri Beglov, David R Hall, Dima Kozakov, Sandor Vajda, Brian G Pierce, Howook Hwang, Thom Vreven, Zhiping Weng, Yangyu Huang, Haotian Li, Xiufeng Yang, Xiaofeng Ji, Shiyong Liu, Yi Xiao, Martin Zacharias, Sanbo Qin, Huan-Xiang Zhou, Sheng-You Huang, Xiaoqin Zou, Sameer Velankar, Joël Janin, Shoshana J Wodak, David Baker, João Garcia Lopes Maia Rodrigues

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Community-wide blind prediction experiments such as CAPRI and CASP provide an objective measure of the current state of predictive methodology. Here we describe a community-wide assessment of methods to predict the effects of mutations on protein-protein interactions. Twenty-two groups predicted the effects of comprehensive saturation mutagenesis for two designed influenza hemagglutinin binders and the results were compared with experimental yeast display enrichment data obtained using deep sequencing. The most successful methods explicitly considered the effects of mutation on monomer stability in addition to binding affinity, carried out explicit side-chain sampling and backbone relaxation, evaluated packing, electrostatic, and solvation effects, and correctly identified around a third of the beneficial mutations. Much room for improvement remains for even the best techniques, and large-scale fitness landscapes should continue to provide an excellent test bed for continued evaluation of both existing and new prediction methodologies.

Original language	English
Pages (from-to)	1980-1987
Number of pages	8
Journal	Proteins: Structure function and bioinformatics
Volume	81
Issue number	11
DOIs	https://doi.org/10.1002/prot.24356
Publication status	Published - Nov 2013

Keywords

Algorithms
Databases, Protein
Mutation
Protein Binding
Protein Interaction Mapping
CAPRI
hemagglutinin
binding
deep mutational scanning
yeast display

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Moretti, R., Fleishman, S. J., Agius, R., Torchala, M., Bates, P. A., Kastritis, P. L., Garcia Lopes Maia Rodrigues, J., Trellet, M., Bonvin, A. M. J. J., Cui, M., Rooman, M., Gillis, D., Dehouck, Y., Moal, I., Romero-Durana, M., Perez-Cano, L., Pallara, C., Jimenez, B., Fernandez-Recio, J., ... Garcia Lopes Maia Rodrigues, J. (2013). Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions. Proteins: Structure function and bioinformatics, 81(11), 1980-1987. https://doi.org/10.1002/prot.24356

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title = "Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions",

abstract = "Community-wide blind prediction experiments such as CAPRI and CASP provide an objective measure of the current state of predictive methodology. Here we describe a community-wide assessment of methods to predict the effects of mutations on protein-protein interactions. Twenty-two groups predicted the effects of comprehensive saturation mutagenesis for two designed influenza hemagglutinin binders and the results were compared with experimental yeast display enrichment data obtained using deep sequencing. The most successful methods explicitly considered the effects of mutation on monomer stability in addition to binding affinity, carried out explicit side-chain sampling and backbone relaxation, evaluated packing, electrostatic, and solvation effects, and correctly identified around a third of the beneficial mutations. Much room for improvement remains for even the best techniques, and large-scale fitness landscapes should continue to provide an excellent test bed for continued evaluation of both existing and new prediction methodologies.",

keywords = "Algorithms, Databases, Protein, Mutation, Protein Binding, Protein Interaction Mapping, CAPRI, hemagglutinin, binding, deep mutational scanning, yeast display",

author = "Rocco Moretti and Fleishman, {Sarel J} and Rudi Agius and Mieczyslaw Torchala and Bates, {Paul A} and Kastritis, {Panagiotis L} and {Garcia Lopes Maia Rodrigues}, Jo{\~a}o and Mika{\"e}l Trellet and Bonvin, {Alexandre M J J} and Meng Cui and Marianne Rooman and Dimitri Gillis and Yves Dehouck and Iain Moal and Miguel Romero-Durana and Laura Perez-Cano and Chiara Pallara and Brian Jimenez and Juan Fernandez-Recio and Samuel Flores and Michael Pacella and {Praneeth Kilambi}, Krishna and Gray, {Jeffrey J} and Petr Popov and Sergei Grudinin and Juan Esquivel-Rodr{\'i}guez and Daisuke Kihara and Nan Zhao and Dmitry Korkin and Xiaolei Zhu and Demerdash, {Omar N A} and Mitchell, {Julie C} and Eiji Kanamori and Yuko Tsuchiya and Haruki Nakamura and Hasup Lee and Hahnbeom Park and Chaok Seok and Jamica Sarmiento and Shide Liang and Shusuke Teraguchi and Standley, {Daron M} and Hiromitsu Shimoyama and Genki Terashi and Mayuko Takeda-Shitaka and Mitsuo Iwadate and Hideaki Umeyama and Dmitri Beglov and Hall, {David R} and Dima Kozakov and Sandor Vajda and Pierce, {Brian G} and Howook Hwang and Thom Vreven and Zhiping Weng and Yangyu Huang and Haotian Li and Xiufeng Yang and Xiaofeng Ji and Shiyong Liu and Yi Xiao and Martin Zacharias and Sanbo Qin and Huan-Xiang Zhou and Sheng-You Huang and Xiaoqin Zou and Sameer Velankar and Jo{\"e}l Janin and Wodak, {Shoshana J} and David Baker and {Garcia Lopes Maia Rodrigues}, Jo{\~a}o",

note = "{\textcopyright} 2013 Wiley Periodicals, Inc.",

year = "2013",

month = nov,

doi = "10.1002/prot.24356",

language = "English",

volume = "81",

pages = "1980--1987",

journal = "Proteins: Structure function and bioinformatics",

issn = "0887-3585",

publisher = "Wiley-Liss Inc.",

number = "11",

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Moretti, R, Fleishman, SJ, Agius, R, Torchala, M, Bates, PA, Kastritis, PL, Garcia Lopes Maia Rodrigues, J, Trellet, M, Bonvin, AMJJ, Cui, M, Rooman, M, Gillis, D, Dehouck, Y, Moal, I, Romero-Durana, M, Perez-Cano, L, Pallara, C, Jimenez, B, Fernandez-Recio, J, Flores, S, Pacella, M, Praneeth Kilambi, K, Gray, JJ, Popov, P, Grudinin, S, Esquivel-Rodríguez, J, Kihara, D, Zhao, N, Korkin, D, Zhu, X, Demerdash, ONA, Mitchell, JC, Kanamori, E, Tsuchiya, Y, Nakamura, H, Lee, H, Park, H, Seok, C, Sarmiento, J, Liang, S, Teraguchi, S, Standley, DM, Shimoyama, H, Terashi, G, Takeda-Shitaka, M, Iwadate, M, Umeyama, H, Beglov, D, Hall, DR, Kozakov, D, Vajda, S, Pierce, BG, Hwang, H, Vreven, T, Weng, Z, Huang, Y, Li, H, Yang, X, Ji, X, Liu, S, Xiao, Y, Zacharias, M, Qin, S, Zhou, H-X, Huang, S-Y, Zou, X, Velankar, S, Janin, J, Wodak, SJ, Baker, D & Garcia Lopes Maia Rodrigues, J 2013, 'Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions', Proteins: Structure function and bioinformatics, vol. 81, no. 11, pp. 1980-1987. https://doi.org/10.1002/prot.24356

TY - JOUR

T1 - Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions

AU - Moretti, Rocco

AU - Fleishman, Sarel J

AU - Agius, Rudi

AU - Torchala, Mieczyslaw

AU - Bates, Paul A

AU - Kastritis, Panagiotis L

AU - Garcia Lopes Maia Rodrigues, João

AU - Trellet, Mikaël

AU - Bonvin, Alexandre M J J

AU - Cui, Meng

AU - Rooman, Marianne

AU - Gillis, Dimitri

AU - Dehouck, Yves

AU - Moal, Iain

AU - Romero-Durana, Miguel

AU - Perez-Cano, Laura

AU - Pallara, Chiara

AU - Jimenez, Brian

AU - Fernandez-Recio, Juan

AU - Flores, Samuel

AU - Pacella, Michael

AU - Praneeth Kilambi, Krishna

AU - Gray, Jeffrey J

AU - Popov, Petr

AU - Grudinin, Sergei

AU - Esquivel-Rodríguez, Juan

AU - Kihara, Daisuke

AU - Zhao, Nan

AU - Korkin, Dmitry

AU - Zhu, Xiaolei

AU - Demerdash, Omar N A

AU - Mitchell, Julie C

AU - Kanamori, Eiji

AU - Tsuchiya, Yuko

AU - Nakamura, Haruki

AU - Lee, Hasup

AU - Park, Hahnbeom

AU - Seok, Chaok

AU - Sarmiento, Jamica

AU - Liang, Shide

AU - Teraguchi, Shusuke

AU - Standley, Daron M

AU - Shimoyama, Hiromitsu

AU - Terashi, Genki

AU - Takeda-Shitaka, Mayuko

AU - Iwadate, Mitsuo

AU - Umeyama, Hideaki

AU - Beglov, Dmitri

AU - Hall, David R

AU - Kozakov, Dima

AU - Vajda, Sandor

AU - Pierce, Brian G

AU - Hwang, Howook

AU - Vreven, Thom

AU - Weng, Zhiping

AU - Huang, Yangyu

AU - Li, Haotian

AU - Yang, Xiufeng

AU - Ji, Xiaofeng

AU - Liu, Shiyong

AU - Xiao, Yi

AU - Zacharias, Martin

AU - Qin, Sanbo

AU - Zhou, Huan-Xiang

AU - Huang, Sheng-You

AU - Zou, Xiaoqin

AU - Velankar, Sameer

AU - Janin, Joël

AU - Wodak, Shoshana J

AU - Baker, David

AU - Garcia Lopes Maia Rodrigues, João

PY - 2013/11

Y1 - 2013/11

N2 - Community-wide blind prediction experiments such as CAPRI and CASP provide an objective measure of the current state of predictive methodology. Here we describe a community-wide assessment of methods to predict the effects of mutations on protein-protein interactions. Twenty-two groups predicted the effects of comprehensive saturation mutagenesis for two designed influenza hemagglutinin binders and the results were compared with experimental yeast display enrichment data obtained using deep sequencing. The most successful methods explicitly considered the effects of mutation on monomer stability in addition to binding affinity, carried out explicit side-chain sampling and backbone relaxation, evaluated packing, electrostatic, and solvation effects, and correctly identified around a third of the beneficial mutations. Much room for improvement remains for even the best techniques, and large-scale fitness landscapes should continue to provide an excellent test bed for continued evaluation of both existing and new prediction methodologies.

AB - Community-wide blind prediction experiments such as CAPRI and CASP provide an objective measure of the current state of predictive methodology. Here we describe a community-wide assessment of methods to predict the effects of mutations on protein-protein interactions. Twenty-two groups predicted the effects of comprehensive saturation mutagenesis for two designed influenza hemagglutinin binders and the results were compared with experimental yeast display enrichment data obtained using deep sequencing. The most successful methods explicitly considered the effects of mutation on monomer stability in addition to binding affinity, carried out explicit side-chain sampling and backbone relaxation, evaluated packing, electrostatic, and solvation effects, and correctly identified around a third of the beneficial mutations. Much room for improvement remains for even the best techniques, and large-scale fitness landscapes should continue to provide an excellent test bed for continued evaluation of both existing and new prediction methodologies.

KW - Algorithms

KW - Databases, Protein

KW - Mutation

KW - Protein Binding

KW - Protein Interaction Mapping

KW - CAPRI

KW - hemagglutinin

KW - binding

KW - deep mutational scanning

KW - yeast display

U2 - 10.1002/prot.24356

DO - 10.1002/prot.24356

M3 - Article

C2 - 23843247

SN - 0887-3585

VL - 81

SP - 1980

EP - 1987

JO - Proteins: Structure function and bioinformatics

JF - Proteins: Structure function and bioinformatics

IS - 11

ER -

Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions

Abstract

Keywords

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