SH3 interactome conserves general function over specific form

Xiaofeng Xin; David Gfeller; Jackie Cheng; Raffi Tonikian; Lin Sun; Ailan Guo; Lianet Lopez; Alevtina Pavlenco; Adenrele Akintobi; Yingnan Zhang; Jean François Rual; Bridget Currell; Somasekar Seshagiri; Tong Hao; Xinping Yang; Yun A. Shen; Kourosh Salehi-Ashtiani; Jingjing Li; Aaron T. Cheng; Dryden Bouamalay; Adrien Lugari; David E. Hill; Mark L. Grimes; David G. Drubin; Barth D. Grant; Marc Vidal; Charles Boone; Sachdev S. Sidhu; Gary D. Bader

doi:10.1038/msb.2013.9

SH3 interactome conserves general function over specific form

Xiaofeng Xin
, David Gfeller
, Jackie Cheng
, Raffi Tonikian
, Lin Sun
, Ailan Guo
, Lianet Lopez
, Alevtina Pavlenco
, Adenrele Akintobi
, Yingnan Zhang
, Jean François Rual
, Bridget Currell
, Somasekar Seshagiri
, Tong Hao
, Xinping Yang
, Yun A. Shen
, Kourosh Salehi-Ashtiani
, Jingjing Li
, Aaron T. Cheng
, Dryden Bouamalay

Adrien Lugari, David E. Hill, Mark L. Grimes, David G. Drubin, Barth D. Grant, Marc Vidal, Charles Boone, Sachdev S. Sidhu, Gary D. Bader

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

57 Scopus citations

Abstract

Src homology 3 (SH3) domains bind peptides to mediate protein-protein interactions that assemble and regulate dynamic biological processes. We surveyed the repertoire of SH3 binding specificity using peptide phage display in a metazoan, the worm Caenorhabditis elegans, and discovered that it structurally mirrors that of the budding yeast Saccharomyces cerevisiae. We then mapped the worm SH3 interactome using stringent yeast two-hybrid and compared it with the equivalent map for yeast. We found that the worm SH3 interactome resembles the analogous yeast network because it is significantly enriched for proteins with roles in endocytosis. Nevertheless, orthologous SH3 domain-mediated interactions are highly rewired. Our results suggest a model of network evolution where general function of the SH3 domain network is conserved over its specific form.

Original language	English
Article number	652
Journal	Molecular Systems Biology
Volume	9
DOIs	https://doi.org/10.1038/msb.2013.9
State	Published - 2013

Funding

Funder number
R01GM067237

Keywords

SH3 domains
network evolution
phage display
protein interaction conservation
yeast two-hybrid

Access to Document

10.1038/msb.2013.9

Cite this

Xin, X., Gfeller, D., Cheng, J., Tonikian, R., Sun, L., Guo, A., Lopez, L., Pavlenco, A., Akintobi, A., Zhang, Y., Rual, J. F., Currell, B., Seshagiri, S., Hao, T., Yang, X., Shen, Y. A., Salehi-Ashtiani, K., Li, J., Cheng, A. T., ... Bader, G. D. (2013). SH3 interactome conserves general function over specific form. Molecular Systems Biology, 9, Article 652. https://doi.org/10.1038/msb.2013.9

@article{ddbc0469e0c045caaffbdbaae3a892bf,

title = "SH3 interactome conserves general function over specific form",

abstract = "Src homology 3 (SH3) domains bind peptides to mediate protein-protein interactions that assemble and regulate dynamic biological processes. We surveyed the repertoire of SH3 binding specificity using peptide phage display in a metazoan, the worm Caenorhabditis elegans, and discovered that it structurally mirrors that of the budding yeast Saccharomyces cerevisiae. We then mapped the worm SH3 interactome using stringent yeast two-hybrid and compared it with the equivalent map for yeast. We found that the worm SH3 interactome resembles the analogous yeast network because it is significantly enriched for proteins with roles in endocytosis. Nevertheless, orthologous SH3 domain-mediated interactions are highly rewired. Our results suggest a model of network evolution where general function of the SH3 domain network is conserved over its specific form.",

keywords = "SH3 domains, network evolution, phage display, protein interaction conservation, yeast two-hybrid",

author = "Xiaofeng Xin and David Gfeller and Jackie Cheng and Raffi Tonikian and Lin Sun and Ailan Guo and Lianet Lopez and Alevtina Pavlenco and Adenrele Akintobi and Yingnan Zhang and Rual, \{Jean Fran{\c c}ois\} and Bridget Currell and Somasekar Seshagiri and Tong Hao and Xinping Yang and Shen, \{Yun A.\} and Kourosh Salehi-Ashtiani and Jingjing Li and Cheng, \{Aaron T.\} and Dryden Bouamalay and Adrien Lugari and Hill, \{David E.\} and Grimes, \{Mark L.\} and Drubin, \{David G.\} and Grant, \{Barth D.\} and Marc Vidal and Charles Boone and Sidhu, \{Sachdev S.\} and Bader, \{Gary D.\}",

year = "2013",

doi = "10.1038/msb.2013.9",

language = "English",

volume = "9",

journal = "Molecular Systems Biology",

issn = "1744-4292",

publisher = "Springer Science and Business Media Deutschland GmbH",

}

Xin, X, Gfeller, D, Cheng, J, Tonikian, R, Sun, L, Guo, A, Lopez, L, Pavlenco, A, Akintobi, A, Zhang, Y, Rual, JF, Currell, B, Seshagiri, S, Hao, T, Yang, X, Shen, YA, Salehi-Ashtiani, K, Li, J, Cheng, AT, Bouamalay, D, Lugari, A, Hill, DE, Grimes, ML, Drubin, DG, Grant, BD, Vidal, M, Boone, C, Sidhu, SS & Bader, GD 2013, 'SH3 interactome conserves general function over specific form', Molecular Systems Biology, vol. 9, 652. https://doi.org/10.1038/msb.2013.9

TY - JOUR

T1 - SH3 interactome conserves general function over specific form

AU - Xin, Xiaofeng

AU - Gfeller, David

AU - Cheng, Jackie

AU - Tonikian, Raffi

AU - Sun, Lin

AU - Guo, Ailan

AU - Lopez, Lianet

AU - Pavlenco, Alevtina

AU - Akintobi, Adenrele

AU - Zhang, Yingnan

AU - Rual, Jean François

AU - Currell, Bridget

AU - Seshagiri, Somasekar

AU - Hao, Tong

AU - Yang, Xinping

AU - Shen, Yun A.

AU - Salehi-Ashtiani, Kourosh

AU - Li, Jingjing

AU - Cheng, Aaron T.

AU - Bouamalay, Dryden

AU - Lugari, Adrien

AU - Hill, David E.

AU - Grimes, Mark L.

AU - Drubin, David G.

AU - Grant, Barth D.

AU - Vidal, Marc

AU - Boone, Charles

AU - Sidhu, Sachdev S.

AU - Bader, Gary D.

PY - 2013

Y1 - 2013

N2 - Src homology 3 (SH3) domains bind peptides to mediate protein-protein interactions that assemble and regulate dynamic biological processes. We surveyed the repertoire of SH3 binding specificity using peptide phage display in a metazoan, the worm Caenorhabditis elegans, and discovered that it structurally mirrors that of the budding yeast Saccharomyces cerevisiae. We then mapped the worm SH3 interactome using stringent yeast two-hybrid and compared it with the equivalent map for yeast. We found that the worm SH3 interactome resembles the analogous yeast network because it is significantly enriched for proteins with roles in endocytosis. Nevertheless, orthologous SH3 domain-mediated interactions are highly rewired. Our results suggest a model of network evolution where general function of the SH3 domain network is conserved over its specific form.

AB - Src homology 3 (SH3) domains bind peptides to mediate protein-protein interactions that assemble and regulate dynamic biological processes. We surveyed the repertoire of SH3 binding specificity using peptide phage display in a metazoan, the worm Caenorhabditis elegans, and discovered that it structurally mirrors that of the budding yeast Saccharomyces cerevisiae. We then mapped the worm SH3 interactome using stringent yeast two-hybrid and compared it with the equivalent map for yeast. We found that the worm SH3 interactome resembles the analogous yeast network because it is significantly enriched for proteins with roles in endocytosis. Nevertheless, orthologous SH3 domain-mediated interactions are highly rewired. Our results suggest a model of network evolution where general function of the SH3 domain network is conserved over its specific form.

KW - SH3 domains

KW - network evolution

KW - phage display

KW - protein interaction conservation

KW - yeast two-hybrid

UR - https://www.scopus.com/pages/publications/84876580944

U2 - 10.1038/msb.2013.9

DO - 10.1038/msb.2013.9

M3 - Article

C2 - 23549480

AN - SCOPUS:84876580944

SN - 1744-4292

VL - 9

JO - Molecular Systems Biology

JF - Molecular Systems Biology

M1 - 652

ER -

SH3 interactome conserves general function over specific form

Abstract

Funding

Keywords

Access to Document

Other files and links

Fingerprint

Cite this