Next-generation large-scale binary protein interaction network for Drosophila melanogaster

Hong Wen Tang; Kerstin Spirohn; Yanhui Hu; Tong Hao; István A. Kovács; Yue Gao; Richard Binari; Donghui Yang-Zhou; Kenneth H. Wan; Joel S. Bader; Dawit Balcha; Wenting Bian; Benjamin W. Booth; Atina G. Coté; Steffi de Rouck; Alice Desbuleux; Kah Yong Goh; Dae Kyum Kim; Jennifer J. Knapp; Wen Xing Lee; Irma Lemmens; Cathleen Li; Mian Li; Roujia Li; Hyobin Julianne Lim; Yifang Liu; Katja Luck; Dylan Markey; Carl Pollis; Sudharshan Rangarajan; Jonathan Rodiger; Sadie Schlabach; Yun Shen; Dayag Sheykhkarimli; Bridget TeeKing; Frederick P. Roth; Jan Tavernier; Michael A. Calderwood; David E. Hill; Susan E. Celniker; Marc Vidal; Norbert Perrimon; Stephanie E. Mohr

doi:10.1038/s41467-023-37876-0

Next-generation large-scale binary protein interaction network for Drosophila melanogaster

Hong Wen Tang, Kerstin Spirohn, Yanhui Hu, Tong Hao, István A. Kovács, Yue Gao, Richard Binari, Donghui Yang-Zhou, Kenneth H. Wan, Joel S. Bader, Dawit Balcha, Wenting Bian, Benjamin W. Booth, Atina G. Coté, Steffi de Rouck, Alice Desbuleux, Kah Yong Goh, Dae Kyum Kim, Jennifer J. Knapp, Wen Xing LeeIrma Lemmens, Cathleen Li, Mian Li, Roujia Li, Hyobin Julianne Lim, Yifang Liu, Katja Luck, Dylan Markey, Carl Pollis, Sudharshan Rangarajan, Jonathan Rodiger, Sadie Schlabach, Yun Shen, Dayag Sheykhkarimli, Bridget TeeKing, Frederick P. Roth, Jan Tavernier, Michael A. Calderwood, David E. Hill, Susan E. Celniker^*, Marc Vidal^*, Norbert Perrimon^*, Stephanie E. Mohr^*

^*Corresponding author for this work

Physics and Astronomy

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

17 Scopus citations

Abstract

Generating reference maps of interactome networks illuminates genetic studies by providing a protein-centric approach to finding new components of existing pathways, complexes, and processes. We apply state-of-the-art methods to identify binary protein-protein interactions (PPIs) for Drosophila melanogaster. Four all-by-all yeast two-hybrid (Y2H) screens of > 10,000 Drosophila proteins result in the ‘FlyBi’ dataset of 8723 PPIs among 2939 proteins. Testing subsets of data from FlyBi and previous PPI studies using an orthogonal assay allows for normalization of data quality; subsequent integration of FlyBi and previous data results in an expanded binary Drosophila reference interaction network, DroRI, comprising 17,232 interactions among 6511 proteins. We use FlyBi data to generate an autophagy network, then validate in vivo using autophagy-related assays. The deformed wings (dwg) gene encodes a protein that is both a regulator and a target of autophagy. Altogether, these resources provide a foundation for building new hypotheses regarding protein networks and function.

Original language	English (US)
Article number	2162
Journal	Nature communications
Volume	14
Issue number	1
DOIs	https://doi.org/10.1038/s41467-023-37876-0
State	Published - Dec 2023

Funding

We thank Jonathan Zirin for helpful comments. This work was supported by NIH NHGRI 5R01HG007118 and NIH NIAMS 5R01AR057352 (to N.P.). Additional support includes NMRC Open Fund Individual Research (OF-IRG) Grant (OFIRG22jul-0007, to H.-W.T.) and a Foundation Grant from the Canadian Institutes of Health Research (to F.P.R.). M.V. is a Chercheur Qualifié Honoraire from the Fonds de la Recherche Scientifique (FRS-FNRS, Wallonia-Brussels Federation, Belgium). N.P. is an investigator of the Howard Hughes Medical Institute. This article is subject to HHMI’s Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript of this article can be made freely available under a CC BY 4.0 license immediately upon publication. We thank Jonathan Zirin for helpful comments. This work was supported by NIH NHGRI 5R01HG007118 and NIH NIAMS 5R01AR057352 (to N.P.). Additional support includes NMRC Open Fund Individual Research (OF-IRG) Grant (OFIRG22jul-0007, to H.-W.T.) and a Foundation Grant from the Canadian Institutes of Health Research (to F.P.R.). M.V. is a Chercheur Qualifié Honoraire from the Fonds de la Recherche Scientifique (FRS-FNRS, Wallonia-Brussels Federation, Belgium). N.P. is an investigator of the Howard Hughes Medical Institute. This article is subject to HHMI’s Open Access to Publications policy. HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript of this article can be made freely available under a CC BY 4.0 license immediately upon publication.

ASJC Scopus subject areas

General Chemistry
General Biochemistry, Genetics and Molecular Biology
General Physics and Astronomy

Access to Document

10.1038/s41467-023-37876-0

Cite this

Tang, H. W., Spirohn, K., Hu, Y., Hao, T., Kovács, I. A., Gao, Y., Binari, R., Yang-Zhou, D., Wan, K. H., Bader, J. S., Balcha, D., Bian, W., Booth, B. W., Coté, A. G., de Rouck, S., Desbuleux, A., Goh, K. Y., Kim, D. K., Knapp, J. J., ... Mohr, S. E. (2023). Next-generation large-scale binary protein interaction network for Drosophila melanogaster. Nature communications, 14(1), Article 2162. https://doi.org/10.1038/s41467-023-37876-0

@article{dda59c8ee03844a49a739bb6599ef0e3,

title = "Next-generation large-scale binary protein interaction network for Drosophila melanogaster",

abstract = "Generating reference maps of interactome networks illuminates genetic studies by providing a protein-centric approach to finding new components of existing pathways, complexes, and processes. We apply state-of-the-art methods to identify binary protein-protein interactions (PPIs) for Drosophila melanogaster. Four all-by-all yeast two-hybrid (Y2H) screens of > 10,000 Drosophila proteins result in the {\textquoteleft}FlyBi{\textquoteright} dataset of 8723 PPIs among 2939 proteins. Testing subsets of data from FlyBi and previous PPI studies using an orthogonal assay allows for normalization of data quality; subsequent integration of FlyBi and previous data results in an expanded binary Drosophila reference interaction network, DroRI, comprising 17,232 interactions among 6511 proteins. We use FlyBi data to generate an autophagy network, then validate in vivo using autophagy-related assays. The deformed wings (dwg) gene encodes a protein that is both a regulator and a target of autophagy. Altogether, these resources provide a foundation for building new hypotheses regarding protein networks and function.",

author = "Tang, \{Hong Wen\} and Kerstin Spirohn and Yanhui Hu and Tong Hao and Kov{\'a}cs, \{Istv{\'a}n A.\} and Yue Gao and Richard Binari and Donghui Yang-Zhou and Wan, \{Kenneth H.\} and Bader, \{Joel S.\} and Dawit Balcha and Wenting Bian and Booth, \{Benjamin W.\} and Cot{\'e}, \{Atina G.\} and \{de Rouck\}, Steffi and Alice Desbuleux and Goh, \{Kah Yong\} and Kim, \{Dae Kyum\} and Knapp, \{Jennifer J.\} and Lee, \{Wen Xing\} and Irma Lemmens and Cathleen Li and Mian Li and Roujia Li and Lim, \{Hyobin Julianne\} and Yifang Liu and Katja Luck and Dylan Markey and Carl Pollis and Sudharshan Rangarajan and Jonathan Rodiger and Sadie Schlabach and Yun Shen and Dayag Sheykhkarimli and Bridget TeeKing and Roth, \{Frederick P.\} and Jan Tavernier and Calderwood, \{Michael A.\} and Hill, \{David E.\} and Celniker, \{Susan E.\} and Marc Vidal and Norbert Perrimon and Mohr, \{Stephanie E.\}",

note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = dec,

doi = "10.1038/s41467-023-37876-0",

language = "English (US)",

volume = "14",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Research",

number = "1",

}

Tang, HW, Spirohn, K, Hu, Y, Hao, T, Kovács, IA, Gao, Y, Binari, R, Yang-Zhou, D, Wan, KH, Bader, JS, Balcha, D, Bian, W, Booth, BW, Coté, AG, de Rouck, S, Desbuleux, A, Goh, KY, Kim, DK, Knapp, JJ, Lee, WX, Lemmens, I, Li, C, Li, M, Li, R, Lim, HJ, Liu, Y, Luck, K, Markey, D, Pollis, C, Rangarajan, S, Rodiger, J, Schlabach, S, Shen, Y, Sheykhkarimli, D, TeeKing, B, Roth, FP, Tavernier, J, Calderwood, MA, Hill, DE, Celniker, SE, Vidal, M, Perrimon, N & Mohr, SE 2023, 'Next-generation large-scale binary protein interaction network for Drosophila melanogaster', Nature communications, vol. 14, no. 1, 2162. https://doi.org/10.1038/s41467-023-37876-0

TY - JOUR

T1 - Next-generation large-scale binary protein interaction network for Drosophila melanogaster

AU - Tang, Hong Wen

AU - Spirohn, Kerstin

AU - Hu, Yanhui

AU - Hao, Tong

AU - Kovács, István A.

AU - Gao, Yue

AU - Binari, Richard

AU - Yang-Zhou, Donghui

AU - Wan, Kenneth H.

AU - Bader, Joel S.

AU - Balcha, Dawit

AU - Bian, Wenting

AU - Booth, Benjamin W.

AU - Coté, Atina G.

AU - de Rouck, Steffi

AU - Desbuleux, Alice

AU - Goh, Kah Yong

AU - Kim, Dae Kyum

AU - Knapp, Jennifer J.

AU - Lee, Wen Xing

AU - Lemmens, Irma

AU - Li, Cathleen

AU - Li, Mian

AU - Li, Roujia

AU - Lim, Hyobin Julianne

AU - Liu, Yifang

AU - Luck, Katja

AU - Markey, Dylan

AU - Pollis, Carl

AU - Rangarajan, Sudharshan

AU - Rodiger, Jonathan

AU - Schlabach, Sadie

AU - Shen, Yun

AU - Sheykhkarimli, Dayag

AU - TeeKing, Bridget

AU - Roth, Frederick P.

AU - Tavernier, Jan

AU - Calderwood, Michael A.

AU - Hill, David E.

AU - Celniker, Susan E.

AU - Vidal, Marc

AU - Perrimon, Norbert

AU - Mohr, Stephanie E.

PY - 2023/12

Y1 - 2023/12

N2 - Generating reference maps of interactome networks illuminates genetic studies by providing a protein-centric approach to finding new components of existing pathways, complexes, and processes. We apply state-of-the-art methods to identify binary protein-protein interactions (PPIs) for Drosophila melanogaster. Four all-by-all yeast two-hybrid (Y2H) screens of > 10,000 Drosophila proteins result in the ‘FlyBi’ dataset of 8723 PPIs among 2939 proteins. Testing subsets of data from FlyBi and previous PPI studies using an orthogonal assay allows for normalization of data quality; subsequent integration of FlyBi and previous data results in an expanded binary Drosophila reference interaction network, DroRI, comprising 17,232 interactions among 6511 proteins. We use FlyBi data to generate an autophagy network, then validate in vivo using autophagy-related assays. The deformed wings (dwg) gene encodes a protein that is both a regulator and a target of autophagy. Altogether, these resources provide a foundation for building new hypotheses regarding protein networks and function.

AB - Generating reference maps of interactome networks illuminates genetic studies by providing a protein-centric approach to finding new components of existing pathways, complexes, and processes. We apply state-of-the-art methods to identify binary protein-protein interactions (PPIs) for Drosophila melanogaster. Four all-by-all yeast two-hybrid (Y2H) screens of > 10,000 Drosophila proteins result in the ‘FlyBi’ dataset of 8723 PPIs among 2939 proteins. Testing subsets of data from FlyBi and previous PPI studies using an orthogonal assay allows for normalization of data quality; subsequent integration of FlyBi and previous data results in an expanded binary Drosophila reference interaction network, DroRI, comprising 17,232 interactions among 6511 proteins. We use FlyBi data to generate an autophagy network, then validate in vivo using autophagy-related assays. The deformed wings (dwg) gene encodes a protein that is both a regulator and a target of autophagy. Altogether, these resources provide a foundation for building new hypotheses regarding protein networks and function.

UR - http://www.scopus.com/inward/record.url?scp=85152543778&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85152543778&partnerID=8YFLogxK

U2 - 10.1038/s41467-023-37876-0

DO - 10.1038/s41467-023-37876-0

M3 - Article

C2 - 37061542

AN - SCOPUS:85152543778

SN - 2041-1723

VL - 14

JO - Nature communications

JF - Nature communications

IS - 1

M1 - 2162

ER -

Next-generation large-scale binary protein interaction network for Drosophila melanogaster

Abstract

Funding

ASJC Scopus subject areas

Access to Document

Other files and links

Fingerprint

Cite this