Publications

2024

An atlas of protein homo-oligomerization across domains of life.

Schweke H, Pacesa M, Levin T, Goverde CA, Kumar P, Duhoo Y, Dornfeld LJ, Dubreuil B, Georgeon S, Ovchinnikov S, Woolfson DN, Correia BE, Dey S, Levy ED

Cell,2024 Feb 15187(4):

DOI: 10.1016/j.cell.2024.01.022

2023

CC(+) : A searchable database of validated coiled coils in PDB structures and AlphaFold2 models.

Kumar P, Petrenas R, Dawson WM, Schweke H, Levy ED, Woolfson DN

Protein Sci,2023 Nov32(11):

DOI: 10.1002/pro.4789

Mesoscale molecular assembly is favored by the active, crowded cytoplasm.

Shu T, Mitra G, Alberts J, Viana MP, Levy ED, Hocky GM, Holt LJ

bioRxiv,2023 Sep 21:

DOI: 10.1101/2023.09.19.558334

Discriminating physiological from non-physiological interfaces in structures of protein complexes: A community-wide study.

Schweke H, Xu Q, Tauriello G, Pantolini L, Schwede T, Cazals F, Lhéritier A, Fernandez-Recio J, Rodríguez-Lumbreras LA, Schueler-Furman O, Varga JK, Jiménez-García B, Réau MF, Bonvin AMJJ, Savojardo C, Martelli PL, Casadio R, Tubiana J, Wolfson HJ, Oliva R, Barradas-Bautista D, Ricciardelli T, Cavallo L, Venclovas Č, Olechnovič K, Guerois R, Andreani J, Martin J, Wang X, Terashi G, Sarkar D, Christoffer C, Aderinwale T, Verburgt J, Kihara D, Marchand A, Correia BE, Duan R, Qiu L, Xu X, Zhang S, Zou X, Dey S, Dunbrack RL, Levy ED, Wodak SJ

Proteomics,2023 Sep23(17):

DOI: 10.1002/pmic.202200323

2022

Molecular and environmental determinants of biomolecular condensate formation.

Villegas JA, Heidenreich M, Levy ED

Nat Chem Biol,2022 Dec18(12):

DOI: 10.1038/s41589-022-01175-4

How gene duplication diversifies the landscape of protein oligomeric state and function.

Mallik S, Tawfik DS, Levy ED

Curr Opin Genet Dev,2022 Oct76:

DOI: 10.1016/j.gde.2022.101966

Affinity and Valence Impact the Extent and Symmetry of Phase Separation of Multivalent Proteins.

Nandi SK, Österle D, Heidenreich M, Levy ED, Safran SA

Phys Rev Lett,2022 Sep 16129(12):

DOI: 10.1103/PhysRevLett.129.128102

A unified statistical potential reveals that amino acid stickiness governs nonspecific recruitment of client proteins into condensates.

Villegas JA, Levy ED

Protein Sci,2022 Jul31(7):

DOI: 10.1002/pro.4361

Synthetic condensate size correlates with yeast replicative cell age.

Heidenreich M, Georgeson JM, Nadav Y, Levy ED

MicroPubl Biol,20222022:

DOI: 10.17912/micropub.biology.000582

The modular cell gets connected.

Michnick SW, Levy ED

Science,2022 Mar 11375(6585):

DOI: 10.1126/science.abo2360

Mutant libraries reveal negative design shielding proteins from supramolecular self-assembly and relocalization in cells.

Garcia Seisdedos H, Levin T, Shapira G, Freud S, Levy ED

Proc Natl Acad Sci U S A,2022 Feb 1119(5):

DOI: 10.1073/pnas.2101117119

PDBe-KB: collaboratively defining the biological context of structural data.

PDBe-KB consortium

Nucleic Acids Res,2022 Jan 750(D1):

DOI: 10.1093/nar/gkab988

QSalignWeb: A Server to Predict and Analyze Protein Quaternary Structure.

Dey S, Prilusky J, Levy ED

Front Mol Biosci,20218:

DOI: 10.3389/fmolb.2021.787510

2021

PDB-wide identification of physiological hetero-oligomeric assemblies based on conserved quaternary structure geometry.

Dey S, Levy ED

Structure,2021 Nov 429(11):

DOI: 10.1016/j.str.2021.07.012

Altered Protein Abundance and Localization Inferred from Sites of Alternative Modification by Ubiquitin and SUMO.

Ulman A, Levin T, Dassa B, Javitt A, Kacen A, Shmueli MD, Eisenberg-Lerner A, Sheban D, Fishllevich S, Levy ED, Merbl Y

J Mol Biol,2021 Oct 15433(21):

DOI: 10.1016/j.jmb.2021.167219

Abundance Imparts Evolutionary Constraints of Similar Magnitude on the Buried, Surface, and Disordered Regions of Proteins.

Dubreuil B, Levy ED

Front Mol Biosci,20218:

DOI: 10.3389/fmolb.2021.626729

"Structuromics": another step toward a holistic view of the cell.

Levy ED, Vogel C

Cell,2021 Jan 21184(2):

DOI: 10.1016/j.cell.2020.12.030

2020

Not Going with the Flow: How Cells Adapt Internal Physics.

Garcia-Seisdedos H, Heidenreich M, Levy ED

Cell,2020 Dec 10183(6):

DOI: 10.1016/j.cell.2020.11.021

Designer protein assemblies with tunable phase diagrams in living cells.

Heidenreich M, Georgeson JM, Locatelli E, Rovigatti L, Nandi SK, Steinberg A, Nadav Y, Shimoni E, Safran SA, Doye JPK, Levy ED

Nat Chem Biol,2020 Sep16(9):

DOI: 10.1038/s41589-020-0576-z

Proteomic analysis reveals the direct recruitment of intrinsically disordered regions to stress granules in S. cerevisiae.

Zhu M, Kuechler ER, Zhang J, Matalon O, Dubreuil B, Hofmann A, Loewen C, Levy ED, Gsponer J, Mayor T

J Cell Sci,2020 Jul 9133(13):

DOI: 10.1242/jcs.244657

PDBe-KB: a community-driven resource for structural and functional annotations.

PDBe-KB consortium

Nucleic Acids Res,2020 Jan 848(D1):

DOI: 10.1093/nar/gkz853

2019

Protein Abundance Biases the Amino Acid Composition of Disordered Regions to Minimize Non-functional Interactions.

Dubreuil B, Matalon O, Levy ED

J Mol Biol,2019 Dec 6431(24):

DOI: 10.1016/j.jmb.2019.08.008

Pooled clone collections by multiplexed CRISPR-Cas12a-assisted gene tagging in yeast.

Buchmuller BC, Herbst K, Meurer M, Kirrmaier D, Sass E, Levy ED, Knop M

Nat Commun,2019 Jul 410(1):

DOI: 10.1038/s41467-019-10816-7

Geometric description of self-interaction potential in symmetric protein complexes.

Empereur-Mot C, Garcia-Seisdedos H, Elad N, Dey S, Levy ED

Sci Data,2019 May 176(1):

DOI: 10.1038/s41597-019-0058-x

Infinite Assembly of Folded Proteins in Evolution, Disease, and Engineering.

Garcia-Seisdedos H, Villegas JA, Levy ED

Angew Chem Int Ed Engl,2019 Apr 1658(17):

DOI: 10.1002/anie.201806092

Evolthon: A community endeavor to evolve lab evolution.

Kaminski Strauss S, Schirman D, Jona G, Brooks AN, Kunjapur AM, Nguyen Ba AN, Flint A, Solt A, Mershin A, Dixit A, Yona AH, Csörgő B, Busby BP, Hennig BP, Pál C, Schraivogel D, Schultz D, Wernick DG, Agashe D, Levi D, Zabezhinsky D, Russ D, Sass E, Tamar E, Herz E, Levy ED, Church GM, Yelin I, Nachman I, Gerst JE, Georgeson JM, Adamala KP, Steinmetz LM, Rübsam M, Ralser M, Klutstein M, Desai MM, Walunjkar N, Yin N, Aharon Hefetz N, Jakimo N, Snitser O, Adini O, Kumar P, Soo Hoo Smith R, Zeidan R, Hazan R, Rak R, Kishony R, Johnson S, Nouriel S, Vonesch SC, Foster S, Dagan T, Wein T, Karydis T, Wannier TM, Stiles T, Olin-Sandoval V, Mueller WF, Bar-On YM, Dahan O, Pilpel Y

PLoS Biol,2019 Mar17(3):

DOI: 10.1371/journal.pbio.3000182

YeastRGB: comparing the abundance and localization of yeast proteins across cells and libraries.

Dubreuil B, Sass E, Nadav Y, Heidenreich M, Georgeson JM, Weill U, Duan Y, Meurer M, Schuldiner M, Knop M, Levy ED

Nucleic Acids Res,2019 Jan 847(D1):

DOI: 10.1093/nar/gky941

2018

Genome-wide C-SWAT library for high-throughput yeast genome tagging.

Meurer M, Duan Y, Sass E, Kats I, Herbst K, Buchmuller BC, Dederer V, Huber F, Kirrmaier D, Štefl M, Van Laer K, Dick TP, Lemberg MK, Khmelinskii A, Levy ED, Knop M

Nat Methods,2018 Aug15(8):

DOI: 10.1038/s41592-018-0045-8

Genome-wide SWAp-Tag yeast libraries for proteome exploration.

Weill U, Yofe I, Sass E, Stynen B, Davidi D, Natarajan J, Ben-Menachem R, Avihou Z, Goldman O, Harpaz N, Chuartzman S, Kniazev K, Knoblach B, Laborenz J, Boos F, Kowarzyk J, Ben-Dor S, Zalckvar E, Herrmann JM, Rachubinski RA, Pines O, Rapaport D, Michnick SW, Levy ED, Schuldiner M

Nat Methods,2018 Aug15(8):

DOI: 10.1038/s41592-018-0044-9

Inferring and Using Protein Quaternary Structure Information from Crystallographic Data.

Dey S, Levy ED

Methods Mol Biol,20181764:

DOI: 10.1007/978-1-4939-7759-8_23

PDB-wide identification of biological assemblies from conserved quaternary structure geometry.

Dey S, Ritchie DW, Levy ED

Nat Methods,2018 Jan15(1):

DOI: 10.1038/nmeth.4510

2017

Proteins evolve on the edge of supramolecular self-assembly.

Garcia-Seisdedos H, Empereur-Mot C, Elad N, Levy ED

Nature,2017 Aug 10548(7666):

DOI: 10.1038/nature23320

Exhaustive search of linear information encoding protein-peptide recognition.

Kelil A, Dubreuil B, Levy ED, Michnick SW

PLoS Comput Biol,2017 Apr13(4):

DOI: 10.1371/journal.pcbi.1005499

2016

Protein-Fragment Complementation Assays for Large-Scale Analysis, Functional Dissection, and Spatiotemporal Dynamic Studies of Protein-Protein Interactions in Living Cells.

Michnick SW, Landry CR, Levy ED, Diss G, Ear PH, Kowarzyk J, Malleshaiah MK, Messier V, Tchekanda E

Cold Spring Harb Protoc,2016 Nov 12016(11):

DOI: 10.1101/pdb.top083543

The Dihydrofolate Reductase Protein-Fragment Complementation Assay: A Survival-Selection Assay for Large-Scale Analysis of Protein-Protein Interactions.

Michnick SW, Levy ED, Landry CR, Kowarzyk J, Messier V

Cold Spring Harb Protoc,2016 Nov 12016(11):

DOI: 10.1101/pdb.prot090027

Young phosphorylation is functionally silent.

Matalon O, Dubreuil B, Levy ED

Science,2016 Oct 14354(6309):

DOI: 10.1126/science.aai8833

Evolution of domain-peptide interactions to coadapt specificity and affinity to functional diversity.

Kelil A, Levy ED, Michnick SW

Proc Natl Acad Sci U S A,2016 Jul 5113(27):

DOI: 10.1073/pnas.1518469113

2015

Decoding a neural circuit controlling global animal state in C. elegans.

Laurent P, Soltesz Z, Nelson GM, Chen C, Arellano-Carbajal F, Levy E, de Bono M

Elife,2015 Mar 114:

DOI: 10.7554/eLife.04241

Symmetry breaking in homo-oligomers: the curious case of mega-hemocyanin.

Garcia Seisdedos H, Steinberg A, Levy ED

Structure,2015 Jan 623(1):

DOI: 10.1016/j.str.2014.12.006

2014

Fast and accurate discovery of degenerate linear motifs in protein sequences.

Kelil A, Dubreuil B, Levy ED, Michnick SW

PLoS One,20149(9):

DOI: 10.1371/journal.pone.0106081

Different subunits belonging to the same protein complex often exhibit discordant expression levels and evolutionary properties.

Matalon O, Horovitz A, Levy ED

Curr Opin Struct Biol,2014 Jun26:

DOI: 10.1016/j.sbi.2014.06.001

High-resolution mapping of protein concentration reveals principles of proteome architecture and adaptation.

Levy ED, Kowarzyk J, Michnick SW

Cell Rep,2014 May 227(4):

DOI: 10.1016/j.celrep.2014.04.009

2013

Extracting insight from noisy cellular networks.

Landry CR, Levy ED, Abd Rabbo D, Tarassov K, Michnick SW

Cell,2013 Nov 21155(5):

DOI: 10.1016/j.cell.2013.11.003

Structural, evolutionary, and assembly principles of protein oligomerization.

Levy ED, Teichmann S

Prog Mol Biol Transl Sci,2013117:

DOI: 10.1016/B978-0-12-386931-9.00002-7

2012

Cellular crowding imposes global constraints on the chemistry and evolution of proteomes.

Levy ED, De S, Teichmann SA

Proc Natl Acad Sci U S A,2012 Dec 11109(50):

DOI: 10.1073/pnas.1209312109

Protein abundance is key to distinguish promiscuous from functional phosphorylation based on evolutionary information.

Levy ED, Michnick SW, Landry CR

Philos Trans R Soc Lond B Biol Sci,2012 Sep 19367(1602):

DOI: 10.1098/rstb.2012.0078

2010

A simple definition of structural regions in proteins and its use in analyzing interface evolution.

Levy ED

J Mol Biol,2010 Nov 5403(4):

DOI: 10.1016/j.jmb.2010.09.028

Molecular characterization of the evolution of phagosomes.

Boulais J, Trost M, Landry CR, Dieckmann R, Levy ED, Soldati T, Michnick SW, Thibault P, Desjardins M

Mol Syst Biol,2010 Oct 196:

DOI: 10.1038/msb.2010.80

Homomeric protein complexes: evolution and assembly.

Venkatakrishnan AJ, Levy ED, Teichmann SA

Biochem Soc Trans,2010 Aug38(4):

DOI: 10.1042/BST0380879

Systemizing the structures and structuring the system.

Levy ED, Teichmann SA

Expert Rev Proteomics,2010 Jun7(3):

DOI: 10.1586/epr.10.33

Cell signaling. Signaling through cooperation.

Levy ED, Landry CR, Michnick SW

Science,2010 May 21328(5981):

DOI: 10.1126/science.1190993

2009

Physicochemical principles that regulate the competition between functional and dysfunctional association of proteins.

Pechmann S, Levy ED, Tartaglia GG, Vendruscolo M

Proc Natl Acad Sci U S A,2009 Jun 23106(25):

DOI: 10.1073/pnas.0812414106

Weak functional constraints on phosphoproteomes.

Landry CR, Levy ED, Michnick SW

Trends Genet,2009 May25(5):

DOI: 10.1016/j.tig.2009.03.003

Self-assembly and evolution of homomeric protein complexes.

Villar G, Wilber AW, Williamson AJ, Thiara P, Doye JP, Louis AA, Jochum MN, Lewis AC, Levy ED

Phys Rev Lett,2009 Mar 20102(11):

DOI: 10.1103/PhysRevLett.102.118106

How perfect can protein interactomes be?

Levy ED, Landry CR, Michnick SW

Sci Signal,2009 Mar 32(60):

DOI: 10.1126/scisignal.260pe11

2008

Assembly reflects evolution of protein complexes.

Levy ED, Boeri Erba E, Robinson CV, Teichmann SA

Nature,2008 Jun 26453(7199):

DOI: 10.1038/nature06942

Evolution and dynamics of protein interactions and networks.

Levy ED, Pereira-Leal JB

Curr Opin Struct Biol,2008 Jun18(3):

DOI: 10.1016/j.sbi.2008.03.003

2007

PiQSi: protein quaternary structure investigation.

Levy ED

Structure,2007 Nov15(11):

DOI: 10.1016/j.str.2007.09.019

CORRIE: enzyme sequence annotation with confidence estimates.

Audit B, Levy ED, Gilks WR, Goldovsky L, Ouzounis CA

BMC Bioinformatics,2007 May 228 Suppl 4(Suppl 4):

DOI: 10.1186/1471-2105-8-S4-S3

Evolution of protein complexes by duplication of homomeric interactions.

Pereira-Leal JB, Levy ED, Kamp C, Teichmann SA

Genome Biol,20078(4):

DOI: 10.1186/gb-2007-8-4-r51

2006

3D complex: a structural classification of protein complexes.

Levy ED, Pereira-Leal JB, Chothia C, Teichmann SA

PLoS Comput Biol,2006 Nov 172(11):

DOI: 10.1371/journal.pcbi.0020155

The origins and evolution of functional modules: lessons from protein complexes.

Pereira-Leal JB, Levy ED, Teichmann SA

Philos Trans R Soc Lond B Biol Sci,2006 Mar 29361(1467):

DOI: 10.1098/rstb.2005.1807

2005

Probabilistic annotation of protein sequences based on functional classifications.

Levy ED, Ouzounis CA, Gilks WR, Audit B

BMC Bioinformatics,2005 Dec 146:

DOI: 10.1186/1471-2105-6-302

Emmanuel Levy