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Title: NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance

Abstract

Axon pathfinding is critical for nervous system development, and it is orchestrated by molecular cues that activate receptors on the axonal growth cone. Robo family receptors bind Slit guidance cues to mediate axon repulsion. In mammals, the divergent family member Robo3 does not bind Slits, but instead signals axon repulsion from its own ligand, NELL2. Conversely, canonical Robos do not mediate NELL2 signaling. Here, we present the structures of NELL-Robo3 complexes, identifying a mode of ligand engagement for Robos that is orthogonal to Slit binding. We elucidate the structural basis for differential binding between NELL and Robo family members and show that NELL2 repulsive activity is a function of its Robo3 affinity and is enhanced by ligand trimerization. Our results reveal a mechanism of oligomerization-induced Robo activation for axon guidance and shed light on Robo family member ligand binding specificity, conformational variability, divergent modes of signaling, and evolution.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [1];  [2];  [3]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of Chicago, IL (United States). Grossman Inst. for Neuroscience, Quantitative Biology and Human Behavior
  2. Brown Univ., Providence, RI (United States); Robert J. and Nancy D. Carney Inst. for Brain Science, Providence, RI (United States)
  3. Univ. of Chicago, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); USDOE Office of Science (SC)
OSTI Identifier:
1608059
Grant/Contract Number:  
AC02-06CH11357; T32 GM077995; R01 NS097161; R01 MH114102; RI-INBRE P20 GM103430; R01 NS095908; S10 RR029205; 1S10OD012289-01A1; 9 P41 GM103622; 1S10OD018090-01
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Pak, Joseph S., DeLoughery, Zachary J., Wang, Jing, Acharya, Nischal, Park, Yeonwoo, Jaworski, Alexander, and Özkan, Engin. NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance. United States: N. p., 2020. Web. doi:10.1038/s41467-020-15211-1.
Pak, Joseph S., DeLoughery, Zachary J., Wang, Jing, Acharya, Nischal, Park, Yeonwoo, Jaworski, Alexander, & Özkan, Engin. NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance. United States. https://doi.org/10.1038/s41467-020-15211-1
Pak, Joseph S., DeLoughery, Zachary J., Wang, Jing, Acharya, Nischal, Park, Yeonwoo, Jaworski, Alexander, and Özkan, Engin. Fri . "NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance". United States. https://doi.org/10.1038/s41467-020-15211-1. https://www.osti.gov/servlets/purl/1608059.
@article{osti_1608059,
title = {NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance},
author = {Pak, Joseph S. and DeLoughery, Zachary J. and Wang, Jing and Acharya, Nischal and Park, Yeonwoo and Jaworski, Alexander and Özkan, Engin},
abstractNote = {Axon pathfinding is critical for nervous system development, and it is orchestrated by molecular cues that activate receptors on the axonal growth cone. Robo family receptors bind Slit guidance cues to mediate axon repulsion. In mammals, the divergent family member Robo3 does not bind Slits, but instead signals axon repulsion from its own ligand, NELL2. Conversely, canonical Robos do not mediate NELL2 signaling. Here, we present the structures of NELL-Robo3 complexes, identifying a mode of ligand engagement for Robos that is orthogonal to Slit binding. We elucidate the structural basis for differential binding between NELL and Robo family members and show that NELL2 repulsive activity is a function of its Robo3 affinity and is enhanced by ligand trimerization. Our results reveal a mechanism of oligomerization-induced Robo activation for axon guidance and shed light on Robo family member ligand binding specificity, conformational variability, divergent modes of signaling, and evolution.},
doi = {10.1038/s41467-020-15211-1},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United States},
year = {2020},
month = {3}
}

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Works referenced in this record:

Molecular basis of synaptic specificity by immunoglobulin superfamily receptors in Drosophila
journal, January 2019


Uniqueness of ab initio shape determination in small-angle scattering
journal, April 2003

  • Volkov, Vladimir V.; Svergun, Dmitri I.
  • Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864
  • DOI: 10.1107/S0021889803000268

Conservation and divergence of axon guidance mechanisms
journal, October 1999


Structural Divergence in O-GlcNAc Glycans Displayed on Epidermal Growth Factor-like Repeats of Mammalian Notch1
journal, July 2018


Structural and Functional Analysis of Slit and Heparin Binding to Immunoglobulin-like Domains 1 and 2 of Drosophila Robo
journal, March 2008

  • Fukuhara, Noémi; Howitt, Jason A.; Hussain, Sadaf-Ahmahni
  • Journal of Biological Chemistry, Vol. 283, Issue 23
  • DOI: 10.1074/jbc.M800688200

DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering
journal, January 2009

  • Franke, Daniel; Svergun, Dmitri I.
  • Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346
  • DOI: 10.1107/S0021889809000338

Slit-Robo signaling
journal, August 2016

  • Blockus, Heike; Chédotal, Alain
  • Development, Vol. 143, Issue 17
  • DOI: 10.1242/dev.132829

Regulation of Commissural Axon Pathfinding by Slit and its Robo Receptors
journal, November 2006


Robo2 contains a cryptic binding site for neural EGFL-like (NELL) protein 1/2
journal, January 2019

  • Yamamoto, Naoka; Kashiwagi, Manabu; Ishihara, Manami
  • Journal of Biological Chemistry, Vol. 294, Issue 12
  • DOI: 10.1074/jbc.RA118.005819

BioXTAS RAW : improvements to a free open-source program for small-angle X-ray scattering data reduction and analysis
journal, September 2017

  • Hopkins, Jesse Bennett; Gillilan, Richard E.; Skou, Soren
  • Journal of Applied Crystallography, Vol. 50, Issue 5
  • DOI: 10.1107/S1600576717011438

Structural insights into the Slit-Robo complex
journal, September 2007

  • Morlot, C.; Thielens, N. M.; Ravelli, R. B. G.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 38
  • DOI: 10.1073/pnas.0705310104

TheDUTT1Gene, a Novel NCAM Family Member Is Expressed in Developing Murine Neural Tissues and Has an Unusually Broad Pattern of Expression
journal, May 1998

  • Sundaresan, Vasi; Roberts, Ian; Bateman, Alex
  • Molecular and Cellular Neuroscience, Vol. 11, Issue 1-2
  • DOI: 10.1006/mcne.1998.0672

New gene, nel, encoding a Mr 93 K protein with EGF-like repeats is strongly expressed in neural tissues of early stage chick embryos
journal, June 1995

  • Matshuhashi, Sachiko; Noji, Sumihare; Koyama, Eiki
  • Developmental Dynamics, Vol. 203, Issue 2
  • DOI: 10.1002/aja.1002030209

Nell2 regulates the contralateral-versus-ipsilateral visual projection as a domain-specific positional cue
journal, February 2019

  • Nakamoto, Chizu; Durward, Elaine; Horie, Masato
  • Development, Vol. 146, Issue 4
  • DOI: 10.1242/dev.170704

A Molecular Mechanism for the Heparan Sulfate Dependence of Slit-Robo Signaling
journal, October 2006

  • Hussain, Sadaf-Ahmahni; Piper, Michael; Fukuhara, Noémi
  • Journal of Biological Chemistry, Vol. 281, Issue 51
  • DOI: 10.1074/jbc.M609384200

Signaling Switch of the Axon Guidance Receptor Robo3 during Vertebrate Evolution
journal, December 2014


Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord
journal, August 1994


Sonic Hedgehog Guides Axons through a Noncanonical, Src-Family-Kinase-Dependent Signaling Pathway
journal, May 2009


Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012

  • Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel
  • Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4
  • DOI: 10.1107/S0907444912001308

Robo2 acts in trans to inhibit Slit-Robo1 repulsion in pre-crossing commissural axons
journal, July 2015


Extracellular Ig domains 1 and 2 of Robo are important for ligand (Slit) binding
journal, June 2004

  • Liu, Zhe; Patel, Kalpana; Schmidt, Hannes
  • Molecular and Cellular Neuroscience, Vol. 26, Issue 2
  • DOI: 10.1016/j.mcn.2004.01.002

Overview of Current Methods in Sedimentation Velocity and Sedimentation Equilibrium Analytical Ultracentrifugation
journal, February 2013

  • Zhao, Huaying; Brautigam, Chad A.; Ghirlando, Rodolfo
  • Current Protocols in Protein Science, Vol. 71, Issue 1
  • DOI: 10.1002/0471140864.ps2012s71

Robo Ig4 Is a Dimerization Domain
journal, November 2017


Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interaction is required for midline crossing in vertebrate spinal cord
journal, January 2005

  • Mambetisaeva, Elvira T.; Andrews, William; Camurri, Laura
  • Developmental Dynamics, Vol. 233, Issue 1
  • DOI: 10.1002/dvdy.20324

Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard
journal, May 2009

  • Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6
  • DOI: 10.1107/S0907444909012098

Structure and functional relevance of the Slit2 homodimerization domain
journal, May 2009

  • Seiradake, Elena; von Philipsborn, Anne C.; Henry, Maud
  • EMBO reports, Vol. 10, Issue 7
  • DOI: 10.1038/embor.2009.95

Production of selenomethionyl-derivatized proteins in baculovirus-infected insect cells
journal, September 2007

  • Cronin, Ciarán N.; Lim, Kheng B.; Rogers, Joe
  • Protein Science, Vol. 16, Issue 9
  • DOI: 10.1110/ps.072931407

Biochemical Characterization and Expression Analysis of Neural Thrombospondin-1-like Proteins NELL1 and NELL2
journal, November 1999

  • Kuroda, Shun'ichi; Oyasu, Miho; Kawakami, Masakatsu
  • Biochemical and Biophysical Research Communications, Vol. 265, Issue 1, p. 79-86
  • DOI: 10.1006/bbrc.1999.1638

Restricted neural epidermal growth factor-like like 2 (NELL2) expression during muscle and neuronal differentiation
journal, December 2002


Structures of netrin-1 bound to two receptors provide insight into its axon guidance mechanism
journal, May 2014


Revisiting Netrin-1: One Who Guides (Axons)
journal, July 2018


Structural Principles in Robo Activation and Auto-inhibition
journal, April 2019


XDS
journal, January 2010

  • Kabsch, Wolfgang
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
  • DOI: 10.1107/S0907444909047337

Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets
journal, April 2012

  • Alfaro, J. F.; Gong, C. -X.; Monroe, M. E.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
  • DOI: 10.1073/pnas.1200425109

MoRDa , an automatic molecular replacement pipeline
journal, August 2015

  • Vagin, Alexey; Lebedev, Andrey
  • Acta Crystallographica Section A Foundations and Advances, Vol. 71, Issue a1
  • DOI: 10.1107/S2053273315099672

The Crystal Structure of Netrin-1 in Complex with DCC Reveals the Bifunctionality of Netrin-1 As a Guidance Cue
journal, August 2014


Robo1 Forms a Compact Dimer-of-Dimers Assembly
journal, February 2018


Nell1-deficient mice have reduced expression of extracellular matrix proteins causing cranial and vertebral defects
journal, March 2006

  • Desai, Jayashree; Shannon, Mark E.; Johnson, Mahlon D.
  • Human Molecular Genetics, Vol. 15, Issue 8, p. 1329-1341
  • DOI: 10.1093/hmg/ddl053

Mechanisms and Molecules of Neuronal Wiring: A Primer
journal, December 2010


Cloning and Characterization of Two Novel Human cDNAs (NELL1 and NELL2) Encoding Proteins with Six EGF-like Repeats
journal, December 1996

  • Watanabe, Takeshi K.; Katagiri, Toyomasa; Suzuki, Mikio
  • Genomics, Vol. 38, Issue 3, p. 273-276
  • DOI: 10.1006/geno.1996.0628

MolProbity : all-atom structure validation for macromolecular crystallography
journal, December 2009

  • Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1
  • DOI: 10.1107/S0907444909042073

Evidence for the existence of two Robo3 isoforms with divergent biochemical properties
journal, December 2005

  • Camurri, Laura; Mambetisaeva, Elvira; Davies, Derek
  • Molecular and Cellular Neuroscience, Vol. 30, Issue 4
  • DOI: 10.1016/j.mcn.2005.07.014

Features and development of Coot
journal, March 2010

  • Emsley, P.; Lohkamp, B.; Scott, W. G.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4
  • DOI: 10.1107/S0907444910007493

Structural insight into Slit–Robo signalling
journal, March 2008

  • Hohenester, Erhard
  • Biochemical Society Transactions, Vol. 36, Issue 2
  • DOI: 10.1042/BST0360251

Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein
journal, July 2001

  • Hu, Huaiyu
  • Nature Neuroscience, Vol. 4, Issue 7
  • DOI: 10.1038/89482

Roundabout 1 exists predominantly as a basal dimeric complex and this is unaffected by binding of the ligand Slit2
journal, June 2014

  • Zakrys, Linas; Ward, Richard J.; Pediani, John D.
  • Biochemical Journal, Vol. 461, Issue 1
  • DOI: 10.1042/BJ20140190

Molecular Logic of Neuronal Self-Recognition through Protocadherin Domain Interactions
journal, October 2015


Structural Basis for Regulation of GPR56/ADGRG1 by Its Alternatively Spliced Extracellular Domains
journal, September 2016


In vitro guidance of retinal axons by a tectal lamina-specific glycoprotein Nel
journal, June 2009

  • Jiang, Yulan; Obama, Hiroya; Kuan, Soh Leh
  • Molecular and Cellular Neuroscience, Vol. 41, Issue 2
  • DOI: 10.1016/j.mcn.2009.02.006

Slit Proteins Bind Robo Receptors and Have an Evolutionarily Conserved Role in Repulsive Axon Guidance
journal, March 1999


An Extracellular Interactome of Immunoglobulin and LRR Proteins Reveals Receptor-Ligand Networks
journal, July 2013


Binding site for Robo receptors revealed by dissection of the leucine-rich repeat region of Slit
journal, October 2004

  • Howitt, Jason A.; Clout, Naomi J.; Hohenester, Erhard
  • The EMBO Journal, Vol. 23, Issue 22
  • DOI: 10.1038/sj.emboj.7600446

Accurate assessment of mass, models and resolution by small-angle scattering
journal, April 2013


slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains.
journal, December 1990

  • Rothberg, J. M.; Jacobs, J. R.; Goodman, C. S.
  • Genes & Development, Vol. 4, Issue 12a
  • DOI: 10.1101/gad.4.12a.2169

Operational redundancy in axon guidance through the multifunctional receptor Robo3 and its ligand NELL2
journal, November 2015


Phaser crystallographic software
journal, July 2007

  • McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
  • Journal of Applied Crystallography, Vol. 40, Issue 4
  • DOI: 10.1107/S0021889807021206

Collaborative and Specialized Functions of Robo1 and Robo2 in Spinal Commissural Axon Guidance
journal, July 2010


Protocadherin cis -dimer architecture and recognition unit diversity
journal, October 2017

  • Goodman, Kerry M.; Rubinstein, Rotem; Dan, Hanbin
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 46
  • DOI: 10.1073/pnas.1713449114

Works referencing / citing this record:

Functional and structural characterization of HspB1/Hsp27 from Chinese hamster ovary cells
journal, August 2019


A General Approach to Access Morphologies of Polyoxometalates in Solution by Using SAXS: An Ab Initio Modeling Protocol
journal, April 2018

  • Li, Mu; Wang, Weiyu; Yin, Panchao
  • Chemistry - A European Journal, Vol. 24, Issue 25
  • DOI: 10.1002/chem.201800344

Intrinsic structural disorder of mouse proNGF
journal, June 2009

  • Paoletti, Francesca; Covaceuszach, Sonia; Konarev, Peter V.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 75, Issue 4
  • DOI: 10.1002/prot.22311

Biochemical characterization and low-resolution SAXS structure of two-domain endoglucanase BlCel9 from Bacillus licheniformis
journal, December 2018

  • de Araújo, Evandro Ares; de Oliveira Neto, Mário; Polikarpov, Igor
  • Applied Microbiology and Biotechnology, Vol. 103, Issue 3
  • DOI: 10.1007/s00253-018-9508-1

WeNMR: Structural Biology on the Grid
journal, November 2012

  • Wassenaar, Tsjerk A.; van Dijk, Marc; Loureiro-Ferreira, Nuno
  • Journal of Grid Computing, Vol. 10, Issue 4
  • DOI: 10.1007/s10723-012-9246-z

Structural Rearrangements in the C-Terminal Domain Homolog of Orange Carotenoid Protein are Crucial for Carotenoid Transfer
journal, February 2019


Structure of a Novel Dimeric SET Domain Methyltransferase that Regulates Cell Motility
journal, October 2018

  • Pivovarova, Yulia; Liu, Jun; Lesigang, Johannes
  • Journal of Molecular Biology, Vol. 430, Issue 21
  • DOI: 10.1016/j.jmb.2018.08.017

Structural basis for iron piracy by pathogenic Neisseria
journal, February 2012

  • Noinaj, Nicholas; Easley, Nicole C.; Oke, Muse
  • Nature, Vol. 483, Issue 7387
  • DOI: 10.1038/nature10823

Structural basis for the assembly of the Sxl–Unr translation regulatory complex
journal, September 2014

  • Hennig, Janosch; Militti, Cristina; Popowicz, Grzegorz M.
  • Nature, Vol. 515, Issue 7526
  • DOI: 10.1038/nature13693

Molecular architecture of the human sperm IZUMO1 and egg JUNO fertilization complex
journal, June 2016

  • Aydin, Halil; Sultana, Azmiri; Li, Sheng
  • Nature, Vol. 534, Issue 7608
  • DOI: 10.1038/nature18595

Structural and mechanistic insights into regulation of the retromer coat by TBC1d5
journal, November 2016

  • Jia, Da; Zhang, Jin-San; Li, Fang
  • Nature Communications, Vol. 7, Issue 1
  • DOI: 10.1038/ncomms13305

AAA+ chaperones and acyldepsipeptides activate the ClpP protease via conformational control
journal, February 2015

  • Gersch, Malte; Famulla, Kirsten; Dahmen, Maria
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms7320

Molecular basis of human CD22 function and therapeutic targeting
journal, October 2017


A viral-fusion-peptide-like molecular switch drives membrane insertion of botulinum neurotoxin A1
journal, December 2018


Unique structural features of a bacterial autotransporter adhesin suggest mechanisms for interaction with host macromolecules
journal, April 2019


Mycobacterium tuberculosis CarD, an essential global transcriptional regulator forms amyloid-like fibrils
journal, July 2018


Molecular architecture of the Jumonji C family histone demethylase KDM5B
journal, March 2019


Nano-encapsulated Escherichia coli Divisome Anchor ZipA, and in Complex with FtsZ
journal, December 2019


ClpP protease activation results from the reorganization of the electrostatic interaction networks at the entrance pores
journal, November 2019


Structural basis of a nucleosome containing histone H2A.B/H2A.Bbd that transiently associates with reorganized chromatin
journal, December 2013

  • Arimura, Yasuhiro; Kimura, Hiroshi; Oda, Takashi
  • Scientific Reports, Vol. 3, Issue 1
  • DOI: 10.1038/srep03510

Crystal structure of Streptococcus pneumoniae pneumolysin provides key insights into early steps of pore formation
journal, September 2015

  • Lawrence, Sara L.; Feil, Susanne C.; Morton, Craig J.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep14352

Disease-Homologous Mutation in the Cation Diffusion Facilitator Protein MamM Causes Single-Domain Structural Loss and Signifies Its Importance
journal, August 2016

  • Barber-Zucker, Shiran; Uebe, René; Davidov, Geula
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep31933

The N-terminal domain of unknown function (DUF959) in collagen XVIII is intrinsically disordered and highly O-glycosylated
journal, November 2018

  • Kaur, Inderjeet; Ruskamo, Salla; Koivunen, Jarkko
  • Biochemical Journal, Vol. 475, Issue 22
  • DOI: 10.1042/bcj20180405

Conserved structure and domain organization among bacterial Slc26 transporters
journal, September 2014

  • Compton, Emma L. R.; Page, Kimberly; Findlay, Heather E.
  • Biochemical Journal, Vol. 463, Issue 2
  • DOI: 10.1042/BJ20130619

Light-activated DNA binding in a designed allosteric protein
journal, July 2008

  • Strickland, D.; Moffat, K.; Sosnick, T. R.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 31, p. 10709-10714
  • DOI: 10.1073/pnas.0709610105

The human IgM pentamer is a mushroom-shaped molecule with a flexural bias
journal, August 2009

  • Czajkowsky, D. M.; Shao, Z.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 35
  • DOI: 10.1073/pnas.0903805106

Two crystal structures reveal design for repurposing the C-Ala domain of human AlaRS
journal, November 2016

  • Sun, Litao; Song, Youngzee; Blocquel, David
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 50
  • DOI: 10.1073/pnas.1617316113

How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans
journal, June 2017

  • Cartmell, Alan; Lowe, Elisabeth C.; Baslé, Arnaud
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 27
  • DOI: 10.1073/pnas.1704367114

DC-SIGN Neck Domain Is a pH-sensor Controlling Oligomerization: SAXS AND HYDRODYNAMIC STUDIES OF EXTRACELLULAR DOMAIN
journal, June 2009

  • Tabarani, Georges; Thépaut, Michel; Stroebel, David
  • Journal of Biological Chemistry, Vol. 284, Issue 32
  • DOI: 10.1074/jbc.m109.021204

Electrostatic Interactions Involving the Extreme C Terminus of Nuclear Export Factor CRM1 Modulate Its Affinity for Cargo
journal, August 2011

  • Fox, Abigail M.; Ciziene, Danguole; McLaughlin, Stephen H.
  • Journal of Biological Chemistry, Vol. 286, Issue 33
  • DOI: 10.1074/jbc.M111.245092

Fission Yeast Swi5-Sfr1 Protein Complex, an Activator of Rad51 Recombinase, Forms an Extremely Elongated Dogleg-shaped Structure
journal, December 2011

  • Kokabu, Yuichi; Murayama, Yasuto; Kuwabara, Naoyuki
  • Journal of Biological Chemistry, Vol. 286, Issue 50
  • DOI: 10.1074/jbc.m111.303339

Interaction of the HIV-1 Intasome with Transportin 3 Protein (TNPO3 or TRN-SR2)
journal, October 2012

  • Larue, Ross; Gupta, Kushol; Wuensch, Christiane
  • Journal of Biological Chemistry, Vol. 287, Issue 41
  • DOI: 10.1074/jbc.M112.384669

Characterization of Enzymes from Legionella pneumophila Involved in Reversible Adenylylation of Rab1 Protein
journal, October 2012

  • Müller, Matthias P.; Shkumatov, Alexander V.; Oesterlin, Lena K.
  • Journal of Biological Chemistry, Vol. 287, Issue 42
  • DOI: 10.1074/jbc.m112.396861

Identification and Structural Characterization of a Legionella Phosphoinositide Phosphatase
journal, July 2013

  • Toulabi, Leila; Wu, Xiaochun; Cheng, Yanshu
  • Journal of Biological Chemistry, Vol. 288, Issue 34
  • DOI: 10.1074/jbc.m113.474239

Differential Role of HAMP-like Linkers in Regulating the Functionality of the Group III Histidine Kinase DhNik1p
journal, July 2014

  • Kaur, Harsimran; Singh, Shikha; Rathore, Yogendra S.
  • Journal of Biological Chemistry, Vol. 289, Issue 29
  • DOI: 10.1074/jbc.M114.554303

Assembly of the Respiratory Mucin MUC5B
journal, June 2014

  • Ridley, Caroline; Kouvatsos, Nikos; Raynal, Bertrand D.
  • Journal of Biological Chemistry, Vol. 289, Issue 23
  • DOI: 10.1074/jbc.m114.566679

Structural Basis for Oxygen Activation at a Heterodinuclear Manganese/Iron Cofactor
journal, October 2015

  • Griese, Julia J.; Kositzki, Ramona; Schrapers, Peer
  • Journal of Biological Chemistry, Vol. 290, Issue 42
  • DOI: 10.1074/jbc.M115.675223

Structural Insight into the 14-3-3 Protein-dependent Inhibition of Protein Kinase ASK1 (Apoptosis Signal-regulating kinase 1)
journal, August 2016

  • Petrvalska, Olivia; Kosek, Dalibor; Kukacka, Zdenek
  • Journal of Biological Chemistry, Vol. 291, Issue 39
  • DOI: 10.1074/jbc.M116.724310

Solution Conformation and Thermodynamic Characteristics of RNA Binding by the Splicing Factor U2AF 65
journal, October 2008

  • Jenkins, Jermaine L.; Shen, Haihong; Green, Michael R.
  • Journal of Biological Chemistry, Vol. 283, Issue 48
  • DOI: 10.1074/jbc.M806297200

Structure-specific recognition protein-1 (SSRP1) is an elongated homodimer that binds histones
journal, June 2018

  • Marcianò, Gabriele; Da Vela, Stefano; Tria, Giancarlo
  • Journal of Biological Chemistry, Vol. 293, Issue 26
  • DOI: 10.1074/jbc.ra117.000994

The antibiotic cyclomarin blocks arginine-phosphate–induced millisecond dynamics in the N-terminal domain of ClpC1 from Mycobacterium tuberculosis
journal, June 2018

  • Weinhäupl, Katharina; Brennich, Martha; Kazmaier, Uli
  • Journal of Biological Chemistry, Vol. 293, Issue 22
  • DOI: 10.1074/jbc.ra118.002251

Direct observation of conformational dynamics of the PH domain in phospholipases Cɛ and β may contribute to subfamily-specific roles in regulation
journal, November 2018

  • Garland-Kuntz, Elisabeth E.; Vago, Frank S.; Sieng, Monita
  • Journal of Biological Chemistry, Vol. 293, Issue 45
  • DOI: 10.1074/jbc.ra118.003656

The dimeric ectodomain of the alkali-sensing insulin receptor–related receptor (ectoIRR) has a droplike shape
journal, November 2019

  • Shtykova, Eleonora V.; Petoukhov, Maxim V.; Mozhaev, Andrey A.
  • Journal of Biological Chemistry, Vol. 294, Issue 47
  • DOI: 10.1074/jbc.RA119.010390

Integrative Structure–Function Mapping of the Nucleoporin Nup133 Suggests a Conserved Mechanism for Membrane Anchoring of the Nuclear Pore Complex
journal, August 2014

  • Kim, Seung Joong; Fernandez-Martinez, Javier; Sampathkumar, Parthasarathy
  • Molecular & Cellular Proteomics, Vol. 13, Issue 11
  • DOI: 10.1074/mcp.m114.040915

Disease-associated mutations alter the dynamic motion of the N-terminal domain of the human cardiac ryanodine receptor
journal, March 2019


Simple rules for passive diffusion through the nuclear pore complex
journal, October 2016

  • Timney, Benjamin L.; Raveh, Barak; Mironska, Roxana
  • The Journal of Cell Biology, Vol. 215, Issue 1
  • DOI: 10.1083/jcb.201601004

Structural evaluation of an amyloid fibril model using small-angle x-ray scattering
journal, June 2017


Calcium-dependent structural changes in human reticulocalbin-1
journal, January 2014

  • Suzuki, N.; Ban, S.; Itoh, E.
  • Journal of Biochemistry, Vol. 155, Issue 5
  • DOI: 10.1093/jb/mvu003

Quaternary structure of the yeast Arc1p-aminoacyl-tRNA synthetase complex in solution and its compaction upon binding of tRNAs
journal, November 2012

  • Koehler, Christine; Round, Adam; Simader, Hannes
  • Nucleic Acids Research, Vol. 41, Issue 1
  • DOI: 10.1093/nar/gks1072

The H-subunit of the restriction endonuclease CglI contains a prototype DEAD-Z1 helicase-like motor
journal, February 2018

  • Toliusis, Paulius; Tamulaitiene, Giedre; Grigaitis, Rokas
  • Nucleic Acids Research, Vol. 46, Issue 5
  • DOI: 10.1093/nar/gky107

Structure of human telomere G-quadruplex in the presence of a model drug along the thermal unfolding pathway
journal, November 2018

  • Bianchi, Federico; Comez, Lucia; Biehl, Ralf
  • Nucleic Acids Research, Vol. 46, Issue 22
  • DOI: 10.1093/nar/gky1092

Structure and hydrodynamics of a DNA G-quadruplex with a cytosine bulge
journal, May 2018

  • Meier, Markus; Moya-Torres, Aniel; Krahn, Natalie J.
  • Nucleic Acids Research, Vol. 46, Issue 10
  • DOI: 10.1093/nar/gky307

Microstructural degeneracy associated with a two-point correlation function and its information content
journal, May 2012


New developments in the ATSAS program package for small-angle scattering data analysis
journal, March 2012

  • Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V.
  • Journal of Applied Crystallography, Vol. 45, Issue 2
  • DOI: 10.1107/s0021889812007662

Combination of X-ray crystallography, SAXS and DEER to obtain the structure of the FnIII-3,4 domains of integrin α6β4
journal, March 2015

  • Alonso-García, Noelia; García-Rubio, Inés; Manso, José A.
  • Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 4
  • DOI: 10.1107/s1399004715002485

Versatile sample environments and automation for biological solution X-ray scattering experiments at the P12 beamline (PETRA III, DESY)
journal, March 2015

  • Blanchet, Clement E.; Spilotros, Alessandro; Schwemmer, Frank
  • Journal of Applied Crystallography, Vol. 48, Issue 2
  • DOI: 10.1107/s160057671500254x

Interpretation of solution scattering data from lipid nanodiscs
journal, February 2018

  • Graziano, Vito; Miller, Lisa; Yang, Lin
  • Journal of Applied Crystallography, Vol. 51, Issue 1
  • DOI: 10.1107/s1600576717018441

Photocage-initiated time-resolved solution X-ray scattering investigation of protein dimerization
journal, September 2018


The structure of VgrG1 from Pseudomonas aeruginosa , the needle tip of the bacterial type VI secretion system
journal, January 2016

  • Spínola-Amilibia, Mercedes; Davó-Siguero, Irene; Ruiz, Federico M.
  • Acta Crystallographica Section D Structural Biology, Vol. 72, Issue 1
  • DOI: 10.1107/S2059798315021142

Structural insights into the interaction of the conserved mammalian proteins GAPR-1 and Beclin 1, a key autophagy protein
journal, August 2017

  • Li, Yue; Zhao, Yuting; Su, Minfei
  • Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 9
  • DOI: 10.1107/S2059798317011822

Flexibility of truncated and full-length glucansucrase GTF180 enzymes from Lactobacillus reuteri 180
journal, March 2014

  • Pijning, Tjaard; Vujičić-Žagar, Andreja; Kralj, Slavko
  • FEBS Journal, Vol. 281, Issue 9
  • DOI: 10.1111/febs.12769

Borrelia outer surface protein C is capable of human fibrinogen binding
journal, March 2019

  • Bierwagen, Paulina; Szpotkowski, Kamil; Jaskolski, Mariusz
  • The FEBS Journal, Vol. 286, Issue 12
  • DOI: 10.1111/febs.14810

A biophysical and structural study of two chitinases from Agave tequilana and their potential role as defense proteins
journal, July 2019

  • Sierra‐Gómez, Yusvel; Rodríguez‐Hernández, Annia; Cano‐Sánchez, Patricia
  • The FEBS Journal, Vol. 286, Issue 23
  • DOI: 10.1111/febs.14993

GGA Autoinhibition Revisited
journal, February 2010


Antagonists Induce a Conformational Change in cIAP1 That Promotes Autoubiquitination
journal, October 2011


Structural Basis for Assembly and Function of a Heterodimeric Plant Immune Receptor
journal, April 2014


Solution Structure, Self-Assembly, and Membrane Interactions of the Matrix Protein from Newcastle Disease Virus at Neutral and Acidic pH
journal, March 2019

  • Shtykova, E. V.; Petoukhov, M. V.; Dadinova, L. A.
  • Journal of Virology, Vol. 93, Issue 6
  • DOI: 10.1128/jvi.01450-18

Molecular Basis of Unusually High Neutralization Resistance in Tier 3 HIV-1 Strain 253-11
journal, April 2018

  • Moyo, Thandeka; Ereño-Orbea, June; Jacob, Rajesh Abraham
  • Journal of Virology, Vol. 92, Issue 14
  • DOI: 10.1128/jvi.02261-17

Структура частиц белка оболочки А вируса картофеля и их диссоциация
journal, January 2018

  • Ксенофонтов, А. Л.; Добров, Е. Н.; Федорова, Н. В.
  • Молекулярная биология, Vol. 52, Issue 6
  • DOI: 10.1134/S0026898418060101

High-resolution structure of a type IV pilin from the metal-reducing bacterium Shewanella oneidensis
journal, February 2015

  • Gorgel, Manuela; Ulstrup, Jakob Jensen; Bøggild, Andreas
  • BMC Structural Biology, Vol. 15, Issue 1
  • DOI: 10.1186/s12900-015-0031-7

The mechanism by which a distinguishing arabinofuranosidase can cope with internal di-substitutions in arabinoxylans
journal, August 2018

  • dos Santos, Camila Ramos; de Giuseppe, Priscila Oliveira; de Souza, Flávio Henrique Moreira
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1212-y

Structural Insights into the Mechanism of Phosphoregulation of the Retinoblastoma Protein
journal, March 2013


Structural Analysis of Influenza A Virus Matrix Protein M1 and Its Self-Assemblies at Low pH
journal, December 2013


An alkaline active feruloyl-CoA synthetase from soil metagenome as a potential key enzyme for lignin valorization strategies
journal, February 2019


The Vibrio cholerae Colonization Factor GbpA Possesses a Modular Structure that Governs Binding to Different Host Surfaces
journal, January 2012


Lectin-Like Bacteriocins from Pseudomonas spp. Utilise D-Rhamnose Containing Lipopolysaccharide as a Cellular Receptor
journal, February 2014


Long non‐coding subgenomic flavivirus RNAs have extended 3D structures and are flexible in solution
journal, September 2019


Maturation of 6S regulatory RNA to a highly elongated structure
text, January 2015

  • Fadouloglou, Vasiliki; Lin, Hong-Tin; Tria, Giancarlo
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2016-00780

Structural and Dynamics Studies of a Truncated Variant of CI Repressor From Bacteriophage TP901-1
text, January 2016

  • Rasmussen, Kim Krighaar; Frandsen, Kristian E. H.; Boeri Erba, Elisabetta
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2016-02731

The Redox State Regulates the Conformation of Rv2466c to Activate the Antitubercular Prodrug TP053
text, January 2015

  • Albesa-Jové, David; Comino, Natalia; Tersa, Montse
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2016-04571

X-Ray Solution Scattering Study of Four Escherichia coli Enzymes Involved in Stationary-Phase Metabolism
text, January 2016

  • Dadinova, Liubov A.; Shtykova, Eleonora V.; Konarev, Petr V.
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2017-00416

Myelin 2′,3′-Cyclic Nucleotide 3′-Phosphodiesterase: Active-Site Ligand Binding and Molecular Conformation
text, January 2012

  • Myllykoski, Matti; Raasakka, Arne; Han, Huijong
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2017-05054

Molecular basis of the 14-3-3 protein-dependent activation of yeast neutral trehalase Nth1
text, January 2017

  • Alblova, Miroslava; Smidova, Aneta; Docekal, Vojtech
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2017-12382

SAXS and stability studies of iron-induced oligomers of bacterial frataxin CyaY
text, January 2017

  • Fekry, Mostafa; Alshokry, Wessen; Grela, Przemysław
  • Deutsches Elektronen-Synchrotron, DESY, Hamburg
  • DOI: 10.3204/pubdb-2017-14027

Combination of SAXS and Protein Painting Discloses the Three-Dimensional Organization of the Bacterial Cysteine Synthase Complex, a Potential Target for Enhancers of Antibiotic Action
journal, October 2019

  • Rosa, Brenda; Marchetti, Marialaura; Paredi, Gianluca
  • International Journal of Molecular Sciences, Vol. 20, Issue 20
  • DOI: 10.3390/ijms20205219

Phosphorylation-mediated PTEN conformational closure and deactivation revealed with protein semisynthesis
journal, July 2013


Structural basis of interprotein electron transfer in bacterial sulfite oxidation
journal, December 2015

  • McGrath, Aaron P.; Laming, Elise L.; Casas Garcia, G. Patricia
  • eLife, Vol. 4
  • DOI: 10.7554/elife.09066

Importin-9 wraps around the H2A-H2B core to act as nuclear importer and histone chaperone
journal, March 2019

  • Padavannil, Abhilash; Sarkar, Prithwijit; Kim, Seung Joong
  • eLife, Vol. 8
  • DOI: 10.7554/eLife.43630