Crystal Structure of VapBC-1 from Nontypeable Haemophilus influenzae and the Effect of PIN Domain Mutations on Survival during Infection
Abstract
Toxin-antitoxin (TA) gene pairs have been identified in nearly all bacterial genomes sequenced to date and are thought to facilitate persistence and antibiotic tolerance. TA loci are classified into various types based upon the characteristics of their antitoxins, with those in type II expressing proteic antitoxins. Many toxins from type II modules are ribonucleases that maintain a PilT N-terminal (PIN) domain containing conserved amino acids considered essential for activity. ThevapBC(virulence-associatedprotein) TA system is the largest subfamily in this class and has been linked to pathogenesis of nontypeableHaemophilus influenzae(NTHi). In this study reported here, the crystal structure of the VapBC-1 complex from NTHi was determined to 2.20 Å resolution. Based on this structure, aspartate-to-asparagine and glutamate-to-glutamine mutations of four conserved residues in the PIN domain of the VapC-1 toxin were constructed and the effects of the mutations on protein-protein interactions, growth ofEscherichia coli, and pathogenesisex vivowere tested. Finally, a novel model system was designed and utilized that consists of an NTHi ΔvapBC-1strain complemented inciswith the TA module containing a mutated or wild-type toxin at an ectopic site on the chromosome. This enabled the analysis of the effect of PIN domain toxin mutants in tandem with their wild-type antitoxin under the controlmore »
- Authors:
-
- Old Dominion Univ., Norfolk, VA (United States)
- Univ. of Kansas, Lawrence, KS (United States)
- Hauptman Woodward Medical Research Inst., Argonne, IL (United States)
- National Inst. of Health, Rockville, MD (United States). National Center for Advancing Translational Sciences
- Publication Date:
- Research Org.:
- Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
- Sponsoring Org.:
- National Institute on Deafness and Other Communication Disorders (NIDCD); National Center for Advancing Translational Sciences (NCATS) Division of Pre-Clinical Innovation Intramural Program; National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); Industrial Macromolecular Crystallography Association; USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1526058
- Grant/Contract Number:
- P30 GM110761; AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Bacteriology
- Additional Journal Information:
- Journal Volume: 201; Journal Issue: 12; Journal ID: ISSN 0021-9193
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; PIN domain; crystal structure; persistence; protein-protein interactions; ribonuclease; toxin-antitoxin
Citation Formats
Molinaro, Ashley L., Kashipathy, Maithri M., Lovell, Scott, Battaile, Kevin P., Coussens, Nathan P., Shen, Min, and Daines, Dayle A. Crystal Structure of VapBC-1 from Nontypeable Haemophilus influenzae and the Effect of PIN Domain Mutations on Survival during Infection. United States: N. p., 2019.
Web. doi:10.1128/JB.00026-19.
Molinaro, Ashley L., Kashipathy, Maithri M., Lovell, Scott, Battaile, Kevin P., Coussens, Nathan P., Shen, Min, & Daines, Dayle A. Crystal Structure of VapBC-1 from Nontypeable Haemophilus influenzae and the Effect of PIN Domain Mutations on Survival during Infection. United States. https://doi.org/10.1128/JB.00026-19
Molinaro, Ashley L., Kashipathy, Maithri M., Lovell, Scott, Battaile, Kevin P., Coussens, Nathan P., Shen, Min, and Daines, Dayle A. Mon .
"Crystal Structure of VapBC-1 from Nontypeable Haemophilus influenzae and the Effect of PIN Domain Mutations on Survival during Infection". United States. https://doi.org/10.1128/JB.00026-19. https://www.osti.gov/servlets/purl/1526058.
@article{osti_1526058,
title = {Crystal Structure of VapBC-1 from Nontypeable Haemophilus influenzae and the Effect of PIN Domain Mutations on Survival during Infection},
author = {Molinaro, Ashley L. and Kashipathy, Maithri M. and Lovell, Scott and Battaile, Kevin P. and Coussens, Nathan P. and Shen, Min and Daines, Dayle A.},
abstractNote = {Toxin-antitoxin (TA) gene pairs have been identified in nearly all bacterial genomes sequenced to date and are thought to facilitate persistence and antibiotic tolerance. TA loci are classified into various types based upon the characteristics of their antitoxins, with those in type II expressing proteic antitoxins. Many toxins from type II modules are ribonucleases that maintain a PilT N-terminal (PIN) domain containing conserved amino acids considered essential for activity. ThevapBC(virulence-associatedprotein) TA system is the largest subfamily in this class and has been linked to pathogenesis of nontypeableHaemophilus influenzae(NTHi). In this study reported here, the crystal structure of the VapBC-1 complex from NTHi was determined to 2.20 Å resolution. Based on this structure, aspartate-to-asparagine and glutamate-to-glutamine mutations of four conserved residues in the PIN domain of the VapC-1 toxin were constructed and the effects of the mutations on protein-protein interactions, growth ofEscherichia coli, and pathogenesisex vivowere tested. Finally, a novel model system was designed and utilized that consists of an NTHi ΔvapBC-1strain complemented inciswith the TA module containing a mutated or wild-type toxin at an ectopic site on the chromosome. This enabled the analysis of the effect of PIN domain toxin mutants in tandem with their wild-type antitoxin under the control of thevapBC-1native promoter and in single copy. This is the first report of a system facilitating the study of TA mutant operons in the background of NTHi during infections of primary human tissuesex vivo.},
doi = {10.1128/JB.00026-19},
journal = {Journal of Bacteriology},
number = 12,
volume = 201,
place = {United States},
year = {Mon Apr 01 00:00:00 EDT 2019},
month = {Mon Apr 01 00:00:00 EDT 2019}
}
Web of Science
Works referenced in this record:
Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes
journal, February 2005
- Pandey, D. P.
- Nucleic Acids Research, Vol. 33, Issue 3
Linking Crystallographic Model and Data Quality
journal, May 2012
- Karplus, P. A.; Diederichs, K.
- Science, Vol. 336, Issue 6084
Toxin-Antitoxin Modules May Regulate Synthesis of Macromolecules during Nutritional Stress
journal, February 2000
- Gerdes, K.
- Journal of Bacteriology, Vol. 182, Issue 3
Mechanism of post-segregational killing by the hoklsok system of plasmid R1: sok antisense RNA regulates formation of a hok mRNA species correlated with killing of plasmid-free cells
journal, November 1990
- Gerdes, K.; Thisted, T.; Martinussen, J.
- Molecular Microbiology, Vol. 4, Issue 11
Autoregulation and Virulence Control by the Toxin-Antitoxin System SavRS in Staphylococcus aureus
journal, February 2018
- Wen, Wen; Liu, Banghui; Xue, Lu
- Infection and Immunity, Vol. 86, Issue 5
Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells.
journal, May 1986
- Gerdes, K.; Rasmussen, P. B.; Molin, S.
- Proceedings of the National Academy of Sciences, Vol. 83, Issue 10
The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family
journal, August 1998
- Gotfredsen, Marie; Gerdes, Kenn
- Molecular Microbiology, Vol. 29, Issue 4
RelE, a global inhibitor of translation, is activated during nutritional stress
journal, November 2001
- Christensen, S. K.; Mikkelsen, M.; Pedersen, K.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 25
Developments in the CCP 4 molecular-graphics project
journal, November 2004
- Potterton, Liz; McNicholas, Stuart; Krissinel, Eugene
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12
The phage abortive infection system, ToxIN, functions as a protein–RNA toxin–antitoxin pair
journal, January 2009
- Fineran, Peter C.; Blower, Tim R.; Foulds, Ian J.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 3
Wake me when it’s over – Bacterial toxin–antitoxin proteins and induced dormancy
journal, May 2016
- Coussens, Nathan P.; Daines, Dayle A.
- Experimental Biology and Medicine, Vol. 241, Issue 12
Diversity of bacterial type II toxin–antitoxin systems: a comprehensive search and functional analysis of novel families
journal, March 2011
- Leplae, Raphaël; Geeraerts, Damien; Hallez, Régis
- Nucleic Acids Research, Vol. 39, Issue 13
Single nucleotide polymorphisms of Beijing lineage Mycobacterium tuberculosis toxin-antitoxin system genes: Their role in the changes of protein activity and evolution
journal, September 2018
- Zaychikova, M. V.; Mikheecheva, N. E.; Belay, Y. O.
- Tuberculosis, Vol. 112
Mini-F plasmid genes that couple host cell division to plasmid proliferation.
journal, August 1983
- Ogura, T.; Hiraga, S.
- Proceedings of the National Academy of Sciences, Vol. 80, Issue 15
Toxin-antitoxin loci vapBC-1 and vapXD contribute to survival and virulence in nontypeable Haemophilus influenzae
journal, January 2012
- Ren, Dabin; Walker, Anna N.; Daines, Dayle A.
- BMC Microbiology, Vol. 12, Issue 1
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions
journal, November 2004
- Krissinel, E.; Henrick, K.
- Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12
Construction of a nontypeable Haemophilus influenzae-specific ectopic delivery vector
journal, June 2004
- Daines, Dayle A.; Smith, Arnold L.
- Journal of Microbiological Methods, Vol. 57, Issue 3
A new type V toxin-antitoxin system where mRNA for toxin GhoT is cleaved by antitoxin GhoS
journal, September 2012
- Wang, Xiaoxue; Lord, Dana M.; Cheng, Hsin-Yao
- Nature Chemical Biology, Vol. 8, Issue 10
Crystal structure of the DNA-bound VapBC2 antitoxin/toxin pair from Rickettsia felis
journal, December 2011
- Maté, María J.; Vincentelli, Renaud; Foos, Nicolas
- Nucleic Acids Research, Vol. 40, Issue 7
Toxins of Prokaryotic Toxin-Antitoxin Systems with Sequence-Specific Endoribonuclease Activity
journal, April 2017
- Masuda, Hisako; Inouye, Masayori
- Toxins, Vol. 9, Issue 4
Structural analysis of the active site architecture of the VapC toxin from Shigella flexneri : Active Site Architecture of
journal, April 2016
- Xu, Kehan; Dedic, Emil; Brodersen, Ditlev E.
- Proteins: Structure, Function, and Bioinformatics, Vol. 84, Issue 7
Regulation of the vapBC-1 Toxin-Antitoxin Locus in Nontypeable Haemophilus influenzae
journal, March 2012
- Cline, Susan D.; Saleem, Sehresh; Daines, Dayle A.
- PLoS ONE, Vol. 7, Issue 3
Identification and characterization of a family of toxin-antitoxin systems related to the Enterococcus faecalis plasmid pAD1 par addiction module
journal, June 2009
- Weaver, K. E.; Reddy, S. G.; Brinkman, C. L.
- Microbiology, Vol. 155, Issue 9
Scaling and assessment of data quality
journal, December 2005
- Evans, Philip
- Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 1, p. 72-82
Structural, functional and biological insights into the role of Mycobacterium tuberculosis VapBC11 toxin–antitoxin system: targeting a tRNase to tackle mycobacterial adaptation
journal, October 2018
- Deep, Amar; Tiwari, Prabhakar; Agarwal, Sakshi
- Nucleic Acids Research, Vol. 46, Issue 21
Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007
- Krissinel, Evgeny; Henrick, Kim
- Journal of Molecular Biology, Vol. 372, Issue 3
XDS
journal, January 2010
- Kabsch, Wolfgang
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3',5'-bispyrophosphate: a model for programmed bacterial cell death.
journal, June 1996
- Aizenman, E.; Engelberg-Kulka, H.; Glaser, G.
- Proceedings of the National Academy of Sciences, Vol. 93, Issue 12
YeeU enhances the bundling of cytoskeletal polymers of MreB and FtsZ, antagonizing the CbtA (YeeV) toxicity in Escherichia coli: YeeU enhances bundling of MreB and FtsZ filaments
journal, May 2012
- Masuda, Hisako; Tan, Qian; Awano, Naoki
- Molecular Microbiology, Vol. 84, Issue 5
MoRDa , an automatic molecular replacement pipeline
journal, August 2015
- Vagin, Alexey; Lebedev, Andrey
- Acta Crystallographica Section A Foundations and Advances, Vol. 71, Issue a1
Enteric virulence associated protein VapC inhibits translation by cleavage of initiator tRNA
journal, April 2011
- Winther, K. S.; Gerdes, K.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 18
Toxin-Antitoxin Systems in Bacteria and Archaea
journal, December 2011
- Yamaguchi, Yoshihiro; Park, Jung-Ho; Inouye, Masayori
- Annual Review of Genetics, Vol. 45, Issue 1
YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB: YeeV targets the cytoskeleton proteins
journal, November 2010
- Tan, Qian; Awano, Naoki; Inouye, Masayori
- Molecular Microbiology, Vol. 79, Issue 1
VapC-1 of Nontypeable Haemophilus influenzae Is a Ribonuclease
journal, May 2007
- Daines, D. A.; Wu, M. H.; Yuan, S. Y.
- Journal of Bacteriology, Vol. 189, Issue 14
Driving Forces of Gyrase Recognition by the Addiction Toxin CcdB
journal, May 2009
- Simic, Mario; De Jonge, Natalie; Loris, Remy
- Journal of Biological Chemistry, Vol. 284, Issue 30
Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
journal, July 1995
- Guzman, L. M.; Belin, D.; Carson, M. J.
- Journal of Bacteriology, Vol. 177, Issue 14, p. 4121-4130
Type IV pili and cell motility
journal, April 1999
- Wall, Daniel; Kaiser, Dale
- Molecular Microbiology, Vol. 32, Issue 1
Structural conservation of the PIN domain active site across all domains of life: Conservation of the PIN Domain
journal, May 2017
- Senissar, M.; Manav, M. C.; Brodersen, D. E.
- Protein Science, Vol. 26, Issue 8
Evidence for Multimerization of Neu Proteins Involved in Polysialic Acid Synthesis in Escherichia coli K1 Using Improved LexA-Based Vectors
journal, September 2000
- Daines, D. A.; Silver, R. P.
- Journal of Bacteriology, Vol. 182, Issue 18
System-Wide Analysis Unravels the Differential Regulation and In Vivo Essentiality of Virulence-Associated Proteins B and C Toxin-Antitoxin Systems of Mycobacterium tuberculosis
journal, February 2018
- Agarwal, Sakshi; Tiwari, Prabhakar; Deep, Amar
- The Journal of Infectious Diseases, Vol. 217, Issue 11
Bacterial addiction module toxin Doc inhibits translation elongation through its association with the 30S ribosomal subunit
journal, April 2008
- Liu, M.; Zhang, Y.; Inouye, M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 15
A Novel Mechanism of Programmed Cell Death in Bacteria by Toxin–Antitoxin Systems Corrupts Peptidoglycan Synthesis
journal, March 2011
- Mutschler, Hannes; Gebhardt, Maike; Shoeman, Robert L.
- PLoS Biology, Vol. 9, Issue 3
Improved R-factors for diffraction data analysis in macromolecular crystallography
journal, April 1997
- Diederichs, Kay; Karplus, P. Andrew
- Nature Structural Biology, Vol. 4, Issue 4
Characteristics of Streptococcus mutans strains lacking the MazEF and RelBE toxinâantitoxin modules
journal, December 2005
- Lemos, José A. C.; Brown, Thomas A.; Abranches, Jacqueline
- FEMS Microbiology Letters, Vol. 253, Issue 2
Crystal structure of Mycobacterium tuberculosis VapC20 toxin and its interactions with cognate antitoxin, VapB20, suggest a model for toxin-antitoxin assembly
journal, October 2017
- Deep, Amar; Kaundal, Soni; Agarwal, Sakshi
- The FEBS Journal, Vol. 284, Issue 23
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
Use of the EpiAirway Model for Characterizing Long-term Host-pathogen Interactions
journal, January 2011
- Ren, Dabin; Daines, Dayle A.
- Journal of Visualized Experiments, Issue 55
The PIN-domain ribonucleases and the prokaryotic VapBC toxin-antitoxin array
journal, October 2010
- Arcus, V. L.; McKenzie, J. L.; Robson, J.
- Protein Engineering Design and Selection, Vol. 24, Issue 1-2
Comprehensive Functional Analysis of Mycobacterium tuberculosis Toxin-Antitoxin Systems: Implications for Pathogenesis, Stress Responses, and Evolution
journal, December 2009
- Ramage, Holly R.; Connolly, Lynn E.; Cox, Jeffery S.
- PLoS Genetics, Vol. 5, Issue 12
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
Kinase Activity of Overexpressed HipA Is Required for Growth Arrest and Multidrug Tolerance in Escherichia coli
journal, October 2006
- Correia, F. F.; D'Onofrio, A.; Rejtar, T.
- Journal of Bacteriology, Vol. 188, Issue 24, p. 8360-8367
Resolving Some Old Problems in Protein Crystallography
journal, May 2012
- Evans, P.
- Science, Vol. 336, Issue 6084
Toxin-Antitoxin Systems in Clinical Pathogens
journal, July 2016
- Fernández-García, Laura; Blasco, Lucia; Lopez, Maria
- Toxins, Vol. 8, Issue 7
PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
A Bacterial Toxin Inhibits DNA Replication Elongation through a Direct Interaction with the β Sliding Clamp
journal, December 2013
- Aakre, Christopher D.; Phung, Tuyen N.; Huang, David
- Molecular Cell, Vol. 52, Issue 5
An introduction to data reduction: space-group determination, scaling and intensity statistics
journal, March 2011
- Evans, Philip R.
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
Simplified Media for the Growth of Haemophilus influenzae from Clinical and Normal Flora Sources
journal, August 1979
- Klein, R. D.; Luginbuhl, G. H.
- Journal of General Microbiology, Vol. 113, Issue 2
chpA and chpB, Escherichia coli chromosomal homologs of the pem locus responsible for stable maintenance of plasmid R100.
journal, November 1993
- Masuda, Y.; Miyakawa, K.; Nishimura, Y.
- Journal of Bacteriology, Vol. 175, Issue 21
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7
journal, June 2008
- Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S.
- Nature Protocols, Vol. 3, Issue 7
Data processing and analysis with the autoPROC toolbox
journal, March 2011
- Vonrhein, Clemens; Flensburg, Claus; Keller, Peter
- Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
A processed noncoding RNA regulates an altruistic bacterial antiviral system
journal, January 2011
- Blower, Tim R.; Pei, Xue Y.; Short, Francesca L.
- Nature Structural & Molecular Biology, Vol. 18, Issue 2
Changes in Frequency and Pathogens Causing Acute Otitis Media in 1995–2003
journal, January 2004
- Casey, Janet R.; Pichichero, Michael E.
- The Pediatric Infectious Disease Journal, Vol. 23, Issue 9
The Small RNA IstR Inhibits Synthesis of an SOS-Induced Toxic Peptide
journal, December 2004
- Vogel, Jörg; Argaman, Liron; Wagner, E. Gerhart H.
- Current Biology, Vol. 14, Issue 24
Analysis of Non-Typeable Haemophilous influenzae VapC1 Mutations Reveals Structural Features Required for Toxicity and Flexibility in the Active Site
journal, November 2014
- Hamilton, Brooke; Manzella, Alexander; Schmidt, Karyn
- PLoS ONE, Vol. 9, Issue 11
Automatic indexing of rotation diffraction patterns
journal, February 1988
- Kabsch, W.
- Journal of Applied Crystallography, Vol. 21, Issue 1
ATP-dependent Degradation of CcdA by Lon Protease: EFFECTS OF SECONDARY STRUCTURE AND HETEROLOGOUS SUBUNIT INTERACTIONS
journal, November 1996
- Van Melderen, Laurence; Thi, Minh Hoa Dao; Lecchi, Paolo
- Journal of Biological Chemistry, Vol. 271, Issue 44
Dynamic Metabolic Adjustments and Genome Plasticity Are Implicated in the Heat Shock Response of the Extremely Thermoacidophilic Archaeon Sulfolobus solfataricus
journal, June 2006
- Tachdjian, S.; Kelly, R. M.
- Journal of Bacteriology, Vol. 188, Issue 12
Crystal Structure of the VapBC Toxin–Antitoxin Complex from Shigella flexneri Reveals a Hetero-Octameric DNA-Binding Assembly
journal, December 2011
- Dienemann, Christian; Bøggild, Andreas; Winther, Kristoffer S.
- Journal of Molecular Biology, Vol. 414, Issue 5
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
Small Toxic Proteins and the Antisense RNAs That Repress Them
journal, December 2008
- Fozo, E. M.; Hemm, M. R.; Storz, G.
- Microbiology and Molecular Biology Reviews, Vol. 72, Issue 4
Construction of a novel shuttle vector for use in Haemophilus influenzae and H. parainfluenzae
journal, December 2010
- Robinson, Esther; Juhas, Mario; Hood, Derek
- Journal of Microbiological Methods, Vol. 83, Issue 3
Spacing of the -10 and -35 regions in the tac promoter. Effect on its in vivo activity.
journal, March 1985
- Brosius, J.; Erfle, M.; Storella, J.
- Journal of Biological Chemistry, Vol. 260, Issue 6
Defined Medium for Growth of Haemophilus influenzae
journal, February 1970
- Herriott, Roger M.; Meyer, Eleanor Y.; Vogt, Marcella
- Journal of Bacteriology, Vol. 101, Issue 2
Defined Nongrowth Media for Stage II Development of Competence in Haemophilus influenzae
journal, February 1970
- Herriott, R. M.; Meyer, E. M.; Vogt, M.
- Journal of Bacteriology, Vol. 101, Issue 2
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen
journal, August 2020
- Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe
- JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome
journal, December 2019
- Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman
- Nature Communications, Vol. 10, Issue 1
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation
journal, February 2021
- Tillu, Vikas A.; Rae, James; Gao, Ya
- Nature Communications, Vol. 12, Issue 1
PHENIX: a comprehensive Python-based system for macromolecular structure solution.
text, January 2010
- Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
- Apollo - University of Cambridge Repository