This content will become publicly available on November 18, 2020
Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions
Abstract
Amino acid availability in Gram-positive bacteria is monitored by T-box riboswitches. T-boxes directly bind tRNAs, assess their aminoacylation state, and regulate the transcription or translation of downstream genes to maintain nutritional homeostasis. Here in this paper, we report cocrystal and cryo-EM structures of Geobacillus kaustophilus and Bacillus subtilis T-box–tRNA complexes, detailing their multivalent, exquisitely selective interactions. The T-box forms a U-shaped molecular vise that clamps the tRNA, captures its 3' end using an elaborate ‘discriminator’ structure, and interrogates its aminoacylation state using a steric filter fashioned from a wobble base pair. In the absence of aminoacylation, T-boxes clutch tRNAs and form a continuously stacked central spine, permitting transcriptional readthrough or translation initiation. A modeled aminoacyl disrupts tRNA-T-box stacking, severing the central spine and blocking gene expression. Our data establish a universal mechanism of amino acid sensing on tRNAs and gene regulation by T-box riboswitches and exemplify how higher-order RNA-RNA interactions achieve multivalency and specificity.
- Authors:
-
[2];
[6];
[1]
- National Inst. of Diabetes and Digestive and Kidney Diseases, Bethesda, MD (United States). Lab. of Molecular Biology
- Stanford Univ., CA (United States). James H. Clark Center
- Univ. Paris-Sud, Gif-sur-Yvette (France). Inst. for Integrative Biology of the Cell (I2BC)
- Univ. of Patras, Patras (Greece)
- National Cancer Inst., Frederick, MD (United States).Center for Cancer Research; Frederick National Lab. for Cancer Research, Frederick, MD (United States)
- Baylor College of Medicine, Houston, TX (United States)
- National Cancer Inst., Frederick, MD (United States). Structural Biophysics Lab., Center for Cancer Research
- Publication Date:
- Research Org.:
- SLAC National Accelerator Lab., Menlo Park, CA (United States)
- Sponsoring Org.:
- USDOE; National Institutes of Health (NIH); European Union (EU)
- OSTI Identifier:
- 1595138
- Grant/Contract Number:
- AC02-76SF00515
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Structural & Molecular Biology
- Additional Journal Information:
- Journal Volume: 26; Journal Issue: 12; Journal ID: ISSN 1545-9993
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Li, Shuang, Su, Zhaoming, Lehmann, Jean, Stamatopoulou, Vassiliki, Giarimoglou, Nikoleta, Henderson, Frances E., Fan, Lixin, Pintilie, Grigore D., Zhang, Kaiming, Chen, Muyuan, Ludtke, Steven J., Wang, Yun-Xing, Stathopoulos, Constantinos, Chiu, Wah, and Zhang, Jinwei. Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions. United States: N. p., 2019.
Web. doi:10.1038/s41594-019-0326-7.
Li, Shuang, Su, Zhaoming, Lehmann, Jean, Stamatopoulou, Vassiliki, Giarimoglou, Nikoleta, Henderson, Frances E., Fan, Lixin, Pintilie, Grigore D., Zhang, Kaiming, Chen, Muyuan, Ludtke, Steven J., Wang, Yun-Xing, Stathopoulos, Constantinos, Chiu, Wah, & Zhang, Jinwei. Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions. United States. doi:10.1038/s41594-019-0326-7.
Li, Shuang, Su, Zhaoming, Lehmann, Jean, Stamatopoulou, Vassiliki, Giarimoglou, Nikoleta, Henderson, Frances E., Fan, Lixin, Pintilie, Grigore D., Zhang, Kaiming, Chen, Muyuan, Ludtke, Steven J., Wang, Yun-Xing, Stathopoulos, Constantinos, Chiu, Wah, and Zhang, Jinwei. Mon .
"Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions". United States. doi:10.1038/s41594-019-0326-7.
@article{osti_1595138,
title = {Structural basis of amino acid surveillance by higher-order tRNA-mRNA interactions},
author = {Li, Shuang and Su, Zhaoming and Lehmann, Jean and Stamatopoulou, Vassiliki and Giarimoglou, Nikoleta and Henderson, Frances E. and Fan, Lixin and Pintilie, Grigore D. and Zhang, Kaiming and Chen, Muyuan and Ludtke, Steven J. and Wang, Yun-Xing and Stathopoulos, Constantinos and Chiu, Wah and Zhang, Jinwei},
abstractNote = {Amino acid availability in Gram-positive bacteria is monitored by T-box riboswitches. T-boxes directly bind tRNAs, assess their aminoacylation state, and regulate the transcription or translation of downstream genes to maintain nutritional homeostasis. Here in this paper, we report cocrystal and cryo-EM structures of Geobacillus kaustophilus and Bacillus subtilis T-box–tRNA complexes, detailing their multivalent, exquisitely selective interactions. The T-box forms a U-shaped molecular vise that clamps the tRNA, captures its 3' end using an elaborate ‘discriminator’ structure, and interrogates its aminoacylation state using a steric filter fashioned from a wobble base pair. In the absence of aminoacylation, T-boxes clutch tRNAs and form a continuously stacked central spine, permitting transcriptional readthrough or translation initiation. A modeled aminoacyl disrupts tRNA-T-box stacking, severing the central spine and blocking gene expression. Our data establish a universal mechanism of amino acid sensing on tRNAs and gene regulation by T-box riboswitches and exemplify how higher-order RNA-RNA interactions achieve multivalency and specificity.},
doi = {10.1038/s41594-019-0326-7},
journal = {Nature Structural & Molecular Biology},
number = 12,
volume = 26,
place = {United States},
year = {2019},
month = {11}
}
Free Publicly Available Full Text
This content will become publicly available on November 18, 2020
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Structural Determinants for Geometry and Information Decoding of tRNA by T Box Leader RNA
journal, November 2013
- Grigg, Jason C.; Ke, Ailong
- Structure, Vol. 21, Issue 11
Sequence requirements for terminators and antiterminators in the T box transcription antitermination system: disparity between conservation and functional requirements
journal, April 2002
- Grundy, F. J.
- Nucleic Acids Research, Vol. 30, Issue 7
The kink-turn: a new RNA secondary structure motif
journal, August 2001
- Klein, D. J.
- The EMBO Journal, Vol. 20, Issue 15
Discovery of Small‐Molecule Antibiotics against a Unique tRNA‐Mediated Regulation of Transcription in Gram‐Positive Bacteria
journal, February 2019
- Frohlich, Kyla M.; Weintraub, Spencer F.; Bell, Janeen T.
- ChemMedChem, Vol. 14, Issue 7
Attenuation in the control of expression of bacterial operons
journal, February 1981
- Yanofsky, Charles
- Nature, Vol. 289, Issue 5800
Identification of thermodynamically relevant interactions between EF-Tu and backbone elements of tRNA
journal, May 2001
- Pleiss, Jeffrey A.; Uhlenbeck, Olke C.
- Journal of Molecular Biology, Vol. 308, Issue 5
Use of Cis- and Trans-Ribozymes to Remove 5' and 3' Heterogeneities From Milligrams of In Vitro Transcribed RNA
journal, January 1996
- Ferre-D'Amare, A. R.; Doudna, J. A.
- Nucleic Acids Research, Vol. 24, Issue 5
Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro.
journal, February 1988
- Sampson, J. R.; Uhlenbeck, O. C.
- Proceedings of the National Academy of Sciences, Vol. 85, Issue 4
Co-crystal structure of a T-box riboswitch stem I domain in complex with its cognate tRNA
journal, July 2013
- Zhang, Jinwei; Ferré-D’Amaré, Adrian R.
- Nature, Vol. 500, Issue 7462
Ultrasonic relaxation evaluation of the thermodynamics of syn-anti glycosidic isomerization in adenosine
journal, September 1974
- Hemmes, Paul R.; Oppenheimer, Leslie; Jordan, Frank
- Journal of the American Chemical Society, Vol. 96, Issue 19
Transacylation rates of aminoacyladenosine moiety at the 3'-terminus of aminoacyl-transfer ribonucleic acid
journal, June 1983
- Taiji, Mutsuo; Yokoyama, Shigeyuki; Miyazawa, Tatsuo
- Biochemistry, Vol. 22, Issue 13
Pervasive tertiary structure in the dengue virus RNA genome
journal, October 2018
- Dethoff, Elizabeth A.; Boerneke, Mark A.; Gokhale, Nandan S.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 45
ATSAS 2.8 : a comprehensive data analysis suite for small-angle scattering from macromolecular solutions
journal, June 2017
- Franke, D.; Petoukhov, M. V.; Konarev, P. V.
- Journal of Applied Crystallography, Vol. 50, Issue 4
Structure and mechanism of the T-box riboswitches: Structure and mechanism of the T-box riboswitches
journal, May 2015
- Zhang, Jinwei; Ferré-D'Amaré, Adrian R.
- Wiley Interdisciplinary Reviews: RNA, Vol. 6, Issue 4
The CASTOR Proteins Are Arginine Sensors for the mTORC1 Pathway
journal, March 2016
- Chantranupong, Lynne; Scaria, Sonia M.; Saxton, Robert A.
- Cell, Vol. 165, Issue 1
A Method for Helical RNA Global Structure Determination in Solution Using Small-Angle X-Ray Scattering and NMR Measurements
journal, October 2009
- Wang, Jinbu; Zuo, Xiaobing; Yu, Ping
- Journal of Molecular Biology, Vol. 393, Issue 3
Structural and Dynamic Basis for Low-Affinity, High-Selectivity Binding of L-Glutamine by the Glutamine Riboswitch
journal, December 2015
- Ren, Aiming; Xue, Yi; Peselis, Alla
- Cell Reports, Vol. 13, Issue 9
The Structural and Functional Diversity of Metabolite-Binding Riboswitches
journal, June 2009
- Roth, Adam; Breaker, Ronald R.
- Annual Review of Biochemistry, Vol. 78, Issue 1
Ensemble cryo-EM elucidates the mechanism of translation fidelity
journal, May 2017
- Loveland, Anna B.; Demo, Gabriel; Grigorieff, Nikolaus
- Nature, Vol. 546, Issue 7656
SEDPHAT – A platform for global ITC analysis and global multi-method analysis of molecular interactions
journal, April 2015
- Zhao, Huaying; Piszczek, Grzegorz; Schuck, Peter
- Methods, Vol. 76
The GA motif: An RNA element common to bacterial antitermination systems, rRNA, and eukaryotic RNAs
journal, August 2001
- Winkler, Wade C.; Grundy, Frank J.; Murphy, Brooke A.
- RNA, Vol. 7, Issue 8
Ribosome•RelA structures reveal the mechanism of stringent response activation
journal, July 2016
- Loveland, Anna B.; Bah, Eugene; Madireddy, Rohini
- eLife, Vol. 5
T box riboswitches in Actinobacteria: Translational regulation via novel tRNA interactions
journal, January 2015
- Sherwood, Anna V.; Grundy, Frank J.; Henkin, Tina M.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 4
An evolving tale of two interacting RNAs-themes and variations of the T-box riboswitch mechanism: NEW INSIGHTS INTO THE T-BOX RIBOSWITCH MECHANISM
journal, June 2019
- Suddala, Krishna C.; Zhang, Jinwei
- IUBMB Life, Vol. 71, Issue 8
High-Precision Isothermal Titration Calorimetry with Automated Peak-Shape Analysis
journal, June 2012
- Keller, Sandro; Vargas, Carolyn; Zhao, Huaying
- Analytical Chemistry, Vol. 84, Issue 11
Specific structural elements of the T-box riboswitch drive the two-step binding of the tRNA ligand
journal, September 2018
- Zhang, Jiacheng; Chetnani, Bhaskar; Cormack, Eric D.
- eLife, Vol. 7
Comparative genomic analysis of T-box regulatory systems in bacteria
journal, February 2008
- Vitreschak, A. G.; Mironov, A. A.; Lyubetsky, V. A.
- RNA, Vol. 14, Issue 4
Hierarchical mechanism of amino acid sensing by the T-box riboswitch
journal, May 2018
- Suddala, Krishna C.; Cabello-Villegas, Javier; Michnicka, Malgorzata
- Nature Communications, Vol. 9, Issue 1
Real-space refinement in PHENIX for cryo-EM and crystallography
journal, May 2018
- Afonine, Pavel V.; Poon, Billy K.; Read, Randy J.
- Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 6
Nutrient-Sensing Mechanisms across Evolution
journal, March 2015
- Chantranupong, Lynne; Wolfson, Rachel L.; Sabatini, David M.
- Cell, Vol. 161, Issue 1
Structure of the trp RNA-binding attenuation protein, TRAP, bound to RNA
journal, September 1999
- Antson, Alfred A.; Dodson, Eleanor J.; Dodson, Guy
- Nature, Vol. 401, Issue 6750
UCSF Chimera?A visualization system for exploratory research and analysis
journal, January 2004
- Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C.
- Journal of Computational Chemistry, Vol. 25, Issue 13
Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria
journal, April 2016
- Dar, D.; Shamir, M.; Mellin, J. R.
- Science, Vol. 352, Issue 6282
A glyS T-box riboswitch with species-specific structural features responding to both proteinogenic and nonproteinogenic tRNA Gly isoacceptors
journal, August 2015
- Apostolidi, Maria; Saad, Nizar Y.; Drainas, Denis
- RNA, Vol. 21, Issue 10
WebLogo: A Sequence Logo Generator
journal, May 2004
- Crooks, Gavin E.; Hon, Gary; Chandonia, John-Marc
- Genome Research, Vol. 14, Issue 6, p. 1188-1190
Amino acid recognition and gene regulation by riboswitches
journal, September 2009
- Serganov, Alexander; Patel, Dinshaw J.
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1789, Issue 9-10
Capture and Release of tRNA by the T-Loop Receptor in the Function of the T-Box Riboswitch
journal, July 2017
- Fang, Xianyang; Michnicka, Malgorzata; Zhang, Yikan
- Biochemistry, Vol. 56, Issue 28
The importance of helix P1 stability for structural pre-organization and ligand binding affinity of the adenine riboswitch aptamer domain
journal, May 2014
- Nozinovic, Senada; Reining, Anke; Kim, Yong-Boum
- RNA Biology, Vol. 11, Issue 5
Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families
journal, November 2017
- Kalvari, Ioanna; Argasinska, Joanna; Quinones-Olvera, Natalia
- Nucleic Acids Research, Vol. 46, Issue D1
The G·U wobble base pair: A fundamental building block of RNA structure crucial to RNA function in diverse biological systems
journal, July 2000
- Varani, Gabriele; McClain, William H.
- EMBO reports, Vol. 1, Issue 1
tRNA-mediated transcription antitermination in vitro: Codon-anticodon pairing independent of the ribosome
journal, August 2002
- Grundy, F. J.; Winkler, W. C.; Henkin, T. M.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 17
Direct modulation of T-box riboswitch-controlled transcription by protein synthesis inhibitors
journal, July 2017
- Stamatopoulou, Vassiliki; Apostolidi, Maria; Li, Shuang
- Nucleic Acids Research, Vol. 45, Issue 17
An Unusual Topological Structure of the HIV-1 Rev Response Element
journal, October 2013
- Fang, Xianyang; Wang, Jinbu; O’Carroll, Ina P.
- Cell, Vol. 155, Issue 3
Clustering procedures for the optimal selection of data sets from multiple crystals in macromolecular crystallography
journal, July 2013
- Foadi, James; Aller, Pierre; Alguel, Yilmaz
- Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 8
Correcting pervasive errors in RNA crystallography through enumerative structure prediction
journal, December 2012
- Chou, Fang-Chieh; Sripakdeevong, Parin; Dibrov, Sergey M.
- Nature Methods, Vol. 10, Issue 1
A universal RNA structural motif docking the elbow of tRNA in the ribosome, RNAse P and T-box leaders
journal, April 2013
- Lehmann, Jean; Jossinet, Fabrice; Gautheret, Daniel
- Nucleic Acids Research, Vol. 41, Issue 10
Structural basis for leucine sensing by the Sestrin2-mTORC1 pathway
journal, November 2015
- Saxton, R. A.; Knockenhauer, K. E.; Wolfson, R. L.
- Science, Vol. 351, Issue 6268
Transfer RNA recognition by aminoacyl-tRNA synthetases
journal, January 1999
- Beuning, Penny J.; Musier-Forsyth, Karin
- Biopolymers, Vol. 52, Issue 1
Ribosome-dependent activation of stringent control
journal, May 2016
- Brown, Alan; Fernández, Israel S.; Gordiyenko, Yuliya
- Nature, Vol. 534, Issue 7606
mRNA structure determines specificity of a polyQ-driven phase separation
journal, April 2018
- Langdon, Erin M.; Qiu, Yupeng; Ghanbari Niaki, Amirhossein
- Science, Vol. 360, Issue 6391
Uncharged tRNA Activates GCN2 by Displacing the Protein Kinase Moiety from a Bipartite tRNA-Binding Domain
journal, August 2000
- Dong, Jinsheng; Qiu, Hongfang; Garcia-Barrio, Minerva
- Molecular Cell, Vol. 6, Issue 2
Solution Structure of the Bacillus subtilis T-box Antiterminator RNA: Seven Nucleotide Bulge Characterized by Stacking and Flexibility
journal, February 2003
- Gerdeman, Melinda S.; Henkin, Tina M.; Hines, Jennifer V.
- Journal of Molecular Biology, Vol. 326, Issue 1
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
RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012
- Scheres, Sjors H. W.
- Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530
Geometric nomenclature and classification of RNA base pairs
journal, April 2001
- Leontis, Neocles B.; Westhof, Eric
- RNA, Vol. 7, Issue 4
Recognition of Cognate Transfer RNA by the 30S Ribosomal Subunit
journal, May 2001
- Ogle, J. M.
- Science, Vol. 292, Issue 5518
Structural basis of specific tRNA aminoacylation by a small in vitro selected ribozyme
journal, June 2008
- Xiao, Hong; Murakami, Hiroshi; Suga, Hiroaki
- Nature, Vol. 454, Issue 7202
Biochemical Features and Functional Implications of the RNA-Based T-Box Regulatory Mechanism
journal, March 2009
- Gutierrez-Preciado, A.; Henkin, T. M.; Grundy, F. J.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 1
Structures of riboswitch RNA reaction states by mix-and-inject XFEL serial crystallography
journal, November 2016
- Stagno, J. R.; Liu, Y.; Bhandari, Y. R.
- Nature, Vol. 541, Issue 7636
tRNA synthetase: tRNA aminoacylation and beyond: Aminoacyl-tRNA synthetases
journal, April 2014
- Pang, Yan Ling Joy; Poruri, Kiranmai; Martinis, Susan A.
- Wiley Interdisciplinary Reviews: RNA, Vol. 5, Issue 4
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
Factors that influence T box riboswitch efficacy and tRNA affinity
journal, September 2015
- Zeng, C.; Zhou, S.; Bergmeier, S. C.
- Bioorganic & Medicinal Chemistry, Vol. 23, Issue 17
Direct Evaluation of tRNA Aminoacylation Status by the T-Box Riboswitch Using tRNA-mRNA Stacking and Steric Readout
journal, July 2014
- Zhang, Jinwei; Ferré-D’Amaré, Adrian R.
- Molecular Cell, Vol. 55, Issue 1
ViennaRNA Package 2.0
journal, November 2011
- Lorenz, Ronny; Bernhart, Stephan H.; Höner zu Siederdissen, Christian
- Algorithms for Molecular Biology, Vol. 6, Issue 1
Structure of the 30 kDa HIV-1 RNA Dimerization Signal by a Hybrid Cryo-EM, NMR, and Molecular Dynamics Approach
journal, March 2018
- Zhang, Kaiming; Keane, Sarah C.; Su, Zhaoming
- Structure, Vol. 26, Issue 3
Molecular envelope and atomic model of an anti-terminated glyQS T-box regulator in complex with tRNAGly
journal, May 2017
- Chetnani, Bhaskar; Mondragón, Alfonso
- Nucleic Acids Research, Vol. 45, Issue 13
Kinetic Analysis of tRNA-Directed Transcription Antitermination of the Bacillus subtilis glyQS Gene In Vitro
journal, August 2004
- Grundy, F. J.; Henkin, T. M.
- Journal of Bacteriology, Vol. 186, Issue 16
Prevalence of syn nucleobases in the active sites of functional RNAs
journal, August 2011
- Sokoloski, J. E.; Godfrey, S. A.; Dombrowski, S. E.
- RNA, Vol. 17, Issue 10
On the wobble GoU and related pairs
journal, January 2000
- Masquida, BenoÎT; Westhof, Eric
- RNA, Vol. 6, Issue 1
tRNA as a positive regulator of transcription antitermination in B. subtilis
journal, August 1993
- Grundy, Frank J.; Henkin, Tina M.
- Cell, Vol. 74, Issue 3
tRNA requirements for glyQS antitermination: A new twist on tRNA
journal, September 2003
- Yousef, M. R.
- RNA, Vol. 9, Issue 9
ykkC riboswitches employ an add-on helix to adjust specificity for polyanionic ligands
journal, August 2018
- Peselis, Alla; Serganov, Alexander
- Nature Chemical Biology, Vol. 14, Issue 9
Emerging Roles for Intermolecular RNA-RNA Interactions in RNP Assemblies
journal, August 2018
- Van Treeck, Briana; Parker, Roy
- Cell, Vol. 174, Issue 4
Identification of Spermidine Binding Site in T-box Riboswitch Antiterminator RNA
journal, October 2015
- Liu, Jia; Zeng, Chunxi; Hogan, Vivian
- Chemical Biology & Drug Design, Vol. 87, Issue 2
T box RNA decodes both the information content and geometry of tRNA to affect gene expression
journal, April 2013
- Grigg, J. C.; Chen, Y.; Grundy, F. J.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 18
Phaser crystallographic software
journal, July 2007
- McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D.
- Journal of Applied Crystallography, Vol. 40, Issue 4
New tRNA contacts facilitate ligand binding in a Mycobacterium smegmatis T box riboswitch
journal, March 2018
- Sherwood, Anna V.; Frandsen, Jane K.; Grundy, Frank J.
- Proceedings of the National Academy of Sciences, Vol. 115, Issue 15
RNA phase transitions in repeat expansion disorders
journal, May 2017
- Jain, Ankur; Vale, Ronald D.
- Nature, Vol. 546, Issue 7657
Convolutional neural networks for automated annotation of cellular cryo-electron tomograms
journal, August 2017
- Chen, Muyuan; Dai, Wei; Sun, Stella Y.
- Nature Methods, Vol. 14, Issue 10
Two-codon T-box riboswitch binding two tRNAs
journal, July 2013
- Saad, N. Y.; Stamatopoulou, V.; Braye, M.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 31