Skeletal Dysplasia Mutations Effect on Human Filamins’ Structure and Mechanosensing

Seppälä, Jonne; Bernardi, Rafael C.; Haataja, Tatu J.  K.; Hellman, Maarit; Pentikäinen, Olli T.; Schulten, Klaus; Permi, Perttu; Ylänne, Jari; Pentikäinen, Ulla

doi:10.1038/s41598-017-04441-x

Title: Skeletal Dysplasia Mutations Effect on Human Filamins’ Structure and Mechanosensing

Journal Article · Mon Jun 26 00:00:00 EDT 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-04441-x· OSTI ID:1490409

Seppälä, Jonne ^[1]; Bernardi, Rafael C. ^[2]; Haataja, Tatu J. K. ^[1]; Hellman, Maarit ^[3]; Pentikäinen, Olli T. ^[1]; Schulten, Klaus ^[4]; Permi, Perttu ^[5]; Ylänne, Jari ^[1]; Pentikäinen, Ulla ^[1]

Univ. of Jyvaskyla (Finland). Dept. of Biological and Environmental Science. Nanoscience Center
Univ. of Illinois, Champaign, IL (United States). Beckman Inst. for Advanced Science and Technology
Univ. of Jyvaskyla (Finland). Dept. of Chemistry
Univ. of Illinois, Champaign, IL (United States). Beckman Inst. for Advanced Science and Technology. Dept. of Physics
Univ. of Jyvaskyla (Finland). Dept. of Biological and Environmental Science. Nanoscience Center. Dept. of Chemistry

Cells’ ability to sense mechanical cues in their environment is crucial for fundamental cellular processes, leading defects in mechanosensing to be linked to many diseases. The actin cross-linking protein Filamin has an important role in the conversion of mechanical forces into biochemical signals. Here, we reveal how mutations in Filamin genes known to cause Larsen syndrome and Frontometaphyseal dysplasia can affect the structure and therefore function of Filamin domains 16 and 17. Employing X-ray crystallography, the structure of these domains was first solved for the human Filamin B. The interaction seen between domains 16 and 17 is broken by shear force as revealed by steered molecular dynamics simulations. The effects of skeletal dysplasia associated mutations of the structure and mechanosensing properties of Filamin were studied by combining various experimental and theoretical techniques. The results showed that Larsen syndrome associated mutations destabilize or even unfold domain 17. Interestingly, those Filamin functions that are mediated via domain 17 interactions with other proteins are not necessarily affected as strongly interacting peptide binding to mutated domain 17 induces at least partial domain folding. Mutation associated to Frontometaphyseal dysplasia, in turn, transforms 16–17 fragment from compact to an elongated form destroying the force-regulated domain pair.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Illinois at Urbana-Champaign, IL (United States); Univ. of Jyvaskyla (Finland)

Sponsoring Organization:: USDOE Office of Science (SC); National Inst. of Health (NIH) (United States); Academy of Finland

Grant/Contract Number:: AC02-05CH11231; 9P41GM104601; 283481; 138327; 278668; 288235; 2000268; jyy2516

OSTI ID:: 1490409

Journal Information:: Scientific Reports, Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 11 works

Citation information provided by
Web of Science

References (78)

Exploring Residue Component Contributions to Dynamical Network Models of Allostery VanWart, Adam T.; Eargle, John; Luthey-Schulten, Zaida Journal of Chemical Theory and Computation, Vol. 8, Issue 8 https://doi.org/10.1021/ct300377a	journal	July 2012
SASBDB, a repository for biological small-angle scattering data Valentini, Erica; Kikhney, Alexey G.; Previtali, Gianpietro Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1047	journal	October 2014
Community structure in social and biological networks Girvan, M.; Newman, M. E. J. Proceedings of the National Academy of Sciences, Vol. 99, Issue 12 https://doi.org/10.1073/pnas.122653799	journal	June 2002
Betulin Is a Potent Anti-Tumor Agent that Is Enhanced by Cholesterol Mullauer, Franziska B.; Kessler, Jan H.; Medema, Jan Paul PLoS ONE, Vol. 4, Issue 4 https://doi.org/10.1371/journal.pone.0005361	journal	April 2009
Upgraded ESRF BM29 beamline for SAXS on macromolecules in solution Pernot, Petra; Round, Adam; Barrett, Ray Journal of Synchrotron Radiation, Vol. 20, Issue 4 https://doi.org/10.1107/S0909049513010431	journal	May 2013
Uniqueness of ab initio shape determination in small-angle scattering Volkov, Vladimir V.; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864 https://doi.org/10.1107/S0021889803000268	journal	April 2003
NAMD2: Greater Scalability for Parallel Molecular Dynamics Kalé, Laxmikant; Skeel, Robert; Bhandarkar, Milind Journal of Computational Physics, Vol. 151, Issue 1 https://doi.org/10.1006/jcph.1999.6201	journal	May 1999
Alignment and Searching for Common Protein Folds Using a Data Bank of Structural Templates Johnson, Mark S.; Overington, John P.; Blundell, Tom L. Journal of Molecular Biology, Vol. 231, Issue 3 https://doi.org/10.1006/jmbi.1993.1323	journal	June 1993
Filamin structure, function and mechanics: are altered filamin-mediated force responses associated with human disease? Sutherland-Smith, Andrew J. Biophysical Reviews, Vol. 3, Issue 1 https://doi.org/10.1007/s12551-011-0042-y	journal	January 2011
Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
High-Density Miniaturized Thermal Shift Assays as a General Strategy for Drug Discovery Pantoliano, M. W.; Petrella, E. C.; Kwasnoski, J. D. Journal of Biomolecular Screening, Vol. 6, Issue 6 https://doi.org/10.1177/108705710100600609	journal	December 2001
Dynamic force sensing of filamin revealed in single-molecule experiments Rognoni, L.; Stigler, J.; Pelz, B. Proceedings of the National Academy of Sciences, Vol. 109, Issue 48 https://doi.org/10.1073/pnas.1211274109	journal	November 2012
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
Human β-Filamin Is a New Protein That Interacts with the Cytoplasmic Tail of Glycoprotein Ibα Takafuta, Toshiro; Wu, Guoxin; Murphy, George F. Journal of Biological Chemistry, Vol. 273, Issue 28 https://doi.org/10.1074/jbc.273.28.17531	journal	July 1998
Structure of three tandem filamin domains reveals auto-inhibition of ligand binding Lad, Yatish; Kiema, Tiila; Jiang, Pengju The EMBO Journal, Vol. 26, Issue 17 https://doi.org/10.1038/sj.emboj.7601827	journal	August 2007
ATSAS 2.1 – towards automated and web-supported small-angle scattering data analysis Petoukhov, Maxim V.; Konarev, Peter V.; Kikhney, Alexey G. Journal of Applied Crystallography, Vol. 40, Issue s1 https://doi.org/10.1107/S0021889807002853	journal	April 2007
Computational Methodologies for Real-Space Structural Refinement of Large Macromolecular Complexes Goh, Boon Chong; Hadden, Jodi A.; Bernardi, Rafael C. Annual Review of Biophysics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-biophys-062215-011113	journal	July 2016
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
The filamins: Organizers of cell structure and function Nakamura, Fumihiko; Stossel, Thomas P.; Hartwig, John H. Cell Adhesion & Migration, Vol. 5, Issue 2 https://doi.org/10.4161/cam.5.2.14401	journal	March 2011
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
BODIL: a molecular modeling environment for structure-function analysis and drug design Lehtonen, Jukka V.; Still, Dan-Johan; Rantanen, Ville-v. Journal of Computer-Aided Molecular Design, Vol. 18, Issue 6 https://doi.org/10.1007/s10822-004-3752-4	journal	June 2004
Dynamical behaviour of the human β ₁ -adrenoceptor under agonist binding Hoelz, Lucas V. B.; Bernardi, Rafael C.; Horta, Bruno A. C. Molecular Simulation, Vol. 37, Issue 11 https://doi.org/10.1080/08927022.2011.572167	journal	September 2011
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Determination of Domain Structure of Proteins from X-Ray Solution Scattering Svergun, Dmitri I.; Petoukhov, Maxim V.; Koch, Michel H. J. Biophysical Journal, Vol. 80, Issue 6 https://doi.org/10.1016/S0006-3495(01)76260-1	journal	June 2001
Stretchy Proteins on Stretchy Substrates: The Important Elements of Integrin-Mediated Rigidity Sensing Moore, Simon W.; Roca-Cusachs, Pere; Sheetz, Michael P. Developmental Cell, Vol. 19, Issue 2 https://doi.org/10.1016/j.devcel.2010.07.018	journal	August 2010
Local force and geometry sensing regulate cell functions Vogel, Viola; Sheetz, Michael Nature Reviews Molecular Cell Biology, Vol. 7, Issue 4 https://doi.org/10.1038/nrm1890	journal	February 2006
Titin-based mechanical signalling in normal and failing myocardium Krüger, Martina; Linke, Wolfgang A. Journal of Molecular and Cellular Cardiology, Vol. 46, Issue 4 https://doi.org/10.1016/j.yjmcc.2009.01.004	journal	April 2009
A Structural Basis for Sequence Comparisons Johnson, Mark S.; Overington, John P. Journal of Molecular Biology, Vol. 233, Issue 4 https://doi.org/10.1006/jmbi.1993.1548	journal	October 1993
Dynamic molecular processes mediate cellular mechanotransduction Hoffman, Brenton D.; Grashoff, Carsten; Schwartz, Martin A. Nature, Vol. 475, Issue 7356 https://doi.org/10.1038/nature10316	journal	July 2011
Otopalatodigital syndrome spectrum disorders: otopalatodigital syndrome types 1 and 2, frontometaphyseal dysplasia and Melnick-Needles syndrome Robertson, Stephen P. European Journal of Human Genetics, Vol. 15, Issue 1 https://doi.org/10.1038/sj.ejhg.5201654	journal	August 2006
A molecular and clinical study of Larsen syndrome caused by mutations in FLNB Bicknell, L. S.; Farrington-Rock, C.; Shafeghati, Y. Journal of Medical Genetics, Vol. 44, Issue 2 https://doi.org/10.1136/jmg.2006.043687	journal	August 2006
Cellular mechanotransduction: putting all the pieces together again Ingber, Donald E. The FASEB Journal, Vol. 20, Issue 7 https://doi.org/10.1096/fj.05-5424rev	journal	May 2006
Frontometaphyseal dysplasia: Mutations inFLNA and phenotypic diversity Robertson, Stephen P.; Jenkins, Zandra A.; Morgan, Timothy American Journal of Medical Genetics Part A, Vol. 140A, Issue 16 https://doi.org/10.1002/ajmg.a.31322	journal	January 2006
Identification of the Region in Actin-binding Protein that Binds to the Cytoplasmic Domain of Glycoprotein Ib _α Meyer, Sylvie C.; Zuerbig, Susanne; Cunningham, Casey C. Journal of Biological Chemistry, Vol. 272, Issue 5 https://doi.org/10.1074/jbc.272.5.2914	journal	January 1997
NMRFAM-SPARKY: enhanced software for biomolecular NMR spectroscopy Lee, Woonghee; Tonelli, Marco; Markley, John L. Bioinformatics, Vol. 31, Issue 8 https://doi.org/10.1093/bioinformatics/btu830	journal	December 2014
Localized mutations in the gene encoding the cytoskeletal protein filamin A cause diverse malformations in humans Robertson, Stephen P.; Twigg, Stephen R. F.; Sutherland-Smith, Andrew J. Nature Genetics, Vol. 33, Issue 4 https://doi.org/10.1038/ng1119	journal	March 2003
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Mechanical strain in actin networks regulates FilGAP and integrin binding to filamin A Ehrlicher, A. J.; Nakamura, F.; Hartwig, J. H. Nature, Vol. 478, Issue 7368 https://doi.org/10.1038/nature10430	journal	September 2011
Filamins in Mechanosensing and Signaling Razinia, Ziba; Mäkelä, Toni; Ylänne, Jari Annual Review of Biophysics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-biophys-050511-102252	journal	June 2012
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone ϕ, ψ and Side-Chain χ ₁ and χ ₂ Dihedral Angles Best, Robert B.; Zhu, Xiao; Shim, Jihyun Journal of Chemical Theory and Computation, Vol. 8, Issue 9 https://doi.org/10.1021/ct300400x	journal	August 2012
Filamins in cell signaling, transcription and organ development Zhou, Alex-Xianghua; Hartwig, John H.; Akyürek, Levent M. Trends in Cell Biology, Vol. 20, Issue 2 https://doi.org/10.1016/j.tcb.2009.12.001	journal	February 2010
Restoring Low Resolution Structure of Biological Macromolecules from Solution Scattering Using Simulated Annealing Svergun, D. I. Biophysical Journal, Vol. 76, Issue 6, p. 2879-2886 https://doi.org/10.1016/S0006-3495(99)77443-6	journal	June 1999
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
Mapping Mechanical Force Propagation through Biomolecular Complexes Schoeler, Constantin; Bernardi, Rafael C.; Malinowska, Klara H. Nano Letters, Vol. 15, Issue 11 https://doi.org/10.1021/acs.nanolett.5b02727	journal	August 2015
Molecular dynamics simulations of large macromolecular complexes Perilla, Juan R.; Goh, Boon Chong; Cassidy, C. Keith Current Opinion in Structural Biology, Vol. 31 https://doi.org/10.1016/j.sbi.2015.03.007	journal	April 2015
Tissue Cells Feel and Respond to the Stiffness of Their Substrate Discher, D. E.; Janmey, Paul; Wang, Yu-li Science, Vol. 310, Issue 5751, p. 1139-1143 https://doi.org/10.1126/science.1116995	journal	November 2005
Cell and molecular mechanics of biological materials Bao, G.; Suresh, S. Nature Materials, Vol. 2, Issue 11 https://doi.org/10.1038/nmat1001	journal	November 2003
Automated matching of high- and low-resolution structural models Kozin, M. B.; Svergun, D. I. Journal of Applied Crystallography, Vol. 34, Issue 1, p. 33-41 https://doi.org/10.1107/S0021889800014126	journal	February 2001
QwikMD — Integrative Molecular Dynamics Toolkit for Novices and Experts Ribeiro, João V.; Bernardi, Rafael C.; Rudack, Till Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep26536	journal	May 2016
The structure of the GPIb–filamin A complex Nakamura, Fumihiko; Pudas, Regina; Heikkinen, Outi Blood, Vol. 107, Issue 5 https://doi.org/10.1182/blood-2005-10-3964	journal	March 2006
Skeletal dysplasias due to filamin A mutations result from a gain-of-function mechanism distinct from allelic neurological disorders† Clark, Alice R.; Sawyer, Gregory M.; Robertson, Stephen P. Human Molecular Genetics, Vol. 18, Issue 24 https://doi.org/10.1093/hmg/ddp442	journal	September 2009
ALSCRIPT: a tool to format multiple sequence alignments Barton, Geoffrey J. "Protein Engineering, Design and Selection", Vol. 6, Issue 1 https://doi.org/10.1093/protein/6.1.37	journal	January 1993
The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability Niesen, Frank H.; Berglund, Helena; Vedadi, Masoud Nature Protocols, Vol. 2, Issue 9 https://doi.org/10.1038/nprot.2007.321	journal	September 2007
Structural basis of filamin A functions Nakamura, Fumihiko; Osborn, Teresia M.; Hartemink, Christopher A. The Journal of Cell Biology, Vol. 179, Issue 5 https://doi.org/10.1083/jcb.200707073	journal	December 2007
Identification and Characterization of Multiple Similar Ligand-binding Repeats in Filamin: IMPLICATION ON FILAMIN-MEDIATED RECEPTOR CLUSTERING AND CROSS-TALK Ithychanda, Sujay Subbayya; Hsu, Dennis; Li, Hanhan Journal of Biological Chemistry, Vol. 284, Issue 50 https://doi.org/10.1074/jbc.M109.060954	journal	October 2009
Dynamical networks in tRNA:protein complexes Sethi, A.; Eargle, J.; Black, A. A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 16 https://doi.org/10.1073/pnas.0810961106	journal	April 2009
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S. Nature Protocols, Vol. 3, Issue 7 https://doi.org/10.1038/nprot.2008.91	journal	June 2008
Stretching Single Talin Rod Molecules Activates Vinculin Binding del Rio, A.; Perez-Jimenez, R.; Liu, R. Science, Vol. 323, Issue 5914 https://doi.org/10.1126/science.1162912	journal	January 2009
Small GTPases in mechanosensitive regulation of endothelial barrier Birukov, Konstantin G. Microvascular Research, Vol. 77, Issue 1 https://doi.org/10.1016/j.mvr.2008.09.006	journal	January 2009
The fundamental role of mechanical properties in the progression of cancer disease and inflammation Mierke, Claudia Tanja Reports on Progress in Physics, Vol. 77, Issue 7 https://doi.org/10.1088/0034-4885/77/7/076602	journal	July 2014
Disease-associated mutations in the actin-binding domain of filamin B cause cytoplasmic focal accumulations correlating with disease severity Daniel, Philip B.; Morgan, Tim; Alanay, Yasemin Human Mutation, Vol. 33, Issue 4 https://doi.org/10.1002/humu.22012	journal	January 2012
UniProt: a hub for protein information Consortium, UniPot Nucleic Acids Research, Vol. 43, Issue D1, p. D204-D212 https://doi.org/10.1093/nar/gku989	journal	October 2014
Ultrastable cellulosome-adhesion complex tightens under load Schoeler, Constantin; Malinowska, Klara H.; Bernardi, Rafael C. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6635	journal	December 2014
The Regulation Mechanism for the Auto-Inhibition of Binding of Human Filamin A to Integrin Pentikäinen, Ulla; Ylänne, Jari Journal of Molecular Biology, Vol. 393, Issue 3 https://doi.org/10.1016/j.jmb.2009.08.035	journal	October 2009
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/S2052252514009324	journal	May 2014
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
The effect of acidic pH on the adsorption and lytic activity of the peptides Polybia-MP1 and its histidine-containing analog in anionic lipid membrane: a biophysical study by molecular dynamics and spectroscopy Martins, Ingrid Bernardes Santana; Viegas, Taisa Giordano; dos Santos Alvares, Dayane Amino Acids, Vol. 53, Issue 5 https://doi.org/10.1007/s00726-021-02982-0	journal	April 2021
Structural insights into the mechanical regulation of molecular recognition sites Vogel, Viola; Thomas, Wendy E.; Craig, David W. Trends in Biotechnology, Vol. 19, Issue 10 https://doi.org/10.1016/s0167-7799(01)01737-1	journal	October 2001
Structure of the G protein chaperone and guanine nucleotide exchange factor Ric-8A bound to Gαi1 McClelland, Levi J.; Zhang, Kaiming; Mou, Tung-Chung Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14943-4	journal	February 2020
Stepwise gating of the Sec61 protein-conducting channel by Sec63 and Sec62 Itskanov, Samuel; Kuo, Katie M.; Gumbart, James C. Nature Structural & Molecular Biology, Vol. 28, Issue 2 https://doi.org/10.1038/s41594-020-00541-x	journal	January 2021
The C-terminal rod 2 fragment of filamin A forms a compact structure that can be extended Ruskamo, Salla; Gilbert, Robert; Hofmann, Gregor Biochemical Journal, Vol. 446, Issue 2 https://doi.org/10.1042/bj20120361	journal	August 2012
Atomic Structures of Two Novel Immunoglobulin-like Domain Pairs in the Actin Cross-linking Protein Filamin Heikkinen, Outi K.; Ruskamo, Salla; Konarev, Peter V. Journal of Biological Chemistry, Vol. 284, Issue 37 https://doi.org/10.1074/jbc.m109.019661	journal	July 2009
A Novel Structural Unit in the N-terminal Region of Filamins Sethi, Ritika; Seppälä, Jonne; Tossavainen, Helena Journal of Biological Chemistry, Vol. 289, Issue 12 https://doi.org/10.1074/jbc.m113.537456	journal	January 2014
FOXC1 Transcriptional Regulatory Activity Is Impaired by PBX1 in a Filamin A-Mediated Manner Berry, F. B.; O'Neill, M. A.; Coca-Prados, M. Molecular and Cellular Biology, Vol. 25, Issue 4 https://doi.org/10.1128/mcb.25.4.1415-1424.2005	journal	January 2005
Community structure in social and biological networks Girvan, Michelle; Newman, M. E. J. arXiv https://doi.org/10.48550/arxiv.cond-mat/0112110	text	January 2001

Cited By (3)

A comprehensive analysis of the allergenicity and IgE epitopes of myosinogen allergens in Scylla paramamosain Yang, Yang; Hu, Meng Jun; Jin, Teng Chuan Clinical & Experimental Allergy, Vol. 49, Issue 1 https://doi.org/10.1111/cea.13266	journal	October 2018
The filamin-B–refilin axis – spatiotemporal regulators of the actin-cytoskeleton in development and disease Baudier, Jacques; Jenkins, Zandra A.; Robertson, Stephen P. Journal of Cell Science, Vol. 131, Issue 8 https://doi.org/10.1242/jcs.213959	journal	April 2018
Mechanisms of Nanonewton Mechanostability in a Protein Complex Revealed by Molecular Dynamics Simulations and Single-Molecule Force Spectroscopy C., Bernardi, Rafael; Ellis, Durner,; Constantin, Schoeler, American Chemical Society https://doi.org/10.5451/unibas-ep72178	text	January 2019