Molecular Paradigms for Biological Mechanosensing

Gomez, David; Peña Ccoa, Willmor J.; Singh, Yuvraj; Rojas, Enrique; Hocky, Glen M.

doi:10.1021/acs.jpcb.1c06330

Molecular Paradigms for Biological Mechanosensing

Journal Article · 28 October 2021 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.1c06330· OSTI ID:1977977

Gomez, David ^[1]; Peña Ccoa, Willmor J. ^[2]; ^[2]; Rojas, Enrique ^[3]; ^[2]

Department of Biology, New York University, New York, New York 10003, United States; Department of Chemistry, New York University, New York, New York 10003, United States
Department of Chemistry, New York University, New York, New York 10003, United States
Department of Biology, New York University, New York, New York 10003, United States

Not provided.

Research Organization:: Parallel Works, Inc., Chicago, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0019695

OSTI ID:: 1977977

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Vol. 125, Issue 44; ISSN 1520-6106

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

References (75)

Physical Biology of the Cell Phillips, Rob; Kondev, Jane; Theriot, Julie https://doi.org/10.1201/9781134111589	book	October 2012
Probing the Stochastic, Motor-Driven Properties of the Cytoplasm Using Force Spectrum Microscopy Guo, Ming; Ehrlicher, Allen J.; Jensen, Mikkel H. Cell, Vol. 158, Issue 4 https://doi.org/10.1016/j.cell.2014.06.051	journal	August 2014
Coarse-Grained Directed Simulation Hocky, Glen M.; Dannenhoffer-Lafage, Thomas; Voth, Gregory A. Journal of Chemical Theory and Computation, Vol. 13, Issue 9 https://doi.org/10.1021/acs.jctc.7b00690	journal	August 2017
Models for the specific adhesion of cells to cells Bell, G. Science, Vol. 200, Issue 4342 https://doi.org/10.1126/science.347575	journal	May 1978
Theory, analysis, and interpretation of single-molecule force spectroscopy experiments Dudko, O. K.; Hummer, G.; Szabo, A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 41 https://doi.org/10.1073/pnas.0806085105	journal	October 2008
Chemical reactions modulated by mechanical stress: Extended Bell theory Konda, Sai Sriharsha M.; Brantley, Johnathan N.; Bielawski, Christopher W. The Journal of Chemical Physics, Vol. 135, Issue 16 https://doi.org/10.1063/1.3656367	journal	October 2011
Perspective: Mechanochemistry of biological and synthetic molecules Makarov, Dmitrii E. The Journal of Chemical Physics, Vol. 144, Issue 3 https://doi.org/10.1063/1.4939791	journal	January 2016
Allostery in Its Many Disguises: From Theory to Applications Wodak, Shoshana J.; Paci, Emanuele; Dokholyan, Nikolay V. Structure, Vol. 27, Issue 4 https://doi.org/10.1016/j.str.2019.01.003	journal	April 2019
FimH Forms Catch Bonds That Are Enhanced by Mechanical Force Due to Allosteric Regulation Yakovenko, Olga; Sharma, Shivani; Forero, Manu Journal of Biological Chemistry, Vol. 283, Issue 17 https://doi.org/10.1074/jbc.M707815200	journal	April 2008
Designing allostery-inspired response in mechanical networks Rocks, Jason W.; Pashine, Nidhi; Bischofberger, Irmgard Proceedings of the National Academy of Sciences, Vol. 114, Issue 10 https://doi.org/10.1073/pnas.1612139114	journal	February 2017
Mechanics of Allostery: Contrasting the Induced Fit and Population Shift Scenarios Ravasio, Riccardo; Flatt, Solange Marie; Yan, Le Biophysical Journal, Vol. 117, Issue 10 https://doi.org/10.1016/j.bpj.2019.10.002	journal	November 2019
Residue-Level Allostery Propagates through the Effective Coarse-Grained Hessian Lake, Peter T.; Davidson, Russell B.; Klem, Heidi Journal of Chemical Theory and Computation, Vol. 16, Issue 5 https://doi.org/10.1021/acs.jctc.9b01149	journal	April 2020
Protein Structural Change Upon Ligand Binding: Linear Response Theory Ikeguchi, Mitsunori; Ueno, Jiro; Sato, Miwa Physical Review Letters, Vol. 94, Issue 7 https://doi.org/10.1103/PhysRevLett.94.078102	journal	February 2005
Quantifying Correlations Between Allosteric Sites in Thermodynamic Ensembles McClendon, Christopher L.; Friedland, Gregory; Mobley, David L. Journal of Chemical Theory and Computation, Vol. 5, Issue 9 https://doi.org/10.1021/ct9001812	journal	August 2009
GPR68 Senses Flow and Is Essential for Vascular Physiology Xu, Jie; Mathur, Jayanti; Vessières, Emilie Cell, Vol. 173, Issue 3 https://doi.org/10.1016/j.cell.2018.03.076	journal	April 2018
Three Weaknesses for Three Perturbations: Comparing Protein Unfolding Under Shear, Force, and Thermal Stresses Languin-Cattoën, Olivier; Melchionna, Simone; Derreumaux, Philippe The Journal of Physical Chemistry B, Vol. 122, Issue 50 https://doi.org/10.1021/acs.jpcb.8b08711	journal	November 2018
Stretch-activated single ion channel currents in tissue-cultured embryonic chick skeletal muscle. Guharay, F.; Sachs, F. The Journal of Physiology, Vol. 352, Issue 1 https://doi.org/10.1113/jphysiol.1984.sp015317	journal	July 1984
A large-conductance mechanosensitive channel in E. coli encoded by mscL alone Sukharev, Sergei I.; Blount, Paul; Martinac, Boris Nature, Vol. 368, Issue 6468 https://doi.org/10.1038/368265a0	journal	March 1994
Responses of Bacillus subtilis to Hypotonic Challenges: Physiological Contributions of Mechanosensitive Channels to Cellular Survival Hoffmann, Tamara; Boiangiu, Clara; Moses, Susanne Applied and Environmental Microbiology, Vol. 74, Issue 8 https://doi.org/10.1128/AEM.01573-07	journal	April 2008
Mechanosensitive Channels: What Can They Do and How Do They Do It? Haswell, Elizabeth S.; Phillips, Rob; Rees, Douglas C. Structure, Vol. 19, Issue 10 https://doi.org/10.1016/j.str.2011.09.005	journal	October 2011
Connecting the Dots between Mechanosensitive Channel Abundance, Osmotic Shock, and Survival at Single-Cell Resolution Chure, Griffin; Lee, Heun Jin; Rasmussen, Akiko Journal of Bacteriology, Vol. 200, Issue 23 https://doi.org/10.1128/JB.00460-18	journal	December 2018
Mechanosensitive Closed-Closed Transitions in Large Membrane Proteins: Osmoprotection and Tension Damping Boucher, Pierre-Alexandre; Morris, Catherine E.; Joós, Béla Biophysical Journal, Vol. 97, Issue 10 https://doi.org/10.1016/j.bpj.2009.08.054	journal	November 2009
Homeostatic Cell Growth Is Accomplished Mechanically through Membrane Tension Inhibition of Cell-Wall Synthesis Rojas, Enrique R.; Huang, Kerwyn Casey; Theriot, Julie A. Cell Systems, Vol. 5, Issue 6 https://doi.org/10.1016/j.cels.2017.11.005	journal	December 2017
The Mechanical Properties of Bacteria and Why They Matter Rojas, Enrique R. Advances in Experimental Medicine and Biology https://doi.org/10.1007/978-3-030-46886-6_1	book	January 2020
Differential effects of lipids and lyso-lipids on the mechanosensitivity of the mechanosensitive channels MscL and MscS Nomura, T.; Cranfield, C. G.; Deplazes, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1200051109	journal	May 2012
Pulling MscL open via N-terminal and TM1 helices: A computational study towards engineering an MscL nanovalve Martinac, Adam D.; Bavi, Navid; Bavi, Omid PLOS ONE, Vol. 12, Issue 8 https://doi.org/10.1371/journal.pone.0183822	journal	August 2017
Structural Investigation of MscL Gating Using Experimental Data and Coarse Grained MD Simulations Deplazes, Evelyne; Louhivuori, Martti; Jayatilaka, Dylan PLoS Computational Biology, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pcbi.1002683	journal	September 2012
Mechanical Activation of MscL Revealed by a Locally Distributed Tension Molecular Dynamics Approach Rajeshwar T., Rajitha; Anishkin, Andriy; Sukharev, Sergei Biophysical Journal, Vol. 120, Issue 2 https://doi.org/10.1016/j.bpj.2020.11.2274	journal	January 2021
Protein structure homology modeling using SWISS-MODEL workspace Bordoli, Lorenza; Kiefer, Florian; Arnold, Konstantin Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.197	journal	December 2008
A large iris-like expansion of a mechanosensitive channel protein induced by membrane tension Betanzos, Monica; Chiang, Chien-Sung; Guy, H. Robert Nature Structural Biology, Vol. 9, Issue 9 https://doi.org/10.1038/nsb828	journal	August 2002
MscL: channeling membrane tension Walton, Troy A.; Idigo, Chinenye A.; Herrera, Nadia Pflügers Archiv - European Journal of Physiology, Vol. 467, Issue 1 https://doi.org/10.1007/s00424-014-1535-x	journal	May 2014
The role of lipids in mechanosensation Pliotas, Christos; Dahl, A. Caroline E.; Rasmussen, Tim Nature Structural & Molecular Biology, Vol. 22, Issue 12 https://doi.org/10.1038/nsmb.3120	journal	November 2015
Dynamics of unbinding of cell adhesion molecules: Transition from catch to slip bonds Barsegov, V.; Thirumalai, D. Proceedings of the National Academy of Sciences, Vol. 102, Issue 6 https://doi.org/10.1073/pnas.0406938102	journal	February 2005
Visualization of the mechanosensitive ion channel MscS under membrane tension Zhang, Yixiao; Daday, Csaba; Gu, Ruo-Xu Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-021-03196-w	journal	February 2021
Molecular basis of force-from-lipids gating in the mechanosensitive channel MscS Reddy, Bharat; Bavi, Navid; Lu, Allen eLife, Vol. 8 https://doi.org/10.7554/eLife.50486	journal	December 2019
Interaction of the Mechanosensitive Channel, MscS, with the Membrane Bilayer through Lipid Intercalation into Grooves and Pockets Rasmussen, Tim; Rasmussen, Akiko; Yang, Limin Journal of Molecular Biology, Vol. 431, Issue 17 https://doi.org/10.1016/j.jmb.2019.05.043	journal	August 2019
Mechanosensitive channel YnaI has lipid-bound extended sensor paddles Hu, Wenxin; Wang, Zhiming; Zheng, Hongjin Communications Biology, Vol. 4, Issue 1 https://doi.org/10.1038/s42003-021-02122-0	journal	May 2021
Single-Cell Census of Mechanosensitive Channels in Living Bacteria Bialecka-Fornal, Maja; Lee, Heun Jin; DeBerg, Hannah A. PLoS ONE, Vol. 7, Issue 3 https://doi.org/10.1371/journal.pone.0033077	journal	March 2012
Dynamic Clustering Regulates Activity of Mechanosensitive Membrane Channels Paraschiv, Alexandru; Hegde, Smitha; Ganti, Raman Physical Review Letters, Vol. 124, Issue 4 https://doi.org/10.1103/PhysRevLett.124.048102	journal	January 2020
Force Triggers YAP Nuclear Entry by Regulating Transport across Nuclear Pores Elosegui-Artola, Alberto; Andreu, Ion; Beedle, Amy E. M. Cell, Vol. 171, Issue 6 https://doi.org/10.1016/j.cell.2017.10.008	journal	November 2017
Mechanoregulated inhibition of formin facilitates contractile actomyosin ring assembly Zimmermann, Dennis; Homa, Kaitlin E.; Hocky, Glen M. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-00445-3	journal	September 2017
The Piconewton Force Awakens: Quantifying Mechanics in Cells Freikamp, Andrea; Cost, Anna-Lena; Grashoff, Carsten Trends in Cell Biology, Vol. 26, Issue 11 https://doi.org/10.1016/j.tcb.2016.07.005	journal	November 2016
Spider Silk Peptide Is a Compact, Linear Nanospring Ideal for Intracellular Tension Sensing Brenner, Michael D.; Zhou, Ruobo; Conway, Daniel E. Nano Letters, Vol. 16, Issue 3 https://doi.org/10.1021/acs.nanolett.6b00305	journal	February 2016
Molecular Force Measurement with Tension Sensors Fischer, Lisa S.; Rangarajan, Srishti; Sadhanasatish, Tanmay Annual Review of Biophysics, Vol. 50, Issue 1 https://doi.org/10.1146/annurev-biophys-101920-064756	journal	May 2021
Elasticity, structure, and relaxation of extended proteins under force Stirnemann, G.; Giganti, D.; Fernandez, J. M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 10 https://doi.org/10.1073/pnas.1300596110	journal	February 2013
Extracellular rigidity sensing by talin isoform-specific mechanical linkages Austen, Katharina; Ringer, Pia; Mehlich, Alexander Nature Cell Biology, Vol. 17, Issue 12 https://doi.org/10.1038/ncb3268	journal	November 2015
Sub-microsecond Protein Folding Kubelka, Jan; Chiu, Thang K.; Davies, David R. Journal of Molecular Biology, Vol. 359, Issue 3 https://doi.org/10.1016/j.jmb.2006.03.034	journal	June 2006
Promoting transparency and reproducibility in enhanced molecular simulations No authors listed Nature Methods, Vol. 16, Issue 8, p. 670-673 https://doi.org/10.1038/s41592-019-0506-8	journal	July 2019
The Two-Pathway Model of the Biological Catch-Bond as a Limit of the Allosteric Model Pereverzev, Yuriy V.; Prezhdo, Eugenia; Sokurenko, Evgeni V. Biophysical Journal, Vol. 101, Issue 8 https://doi.org/10.1016/j.bpj.2011.09.005	journal	October 2011
Catch-Bond Mechanism of Force-Enhanced Adhesion: Counterintuitive, Elusive, but … Widespread? Sokurenko, Evgeni V.; Vogel, Viola; Thomas, Wendy E. Cell Host & Microbe, Vol. 4, Issue 4 https://doi.org/10.1016/j.chom.2008.09.005	journal	October 2008
Biophysics of Catch Bonds Thomas, Wendy E.; Vogel, Viola; Sokurenko, Evgeni Annual Review of Biophysics, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.biophys.37.032807.125804	journal	June 2008
Theoretical Aspects of the Biological Catch Bond Prezhdo, Oleg V.; Pereverzev, Yuriy V. Accounts of Chemical Research, Vol. 42, Issue 6 https://doi.org/10.1021/ar800202z	journal	June 2009
Catch-bond mechanism of the bacterial adhesin FimH Sauer, Maximilian M.; Jakob, Roman P.; Eras, Jonathan Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10738	journal	March 2016
Vinculin forms a directionally asymmetric catch bond with F-actin Huang, Derek L.; Bax, Nicolas A.; Buckley, Craig D. Science, Vol. 357, Issue 6352 https://doi.org/10.1126/science.aan2556	journal	August 2017
Molecular mechanism for direct actin force-sensing by α-catenin Mei, Lin; Espinosa de los Reyes, Santiago; Reynolds, Matthew J. eLife, Vol. 9 https://doi.org/10.7554/eLife.62514	journal	September 2020
Structural basis of αE-catenin–F-actin catch bond behavior Xu, Xiao-Ping; Pokutta, Sabine; Torres, Megan eLife, Vol. 9 https://doi.org/10.7554/eLife.60878	journal	September 2020
Direct observation of catch bonds involving cell-adhesion molecules Marshall, Bryan T.; Long, Mian; Piper, James W. Nature, Vol. 423, Issue 6936 https://doi.org/10.1038/nature01605	journal	May 2003
Regulatory element in fibrin triggers tension-activated transition from catch to slip bonds Litvinov, Rustem I.; Kononova, Olga; Zhmurov, Artem Proceedings of the National Academy of Sciences, Vol. 115, Issue 34 https://doi.org/10.1073/pnas.1802576115	journal	August 2018
Catch Bonds in Adhesion Thomas, Wendy Annual Review of Biomedical Engineering, Vol. 10, Issue 1 https://doi.org/10.1146/annurev.bioeng.10.061807.160427	journal	August 2008
Structural Basis for Mechanical Force Regulation of the Adhesin FimH via Finger Trap-like β Sheet Twisting Le Trong, Isolde; Aprikian, Pavel; Kidd, Brian A. Cell, Vol. 141, Issue 4 https://doi.org/10.1016/j.cell.2010.03.038	journal	May 2010
Biomolecular modeling thrives in the age of technology Schlick, Tamar; Portillo-Ledesma, Stephanie Nature Computational Science, Vol. 1, Issue 5 https://doi.org/10.1038/s43588-021-00060-9	journal	May 2021
Steered molecular dynamics and mechanical functions of proteins Isralewitz, Barry; Gao, Mu; Schulten, Klaus Current Opinion in Structural Biology, Vol. 11, Issue 2 https://doi.org/10.1016/S0959-440X(00)00194-9	journal	April 2001
Flyby reaction trajectories: Chemical dynamics under extrinsic force Liu, Yun; Holm, Soren; Meisner, Jan Science, Vol. 373, Issue 6551 https://doi.org/10.1126/science.abi7609	journal	July 2021
Free Energy Surfaces from Single-Molecule Force Spectroscopy Hummer, Gerhard; Szabo, Attila Accounts of Chemical Research, Vol. 38, Issue 7 https://doi.org/10.1021/ar040148d	journal	July 2005
A Review of Enhanced Sampling Approaches for Accelerated Molecular Dynamics Tiwary, Pratyush; van de Walle, Axel Multiscale Materials Modeling for Nanomechanics https://doi.org/10.1007/978-3-319-33480-6_6	book	January 2016
Infinite switch simulated tempering in force (FISST) Hartmann, Michael J.; Singh, Yuvraj; Vanden-Eijnden, Eric The Journal of Chemical Physics, Vol. 152, Issue 24 https://doi.org/10.1063/5.0009280	journal	June 2020
A method for accelerating the molecular dynamics simulation of infrequent events Voter, Arthur F. The Journal of Chemical Physics, Vol. 106, Issue 11 https://doi.org/10.1063/1.473503	journal	March 1997
Hyperdynamics: Accelerated Molecular Dynamics of Infrequent Events Voter, Arthur F. Physical Review Letters, Vol. 78, Issue 20 https://doi.org/10.1103/PhysRevLett.78.3908	journal	May 1997
WExplore: Hierarchical Exploration of High-Dimensional Spaces Using the Weighted Ensemble Algorithm Dickson, Alex; Brooks, Charles L. The Journal of Physical Chemistry B, Vol. 118, Issue 13 https://doi.org/10.1021/jp411479c	journal	February 2014
Wepy: A Flexible Software Framework for Simulating Rare Events with Weighted Ensemble Resampling Lotz, Samuel D.; Dickson, Alex ACS Omega, Vol. 5, Issue 49 https://doi.org/10.1021/acsomega.0c03892	journal	December 2020
Actin Filament Strain Promotes Severing and Cofilin Dissociation Schramm, Anthony C.; Hocky, Glen M.; Voth, Gregory A. Biophysical Journal, Vol. 112, Issue 12 https://doi.org/10.1016/j.bpj.2017.05.016	journal	June 2017
Mechanical and kinetic factors drive sorting of F-actin cross-linkers on bundles Freedman, Simon L.; Suarez, Cristian; Winkelman, Jonathan D. Proceedings of the National Academy of Sciences, Vol. 116, Issue 33 https://doi.org/10.1073/pnas.1820814116	journal	July 2019
Mechanically tuning actin filaments to modulate the action of actin-binding proteins Jégou, Antoine; Romet-Lemonne, Guillaume Current Opinion in Cell Biology, Vol. 68 https://doi.org/10.1016/j.ceb.2020.09.002	journal	February 2021
Evolutionarily diverse LIM domain-containing proteins bind stressed actin filaments through a conserved mechanism Winkelman, Jonathan D.; Anderson, Caitlin A.; Suarez, Cristian Proceedings of the National Academy of Sciences, Vol. 117, Issue 41 https://doi.org/10.1073/pnas.2004656117	journal	September 2020
Mechanosensing through Direct Binding of Tensed F-Actin by LIM Domains Sun, Xiaoyu; Phua, Donovan Y. Z.; Axiotakis, Lucas Developmental Cell, Vol. 55, Issue 4 https://doi.org/10.1016/j.devcel.2020.09.022	journal	November 2020

Similar Records

Towards a more healthy conservation paradigm: integrating disease and molecular ecology to aid biological conservation†

Journal Article · 2020 · Journal of Genetics · OSTI ID:1799575

Gupta, Pooja; Robin, V. V.; Dharmarajan, Guha

Interfacial Reactivity of Radionuclides: Emerging Paradigms from Molecular Level Observations

Journal Article · 2011 · Mineralogical Magazine · OSTI ID:1029044

Felmy, Andrew R; Ilton, Eugene S; Rosso, Kevin M; +1 more

A new paradigm for the molecular basis of rubber elasticity

Journal Article · 2015 · Contemporary Physics · OSTI ID:1239115

Hanson, David E.; Barber, John L.

Related Subjects

Chemistry

Molecular Paradigms for Biological Mechanosensing

Citation Formats

References (75)

Similar Records

Related Subjects