[en] Recent literature provides increasing samples of structural studies relying on ion mobility coupled to mass spectrometry in view of characterizing gas-phase conformation and energetics properties of biomolecular ions. A typical framework consists in experimentally monitoring the collisional cross sections for various experimental conditions and using them as references to select appropriate candidate structures issued from theoretical modeling. Although it has proved successful for structural assignment, this process is resource costly and lengthy, namely due to intricacies in the selection of appropriate input geometries. In the present work, we propose simplified methodologies dedicated to the systematic screening of ion mobility data acquired on systems built from repetitive subunits and detail their application to challenging artificial molecular switch systems. Capitalizing on coarse-grained design, we first demonstrate how the assimilation of subunits into adequately assembled building-blocks can be used for fast assignments of a system topology. Further focusing on topology-specific differential ion mobility trends, we show that the building-block assemblies can be fused into single fully convex solid figure models, i.e., sphere and cylinder, whose projected areas follow a two-parameter power formalism A × nB. We show that the fitting parameters A and B were assigned as structural descriptors respectively associated with the dimensions of each constitutive subunit, i.e., size parameter, and with their assembled tridimensional arrangement, i.e., shape parameter. The present work provides a ready-to-use method for the screening of IM-MS data sets that is expected to facilitate the eventual design of input structures whenever advanced modeling calculations are required.
Disciplines :
Chemistry
Author, co-author :
Hanozin, Emeline ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)
Morsa, Denis ; Université de Liège - ULiège > Département de chimie (sciences) > Laboratoire de spectrométrie de masse (L.S.M.)
De Pauw, Edwin ; Université de Liège - ULiège > Département de chimie (sciences) > Chimie analytique inorganique
Language :
English
Title :
Two-Parameter Power Formalism for Structural Screening of Ion Mobility Trends: Applied Study on Artificial Molecular Switches
Publication date :
September 2019
Journal title :
Journal of Physical Chemistry. A
ISSN :
1089-5639
eISSN :
1520-5215
Publisher :
American Chemical Society, Washington, United States - District of Columbia
Cheng, C.; McGonigal, P. R.; Stoddart, J. F.; Astumian, R. D. Design and Synthesis of Nonequilibrium Systems. ACS Nano 2015, 9, 8672-8688, 10.1021/acsnano.5b03809
McCreery, R. L. Molecular Electronic Junctions. Chem. Mater. 2004, 16, 4477-4496, 10.1021/cm049517q
Collin, J.-P.; Dietrich-Buchecker, C.; Gaviña, P.; Jimenez-Molero, M. C.; Sauvage, J. P. Shuttles and Muscles: Linear Molecular Machines Based on Transition Metals. Acc. Chem. Res. 2001, 34, 477-487, 10.1021/ar0001766
Basu, S.; Coskun, A.; Friedman, D. C.; Olson, M. A.; Benitez, D.; Tkatchouk, E.; Barin, G.; Yang, J.; Fahrenbach, A. C.; Goddard, W. A., III; Stoddart, J. F. Donor-Acceptor Oligorotaxanes Made to Order. Chem.-Eur. J. 2011, 17, 2107-2119, 10.1002/chem.201001822
Zhu, Z.; Bruns, C. J.; Li, H.; Lei, J.; Ke, C.; Liu, Z.; Shafaie, S.; Colquhoun, H. M.; Stoddart, J. F. Synthesis and Solution-State Dynamics of Donor-Acceptor Oligorotaxane Foldamers. Chem. Sci. 2013, 4, 1470-1483, 10.1039/c3sc00015j
Wang, Y.; Frasconi, M.; Liu, W.-G.; Sun, J.; Wu, Y.; Nassar, M. S.; Botros, Y. Y.; Goddard, W. A., III; Wasielewski, M. R.; Stoddart, J. F. Oligorotaxane Radicals under Orders. ACS Cent. Sci. 2016, 2, 89-98, 10.1021/acscentsci.5b00377
Scarff, C. A.; Snelling, J. R.; Knust, M. M.; Wilkins, C. L.; Scrivens, J. H. New Structural Insights into Mechanically Interlocked Polymers Revealed by Ion Mobility Mass Spectrometry. J. Am. Chem. Soc. 2012, 134, 9193-9198, 10.1021/ja2118656
Belowich, M. E.; Valente, C.; Smaldone, R. A.; Friedman, D. C.; Thiel, J.; Cronin, L.; Stoddart, J. F. Positive Cooperativity in the Template-Directed Synthesis of Monodisperse Macromolecules. J. Am. Chem. Soc. 2012, 134, 5243-5261, 10.1021/ja2107564
Hanozin, E.; Mignolet, B.; Morsa, D.; Sluysmans, D.; Duwez, A.-S.; Stoddart, J. F.; Remacle, F.; De Pauw, E. Where Ion Mobility and Molecular Dynamics Meet to Unravel the (Un)Folding Mechanisms of an Oligorotaxane Molecular Switch. ACS Nano 2017, 11, 10253-10263, 10.1021/acsnano.7b04833
Schröder, H. V.; Mekic, A.; Hupatz, H.; Sobottka, S.; Witte, F.; Urner, L. H.; Gaedke, M.; Pagel, K.; Sarkar, B.; Paulus, B.; Schalley, C. A. Switchable Synchronisation of Pirouetting Motions in a Redox-Active [3]Rotaxane. Nanoscale 2018, 10, 21425-21433, 10.1039/C8NR05534C
Kanu, A. B.; Dwivedi, P.; Tam, M.; Matz, L.; Hill, H. H. J. Ion Mobility-Mass Spectrometry. J. Mass Spectrom. 2008, 43, 1-22, 10.1002/jms.1383
Bush, M. F.; Hall, Z.; Giles, K.; Hoyes, J.; Robinson, C. V.; Ruotolo, B. T. Collision Cross Sections of Proteins and Their Complexes: A Calibration Framework and Database for Gas-Phase Structural Biology. Anal. Chem. 2010, 82, 9557-9565, 10.1021/ac1022953
López, A.; Tarragó, T.; Vilaseca, M.; Giralt, E. Applications and Future of Ion Mobility Mass Spectrometry in Structural Biology. New J. Chem. 2013, 37, 1283, 10.1039/c3nj41051j
Shvartsburg, A. A. Differential Ion Mobility Spectrometry: Nonlinear Ion Transport and Fundamentals of FAIMS; CRC Press.; Boca Raton, FL, 2008.
Ruotolo, B. T.; Benesch, J. L. P.; Sandercock, A. M.; Hyung, S.-J.; Robinson, C. V. Ion Mobility-Mass Spectrometry Analysis of Large Protein Complexes. Nat. Protoc. 2008, 3, 1139-1152, 10.1038/nprot.2008.78
Cramer, C. J. Essential of Computational Chemistry: Theories and Models; Wiley: New York, 2004.
Benitez, D.; Tkatchouk, E.; Yoon, I.; Stoddart, J. F.; Goddard, W. A. Experimentally-Based Recommendations of Density Functionals for Predicting Properties in Mechanically Interlocked Molecules. J. Am. Chem. Soc. 2008, 130, 14928-14929, 10.1021/ja805953u
Riniker, S.; Allison, J. R.; van Gunsteren, W. F. On Developing Coarse-Grained Models for Biomolecular Simulation: A Review. Phys. Chem. Chem. Phys. 2012, 14, 12423-12430, 10.1039/c2cp40934h
Shvartsburg, A. A.; Jarrold, M. F. An Exact Hard-Spheres Scattering Model for the Mobilities of Polyatomic Ions. Chem. Phys. Lett. 1996, 261, 86-91, 10.1016/0009-2614(96)00941-4
Wyttenbach, T.; von Helden, G.; Batka, J. J.; Carlat, D.; Bowers, M. T. Effect of the Long-Range Potential on Ion Mobility Measurements. J. Am. Soc. Mass Spectrom. 1997, 8, 275-282, 10.1016/S1044-0305(96)00236-X
Wyttenbach, T.; Bleiholder, C.; Bowers, M. T. Factors Contributing to the Collision Cross Section of Polyatomic Ions in the Kilodalton to Gigadalton Range: Application to Ion Mobility Measurements. Anal. Chem. 2013, 85, 2191-2199, 10.1021/ac3029008
von Helden, G.; Gotts, N. G.; Maitre, P.; Bowers, M. T. The Structures of Small Iron-Carbon Cluster Anions. Linear to Planar to Three-Dimensional. Chem. Phys. Lett. 1994, 227, 601-608, 10.1016/0009-2614(94)00871-X
Bowers, M. T. Cluster Ions: Carbon, Met-Cars, and Sigma-Bond Activation. Acc. Chem. Res. 1994, 27, 324-332, 10.1021/ar00047a002
Bleiholder, C.; Wyttenbach, T.; Bowers, M. T. A Novel Projection Approximation Algorithm for the Fast and Accurate Computation of Molecular Collision Cross Sections (I). Method. Int. J. Mass Spectrom. 2011, 308, 1-10, 10.1016/j.ijms.2011.06.014
Marklund, E. G.; Degiacomi, M. T.; Robinson, C. V.; Baldwin, A. J.; Benesch, J. L. P. Collision Cross Sections for Structural Proteomics. Structure 2015, 23, 791-799, 10.1016/j.str.2015.02.010
Pagel, K.; Harvey, D. J. Ion Mobility-Mass Spectrometry of Complex Carbohydrates: Collision Cross Sections of Sodiated N-Linked Glycans. Anal. Chem. 2013, 85, 5138-5145, 10.1021/ac400403d
Morsa, D.; Defize, T.; Dehareng, D.; Jérôme, C.; De Pauw, E. Polymer Topology Revealed by Ion Mobility Coupled with Mass Spectrometry. Anal. Chem. 2014, 86, 9693-9700, 10.1021/ac502246g
Haler, J. R. N.; Morsa, D.; Lecomte, P.; Jérôme, C.; Far, J.; De Pauw, E. Predicting Ion Mobility-Mass Spectrometry Trends of Polymers Using the Concept of Apparent Densities. Methods 2018, 144, 125-133, 10.1016/j.ymeth.2018.03.010
Kaddis, C. S.; Lomeli, S. H.; Yin, S.; Berhane, B.; Apostol, M. I.; Kickhoefer, V. A.; Rome, L. H.; Loo, J. A. Sizing Large Proteins and Protein Complexes by Electrospray Ionization Mass Spectrometry and Ion Mobility. J. Am. Soc. Mass Spectrom. 2007, 18, 1206-1216, 10.1016/j.jasms.2007.02.015
Marrink, S. J.; de Vries, A. H.; Mark, A. E. Coarse Grained Model for Semiquantitative Lipid Simulations. J. Phys. Chem. B 2004, 108, 750-760, 10.1021/jp036508g
Warshel, A. Multiscale Modeling of Biological Functions: From Enzymes to Molecular Machines (Nobel Lecture). Angew. Chem., Int. Ed. 2014, 53, 10020-10031, 10.1002/anie.201403689
Giles, K.; Pringle, S. D.; Worthington, K. R.; Little, D.; Wildgoose, J. L.; Bateman, R. H. Applications of a Travelling Wave-Based Radio-Frequency-Only Stacked Ring Ion Guide. Rapid Commun. Mass Spectrom. 2004, 18, 2401-2414, 10.1002/rcm.1641
Shvartsburg, A. A.; Smith, R. D. Fundamentals of Traveling Wave Ion Mobility Spectrometry. Anal. Chem. 2008, 80, 9689-9699, 10.1021/ac8016295
Gabelica, V.; Shvartsburg, A. A.; Afonso, C.; Barran, P.; Benesch, J. L. P.; Bleiholder, C.; Bowers, M. T.; Bilbao, A.; Bush, M. F.; Campbell, J. L.; Campuzano, I. D. G.; Causon, T.; Clowers, B. H.; Creaser, C. S.; De Pauw, E.; Far, J.; Fernandez-lima, F.; Fjeldsted, J. C.; Giles, K.; Groessl, M.; Hogan, C. J. J.; Hann, S.; Kim, H. I.; Kurulugama, R. T.; May, J. C.; McLean, J. A.; Pagel, K.; Richardson, K.; Ridgeway, M. E.; Rosu, F.; Sobott, F.; Thalassinos, K.; Valentine, S. J.; Wyttenbach, T. Recommandations for Reporting Ion Mobility Mass Spectrometry Measurements. Mass Spectrom. Rev. 2019, 38, 291, 10.1002/mas.21585
Shvartsburg, A. A.; Mashkevich, S. V.; Baker, E. S.; Smith, R. D. Optimization of Algorithms for Ion Mobility Calculations. J. Phys. Chem. A 2007, 111, 2002-2010, 10.1021/jp066953m
Scarff, C. A.; Thalassinos, K.; Hilton, G. R.; Scrivens, J. H. Travelling Wave Ion Mobility Mass Spectrometry Studies of Protein Structure: Biological Significance and Comparison with X-Ray Crystallography and Nuclear Magnetic Resonance Spectroscopy Measurements. Rapid Commun. Mass Spectrom. 2008, 22, 3297-3304, 10.1002/rcm.3737
Benesch, J. L. P.; Ruotolo, B. T. Mass Spectrometry: Come of Age for Structural and Dynamical Biology. Curr. Opin. Struct. Biol. 2011, 21, 641-649, 10.1016/j.sbi.2011.08.002
Bruns, C. J.; Stoddart, J. F. Mechanically Interlaced and Interlocked Donor-Acceptor Foldamers. Adv. Polym. Sci. 2013, 261, 271-294, 10.1007/12_2013_245
Sluysmans, D.; Hubert, S.; Bruns, C. J.; Zhu, Z.; Stoddart, J. F.; Duwez, A. Synthetic Oligorotaxanes Exert High Forces When Folding under Mechanical Load. Nat. Nanotechnol. 2018, 13, 209-214, 10.1038/s41565-017-0033-7
Sluysmans, D.; Devaux, F.; Bruns, C. J.; Stoddart, J. F.; Duwez, A. Dynamic Force Spectroscopy of Synthetic Oligorotaxane Foldamers. Proc. Natl. Acad. Sci. U. S. A. 2018, 115, 9362-9366, 10.1073/pnas.1712790115
Degiacomi, M. T. On the Effect of Sphere-Overlap on Super Coarse-Grained Models of Protein Assemblies. J. Am. Soc. Mass Spectrom. 2019, 30, 113-117, 10.1007/s13361-018-1974-2
Vouk, V. Projected Area of Convex Bodies. Nature 1948, 162, 330-331, 10.1038/162330a0
Jennings, B. R.; Parslow, K. Particle Size Measurement: The Equivalent Spherical Diameter. Proc. R. Soc. London, Ser. A 1988, 419, 137-149, 10.1098/rspa.1988.0100
Vickers, G. T. The Projected Areas of Ellipsoids and Cylinders. Powder Technol. 1996, 86, 195-200, 10.1016/0032-5910(95)03049-2
Slepian, Z. Average Projected Area Theorem-Generalization to Higher Dimensions. arXiv:1109.0595 2012, 1-12
Salbo, R.; Bush, M. F.; Naver, H.; Campuzano, I.; Robinson, C. V.; Pettersson, I.; Jørgensen, T. J. D.; Haselmann, K. F. Traveling-Wave Ion Mobility Mass Spectrometry of Protein Complexes: Accurate Calibrated Collision Cross-Sections of Human Insulin Oligomers. Rapid Commun. Mass Spectrom. 2012, 26, 1181-1193, 10.1002/rcm.6211
Shelimov, K. B.; Jarrold, M. F. Conformations, Unfolding, and Refolding of Apomyoglobin in Vacuum: An Activation Barrier for Gas-Phase Protein Folding. J. Am. Chem. Soc. 1997, 119, 2987-2994, 10.1021/ja962914k
Shelimov, K. B.; Clemmer, D. E.; Hudgins, R. R.; Jarrold, M. F. Protein Structure in Vacuo: Gas-Phase Conformations of BPTI and Cytochrome. J. Am. Chem. Soc. 1997, 119 (9), 2240-2248, 10.1021/ja9619059
Wyttenbach, T.; Bowers, M. T. Structural Stability from Solution to the Gas Phase: Native Solution Structure of Ubiquitin Survives Analysis in a Solvent-Free Ion Mobility-Mass Spectrometry Environment. J. Phys. Chem. B 2011, 115, 12266-12275, 10.1021/jp206867a
Ching, C. B.; Hidajat, K.; Uddin, M. S. Evaluation of Equilibrium and Kinetic Parameters of Smaller Molecular Size Amino Acids on KX Zeolite Crystals via Liquid Chromatographic Techniques. Sep. Sci. Technol. 1989, 24, 581-597, 10.1080/01496398908049793
Baldwin, A. J.; Lioe, H.; Hilton, G. R.; Baker, L. A.; Rubinstein, J. L.; Kay, L. E.; Benesch, J. L. P. The Polydispersity of AB-Crystallin Is Rationalized by an Interconverting Polyhedral Architecture. Structure 2011, 19, 1855-1863, 10.1016/j.str.2011.09.015
Marcoux, J.; Robinson, C. V. Twenty Years of Gas Phase Structural Biology. Structure 2013, 21, 1541-1550, 10.1016/j.str.2013.08.002
Sharon, M.; Robinson, C. V. The Role of Mass Spectrometry in Structure Elucidation of Dynamic Protein Complexes. Annu. Rev. Biochem. 2007, 76, 167-193, 10.1146/annurev.biochem.76.061005.090816
Eschweiler, J. D.; Rabuck-Gibbons, J. N.; Tian, Y.; Ruotolo, B. T. CIUSuite: A Quantitative Analysis Package for Collision Induced Unfolding Measurements of Gas-Phase Protein Ions. Anal. Chem. 2015, 87, 11516-11522, 10.1021/acs.analchem.5b03292
Kulesza, A.; Marklund, E. G.; MacAleese, L.; Chirot, F.; Dugourd, P. Bringing Molecular Dynamics and Ion-Mobility Spectrometry Closer Together: Shape Correlations, Structure-Based Predictors and Dissociation. J. Phys. Chem. B 2018, 122, 8317-8329, 10.1021/acs.jpcb.8b03825