Design and performance of a second-generation surface-induced dissociation cell for Fourier transform ion cyclotron resonance mass spectrometry of native protein complexes.

A second-generation ("Gen 2") device capable of surface-induced dissociation (SID) and collision-induced dissociation (CID) for Fourier transform ion cyclotron resonance mass spectrometry of protein complexes has been designed, simulated, fabricated, and experimentally compared to a first-generation device ("Gen 1"). The primary goals of the redesign were to 1) simplify SID by reducing the number of electrodes, 2) increase CID and SID sensitivity by lengthening the collision cell, and 3) increase the mass range of the device for analysis of larger multimeric proteins, all while maintaining the normal instrument configuration and operation. Compared to Gen 1, Gen 2 exhibits an approximately 10x increase in sensitivity in flythrough mode, 7x increase in CID sensitivity for protonated leucine enkephalin (m/z 556) and 14x increase of CID sensitivity of 53 kDa streptavidin tetramer. It also approximately doubles of the useful mass range (from m/z 8,000 to m/z 15,000) using a rectilinear ion trap with a smaller inscribed radius or triples it (to m/z 22,000) using a hexapole collision cell and yields a 3-10x increase in SID sensitivity. We demonstrate the increased mass range and sensitivity on a variety of model molecules spanning nearly 3 orders of magnitude in absolute mass and present examples where the high resolution of the FT-ICR is advantageous for deconvoluting overlapping SID fragments.

[1]  S. Lindert,et al.  Relative interfacial cleavage energetics of protein complexes revealed by surface collisions , 2019, Proceedings of the National Academy of Sciences.

[2]  C. D. Boone,et al.  Topological Analysis of Transthyretin Disassembly Mechanism: Surface-Induced Dissociation Reveals Hidden Reaction Pathways. , 2019, Analytical chemistry.

[3]  Zachary L. VanAernum,et al.  Surface-Induced Dissociation of Noncovalent Protein Complexes in an Extended Mass Range Orbitrap Mass Spectrometer. , 2018, Analytical chemistry.

[4]  Zachary L. VanAernum,et al.  Surface-Induced Dissociation: An Effective Method for Characterization of Protein Quaternary Structure. , 2018, Analytical chemistry.

[5]  Zachary L. VanAernum,et al.  Localization of Protein Complex Bound Ligands by Surface-Induced Dissociation High-Resolution Mass Spectrometry. , 2018, Analytical chemistry.

[6]  L. Paša-Tolić,et al.  Surface Induced Dissociation Coupled with High Resolution Mass Spectrometry Unveils Heterogeneity of a 211 kDa Multicopper Oxidase Protein Complex , 2018, Journal of The American Society for Mass Spectrometry.

[7]  D. Baker,et al.  Confirmation of intersubunit connectivity and topology of designed protein complexes by native MS , 2018, Proceedings of the National Academy of Sciences.

[8]  Iain D G Campuzano,et al.  An Integrated Native Mass Spectrometry and Top-Down Proteomics Method that Connects Sequence to Structure and Function of Macromolecular Complexes , 2017, Nature chemistry.

[9]  Randall E. Pedder,et al.  Surface-Induced Dissociation of Protein Complexes in a Hybrid Fourier Transform Ion Cyclotron Resonance Mass Spectrometer. , 2017, Analytical chemistry.

[10]  Albert J. R. Heck,et al.  Native Mass Spectrometry: What is in the Name? , 2016, Journal of The American Society for Mass Spectrometry.

[11]  M. F. Bush,et al.  Analysis of Native-Like Ions Using Structures for Lossless Ion Manipulations. , 2016, Analytical chemistry.

[12]  J. Brodbelt.  Ion Activation Methods for Peptides and Proteins. , 2016, Analytical chemistry.

[13]  Micah T. Nelp,et al.  Refining the Structural Model of a Heterohexameric Protein Complex: Surface Induced Dissociation and Ion Mobility Provide Key Connectivity and Topology Information , 2015, ACS central science.

[14]  V. Wysocki,et al.  Surface-Induced Dissociation Mass Spectra as a Tool for Distinguishing Different Structural Forms of Gas-Phase Multimeric Protein Complexes. , 2015, Analytical chemistry.

[15]  V. Wysocki,et al.  Surface-Induced Dissociation of Homotetramers with D2 Symmetry Yields their Assembly Pathways and Characterizes the Effect of Ligand Binding. , 2015, Chemistry & biology.

[16]  J. Brodbelt,et al.  Characterization of native protein complexes using ultraviolet photodissociation mass spectrometry. , 2014, Journal of the American Chemical Society.

[17]  C. Eyers,et al.  The power of ion mobility-mass spectrometry for structural characterization and the study of conformational dynamics. , 2014, Nature chemistry.

[18]  V. Wysocki,et al.  Surface induced dissociation: dissecting noncovalent protein complexes in the gas phase. , 2014, Accounts of chemical research.

[19]  V. Wysocki,et al.  Surface Induced Dissociation Yields Quaternary Substructure of Refractory Noncovalent Phosphorylase B and Glutamate Dehydrogenase Complexes , 2014, Journal of The American Society for Mass Spectrometry.

[20]  N. Kelleher,et al.  From protein complexes to subunit backbone fragments: a multi-stage approach to native mass spectrometry. , 2013, Analytical chemistry.

[21]  V. Wysocki,et al.  Dissecting the large noncovalent protein complex GroEL with surface-induced dissociation and ion mobility-mass spectrometry. , 2013, Analytical chemistry.

[22]  Carol V Robinson,et al.  Mass spectrometry of intact membrane protein complexes , 2013, Nature Protocols.

[23]  V. Wysocki,et al.  Impact of charge state on gas-phase behaviors of noncovalent protein complexes in collision induced dissociation and surface induced dissociation. , 2013, The Analyst.

[24]  Albert J R Heck,et al.  High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies , 2012, Nature Methods.

[25]  V. Wysocki,et al.  Protein subunits released by surface collisions of noncovalent complexes: nativelike compact structures revealed by ion mobility mass spectrometry. , 2012, Angewandte Chemie.

[26]  J. Vogel,et al.  Hfq and its constellation of RNA , 2011, Nature Reviews Microbiology.

[27]  O. Weichenrieder,et al.  Structural basis for RNA 3′-end recognition by Hfq , 2011, Proceedings of the National Academy of Sciences.

[28]  Eric D. Dodds,et al.  Revealing the quaternary structure of a heterogeneous noncovalent protein complex through surface-induced dissociation. , 2011, Analytical chemistry.

[29]  M. Gross,et al.  Native electrospray and electron-capture dissociation in FTICR mass spectrometry provide top-down sequencing of a protein component in an intact protein assembly , 2010, Journal of the American Society for Mass Spectrometry.

[30]  A. Heck.  Native mass spectrometry: a bridge between interactomics and structural biology , 2008, Nature Methods.

[31]  V. Wysocki,et al.  Surface-induced dissociation shows potential to be more informative than collision-induced dissociation for structural studies of large systems , 2008, Journal of the American Society for Mass Spectrometry.

[32]  V. Wysocki,et al.  Surface-induced dissociation of peptides and protein complexes in a quadrupole/time-of-flight mass spectrometer. , 2008, Analytical chemistry.

[33]  V. Wysocki,et al.  Surface-induced dissociation of small molecules, peptides, and non-covalent protein complexes , 2008, Journal of the American Society for Mass Spectrometry.

[34]  C. Robinson,et al.  Ion mobility-mass spectrometry reveals long-lived, unfolded intermediates in the dissociation of protein complexes. , 2007, Angewandte Chemie.

[35]  V. Wysocki,et al.  Symmetrical gas-phase dissociation of noncovalent protein complexes via surface collisions. , 2006, Journal of the American Chemical Society.

[36]  C. Robinson,et al.  Tandem mass spectrometry reveals the quaternary organization of macromolecular assemblies. , 2006, Chemistry & biology.

[37]  J. Laskin.  Energetics and dynamics of fragmentation of protonated leucine enkephalin from time- and energy-resolved surface-induced dissociation studies. , 2006, The journal of physical chemistry. A.

[38]  R. Bateman,et al.  Applications of a travelling wave-based radio-frequency-only stacked ring ion guide. , 2004, Rapid communications in mass spectrometry : RCM.

[39]  A. Heck,et al.  Native protein mass spectrometry: from intact oligomers to functional machineries. , 2004, Current opinion in chemical biology.

[40]  J. Shabanowitz,et al.  Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  E. Denisov,et al.  Surface-induced dissociation in a Fourier transform ion cyclotron resonance mass spectrometer: instrument design and evaluation. , 2002, Analytical chemistry.

[42]  J. Klassen,et al.  Thermal decomposition of a gaseous multiprotein complex studied by blackbody infrared radiative dissociation. Investigating the origin of the asymmetric dissociation behavior. , 2001, Analytical chemistry.

[43]  K. L. Scheycor,et al.  Design and performance of an in-line surface-induced dissociation device in a four-sector mass spectrometer , 1995, Journal of the American Society for Mass Spectrometry.

[44]  R A Chorush,et al.  Surface-induced dissociation of multiply-protonated proteins. , 1995, Analytical chemistry.

[45]  R. Cooks,et al.  Surface-induced dissociation of molecular ions in a quadrupole ion trap mass spectrometer , 1991, Journal of the American Society for Mass Spectrometry.

[46]  B. Chait,et al.  Observation of the heme-globin complex in native myoglobin by electrospray-ionization mass spectrometry , 1991 .

[47]  B. Ganem,et al.  Detection of noncovalent receptor-ligand complexes by mass spectrometry , 1991 .

[48]  M. Mann,et al.  Electrospray ionization for mass spectrometry of large biomolecules. , 1989, Science.

[49]  R. Cooks,et al.  A tandem time-of-flight mass spectrometer for surface-induced dissociation , 1987 .

[50]  R. Cooks,et al.  A tandem quadrupole mass spectrometer for the study of surface-induced dissociation , 1987 .

[51]  I. Campuzano,et al.  Fourier Transform-Ion Cyclotron Resonance Mass Spectrometry as a Platform for Characterizing Multimeric Membrane Protein Complexes , 2017, Journal of The American Society for Mass Spectrometry.

[52]  J. Brodbelt.  Photodissociation in ion traps , 2010 .

[53]  Peter R. Griffiths,et al.  Theory and Instrumentation , 2002 .

[54]  V. Wysocki,et al.  Thermal decomposition kinetics of protonated peptides and peptide dimers, and comparison with surface-induced dissociation. , 1995, Rapid communications in mass spectrometry : RCM.