Charge-State Dependent Compaction and Dissociation of Protein Complexes: Insights from Ion Mobility and Molecular Dynamics
Abstract
Collapse to compact states in the gas phase, with smaller collision cross sections than calculated for their native-like structure, has been reported previously for some protein complexes although not rationalized. Here we combine experimental and theoretical studies to investigate the gas-phase structures of four multimeric protein complexes during collisional activation. Importantly, using ion mobility-mass spectrometry (IM-MS), we find that all four macromolecular complexes retain their native-like topologies at low energy. Upon increasing the collision energy, two of the four complexes adopt a more compact state. This collapse was most noticeable for pentameric serum amyloid P (SAP) which contains a large central cavity. The extent of collapse was found to be highly correlated with charge state, with the surprising observation that the lowest charge states were those which experience the greatest degree of compaction. We compared these experimental results with in vacuo molecular dynamics (MD) simulations of SAP, during which the temperature was increased. Simulations showed that low charge states of SAP exhibited compact states, corresponding to collapse of the ring, while intermediate and high charge states unfolded to more extended structures, maintaining their ring-like topology, as observed experimentally. To simulate the collision-induced dissociation (CID) of different charge states of SAP, we used MS to measure the charge state of the ejected monomer and assigned this charge to one subunit, distributing the residual charges evenly among the remaining four subunits. Under these conditions, MD simulations captured the unfolding and ejection of a single subunit for intermediate charge states of SAP. The highest charge states recapitulated the ejection of compact monomers and dimers, which we observed in CID experiments of high charge states of SAP, accessed by supercharging. This strong correlation between theory and experiment has implications for further studies as well as for understanding the process of CID and for applications to gas-phase structural biology more generally.
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CID tends to benefit from supercharging, allowing more SID-like dissociation.
“Instead, CID tends to benefit from supercharging, allowing more SID-like dissociation.67”
From Higher-order structural characterisation of native proteins and complexes by top-down mass spectrometry (2020) · cites this paper as [67]
Subunit dissociation is suppressed in CID for charge-reduced precursors.
“In contrast, subunit dissociation is suppressed in CID for charge-reduced precursors.”
From Higher-order structural characterisation of native proteins and complexes by top-down mass spectrometry (2020) · cites this paper as [67]
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- Authors
- Hall, Z., Politis, A., Bush, M. F., Smith, L. J., & Robinson, C. V.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Robinson, Carol V.
- Venue
- Journal of the American Chemical Society
- Publisher
- American Chemical Society (ACS)
- Published
- 2012-02-13
- Volume
- 134
- Issue
- 7
- Pages
- 3429-3438
- ISSN
- 0002-7863 (ISSN-L)
- 1520-5126
- OpenAlex
- W2039125944
- Cited by
- 267
- References
- 70
- Citations by year
- 2026: 11 · 2025: 9 · 2024: 16 · 2023: 12 · 2022: 15 · 2021: 12 · 2020: 21 · 2019: 23 · 2018: 14 · 2017: 18 · 2016: 35 · 2015: 31 · 2014: 21 · 2013: 16 · 2012: 13
- FWCI
- 11.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of the American Chemical Society (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Mass Spectrometry Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Atomic and Molecular Physics
- Keywords
- charge state dependence, collision-induced dissociation, serum amyloid P component, gas-phase protein structure, collisional activation, supercharging, protein unfolding
- MeSH terms
- Animals, Bacillus subtilis, Bacterial Proteins, Humans, Ions, Multiprotein Complexes, Molecular Dynamics Simulation, Protein Unfolding
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