Determination of viral protein assembly and function by mass spectrometry - Dr. Alison E. Ashcroft, University of Leeds, UK
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2 case study: Application of viral proteins using SYNAPT HDMS Determination of viral protein assembly and function by mass spectrometry - Dr. Alison E. Ashcroft, University of Leeds, UK The assembly of viral proteins into a range of macromolecular complexes of strictly defined architecture is one of nature s wonders. Unravelling the details of these complex structures and the associated self-assembly pathways, which lead to their efficient and precise construction, will play an important role in the development of viral therapeutics. It will also be important in bio-nanotechnology where there is a plethora of applications for such well-defined macromolecular complexes, including cell-specific drug delivery, and as substrates for the formation of novel materials with unique electrical and magnetic properties. Mass spectrometry has the ability not only to measure masses accurately but also to provide vital details, including recently cross-sectional area measurements, regarding the composition and stoichiometry of intact, non-covalently bound macromolecular complexes under near-physiological conditions 9. It is thus ideal for exploring the assembly and function of viruses. The detailed molecular mechanisms underlying the in vitro selfassembly reactions of viruses are difficult to investigate because intermediates on the assembly pathways are not only present in limited amounts but are also transient. In the Mass Spectrometry Facility in the Astbury Centre for Structural Molecular Biology at the University of Leeds ESI/MS and ESI/IMS/MS are being employed to characterize the detailed molecular mechanism of ssrna virus assembly. In studies of the bacteriophage MS2, reassembly of the coat protein into a T=3 capsid shell is initiated by a sequencespecific non-covalent coat protein-rna stem-loop interaction. The entire assembly into the intact capsid can be monitored on-line and key intermediates are being characterised using state-of-the art MS methods. 10,11 Figure 6. Intermediates observed in the virus capsid reassembly of the bacteriophage MS2 using nanoesi/ms on the SYNAPT HDMS 10,11. The m/z spectrum shows the key intermediates: A, the initial complex of the coat protein dimer and RNA stem-loop (33.5 kda); B, [3(CP2+RNA) + 3CP2] (182.7 kda); C, [3(CP2+RNA) + 2CP2 + CP] (169.1 kda); D, [5(CP2+RNA) + 5CP2] (304.8 kda). The broad signal at m/z 15,000 20,000 is indicative of complete capsid formation. Figure 7. nanoesi/ims/ms DriftScope plot showing the key intermediates observed in the virus capsid reassembly of the bacteriophage MS2. 10,11 Using ESI/MS/MS not only achieves separation of the individual components (which are usually observed as overlapping charge state distributions in the m/z spectrum) in the complex reaction mixtures but also highlights the presence of multiple conformers of each species and simultaneously provides cross-sectional area calculations to complement the mass measurements.
3 SYNAPT High Definition Mass Spectrometry A powerful analytical technique for structural biology Leading researchers continuously strive for a more complete understanding of the dynamic nature of living cells and the interaction of molecules within those cells protein structures. Understanding the structure of a protein helps us to understand its true function: how it works, what it does, and how it redesigns itself under certain conditions. Highly advanced studies of the folding, unfolding, and refolding of protein structures is underway by some of the world s most renowned scientists whose ultimate aim is to achieve significant and impactful advances in medical science. Defining the structures and functions of macromolecular machines and transient assemblies is central to modern molecular and cell biology. Native mass spectrometry and the newly emerging ion mobility separation techniques are proving invaluable for defining substructures and stoichiometries of components of such multicomponent systems. The information provided complements that from X-ray, NMR and electron microscopy in structural biology. Sir Tom Blundell FRS, FMedSci William Dunn Professor of Biochemistry and Chair, School of Biological Sciences, University of Cambridge, UK Research techniques of today and for the future Researchers working in structural biology use a number of biophysical techniques to analyze protein structures, techniques such as X-ray crystallography, nuclear magnetic resonance (NMR) cryo-electron microscopy, and dynamic light scattering techniques. High Definition Mass Spectrometry (HDMS ) is a powerful new analytical tool for structural biology research. Coupling electrospray ionization (ESI) with high efficiency ion mobility mass spectrometry (SYNAPT HDMS) has revolutionized the structural analysis of peptides, proteins, and protein complexes. Recent scientific breakthroughs, including the determination of overall size, shape, and subunit architecture of protein complexes, have catapulted ion mobility mass spectrometry to the forefront as a key technology for worldwide proteomics and structural biology initiatives. With HDMS you can: n Better understand the function of the protein structure, the way it folds and unfolds n Preserve and accurately mass measure intact protein complexes n Measure the size and shape changes for simple and heterogeneous protein complexes n Achieve consistent measurements of protein complex size determined by high efficiency ion mobility MS and other biophysical techniques, such as X-ray crystallography and dynamic light scattering techniques A new generation of mass spectrometry for structural biology Waters works closely with customers and key research partners around the world, to gain a keen understanding of their needs and experiences, to deliver purposeful and innovative MS technologies, which in turn enable researchers to make meaningful scientific advancements. Waters SYNAPT HDMS System is the perfect embodiment to this ideal. This award winning platform (Pittcon Editor s 2007 Gold Award and Frost and Sullivan 2008 Product Innovation Award) allows you to redefine your research boundaries by providing the capability to analyze samples differentiated by size, shape, charge, and mass. Using novel Triwave Technology, the SYNAPT HDMS System combines high-efficiency ion mobility-based measurements and separation with high performance quadrupole and time-of-flight mass spectrometry, which provides a unique and enabling technology platform ideally suited to structural biology research (see Figure 1).
4 Triwave Technology, enabling ion mobility separations at the limits of MS detection in the SYNAPT HDMS System. Figure 1. The SYNAPT HDMS Technology platform. How can SYNAPT HDMS help to advance research capabilities for the structural biologist? Detect and measure multiple protein conformations When a protein is analyzed under native mass spectrometric conditions, its shape can be maintained, measured, and a collisional cross section (gas phase size) can be assigned 1,2.,4 With SYNAPT HDMS, collisional cross section (CCS) measurements are made possible by high-efficiency ion-mobility using unique Triwave Technology. This assigned shape and size is consistent with that determined by X-ray crystallography and NMR. 3 Figure 2. Ion mobility-mass spectrometry of TRAP protein 1 showing how native protein ring structure can be maintained and its cross section measured within the mass spectrometer. Analyze small proteins to large heterogeneous complexes Through its extended oa-tof mass range, the SYNAPT HDMS allows you to analyze a much broader number of large biological macromolecules. 5 When ionizing biological macromolecules under native conditions, such as the chaperone protein GroEL (800 kda), the protein complex remains folded and exhibits relatively few charges. It therefore appears high in the m/z scale, and is incompatible with many types of conventional mass spectrometer. The SYNAPT HDMS has a broad oa-tof m/z range of 100,000 m/z, which provides the capability to analyze peptides to some of the largest protein complexes ever observed by mass spectrometry. 5 Figure 3. Electrospray mass spectrum of the Chaperone protein GroEL. GroEL remains folded in it s native tetradecamer structure.
5 Probe structure and interactions The broad mass range (up to 32 k amu) of the resolving quadrupole allows for high m/z protein species to be selected for subsequent MS/MS activation and fragmentation 6,7. This provides you with the ability to characterize individual subunits and subcomplexes, assess protein:protein or protein:ligand binding affinties, and to generate a subunits interaction map for your complex of interest 2,8. This is especially beneficial for macromolecular complexes, which do not currently have a known crystal structure. Figure 4. MS/MS of the (800KDa) GroEL protein complex (precursor ion m/z 11,440 (+71)). The spectra show how disassembly of the protein complex can be investigated by using different collision energies. Acquity UPLC System with the Synapt HDMS System. Figure 5. Nanoelectrosray: enables gentle, sensitive introduction of the biological sample into the mass spectrometer. A holistic approach for structural biology research Retain protein structures in the mass spectrometer The SYNAPT HDMS System allows the native protein structure to be retained 1 when transferred from the solution phase into the gas phase of the mass spectrometer. The nanoelectrospray ionization source provides a gentle form of ionization that is able to maintain noncovalent interactions within a protein complex. The ability of MS to determine unambiguously the stoichiometry of protein complexes is now widely accepted. This, coupled with its capacity to tackle heterogeneous and polydisperse assemblies, has led to its widespread application in supporting other structural biology approaches, particularly X-ray analysis and EM. PROF. CAROL ROBINSON, FRS AND DR. MICHAL SHARON University of Cambridge, UK The SYNAPT High Definition MS System expands on the capabilities of conventional MS instrumentation by combining high-efficiency ion mobility with high performance mass spectrometry. This exciting combination of technologies when used as a complementary approach to other research techniques will be of growing importance to the structural biologist in defining multi-protein assemblies of ever increasing complexity.
6 Sales Offices: Austria Australia Belgium and Luxembourg Brazil Canada China Czech Republic Denmark Finland France Germany Hong Kong Hungary India Ireland Italy Japan Korea Mexico The Netherlands Norway Poland Puerto Rico Russia/CIS / Singapore Spain Sweden Switzerland Taiwan UK US References 1. Ruotolo G, Campuzano I, Sandercock AM, Bateman RH, Robinson CV. Evidence for Macromolecular Protein Rings in the Absence of Bulk Water. Science Dec 9; 310, Sharon M, Robinson CV. The Role of Mass Spectrometry in Structure Elucidation of Dynamic Protein Complexes. Ann. Rev. Biochem. 2007, 76, Antson AA, Dodson EJ, Dodson G, Greaves RB, Chen X, Gollnick P. Structure of the trp RNA-binding Attenuation Protein, TRAP, Bound to RNA. Nature Sep 16;401(6750): Ruotolo BT, Benesch JL, Sandercock AM, Hyung SJ, Robinson CV. Ion Mobility-Mass Spectrometry Analysis of Large Protein Complexes. Nature Protocols. 2008;3(7): Lorenzen K, Olia AS, Uetrecht C, Cingolani G, Heck AJ. Determination of Stoichiometry and Conformational Changes in the First Step of the P22 Tail Assembly. J. Mol. Biol May 30;379 (2): Benesch JL, Ruotolo BT, Simmons DA, Robinson CV. Protein Complexes in the Gas Phase: Technology for Structural Genomics and Proteomics. Chem. Rev Aug;107(8): Ruotolo BT, Hyung SJ, Robinson PM, Giles K, Bateman RH, Robinson CV. Ion Mobility-Mass Spectrometry Reveals Long-Lived Unfolded Intermediates in the Dissociation of Protein Complexes. Angew Chem Int Ed Engl. 2007; 46(42): Taverner T, Hernandez H, Sharon M, Ruotolo BT, Matak-Vinkovic D, Devos D, Russell RB, Robinson CV. Subunit Architecture of Intact Protein Complexes from Mass Spectrometry and Homology Modelling. Acc Chem Res May;41(5): Morton VL, Stockley PG, Stonehouse NJ, Ashcroft AE. Insights Into Virus Capsid Assembly from Non-covalent Mass Spectrometry. Mass Spectrom Rev May Stockley PG, Rolfsson O, Thompson GS, Basnak G, Francese S, Stonehouse NJ, Homans SW, Ashcroft AE. A Simple, RNA-Mediated Allosteric Switch Controls the Pathway to Formation of a T=3 Viral Capsid. J Mol Biol Jun 1;369(2): Rolfsson O, Toropova K, Morton VL, Francese S, Basnak G, Thompson GS, Homans SW, Ashcroft AE, Stonehouse NJ, Ranson NA, Stockley PG. RNA Packing Specificity and Folding During Assembly of the Bacteriophage MS2. J. Computational & Mathematical Medicine, in press, Other useful structural biology references: n Smith DP, Giles K, Bateman RH, Radford SE, Ashcroft AE. Monitoring Copopulated Conformational States during Protein Folding Events Using Electrospray Ionization-Ion Mobility Spectrometry-Mass Spectrometry. J Am Soc Mass Spectrom Dec;18(12): n Barrera NP, Di Bartolo N, Booth PJ, Robinson CV. Micelles Protect Membrane Complexes from Solution to Vacuum. Science Jul 11;321(5886): n Alverdi V, Mazon H, Versluis C, Hemrika W, Esposito G, van den Heuvel R, Scholten A, Heck AJ. cgmp-binding Prepares PKG for Substrate Bindong by Disclosing the C-terminal Domain. J Mol Biol Feb 1;375(5): Acknowledgements Dr. Stefan Knapp and Dr. Frank Soboot, Structural Genomics Consortium, University of Oxford for the figures on the front cover. Waters Corporation 34 Maple Street Milford, MA U.S.A. T: F: Waters is a registered trademark of Waters Corporation. The Science of What s Possible, SYNAPT, HDMS, High Definition Mass Spectrometry, High Definition MS, and DriftScope are trademarks of Waters Corporation. All other trademarks are the property of their respective owners Waters Corporation Printed in the U.S.A. August EN PC-XX
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