Conformational States of Macromolecular Assemblies Explored by Integrative Structure Calculation

Overview

Journal Structure

Publisher Cell Press

Specialties Biochemistry
Biotechnology
Cell Biology
Molecular Biology

Date 2013 Sep 10

PMID 24010709

Citations 16

Authors

Konstantinos Thalassinos

Arun Prasad Pandurangan

Min Xu

Frank Alber

Maya Topf

Affiliations

Soon will be listed here.

Abstract

A detailed description of macromolecular assemblies in multiple conformational states can be very valuable for understanding cellular processes. At present, structural determination of most assemblies in different biologically relevant conformations cannot be achieved by a single technique and thus requires an integrative approach that combines information from multiple sources. Different techniques require different computational methods to allow efficient and accurate data processing and analysis. Here, we summarize the latest advances and future challenges in computational methods that help the interpretation of data from two techniques-mass spectrometry and three-dimensional cryo-electron microscopy (with focus on alignment and classification of heterogeneous subtomograms from cryo-electron tomography). We evaluate how new developments in these two broad fields will lead to further integration with atomic structures to broaden our picture of the dynamic behavior of assemblies in their native environment.

Citing Articles

Mapping the Multiscale Proteomic Organization of Cellular and Disease Phenotypes.

Cesnik A, Schaffer L, Gaur I, Jain M, Ideker T, Lundberg E Annu Rev Biomed Data Sci. 2024; 7(1):369-389.

PMID: 38748859 PMC: 11343683. DOI: 10.1146/annurev-biodatasci-102423-113534.

Molecular Dynamics and Other HPC Simulations for Drug Discovery.

Kotev M, Diaz Gonzalez C Methods Mol Biol. 2023; 2716:265-291.

PMID: 37702944 DOI: 10.1007/978-1-0716-3449-3_12.

Are the Gas-Phase Structures of Molecular Elephants Enduring or Ephemeral? Results from Time-Dependent, Tandem Ion Mobility.

Zercher B, Hong S, Roush A, Feng Y, Bush M Anal Chem. 2023; 95(25):9589-9597.

PMID: 37294019 PMC: 10549206. DOI: 10.1021/acs.analchem.3c01222.

Development of a Chemically Modified Sensor Based on a Pentapeptide and Its Application for Sensitive Detection of Verbascoside in Extra Virgin Olive Oil.

Munteanu I, Gradinaru V, Apetrei C Int J Mol Sci. 2022; 23(24).

PMID: 36555346 PMC: 9778896. DOI: 10.3390/ijms232415704.

Peptide-Protein Interactions: From Drug Design to Supramolecular Biomaterials.

Caporale A, Adorinni S, Lamba D, Saviano M Molecules. 2021; 26(5).

PMID: 33668767 PMC: 7956380. DOI: 10.3390/molecules26051219.

References

Degiacomi M, Iacovache I, Pernot L, Chami M, Kudryashev M, Stahlberg H . Molecular assembly of the aerolysin pore reveals a swirling membrane-insertion mechanism. Nat Chem Biol. 2013; 9(10):623-9. DOI: 10.1038/nchembio.1312. View

Briggs J . Structural biology in situ--the potential of subtomogram averaging. Curr Opin Struct Biol. 2013; 23(2):261-7. DOI: 10.1016/j.sbi.2013.02.003. View

Maurer U, Zeev-Ben-Mordehai T, Pandurangan A, Cairns T, Hannah B, Whitbeck J . The structure of herpesvirus fusion glycoprotein B-bilayer complex reveals the protein-membrane and lateral protein-protein interaction. Structure. 2013; 21(8):1396-405. PMC: 3737472. DOI: 10.1016/j.str.2013.05.018. View

Zhu Y, Carragher B, Glaeser R, Fellmann D, Bajaj C, Bern M . Automatic particle selection: results of a comparative study. J Struct Biol. 2004; 145(1-2):3-14. DOI: 10.1016/j.jsb.2003.09.033. View

Leitner A, Reischl R, Walzthoeni T, Herzog F, Bohn S, Forster F . Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol Cell Proteomics. 2012; 11(3):M111.014126. PMC: 3316732. DOI: 10.1074/mcp.M111.014126. View

Rozbesky D, Man P, Kavan D, Chmelik J, cerny J, Bezouska K . Chemical cross-linking and H/D exchange for fast refinement of protein crystal structure. Anal Chem. 2011; 84(2):867-70. DOI: 10.1021/ac202818m. View

Beveridge R, Chappuis Q, MacPhee C, Barran P . Mass spectrometry methods for intrinsically disordered proteins. Analyst. 2012; 138(1):32-42. DOI: 10.1039/c2an35665a. View

Suhre K, Navaza J, Sanejouand Y . NORMA: a tool for flexible fitting of high-resolution protein structures into low-resolution electron-microscopy-derived density maps. Acta Crystallogr D Biol Crystallogr. 2006; 62(Pt 9):1098-100. DOI: 10.1107/S090744490602244X. View

Iacob R, Engen J . Hydrogen exchange mass spectrometry: are we out of the quicksand?. J Am Soc Mass Spectrom. 2012; 23(6):1003-10. PMC: 3389995. DOI: 10.1007/s13361-012-0377-z. View

10.

Lasker K, Forster F, Bohn S, Walzthoeni T, Villa E, Unverdorben P . Molecular architecture of the 26S proteasome holocomplex determined by an integrative approach. Proc Natl Acad Sci U S A. 2012; 109(5):1380-7. PMC: 3277140. DOI: 10.1073/pnas.1120559109. View

11.

Kawabata T . Multiple subunit fitting into a low-resolution density map of a macromolecular complex using a gaussian mixture model. Biophys J. 2008; 95(10):4643-58. PMC: 2576401. DOI: 10.1529/biophysj.108.137125. View

12.

Uetrecht C, Barbu I, Shoemaker G, van Duijn E, Heck A . Interrogating viral capsid assembly with ion mobility-mass spectrometry. Nat Chem. 2011; 3(2):126-32. DOI: 10.1038/nchem.947. View

13.

Schmidt C, Zhou M, Marriott H, Morgner N, Politis A, Robinson C . Comparative cross-linking and mass spectrometry of an intact F-type ATPase suggest a role for phosphorylation. Nat Commun. 2013; 4:1985. PMC: 3709506. DOI: 10.1038/ncomms2985. View

14.

Hu W, Walters B, Kan Z, Mayne L, Rosen L, Marqusee S . Stepwise protein folding at near amino acid resolution by hydrogen exchange and mass spectrometry. Proc Natl Acad Sci U S A. 2013; 110(19):7684-9. PMC: 3651421. DOI: 10.1073/pnas.1305887110. View

15.

Alber F, Forster F, Korkin D, Topf M, Sali A . Integrating diverse data for structure determination of macromolecular assemblies. Annu Rev Biochem. 2008; 77:443-77. DOI: 10.1146/annurev.biochem.77.060407.135530. View

16.

Henderson R, Sali A, Baker M, Carragher B, Devkota B, Downing K . Outcome of the first electron microscopy validation task force meeting. Structure. 2012; 20(2):205-14. PMC: 3328769. DOI: 10.1016/j.str.2011.12.014. View

17.

Scheres S, Valle M, Nunez R, S Sorzano C, Marabini R, Herman G . Maximum-likelihood multi-reference refinement for electron microscopy images. J Mol Biol. 2005; 348(1):139-49. DOI: 10.1016/j.jmb.2005.02.031. View

18.

Al-Amoudi A, Castano-Diez D, Devos D, Russell R, Johnson G, Frangakis A . The three-dimensional molecular structure of the desmosomal plaque. Proc Natl Acad Sci U S A. 2011; 108(16):6480-5. PMC: 3081036. DOI: 10.1073/pnas.1019469108. View

19.

Clare D, Vasishtan D, Stagg S, Quispe J, Farr G, Topf M . ATP-triggered conformational changes delineate substrate-binding and -folding mechanics of the GroEL chaperonin. Cell. 2012; 149(1):113-23. PMC: 3326522. DOI: 10.1016/j.cell.2012.02.047. View

20.

DiMaio F, Tyka M, Baker M, Chiu W, Baker D . Refinement of protein structures into low-resolution density maps using rosetta. J Mol Biol. 2009; 392(1):181-90. PMC: 3899897. DOI: 10.1016/j.jmb.2009.07.008. View